Submitted:

30 April 2024

Posted:

30 April 2024

You are already at the latest version

Abstract
Fish species diversity in the Black Sea is affected by the introduction of non-indigenous species, particularly through the process of "mediterranization" and the expansion of the ranges of invasive species. In August 2023, we documented an increasing quantity of four non- indigenous sparid species, namely Spicara smaris (Linnaeus, 1758), Diplodus puntazzo (Walbaum, 1792), Diplodus annularis (Linnaeus, 1758), and Lithognathus mormyrus (Linnaeus, 1758), in the coastal Bulgarian waters of the Black Sea, based on citizen science data obtained from small-scale fisheries and pelagic trawlers. However, in the autumn of 2022, only small quantities of S. smaris were collected periodically, indicating significant fluctuations in abundance and occasional presence. The other three species were recorded in August 2023 in the central coastal region near the Fandakliyska River, at depths of less than 10 m. This brief communication presents information on the identified species, including sampling locations and biological data, and examines the sparid species records in the Black Sea. In addition, we reviewed recent studies on the distribution and biological traits of the identified species in their natural Mediterranean habitats.
Keywords: 
mediterranization of Black Sea; non-indigenous Sparid fish; fish species biodiversity
Subject: 
Environmental and Earth Sciences  -   Environmental Science

1. Introduction

The Black Sea, a basin distinguished by low-salinity waters and anoxic conditions below 200 m, exhibits higher productivity than the Mediterranean Sea, yet supports a lower level of biodiversity. The fauna of the Black Sea comprises a complex and dynamic assemblage of indigenous and immigrant species, reflecting the region's geological, climatic, and anthropogenic influence. A limited variety of species facilitates the introduction of exotic invaders and renders biodiversity particularly vulnerable to bioinvasion [1,2,3,4].
The concept of "mediterranization" refers to the increasing presence and impact of Mediterranean species in the Black Sea ecosystem. This phenomenon is attributed to the introduction of non-indigenous species (NIS) by human activities such as ballast water from ships and intentional or unintentional release. Moreover, the natural dispersal of species through the Bosphorus Strait, which connects the Black Sea and Mediterranean Sea, as well as climate change, which affects environmental conditions and biogeographical boundaries, also contribute to this process [2,4].
The connection between the Black Sea and Mediterranean Sea has been subject to numerous interruptions and reconnections owing to fluctuations in sea levels, climatic shifts, and geological processes, as documented by the geological history of the area. As a result, the Black Sea has transformed into a brackish sea and numerous species have emerged or evolved in this region. The process of Mediterranean fauna penetrating the Black Sea is ongoing. Occasionally, Mediterranean Sea species previously unobserved in the Black Sea were discovered in this region [5]. The current fish fauna in the Black Sea comprises of approximately 190 species [6]. Analysis of the geographic origins of marine fish species indicated that the majority (59.26%) had an Atlantic-Mediterranean origin, 7.41% were cosmopolitan in nature, 31.22% were Ponto-Caspian relics (endemic to the region), and 2.12% were introduced from the Indo-Pacific and European waters [6].
The number of alien species in the Black Sea has recently increased, raising concerns regarding their potential impact on indigenous fish populations and ecosystems [7]. Notably, records of NIS species in the Black Sea have included members of the Sparidae family, which comprises approximately 150 species in 37 genera [8], and is primarily found in shallow temperate and tropical waters. NIS Sparid species are more commonly found along the Turkish coast and may play a role in local fisheries. Despite the expansion of Sparidae's range to the Black Sea, there is a scarcity of information on these fish species and their abundance, particularly in the Bulgarian sector. Consequently, citizen science could be a valuable tool for collecting data and monitoring the distribution of non-indigenous species.
In this study, we used citizen science from both small-scale fisheries and pelagic trawlers to expand data collection and engage the public in the scientific process. These data indicate the presence of four non-indigenous species of Sparidae fish in the coastal waters of the Bulgarian Black Sea sector during autumn 2022 and the warm season of 2023. The aim of this brief communication was to provide information on non-indigenous Sparidae species in Bulgarian Black Sea waters and summarize their previous sightings in the Black Sea. Furthermore, we reviewed recent studies on the distribution and biological traits of the identified species in their natural Mediterranean habitats.

2. Materials and Methods

This study implemented a research strategy developed by the Institute of Fish Resources with Aquarium in Varna, Bulgaria, which incorporates citizen science data (properly documented and accompanied by live samples or photographs) obtained from small-scale fisheries and pelagic trawlers between 2022-2023. This approach facilitated the identification of non-indigenous Sparidae species in Bulgarian Black Sea waters during the periods September-November 2022 and August-October 2023 (Figure 1).
The samples were collected using small fishing boats with passive fishing gear and a mesh size of 32 × 32 mm at depths of 1-10 meters along the central Bulgarian coast (near Byala and Kara Dere), as well as from pelagic trawlers operating at depths ranging from 25 m to 45 m (between C. Kaliakra and Tsarevo). The trawlers were equipped with midwater otter trawls (OTM) with mesh sizes of 16 × 16 mm and 18 × 1 8 mm. The lengths and weights of the specimens were measured onboard the fishing vessel.

