Species of Ulva (Ulvophyceae, Chlorophyta) as indicators of salinity

Ecological Indicators 85 (2018) 253–261

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Review article

Species of Ulva (Ulvophyceae, Chlorophyta) as indicators of salinity

MARK

Andrzej S. Rybak Department of Hydrobiology, Institute of Environmental Biology, Faculty of Biology, Adam Mickiewicz University, Umultowska Street No 89, PL61–614 Poznań, Poland

A R T I C L E I N F O

A B S T R A C T

Keywords: Distribution Habitat Macroalgae Salinity indicator Ulva

Salinity is one of the main determinants of species diversity in macroalgae. This study analyzes the occurrence of 16 species of the genus Ulva (Ulvaceae, Chlorophyta) in the salinity gradient. Ulva populations originated mainly from shores and estuaries with a minor number occurring in ocean lagoons, coastal lakes, canals and rivers. Ulva species were found in waters where salinity ranged from < 0.5 to 49 PSU. Most species were most commonly found in euhaline waters. It was observed that Ulva species with tubular thalli were present in a very wide range of saline waters (from fresh to hyperhaline waters). Ulva species with leaf-shaped thalli, however, were encountered chiefly in euhaline waters while being least often present in hyperhaline waters. It has been shown that the morphotype of the thallus (leaf-shaped or tubular) is correlated with water salinity levels. Ulva species with leaf-shaped thalli are not found in fresh (< 0.5 PSU) and poorly saline (< 10 PSU) waters, whereas tubular species are recorded in freshwater, brackish, and marine ecosystems (from 0 to 39 PSU).

1. Introduction Salinity is one of the main environmental factors influencing species richness of marine organisms living in near-coastal ecosystems (for example in estuaries or fiords) and in near-surface habitats which remain under strong and permanent influence of salinity stress (Ojaveer et al., 2010). For instance, the number of phytobenthic species increases with the increasing salinity of marine waters (Hoffmann 1932; Munda 1978; Wallentinus 1979; Nielsen et al., 1995; Telesh et al., 2013). Changes in the diversity of phytobenthic species across the salinity gradient have been discussed in detail on the example of the Baltic Sea (Larsen and Sand-Jensen 2006; Schubert et al., 2011; ŚliwińskaWilczewska et al., 2016; Tedesco et al., 2016). These species fluctuations display a polynomial trend, with a minimal number of species in the horohalinicum zone where salinity remains in the range of 5 – 8 PSU (Schubert et al., 2011). Also, it has been observed that in the coastal waters of Sweden and Denmark (15 – 30 PSU) there were > 300 species of macroalgae whereas only 42 species were identified in the offshore freshened waters of the Gulf of Bothnia (1 – 4 PSU) (Middelboe et al., 1997; Larsen and Sand-Jensen 2006). It needs to be noted that the number of macroalgae species in the Baltic Sea does not increase linearly as salinity increases but follows an irregular pattern (Wallentinus 1991). The decrease in the number of phytobenthic species along with the decrease in water salinity is more evident among the Rhodophyta Wettstein (1901), and Ochrophyta Cavalier-Smith in Cavalier-Smith

and Chao (1996) phylum (Class: Phaeophyceae Kjellman (1891)), than among the Chlorophyta Reichenbach (1834) phylum (Nielsen et al., 1995). However, it was observed that in the freshened waters of the northern Baltic the percentage of green algae in the total quantity of macroalgae increased. This is due to the dominance of euhaline species and the presence of freshwater species deposited by rivers (Wallentinus 1991; Nielsen et al., 1995; Messyasz et al., 2015; Staniszewska et al., 2015). Salinity is one of the major abiotic factors which determines habitat niches of green algae from the Ulva genus (Ulvaceae) (Xiao et al., 2016). The current number of recognized Ulva taxa exceeds 120 (Guiry and Guiry 2017). There are several cosmopolitan and dominant species in the sea littoral, such as Ulva lactuca, U. rigida, U. compressa, U. intestinalis, or U. prolifera. Species of the genus Ulva are epilithic macroalgae, which can colonise anthropogenic substrates (ship hulls or concrete structures in ports).Within the genus, one distinguishes three basic morphological groups in view of the differences in the development of the thallus. Ulva species are grouped thus, depending on the thallus type, Ulva species are grouped as follows: (i) tubular, consisting of a single cell layer (cell layer visible in cross-section); (ii) leaf-like, where the thallus is composed of two cell layers, and (iii) tubular leaf-like, which can be composed of one or two layers of cells in different parts of the thallus. Until the 1990s, the taxonomy of these green algae had relied on thallus forms, which served as a basis for dividing the group into two distinct subgroups: (i) Enteromorpha Link 1820 and (ii) Ulva

