CC BY
8
Protistology 15 (4), 206-219 (2021)
Protistology
The impact of nuisance planktonic invaders on pelagic communities: a review of the Baltic Sea case studies
Irena V. Telesh1 and Elena N. Naumenko2
1 Zoological Institute, Russian Academy of Sciences, St. Petersburg, Russia
2 Kaliningrad State Technical University, Kaliningrad, Russia
| Submitted September 3, 2021 | Accepted September 29, 2021 |
Summary
The article focuses on the effects of planktonic nonindigenous species on pelagic communities in the Baltic Sea that can be assessed using the basic principles of invasion biology, ecological physiology, trophic dynamics in food chains, and production hydrobiology. The ecosystem effects of nuisance unicellular species (the potentially toxic bloom-forming dinoflagellates Prorocentrum cordatum) and multicellular invaders (the carnivorous fishhook water flea Cercopagispengoi) are reviewed and illustrated by the data from the Baltic estuaries and coastal lagoons. The putative effects of trophic interactions in plankton on the possible new protistan alien species introductions and the magnitude of harmful dinoflagellate blooms are suggested to occur in the future Baltic Sea due to the ongoing desalinization process under the changing climate.
Key words: biological invasions, Cercopagis pengoi, harmful algal bloom, Impact index, Prorocentrum cordatum, protists
Do non-indigenous species always affect native communities?
The penetration of alien species into new environments is currently one of the major drivers for global change in species biogeography and ecosystem health, which is linked tightly with multiple environmental alterations due to the onslaught of human activities (Simberloff, 2011; Darling and Carlton, 2018; Ojaveer et al., 2021; Ricciardi et al., 2021). Many invaders cause adverse effects and/or pose an elevated risk of impact to native species, communities and ecosystems, or economic implications (Ojaveer et al., 2021; Vilizzi et al., 2021).
Other nonindigenous species invade new environments without noticeable effects, or the effect is delayed, sometimes because of multidimensional niche differentiation, which buffers the impact of invasion (Telesh et al., 2016; Borza et al., 2021). Negligible effect of an invader can be observed also due to occupation of available and vacant ecological niches, although empty niches are extremely rare in the diverse and species-rich aquatic communities (Chesson, 2000; Elliott, 2003; Telesh et al., 2011a, 2011b, 2013; Litchman et al., 2012).
At microorganisms' level, the introductions of alien species are often "invisible", and because of the fewer dispersal barriers for microbes, compared
doi:10.21685/1680-0826-2021-15-4-2 © 2021 The Author(s)
Protistology © 2021 Protozoological Society Affiliated with RAS
with macroorganisms, environmental change might play a disproportionately large role in allowing microorganisms to spread (Litchman, 2010). Alternatively, microbial introductions can have evident nuisance ecosystem consequences. A good example of the microbial invasion with the delayed though devastating effects is the peculiar history of invasion of the Baltic Sea by the bloom-forming potentially toxic dinoflagellates Prorocentrum cor-datum (Ostenfeld) J.D.Dodge, 1975 in the 1980-s (Telesh et al., 2016). Nowadays, these unicellular planktonic protists form harmful blooms (red tides) in this sea and in the marine coastal waters globally (Glibert, 2020).
In the brackish-water Baltic Sea, which has been the area of intensive ongoing invasion processes (Leppakoski and Olenin, 2000; Olenin et al., 2017), P. cordatum is generally accepted as the only one truly invasive phytoplankton species because the dynamics and importance of only this unicellular alien meets the major established requirements of the ''invader'' (discussed in details by Olenina et al., 2010). Currently, the multiple negative ecosystem effects of red tides caused by P. cordatum are well identifiable. Moreover, the fine mechanisms of their invasive success, such as mixotrophic feeding mode, high adaptability of cells to external stresses, and intrapopulation heterogeneity in the uptake of different nutrient substrates, have been largely unveiled (Matantseva et al., 2016, 2018; Knyazev et al., 2018; Skarlato et al., 2018a, 2018b; Anderson et al., 2019; Glibert, 2020; Pechkovskaya et al., 2020; Telesh et al., 2020, 2021). However, linkage of this knowledge with predictive invasion theories and forecasts of nuisance ecosystem effects is still in its infancy because the integration ofmicrobial biology into invasion science has been insufficient so far (Ricciardi et al., 2021).
For many multicellular planktonic invaders, the impact assessment can be even a greater challenge than for the unicellular aliens. For example, the carnivorous fishhook water flea Cercopagis pengoi (Ostroumov, 1891), native to the Ponto-Caspian region, is one of such invaders in plankton of the Baltic Sea. It was discovered there for the first time in 1992 (Ojaveer and Lumberg, 1995), and during the following several years these nonindigenous cladocerans successfully colonized the entire Baltic Sea, including the Vistula and Curonian lagoons (Naumenko and Polunina, 2000; Telesh and Oja-veer, 2002; Telesh, 2018, and references therein). Nowadays, C. pengoi is the only one multicellular
alien species in plankton of the Baltic Sea, which is likely to have a strong impact on ecosystem functions (Olenin et al., 2017), particularly, on the pelagic food-web dynamics, which backs up fish feeding and fisheries. Specifically, the recent results suggested that in certain regions of the Baltic Sea, naturalization of C. pengoi might have caused population decline of the common pelagic copepods Eurytemora affinis (Poppe, 1880) that are the essential food for planktivorous fish (Naumenko and Telesh, 2019).
Meanwhile, usually it is problematic to demonstrate clearly the adverse ecosystem effects of certain invasive species (Simberloff, 2011; Vilizzi et al., 2021), mainly due to multiple external stressors as well as sheer complexity and low predictability of biotic interactions in plankton that are nonlinear, multidimensional, and even chaotic (Telesh et al., 2019). Therefore, it is often difficult to determine whether there was a reduction in the community/ ecosystem integrity or damage at one or more levels of biological organization (cell, individual, population, community and ecosystem) because of nonindigenous species, or whether the invaders have been assimilated without any considerable effect (Elliott, 2003; Jeschke et al., 2014).
Searching for frameworks to predict ecosystem susceptibility to invasions: biotic interactions versus external stressors
The role ofbiotic interactions in transformations of pelagic communities caused by biological invasions has been a hot research issue during the recent decades. Particularly, it was shown by experiments and imitation modeling that population dynamics of planktonic cladocerans is regulated mainly by predation and competitive interactions; moreover, competition for food prevents invasion of the community by the alien species (Dgebuadze and Fe-niova, 2009). The latter conclusion can be supported by the discovery of the two decades-long delay in the bloom formation by P. cordatum after its introduction to the Baltic Sea, which was likely caused by the competition of this alien with four native congeneric species since their ecological niches largely overlapped (Telesh et al., 2016).