3. Results

This study, conducted during the summer-autumn seasons of 2022-2023, documented the presence and increasing quantities of four non-indigenous species in coastal Bulgarian Black Sea waters: Spicara smaris (Linnaeus, 1758), Lithognathus mormyrus (Linnaeus, 1758), Diplodus puntazzo (Walbaum, 1792), and Diplodus annularis (Linnaeus, 1758) (Table 1, Figure 1 and Figure 2).
Among them, S. smaris was the most frequently observed NIS species. This species was identified at 16 different locations, mostly along the central and southern coasts, with quantities ranging from 0.01 to 60 kg and medium sizes ranging from 7.9 to 12.4 cm in length and 5.61 to 19.9 g in weight. S. smaris was recorded mostly at depths < 30 m. It should be noted that S. smaris quantity was very low during the observations in autumn of 2022, within the ranges of 0.01 to 0.05 kg, indicating a large fluctuation in the species' abundance and the possibility of occasional presence only.
Spicara smaris is commonly referred to as the picarel and is endemic to the Mediterranean Sea and eastern Atlantic Ocean. Greyish-above and silvery-below colouration vary according to factors such as age, sex, and season [9,10]. S. smaris inhabits muddy and rocky bottoms, as well as seagrass beds, with juveniles preferring seagrass beds as nursery areas [11,12,13]. It is classified as an omnivorous species, with a diet comprising zooplanktonic crustaceans, meroplanktonic larvae, and fish larvae [14]. The species can reach a maximum length of 21.24 cm [15], although the most commonly observed sizes in the Black Sea are 11.5 - 14.0 cm [16].
This species was initially discovered in the Black Sea near the coast of Türkiye by [17] and was later reported by [16,18,19]. S. smaris was first reported on the Bulgarian Black Sea coast by [20], a single specimen collected near Cape Galata, Varna District (Table 2). However, in recent years, their range and abundance have expanded and the species has periodically been found off the coasts of Bulgaria, Romania, and Russia. This species is more abundant along the eastern coast of Türkiye, where it contributes to commercial fisheries, with catch doubling between 1976 and 1991 [16]. Found at depths ranging from 15 m to 170 m [16], mainly in the upper layer, S. smaris can compete with native fish species for food and space, and may also prey on their eggs and larvae.
S. smaris is a protogynous sequential hermaphrodite fish, indicating that individuals first mature as females and later can become males. According to [46], the spawning season of S. smaris in the Mediterranean region begins in February and ends in May. [47] study, conducted in the Eastern Black Sea, found that the spawning season in this area was between May and June. This difference in spawning seasons is attributed to a variety of factors, including habitat conditions and food availability. We found small individuals with length of 7.9-9.2 cm, indicating the possibility of local reproduction of S. smaris.
Lithognathus mormyrus, referred to as the Atlantic striped sea bream, sand steenbras, or sand smelt, is a demersal marine species commonly found in the Mediterranean Sea, Atlantic Ocean, Southwestern Indian Ocean, and the Red Sea [48]. L. mormyrus is a non-indigenous species of Mediterranean origin that was first discovered in the Black Sea in 1958 near Varna Bay, as reported by [21]. Subsequently, this species was recorded along the coasts of Bulgaria and Romania during the 1980s [22,23,24] (Table 2). More recent findings by [24] and [26] revealed the presence of this species on the South Coast of Crimea and near Cape Aya. Atlantic striped bream has also been reported on the coast of Türkiye [27,28,29,31,32,49] and off the Caucasus coast [25,50]. This species has been observed in the coastal waters of the southeastern Crimea, specifically within the protected region of the Karadag Nature Reserve [33]. The recent adaptation of this species to the conditions of the Black Sea has been demonstrated by the presence of juveniles in Cossack Bay off the coast of Sevastopol and spawned individuals off the coast of Abkhazia [51,52]. Furthermore, according to [5], Atlantic striped sea bream is found under estuarine conditions near large rivers.
According to our records, a significant increase in the quantity of L. mormyrus was observed in the coastal waters around Byala at depths of < 10 m near the mouth of the Fandakliyska River in August 2023. The catch of this species was 20 kg with an average length and weight of 20 cm and 107 g, respectively. [53] reported that the asymptotic length of this species is 30.18 cm in the Gulf of Tunis. L. mormyrus is found at depths ranging from 0 to 150 m, with a preference for water between 10 and 30 m [54]. The preferred habitats of striped sea bream are rocky and sandy bottoms, and seagrass beds. In the Mediterranean region, it is commonly found in estuaries and lagoons, where juveniles often find essential nursing habitats [48].
Striped sea bream primarily consumes teleosts, crustaceans, molluscs, echinoderms, annelids, spongia and plantae and its diet vary across different life stages [55,56]. The species is a protandric hermaphrodite, indicating that some individuals change sex from male to female during their lifetime. Males reach sexual maturity at 16.21 cm (2.5 years), and females at 19.04 cm (3.6 years) [57]. [58] research from the Mediterranean Sea surrounding Eastern Libya concluded that the breeding season for the striped seabream is between May and August. In contrast, [59] findings indicate that the population in the Köyceğiz Lagoon, Türkiye, reproduces from late April until early June, which aligns with [60] results from Baymelek Lagoon, Türkiye. In the coastal waters of the Thracian Sea, Greece, the spawning period of striped sea bream ranges from May to September, with gamete emissions peaking in June-August [57]. Recent research has suggested a potential increase in L. mormyrus populations in the Black Sea [33]. Although this species has been noted to reproduce in the Black Sea, further research is needed to determine the spawning period in this basin [29].
Diplodus puntazzo, referred to as the sharpsnout seabream, has been observed in the coastal waters of Türkiye according to studies conducted by [38,41,42,43]. It is considered a rare and temporary inhabitant of the Bulgarian Black Sea coastal waters [21,34,35,36,37]. It is worth to note that the sharpsnout seabream can also be found off the coasts of Crimea [39] and Romania [40] (Table 2). During the current observations, a single catch of D. puntazzo with a weight of 60 kg, mean length of 22.3 cm and weight of 167.8 g was documented (Table 1). The location where this catch was made was close to Byala and the Fandakliyska River at a depth of less than 10 m.
Typically, D. puntazzo can grow to a maximum length of 60 cm, but it is mostly approximately 30 cm long [61]. In the eastern Adriatic Sea, the asymptotic length of this species is estimated at 45.28 cm [62]. Its diet is comprised of Plantae, Spongia, Tunicata, Echinodermata, Crustacea, Annelida, Mollusca, and Teleostei, with plants being the most important food source [63]. The species is found throughout the Mediterranean basin, including in the Strait of Gibraltar and the Adriatic, Aegean, Ionian, and Levantine Seas.
Similar to other Sparidae species, they are hermaphrodites. Young individuals are male, and after maturity they can transform into females. In its natural habitat, D. puntazzo spawns in the coastal waters between October and March [64]. Adults of this species usually reside in surf zones, with their preferred habitats being rocky bottoms and seagrass beds [63]. However, juveniles are also found in lagoons, brackish waters, and littoral pools [65]. The spawning times of species vary depending on the area they inhabit. For example, [66] noted that September through February was the reproductive period for the species off the Canary Islands. According to research conducted by [64], specimens from the Gulf of Tunis, Central Mediterranean, reproduce from September to December. [62] found that the spawning period of sharpsnout seabream in the Adriatic Sea occurred between August and October. Similarly, in a 2021 study by [41] on a southern Black Sea D. puntazzo population, the spawning period was found to be from August until November.
Diplodus annularis, referred to as annular seabream, is widely distributed in the eastern Atlantic and Mediterranean Seas [54]. This demersal fish species inhabits seagrass beds in shallow waters ranging from 0 to 50 m in depth [61], with a preference for Posidonia beds [67].
Based on a study by [45], D. annularis was observed in Sinop, Türkiye (Table 2). It was previously known as a common species along the Bulgarian coast of the Black Sea near Balchik, Varna, Nessebar, Pomorie, Burgas, and Sozopol [34,35,44]. Later, it was considered a rare summer visitor to Bulgarian Black Sea waters [21,37]. The current observations detected D. annularis in the central part of Bulgarian waters near the Fandakliyska River and Byala (at depths <10 m), with a catch quantity of 50 kg, mean lengths of 19.7 cm, and weight of 114 g.
As an omnivorous diurnal feeder, it primarily feeds on Mollusks, Teleosts, and small crustaceans [68,69,70]. Previous studies designated D. annularis as a protandrous species. However, recent findings by [71]. (2011) revealed a reproductive phenomenon known as non-functional hermaphroditism in this species. In this case, both male and female reproductive tissues are present, but do not function simultaneously, differing from sequential and simultaneous hermaphroditism, in which the reproductive tissues of both sexes are active at some point.
The spawning period of annular seabream varied between regions. [67] concluded that annular seabreams from the Gulf of Gables, Central Mediterranean, were reproducing from March to June. The spawning period for this species from the southern coast of Mallorca, northwestern Mediterranean Sea, peaks in May and June [71]. In contrast to the late spring-early summer breeding period demonstrated by [71], in the Central-Western Mediterranean Seas D. annularis has been noted to reproduce in late winter-spring, peaking between April and May [72]. The populations in the Adriatic Sea start spawning from the end of April and continue until the end of August, as reported by [73]. Variations in spawning times among populations can be attributed to differences in habitat conditions, with a special emphasis on the effects of temperature and food availability [67]. Further studies are required to investigate the reproductive cycle of D. annularis in the Black Sea.

