Distribution of Polychaetes of the Family Dorvilleidae (Annelida) on the Shelf of Crimea

全文:

Introduction

The polychaetes of the family Dorvilleidae are widespread in the world ocean. In the 1970s, eight genera of this family were known [1]. Further studies of ecosystems, including deep-sea ones, in the zones of hydrothermal, methane and other seeps, led to the discovery of many new representatives of Dorvilleidae adapted to existence in these marginal biotopes. Notably, these polychaetes have been observed to dominate the macrozoobenthos community in cold methane seeps, hydrothermal vents, whale bone accumulations and sediments within the oxygen minimum zone [2]. Dorvilleids exhibit a remarkable tolerance to sulfides and these polychaeteshave been identified in sulfide sediments found in both shallow waters and polluted estuaries [2–4]. Dorvilleidaeare regarded as opportunistic species capable of colonising diverse habitats characterised by the presence of organic matter and heavy metals [2]. Observations have revealed that certain Dorvilleidae species form substantial aggregations in areas of intensive fish aquaculture, with their abundance also increasing in proximity to mussel farms. Consequently, these species can be utilised as indicators of the aquaculture impact on the surrounding biota ¹[5].

To date, researchers have documented more than 200 species belonging to 31 genera of Dorvilleidae. Of these, three genera are known to occur in the Black Sea ² [6–8], namely Protodorvillea kefersteini (McIntosh, 1869), Dorvillea rubrovittata (Grube, 1855), Schistomeringos rudolphii (Delle Chiaje, 1828) and Schistomeringos neglecta (Fauvel, 1923). The latter species is listed for the Bosporus outlet area of the Black Sea and the coasts of Bulgaria and apparently belongs to the complex of species inhabiting the zone of action of the waters of the Sea of Marmara ³ [9]. The first three species are listed for many areas of the Black Sea ⁴ [9–13], however, there is little data on their distribution and occurrence in different biotopes. No representatives of Dorvilleidae have been recorded in the Sea of Azov [8, 14, 15].

Given the increased interest in this polychaete family, a more detailed analysis of the ecological characteristics, distribution and quantitative representation of Dorvilleidae in the Black Sea becomes relevant, which is the aim of this paper.

Materials and methods

The macrozoobenthos samples from R/V Professor Vodyanitsky expeditions (cruises Nos. 64, 68, 70, 72, 75, 84, 86, 90, 96, 108) in 2010–2019 served as the present study material. The work was performed on the shelf of the northern part of the Black Sea from the coast of Romania to the Caucasian coast (Tuapse area) as well as in the Sea of Azov off the coast of Crimea. The stations were carried out in the depth range from 10 to 137 m. The salinity levels in the Black Sea ranged from 16.89 to 18.47‰ and in the Azov Sea, they fluctuated between 12.53 and 15.22‰ during the sampling. Collected from 291 stations, the materials obtained from the bottom grab samples were utilised. Bottom sediments were collected employing an Okean-50 bottom grab, with a capture area of 0.25 m². The collected sediments were then subjected to sieve washing, with the smallest mesh size employed being 1 mm.

Materials from benthic surveys carried out in the coastal areas of Crimea by the Benthos Ecology Department of IBSS from 1997 to 2023 were also utilised in the analysis. A series of studies were conducted in a number of locations throughout the region, including Karkinit Bay, Lake Donuzlav, the bays of Sevastopol, the Kara Dag water area and Feodosia Bay. In addition, a number of underwater caves of both natural and artificial origin in southeastern and southwestern Crimea were also investigated [16]. In 2005, year-round macrozoobenthos surveys were conducted at two stations (6–7.5 m depth) in the western part of Kruglaya Bay. Samples from loose substrates were taken with a diving bottom grab (S = 0.04 m²), typically in two repetitions. Material was collected from hard surfaces using a frame (S = 0.04 m²) with a silk bolting cloth bag sewn to it. A total of 440 stations, with a depth range of 0–25 m, were carried out. The collected material was then subjected to sieve washing, with the sieves having a mesh diameter of 0.5 mm. Following this, all specimens were fixed in 4% neutralised formalin. Taxonomic identification of polychaetes was facilitated by the utilisation of literature data ⁵ [7].