Unicellular eukaryotes in plankton are highly sensitive to both local and global environmental changes, such as composition and concentration of nutrient substrates, irradiance, water temperature and
others, reacting to them by structural transformations of the communities as well as by the alterations in species' abundance, biomass, and productivity (Litchman et al., 2012; Schubert and Telesh, 2017; Schubert et al., 2017). The Baltic Sea studies revealed significant influence of water salinity on the structure and functions ofnatural phytoplankton communities (Olli et al., 2011) and the bacterial plankton (Herlemann et al., 2011, 2014; Dupont et al., 2014). At the same time, it was discovered that, unexpectedly, the concentration of dissolved and suspended nutrient substrates in the Baltic waters, which reflects the level of eutrophication, demonstrated only a weak correlation with the changes in phytoplankton community composition in this brackish-water sea (Olli et al., 2011). Meanwhile, the mesocosm experiments proved that salinity is another effective environmental factor, which defines species diversity ofphytoplankton, since the algal species number in mesocosms was decreasing with the increasing salinity, while the tendency was the opposite when the concentration of nutrients was increasing (Larson and Belovsky, 2013). Thus, the complex and (often) controversial effects of different environmental factors on the structure of pelagic communities as well as the effects of trophic interactions on ecosystems' invasibility, including their susceptibility to harmful, bloom-forming non-indigenous phytoplankton species, need to be unveiled and evaluated for the prognostic purposes (Barton et al., 2013).
In the last 30 years, a number of impact assessment frameworks that allowed for evaluating the environmental and/or socio-economic effects of invasive species were developed (Blackburn et al., 2014; Crystal-Ornelas and Lockwood, 2020; Ric-ciardi et al., 2021, and references therein). Specifically, the comparative functional response approach was introduced, whereby the impacts of invasive species were compared with analogous native species as eco-evolutionary baselines, and the Invader Relative Impact Potential was suggested as a metric for understanding the ecological impacts of alien species (Dick et al., 2017). This approach has been recognized as a reliable tool for explaining the effects of existing alien species and predicting the potential future invaders from a plethora of taxa under a wealth of different contexts such as habitat complexity, temperature and dissolved oxygen regimes, water chemistry gradients, higher order predators, and parasites (reviewed by Dickey et al., 2020).
A large array of studies also attempted at finding traits to predict invasiveness (i.e. establishment and spread of new aliens); many of those, however, have failed to robustly predict ecological impact of species spanning diverse taxonomic and trophic groups, and no correlations between invasiveness and ecological impact were detected (Dickey et al., 2020; Ricciardi et al., 2021, and references therein).
Thus, the general predictive understanding of the ecological impacts of non-native species in aquatic ecosystems has been slow to mature (Ricciardi et al., 2013; Dickey et al., 2018; Vimercati et al., 2020). Therefore, for the variable, species-rich and heterogeneous plankton communities, simple and user-friendly metrics for the invaders' impact assessment are still rather scarce (Telesh et al., 2001; Laxson et al., 2003; Dick et al., 2017; Dickey et al., 2020; Ricciardi et al., 2021).
Trophic dynamics and invasion theory allow for evaluating the impact of carnivorous alien zooplankters on pelagic communities
Planktonic predators provide top-down control of grazers thus affecting directly the productivity of herbivorous zooplankton, which serves as basic food for pelagic fish, and indirectly influencing the primary productivity of phytoplankton, including the development of harmful blooms of various pro-tistan species and the cyanobacteria. Therefore, evaluation of the impact of carnivorous planktonic aliens is of utmost importance for both predicting the fish forage supply and forecasting harmful algal blooms.
By using the comparative functional response approach, a metric for evaluation ofthe effect ofcar-nivorous invasive zooplankters on native communities was suggested two decades ago (Telesh et al., 2001). However, since this method was first presented in the national Russian-language journal, here we provide an additional, detailed description of the calculation algorithm for this authentic metric.
The impact of the C. pengoi population on the structure and functioning of plankton community was assessed by calculating the Impact index (here and after: Ii; in the original version: I), which was developed using the data on C. pengoi in the Neva Estuary (the Gulf of Finland, the Baltic Sea). This algorithm was elaborated using the basic principles of invasion biology (Parker et al., 1999) as well as ecological physiology, trophic dynamics in food cha-
Fig. 1. The relations between biomass (B) of Cercopagispengoi and production (P) of rotifers and copepods Eurytemora affinis in the Vistula Lagoon. A — Correlation of the biomass of C. pengoi (Bcerco, mg/m3) with the average annual daily production rate of rotifers (Prot, cal/m3); B — shifted-data analysis correlates the C. pengoi biomass (B, mg/m3) in June with the daily production rate (P, cal/m3) of E. affinis during the preceding month, in May (calculated using the data from: Naumenko and Telesh, 2019).
ins, and production hydrobiology (Alimov, 2003). Applicability of the algorithm was verified by the data on the pelagic food-web dynamics in the Lake Ontario (Laxson et al., 2003).
Initially, Parker et al. (1999) proposed to view the impact (I) of an invader on the community of living organisms in a water body as the product of the invader's range (R), abundance (A) and per capita effect (E): I = R x A x E, later termed the "Parker-Lonsdale" equation. Telesh et al. (2001) suggested the assessment of the impact as a modification of the Parker-Lonsdale equation (Parker et al., 1999). Specifically, in the case when the population of C. pengoi inhabits the entire study region (e.g., in the Vistula Lagoon), in this modified calculation algorithm the parameter R (range) was skipped. Additionally, the authors infer that the share of the invader in the overall zooplankton abundance reflects the role of C. pengoi in plankton community more precisely than the absolute value of its abundance (A). The per capita effect (E) of C. pengoi was measured by calculating the ratio of its daily consumption rate to daily production rate ofits preys. Thus, unlike the Parker-Lonsdale equation, the modified metric of the impact (Ii) considers not the absolute but the relative values ofthe parameters, namely: the contribution of C. pengoi to overall zooplankton abundance, and the ratio of the daily consumption rate of Cercopagis to the production rate ofits potent prey organisms (Telesh et al., 2001):
H = Ncerco / N) X (C / PJ,
(1)
where Ii is Impact index, a measure of predation pressure of Cercopagis on zooplankton (a dimen-sionless value); N is the maximum abundance
' ' cerco
of C. pengoi (ind/m3); Nz is the total abundance of zooplankton (ind/m3) at the date when N is
cerco
maximal; C is the daily consumption rate of C.
cerco
pengoi (cal/m3), and Phz is the daily production rate of herbivorous zooplankton that C. pengoi might feed on (cal/m3).
Based on the data from the literature and own results described in Laxson et al. (2003), all non-predatory cladocerans, nauplia of copepods, cope-podites I—III, and I—VI stages of the calanoid copepods (Eurytemora affinis, Acartia tonsa) were considered as potent prey organisms for Cercopagis. The index Ii is assessed for the periods (dates) of maximum population density of the invader during summer seasons.