4. Discussion

Non-indigenous fish species can have a range of impacts on the native biodiversity, ecosystem functioning, and human well-being of invaded regions, which are determined by their ecological traits, interactions, and environmental conditions. These impacts include increased competition, predation on local fish species, increased herbivory, transmission of parasites or diseases that can affect native fish species, and hybridisation, which can influence the genetic integrity and diversity of native populations [74,75,76]. Some non-indigenous fish species have the potential to become invasive, establish populations, proliferate, and have ecological and economic effects on native species and fisheries [3].
Over the past few decades, the discovery of 28 new fish species [7] in the Black Sea has demonstrated the effects of both the "mediterranization" process and the accidental introduction of exotic species of Indo-Pacific origin on fish species diversity [6,39,77]. Moreover, some species have already expanded their range, such as Sarpa salpa, which was first detected along the southwestern coast of Crimea in 1999 and has since become a common species in this region [24,78,79].
Turkey's coastal regions host NIS Sparid species more frequently, which may have implications for the local fishing industry. According to the citizen science data collected in this study, S. smaris appears to be the most frequently observed NIS species in 2022-2023, detected at 16 locations, primarily along the central and southern Bulgarian Coast. We observed an increase in the quantity of identified Sparid species in the central part of the Bulgarian coast in August 2023 (up to 60 kg), compared to the autumn season of 2022, when only S. smaris was detected with a maximum catch of 0.05 kg. Notably, high oscillations in abundance suggest the occasional presence of this species along the Bulgarian coast. However, the presence of small individuals also provides options for local reproduction. Additionally, single records of L. mormyrus, D. puntazzo, and D. annularis were discovered in shallow waters close to the Fandakliyska River at depths of less than 10 m, but their catches were not low, and ranged between 20-60 kg per species.
The identified Sparidae fish were classified as omnivorous and hermaphroditic, which may provide certain advantages over the native species. Furthermore, their ability to adapt to the Black Sea's climatic changes is facilitated by the region's projected warming, with a maximum increase in sea surface temperature with 2.81-0.53°C per century in summer [80]. The effects of climate change may support the introduction of new species and adaptation of existing species, potentially affecting physiology, migration, aggregation formation, food availability, and reproduction processes. The Black Sea ecosystem is highly susceptible to both environmental and anthropogenic stressors [81], and increased overfishing pressure can render fish stocks more vulnerable to future climate change and potential biological invasions.
Finally, it is crucial to recognize that non-indigenous species can offer prospects for profitable utilization, transforming environmental issues into economic advantages. For example, the Muricidae snail Rapana venosa, which was introduced to the Black Sea from the Japan Sea in the 1940s, has emerged as a valuable target for local fishing industries, generating a new revenue stream [82]. Managing non-indigenous species in marine ecosystems can help to sustainably utilise their commercial potential without causing ecological disturbances.

5. Conclusions

Four non-native sparid species, Lithognathus mormyrus, Spicara smaris, Diplodus puntazzo, and Diplodus annularis, were monitored through citizen science data collection obtained from small-scale fisheries and pelagic trawlers operating along the Bulgarian coastline of the Black Sea. The highest catch of these species was recorded in August 2023, weighing–20-60 kg per species. While S. smaris was the most frequently observed NIS species, with 16 detections during warm months of 2022-2023, its quantity fluctuated significantly in this period, with possibility of occasional presence only. The species was detected primarily along the central and southern Bulgarian coasts, with catch ranging from 0.01 to 60 kg and mean lengths ranging from 7.9 to 12.4 cm.
The other Spridae species, L. mormyrus, D. puntazzo, and D. annularis, were documented with single catches in August 2023 in central coastal regions at depths of less than 10 m, particularly close to the Fandakliyska River. The identified Sparidae are omnivorous and hermaphroditic fish, providing certain advantages over native species. These fish can adapt to the projected warming of the Black Sea, particularly considering that their reproductive processes are influenced by temperature and food availability. Effective management is essential for capitalising on the commercial potential of non-native species.

Author Contributions

Conceptualization, F.Ts., V.M., E.P.P., T. S., K.G., S.V., Z.M., and M.G.; methodology, F.Ts., V. M. and T.S.; software, F.Ts. and R. S; validation, F. Ts., V.M, T.S., and E.P. P: formal analysis, F. Ts., V. M, T.S.; Investigation, F. Ts., E. P. P, T. S., R. S., L. N., K. G., S. V., M. G, Z. M; Resources, F. Ts., and E. P. P: data curation, F.Ts. and E. P. P.; writing, original draft preparation; F. Ts., V. M, T. S., L. N. and K. G; writing—review and editing, F. Ts. and V. M; visualization, F.Ts., R. S: supervision, F.Ts., V. M and E. P. P; project administration, E.P.P; funding acquisition, E.P.P. All the authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by MASRI: Infrastructure for Sustainable Development of Marine Research and Participation in the European Infrastructure EURO - ARGO - MASRI is a project of the National Roadmap for Scientific Infrastructure (2020 – 2027) of The Republic of Bulgaria.

Data Availability Statement

The data presented in this study are available upon request from the corresponding author. The data are not publicly available due to institutional restrictions.

