Background

Floristic diversity of macrophytes in the Black Sea is estimated as more than 330 species, but this number is less than a quarter of the Mediterranean algae (Milchakova, 2003; 2011). Also, the production and biomass of the Black Sea macrophytobenthos are much higher than in the Mediterranean and other southern Eurasian seas. For the coastal zone of the Black Sea basin, including its northern part along the Crimean coast, there is typically a belt of Cystoseira sp. and Phyllophora crispa biocenoses, and their distribution is ranged from 0.5 to 20 m in depth (Kalugina-Gutnik, 1975; Milchakova, 2003; 2011). As the main primary producers, macroalgae play an important role in coastal ecosystems, although they are also vulnerable to ecological stresses. In consequence of pollution and excessive eutrophication the growth rate of macrophytes has slowed down, the lower boundary of the algae distribution moved towards the coastline, some species’ distribution areas decreased until they disappeared from large areas of the Black Sea (Milchakova et al., 2011). The best-known examples are the nearly complete degradation of Phyllophora beds in the northwestern part of the Black Sea, and a partial disappearance of the Cystoseira spp. along the Romanian shores in the late 1970s and in the Odessa Gulf in the early 1980s as well as in some areas of the Crimean coastal zone, including marine protected areas (Zaitsev, 2006; Milchakova, 2011; Milchakova et al., 2011).

Although the main limiting factor in the distribution of algae at depth is light, the availability of a solid substrate of natural or artificial origin as well as benthic shell deposits and live bivalves is essential to their dissemination (Kalugina-Gutnik, 1975; Milchakova, 2011).

The shell-bearing gastropod Rapana venosa (Valenciennes, 1846) invaded the Black Sea in the early 1940s (Drapkin, 1953; Chuhchin, 1984; Bondarev, 2014). This invasive species occupied a free niche as a top predator in the benthic food chain and by now it has become an integral part and an important element of the coastal ecosystem (Bondarev, 2015). The ecology of R. venosa also is a matter of primary concern as this is an important object of fishery in some Black Sea countries.

Given the destructive impact of invasive species R. venosa on the biocenoses of bivalve mollusks in the Black Sea (Chuhchin, 1984; Bondarev, 2014; 2015) the study of its ecological and development features is an important task for monitoring of benthic biocenoses. However, the ecological impact of R. venosa is not limited to predation only, since the mollusk shells serve as a substrate for various epibionts (Savini et al., 2004; Emelyanov et al., 2010; Bondarev, 2016; Bondarev and Revkov, 2017a; 2017b) most prominently for macroalgae. They, in turn, are a habitat for epiphyton (Makkaveeva, 1979; Bondarev and Revkov, 2017a; 2017b) and can be used as a refuge for juvenile fish species (Bondarev, 2016; Bondarev and Revkov, 2017a). On a soft substrate, the presence of algae and their epiphyton is closely associated with R. venosa, but the composition of this consort community and its participation in the benthic ecosystem are poorly understood. The high density of R. venosa, which in some areas of the northern part of the Black Sea reaches up to 120 ind./m² (Bondarev, 2015) and the ability to migrate over fairly long distances (Bondarev, 2014), specifies the need to explore its consortiums.

Due to R. venosa tolerance to a wide range of environmental conditions as well as ecological and morphological plasticity its area of distribution in the Black Sea is significant and covers a range of depths from the shoreline to 50 m (Bondarev, 2010; 2014). Distribution of R. venosa by depth is limited by the cold intermediate layer with constant temperature near 8ºC. As the type of substrate does not limit the distribution of R. venosa it can be found anywhere where its preferred food Bivalves are present (Bondarev, 2014).

Local populations of R. venosa are formed on areas with stable food resources. It has been found that R. venosa demonstrate selective predation (Savini and Occhipinti-Ambrogi, 2006), which generates conservative feeding behavior (Bondarev, 2015). Most of the annual living cycle of R. venosa passes within a certain biotope with specific prey species inhabit in (Bondarev, 2014; 2015). Rapa - whelks, which live on sand bottom, migrates in summer in search of a solid substrate for laying eggs, and after spawning they return back for feeding and wintering. During the wintering period, the whole or part of the Rapa - whelk is buried in the ground. R. venosa inhabiting on rocky grounds in the Black Sea also migrates to the sandy bottom areas for burrowing into the ground during winter cooling and returns back in the spring to rocks for feeding and summer breeding (Bondarev, 2010; 2014).