Calculation of the Impact index using the data from the Neva Estuary and the eastern Gulf of Finland (Telesh et al., 2001), the Vistula Lagoon (Naumenko and Telesh, 2019), the central Gulf of Finland and the open Baltic Sea (Litvinchuk and Telesh, 2006) demonstrated long-term dynamics ofthe effects of non-indigenous cladoceran C. pengoi on native zooplankton communities. Using the most recent data from the Vistula Lagoon (Naumenko and Telesh, 2019), it was possible to show that the biomass of C. pengoi strongly (R2 = 0.87, p < 0.05) correlated positively with the daily production rate of rotifers, their potent preys, and this relation can be described by the binomial equation (Fig. 1, A). Moreover, the shifted-data meta-analysis of
Fig. 2. The monthly average daily production rate of Eurytemora affinis (Peuryt, cal/m3) and predation pressure of Cercopagis pengoi expressed as the Impact index during the same months in the Vistula Lagoon. Impact values (Impact x 100) were averaged for each month when the annual maxima of C. pengoi abundance were observed (n=2 in May, July and August; n=10 in June). Based on the data from Naumenko and Telesh (2019).
the same database (Naumenko and Telesh, 2019) demonstrated strong correlation (R2 = 0.74, p < 0.05) between the biomass of C. pengoi in June and the daily production rate of E. affinis during the preceding month (May) in the Vistula Lagoon (Fig. 1, B).
Moreover, the results showed that the maximum Ii values were usually registered in June, and during the succeeding months, in July and August, i.e. after the highest predation pressure of C. pengoi, the productivity of E. affinis decreased substantially (Fig. 2).
These results allow suggesting that nauplial stages and juveniles of E. affinis were the preferable food for Cercopagis in the Vistula Lagoon. Importantly, the data also confirmed that the share of C. pengoi in the overall biomass of cladocerans has been increasing exponentially during the recent two decades; meanwhile, the specific daily production rate of E. affinis has been decreasing (R2 = 0.97, p < 0.05) since 1999 (see Fig. 7 in Naumenko and Telesh, 2019). Thus, elimination of nauplia and younger copepodites ofthe grazer E. affinis by the planktonic predator C. pengoi impacted the pelagic community significantly and might have caused serious alterations in the overall plankton community structure, primary productivity of phytoplankton, production of copepods, and availability of fish food supply.
Biological invasions in plankton cause controversial effects that trigger ecosystem alterations
The unprecedented rate of human-mediated species introductions into new environments over recent centuries has numerous far-reaching consequences, including impacts on human health and the economy, and alterations ofrecipient ecosystems (Perrings, 2002; Ojaveer et al., 2021). Biological invasions can have important effects on the structure and integrity of native communities, and these effects often extend beyond their most frequently documented direct ecological modifications (Feit et al., 2018; Telesh et al., 2019). In particular, the invaders can cause rapid and long-lasting changes to the structure and functions of ecosystems — the so-called regime shifts, with major implications for biodiversity, ecosystem services, and human wellbeing and livelihoods (Shackleton et al., 2018; Ricciardi et al., 2021).
The impact of the invaders can differ in various environmental conditions, different habitats and communities, depending on the ecological niche dimensions of the alien species. The ecological niche of the predatory fishhook water flea C. pengoi is rather broad. For example, C. pengoi is highly tolerant to a wide range of salinities and can inhabit both fresh waters, e.g. the Great Laurentian Lakes (MacIsaac et al., 1999; Laxson et al., 2003), and marine environments such as the Southern Caspian Sea with salinity of 121 (Bagheri et al., 2014). Recent studies in the brackish-water Neva Estuary (eastern Gulf of Finland, the Baltic Sea) showed that biomass of C. pengoi was the highest at salinity ca. 2.6 and water temperature around 18 °C (Golubkov et al., 2020). These results are consistent with the earlier findings showing that C. pengoi has a broad ecological niche. Thus, in different areas of the Baltic Sea, this invader has been registered at salinities 0.3—6.0 in a wide range of temperatures: 4-24 °C (Krylov et al., 1999; Ojaveer et al., 2004; Litvinchuk and Telesh, 2006; Bielecka et al., 2014; Rowe et al., 2016; Helenius et al., 2017; Naumenko, 2018).
1 Salinity is reported using the Practical Salinity Scale approved by the Joint Panel of Oceanographic Tables and
Standards, according to which salinity is defined as a pure ratio, and has no dimensions or units.
The ecological impacts ofnonindigenous species in marine ecosystems include but are not limited to alteration of biodiversity and food webs, habitats and community structure, displacement of native species due to competition and predation, as well as the spread of disease agents (Bax et al., 2003; Litchman, 2010; Telesh et al., 2016, 2020; Olenin et al., 2017). As shown recently, the diverse and highly productive mesozooplankton of the Vistula Lagoon harbors 74 species, including rotifers (36), cladocerans (16) and copepods (22 species) (Naumenko and Telesh, 2019). The latter study confirmed that in this shallow brackish lagoon, C. pengoi usually appeared in plankton in May when water warmed up to 15 °C, as shown earlier by Naumenko (2018), and reached their maximum in June, occupying a comfortable niche in the abundant, species-rich and productive community at temperatures not exceeding 20 °C. Moreover, the monthly averaged values of abundance, biomass and productivity of E. affinis, C. pengoi, and A. tonsa (another common and abundant non-indigenous species in the Vistula Lagoon, see Khanaychenko et al., 2019, and references therein) demonstrated a clear seasonal demarcation of their populations.
High Impact index values, calculated according to Telesh et al. (2001) during the maximum population development of C. pengoi, and sharp decline of daily production rate of E. affinis after the population peak of this invasive predator confirmed that nauplii and juveniles of E. affinis were the preferable food items for Cercopagis in the Vistula Lagoon (Naumenko and Telesh, 2019). Meanwhile, the copepods A. tonsa were on average 10 times less abundant, compared to E. affinis. However, the results allow assuming that during their maximum productivity in July, A. tonsa can also contribute significantly as prey and have a potential to sustain the population of C. pengoi later in the season, during July and August.
These results (Naumenko and Telesh, 2019) are consistent with the earlier studies that used stable isotopes to demonstrate food-web changes after the Baltic Sea invasion by C. pengoi (Gorokhova et al., 2005). The laboratory experiments revealed effective consumption of the nauplii and copepodites of E. affinis by C. pengoi (Simm et al., 2006; Lehtiniemi and Gorokhova, 2008). The recent findings in the Vistula Lagoon support those previous results by showing additionally that in certain regions of the Baltic Sea, naturalization of C. pengoi might have caused the population decline of the common
pelagic copepods E. affinis that serve as prey not only for Cercopagis but also for planktivorous fish (Naumenko and Telesh, 2019). In this context, the latter results that demonstrated certain periodicity in the development of C. pengoi population and revealed the statistically reliable increase in the share of this predator in zooplankton of the Vistula Lagoon can inform the future prognostic modeling of the impact of this invader on the planktivorous fish stock and yield.
However, so far any forecasts of the putative long-term population development of C. pengoi face certain challenges because the effects of this introduction to the Baltic Sea have been multidirectional and sometimes controversial. Moreover, complexity of biotic interactions in plankton that are nonlinear and even chaotic as well as numerous confounding environmental factors act as strong external stressors that affect the invaders' impact on native communities (Telesh et al., 2019).
In Figure 3, we summarized the positive and negative ecosystem effects of C. pengoi on the recipient plankton communities and outlined its cumulative role as a nuisance ecosystem modifier.