Acknowledgments

This research was supported by MASRI: Infrastructure for Sustainable Development of Marine Research and Participation in the European Infrastructure EURO - ARGO - MASRI is a project of the National Roadmap for Scientific Infrastructure (2020 – 2027) of The Republic of Bulgaria, gratefully acknowledged by the authors.

Conflicts of Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

References

  1. Dumont, H. J.; Shiganova, T. A.; Niermann, U. (Eds.). Aquatic invasions in the Black, Caspian, and Mediterranean seas, Springer Science & Business Media 2004, Vol. 35.
  2. Oğuz, T.; Öztürk, B.; Temel, O.Ğ.U.Z. Mechanisms impeding the natural mediterranization process of Black Sea fauna. Journal of Black Sea/Mediterranean Environment 2011, 17(3), pp.234-253.
  3. Boltachev A.; Karpova E. Faunistic Revision of Alien Fish Species in the Black Sea. Russian Journal of Biological Invasions 2014, 5 (4), 225–241. [CrossRef]
  4. Shalovenkov, N. Alien species invasion: Case study of the Black Sea. Coasts and estuaries. Elsevier, 2019, 547-568. [CrossRef]
  5. Guskov G.E. Analysis of Distribution of Striped Seabream (Lithognathus mormyrus L., 1758) (Actinopterygii: Sparidae) in the Black Sea. Russian Journal of Biological Invasions, 2021, 12 (2), pp. 176–181. [CrossRef]
  6. Yankova M.; Pavlov D.; Ivanova P.; Karpova E.; Boltachev A.; Öztürk B.; Bat L.; Oral M.; Mgeladze M. Marine fishes in the Black Sea: recent conservation status. Mediterranean Marine Science 2014, 15(2), pp. 366-379. [CrossRef]
  7. Çinar, M.E.; Bilecenoğlu, M.; Yokeş, M.B.; Öztürk, B.; Taşkin, E., Bakir, K.;Doğan, A.; Açik, Ş. (2021) Current status (as of end of 2020) of marine alien species in Türkiye. PLoS ONE, 2021, 16(5): e0251086. [CrossRef]
  8. Nelson, J. S.; Grande, T. C.; Wilson, M. V. H. 2016. Fishes of the World. 5th ed.; John Wiley & Sons, 2016, pp. 707.
  9. Şalcioğlu, A.; Gubili, C.; Krey, G.; Sakinan, S.; Bi̇lgi̇n, R. Molecular characterization and phylogeography of Mediterranean picarels (Spicara flexuosa, S. maena and S. smaris) along the coasts of Turkey and the Eastern Mediterranean. Regional Studies in Marine Science 2021, 45, 101836, pp 1-13. [CrossRef]
  10. Froese, R.; Pauly, D. Editors. FishBase. World Wide Web electronic publication. Available online: Search FishBase (accessed on 29/04/2024).
  11. Dulčić, J.; Pallaoro, A.; Cetinić, P.; Kraljević, M.; Soldo, A.; Jardas, I. Age, growth and mortality of picarel, Spicara smaris L.(Pisces: Centracanthidae), from the eastern Adriatic (Croatian coast). Journal of Applied Ichthyology 2003, 19(1), pp. 10-14. [CrossRef]
  12. Bektas, Y.; Aksu, I.; Kalayci, G.; Irmak, E.; Engin, S.; Turan, D. Genetic differentiation of three Spicara (Pisces: Centracanthidae) species, S. maena, S. flexuosa and S. smaris: and intraspecific substructure of S. flexuosa in Turkish coastal waters. Turkish Journal of Fisheries and Aquatic Sciences 2018, 18(2), pp. 301-311. [CrossRef]
  13. Guidetti, P. Differences among fish assemblages associated with nearshore Posidonia oceanica seagrass beds, rocky–algal reefs and unvegetated sand habitats in the Adriatic Sea. Estuarine, Coastal and Shelf Science 2000, 50(4), pp. 515-529. [CrossRef]
  14. Karachle, P. K.; StergIou, K. I. Diet and feeding habits of Spicara maena and S. smaris (Pisces, Osteichthyes, Centracanthidae) in the North Aegean Sea. acta aDrIatIca 2014, 55(1), pp. 75-84.
  15. Tsangridis, A.; Filippoussis, N. Length-based approach to the estimation of growth and mortality parameters of Spicara smaris (L. ) in the Saranikos Gulf, Greece, and remarks on the application of the Beverton and Holt relative yield per recruit model. FAO Fish. Rep. 1988, 412, pp. 94-107.
  16. Ismen, A. Growth, mortality and yield per recruit model of picarel (Spicara smaris L.) on the eastern Turkish Black Sea coast. Fisheries Research 1995, 22(3-4), pp. 299-308. [CrossRef]
  17. Kessler, K. T. A zoological voyage to the northern coast of the Black Sea and Crimea in 1858. Kyiv, Ukraine 1860, 1–248, Pls. 1–2.
  18. Svetovidov, A.N. The Black Sea Fishes. Nauka, Moscow 1964. [The Fishes of the Black Sea]. Nauka Publ., Moscow-Leningrad, pp. 551. (In Russian).
  19. Bilgin, Ö.; Çarli, U.; Erdoğan, S.; Mavi̇ş, M. E.; Göksu, M.; Gürsu, G. G.; Yilmaz, M. Determination of Amino Acid Content of Picarel (Spicara smaris) Caught in the Black Sea (Around Sinop Peninsula) Using LC-MS / MS and Its Weight-Length Relationship. Türk Tarım ve Doğa Bilimleri Dergisi 2019, 6(2), pp. 130-136. (In Turkish). [CrossRef]
  20. Stojanov, S. Zwei fur die ichthyofauna des Schwarzen meers unbenannte arten aus der familie Maenidae. Bulletin de l’Institut Zoologique de l’Academie des Sciences de Bulgarie 1954, 3, pp. 257-271. (In Bulgarian, German summery).
  21. Stojanov S.; Gueorguiev, G.; Ivanov, L.; Hristov, D.; Kolarov, P.; Alexandrova, K.; Karapetkova M. 1963.The fishes of Black Sea. Varna, Bulgaria, 1963 pp. 246 (In Bulgarian).
  22. Stanciu M.; Ilie G. Lithognatus mormyrus, a new species of Sparidae at the Romanian littoral. Pontus Euxinus, Studii si cercetari CSMN-Constanta 1980, pp. 107–110.
  23. Vasil’eva, E.D. Fish of the Black Sea. Key to Marine, Brackish Water,Euryhaline, and Migratory Species with Color Illustrations, Collected by: S.V.Bogorodsky. VNIRO, Moscow, 2007; pp. 238. (In Russian).
  24. Boltachev A.R.; Karpova E.P.; Kirin M.P. The first discovery of the Atlantic shrew Lithognathus mormyrus (L., 1758) (Osteichthyes, Sparidae) in the Black Sea coastal zone of Crimea). Marine Ecological Journal 2013. T.ХII.No4. C. 96.
  25. Guchmanidze, A.; Boltachev, A. Notification of the first sighting of sand steenbras Lithognathus mormyrus (Linnaeus, 1758) and modern species diversity of the family Sparidae at the Georgian and Crimean Black Sea coasts. Journal of the Black Sea/Mediterranean Environment 2017, 23(1). pp. 48–55.