Results and discussion

During the course of the study focused on cruise materials (on loose substrates at a depth of more than 10 m), dorvilleids were identified at 52 out of 291 stations in the Black Sea. Conversely, no dorvilleids were recorded in the Sea of Azov (21 stations). P. kefersteini was recorded at 30 stations, S. rudolphii – at 19 and D. rubrovittata – at three stations (Fig. 1). Thus, dorvilleids are relatively rare species on soft bottoms in the open sea, with only P. kefersteini demonstrating 10% occurrence, while S. rudolphii and D. rubrovittata have 6.5 and 1% occurrence, respectively. The maximum density of dorvilleids reached 704 ind.·m⁻².

In the Crimean coastal area (1–22 m depth), dorvilleids were found in almost all areas on soft bottoms and in fouling (Fig. 1). Their density exhibited significant fluctuations within broad limits, consistently being higher in comparison to areas in the open sea. Representatives of this family were also found in underwater caves and channels.

 

Fig. 1. Distribution of Dorvilleidae in the northern part of the Black Sea

 

Dorvillea rubrovittata

D. rubrovittata is an Atlantic-Mediterranean species [1, 7, 17]; in the Black Sea, it is indicated for the Bosporus outlet area of the Black Sea, the coasts of Turkey and Bulgaria [7, 9] and also found ⁶off the coasts of the Caucasus and Crimea [7, 18, 19]. This species is considered to be relatively rare, with documented occurrences in minimal numbers on the shell and in the fouling of rocks and stones at a depth of 0–50 m ⁵ [7, 9]. It has not been recorded off the coast of Romania [10] and is generally found in the northwestern Black Sea (NWBS) ⁴ [20, 21].

In our samples, D. rubrovittata (Fig. 2, a) was found in open sea areas only near the western shores of Crimea and in Karkinit Bay at a depth of 14–30 m on shell substrates. Its density was 4–16 ind.·m⁻² (Fig. 1).

In the coastal shallow water area, the species was recorded in rock and stone fouling in the areas of Kara Dag, Tarkhankut and Donuzlav. In the bays of Sevastopol, it was found in the fouling of oyster farm cages [22]. In these biotopes, its abundance did not exceed 13 ind.·m⁻². Higher density values of D. rubrovittata were recorded on the walls of underwater caves in the areas of Balaklava and KaraDag (up to 125 ind.·m⁻² at a depth of 2 m). In the underground Balaklava canal in the fouling of concrete walls at a depth of 2 m, the maximum values of this indicator were recorded – up to 438 ind.·m⁻². Conditions in the canal differ from other biotopes due to poor hydrodynamics and low light levels.

 

Fig. 2. Dorvillea rubrovittata (a); Protodorvillea kefersteini (b)

 

It is evident that D. rubrovittata is prevalent along the Black Sea coast of Crimea. The species has been recorded predominantly in the fouling biotope of hard substrates, with relatively large aggregations observed in areas of reduced hydrodynamics.

Schistomeringos rudolphii

S. rudolphii is widespread in the Atlantic Ocean (European and American coasts), the Mediterranean Sea and is also indicated for parts of the Pacific and Indian Oceans [1, 7, 9, 17]. There are isolated records of this species in the Black Sea. The species has been recorded in the Bosporus outlet area of the Black Sea ², the coasts of Turkey and Bulgaria [8–10, 13]. There are also two indications of S. rudolphii for the Caucasus coasts [11, 15]. In Crimea, the species was found only in Sevastopol Bay on sandy-shell substrates among Zostera roots ^{6, 7}. The next occurrence of S. rudolphi was also recorded near Sevastopol at the end of the 20th century [23]. The first records of this species in the northwestern Black Sea date back to the end of the 20th and beginning of the 21st century, when it was found ⁴ in the shallow waters of Yagorlyk, Tendra and Karkinit Bays [12].

In our materials, S. rudolphii was recorded in open sea areas on soft bottoms along the entire Crimean coast (Fig. 1). The species was found at depths of 10–45 m, with one occurrence at a depth of 88 m. The maximum density values were recorded in the Karkinit Bay (240 ind.·m⁻²) and the Kerch pre-strait area (210 ind.·m⁻²) at depths of 20 and 34 m, respectively.

