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.
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.