Abbreviations: ANOVA, analysis of variance; ITS, internal transcribed sequences; NASA, National Aeronautics and Space Administration; PSU, practical salinity units; rbcL, ribulose-1,5bisphosphate carboxylase/oxygenase gene; rDNA, ribosomal deoxyribonucleic acid; ROS, reactive oxygen species; SSS, sea surface salinity; UPGMA, unweighted pair group method with arithmetic mean E-mail address: [email protected]. http://dx.doi.org/10.1016/j.ecolind.2017.10.061 Received 22 August 2017; Received in revised form 20 October 2017; Accepted 25 October 2017 1470-160X/ © 2017 Elsevier Ltd. All rights reserved.

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stipulated in Guiry and Guiry (2017). All species were divided into three morphological types. The first group consisted of 7 species with leaf-like thalli (e.g. U. australis, U. lactuca and U. rigida), the second comprised 8 species with tubular thalli, e.g. U. compressa, U. flexuosa or U. prolifera. The third group included 1 species (U. linza) with tubular leaf-like thallus (Table 1).

Linnaeus 1753 (Blomster et al., 2002; Hayden et al., 2003). The genus Enteromorpha encompassed only species with tubular thalli (e.g. Ulva compressa and U. flexuosa), while the Ulva comprised leaf-like thallus species (e.g. U. lactuca and U. rigida). Following the introduction of molecular markers in phylogenetic studies of these macroalgae, the above division was rejected. Both types were found to be very closely related evolutionary entities (Hayden et al., 2003). The cosmopolitan nature of the Ulva genus and the high resistance of its species to fluctuations of physical and chemical conditions in the tidal zone result in the formation of large blooms called “green tides” (Guidone and Thornber 2013; Perrot et al., 2014). The occurrence of mono- or poly-species blooms of Ulva in the marine littoral and estuaries is probably related to the progressive eutrophication of coastal waters (Smetacek and Zingone 2013). “Green tides” that persist for a long time in the coastal areas have a negative impact on aquatic organisms and on the local economy (Fletcher 1996). Ulva species are also found in freshwater systems with salinity below 0.5 PSU (Mareš et al., 2011; Schroeder et al., 2013; Rybak et al., 2014). It has been observed that in systems of that kind (rivers, ponds and lakes) U. flexuosa can form large-surface mats reminiscent of the “green tides” from marine ecosystems (Rybak 2016). Marine Ulva species with leaf-like thalli tend to prefer both euhaline (30–40 PSU) and polyhaline (18–30 PSU) tidal waters (tidal euhaline to polyhaline waters). The species, however, are less common in mesohaline waters (5–18 PSU), in contrast to tubular species (Koeman and Van Den Hoek 1981). In the literature on the ecology of the Ulva genus offers no precise data on the preference of particular species for a particular type of water, e.g. hyperhaline (> 40 PSU) or oligohaline (0.5–5 PSU). Therefore, this study set out from the premise that an analysis of habitats populated by the species of the Ulva genus would allow species or groups of species associated with particular salinity zones to be distinguished as a result. Thus, we investigated species diversity of Ulva along the salinity gradient. The purpose of the study was to: (i) identify the varied Ulva species occurring throughout the salinity gradient, (ii) indicate which Ulva species occur in a similar or different salinity, (iii) determine whether there is a link between Ulva morphotypes and the occurrence of a given species in a particular salinity zone.

2.3. Statistical analysis STATISTICA 13.0 (StatSoft, Tulsa, OK, USA) and MVSP 3.22 – Multi Variate Statistical Package (KCS, Pentraeth, United Kingdom) software was used for the statistical analysis of the collected data. For all Ulva species for which salinity zones were determined, cluster analysis was performed to recognize internal differentiation of Ulva niches. Cluster analysis of environmental feature (salinity) was performed using the UPGMA method with percent similarity distance. Classification of salinity zones was defined using Caspers’ method (Caspers, 1959). Differences in the average values of salinity in different sites and between morphological types of Ulva thalli were assessed using one-way ANOVA test. 3. Results 3.1. The differentiation of Ulva habitats

2. Materials and methods

Ulva populations included in the habitat salinity analysis originated from marine and inland ecosystems. More than 44% of these habitats were located in sea bays and 34.4% on seashore rock formations. Estuaries had a high proportion among Ulva habitats, accounting for > 7% of all analyzed habitats. Percentages of such ecosystems as lagoons, marine lakes, canals, and salt ponds ranged between 1% and 4%. Ulva species were least common in atolls, lakes, island shorelines, ponds, and rivers (< 1% of all analyzed sites) (Table A.1). Of the studied species, only Ulva prolifera was found in 7 different types of aquatic ecosystems. As many as seven species (U. compressa, U. curvata, U. flexuosa, U. intestinalis, U. lactuca, U. rigida and U. rotundata) have been reported in 5 different types of ecosystems. The least diverse habitats were populated by two species: U. linza and U. ralfsii, whose populations were present only in sea bays, on rocky shores and in estuaries (Table A.1).

