Introduction
Marine alien species are a worldwide problem, drastically altering food web structure, native habitats, and biodiversity (IPBES, Reference Díaz, Settele, Brondízio, Ngo, Guèze, Agard, Arneth, Balvanera, Brauman, Butchart, Chan, Garibaldi, Ichii, Liu, Subramanian, Midgley, Miloslavich, Molnár, Obura, Pfaff, Polasky, Purvis, Razzaque, Reyers, Chowdhury, Shin, Visseren-Hamakers, Willis and Zayas2019). The ecological damage they create also causes billions of dollars in economic losses (Cuthbert et al., Reference Cuthbert, Pattison, Taylor, Verbrugge, Diagne, Ahmed, Leroy, Angulo, Briski, Capinha, Catford, Dalu, Essl, Gozlan, Haubrock, Kourantidou, Kramer, Renault, Wasserman and Courchamp2021; Macêdo et al., Reference Macêdo, Haubrock, Klippel, Fernandez, Leroy, Angulo, Carneiro, Musseau, Rocha and Cuthbert2023). The Mediterranean Sea is one of the most invaded ecosystems in the world, and Türkiye is significantly affected by this invasion. Recent studies showed that as of the end of 2020, a total of 539 marine alien species have been recorded on Turkish coasts, constituting approximately 65% of the marine alien species recorded in the Mediterranean (Çinar et al., Reference Çinar, Bilecenoğlu, Yokeş, Öztürk, Taşkin, Bakir, Doğan and Açik2021). Of these, 404 alien species have become established, and the number of alien records continues to increase (Aydın et al., Reference Aydın, Karadurmuş, Karhan and Yokeş2024).
Recent biodiversity surveys in a heavily polluted coastal area in the Sea of Marmara in 2023 revealed the presence of an established population of Atlantic bat star Asterina stellifera (Möbius, Reference Möbius1859). Asterina stellifera is an Atlantic temperate sea star whose native range extends from Cabo Frio (Brazil) to Mar del Plata (Argentina) in the western Atlantic Ocean and from Senegal to Namibia (southwest Africa) in the eastern Atlantic Ocean (Clark and Downey, Reference Clark and Downey1992). It is a non-selective omnivorous predator inhabiting rocky, rubble, sandy, or muddy bottoms in shallow water, from the intertidal down to a depth of 50 m (Farias et al., Reference Farias, Meretta and Cledón2012; Solís-Marín et al., Reference Solís-Marín, Alvarado, Abreu-Pérez, Aguilera, Alió, Bacallado-Aránega, Barraza, Benavides-Serrato, Benítez-Villalobos, Betancourt-Fernández, Borges, Brandt, Brogger, Borrero-Pérez, Buitrón-Sánchez, Campos, Cantera, Clemente, Cohen-Renjifo, Coppard, Costa-Lotufo, Del Valle-garcía, Díaz, Díaz de Vivar, Díaz-Martínez, Durán-González, Epherra, Escolar, Francisco, Freire, García-Arrarás, Gil, Guarderas, Hadel, Hearn, Hernández, Hernández-Delgado, Herrera-Moreno, Herrero-Pérezrul, Hooker, Honey-Escandón, Lodeiros, Luzuriaga, Manso, Martín, Martinez, Martínez, Moro-Abad, Mutschke, Navarro, Neira, Noriega, Palleiro-Nayar, Pérez, Pérez-Ruzafa, Prieto-Rios, Reyes, Rodríguez, Rubilar, Sancho-Mejía, Sangil, Silva, Sonnenholzner, Ventura, Tablado, Tavares, Tiago, Tuya, Williams, Alvarado and FA2013). The present record represents the first known occurrence of this species outside the Atlantic Ocean. It also marks the second record of an alien sea star in the Sea of Marmara, following the report of Asterias rubens (also of Atlantic origin) approximately 30 years ago (Albayrak, Reference Albayrak1996).
