Transitional waters, including coastal lagoons, brackish inlets and estuaries, are important and fragile ecosystems in the coastal landscape. They are largely influenced by freshwater inflows from the continental system interacting with marine waters. Estuaries are characterized by a specific and highly dynamic hydrological regime, which results in a complex and variable distribution of environmental factors, including water salinity and chemical composition, flows of organic and mineral matter, sedimentation intensity and sediment properties. Permanent fluxes of nutrients and organic matter support intensive nutrient cycling and result in high productivity (Levin et al. 2001; Elliot and Whitfield 2011). In general, estuarine biota are considered to have high abundance and biomass but low diversity (Levin et al. 2001; Tweedley et al. 2016), and salinity is commonly considered the key factor affecting the distribution of organisms in estuarine areas. The strong concurrent spatial and temporal gradients and variability in salinity (and therefore osmotic pressure on the organisms) and other related environmental factors inevitably result in structuring estuarine communities and, thus, the functioning of these ecosystems.
Most zonation and classification schemes proposed to date for transitional waters focus mainly on the hydrological regime and the mean salinity as generally the more obvious environmental factors. These schemes are, however, not applicable consistently to any type of estuarine system and do not always correspond to the observed distribution of biota along estuarine gradients (Taupp, Wetzel 2014; Udalov et al. 2021). Biologically relevant schemes taking into account the zonation of biotic communities are under development (Elliot and Whitfield 2011; Tweedley et al. 2016). Of these, the most widely known is a species minimum concept introduced by Remane (1934). Based on macrozoobenthos data for the Baltic Sea, he argued that marine metazoan species, as a rule, were never found in waters with salinities below 5–8, while freshwater organisms did not occur at salinities above 0.5. As a result, a zone with the lowest number of taxa occurred at salinities between 5 and 8, where a small group of true brackish-water organisms prevailed. Later, Khlebovich (1969) found that sharp changes in the ionic composition of seawater diluted with fresh water occur in this “critical salinity” zone. He further argued that these ionic changes constitute a physico-chemical barrier between marine and freshwater faunas. Kinne (1971) gave the name "horohalinicum" to the 5–8 segment of the salinity gradient. This specific water area with a narrow salinity range was treated as an ecological ‘‘border”, i.e., an ecotone that separated marine and freshwater faunas. Despite being widely applicable, this concept has been increasingly criticized. Studies conducted along the full salinity gradient across a number of estuarine systems provided no evidence of the existence of purely brackish species (Whitfield et al. 2012; and references therein). The other main objection to the Remane model is that it tends to portray a static picture based on some “averaged” salinity, while one of the most prominent characteristics of brackish zones in many estuaries is the lack of stability in salinity, with its diurnal, seasonal, and annual fluctuations (Blanchet et al. 2014). In addition, planktonic protists in Baltic waters demonstrate a maximum species richness in the horohalinicum zone, which goes against the Remane model (Telesh et al. 2011; Filker et al. 2019); instead, this pattern corresponds the “edge effect,” a general ecotone concept (Azovsky et al. 1998).
According to Attrill and Rundle (2002), an estuary, as a transition zone linking freshwater and marine systems, could potentially be considered as either an ecotone or as an ecocline. An ecotone is an area of relatively abrupt spatial change in species occurrence and abundance, producing a narrow transition zone between two different and relatively homogeneous freshwater and marine communities. In contrast, an ecocline represents a more gradual, progressive change (both spatial and ecological) comprising a series of distinct assemblages along the estuarine salinity gradient. Most importantly, an ecocline is a response to the gradual change in some major environmental factor, while other factors (acting at a different scale) influence the further subdivision of the biota within the gradient. In general, the intensity of a boundary or transition zone tends to increase with the spatial overlap of multiple environmental gradients (Azovsky et al. 1998). Some further studies confirm that shifts in the composition and structure of estuarine assemblages correspond more closely to an ecocline than to an ecotone model (Chaves et al. 2018), while in other cases, a combination of both types was observed, i.e., an ecocline containing one or a series of ecotones (Modéran et al. 2010; Udalov et al. 2021). Although the ecoclinal characteristics seemed to be a general feature of estuarine biocenoses, the ecotone could be more system-specific and biological compartment-specific. In particular, the patterns in estuarine macrobenthic communities were related mainly to two independent drivers: salinity and sediment type (Teske and Wooldridge 2003; Udalov et al. 2004; 2021; Chertoprud et al., 2013).
Community patterns in a changing environment have traditionally been analyzed in terms of taxonomic differences using species abundances, composition and diversity. However, focusing solely on taxonomy could neglect important information on ecosystem function, and consequently, a complementary approach, biological trait analysis (BTA), has received extensive attention in recent decades (Bremner 2008). This approach quantifies the value and range of organismal traits, i.e., attributes of life history, trophic relations, morphology and behavior, that influence their performance and thus ecosystem functioning. Therefore, a trait-based approach may highlight patterns within and across ecosystems that are not apparent in taxonomic-based approaches (Bremner 2008; van der Linden et al. 2017).
