INTRODUCTION

Out of the 46 valid species of Cystoseira sensu lato dominant on the shelf of the Mediterranean Sea and adjacent areas of the Atlantic Ocean [29, 36], only five were found in the Black Sea and only two species were widespread: Cystoseira bosphorica (previously identified here as C. crinita) and Treptacantha barbata (=C. barbata) [15, 16, 29, 40]. Both species grow in a wide range of depths (from 0.2–0.3 to 10–15 m) and play a significant role in the formation of benthic plant communities, accounting for the larger fraction of their biomass [5, 10, 12, 33, 34]. However, in recent decades, as a result of the impact of many factors (a decrease in the water transparency, eutrophication, introduction of alien species, destruction of biotopes, increase in recreational load, climate change, etc.), the penetration depth, area, and total biomass of the Cystoseira tangle are decreasing; in addition, the phytodiversity of large areas of the Black Sea shelf is decreasing [3–5, 8–10, 12–14, 17, 33, 34, 43].

Degradation (decrease in productivity and species richness) of Cystoseira communities can be the result of both a synchronous (independent) response of populations of dominants and associated species to unfavorable changes in habitat and a decrease in the participation of C. bosphorica and T. barbata in their formation. At the same time, the role of the second factor in this process remains unclear, for at least three reasons. First, Cystoseira can have both negative (competition) and positive (as shelter, substrate) effects on other species. Second, they can dominate at different depths, and the nature of the influence of dominants on the species richness of phytocenoses may differ under different environmental conditions. It is known that the more severe these conditions, the weaker the competitive effect of dominants on the accompanying species, but the stronger the protective functions of such species are manifested [1, 2, 18, 19]. There is evidence that this pattern is typical of both terrestrial and aquatic (benthic marine) communities [19, 25, 30, 45]. Third, studies on Black Sea phytobenthos, with a few exceptions [20, 34], hardly investigated at all interspecific relations, including the influence of dominants on the state of other macroalgae species populations.

The aim of our study was to quantitatively assess the joint influence of species of the genus Cystoseira sensu lato on accompanying macroalgae species, species richness, composition, and biomass of communities in general, by comparing areas of cenoses (samples) with relatively high and low biomasses of these species.

MATERIALS AND METHODS

Methods for Collecting Factual Material

The study is based on 155 samples of the macrophytobenthos taken from June 29 to August 8, 2018, on the shelf of the Black Sea near Cape Bolshoi Utrish (Krasnodar krai; Abrau Peninsula) (Fig. 1). One hundred and ten samples were taken in Cystoseira communities (0.3–10 m), 29 at shallower depths (0 and 0.15 m, dominant Ceramium ciliatum), and 16 at a depth of 15–20 m (dominants Codium vermilara and Phyllophora crispa). In Cystoseira communities, samples were taken at depths of 0.3–0.5 (25 samples), 1–2 (38), 5 (26), and 10 m (21).

Fig. 1.
figure 1

Study area and sampling map.

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Samples were taken from an area of ​​0.25 m2 in homogeneous habitats. The majority of the samples at each depth were taken in a regular way on two transects of ten sites. Samples taken on transects at the same depth were at a distance from 1 to 8–10 m from each other, depending on the bottom topography. Additionally, several more samples were taken to increase the contrast of the sampling between transects. In this case, the plots were established in the areas of communities with the highest and lowest projective cover of C. bosphorica and T. barbata, which was assessed visually. All macrophytic algae from each frame were collected in a separate gauze bag using a set of scrapers. Then each sample was sorted according to species, dried with filter paper, and each species was weighed [35]. Cortical algae and microepiphytes were not considered.

Analysis Methods

Analysis of the factual material included the following steps:

(1) For each sample (site), the values ​​of the following indicators were calculated: (1) total wet algal biomass per 1 m2 (W); (2) biomass of each species (Wi); (3) joint biomass of C. bosphorica and T. barbata (WС); (3) total biomass of accompanying species (WS = W – WС); (4) number of accompanying macroalgae species per 0.25 m2 (SS, local species richness).