Material and methods
The data for Asterina stellifera specimens reported here were obtained during a biodiversity survey as a part of an assessment of the ecological quality of the coast of an oil refinery in the Gulf of Izmit (northeastern Sea of Marmara) on 2–3 November 2023.
In that study, in order to take inventory of common faunal species of the area (covering approximately 3 km long coastal zone), and also to collect data on population sizes, underwater transects (each of approximately 200 m in length) placed parallel to the shore at 4 and 8 m depths were surveyed by SCUBA divers. Along with other fauna, all visible A. stellifera specimens were counted within the transects, and eight of them were collected and preserved in 96% ethanol for morphological and molecular study. Descriptions of the transects in which the species was present are provided in Table 1.
Details of transects in which Asterina stellifera was present
Morphological identification of the species was based on the original description given by Möbius (Reference Möbius1859) and more recent descriptions by Clark and Downey (Reference Clark and Downey1992) and O’Loughlin and Waters (Reference O’Loughlin and Waters2004). Morphological terminology here also follows that of Clark and Downey (Reference Clark and Downey1992) and O’Loughlin and Waters (Reference O’Loughlin and Waters2004). Identity of the species, based on morphology, was confirmed by molecular genetic analysis. The specimens studied herein are preserved in ethanol and deposited in the collection at AMBRD Laboratories (Istanbul, Türkiye).
For genetic analysis, 10 tube feet of a specimen were used. Total DNA was extracted by using the Genomic DNA Isolation Kit (AMBRD, Türkiye) according to user’s manual. Mitochondrial Cytochrome c Oxidase Subunit I (COI) gene was partially amplified by using COIEchinoF (ATAATGATAGGAGGRTTTGG) and COIEchinoR (GCTCGTGTRTCTACRTCCAT) primers. PCR mixture included 10 ng of genomic DNA, 5 μl of 5X PCR Master Mix (AMBRD), augmented with MgCl2 to a final concentration of 2.0 mM, 0.1 μM of each primer, and final volume was 25 μl. PCR steps were as follows: initial denaturation at 95°C for 2 min; 30 cycles of denaturation at 95°C for 30 s; annealing at 50°C for 30 s; extension at 72°C for 1 min. The PCR was completed with a final extension step at 72°C for 5 min. The product was sequenced using COIEchinoF (Macrogen Europe, Netherlands). The sequence is deposited in NCBI GenBank under accession number PV599415.
Phylogenetic analysis was conducted on MEGA X platform (Kumar et al., Reference Kumar, Stecher, Li, Knyaz and Tamura2018). Additional sequences of Asterina spp. obtained from NCBI GenBank were also included for phylogenetic analysis (Table 2). Sequences were aligned automatically and trimmed to minimise missing characters. The final data matrix consisted of 621 bases. The best-fit model of evolution was determined using the Akaike information criterion (Akaike, Reference Akaike1974) implemented in MEGA X. ‘T92+G+I’ was determined to be the best-fit model. Neighbour Joining was tested with 500 bootstrap replicates. Cryptasterina pacifica and Patiria miniata were used as out-group taxa.
Species used in the phylogenetic analysis
a Specimen sequenced in this study.
Results
Systematic account
Class Asteroidea de Blainville, Reference de Blainville and Levrault1830
Order Valvatida Perrier, Reference Perrier1884
Family Asterinidae Gray, Reference Gray1840
Asterina stellifera (Möbius, Reference Möbius1859)
(Figure 1)
Asterina stellifera (Möbius, Reference Möbius1859), live specimen (R = 35 mm), Gulf of Izmit, Sea of Marmara. Abactinal (left) and actinal views. Scale bar: 10 mm (photographs by S.Ü. Karhan).