The major positive effect of this invasion is the enrichment of plankton diversity by a new invertebrate predator, which restructured the pelagic food web thus enhancing stability of zooplankton community in stressful conditions (Naumenko and Telesh, 2019). This alien also increased food competition in the plankton and bentho-pelagic ecosystems between several invertebrates and fish species (Kotta et al., 2004; Ojaveer et al., 2004), stimulating energy turnover through the community and enhancing benthic-pelagic coupling. Another positive role ofthis invader is that in late summer and early autumn, it can constitute a large proportion in the diet of major planktivorous fish species of the Baltic Sea, e.g., the sticklebacks Gasterosteus acu-leatus and Pungitius pungitius, the Atlantic herring Clupea harengus and the European sprat Sprattus sprattus (Gorokhova et al., 2004; Ojaveer et al., 2004). C. pengoi can make up to 83% of the diet of large (adult) herring (Ojaveer and Lumberg, 1995) and up to 100% ofthe diet ofnine-spined stickleback and bleak in the Baltic Sea (Lankov et al., 2010).
Negative effects of C. pengoi are also numerous and, therefore, alarming (Fig. 3). Predation of C. pengoi on herbivorous copepods and cladocerans eliminates the phytoplankton grazers and thus promotes modifications in the pelagic community structure favoring the enhanced primary production and
Fig. 3. Major positive and negative effects and cumulative role of Cercopagis pengoi in the recipient communities. Images: female of C. pengoi with one resting egg in the brood pouch (a); female with two resting eggs (b); male (c); female body, with embryos in the brood pouch (d); juvenile specimen at stage I (e). Photos I.V. Telesh (a, d-e), scales (d, e): ^m. Drawings (b, c): modified from Telesh and Heerkloss (2004).
algal blooms in the low-salinity environments (Naumenko and Telesh, 2019). These devastating effects have a potential to initiate secondary (biological) pollution and cause water quality deterioration (Telesh, 2018).
To date, the most important negative effect of C. pengoi is the elimination of planktonic rotifers, cladocerans and juvenile copepods; this suppression deteriorates the food supply for planktivorous fish and, therefore, threatens fishery in the Vistula Lagoon. Moreover, even though C. pengoi is an acceptable food source for some fish, as mentioned above, many fish species avoid feeding on these cladocerans and demonstrate negative values of the electivity index (Lankov et al., 2010). Besides, as shown earlier, C. pengoi can injure fish stomachs by its long and sharp hooked caudal spine (Antsulevich and Valipakka, 2000; Leppakoski and Olenin, 2000). Finally, they clog and foul fishing nets causing harm to fisheries accompanied by economic losses (Ojaveer and Lumberg, 1995; Krylov et al., 1999).
Due to the accumulated data, C. pengoi along withjust a few other invaders (Dreissena polymorpha, Marenzelleria spp. and Neogobius melanostomus) was named as the nonindigenous species that has the substantial knowledge base with over 100 impact
records and with more than ten papers published on their biological and ecological effects (Ojaveer et al., 2021). Meanwhile, it is worthy of note that despite being the only one nonindigenous species that is likely to have a strong impact on ecosystem functioning in the pelagic zone of the Baltic Sea (Olenin et al., 2017), according to the present knowledge, C. pengoi is not considered as a serious threat to aquatic ecosystems globally (Vilizzi et al., 2021).
The putative effects of carnivorous planktonic aliens on the future invasions, community structure and harmful dinoflagellate blooms
Currently, we only can speculate that the greatest challenge for the future of the Baltic coastal lagoons, e.g., the eastern Gulf of Finland or the Vistula Lagoon, can be the potent invasion by the bloom-forming dinoflagellates Prorocentrum cor-datum that so far have not yet populated these low-salinity environments (Golubkov et al., 2019; Kownacka et al., 2020; E. Naumenko, pers. com.). Meanwhile, the natural salinity tolerance range of P. cordatum is very broad: in the Baltic Sea waters, these flagellates prosper at salinities 2—22; however, their
Table 1. The minimum and maximum values of water temperature (T, °C) and salinity range of occurrence of Prorocentrum cordatum and Cercopagis pengoi in the Baltic Sea, and survival of
Acartia tonsa in the experiments.
Species T, °C Salinity References
Prorocentrum cordatum 3.0 - 24.0 2.0 - 22.0 Telesh et al., 2016
Cercopagis pengoi 4.0 - 24.0 0.3 - 6.0 Golubkov et al., 2020 (and references therein)
Acartia tonsa 5.0 - 34.0 6.0 - 30.0 Peck et al., 2015 (and references therein)
optimum salinity range, which allows for blooming, is much narrower: 6.1—9.7 (Telesh et al., 2016). The lower segment of the salinity tolerance range of P. cordatum partly coincides with that of C. pengoi in the Baltic Sea: 0.3-6.0 (Golubkov et al., 2020, and references therein) (Table 1).
Moreover, the common in the Baltic Sea and abundant non-indigenous calanoid copepods A. tonsa are known as effective grazers of P. cordatum (reviewed by Khanaychenko et al., 2019). This and other typical representatives of both graspers and filtrators among calanoid copepods can graze on P. cordatum either selectively or non-selectively. Importantly, the copepods do not avoid these dinoflagellates in the mixture with other food particles, perceiving them as non-toxic edible micro-algae. Therefore, the trophic structure of plankton likely determines the harmful algal blooms' development, magnitude and duration due to the complex interplay of external triggers and internal driving forces ofplankton dynamics within the communities (Telesh et al., 2019, 2021). Indeed, one should expect that, in the cases when the grazing pressure on the blooming dinoflagellates is high enough to restrict their excessive growth rate, the bloom does not develop or, once started, it terminates quickly. However, so far the evidences of the role of grazers in controlling the dynamics of Prorocentrum blooms are rare and largely controversial (Khanaychenko et al., 2019, and references therein).
Besides, the comparison of ecological niche dimensions of A. tonsa and C. pengoi in the Baltic Sea with environmental preferences of P. cordatum demonstrates low capacity of the latter population to be top-down controlled by the planktonic crustaceans. Specifically, we compared water temperature and salinity preferences, i.e. optimum values for population development ofthese nonindigenous species in the Baltic Sea; for A. tonsa, the same parameters during the optimum egg production
rate in the experiments (Peck et al., 2015) were considered (Fig. 4).
This comparison allows concluding that the mixotrophic, potentially toxic bloom-forming dinoflagellates P. cordatum and the herbivorous calanoid copepods A. tonsa have similar ranges of preferable water temperatures (16—25 °C) that partly coincide with that of C. pengoi, and comparable lower temperature tolerance limits (Table 1, Fig. 4). However, the optimum salinities for all three species differ substantially and do not overlap at all. In particular, the range of salinity values allowing for bloom development of P. cordatum in the Baltic Sea is rather narrow: 7.9 ± 1.8 (Telesh et al., 2016). The optimum salinities for C. pengoi in this water body are 0.4—4.3 (Golubkov et al., 2020), and for A. tonsa, the preferable salinities are 10.0—20.0 (Peck et al., 2015). Thus, the co-occurrence and, consequently, the suppression of P. cordatum population by planktonic crustaceans nowadays is unlikely, neither through grazing by A. tonsa nor due to community restructuring effects caused by C. pengoi.