In coastal samples, S. rudolphii was found at a depth of 2–22 m at some stations on the eastern and southern coasts of Crimea (Feodosia Bay, Kara Dag area, Laspi Bay), in many bays of southwestern Crimea and also in Lake Donuzlav. The density of these polychaetes was relatively low, but sometimes it reached 300 ind.·m⁻² (Laspi Bay, 13 m depth) [24]. The species was discovered to inhabit a variety of substrates, yet it was most frequently observed in association with shell substrates and among macrophytes (Fig. 3).

It has been observed that S. rudolphii is present in Donuzlav and Kruglaya Bay, where it has been recorded inhabiting areas of algae fam. Characeae and sea grasses Potamogeton and Zostera, growing on silty substrates at a depth of 2–7 m. The species has also been found in small numbers (8–50 ind.·m⁻²) in the fouling of the walls of caves and underground Balaklava canal.

Protodorvillea kefersteini

P. kefersteini is an Atlantic-Mediterranean species indicated for the North American and European coasts, widely distributed in the seas of the Mediterranean basin [1, 9, 17]. The distribution of P. kefersteini has been documented in nearly all areas of the Black Sea [7–10, 13]. However, it did not occur in the NWBS until

 

Fig. 3. Occurrence of Schistomeringos rudolphii on different sediments

 

almost the beginning of the 21^st century [20]. The first detection of this species refers to the pseudomeiobenthos of Yagorlyk Bay [12]. In subsequent years, P. kefersteini was identified in the shallow waters of Tendra and Karkinit Bays. No records of the species have been found in other NWBS areas ⁴ [25]. It is likely that the species inhabits the shores of the Caucasus, its occurrence is known off the coast of the Taman Peninsula [26]. P. kefersteini has been documented as a species that is abundant in certain Crimean coastal areas, as well as in the coastal waters of Bulgaria [6, 7].

In open sea areas, we encountered P. kefersteini (Fig. 2, b) in almost the entire northern part of the Black Sea, with the exception of the Caucasian coasts (Fig. 1). The species was recorded at depths of 12–45 m, with a single occurrence off the Southern Coast of Crimea at a depth of 94 m. P. kefersteini was predominantly found on sandy-shell substrates, with occasional instances of silty substrates. Its density was found to vary from 4 to 464 ind.^.m⁻².

The species was recorded in the majority of the coastal shallow water areas of Crimea that were the subject of the study, with the areas in question being located along the eastern and southern coasts (Kerch pre-strait area, Feodosia Bay, Kara Dag water area, Laspi Bay), off southwestern Crimea as well as in Karkinit Bay and Lake Donuzlav. P. kefersteini was recorded at a depth of 1–17 m on sandy-shell substrates with different degrees of siltation. Its density varied within large limits and in some areas reached such significant values as 1200 ind.^.m⁻² (Laspi Bay, 13 m depth, sandy-shell substrate) and 4975 ind.·m⁻² (Kara Dag water area, Experimental mussel farm area, 7 m depth, silty sand).

P. kefersteini was recorded in all bays and gulfs under study off the coast of southwestern Crimea, and during the summer surveys its occurrence and average density varied considerably in different areas (Table).

In the abovementioned areas, the occurrence of P. kefersteini did not generally exceed 50% and in Kazachya Bay, it was 50% with relatively low average density 62 ind.·m⁻². An exception was observed in Kruglaya Bay, where the occurrence was 88% and the average density was 2514 ind.·m⁻². Herewith, the maximum density of the species (13,215 ind.·m⁻²) was recorded in summer 2004 (4 m depth, coarse sand). Work carried out in the bay in 1990 also recorded relatively high levels of P. kefersteini, with its occurrence of 40% and average density of 280 ind.·m⁻² [27]. According to our data obtained in 2013 in Kruglaya Bay, the maximum density of the species in May was 11,288 ind.·m⁻², and in November, it reached 13,375 ind.·m⁻² (5–6 m depth at sampling stations, coarse sand), with the average density being 2893 ind.·m⁻².

 

Quantitative parameters of P. kefersteini distribution at coastal areas of southwestern Crimea

Study area	Occurrence, %	Mean density, ind.·м−2
Balaklava Bay	18	10
Sevastopol Bay	6	4
Kruglaya Bay	88	2514
Streletskaya Bay	9	233
Kazachya Bay	50	62
Cape Fiolent	33	217
Coast near the village of Lyubimovka	10	76
Donuzlav Lake	24	9

 

Thus, in Kruglaya Bay, the population of P. kefersteini has been recorded for many years and it has always been characterised by high density. It is hypothesised that the high abundance of this species during summer surveys is due to recruitment of juveniles. It is further assumed that the Black Sea is the breeding ground for P. kefersteini during the summer season as mature individuals were found in June [7]. Seasonal surveys carried out in 2005 in Kruglaya Bay showed that the species is present in the benthos throughout the year in significant numbers, reaching a maximum in July (Fig. 4).