2.1. Sources of data

3.2. Environmental niches of Ulva species

Information on the occurrence of 16 species of the Ulva genus in the world's waters was obtained from scientific publications published between 1978 and 2016. Sources of the data included research studies which provided information on: (i) the habitat and type of ecosystem in which an Ulva population was present, (ii) identification of thalli samples to the species level, and (iii) the actual salinity of the habitat, expressed in PSU − Practical Salinity Units (measured during field research). It has been adopted that information on habitat salinity for each Ulva population must originate from accurate field measurements; data based on salinity models derived from satellite imagery (NASA Aquarius) or the maps of annual mean sea surface salinity (SSS) was not taken into consideration. In the database, each species of Ulva was represented by 30 populations. Habitats of Ulva species were located in worldwide water ecosystems (Fig. 1), while the analyzed database comprised the total of 480 records (Table A.1).

Species of the Ulva genus included in the analysis were present across the entire spectrum of water salinity, from < 0.5 to 49 PSU. Most of the analyzed species (10) were determined in polyhaline waters (salinity 18 – 30 PSU) (Fig. 2). Only 5 species were found most frequently in euhaline waters (30 – 40 PSU). Only one species (U. torta) occurred most often in mesohaline waters (5 – 18 PSU). An analysis of the prevalence of Ulva species in polyhaline habitats shows that they are predominantly encountered in the upper salinity limit of this zone, i.e. where salinity levels reach 28–30 PSU. Collation of salinities of Ulva habitats made it possible to determine the species or pairs of species occurring in waters with corresponding or different salinity levels (Fig. 3). The first group comprised cosmopolitan species that occurred mainly in oligohaline to euhaline waters, such as U. compressa, U. intestinalis, U. linza and U. torta. Within this group, the following pairs of species were observed in waters of the same salinity: U. torta – U. linza, U. compressa – U. intestinalis. The opportunistic species U. flexuosa is the only one inhabiting freshwater ecosystems (< 0.5 PSU), although it was largely found in polyhaline waters and least frequently in euhaline waters (> 38 PSU). Another group of species (including U. laetevirens, U. curvata, U. kylinii, and U. clathrata) was found to populate habitats ranging from mesohaline to euhaline. Only U. prolifera was the only one to have been encountered in oligohaline waters, while U. fasciata, U. lactuca and U. rigida were observed in zones

2.2. Taxonomy and species identification Ulva species were identified to the species level using classical morphological methods (78.5% of all cases); the remaining 21.5% of the samples were determined by molecular methods (sequencing of ITS rDNA regions and rbcL gene). The employed nomenclature followed the current mandatory designations for species of the genus Ulva as 254

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Fig. 1. Distribution of sampling locations of Ulva species.

3.3. Correlation between salinity and Ulva morphology

Table 1 List of Ulva species included in the analysis.

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16

Full name of species

Thallus form

Ulva australis Areschoug 1854: 370 (syn.: Ulva pertusa Kjellman 1897: 4) Ulva clathrata (Roth) C. Agardh 1811: 23 (syn.: Ulva muscoides Clemente 1807: 320) Ulva compressa Linnaeus 1753: 116 Ulva curvata (Kützing) De Toni 1889: 116 Ulva fasciata Delile 1813: 297 Ulva flexuosa Wulfen 1803: xxii Ulva intestinalis Linnaeus 1753: 1163 Ulva kylinii (Bliding) H.S. Hayden, Blomster, Maggs, P.C. Silva, M.J. Stanhope & J.R. Waaland 2003: 289 Ulva lactuca Linnaeus 1753: 1163 (syn.: Ulva fenestrata Postels & Ruprecht 1840: 21) Ulva laetevirens Areschoug 1854: 370 Ulva linza Linnaeus 1753: 1163

leaf-like

Ulva prolifera O.F. Müller 1778: 7 Ulva ralfsii (Harvey) Le Jolis 1863: 54 Ulva rigida C. Agardh 1823: 410 (syn.: Ulva scandinavica Bliding 1969: 554, nom. inval.) Ulva rotundata Bliding 1968: 566 Ulva torta (Mertens) Trevisan 1841: 480