Thus, there are two principal R. venosa ecomorphs distinguished by their habitat on sandy and rocky substrate differ by their epibiontic organisms (Savini et al., 2004; Emelyanov et al., 2010; Bondarev and Revkov, 2017a; 2017b). Previous studies of the R. venosa fouling in the northern part of the Black Sea have identified 14 species of macroalgae (Emelyanov et al., 2010).

The aims of the present work are the study of diversity and listing of alga taxa which detected on the shells of sandy and rocky R. venosa ecomorphs, and representation of their assemblages in different areas of the northern Black Sea coastal zone (Figure 1).

The research was funded Russian Academy of Sciences and carried out in the A.O. Kovalevskiy Institute of Marine Biological Research (Sevastopol) within the framework of the state scientific task on the topics "Monitoring the biological diversity of the hydrobionts of the Black Sea-Azov basin and developing effective measures to preserve it" (No. 1001-2014-0014) and "Regularities of formation and anthropogenic transformation of biodiversity and bioresources of the Azov-Black Sea basin and other regions of the World Ocean" (No. AAAA-A18-118020890074-2).

1 Material and Methods

R. venosa specimens were collected at 7 areas of the northern part of the Black Sea (Figure 1) during the period from 2008 to 2017 (Table 1).

Table 1 The regions of investigation with the date of sampling, the samples number, the depth (m) and ground type

In total, 974 specimens of R. venosa were sampled. Sampling in the coastal zone (less than 15 m depth) was carried out by SCUBA and snorkel diving, while for deeper zone (up to 40 m) the "Ocean-50" grab corer was used. Simultaneous visual observation and photographic images were carried out in situ on each dive. Each specimen of R. venosa was placed in a separate plastic bag with a label.

The linear dimensions of the study specimens were measured with a caliper with an accuracy of 0.1 mm, and weighing was carried out on an electronic scale with an accuracy of 0.1 g. The R. venosa shell height (H) measurement is from the apex to the end of the siphonal channel, and the shell width is the maximum diameter of the last whorl (D). Age of R. venosa was determined by spawning marks (Chuhchin, 1984; Bondarev, 2010).

Algal coating was evaluated as a percentage (%) of the total outer surface area of shells. Average values (M) and standard deviation (σ) were calculated with the tools of the Excel program.

The occurrence of epibionts on R. venosa shell was evaluated according to the following scale: 0 – taxa is not detected, 1 – rare, 2 – seldom, 3 – common, 4 – very common (Table 2).

2 Results

In total 65 species of macroalgae, namely 20 Chlorophyta species, 16 Ochrophyta (Phaeophyceae) species and 29 Rhodophyta species were found on the shells of live specimens of R. venosa (Table 2).

Among 20 Chlorophyta species the richness is higher for two green algae genera, namely Cladophora (4 species) and Ulva (6 species), which dominate in the R. venosa consortium at 0.5 – 15 m depth. The highest incidence was found for Ulva rigida with the average thallus length is 0.5 – 5 cm and the maximum length exceeds 25 cm. The fouling of Ulva intestinalis is commonly observed with the thalli length up to 23 cm (Figure 2). The high frequency of occurrence is also typical of green algae Chaetomorpha aerea and Cladophoropsis membranaceae. Cladophora albida, Cladophora laetevirens and Cladophora liniformis are often found on sandy Rapa whelk (Table 1). As a rule, the linear dimensions of filamentous algae and flat bushy thalli (from 3–10 cm) are lower than those for the species with plate thalli.

Figure 2 Macroalgae at the sandy ecomorph shell of Rapana venosa (5 m depth, region 3): Ulva intestinalis (maximum thallus length is 23 cm), Ulva rigida (thallus length is 16 cm), Cladophoropsis membranaceae and Cladophora laetevirens

The comparison of  alga list for two R. venosa ecomorphs’ shows that the diversity and abundance of green algae is distinctly higher on the sandy ecomorph vs. the rocky one (Table 2). Parameters of Chlorophyta abundance are the highest at a depth of up to 5 m; they are significantly reduced between 10 and 15 m and from 15 to 20 m they are decreased sharply.

Ochrophyta (Phaeophyceae) species found on R. venosa shells have a relatively low frequency of occurrence. The most common brown alga are: Cladostephus spongiosum (Figure 3), Ralfsia verrucosa and Zanardinia typus; other fouling species on R. venosa shells are rare (Table 2). It is worth noting that Cystoseira spp., which form biocenoses with nearly continuous cover on the rocks at the coastal zone, were found on R. venosa shells only as seedlings or single small bushes up to 15 cm in height.