It is evident that high density values of this species are also present in other Black Sea areas. In the Taman Peninsula, the average density of P. kefersteini was recorded as 320 ind.·m⁻² [26], near Kara Dag – 445 ind.·m⁻², with its maximum of 2000 ind.·m⁻² [7]. Along the Bulgarian coast, P. kefersteini is categorised as a mass species, exhibiting an average density of 556 ind.·m⁻² in specific biocenoses, with its maximum of 6200 ind.·m⁻² [6].

 

Fig. 4. Seasonal dynamics of P. kefersteini density in Kruglaya Bay(2005)

 

Consequently, the population of P. kefersteini in Kruglaya Bay exhibited remarkably elevated quantitative indices over an extended period when compared to all other areas under study. This prompts the question of the underlying causes of this phenomenon. The following hypothesis is proposed.

P. kefersteini belongs to small species of the family Dorvilleidae, which are characterised by feeding on microalgae and bacterial film, which is possible due to the peculiarities of their mouth apparatus structure [4]. It can be assumed that the forage supply of this species is extremely high in Kruglaya Bay.

Kruglaya Bay is located within the Sevastopol municipal boundaries and experiences a high recreational load. During the summer and autumn period, elevated concentrations of organic nitrogen and phosphorus, in addition to nitrates, have been recorded in the sea water. This observation is corroborated by long-term data [28]. Studies have shown that the ammonium nitrogen content in bottom sediments of Kruglaya Bay is about 10 times higher than in the sediments of the open sea [27]. It can be hypothesised that the elevated level of organic pollution in Kruglaya Bay contributes to the augmentation of the polychaete forage base and is a contributing factor to the mass development of P. kefersteini in this water area.

It should also be noted that the bays of Sevastopol are characterised by the presence of jet gas emissions (cold gas seeps) caused by methane flow from the deep sediment layers into the surface substrate horizons. Seeps in this area were registered at shallow depths (from 11–12 m) [29]. The presence of methanotrophic microorganisms forming bacterial mats has been demonstrated in the area surrounding jet gas outlets [30]. Evidence has been found which suggests the presence of jet gas emissions in the Kruglaya Bay area [31]. In other regions of the world ocean, research conducted on methane seeps ecosystems has revealed the prevalence of dorvilleids within these environments. These organisms are particularly abundant in the bacterial mats that proliferate around the seeps, with their abundance reaching up to 92% of the total macrofauna [3, 32]. There is evidence to suggest that certain members of the family Dorvilleidae consume chemosynthetic bacteria as part of their diet [4]. It has been hypothesised that the dorvilleids assemblages observed in proximity to methane seeps can be attributable to the forage specialisation of these polychaetes on specific prokaryotes [2, 3]. Assuming the presence of bacterial mats in Kruglaya Bay, formed around jet gas emissions, and their role as a forage source for P. kefersteini, it can be deduced that the development of a stable population of the species within this water area is a consequence.

Conclusion

Three species of the family Dorvilleidae were recorded in the northern Black Sea during the study: Dorvillea rubrovittata (Grube, 1855), Schistomeringos rudolphii (Delle Chiaje, 1828), Protodorvillea kefersteini (McIntosh, 1869). All of the above species are considered to be fairly widespread; however, their bathymetric range is limited to the photic zone (up to 50 m). This can be related to their feeding habits, which are specialised on microand macrophytes. The data obtained suggest that the distribution of dorvilleids in the Azov-Black Sea basin is also influenced by water salinity. It can be hypothesised that the salinity of 17–18‰, which is typical of the Black Sea, is a limiting factor for dorvilleids. To date, no species of dorvilleids has been found in the Sea of Azov, despite the recent increase in its salinity (up to 15‰) and pontization of the fauna. This can be indicative of the rarity of dorvilleids in the NWBS where coastal areas can be subject to desalination processes.