Statistically significant differences were observed between salinities of habitats of leaf-like and tubular species, with P < 0.005 (Fig. 4). Species with leaf-like thalli were absent in waters below 10 PSU, as opposed to tubular species (Fig. 4A and 4B). Also, the latter were found in freshwater and hyperhaline ecosystems (0 – 39 PSU). Meanwhile, Ulva species with leaf-like thalli were observed mainly in mesohaline waters and least often in hyperhaline waters. The tubular leaf-like species (U. linza) was excluded from the statistical comparison because the sample was deemed to be insufficiently representative, particularly when compared with the other two morphological groups. The habitat niche defined by the gradient of salinity for Ulva linza is disjunctive as the species was found in oligohaline and poly-euhaline waters. There is no data on the occurrence of this species in mesohaline waters (Fig. 4A and Table 2).

tubular-like tubular-like leaf-like leaf-like tubular-like tubular-like tubular-like leaf-like leaf-like tubular-leaf like tubular-like tubular-like leaf-like

4. Discussion 4.1. Impacts of salinity on Ulva species distribution and development

leaf-like tubular-like

Salinity is one of the primary factors restricting growth and development of macroalgae in the intertidal zones, estuaries and freshwater ecosystems (Hart et al., 2003; Jahnke and White 2003; Parida and Das 2005; James et al., 2009; Gittenberger et al., 2014). Changes in salinity and trophy have a bearing on the formation of “green tides” by species of the Ulva genus (Reed and Russell 1978; Martins et al., 1999; Yamochi 2013). Salinity, temperature, and nutrients fluctuation affects the growth of the thalli and the life cycle of Ulva (Malta et al., 1999; Sousa et al., 2007). This environmental factors causing changes in thallus morphology (formation of branches), as well as impacting spore release or the sprouting and growth of propagules (Mantri et al., 2010; ChávezSánchez et al., 2017). Changes in salinity may affect macroalgae in three ways: (1) osmotic stress with direct impact on cellular water potential; (2) salt stress caused by the inevitable uptake or loss of ions – which is simultaneously a part of the acclimation – with the resulting toxic effect of the Na+ on the cellular structure, and (3) change in the cellular ionic ratios due to the selective ion permeability of the membrane (Kirst 1990; Karsten et al., 1991). Ulva species react and adapt to

with similar salinity (from 10 to 39 PSU). The analysis did not show similarities in salinity between the habitats of U. australis and U. rotundata, as U. rotundata was recorded in hyperhaline waters with salinity > 48 PSU and U. australis in the upper value range for euhaline waters (40 PSU). As regards U. ralfsii, salinity zones in which it was present suggest its distinct habitat requirements in comparison with other species of Ulva. U. ralfsii was most commonly found in polyhaline waters, as well as in mesohaline and hyperhaline waters (42 PSU). U. curvata (14 – 34 PSU), U. rigida (15 – 37 PSU), U. laetevirens (15 – 38 PSU) and U. kylinii (16 – 39 PSU) have proved to occur in the narrowest salinity range. One the other hand, the broadest range of salinity was characteristic for U. flexuosa (0 – 38 PSU), U. rotundata (10 – 48 PSU), U. intestinalis and U. compressa (0.6 – 38 PSU) (Table 2).

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Fig. 2. Mean values and ranges of water salinity in Ulva habitats.

Fig. 3. Dendrogram of niche similarity obtained from cluster analysis (UPGMA) of salinity for sixteen species of Ulva.

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Table 2 Occurrence of Ulva species and salinity of water.

Occurrence of Ulva in the zones of salinity: red marked – species has not occurred, orange marked – species occurred, green marked – species was found here mostly.