(2) Samples with dominant Cystoseira from each depth were ranked according to increasing total biomass of these species (WС), then divided into two equal or approximately equal (with a difference of one sample) groups: with biomass values ​​above the median (high biomass, HBC) and with biomass values below the median (low biomass, LBC). For each selected group, the following was determined: total number of accompanying species (NS), average values ​​of the above characteristics (Table 1), average values ​​of the biomass of each species (taking into account samples in which the species was not present) (WА), as well as their occurrence (proportion of samples in a group with the presence of a species to the total number of samples, F). The average values ​​of the biomass of the species are shown in Table 2; their occurrence values are shown in Table 3.

Table 1.   Biomass and species richness of communities of the Abrau Peninsula of Black Sea with high and low biomass of C. bosphorica and T. barbata
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Table 2.   Average biomass of algal species (WА, g/m2) in different communities of Abrau Peninsula of Black Sea
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Table 3.   Occurrence of algal species (F) in different communities of Abrau Peninsula of Black Sea
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(3) In order to assess the nature of changes in the occurrence and biomass of accompanying species with decreased participation of Cystoseira (synchronous or compensatory), we compared the values of characteristics WА and F for each species in groups of samples with low and high Cystoseira density. The statistical significance of the differences between the WА values was estimated using one-way analysis of variance (ANOVA); between F values, using Student’s t-test.

(4) If a decrease in participation of Cystoseira affects the distribution and occurrence of accompanying macroalgae species, then this may affect the degree of homogeneity of the species composition of algocenoses at different depths. As an indicator of the species similarity of the studied areas of the communities, we used the Sorensen coefficient (Ks = 2С/(А + В), where A and B are the number of species in the groups of samples from two compared areas (depths); С is the total number of species in the compared areas). Species similarity between all sites was estimated, and individual estimates were obtained for variants with low and high Cystoseira participation. The significance of their difference (mean ​​ similarity values) was determined by ANOVA.

RESULTS AND DISCUSSION

In total, 48 macroalgae species were identified in the studied Cystoseira cenoses, including 27 species of red (Rhodophyta), 11 brown (Ochrophyta, Phaeophyceae), and 10 green (Chlorophyta).

The values ​​of indicators characterizing whole macrophytobenthos communities with high and low Cystoseira biomass are shown in Table 1. The following can be seen from Table 1:

(1) The total biomass of C. bosphorica and T. barbata was maximum at depths of 1–2 m. At shallower (0.3–0.5 m) and greater depths (5 and 10 m), it was lower. At all depths, the total biomass of samples with HBC on average was statistically significantly higher than that with LBC.

(2) In the upper phytal zone (from 0.3 to 2 m), a high abundance of accompanying species was observed in samples with a low participation of Cystoseira. Conversely, at depths of 5 and 10 m, a high biomass of accompanying species was found in samples with a high biomass of Cystoseira. The share of biomass of accompanying species in samples with LBC was higher than in cenoses with HBC, and at shallow depths, the difference was statistically significant; at great depths it was not (Table 1).

It also follows from the table that in areas with a low density of Cystoseira in the composition of accompanying species dominance of epiliths was observed (76–99% of the biomass of accompanying species at all depths, except 5 m). The increase in abundance of basiphytes (Cystoseira) was accompanied by an increased role of epiphytes.

(3) At the shallowest (0.3–0.5 m) and deepest (10 m) areas, the contribution of species of different ecological groups (epiphytes and epiliths) to the biomass of associated species of communities with HBC was approximately the same. Epiphytes prevail at depths of 1–2 and 5 m. A decrease in the biomass of Cystoseira by 2.2–3.9 times in groups with LBC led to a significant decrease in the participation of epiphytes (by 1.8–13.1 times) and an increase in the participation of obligate epiliths (by 1.3–10.1 times). As a result, in most areas with LBC, obligate epiliths were the dominant group among the associated species in terms of biomass.

(4) For most depths, the number of epiphyte species recorded in samples with LBC was lower, and epiliths were both higher and lower than in samples with a high participation of Cystoseira. As a result, at most depths, the total number of species recorded in samples with LBC was slightly lower than in samples with their high participation. In general, for all depths, 35 species were recorded in the first group, and 39 species were revealed in the second. At depths from 0.3 to 5 m, samples with low participation of Cystoseira were characterized by higher average values ​​of local richness (SS) than samples with a higher biomass of these species; however, these differences were not statistically significant. At a depth of 10 m, on the contrary, a decrease in the biomass of Cystoseira corresponded to a decrease in SS, and the difference was statistically significant.