Figure 3 R. venosa on sandy bottom in situ (4.5 m depth, region 3) fouled by alga species: Peyssonnelia dubyi, Corallina sp., Cladostephus spongiosum (dominant) with epiphytes Ulva rigida, Vertebrata subulifera, Acrochaetium sp.

The highest species richness (29) among R. venosa fouling is characteristic of Rhodophyta. Among them the highest frequency of occurrence was observed for cortical algae Peyssonnelia dubyi (Figure 4) which was found very common both on sandy and rocky ecomorphs of R. venosa (Table 2).

A high occurrence of Phymatolithon lenormandii was also revealed on the rocky ecomorphs and less on the sandy ecomorphs. Other species of red algae are rare in the fouling of shells as they are characteristic of sandy ecomorphs mainly. At depths exceeding 20 m only the thalli of red algae Phyllophora crispa and Coccotylus truncatus were sporadically found (Table 2).

The largest variety and quantity of macroalgae were found at 4–8 m depth (Table 2). The shells of R. venosa specimens vary widely in macroalgae species’ diversity and the intensity of their fouling, even within local populations and ecomorphs. Thus on the surface of the individual shells one can detect from 1–8 species of macroalgae. The composition of macroalgae and the frequency of their occurrence on the rocky and sandy ecomorphs are different. Generally, 65 species of fouling macroalgae were found on sandy ecomorphs and 21 species on rocky ecomorphs in the northern part of the Black Sea.

The complex of algae fouling of each R. venosa shell usually consist of 2 – 4 species (Table 3) with predominance of 1–2 species and a small proportion of secondary ones, sometimes up to 7 species. The relatively stable combinations of fouling macroalgae which were identified on R. venosa can be treated as the aggregation complexes. The most common complexes for sandy and rocky ecomorphs of R. venosa are shown in Table 3.

The combinations of 10 alga species occur on about 90% of the samples analyzed (Table 3). The principal combinations can be supplemented with other algae that also can form their own combinations or mono-species fouling. The greatest species diversity and the occurrence in aggregation complexes on sandy R. venosa ecomorph are typical for green algae with filamentous and plate thalli. The encrusting algae Peyssonnelia dubyi and Phymatolithon lenormandii dominate mostly in the complexes the rocky R. venosa, and sometimes on the sandy ecomorph also (Table 2; Table 3).

The area of R. venosa shells covered with macroalgae fouling ranges from 0 to 100% and varies greatly even within the same biotope and region (Table 4).

In regions 1 and 5, where the Rapa whelk lives on sandy bottom, no algae fouling was found on the shells. On the Rapa whelks, living on various types of loose grounds in regions 2, 6 and 7, the level of algal fouling development is also low. Meanwhile the greatest diversity of macroalgae (63 of 65 totally registered species), the maximum area of coverage (up to 100%) and the highest fouling ratios were found also on sandy R. venosa (region 3). The highest indices of development of algae for rock Rapa whelk are also observed in region 3 (Table 4).

The abundance of encrusting sessile species with rigid calcareous skeleton was also discovered in Sevastopol area. The most common are polychaetes (fam. Serpulidae), Bryozoa and barnacle (Crustacea) Amphibalanus improvisus (Darwin). These sessile living forms obviously compete with macroalgae for the surface of R. venosa shells. But after the death of those animal epibionts their skeletons create rough surfaces on the R. venosa shell which facilitate settling of macroalgae spores. The R. venosa shell surfaces perforated by drilling Porifera fam. Clionaidae, namely Pione vastifica (Hancock), are also favorable for the growth and development of algae, especially Cladophora spp. and Cladophoropsis membranaceae. The R. venosa shells completely overgrown with algae (Figure 5A) have been densely perforated by P. vastifica (Figure 5B).

The R. venosa shells with 100% covering of fouling algae as well as the domination of one species which can completely cover the entire shell surface (Figure 4; Figure 5A) are rare. R. venosa shells which were primarily found with the ventral surface are completely or partly free from algae due to the contact with the substrate. As a rule, fouling algae accumulates on the most convex part of the dorsal side of the shell (Figure 2; Figure 3), which has the greatest exposure to sunlight and is not covered or blocked with a thin layer of sandy substrate when the gastropod buries its shell in search of food or during the winter rest time.