(expressed by the fastest photosynthetic rate) were achieved at 30 PSU (FitzGerald 1978). Experimental studies have shown that the fastest biomass gain in U. clathrata occurs in cultures where salinity ranges from 20 to 40 PSU (Moll and Deikman 1995). The findings are similar to those of Conover’s (1964), who found that U. clathrata demonstrates optimal growth between 25 and 35 PSU. In another study, Kapraun (1970) observed that U. clathrata developed best in a salinity of 27 – 29 PSU, while optimal sporulation ensued at 15 – 30 SU. Another analyzed tubular species, U. prolifera, shows significant similarity to U. clathrata in terms of habitat salinity. As previously observed with respect to preferred habitats, U. prolifera tends to be encountered in waters at the poly- and low-euhaline boundary. Similarly to, U. clathrata, the species was most commonly found in waters of salinity of ± 30 PSU. However, U. prolifera was also found in low salinity (2 PSU) oligohaline waters. Kier and Todd (1967) found that the blooms of U. prolifera occurred in a lagoon under conditions of high (45 PSU) or low (12 PSU) salinity. Most commonly, the populations of U. prolifera have been reported in oligohaline and euhaline waters; mainly in estuaries (4 – 19 PSU) and coastal lakes (7 – 26 PSU) (Ogawa et al., 2013). Experimental studies have shown that the highest rate of photosynthesis in U. prolifera occurs in cultures with salinity of 26–32 PSU. On the other hand, the highest growth of thalli was recorded in saline medium at 14–32 PSU (Xiao et al., 2016). The above findings confirm the association of U. prolifera with polyhaline waters. The distribution of Ulva flexuosa population in the salinity gradient is very diverse. This is due to the complex make-up of U. flexuosa taxon, which comprises several subspecies (Blomster et al., 2002; Hayden et al., 2003; Rybak 2015). Essentially, Ulva flexuosa is characterized by a very wide range of occurrence, from ultra-oligohaline to hyperhaline zones. For instance, U. flexuosa subsp. pilifera is observed in freshwater bodies (rivers and lakes), U. flexuosa subsp. flexuosa in brackish waters, and U. flexuosa subsp. paradoxa in hyperhaline waters. Information on the impact of salinity on the development of river and lake populations of U. flexuosa subsp. pilifera is quite scanty (Mareš et al., 2011; Rybak et al., 2014). These populations develop very rapidly and create large blooms in < 0.5 PSU waters (Mareš et al., 2011; Messyasz and Rybak 2011; Rybak et al., 2012). As regards marine populations of U. flexuosa, the fastest biomass growth rate and zoospore production was observed in 25 – 35 PSU media (Imchen 2012). Also, populations of Ulva flexuosa subsp. flexuosa were found at low- and high-salinity brackish sites in rivers (0.9 – 3 PSU) (Ogawa et al., 2013). Ulva flexuosa subsp. paradoxa is recorded in highly saline marine ecosystems (> 35 PSU) as well as in anthropogenic systems (canals, reservoirs at artificial fertilizer sites, mineral water closures, canals and ponds in the vicinity of saline facilities), where salinity exceeds 50 PSU (Rybak et al., 2014). Ulva flexuosa subsp. paradoxa is the only taxon of Ulva type capable of

low-saline and hyper-saline conditions. A number of reports have indicated that when Ulva species are subjected to salinity stress, reactive oxygen species (ROS) accumulate rapidly and cause oxidative stress (Collen and Davison 2001; Luo and Liu 2011). 4.2. Optimum salinity conditions for tubular-like species of Ulva The most common marine Ulva species with tubular thalli are U. compressa and U. intestinalis. Experimental research on the growth rate of U. intestinalis by Martins et al. (1999) showed slight growth of thalli in media where salinity was below 3 PSU. In a < 1 PSU medium all the thalli were dying. The growth rate of U. intestinalis at < 5 PSU and > 25 PSU was very low as well. At the same time, the highest growth rate of the thalli of this species was observed at 15 and 20 PSU (Martins et al., 1999). Furthermore, it has been noted that changes in salinity affect the morphology of U. intestinalis thalli. Incubation in water with salinity > 35 PSU stimulated the formation of numerous branches on the thallus (“bottle brush” form) (Reed and Russell 1978). A review of U. intestinalis habitats indicates the most frequent occurrence of this species in oligo/mesohaline (5 PSU) and euhaline (30 – 40 PSU) waters. The second most common species in the seas, i.e. U. compressa, displays broad tolerance to daily and seasonal salinity fluctuations (Leskinen et al., 2004). Experimental studies have shown that U. compressa occurs in a salinity range from 0 to 34 PSU (Taylor et al., 2001). However, in the Baltic Sea for instance, the distribution of the U. compressa population is correlated with a more specific level of salinity than originally assumed (Nielsen et al., 1995; Tolstoy and Willén, 1997). Research by Leskinen et al. (2004) into the distribution of the U. compressa population off the coast of Scandinavia has shown that the species was absent in habitats where salinity was below 15 PSU. It would follow that salinity significantly limits the occurrence of U. compressa in the Baltic Sea. This conclusion was confirmed by experimental research (Koeman and Van Den Hoek 1981), which demonstrated that U. compressa thalli did not develop properly in very low salinity waters. Low salinity (not exceeding several PSU) is necessary for the proper development of the thalli. In fresh water (< 0.5 PSU), the development of U. compressa was halted. On the other hand, the fastest growth of thalli was recorded in a salinity medium of 6.8 PSU (Taylor et al., 2001). Our comparison shows the most frequent occurrence of U. compressa in poly- and euhaline waters, i.e. within a salinity range of 18 – 40 PSU. This species, just as U. intestinalis, was also found in the oligohaline waters. Comparison of the habitats of Ulva clathrata populations shows that this green alga was observed in mesohaline (3 populations), polyhaline (9) and euhaline (18) waters. Ulva clathrata was most commonly found in saline waters with 31 PSU. In culture, optimum growth conditions 257

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Fig. 4. Comparison of Ulva morphological types with respect to water salinity. A: Detailed dispersion of Ulva morphotypes in the salinity gradient. B: Results of one-way ANOVA test showing significance of differences between mean level of water salinity in which two morphotypes of Ulva occurred.