Asteriscus stellifer Möbius, Reference Möbius1859: 4 [type locality: Brazil]
Asteriscus brasiliensis – Lütken, Reference Lütken1859: 57
Asteriscus marginatus – Hupé, Reference Hupé1857: 100 [nomen nudum]
Asteriscus minutus – Müller and Troschel, Reference Müller and Troschel1842: 41
Enoplopatiria marginata – Verrill, Reference Verrill1913: 480
Enoplopatiria siderea – Verrill, Reference Verrill1913: 480
Patiria stellifer – Fisher, Reference Fisher1919: 410
Material
The Gulf of Izmit, Sea of Marmara, Türkiye (see Table 1 for location descriptions): Transect I, 2 November 2023, 5 specimens observed (1 collected); Transect II, 3 November 2023, 52 specimens observed (3 collected); Transect III, 3 November 2023, 4 specimens observed (1 collected); Transect IV, 3 November 2023, 26 specimens observed (3 collected).
Diagnosis
The following diagnosis is based on the present specimens and descriptions by Clark and Downey (Reference Clark and Downey1992) and O’Loughlin and Waters (Reference O’Loughlin and Waters2004), with some modification.
Depressed, distinctly stellate (R/r = 1.9–2.1, this work), with 5 short, discrete, rather obtuse, distally pointed rays, interradial margin strongly incurved. Size rather large for the genus, up to R = 70 mm (R = 65 mm for the largest specimen in the present collection). Pedicellariae numerous abactinally, with a large, rounded basal piece, predominantly bi-valved, fasciculate.
Extensive abactinal papulate areas of weakly notched or shallow crescent-shaped plates, narrow interradial non-papulate margin of proximally rounded plates; upper rays with variably developed carinal series of plates irregular in arrangement, up to 4 longitudinal series of plates along each side of rays; papular spaces large, secondary plates and papulae numerous, small secondary plates encroach on primary plates; abactinal plates with spinelet-bearing ridges and domes; denuded plates with glassy convexities; abactinal spinelets digitiform to conical, rounded distally; spinelets spaced on plates closely, not in tufts; interradial plates in short series perpendicular to margin; superomarginal and inferomarginal plates in distinct series, covered with abactinal-type spinelets; projecting inferomarginal plates form marginal edge.
Actinal plates in oblique series. Actinal spines per plate (as determined in this work): oral 6–8; suboral 1–4; furrow 3–5 proximally, webbed; subambulacral 1–3; adradial row of actinal plates with a complete series of spines; actinal interradial predominantly 2–3 in mid-interradius; interradial actinal spines digitiform to conical.
Interradial margin supported by internal contiguous projections of abactinal and actinal plates; superambulacral and superactinal plates absent.
Colour (live)
Abactinal surface greyish or greenish-cream mottled with light and dark olive-green, more heavily around the disc and on proximal upper rays; actinal surface cream, sometimes with a light green tinge on distal interradii.
Genetic analysis
COI sequence of the analysed specimen showed 99.36% and 99.03% identities with Asterina stellifera sequences from Uruguay and Brazil, respectively (Figure 2). Phylogenetic analysis revealed that the COI sequence is useful in determining Asterina species without any doubt.
Neighbour Joining tree obtained by mitochondrial COI gene sequences of the sample from this study (framed in red) and sequences deposited in the NCBI GenBank. Branch support values above 50% obtained after 500 bootstrap replicates are indicated. The scale bar is expected to change per site.