After spawning in the nutritionally active period, the edge of the last whorl of young (from 2+ to 4 years old) R. venosa is quickly accrued and remains free of fouling (Figure 6) for up to 6 months, even during the period of intensive algae growth. It was revealed that R. venosa less than 2 years of age are usually deprived of fouling because of high growth rate. The shell growth rate is distinctly decreased in individuals older than 5 years. In the Black Sea populations of R. venosa individuals under the age of 5 years dominate (up to 96.8%) and the growing edge area might be up to 30% of the total surface of the shell. Thus, the post spawning growth complicates the correct assessment of the shell fouling surface valuation.

3 Discussion

The number of fouling algae (65 species) that exceeds by 4.5 times the amount of taxa (14 species) in previous studies (Emelyanov et al., 2010) has been detected as a result of targeted works in region 3 which was chosen on the basis of reconnaissance investigations.

In the earlier study of fouling of R. venosa shells in the Black Sea, it was remarked that the differences between ecomorphs of R. venosa are not dependent on the type of substrate (Emelyanov et al., 2010). According to our data, the species diversity and the density of fouling on both sandy and rocky ecomorphs of R. venosa shells can vary greatly by area and depth (Table 2; Table 4), which partly correspond to previously published data (Emelyanov et al., 2010).

As follows from Table 4, there are two opposite tendencies in the distribution of algae fouling. The absence of algal fouling (regions 1, 5) or their minimal amount (regions 2, 7) was found on sandy R. venosa. At the same time, the maximum development indices and the number of species (63) of algae are also found on sand Rapa whelks (region 3). Obviously, the development of fouling is influenced by a complex of environmental factors.

The fact that R. venosa shells collected on the sandy substrate at Mamaia Beach (region 1) do not have fouling algae could be explained by the water and sand movement acting as an abrasive which cleanse the shell surface in the near-bottom layer at the shallow water area (0 – 1.5 m). It is notable that fouling algae is also low (0 – 10%, M – 4%, σ – 2.5) on sandy ecomorphs of R. venosa that inhabit near the Kerch Strait (region 7) at 8–15 m depth (Table 3). These data are close to those given in (Emelyanov et al., 2010) which reported only two species of algae recorded on the Rapa whelk from the Kerch Strait, namely Ulva sp. and Cladostephus spongiosum, that were observed in the fouling with their frequency of occurrence not exceeding 2%. It may be assumed that in the Kerch Strait, as well as in the area of the Adriatic Sea where the frequency of algae on the sandy ecomorphs does not exceed 2% or is close to zero (Savini et al., 2004), R. venosa has to dig deeper into the sand for hunting than in the Sevastopol area. Such deep burial prevents the development of algae on the surface of the R. venosa shell. It is also likely that the sand moved by the flowing water works as an abrasive and prevents algal fouling in the Kerch Strait and the Adriatic Sea more active than in Sevastopol region.

A feature of R. venosa fouling from comparatively deep-sea habitats is a smaller number or a total absence of algae, particularly green, due to the reduction of light. So, at a depth of over 20 m, only the red algae Phyllophora crispa and Coccotylus truncatus which can grow up to 60 m depth in the Black Sea (Kalugina-Gutnik, 1975; Milchakova, 2011) were sporadically found.

Anyway the expansion of attached algae and their epiphyton on sand and other kinds of loose substrates are strongly associated with the presence of R. venosa shells. It is known that the highest number of macroalgae species and their maximum development were recognized on the subtidal zone where the level of insolation is high enough, and the wave energy no longer exerts inhibitory effects on the development of thalli (Kalugina-Gutnik, 1975). As a consequence the maximum species diversity of algae (63) and their density of cover (up to 100%) were found precisely in region 3 at the depths of 4-10 m on sandy R. venosa shells which is the only solid substrate favorable for algae development here.

R. venosa of rocky substrates can also differ in the density of fouling by algae and their diversity is dependent upon the particular sea bottom profile. The specimens from steep coastal cliffs have virtually no algal species with bushy, branched and elongated plate-shaped thalli, as active hydrodynamic processes hinder their development. Cortical red algae, particularly Peyssonnelia dubyi and Phymatolithon lenormandii that dominate on this type of bottom, are distributed mainly in rocky R. venosa ecomorph populations.