PSU medium U. linza produces the highest number of zoospores whereas poorest production was observed at 15 and 35 PSU (Imchen 2012). An experimental study by Ichihara et al. (2013) demonstrated that U. linza develops optimally in a salinity of 30 PSU. At 5 PSU, the thalli reached 95% vitality, which dropped to only 20% in fresh water (0 PSU) (Ichihara et al., 2013). The above bears out our own observations, namely that U. linza finds the best conditions for development in saline waters at ± 30 PSU. Another species which displays similar requirements in terms of salinity is U. torta. This species was found in much the same habitats as U. linza However, in the case of U. torta one observes a continuous population across the salinity gradient ranging from 0.9 to 35.7 PSU. Most populations of these macroalgae were found in mesohaline waters

developing in brine waters with extremely high salinity (Rybak 2015). The analysis of distribution patterns of Ulva species in the salinity gradient also included U. linza, the only tubular leaf-like species. To a substantial degree, its habitats overlap with those of U. flexuosa, as the species was found in waters from 0.9 to 35 PSU. However, a detailed analysis of U. linza habitats leads to the conclusion that the species clearly has two developmental optima in the entire water gradient. The first optimum occurs in low-oligohaline waters and the second in polyhaline waters (Fig. 4), though it should be noted that the majority of its populations were found to occur in the polyhaline zone, at 29 PSU. In contrast, only few U. linza populations were reported in oligohaline waters. Kjeldsen and Phinney (1972) recorded an optimum growth for U. linza at 30 – 35 PSU. It has also been shown that in a 30 258

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characterizes euhaline waters (30 – 40 PSU). Several U. fasciata populations were observed in polyhaline waters (18 – 30 PSU) and a minor number of those was determined in mesohaline waters (5 – 18 PSU); the species was not found in oligo- and hyperhaline waters. It was experimentally confirmed that in hyperhaline (45 PSU) and mesohaline (15 PSU) medium the growth of U. fasciata is inhibited (Chen and Zou 2015). Two closely related species, U. curvata and U. laetevirens, were found in habitats whose salinities were closely matched. The former was encountered within the salinity range of 14–34 PSU and the latter in waters between 15 and 38 PSU. This tallies with the results of cultural experiments which demonstrated very good growth of germlings and young blades of U. curvata in 17–34 PSU media (Koeman and Van Den Hoek, 1981). Probably the optimum for the development of the species is achieved at ± 30 PSU (at the boundary of poly/euhaline waters), where the populations of U. curvata are most often recorded. The second of the aforesaid, U. laetevirens, was observed most frequently in euhaline waters (35 PSU), with a few populations occurring in mesohaline waters. Unfortunately, literature offers no experimental data on the tolerance of U. laetevirens to fluctuations in salinity.

with a salinity of 14 PSU. On the other hand, Barinova et al. (2004) assert that U. torta is an indicator of strongly saline habitat (salinity pools of the Dead Sea, > 40 PSU). It is also reported that U. torta is most frequently encountered in estuaries, salt marshes and sandy mudflats, which makes it a very brackish species (Brodie et al., 2007). The ecology of U. kylinii and U. ralfsii is very poorly understood. There is also no experimental data indicating the optimal salinity at which both of these reach highest biomass growth, photosynthesis rate or zoospore production. Current knowledge of these species is limited to their taxonomy (to a large extent based on molecular methods) and requires being supplemented with environmental research. Information concerning the salinity of U. kylinii habitats suggests that the species is associated with polyhaline and euhaline waters. U. kylinii was most commonly found in 31.5 PSU waters, while the lowest salinity at which this species was recorded was 16.5 PSU. The salinity range in which tubular U. kylinii occurred (from 16.5 to 39.5 PSU) is very similar to that of leaf-like species such as U. curvata and U. laetevirens (Fig. 2). In turn, U. ralfsii stands out for its very characteristic range of salinity in which populations of this species were recorded. This green alga was found in waters from meso- to low-hyperhaline (8.3 – 42 PSU). It is the sole Ulva species with tubular thallus to occur in low-hyperhaline waters and one of two (along with U. rotundata) that was observed in this salinity zone. Nonetheless, populations of U. ralfsii were most frequently encountered in high-polyhaline waters (28 PSU).