  26. Gus’kov, G.; Zherdev, N; Bukhmin, D. New and Rare Fish Species off the Northern Shore of the Black Sea and Anthropogenic Factors Affecting their Penetration and Naturalization. Sea 2022, 1, pp. 66-81. [CrossRef]
  27. Engin, S.; Keskin, A.; Akdemir, T.; Seyhan, D. Occurrence and new geographical record of striped seabream Lithognathus mormyrus (Linnaeus, 1758) in the Turkish coast of Black Sea. Turkish Journal of Fisheries and Aquatic Sciences 2015, 15(4), pp. 937-940. [CrossRef]
  28. Satilmis, H.; Sumer, C.; Aksu, H.; Çelik, S. About the new record of striped Seabream, Lithognathus mormyrus (Linnaeus, 1758) (Pisces: Teleostei: Sparidae) from the coastal waters of the southern Black Sea, Türkiye. Journal of Animal and Veterinary Advances 2014, 13(3), pp. 171-173.
  29. Kasapoğlu, N.; Çankırılıgil, E.; Düzgüneş, Z.; Çakmak, E.; Eroğlu, O. The bio-ecological and genetic characteristics of sand steenbras (Lithognathus mormyrus) in the Black Sea. Journal of the Black Sea/Mediterranean Environment 2020, 26(3), pp. 249-262.
  30. Aydin, M. The new maximum length of the striped sea bream (Lithognathus mormyrus L., 1758) in the Black Sea region. Aquatic Sciences and Engineering 2018, 33(2), pp. 50-52. [CrossRef]
  31. Aydin, M.; Sözer, A. The Length–Weight Relationship and Condition Factor of a Non-Native Fish Species: Striped Sea Bream (Lithognathus mormyrus L., 1758) in the Black Sea. Journal of Anatolian Environmental and Animal Sciences 2019, 4(3), pp. 319-324. [CrossRef]
  32. Karadurmuş, U.; Aydin, M. (2021). Morphological Characterization of Lithognathus mormyrus (Linnaeus, 1758) Populations in the Southern Black Sea (Türkiye). Aquatic Sciences and Engineering 2021, 37(1), pp. 38-45. [CrossRef]
  33. Maltsev V.; Vasilets V.E. First detection of the striped sea breams Lithognathus mormyrus (Sparidae) off the coast of South – Eastern Crimea. In the collection: Biological diversity: study, conservation, restoration, rational use. In Proceedings of the Materials of the II International Scientific and Practical Conference. 2020. pp. 621-626.
  34. Drensky P. Synopsis and distribution of fishes in Bulgaria. Annulaire de l’Universite de Sofia, Faculte de Sciences 1948, 44(3), pp. 11-71. (In Bulgarian, English summery).
  35. Drensky P. Fishes of Bulgaria. Fauna of Bulgaria 1951, 2. Sofia, BAS, 270 p. (In Bulgarian).
  36. Gueorguiev G.; Alexandrova, K.; Nikoloff, D. Observations sur la reproduction des poisons le long du littoral Bulgare de la Mer Noire. Bulletin de l’Institut Zoologique de l’Academie des Sciences de Bulgarie 1960, 9, pp. 255-292. (In Bulgarian, French summery).
  37. Manolov J. Apercu sur la composition d’espece de la familie Sparidae (Pisces) dans les eaux du littoral Bulgare de la Mer Noire. Proceedings of the Institute of Oceanography and Fisheries – Varna 1970, 10, pp. 165-189. (In Bulgarian, French summery).
  38. Bat, L.; Erdem, Y.; Ustaoglu, S.; Yardim, Ö; Satilmis, H. A study on the fishes of the central Black Sea coast of Türkiye. Journal of Black Sea/Mediterranean Environment 2005, 11(3), pp. 281-296.
  39. Boltachev, A.; Karpova, E.; Danilyuk, O. Findings of new and rare fish species in the coastal zone of the Crimea (the Black Sea). Journal of Ichthyology 2009, 49, pp. 277-291. [CrossRef]
  40. Papadopol, N.; Antone, V.; Bilba, A. New Data on the Sighting of Rare Fish Species of Mediterranean Origin in Romanian Black Sea Waters. Revista Cercetări Marine-Revue Recherches Marines-Marine Research Journal 2016, 46(2), pp. 4-9. [CrossRef]
  41. Aydin, M.; Saglam, H. First report of predation on egg capsules of invasive Rapa whelk by sharpsnout seabream (Diplodus puntazzo) in the Black Sea. Thalassas: An International Journal of Marine Sciences 2019, 35, pp. 319-321. [CrossRef]
  42. Aydın, M.; Özdemir, Ç. Age, growth, reproduction and fecundity of the Sharpsnout Seabream (Diplodus puntazzo Walbaum, 1792) in the Black Sea region. Turkish Journal of Fisheries and Aquatic Sciences 2021, 22(5). [CrossRef]
  43. Aydin, M. Maximum length and weight of sharpsnout seabream (Diplodus puntazzo Walbaum, 1792) for Black Sea and East Mediterranean Sea. Turkish Journal of Maritime and Marine Sciences 2019, 5(2), pp. 127-132.
  44. Drensky P. Contribution a l’etude des poisons de la Mer Noire, recoltes sur les cotes Bulgares. Journal of the Bulgarian Academy of Sciences 1923, 25, pp. 6-112. (In Bulgarian, French Summery).
  45. Samsun, O.; Akyol, O.; Ceyhan, T.; Erdem, Y. Length-weight relationships for 11 fish species from the Central Black Sea, Türkiye. Ege Journal of Fisheries and Aquatic Sciences 2017, 34(4), pp. 455-458. [CrossRef]
  46. Karlou-Riga, C.; Petza, D.; Charitonidou, K.; Anastopoulos, P.; Koulmpaloglou, D. S.; Ganias, K. Ovarian dynamics in picarel (Spicara smaris, L., Sparidae) and implications for batch fecundity and spawning interval estimation. Journal of Sea Research 2020, 160, 101894. [CrossRef]
  47. ŞAHİN, T.; GENÇ, Y. Some biological characteristics of picarel (Spicara smaris, Linnaeus 1758) in the Eastern Black Sea Coast of Türkiye. Turkish Journal of Zoology 1999, 23(5), pp. 149-156. (In Turkish).
  48. Hammami, I.; Bahri-Sfar, L.; Kaoueche, M.; Grenouillet, G.; Lek, S.; Kara, M.H.; Ben Hassine, O. Morphological characterization of striped seabream (Lithognathus mormyrus, Sparidae) in some Mediterranean lagoons. Cybium 2013, 37(1-2), pp. 127-139.
  49. Aydın, M. Mırmır balığının (Lithognathus mormyrus L., 1758) Karadeniz’deki varlığı. Turkish Journal of Maritime and Marine Sciences 2017, 3, pp. 49-54.
  50. Guskov G.E.; Zhivoglyadov A.A.; Chepurnaya T.A.; Shimanskaya E.I. Detection of the Atlantic shrew Lithognathus mormyrus in net catches off the Caucasian coast of the Russian Federation. Modern problems of science and education 2017, (5).