Few studies have applied BTA to analyze the functional structure of estuarine benthic communities. Barnes and Hendy (2015) revealed changes in the functional diversity and composition of macrofauna in a South African estuary. In two Brazilian estuaries, polychaetas displayed higher levels of taxonomic and functional diversity that increased seaward, while mollusk functioning remained similarly low along the estuarine gradient (van der Linden et al. 2017). Van der Wal et al. (2017) reported sediment grain size and current velocity to be the key factors determining the proportion of feeding modes and motility of macrofauna in the Westerschelde estuary, while salinity had a lesser effect. In contrast, in the Chernaya estuary (White Sea), the trophic structure of macrobenthos depends primarily on salinity and on the amount of organic matter, while the trophic structure of the meiobenthic assemblages is not related to salinity and depends on the sediment type (Udalov et al. 2004).
In several comparative studies, it has been found that different groups of organisms, e.g., micro, meio- and macrobenthos, are driven by different sets of environmental variables and therefore have demonstrated particular taxon-specific distribution patterns in the same habitat (Udalov et al. 2004, 2021; Azovsky et al. 2022). In most of the studies on estuarine systems, however, only metazoan groups were considered, while the distribution of benthic protists is poorly explored.
Webb (1956) and Parker (1981) described the distribution of interstitial protists in estuaries of Great Britain. A detailed study of benthic protists (diatoms, ciliates and heterotrophic flagellates) has been carried out in a small subarctic estuary (Chernaya River, the White Sea). Spatial patterns in species composition, diversity and trophic structure along the salinity gradient have been examined, as well as interannual and seasonal variations (Burkovsky, Mazei 2001; Mazei et al. 2001; Mazei, Burkovsky 2002, 2005, 2006; Saburova et al. 2001; Tikhonenkov et al. 2006; Tikhonenkov, Mazei 2006; Udalov et al. 2004). Recently, a series of studies have been carried out on different groups of planktonic protists in several estuarine ecosystems and surrounding coasts of the South China Sea (Jiang et al. 2021; Li et al. 2021; Zhu et al. 2021). Biodiversity, community composition, spatial distribution and seasonal dynamics were investigated using environmental RNA high-throughput sequencing, and the relative importance of environmental filtering and stochastic processes in assemblage structuring was assessed. Salinity, water depth, and temperature were the primary factors controlling the distribution of the protists.
There have been a few attempts to apply BTA and functional-based approaches to ciliate communities (Moreira et al. 2022; Vlaičević et al. 2022). In particular, Xu et al. (2018b, c) investigated the spatial and temporal variation in the functional structure and diversity of benthic ciliates in the Yangtze Estuary. Significant correlations were found between biological traits (in particular, feeding type and body size), functional divergence and environmental variables (salinity, sediment grain size, hydrodynamic conditions, temperature and nutrients), suggesting that the functional diversity of benthic ciliates had an advantage over classical diversity measures for environmental status assessments. Liu et al. (2021) compared the ciliate communities in intertidal, neritic and oceanic water areas in terms of taxonomy, motility and feeding habit composition. In the intertidal zone, the communities differed significantly among habitat types but not among sites. The BTA revealed the geographical pattern of ciliates on a large scale, but to distinguish the community variation on a local scale, taxonomy-based methods have higher resolution than ecological traits. They also found that environmental selection was the major process structuring the taxonomic composition in intertidal water, while spatial processes were important in neritic and oceanic waters. Environmental factors (habitat type, salinity, and Chl a concentration) were the most important in determining variations in the functional structure.
In general, the microeukaryotic community patterns in estuaries and the potential mechanisms underlying these patterns are still poorly recognized.
In the present study, we described and compared the diversity and taxonomic and functional structures of intertidal ciliate assemblages along two contrasting estuaries: a large tropical estuary and a relatively small subarctic estuary. More specifically, we aimed to test the following hypotheses, implied by general paradigms in estuarine ecology (Wall et al. 2001; Attrill and Rundle 2002; Bremner 2008; Elliot and Whitfield 2011):
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Estuarine ciliate assemblages in general have high abundance and biomass but low diversity;
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There is diversity minimum and highest variability in the oligohaline region (“critical salinity” zone);
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The estuarine ciliate assemblages, especially in the upper reaches (“critical salinity” zone), are dominated by r-strategists, i.e., short-lived, small-bodied, bacterio- and detritivores, compared to the outermost coastal areas;
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The spatial pattern in the larger estuary is closer to the ecocline, and that in the shorter estuary is closer to the ecotone;
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Functional (trait-based) community attributes demonstrate more consistent patterns than taxonomy-based attributes.