Nevertheless, the extreme survival ranges of the major abiotic characteristics of these planktonic invaders in the Baltic Sea are very wide, and their lower salinity tolerance limits are largely overlapping (Table 1). Thus, in the future the putative coexistence of P. cordatum, C. pengoi and A. tonsa in the shallow brackish-water Baltic coastal environments, e.g., in the Vistula Lagoon or in the eastern Gulf of Finland, is highly probable because of the ongoing desalinization of the Baltic Sea coastal waters due to changing climate (Rajasilta et al., 2014; Vuorinen et al., 2015). In the latter case, the elimination of herbivorous cladocerans and other grazers by C. pen -goi would presumably favor phytoplankton proliferation, including the potentially toxic bloom-forming dinoflagellates, and could thus trigger the formation of devastating red tides in the oligohaline coastal waters and lagoons of the Baltic Sea.
Fig. 4. Schematic representation ofwater temperature/salinity preferences (i.e. optimum values for population development) of three non-indigenous planktonic species in the Baltic Sea: the fishhook water flea Cercopagis pengoi, the dinoflagellates Prorocentrum cordatum, and the calanoid copepods Acartia tonsa (for A. tonsa, the egg production rate in the experiments was considered; data from: Peck et al., 2015). The dotted lines and the diagonally striped areas in the water temperature/salinity 'niches' of A. tonsa and C. pengoi indicate the water temperature range, which overlaps with the relevant characteristic for P. cordatum. The broken lines indicate the lower temperature tolerance limits. Images: C. pengoi, female body, with embryos in the brood pouch, scale bar 300 ^m, photo I.V. Telesh; P. cordatum, live cell, scale bar 20 ^m, from open sources; A. tonsa, photo courtesy of L.S. Svetlichny.
Outlook
The current knowledge of the ecosystem effects of the nuisance unicellular species (the potentially toxic bloom-forming dinoflagellates Prorocentrum cordatum) and multicellular invaders (the carnivorous fishhook water flea Cercopagis pengoi) allows concluding about the increasing role of invasive species in plankton of the Baltic Sea estuaries and coastal lagoons. Because of broad ecological niches of these aliens, biotic interactions rather than external environmental stressors can be considered as the primary drivers of plankton dynamics, composition, abundance, and productivity. The basic principles of invasion biology, ecological physiology, and production hydrobiology promote the current and future assessments of the impact of planktonic non-
indigenous species on the native communities. Summarizing the multiple effects of C. pengoi, one of the most influential pelagic invaders in the Baltic Sea, we can conclude that its cumulative role is the nuisance ecosystem modifier. The recent data from the Vistula Lagoon show that the contribution of this alien species to the overall cladoceran biomass has been consistently increasing during the past two decades. Therefore, we can infer that in the future, top-down control ofplanktonic grazers by C. pengoi will possibly contribute to the deterioration of fish food supply and presumably restructure the pelagic community in a way, which can promote harmful algal blooms and new protistan alien species introductions to the Baltic coastal waters. The robust evaluation of trophic interactions in plankton by using the available impact assessment frameworks and reliable metrics, experimental results and field
studies could inform the future prognostic modeling ofthe invaders' effects on the timing and magnitude ofred tides as well as on the perspectives offish stock and yield in the Baltic Sea and beyond.
Acknowledgements
This research was funded in parts by the Russian Foundation for Basic Research (project 19-0400217), and the Ministry of Science and Higher Education of the Russian Federation (project AAAA-A19-119020690091-0; use of the basic equipment). The English language in the manuscript was checked by the "Effective Language Tutoring Services".
References
Alimov A.F. 2003. Towards a theory of the functioning of aquatic ecosystems. Backhuys Publishers, Leiden. https://searchworks.stanford. edu/view/5546512
Anderson C.R., Berdalet E., Kudela R.M., Cusak C.K., Silke J., O'Rourke E. et al. 2019. Scaling up from regional case studies to a global Harmful Algal Bloom observing system. Front. Mar. Sci. 6, 250. https://doi.org/10.3389/fmars.2019.00250 Antsulevich A. and Valipakka P. 2000. Cercopagis pengoi — new important food object of the Baltic herring in the Gulf of Finland. Int. Rev. Hydrobiol. 85(5-6), 609—619. D0I:10.1002/1522-2632(200011)85:5/6<609::AID-IR0H609>3.0. CO; 2-S
Bagheri S., Niermann U., Mansor M. and Yeok F.S. 2014. Biodiversity, distribution and abundance of zooplankton in the Iranian waters of the Caspian Sea off Anzali during 1996—2010. J. Mar. Biolog. Assoc. U.K.. 94, 129—140. https://doi.org/10.1017/ S0025315413001288
Barton P.S., Cunningham S.A., Manning A.D., Gibb H., Lindenmayer D.B., Raphael K. and Didham R.K. 2013. The spatial scaling of beta diversity. Global Ecol. Biogeogr. 22, 639—647. https: //doi.org/10.1111/geb.12031
Bax N., Williamson A., Aguero M., Gonzalez E. and Geeves W. 2003. Marine invasive alien species: a threat to global biodiversity. Marine Policy. 27 (4), 313—323. https://doi.org/10.1016/S0308-597X (03)00041-1
Bielecka L., Krajewska-Soltys A. and Mudrak-Cegiolka S. 2014. Spatial distribution and population characteristics of the invasive cladoceran Cercopagis pengoi in the Polish coastal zone seven years after the first record. Oceanol Hydrobiol Stud. 43, 201-210. https://doi.org/10.2478/s13545-014-0134-y Blackburn T.M., Essl F., Evans T., Hulme P.E., Jeschke J.M., Kühn I. et al. 2014. A unified classification of alien species based on the magnitude of their environmental impacts. PLOS Biol. 12 (5), e1001850. https://doi.org/10.1371/journal.pbio. 1001850
Borza P., Arbaciauskas K. and Zettler M.L. 2021. Multidimensional niche differentiation might buffer invasion impacts: the case of oligohaline corophiids (Crustacea: Amphipoda) in the Baltic Sea. Biol. Invasions. 23, 1891-1900. https://doi. org/10.1007/s10530-021-02479-7
Chesson P. 2000. Mechanisms of maintenance of species diversity. Annu. Rev. Ecol. Syst. 31, 343366. https://www.annualreviews.org/doi/abs/10. 1146/annurev.ecolsys.31.1.343
Crystal-Ornelas R. and Lockwood J.L. 2020. The 'known uknowns' of invasive species impact measurement. Biol. Invasions. 22, 1513-1525. https://doi.org/10.1007/s10530-020-02200-0
Darling J.A. and Carlton J.T. 2018. A framework for understanding marine cosmopolitanism in the Anthropocene. Front. Mar. Sci. 5, 293. https://doi. org/10.3389/fmars.2018.00293
Dgebuadze Yu.Yu. and Feniova I.Yu. 2009. Stochastic and deterministic mechanisms structuring aquatic communities invaded by alien species. Biological invasions: Towards a Synthesis. NeoBiota. 8, 61-74.