  51. Dbar, R.S.; Vol’ter, E.R.; Malandziya, V.I. On the question of the invasion of the sand steenbras Lithognathus mormyrus (Linnaeus, 1758) into the Black Sea on the example of the water area of Abkhazia. In Proceedings of the Biologicheskoe raznoobrazie: Izuchenie, sokhranenie, vosstanovlenie, ratsional’noe ispol’zovanie. Mat. II Mezhdunar.nauchno-praktich. konf. (Biological Diversity: Re-search, Conservation, Restoration, and Rational Use.Proc. II Int. Sci.-Pract. Conf. Kerch, (May 27–30,2020)), Simferopol: Arial, 2020, pp. 293–297.
  52. Karpova, E. P. Naturalization of striped seabream Lithognathus mormyrus (Sparidae) in the Black Sea. Russian Journal of Biological Invasions 2020, 11, pp. 220-224. [CrossRef]
  53. Khaldi, A.; Chater, I.; Elleboode, R.; Mahé, K.; Chakroun-Marzouk, N. Age, growth and mortality of the striped seabream Lithognathus mormyrus (Linnaeus, 1758) in the Gulf of Tunis (Central Mediterranean Sea). Journal of the Marine Biological Association of the United Kingdom 2021. 101(1), pp. 159-167. [CrossRef]
  54. Bauchot, M.L.; Hureau, J.C. Sparidae. In Fishes of the north-eastern Atlantic and the Mediterranean. Editor 1 Whitehead P. J. P., Editor 2 Bauchot M. L., Editor 3 Hureau J. C., Editor 4 Nielsen J., Editor 5 Tortonese E., Eds.; UNESCO: Paris, France, 1986; Volume 2, pp. 883-907.
  55. Jaerisch, J.; Zander, C. D.; Giere, O. Feeding behaviour and feeding ecology of two substrate burrowing teleosts, Mullus surmuletus (Mullidae) and Lithognathus mormyrus (Sparidae), in the Mediterranean Sea. Bulletin of Fish Biology 2010, 12, pp. 27-39.
  56. Hamida, N. B. H.; Hamida, O. B. A. B. H.; Jarboui, O.; Missaoui, H. Diet composition and feeding habits of Lithognathus mormyrus (Sparidae) from the Gulf of Gabes (Central Mediterranean). Journal of the Marine Biological Association of the United Kingdom 2016, 96(7), pp. 1491-1498. [CrossRef]
  57. Kallianiotis, A.; Torre, M.; Argyri, A. Age, growth, mortality, reproduction and feeding habits of the striped seabream, Lithognathus mormyrus (Pisces: Sparidae) in the coastal waters of the Thracian Sea, Greece. Scientia Marina 2005, 69(3), pp. 391-404. [CrossRef]
  58. Ali, S.; Al Fergani, E. S. (2016). Reproductive Biology of the Striped Seabream Lithognathus mormyrus (Linnaeus, 1758) from Al Haneah Fishing Site, Mediterranean Sea, Eastern Libya. Journal of Life Sciences 2016, 10, pp. 171-181. [CrossRef]
  59. Reis, I.; Ateş, C. Age, growth, length–weight relation, and reproduction of sand steenbras, Lithognathus mormyrus (Actinopterygii: Perciformes: Sparidae), in the Köyceğiz Lagoon, Mediterranean. Acta Ichthyologica et Piscatoria 2020, 50(4), pp. 445-451. [CrossRef]
  60. Emre, Y.; Balik, İ.; Sümer, Ç.; Oskay, D. A.; Yeşilçimen, H. Ö. Age, growth, length-weight relationship and reproduction of the striped seabream (Lithognathus mormyrus L., 1758)(Sparidae) in the Beymelek Lagoon (Antalya, Türkiye). Turkish Journal of Zoology 2010, 34(1), pp. 93-100. [CrossRef]
  61. Fischer, W.; Bauchot, M.L.; Schneider, M. Fiches FAO d'identification pour les besoins de la peche revision 1. Mediterranee et mer Noire. Zone de peche 37 1987, (2): Vertebres, Rome, FAO, pp. 761-1530.
  62. Kraljevic, M.; Matic-Skoko, S.; Ducic, J.; Pallaoro, A.; Jardas, I.; Glamuzina, B. Age and growth of sharpsnout seabream Diplodus puntazzo (Cetti, 1777) in the eastern Adriatic Sea. Cahiers de biologie marine 2007, 48(2), pp. 145- 154.
  63. Chaouch, H.; Hamida, O. B. A. B. H.; Ghorbel, M.; Jarboui, O. Diet composition and food habits of Diplodus puntazzo (Sparidae) from the Gulf of Gabès (Central Mediterranean). Journal of the Marine Biological Association of the United Kingdom 2013, 93(8), pp. 2257-2264. [CrossRef]
  64. Mouine, N.; Francour, P.; Ktari, M. H.; Chakroun-Marzouk, N. Reproductive Biology of Four Diplodus Species Diplodus vulgaris, D. annularis, D. sargus sargus and D. Puntazzo (Sparidae) in the Gulf of Tunis (Central Mediterranean). Journal of the Marine Biological Association of the United Kingdom 2012, 92(3), pp. 623–31. [CrossRef]
  65. Ventura, D.; Jona Lasinio, G.; Ardizzone, G. Temporal partitioning of microhabitat use among four juvenile fish species of the genus Diplodus (Pisces: Perciformes, Sparidae). Marine Ecology 2015, 36(4), pp. 1013-1032. [CrossRef]
  66. Pajuelo, J. G.; Lorenzo, J. M.; Domínguez-Seoane, R. Gonadal development and spawning cycle in the digynic hermaphrodite sharpsnout seabream Diplodus puntazzo (Sparidae) off the Canary Islands, northwest of Africa. Journal of Applied Ichthyology 2008, 24(1), pp. 68-76. [CrossRef]
  67. Chaouch, H.; Hamida-Ben Abdallah, O.; Ghorbel, M.; Jarboui, O. Reproductive biology of the annular seabream, Diplodus annularis (Linnaeus, 1758), in the Gulf of Gabes (Central Mediterranean). Journal of Applied Ichthyology 2013, 29(4), pp. 796-800. [CrossRef]
  68. Pita, C.; Gamito, S.; Erzini, K. Feeding habits of the gilthead seabream (Sparus aurata) from the Ria Formosa (southern Portugal) as compared to the black seabream (Spondyliosoma cantharus) and the annular seabream (Diplodus annularis). Journal of Applied Ichthyology 2002, 18(2), pp. 81–86. [CrossRef]
  69. Sánchez-Jerez, P.; Gillanders, B.M.; Rodriguez-Ruiz, S.; Ramos-Esplá, A.A. Effect of an artificial reef in Posidonia meadows on fish assemblage and diet of Diplodus annularis. ICES Journal of Marine Science.: Journal Du Conseil 2002, 59, pp. 59-68. [CrossRef]
  70. Chaouch, H.; Hadj Hamida, O.B.; Ghorbel, M.; Othman, J. Feeding habits of the annular seabream, Diplodus annularis (Linnaeus, 1758) (Pisces: Sparidae), in the Gulf of Gabes (Central Mediterranean). Cahiers de Biologie Marine 2014, 55(1), pp. 13- 19.