4.4. The tolerance of Ulva to low-salinity and freshwater conditions Intertidal species of Ulva have to tolerate desiccation as well as drastic variation in salinity, thus requiring a high osmotic potential and water-holding capacity (Smith and Berry 1986; Kamer and Fong 2000; Holzinger et al., 2015). Numerous Ulva species represent very good model organisms for macroalgae and much effort has been made to investigate ecophysiological, tolerance-related responses in the course of colonization of the intertidal zone (Gao et al., 2011). Different Ulva species have been investigated concerning their ability to tolerate osmotic stress (Dickson et al., 1982; Young et al., 1987; Holzinger et al., 2015; Gao et al., 2016). A very interesting mechanism of Ulva tolerance to changes in salinity is described on the example of U. limnetica. It is the only Ulva species in the world occurring exclusively in freshwater (Ryukyu Island rivers, Japan) (Ichihara et al., 2009). Experimental studies on U. limnetica showed 100% thalli survivability after 7 days of incubation in a salinity from 0 to 30 PSU (Ichihara et al., 2013). This demonstrates that although Ulva limnetica is a species that has adapted to freshwater habitats it has not lost its ability to survive in marine waters of varying degrees of salinity (Ichihara et al., 2013). In addition, U. limnetica was found to over-express ULL (Ulva-lectin-like) genes, which probably constitutes a mechanism of adaptation or increased tolerance of this species to decreased water salinity (Ichihara et al., 2011). In the case of marine Ulva species with leaf-like thalli, such as U. australis, Ichihara et al. (2013) found no cell viability at salinity < 5 PSU. The thalli of these species died less than 3–4 days from the start of incubation. On the other hand, the unspecified species of Ulva sp. (leaflike thalli), which were sampled from the Pacific Ocean (at 33 m depth and salinity > 35 PSU), were characterized by extremely poor resistance to low salinity. At a salinity of 0 and 5 PSU the thalli of those green algae died within 24 h after being placed in the culture (Ichihara et al., 2013). These data indicate that eu- and hyperhaline species with leaf-like thalli, such as U. australis, U. lactuca and U. rigida, lack tolerance to the freshening of waters. Leaf-like species, although capable of developing when exposed to short-term fluctuations in salinity levels (e.g. in estuaries and tidal zones), do not persist in freshwater. On the other hand, Biebl (1956) found that tubular marine species—U. clathrata—can tolerate 0.5 – 2.0 times the concentration of normal sea water for up to seven days. This species was also able to tolerate distilled water for three days and recover if transferred back into normal sea water. Biebl (1956) attributed the ability to resist plasmolysis in U. clathrata to its osmoregulatory mechanism, which is capable of accumulating salts against a diffusion gradient (FitzGerald 1978). Among tubular Ulva species, only U. limnetica and U. flexuosa are

4.3. Optimum salinity conditions for leaf-like species of Ulva Ulva lactuca and Ulva rigida (Guiry and Guiry 2017) are the most common Ulva species with leaf-like thalli. The optimal level of salinity for the development of U. rigida is in the range of 35 – 40 PSU (De Casabianca and Posada 1998). This species was most often found in waters with a salinity of 34 − 35 PSU (Chávez-Sánchez et al., 2017). Likewise findings had also been obtained in experimental studies (Zavodnik 1975). The data on distribution of U. rigida analyzed in this study indicates that the species occurs in 30 – 35 PSU waters. As for “green tides” produced by U. rigida, they were most often recorded in salinity > 20 PSU (Fillit 1995). In turn, the cosmopolitan species U. lactuca under culture conditions was more tolerant to hypersalinity than hyposalinity (Murthy et al., 1988). The highest number of U. lactuca habitats was associated with euhaline waters (30 – 40 PSU). However, this species was most commonly found at a salinity level of 20 PSU. The above observations were confirmed in laboratory cultures where the highest U. lactuca biomass was obtained at 20 – 28.5 PSU (Bruhn et al., 2011; Nielsen et al., 2011). In many cases, the salinity ranges in which leaf-like Ulva species achieve developmental optimum coincide or are very similar. For U. rotundata, the optimal development is observed in waters between 26–36 PSU (De Casabianca 1989). Ulva australis, on the other hand, achieves the fastest growth rate at 15 – 40 PSU, but the buildup of its thalli decreases rapidly in oligohaline and hyperhaline waters (Choi et al., 2010). Most populations of U. rotundata and U. australis were recorded in waters where salinity reached 33 PSU and 29 PSU, respectively. The highest number of U. australis habitats was recorded in poly- and euhaline waters. Thalli of U. australis were not observed in oligo- and hyperhaline waters, which is consistent with the data provided by Choi et al. (2010). U. rotundata is shows greater preference for euhaline and hyperhaline waters (up to 48 PSU). The leaf-like Ulva fasciata displays high tolerance to short-lived saline changes during diurnal tides. Also germlings of U. fasciata demonstrated constant growth at 25–34 PSU salinity amplitude in culture (Chen and Zou 2015), whereby the fastest growth of the thalli was observed in a salinity of 30 PSU. In contrast, U. fasciata produced the largest quantity of zoospores in a salinity of 15 PSU (Mantri et al., 2010). In the wild, populations of U. fasciata are most commonly found in ecosystems with a salinity of 32 PSU. Thus, the optimal salinity for the development of this green algae is within the range which 259