Dick J.T.A., Laverty C., Lennon J.J., Barrios-O'Neill D., Mensink P.J., Britton J.R. et al. 2017. Invader relative Impact Potential: a new metric to understand and predict the ecological impacts of existing, emerging and future invasive alien species. J. Appl. Ecol. 54, 1259-1267. https://doi.org/ 10.1111/1365-2664.12849
Dickey J.W.E., Cuthbert R.N., Rea M., Laverty C., Crane K., South J. et al. 2018. Assessing the Relative potential ecological impacts and invasion risks of emerging and future invasive alien species. NeoBiota. 40, 1-24. https://doi.org/10.3897/neo-biota.40.28519
Dickey J.W.E., Cuthbert R.N., South J., Britton J.R., Caffrey J., Chang X. et al. 2020. On the RIP: using Relative Impact Potential to assess the
ecological impacts of invasive alien species. Neo-Biota. 55, 27-60. https://doi.org/10.3897/neo-biota.55.49547
Dupont C.L., Larsson J., Yooseph S., Ininbergs K., Goll J. et al. 2014. Functional tradeoffs underpin salinity-driven divergence in microbial community composition. PLOS ONE. 9(2), e89549. http://dx. doi.org/10.1371/journal.pone.0089549
Elliott M. 2003. Biological pollutants and biological pollution — an increasing cause for concern. Mar. Pollut. Bull. 46, 275—280. DOI: 10.1016/S00 25-326X(02)00423-X
Feit B., Gordon C.E., Webb J.K., Jessop T.S., Laffan S.W., Dempster T. and Letnic M. 2018. Invasive cane toads might initiate cascades of direct and indirect effects in a terrestrial ecosystem. Biol. Invasions. 20, 1833—1847. https://doi.org/10.1007/ s10530-018-1665-8
Glibert P.M. 2020. Harmful algae at the complex nexus of eutrophication and climate change. Harmful Algae. 91, 101583. https://doi.org/10.1016/ j.hal.2019.03.001
Golubkov M.S., Litvinchuk L.F. and Golubkov S.M. 2020. Effects of environmental gradients on the biomass of alien Cercopagis pengoi in the Neva Estuary. Front. Mar. Sci. 7, 573289. https://doi.org/ 10.3389/fmars.2020.573289
Golubkov M., Nikulina V. and Golubkov S. 2019. Effects of environmental variables on midsummer dinoflagellate community in the Neva Estuary (Baltic Sea). Oceanologia. 61, 197—207. https://doi. org/10.1016/j.oceano.2018.09.001
Gorokhova E., Fagerberg T. and Hansson S. 2004. Predation by herring (Clupea harengus) and sprat (Sprattus sprattus) on Cercopagis pengoi in a western Baltic Sea bay. ICES J. Mar. Sci. 61, 959— 965. https://doi.org/10.1016/jicesjms.2004.06.016 Gorokhova E., Hansson S., Höglander H. and Andersen C.M. 2005. Stable isotopes show food web changes after invasion by the predatory cladoceran Cercopagis pengoi in a Baltic Sea bay. Oecologia. 143, 251—259. https://www.jstor.org/stable/20062243
Helenius L.K., Leskinen E., Lehtonen H. and Nurminen L. 2017. Spatial patterns of littoral Zooplankton assemblages along a salinity gradient in a brackish sea: A functional diversity perspective. Estuar. Coast. Shelf Sci. 198, 400—412. http://dx. doi.org/10.1016/j.ecss.2016.08.031
Herlemann D.P.R., Labrenz M., Jürgens K., Bertilsson S., Waniek J.J. and Andersson A.F. 2011. Transitions in bacterial communities along
the 2000 km salinity gradient of the Baltic Sea. ISME J. 1571-1579. http://dx.doi.org/10.1038/ ismej.2011.41
Herlemann D.P.R., Woelk J., Labrenz M. and Jürgens K. 2014. Diversity and abundance of "Pelagibacterales" (SAR11) in the Baltic Sea salinity gradient. Systematic and Applied Microbiology. 37, 601-604. https://doi.org/10.1016/j.syapm.2014. 09.002
Jeschke J.M., Bacher S., Blackburn T.M., Dick J.T.A., Essl F., Evans T. et al. 2014. Defining the impact ofnon-native species. Conservation Biology. 28, 1188-1194. https://doi.org/10.1111/cobi.12299 Khanaychenko A.N., Telesh I.V. and Skarlato S.O. 2019. Bloom-forming potentially toxic dinoflagellates Prorocentrum cordatum in marine plankton food webs. Protistology. 13 (3), 95-125. doi:10.2 1685/1680-0826-2019-13-3-1
Knyazev N.A., Pechkovskaya S.A., Skarlato S.O., Telesh I.V. and Filatova N.A. 2018. The impact oftemperature stress on DNA and RNA synthesis in potentially toxic dinoflagellates Prorocentrum minimum. J. Evol. Biochem. Physiol. 54 (5), 383-389. doi:10.1134/S002209301805006X
Kotta J., Simm M., Kotta I., Kanosina I., Kallaste K. and Raid T. 2004. Factors controlling long-term changes ofthe eutrophicated ecosystem of Pärnu Bay, Gulf of Riga. Hydrobiologia. 514, 259268. doi:10.1023/B:hydr.0000018224.56324.44
Kownacka J., Calkiewicz J. and Kornijyw R. 2020. A turning point in the development ofphyto-plankton in the Vistula Lagoon (southern Baltic Sea) at the beginning of the 21st century. Oceanologia. 62, 538-555. https://doi.org/10.1016/j.oceano. 2020.08.004
Krylov P.I., Bychenkov D.E., Panov V.E., Rodionova N.V. and Telesh I.V. 1999. Distribution and seasonal dynamics of the Ponto-Caspian invader Cercopagis pengoi (Crustacea, Cladocera) in the Neva Estuary (Gulfof Finland). Hydrobiologia. 393, 227-232. doi:10.1023/A:1003558919696
Lankov A., Ojaveer H., Simm M., Pöllupüü M. and Möllmann C. 2010. Feeding ecology of pelagic fish species in the Gulf of Riga (Baltic Sea): The importance of changes in the zooplankton community. J.Fish Biol. 77(10), 2268-2284. https:// doi.org/10.1111/j.1095-8649.2010.02805.x
Larson C.A. and Belovsky G.E. 2013. Salinity and nutrients influence species richness and evenness of phytoplankton communities in microcosm experiments from Great Salt Lake, Utah, USA. J.