The inclined and subhorizontal surfaces of rocks are covered with a "carpet" of macroalgae, mainly with bushy thalli. Meanwhile the diversity of algae on the rocky biotope is significantly different from the fouling of local R. venosa. The rocky rapa whelks inhabiting the Cystoseira biocenoses are dominantly covered by encrusting species of macroalgae, particularly Peyssonnelia dubyi, Phymatolithon lenormandii, Zanardinia typus, and other algae are represented by small thalli or sprouts. This is probably due to the fact that Cystoseira branches moved by the water mass act mechanically on the surface of the R. venosa shell and remove fragile sprouts of bushy alga forms. Furthermore, the high density of the Cystoseira bushes prevents the penetration of light to the bottom where R. venosa inhabits, which hinders the growth of photophilous alga species. That is why small bushes of Cystoseira spp. were found rarely and only on sandy R. venosa shells in the areas where the density of Cystoseira is high in the coastal zone.

Direct comparison of our data with R. venosa algal fouling from the Mediterranean Sea is not possible because there is no available list of taxa for this region. For the coastal waters of the Adriatic Sea only some notes such as "red encrusting algae and green algal turf" were listed for 546 specimens including 302 sandy and 244 rocky ecomorphs (Savini et al., 2004). The frequency of green algae on the rocky ecomorphs of R. venosa is 69% and cortical red algae is 16%, whereas the frequency of these macroalgae on the sandy ecomorphs does not exceed 2% or is close to zero in Adriatic Sea (Savini et al., 2004). These indicators are comparable with the data for some of the areas in the Black Sea that we studied. However, it should be noted that the fouling of R. venosa by brown algae in the Adriatic Sea has not been specified at all (Savini et al., 2004). But in the Black Sea Cladostephus spongiosum, Cystoseira sp. and Zanardinia typus have been indicated for 5 and 11 of the 12 areas, respectively (Emelyanov et al., 2010). By our data perennial species Cladostephus spongiosum, Ralfsia verrucosa and Zanardinia typus are dominant among Ochrophyta (Phaeophyceae) in R. venosa fouling (Table 1; Table 2). It is very likely that with the expansion of research in the Mediterranean, brown algal fouling will be found.

The present list of macroalgae in the fouling on R. venosa that includes 65 species is not complete since its shell is a favorable substrate. At the same time, R. venosa has the ability to move, avoiding negative factors of external influence while contributing to the preservation of epiphytes. Distribution of R. venosa on sandy and other soft substrates helps to expand the habitat of the fouling algae. Thus, R. venosa, being a dangerous enemy for filter feeders bivalves (Chuhchin, 1984; Bondarev, 2010; Bondarev, 2014; Bondarev, 2015) unwittingly contributes to the conservation of some species diversity and the expansion of areas and habitat range of algae in the Black Sea. But additional studies are needed to estimate of R. venosa ecological effects.

4 Conclusions

The R. venosa shell is a favorable substrate for the development of attached algae. The list of alga fouling of Rapa whelk currently includes 65 species: Chlorophyta – 20, Ochrophyta (Phaeophyceae) – 16 and Rhodophyta – 29 species. Meanwhile this list of will be extended in future with the number of samples increasing and the expansion of investigating areas.

The greatest number of algae species (65) was found on sandy R. venosa shells, and on the rocky ecomorph – 21 species. The diversity of fouling algae species and their indices of development on the both ecomorph depend on the environmental factors inherent in a particular region and range of depths.

On sand and other loose grounds R. venosa shells are almost the only substrate favorable for algae development that expands the range of their spreading. However, there are two opposite trends in the development of algae on sandy rapa whelk: the extreme high and low indices are inherent in this ecomorph.

The invasive species R. venosa supposedly plays a positive role in preservation and dissemination of algae when the deterioration of the ecological situation in some areas of the Black Sea poses a threat to the existence of certain species. However, adequate experimental studies are needed to determine its ecological effects.

Authors’ contributions

IPB conceived the study, conducted the bulk of sampling, made field identification of alga and invertebrates, and made all tables, photos and illustrative figures. NAM verified alga species identification in laboratory. Both the authors wrote the manuscript, contributed to data interpretation and approved the final manuscript version.

Acknowledgments

We thank all those who have in different stages of the study helped in sampling and handling the samples, Mrs. Kathleen Parsons, UK and Mrs. Irina Stepanova, St. Petersburg (Department of Interfaculty Disciplines, Sector of Foreign Languages, North-West Institute of Management, branch of the Russian Presidential Academy of National Economy and Public Administration) for revising the English and two anonymous reviewers, whose suggestions and comments improved the manuscript.

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