  71. Alonso-Fernández, A.; Alós, J.; Grau, A.; Domínguez-Petit, R.; Saborido-Rey, F. The Use of Histological Techniques to Study the Reproductive Biology of the Hermaphroditic Mediterranean Fishes Coris julis, Serranus scriba, and Diplodus annularis. Marine and Coastal Fisheries 2011, 3(1), pp. 145–159. [CrossRef]
  72. Donnaloia, M.; Zupa, W.; Arnesano, M.; Neglia, C.; Facchini, M. T.; Carbonara, P. Reproductive biology of Diplodus annularis (linnaeus, 1758) in the central-western mediterranean seas. Biol Mar Mediterr 2017, 24(1), pp. 182-183.
  73. Matić-Skoko, S.; Kraljević, M.; Dulčić, J.; Jardas, I. Age, growth, maturity, mortality, and yield-per-recruit for annular sea bream (Diplodus annularis L.) from the eastern middle Adriatic Sea. Journal of Applied Ichthyology 2007, 23(2), pp. 152-157. [CrossRef]
  74. Gherardi, F. Biological invasions in inland waters: an overview. Biological invaders in inland waters: profiles, distribution, and threats 2007, pp. 3-25.
  75. Arndt, E.; Givan, O.; Edelist, D.; Sonin, O.; Belmaker, J. Shifts in eastern Mediterranean fish communities: Abundance changes, trait overlap, and possible competition between native and non-native species. Fishes 2018, 3(2), pp. 19. [CrossRef]
  76. Milardi, M.; Gavioli, A.; Soininen, J.; Castaldelli, G. Exotic species invasions undermine regional functional diversity of freshwater fish. Scientific Reports 2019, 9(1), 17921. [CrossRef]
  77. Turan, C.; Gürlek, M.; Özeren, A.; DOĞDU, S. A. First Indo-Pacific fish species from the Black Sea coast of Turkey: Shrimp scad Alepes djedaba (Forsskål, 1775)(Carangidae). Natural and Engineering Sciences 2017, 2(3), pp. 149-157. [CrossRef]
  78. Boltachev, A.R.; Yurakhno, V.M. New data on continuous mediterranization of ichthyofauna of the BlackSea, Vopr. Ikhtiol 2002, 42(6), pp. 744–750.
  79. Boltachev, A.R.; Karpova, E.P. Morskie ryby Krymskogo poluostrova (Marine Fishes of Crimean Peninsula), Simferopol: BiznesInform 2012.
  80. Schaltout, M.; Omstedt, A. Recent sea surface temperature trends and future scenarios for the Mediterranean Sea. Oceanologia 2014, 56(3), pp. 411-443.
  81. Daskalov, G.; Boicenko, L.; Grishin, A.; Lazar, L.; Mihneva, V.; Shlyahov, V.; Zengin, M. 2017. The architecture of collapse: Regime shift and recovery in a hierarchically structured marine ecosystem. Global Change Biology 2017, 23(4), pp. 1486-1498. [CrossRef]
  82. FAO. The State of Mediterranean and Black Sea Fisheries 2022. General Fisheries Commission for the Mediterranean. Rome: FAO 2022. [CrossRef]
Figure 1. Map of the Bulgarian Black Sea sector, including locations of the collected Sparidae fish (a) localities of S. smaris in 2022-2023 and (b) localities of L. mormyrus, D. annualis, and D. puntazzo in 2023.
Figure 1. Map of the Bulgarian Black Sea sector, including locations of the collected Sparidae fish (a) localities of S. smaris in 2022-2023 and (b) localities of L. mormyrus, D. annualis, and D. puntazzo in 2023.
Preprints 105285 g001
Figure 2. Non-indigenous Sparidae fish found in 2023: A) L. mormyrus, B) D. puntazzo, C) S. smaris, and D) D. annularis. (The Aquarium Varna received live fish specimens that were subsequently photographed).
Figure 2. Non-indigenous Sparidae fish found in 2023: A) L. mormyrus, B) D. puntazzo, C) S. smaris, and D) D. annularis. (The Aquarium Varna received live fish specimens that were subsequently photographed).
Preprints 105285 g002
Table 1. Citizen science data for identified non-indigenous sparid species, including sampling dates, coordinates, depths, catch quantities, mean length, and mean weight per locality.
Table 1. Citizen science data for identified non-indigenous sparid species, including sampling dates, coordinates, depths, catch quantities, mean length, and mean weight per locality.
NIS
Fish species
Finding date Fishing gear
mesh size
Coordinates Depth (m)
Catch quantity (kg) Mean Length (cm) Mean weight (g)
Latitude Longitude
S. smaris 13.09.2022 16/16 mm 43.193 28.061 18 21.4 0.01057 7.9 5.61
1.11.2022 16/16 mm 42.982 27.926 26.5 27.1 0.01666 9.5 8.33
1.11.2022 18/18 mm 42.970 27.947 27 23.4 0.00846 9.6 8.46
2.11.2022 16/16 mm 43.067 27.949 24.7 27.8 0.00884 9.7 8.84
2.11.2022 18/18 mm 43.063 27.942 24 29 0.00622 8.6 6.22
10.11.2022 16/16 mm 43.182 28.022 23.3 23.2 0.03335 8.84 6.67
11.11.2022 18/18 mm 42.951 27.947 27.2 24.4 0.02146 8.9 7.15
15.11.2022 16/16 mm 43.381 28.527 32.6 32.4 0.00711 8.9 7.11
18.11.2022 18/18 mm 42.890 27.946 32.9 30.5 0.04728 9.2 7.73
31.8.2023 16X16 mm 42.979 27.925 25 26.2 40.95 12.3 19.12
31.8.2023 16X16 mm 42.978 27.924 24.9 26.4 7.23 12.3 19.9
31.8.2023 16X16 mm 43.048 27.929 26.2 25 6 12.4 18.8
31.8.2023 16X16 mm 42.980 27.923 25.1 26.1 4 12.2 19.66
31.8.2023 32/32 mm 42.895 27.902 1 5 60 12.4 18.96
6.10.2023 16X16 mm 42.261 27.980 43.3 42 28.5 11 14.32
13.10.2023 16X16 mm 42.808 28.036 32.1 35.5 7.1 10.93 14.25
L. mormyrus 28.8.2023 32/32 mm 42.902 27.901 1 5 20 20 107
D. puntazzo 30.8.2023 32/32 mm 42.912 27.899 1 5 60 22.3 167.8
D. annularis 29.8.2023 32/32 mm 42.907 27.899 1 5 50 19.7 114
Table 2. Summarized data on discoveries of non-indigenous Sparid species in Black Sea.
Table 2. Summarized data on discoveries of non-indigenous Sparid species in Black Sea.
Species Location of
Detection
Year of
Discovery
Reference
Spicara smaris Coast of Türkiye 1860-1964 [17,18]
Cape Galata, Varna (Bulgaria) 1952 [20]
Coast of Türkiye from Sinop to the Georgian border 1991 and 1992 [16]
Sinop (Türkiye) 2018 [19]
Lithognathus mormyrus Varna Bay
Romania-Bulgaria
1958
1980-2013
[21]
[5,22,23,24]
Varna (Bulgaria) 2007 [5]
Near the mouth of the Hosta River, Matsesta R., Kudepsta R., Mzymta R. (Russia) 2007 [5]
Sukhumi, Pitsunda (Ab-khazia) 2013 [5]
Cape Aya (Crimea) 2013 [5,24,25]
Crimea 2013 [26]