Plankton Res. 35(5), 1154-1166. https://doi.org/ 10.1093/plankt/fbt053
Laxson C.L., McPhedran K.N., Makarewicz J.C., Telesh I.V. and MacIsaac H.J. 2003. Effects of the nonindigenous cladoceran Cercopagis pengoi on the lower food web of Lake Ontario. Freshwat. Biol. 48, 2094-2106. https://doi.org/10.1046Xj.1365-2427.2003.01154.x
Lehtiniemi M. and Gorokhova E. 2008. Predation of the introduced cladoceran Cercopagis pengoi on the native copepod Eurytemora affinis in the northern Baltic Sea. Marine Ecology Progress Series. 362, 193-200. https://doi.org/10.3354/meps07441 Leppäkoski E. and Olenin S. 2000. Non-native species and rates of spread: lessons from the brackish Baltic Sea. Biol. Invasions. 2, 151-163. doi: 10.1023/ A:1010052809567
Litchman E. 2010. Invisible invaders: nonpathogenic invasive microbes in aquatic and terrestrial ecosystems. Ecology Letters. 13, 1560-1572. https:// doi.org/10.1111/j.1461-0248.2010.01544.x
Litchman E., Edwards K.F., Klausmeier C.A. and Thomas M.K. 2012. Phytoplankton niches, traits and eco-evolutionary responses to global environmental change. Mar. Ecol. Prog. Ser.. 470, 235-248. https://doi.org/10.3354/meps09912
Litvinchuk L.F. and Telesh I.V. 2006. Distribution, population structure and ecosystem effects of the invader Cercopagis pengoi (Polyphemoidea, Cladocera) in the Gulf of Finland and the open Baltic Sea. Oceanologia. 48, 243-257. https://www. iopan.pl/oceanologia/48_S.html#A14
MacIsaac H.J., Grigorovich I.A., Hoyle J.A., Yan N.D. and Panov V.E. 1999. Invasion of Lake Ontario by the Ponto-Caspian cladoceran predator Cercopagis pengoi. Can. J. Fish. Aquat. Sci. 56, 1-5. https://doi.org/10.1139/cjfas-56-1-1
Matantseva O., Pozdnyakov I., Voss M., Liskow I. and Skarlato S. 2018. The uncoupled assimilation of carbon and nitrogen from urea and glycine by the bloom-forming dinoflagellate Prorocentrum minimum. Protist. 169(5), 603-614. https://doi.org/10. 1016/j.protis.2018.05.006
Matantseva O., Skarlato S., Vogts A., Pozdnyakov I., Liskow I., Schubert H. and Voss M. 2016. Superposition of individual activities: urea-mediated suppression ofnitrate uptake in the dinoflagellate Prorocentrum minimum revealed at the population and single-cell levels. Front. Microbiol. 7, 1310. https://doi.org/10.3389/fmicb.2016.01310
Naumenko E.N. 2018. Seasonal and long-term dynamics of population abundance of the invasive
species Cercopagis pengoi (Ostroumov, 1891) in the Vistula (Kaliningrad) Lagoon of the Baltic Sea. Rus. J. Biol. Invasions. 9(2), 147—154. https://link. springer.com/article/10.1134/S2075111718020 08X
Naumenko E.N. and Polunina Yu.Yu. 2000. Cercopagis pengoi (Ostroumov, 1891) (Crustacea, Cladocera) — new invader in the Vistula Lagoon of the Baltic Sea. In: Alien Species in the European Seas of Russia, Apatity, pp. 121—130 (in Russian).
Naumenko E.N. and Telesh I.V. 2019. Impact of the invasive species Cercopagis pengoi (Ostroumov, 1891) on the structural and functional organization of zooplankton in the Vistula Lagoon of the Baltic Sea. Rus. J. Biol. Invasions. 10(3), 246—257. http://link. springer.com/article/10.1134/S2075111719030081 Ojaveer H., Kotta J., Outinen O., Einberg H., Zaiko A. and Lehtiniemi M. 2021. Meta-analysis on the ecological impacts of widely spread non-indigenous species in the Baltic Sea. Sci. Total Environ. 786, 147375. https://doi.org/10.1016/). scitotenv.2021.147375
Ojaveer H. and Lumberg A. 1995. On the role of Cercopagis (Cercopagis) pengoi (Ostroumov) in Parnu Bay and the NE part of the Gulf of Riga ecosystem. Proc. Estonian Acad. Sci. Ser. Ecol. 5, 20—25. https://www.researchgate.net/publication /29725481
Ojaveer H., Simm M. and Lankov A. 2004. Population dynamics and ecological impact of the nonindigenous Cercopagis pengoi in the Gulf of Riga (Baltic Sea). Hydrobiologia. 522, 261—269. doi: 10. 1023/B:HYDR.0000029927.91756.41
Olenin S., Gollasch S., Lehtiniemi M., Sapota M. and Zaiko A. 2017. Biological invasions. In: Biological Oceanography of the Baltic Sea (Eds: Snoeijs-Leijonmalm P., Schubert H. and Rad-ziejewska T.). Springer Science+Business Media, Dordrecht, pp. 193—232. https://link.springer.com/ chapter/10.1007/978-94-007-0668-2_5
Olenina I., Wasmund N., Hajdu S., Jurgensone I., Gromisz S., Kownacka J. et al. 2010. Assessing impacts of invasive phytoplankton: the Baltic Sea case. Mar. Pollut. Bull. 60, 1691—1700. https://doi. org/10.1016/j.marpolbul.2010.06.046
Olli K., Klais R., Tamminen T., Ptacnik R. and Andersen T. 2011. Long term changes in the Baltic Sea phytoplankton community. Boreal Environ. Res. 16 (Suppl. A), 3—14.
Parker I.M., Simberloff D., Lonsdale W.M., Goodell K., Wonham M., Kareiva P.M. et al. 1999. Impact: toward a framework for understanding the
ecological effects of invaders. Biol. Invasions. 1(1), 3—19. https://link.springer.com/article/10.1023% 2FA%3A1010034312781
Pechkovskaya S.A., Knyazev N.A.., Matantseva O.V., Emelyanov A.K., Telesh I.V., Skarlato S.O. and Filatova N.A. 2020. Dur3 and nrt2 genes in the bloom-forming dinoflagellate Prorocentrum minimum: Transcriptional responses to available nitrogen sources. Chemosphere. 241, 125083. https:// doi.org/10.1016/j.chemosphere.2019.125083
Peck N., Peters J., Diekmann R., Laakmann S. and Renz J. 2015. Interactive effects oftemperature and salinity on population dynamics ofthe calanoid copepod Acartia tonsa. J. Plankton Res. 37(1), 197—210. doi:10.1093/plankt/fbu093
Perrings C. 2002. Biological invasions in aquatic systems: The economic problem. Bull. Mar. Sci. 70 (2), 541—552. https://www.researchgate. net/publication/233675727
Rajasilta M., Hänninen J. and Vuorinen I. 2014. Decreasing salinity improves the feeding conditions of the Baltic herring (Clupea harengus membras) during spring in the Bothnian Sea, northern Baltic. ICES J. Mar. Sci. 71(5), 1148—1152. https://doi. org/10.1093/icesjms/fsu047
Ricciardi A., Hoopes M.F., Marchetti M.P. and Lockwood J.L. 2013. Progress toward understanding the ecological impacts of non-native species. Ecol. Monogr. 83, 263—282. https://doi.org/10.18 90/13-0183.1
Ricciardi A., Iacarella J.C., Aldridge D.C., Blackburn T.M., Carlton J.T., Catford J.A. et al. 2021. Four priority areas to advance invasion science in the face ofrapid environmental change. Environ. Rev. 29, 119—141. https://doi.org/10.1139/er-2020 -0088