D. rubrovittata is a common species on the Black Sea coasts of Crimea. It occurs mainly in the biotope of hard substrates fouling and forms relatively large aggregations in areas with poor hydrodynamics and low light levels (underwater channels and caves), where its density reached 438 ind.·m⁻². The species was first found by us in the northwestern part of the Black Sea.

S. rudolphii was previously considered rare in the Black Sea, with only isolated occurrences documented. In the present study, the species was recorded in low numbers (2–300 ind.·m⁻²) on soft bottoms along the entire Crimean coast. The species was most frequently found on shell substrates and among macrophytes. In Lake Donuzlav, S. rudolphii was observed to be widespread in areas of algae fam. Characeae and sea grasses Potamogeton and Zostera.

P. kefersteini was recorded in almost the entire northern part of the Black Sea (excluding the Caucasian coasts) on sandy-shell substrates with varying degrees of siltation. It is a mass species and its density reached significant values in some areas. In Kruglaya Bay (Sevastopol area), a stable population of this species with the highest occurrence (up to 88 %) and density (up to 13,215 ind.·m⁻²) was recorded for a long time. The features of Kruglaya Bay are as follows: firstly, there is an increased level of organic pollution, and secondly, there is the presence of jet gas emissions around which bacterial mats can form. It is hypothesised that this leads to the formation of large assemblages of bacteria and microalgae which are a forage base for P. kefersteini.

 

¹ Ross, J., McCarty, A., Davey, A., Pender, A. and MacLeod, C., 2016. Understanding the Ecology of Dorvilleid Polychaetes in Macquarie. Fisheries Research and Development Corporation, 2016. Available at: https://www.imas.utas.edu.au/__data/assets/pdf_file/0010/905752/2014-038-DLD-Dorvs.pdf [Accessed: 2 December 2024].

² Bobretsky, N., 1870. [Materials for the Black Sea Fauna. Annelidae (Annelida, Polychaeta)]. In: KOE, 1870. Zapiski Kievskogo Obshchestva Estestvoispytateley. Vol. 1, iss. 2, pp. 188–274 (in Russian).

³ Rullier, F., 1963. Les Annélides Polychètes du Bosphore, de la Mer de Marmara et de la Mer Noire, en Relation avec Celles de la Méditerranée. Rapports et Procès-Verbaux des Réunions Commission Internationale pour l’Exploration Scientifique de la Mer Méditerranée. Monaco. Vol. 17, pp. 161–260.

⁴ Bondarenko, A.S., 2012. [Ecology of Polichetes of the Northeastern Black Sea]. Extended Abstract of PhD Thesis. Sevastopol, 23 p. (in Russian).

⁵ Vinogradov, K.A. and Losovskaya, G.V., 1968. The Type of Segmeted Worms – Annelida. In: F. D. Mordukhay-Boltovskoy, ed., 1968. Field Guide for the Black Sea and Sea of Azov Fauna. Kiev: Naukova Dumka. Vol. 1: Free-Living Invertebrates, pp. 251–405 (in Russian).

⁶ Yakubova, L.I., 1930. [List of Archiannelidae and Polychaeta of Sevastopol Bay of the Black Sea]. Izvestiya AN SSSR. Series 7. Physical and Mathematical Division, (9), pp. 863–881 (in Russian).

⁷ Pereyaslavtseva, S.M., 1891. [Additions to the Black Sea Fauna]. In: Kharkov University, 1891. Trudy Obshchestva Ispytateley Prirody at the Kharkov University. Vol. 25, pp. 235–274 (in Russian).

作者简介

Natalya Boltachоva

A.O. Kovalevsky Institute of Biology of the Southern Seas of RAS

编辑信件的主要联系方式.
Email: nboltacheva@mail.ru
ORCID iD: 0000-0003-0618-1992
SPIN 代码: 6287-9073
Scopus 作者 ID: 36149089700

Leading Research Associate, PhD (Biol.)

俄罗斯联邦, Sevastopol

Elena Lisitskaya

A.O. Kovalevsky Institute of Biology of the Southern Seas of RAS

Email: e.lisitskaya@gmail.com
ORCID iD: 0000-0002-8219-4616
SPIN 代码: 4973-5446
Scopus 作者 ID: 6504112143
Researcher ID: T-1970-2017

Senior Research Associate, PhD (Biol.)

俄罗斯联邦, Sevastopol

参考

补充文件