Tables 2 and 3 present data on the average biomass (WА) and occurrence (F) of accompanying macroalgae species in communities with different participation of Cystoseira. Clearly, the species have different reactions to a decrease in the Cystoseira biomass and, according to these characteristics, can be combined into three groups: (1) species that increase the biomass and occurrence at most depths (compensatory or positive response); (2) species that reduce the values ​​of these characteristics (synchronous or negative response) and (3) species with an indeterminate response (having approximately the same or both higher and lower WА and F values ​​in the samples of the compared groups).

The first group consists of eight species (17% of the total number of accompanying species). These are obligate (Padina pavonica, Dictyota fasciola, Phyllophora crispa, Cladostephus spongiosum, and Cladophoropsis membranacea) and facultative (Ceramium ciliatum, Gelidium crinale, and Laurencia coronopus) epiliths, which have predominantly competitive relationships with Cystoseira. Most of them (six out of the eight species) have a very low abundance in communities with a high participation of Cystoseira or they almost never occur in them. In particular, Ceramium ciliatum and Phyllophora crispa penetrate into the sparse Cystoseira tangle from adjacent cenoses (from shallower and deeper areas), where they are dominant.

Another two species from this group, Cladostephus spongiosum and Cladophoropsis membranacea, have a less definite response to a decrease in participation of Cystoseira. As follows from our data, at depths from 1 to 10 m, they clearly preferred areas with a low density of Cystoseira, while at 0.3–0.5 m, this effect is not pronounced. It can be assumed that in shallow waters, under conditions of high wave activity, these species use the Cystoseira canopy as shelter, and at great depths, they compete with them for substrate. Interestingly, Cladophoropsis membranacea has demonstrated an increase in occurrence and biomass in recent decades compared to the 1950s–1970s. [34]. Therefore, it is possible that the increase in occurrence of this species is associated with a weakening of topical competition with Cystoseira.

Group 2 included 11 species (24% of the total number of associated species). These were mainly epiphytes (Sphacelaria cirrosa, Laurencia obtusa, Vertebrata subulifera etc.), which were expected to respond negatively to a decrease in the total biomass of Cystoseira and two species that are capable of epilithic growth (Chaetomorpha linum and Polysiphonia opaca). Most of the species of this group are considered characteristic and constant for Cystoseira communities [6, 7].

The third group consists of 15 species (33%) belonging to different ecological groups (obligate and optional epiliths, epiphytes). It can be suggested that these are macroalgae more or less indifferent to the effect of the considered factor, as well as species that were less abundant in our study (Ellisolandia elongata, Gelidium spinosum, Ceramium diaphanum, C. virgatum) the response of which to changes in Cystoseira biomass is difficult to determine. The group also included Codium vermilara, which rarely grows in Cystoseira communities, regardless of the degree of their dominance at the sites.

Lastly, we found some species in single samples (listed in the caption to Table 2). Seven of them were found only in samples with a high Cystoseira biomass, and five, in samples with a low biomass. This was a heterogeneous group, consisting of rare species, as well as species confined to other habitats and uncharacteristic of Cystoseira communities.

In general, as follows from Tables 2 and 3, among the ten obligate epiliths found in all areas, half were characterized by a higher occurrence and biomass in areas with LBC. The rest of the epiliths showed no particular preference in this regard. Among the 20 epiphytes that we identified at all depths, only 9 clearly preferred the areas of communities with a high Cystoseira biomass. At the same time, among the 16 species capable of growing both as epiliths and as epiphytes, only one-third showed a positive or negative response to a change in Cystoseira abundance.

It also follows from Tables 2 and 3 that at depths of 0.3–0.5 m, six species (a quarter of the total number of species identified at this depth) have a well-pronounced response (positive or negative) to a change in participation of Cystoseira; at depths of 1–2 m, 12 species (one-third of species identified at this depth); at depth of 5 m, 14 species (41%); and at depth of 10 m, 11 species (42%). Thus, the proportion of such species increased with depth. However, at depths of 0.3–5 m, the number of species responding positively to a decrease in Cystoseira biomass was somewhat higher than the number of species with the opposite response. At a depth of 10 m, the response of species to this effect was predominantly negative (in nine versus two species). This may mean that the role of Cystoseira as a species forming cenosis increases with depth.