Çamburnu Harbour-Trabzon (Türkiye) 2013 [27]



























Diplodus puntazzo












Diplodus annularis
Arhavi-Artvin (Türkiye)
Derepazarı-Rize (Türkiye)
Pazar-Rize (Turkiey)
Rumeli Feneri-İstanbul (Türkiye)
Sinop (Türkiye)
Kobuleti (Georgia)

Dzhubga (Russia)
Sevastopol (Crimea)

Aya Cape (Crimea)

Trabzon (Türkiye)
Kazachya Bay (Crimea)

Caucasus
Yalta (Crimea)
Lazarevskoe (Russia)
Gelendzhik (Russia)
Ordu (Turkiey)

Novorossiysk (Russia)
Maly Utrish (Russia)
Sukko (Russia)
Karadag biological station (Crimea)
Ordzhonikidze (Crimea)
Turkish coast

South-Eastern Crimea
Near Burgas (Bulgaria)
Near Sozopol (Bulgaria)
Bulgarian Black Sea coast


Sinop and Samsun (Türkiye)

Crimea
Agigea (Romania)
Hopa region (Türkiye)
between Sinop and Hopa (Türkiye)
Ordu (Türkiye)
Black Sea from Balchik to Sozopol (Bulgaria)

Bulgarian Black Sea (rare presence)

Central Black Sea, Sinop (Türkiye)
2013
2013-2014
2013
2013
2013
2014
2014
2014

2015

2015
2016
2016
2016
2016
2017
2017-2018

2019
2019
2019
2019

2020
2020

-
1948
1950
1960-1970


between January 1998 and February 2003
from 1999 to 2008
2016
2017
between April 2018 and March 2019
2019
1923-1951


1960-1970

between
September 2016 and February 2017
[27] Engin et. al. (2015)
[27] Engin et. al. (2015)
[27] Engin et. al. (2015)
[27] Engin et. al. (2015)
[28] Satilmis et. al. (2014)
[25] Guchmanidze and Boltachev (2017)
[5] Guskov (2021)
[5] Guskov (2021)
[25] Guchmanidze and Boltachev (2017)
[29] Kasapoğlu et. al. (2020)
[25] Guchmanidze and Boltachev (2017)
[26] Gus'kov et. al. (2022)
[5] Guskov (2021)
[5] Guskov (2021)
[5] Guskov (2021)
[30,31] Aydin (2018), Aydin and Sözer (2019)
[5] Guskov (2021)
[5] Guskov (2021)
[5] Guskov (2021)
[5] Guskov (2021)

[5] Guskov (2021)
[32] Karadurmuş and Aydin (2021)
[33] Maltsev et. al. (2020)
[34] Drensky (1948)
[35] Drensky (1951)
[21,36,37] Gueorguiev et al. (1960), Stojanov et al. (1963), Manolov (1970)
[38] Bat et. al. (2005)

[39] Boltachev et. al. (2009)
[40] Papadopol et. al. (2016)
[41] Aydin and Saglam (2019)
[42] Aydın and Özdemir (2021)
[43] Aydin (2019)
[34,35,44] Drensky (1923, 1948,1951)

[21,37] Stojanov et al., 1963; Manolov, 1970
[45] Samsun et. al. (2017)
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.
Copyright: This open access article is published under a Creative Commons CC BY 4.0 license, which permit the free download, distribution, and reuse, provided that the author and preprint are cited in any reuse.

Altmetrics

Downloads

130

Views

140

Comments

0

Subscription

Notify me about updates to this article or when a peer-reviewed version is published.

Email

Prerpints.org logo

Preprints.org is a free preprint server supported by MDPI in Basel, Switzerland.

Subscribe

© 2025 MDPI (Basel, Switzerland) unless otherwise stated