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observed in freshwater lakes and rivers (Ichihara et al., 2009; Mareš et al., 2011; Rybak 2015). U. flexuosa is an opportunistic species occurring in waters with highly varied salinity levels, spanning (i) marine, (ii) oceanic (eulittoral islands), (iii) estuary and (iv) freshwater (riverine and lacustrine) ecosystems. U. limnetica is exclusively confined to freshwater ecosystems (< 0.5 PSU). 5. Conclusions This study identifies Ulva species with very specific habitat niches associated with the level of water salinity (e.g. U. ralfsii), as well as indicates which species and groups of species tend to be found in very similar waters (e.g. U. facsciata − U. lactuca) or occur at identical salinity levels (e.g. U. compressa − U. intestinalis). Furthermore, it has been observed that tubular species are characterized by a wider range of salinity tolerance than species with leaf-like thalli, given that leaflike species were not found in habitats below 10 PSU. Conversely, the vast majority of tubular species did not occur in waters where salinity exceeded 39 PSU, unlike certain species with leaf-like thalli (e.g. U. australis and U. rotundata). It may be conjectured that the evolutionarily earlier taxa with tubular thalli (both marine and freshwater ones), have not yet lost the mechanisms of tolerance and rapid adaptation to salinity changes in the process of natural selection. This adaptive capacity is well exemplified by the oldest evolutionary species with tubular thalli: (i) naturally occurring in freshwater, but maintaining vitality and development following an artificial transfer to saltwater (e.g. U. limnetica), (ii) occurring naturally in marine waters and, after an artificial transfer to freshwater, developing to a limited extent; subsequent retransfer to marine waters causes complete restoration of vitality and resumption of proper development (e.g. U. clathrata), and (iii) living in a very broad gradient of salinity, from freshwaters to hyperhaline habitats (e.g. U. flexuosa). Acknowledgments I am grateful to Professor Emeritus Lubomira Burchardt who, upon being acquainted with the concept of this research, suggested that a written report should be submitted to the Ecological Indicators. This research was partially supported by the project S/P – B/028: “Interrelation among abiotic and biotic factors in aquatic ecosystems: environmental and experimental research”. The author is very grateful to the reviewer’s valuable comments which helped to improve the manuscript. The author would also like to thank Szymon Nowak for proofreading. The author declares that there is no conflict of interest. Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j.ecolind.2017.10.061. References Śliwińska-Wilczewska, S., Pniewski, F., Latała, A., 2016. Allelopathic activity of the picocyanobacterium Synechococcus sp. under varied light, temperature, and salinity conditions. Int. Rev. Hydrobiol. 101 (1–2), 69–77. Barinova, S.S., Tsarenko, P.M., Nevo, E., 2004. Algae from experimental pools on the Dead Sea coast, Israel. Isr. J. Plant Sci. 52, 265–275. Biebl, R., 1956. Zellphysiologisch-ökologische untersuchungen an Enteromorpha clathrata (Roth) greville. Bet. Dt. Bot. Ges. 69, 75–86. Blomster, J., Bäck, S., Fewer, D.P., Kiirikki, M., Lehvo, A., Maggs, C.A., Stanhope, M.J., 2002. Novel morphology in Enteromorpha (Ulvophyceae) forming green tides. Am. J. Bot. 89, 1756–1763. Brodie, J., Maggs, C.A., John, D.M., 2007. Edition 1. Green Seaweeds of Britain and Irleand. British Phycological Society. Bruhn, A., Dahl, J., Nielsen, H.B., Nikolaisen, L., Rasmussen, M.B., Markager, S., Olesen, B., et al., 2011. Bioenergy potential of Ulva lactuca, biomass yield, methane production and combustion. Bioresour. Technol. 102 (3), 2595–2604. Caspers, 1959. Vorschläge einer brackwassernomenklatur (The venice system). Int. Rev. gesamten Hydrobiol. Hydrogr. 44 (1959), 313–315. Cavalier-Smith, T., Chao, E.E., 1996. 18S rRNA sequence of Heterosigma carterae

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