Discussion
To date, 129 alien species have been recorded in the Sea of Marmara (Aydın et al., Reference Aydın, Karadurmuş, Karhan and Yokeş2024; Çinar et al., Reference Çinar, Bilecenoğlu, Yokeş, Öztürk, Taşkin, Bakir, Doğan and Açik2021; Taşkın, Reference Taşkın, Işinibilir, AE and Malej2024; Taşkın et al., Reference Taşkın, Evcen and Bilgiç2023). Approximately 21% of these species are of Atlantic origin, and 6 species are estimated to have come from the Western Atlantic. The origin of 24% of the species has not yet been determined (Çinar et al., Reference Çinar, Bilecenoğlu, Yokeş, Öztürk, Taşkin, Bakir, Doğan and Açik2021). Most of the alien species detected on the Mediterranean coasts of Türkiye originate from the Red Sea and entered the Mediterranean via the Suez Canal, whereas the vast majority (71%) of the alien species in the Sea of Marmara were introduced by shipping. Although Asterina stellifera is mostly distributed along the coasts of South America, it is also known to be found on the coasts of West Africa (Clark and Downey, Reference Clark and Downey1992). Given that the Gulf of Izmit is one of the busiest hubs in international maritime trade, visited by approximately 12,000–15,000 vessels annually (Eyüboğlu and Eyüboğlu, Reference Eyüboğlu and Eyüboğlu2020), and considering the known introduction pathways of alien species to the Sea of Marmara, it is highly likely that the A. stellifera population found in the Gulf of Izmit was introduced via shipping. Furthermore, the high similarity of the COI sequence obtained from the individual sampled in the Gulf of Izmit with sequences from South American samples strongly suggests that this population is of South American origin.
Studies on Asterina stellifera have shown that the population of the species on the coasts of South America has decreased to the point of being listed as endangered (Calil et al., Reference Calil, da Rocha, Freire and Roper2009). It is thought that habitat loss and pollution due to industrialisation, agriculture, and tourism have reduced biodiversity and therefore the A. stellifera population has been negatively affected (Albano et al., Reference Albano, Lana, Bremec, Elias, Martins, Venturini, Muňiz, Rivero, Vallarino and Obenat2013; Farias et al., Reference Farias, Meretta and Cledón2012). In addition, the invasive alien seaweed Undaria pinnatifida, which is widespread in the region, covers the feeding areas of A. stellifera, and the diet of the invasive alien sea slug Pleurobranchaea maculata overlaps with that of A. stellifera, creating pressure on A. stellifera populations (Casas et al., Reference Casas, Scrosati and Piriz2004; Farias et al., Reference Farias, Meretta and Cledón2012, Reference Farias, Obenat and Goya2015; Meretta et al., Reference Meretta, Matula and Casas2012, Reference Meretta, Rubilar, Cledon and Ventura2014).
Our finding of 87 specimens in four different 200-meter transects along approximately a 3-km stretch of coast (see ‘Material’ section in the Results) suggests that Asterina stellifera has adapted well to its new environment and established a population in the Gulf of Izmit, one of the most industrialised and polluted areas of the Turkish coast (Eyüboğlu and Eyüboğlu, Reference Eyüboğlu and Eyüboğlu2020). Another sea star species that invaded the Sea of Marmara, Asterias rubens, competed with the native sea star species Marthasterias glacialis and caused great devastation on the native Mediterranean mussel Mytilus galloprovincialis populations (Çinar et al., Reference Çinar, Bilecenoğlu, Yokeş and Güçlüsoy2023; Yilmaz and Sadler, Reference Yilmaz, Sadler, Toker and Turan2001), resulting in both ecological and economic impacts. Just as Asterias rubens did in the past, the possibility of Asterina stellifera invading this sea in the future should not be ruled out. Therefore, research on the effects of this recently introduced A. stellifera on the native ecosystem is urgently needed.
Acknowledgements
We are grateful to Ziya Çaylarbaşı for his great help in the fieldwork. We also thank our colleagues in the Institute of Environmental Sciences, Boğaziçi University, for their institutional support.
Author contributions
S.Ü.K. performed specimen collection and morphological examination. M.B.Y. performed molecular analyses. Both authors equally participated in the preparation of the manuscript.
Funding
This work was partially funded by Turkish Petroleum Refineries Corporation (TÜPRAŞ).
Competing interests
The authors declare none.
Data availability
The authors confirm that the data supporting the findings of this study are available within the article. The COI sequence generated is available through the GenBank database. Additional information is available from the authors upon reasonable request.
Ethical standards
Not applicable.