The average values ​​of the Sorensen species similarity coefficient between the sites of cenoses with HBC were 0.68 ± 0.02, n = 6; with LBC, 0.70 ± 0.04, n = 6. As can be seen, the difference between them is small and not statistically significant (ANOVA, F4.96= 0.31, р = 0.05). This suggests that a two- to fourfold change in the participation of Cystoseira did not significantly affect the degree of species homogeneity (differentiation) of macrophytobenthos along the depth gradient.

The phenomenon when a decrease in the abundance or loss of some species from communities is accompanied by an increase in the number of others is known as the density compensation effect (DCE) [24, 28, 31]. It can be accompanied by a niche (spectrum of occupied habitats) expansion of the remaining species and, in this case, it is part of a broader concept: the ecological release effect [24, 28]. It was assumed that the DCE can contribute to stabilization of the functional parameters of ecosystems with a decrease in their species richness and is one of the indicators of the role of interspecies competition in the structuring of communities [21, 28, 48]. It was shown that the exchange surface in the basiphyte–epiphyte system remains at a relatively constant level in the eutrophication and water mobility gradient: a decrease in productivity of Black Sea Cystoseira is compensated by an increase in the role of production (and biomass) of epiphytes [11].

Thus, if we interpret our results using this concept, we can conclude that both the niche expansion effect (penetration of new species into communities at their upper and lower boundaries) and DCE (the decrease in Cystoseira biomass by 50–75% was accompanied by an increase in biomass of obligate epiliths) were revealed in the studied communities. However, the degree of their manifestation can be considered low, since in absolute values the compensatory growth of the epilithic biomass was significantly lower on the whole than the decrease in total Cystoseira biomass: at depths of 0.3–0.5 m, by 16 times; 1–2 m, by 14 times; 5 m, by 87 times; and 10 m, by 168 times. Moreover, as can be seen from these data, the intensity of compensatory processes decreased with depth. It is also known that the lower phytal zone underwent the most intense degradation during the period of global restructuring of the Black Sea ecosystem [14, 17, 33, 34].

In the Mediterranean Sea, species with similar importance, in addition to T. barbata (C. bosphorica is most likely absent in the Mediterranean Sea [22]), are other species of the genus Cystoseira and related genera of brown algae (Cystoseira sensu lato): C. compressa, C. amentacea var. stricta, C. usneoides, Carpodesmia tamariscifolia, C. crinita, C. zosteroides, Treptacantha sauvageauana, T. ballesterosii). All these species have thalli with a developed three-dimensional structure, which ensures the formation of additional habitats and ecological niches for plants and animals settling here [37, 38, 42, 44]. All these species of Cystoseira sensu lato are dominants of associations of the same name at depths from 0.5 to 10–15 m and deeper [26, 27, 39]. In recent decades, in the Mediterranean Sea, due to warming and anthropogenic impact, Cystoseira have become rarer and their disappearance has been accompanied by a significant decrease in species diversity of the cenoses [23, 32, 41, 46, 47]. The main accompanying species able to inhabit the vacant niches and form new communities are Padina pavonica, Dictyota dichotoma, Ellisolandia elongata, and Halopteris scoparia [23], e.g., species (or their vicar analogs) that in our study also demonstrated an exclusively positive (Padina pavonica, Dictyota fasciola) or positive at some depths (Ellisolandia elongata) response to a decrease in the proportion of Cystoseira in the cenosis (Halopteris scoparia in the Black Sea is now encountered very rarely).

Such observations in weakly perturbed and slightly polluted regions of the Black Sea are rare; among them is the discovery of a significant reduction of T. barbata tangle on the Mary Magdalene Bank by the beginning of the 21st century and distribution of Cladostephus spongiosum [34], which also agrees with our data.

Thus, our results show that a two- to fourfold decrease in the participation of Cystoseira in the macrophytobenthic communities of the Russian Black Sea shelf unassociated with a significant change in the quality of the environment generally has no significant effect on the species richness of communities and the degree of homogeneity (differentiation) of vegetative cover along the depth gradient. However, this leads to a decrease in the total biomass of these cenoses and multidirectional change in the participation (biomass, occurrence) of many accompanying macroalgae species. In this case, negative consequences were observed for about 50% of the epiphytic species of these communities; positive consequences were revealed for the species of adjacent cenoses at shallower and greater depths, as well as for about half the epilithic species. At the same time, the response of cenoses to decreased biomass of C. bosphorica and T. barbata, as well as its negative character (decrease in productivity and species richness), was more pronounced at greater depths.