Rowe O.F., Guleikova L., Brugel S., Byström P. and Andersson A. 2016. A potential barrier to the spread of the invasive cladoceran Cercopagis pengoi (Ostroumov 1891) in the Northern Baltic Sea. Reg. Stud. 3, 8—17. https://doi.org/10.1016Xj.rsma. 2015.12.004
Shackleton R.T., Biggs R., Richardson D.M. and Larson B.M.H. 2018. Social-ecological drivers and impacts of invasion-related regime shifts: consequences for ecosystem services and human wellbeing. Environ. Sci. Policy. 89, 300—314. https: //doi.org/10.1016/j.envsci.2018.08.005
Schubert H. and Telesh I. 2017. Estuaries and coastal lagoons. In: Biological Oceanography of the Baltic Sea (Eds: Snoeijs-Leijonmalm P., Schubert H. and Radziejewska T.). Springer Sci-
ence+Business Media, Dordrecht, pp. 483—509. https://doi.org/10.1007/978-94-007-0668-2_13
Schubert H., Telesh I., Nikinmaa M. and Skarlato S. 2017. Physiological adaptations. In: Biological Oceanography of the Baltic Sea (Eds: Sno-eijs-Leijonmalm P., Schubert H. and Radziejewska T.). Springer Science+Business Media Dordrecht, pp. 255-278. https://doi.org/10.1007/978-94-007-0668-2_7
Simberloff D. 2011. How common are invasion-induced ecosystem impacts? Biol. Invasions. 13, 1255-1268. https://link.springer.com/article/10. 1007/s10530-011-9956-3
Simm M., Lankov A., Pöllupüü M. and Oja-veer H. 2006. Estimation of consumption rates of the predatory cladoceran Cercopagis pengoi in laboratory conditions. In: Alien invasive species in the north-eastern Baltic Sea: population dynamics and ecological impacts (Eds: Ojaveer H. and Kotta J.). Estonian Marine Institute Report Series 14, Tallinn, pp. 42-47. https://www.etis.ee/Portal/ Publications/Display/e11afea1-91a4-4251-ac86-29f9ce51d91a
Skarlato S., Filatova N., Knyazev N., Berdieva M. and Telesh I. 2018a. Salinity stress response of the invasive dinoflagellate Prorocentrum minimum. Estuar. Coast. Shelf Sci. 211, 199-207. https://doi. org/10.1016/j.ecss.2017.07.007
Skarlato S.O., Telesh I.V., Matantseva O.V., Po-zdnyakov I.A., Berdieva M.A., Schubert H., Filatova N.A., Knyazev N.A. and Pechkovskaya S.A. 2018b. Studies of bloom-forming dinoflagellates Prorocentrum minimum in fluctuating environment: contribution to aquatic ecology, cell biology and invasion theory. Protistology. 12(3), 113-157. doi: 10.21685/1680-0826-2018-12-3-1
Telesh I.V. 2018. Cercopagis pengoi. In: The Most Dangerous Invasive Species in Russia (TOP-100) (Eds: Dgebuadze Yu.Yu., Petrosyan V.G. and Khlyap L.A.). KMK Publ., Moscow, pp. 379-384 (in Russian). http://www.sevin.ru/top100worst/ monograph.html
Telesh I.V., Bolshagin P.V. and Panov V.E. 2001. Quantitative estimation of the impact of the alien species Cercopagis pengoi (Crustacea: Ony-chopoda) on the structure and functioning of plankton community in the Gulf of Finland, Baltic Sea. Dokl. Biol. Sci. 377(1), 157-159. doi: 10.1023/ a:1019278212086
Telesh I.V. and Heerkloss R. 2004. Atlas of estu-arine zooplankton ofthe southern and eastern Baltic Sea. Part II: Crustacea. Naturwissenschaftliche
Forschungsergebnisse, Bd. 72. Verlag Dr. Kovac, Hamburg. https://www.verlagdrkovac.de/978-3-8300-1500-0.htm
Telesh I.V., Khanaychenko A.N. and Skarlato S.O. 2020. The interplay oftwo invaders: can blooms ofthe potentially toxic dinoflagellates Prorocentrum cordatum be downregulated by the neritic copepods Acartia tonsa? Protistology. 14(3), 103-111. doi:10. 21685/1680-0826-2020-14-3-1
Telesh I.V. and Ojaveer H. 2002. The predatory water flea Cercopagis pengoi in the Baltic Sea: invasion history, distribution and implications to ecosystem dynamics. In: Invasive Aquatic Species of Europe—Distribution, Impacts and Management (Eds: Leppäkoski E., Gollasch S. and Olenin S.). Kluwer Publishers, Dordrecht, pp. 62-65. https:// link.springer.com/chapter/ 10.1007/978-94-015-9956-6_7
Telesh I.V., Schubert H., Joehnk K.D., Heerkloss R., Schumann R., Feike M., Schoor A. and Skarlato S.O. 2019. Chaos theory discloses triggers and drivers of plankton dynamics in stable environment. Sci. Rep. 9, 20351. https://doi.org/ 10.1038/s41598-019-56851-8
Telesh I.V., Schubert H. and Skarlato S.O. 2011a. Revisiting Remane's concept: evidence for high plankton diversity and a protistan species maximum in the horohalinicum of the Baltic Sea. Mar. Ecol. Progr. Ser. 421, 1-11. https://doi.org/10.3354/ meps08928
Telesh I.V., Schubert H. and Skarlato S.O. 2011b. Protistan diversity does peak in the horohalinicum of the Baltic Sea: Reply to Ptacnik et al. (2011). Mar. Ecol. Progr. Ser. 432, 293-297. https: //doi.org/10.3354/meps09217
Telesh I., Schubert H. and Skarlato S. 2013. Life in the salinity gradient: Discovering mechanisms behind a new biodiversity pattern. Estuar. Coast. ShelfSci. 135, 317-327. http://dx.doi.org/10.1016/j. ecss.2013.10.013
Telesh I.V., Schubert H. and Skarlato S.O. 2016. Ecological niche partitioning of the invasive dinoflagellate Prorocentrum minimum and its native congeners in the Baltic Sea. Harmful Algae. 59, 100111. http://dx.doi.org/10.1016/j.hal.2016.09.006
Telesh I., Schubert H. and Skarlato S. 2021. Abiotic stability promotes dinoflagellate blooms in marine coastal ecosystems. Estuar. Coast. Shelf Sci. 251, 107239. https://doi.org/10.1016/). ecss.2021.107239
Vilizzi L., Copp G.H., Hill J.E., Adamovich B., Aislabie L., Akin D. et al. 2021. A global-scale screening of non-native aquatic organisms to identify potentially invasive species under current and future climate conditions. Sci. Total Environ. 788, 147868. https://doi.org/10.1016Zj.scitotenv.2021.147868
Vimercati G., Kumschick S., Probert A.F., Volery L. and Bacher S. 2020. The importance of assessing positive and beneficial impacts of alien species. NeoBiota. 62, 525-545. https://doi.org/ 10.3897/neobiota.62.52793
Vuorinen I., Hanninen J., Rajasilta M., Laine P., Eklund J., Montesino-Pouzols F., Corona F., Junker K., Meier H.E.M. and Dippner J.W. 2015. Scenario simulations of future salinity and ecological consequences in the Baltic Sea and adjacent North Sea areas - implications for environmental monitoring. Ecol. Indic. 50, 196-205. https://doi. org/10.1016/j.ecolind.2014.10.019
Address for correspondence: Irena V. Telesh. Zoological Institute RAS, Universitetskaya Emb. 1, 199034 St. Petersburg, Russia; e-mail: [email protected]
