Taxonomy

Short description

It is a colonial species, creamy whitish in colour (Figure 2C–D, 3A). It was found growing on net surfaces of bluefin tuna cages, developing short and long lobes with a cloacal opening at tip of each lobe (Figure 2A–D). The colony has a characteristic reticulate pattern. The colony thickness is around 2–3 mm (Figure 3C, D). Spicules embedded into the surface layer of tunic, 10–50 μm (N = 20) in diameter (average: 31.3 μm ± 2.47 SE), with sharply tipped short rays, about 10–20 in visible field (Figure 3B). The thorax and abdomen almost 1 mm long (Figure 4A–C); thorax with six small pointed lobes in the oral syphon and wide atrial aperture on branchial sac; with four rows of stigmata, first row contains eight or nine stigmata per side; thoracic organ could not be observed (Figure 4B). The abdomen with a straight digestive system; containing a spherical-shaped testis with a spiralled sperm duct forming 6–8 turns before passing straight towards atrial aperture (Figure 4C). It has also incubating oocytes with one large and two small eggs (Figure 4D). Larvae placed within the tunic beneath zooids; with six pairs of lateral ampullae and three adhesive papillae (Figure 4E).

Fig. 2. A–B. Nets of bluefin tuna cages, C–D. Didemnum vexillum colonies on nets.

Fig. 3. A. A Didemnum vexillum colony, general view, B. spicules of colonies, C–D. colony vertical section showing main canals. Scale bar: A = 2 mm, B = 55 μm, C = 2 mm, D = 1.7 mm.

Fig. 4. A. Whole zooid, ventro-lateral view, B. thorax, C. abdomen, D. oocytes, E. larva. Scale bar: A = 0.17 mm, B = 120 μm, C = 90 μm, D = 55 μm, E = 215 μm.

Associated fauna

Nets surrounding the bluefin tuna cages were densely covered with the invasive colonial ascidian D. vexillum. This species almost clogged nets opening in some parts, hindering water circulations inside cages. A few species (some algae and actinarians) were observed to be associated with it, but no sessile encrusting invertebrates were observed on nets.

Distribution

Didemnum vexillum is native to Japan (Lambert, Reference Lambert2009). It is spreading in cool temperate areas via human assistance (Kleeman, Reference Kleeman2009). It has become introduced in several regions including New Zealand, the eastern Atlantic (Netherlands, France, Ireland, United Kingdom, Spain), western Mediterranean, and both the west and east coasts of the United States and Canada (Lambert, Reference Lambert2009; Stefaniak et al., Reference Stefaniak, Zhang, Gittenberger, Smith, Holsinger, Lin and Whitlatch2012; Tagliapietra et al., Reference Tagliapietra, Keppel, Sigovini and Lambert2012; Ordóñez et al., Reference Ordóñez, Pascual, Fernández-Tejedor, Pineda, Tagliapietra and Turon2015; McKenzie et al., Reference McKenzie, Reid, Lambert, Matheson, Minchin, Pederson, Brown, Curd, Gollash, Goulletquer, Occhipinti-Ambrogi, Simard and Therriault2017). The present study expands its distributional range to the eastern Mediterranean (Aegean Sea).

Habitat

This species densely colonizes natural and artificial substrates at depths ranging from 1 to 81 m depth (Bullard et al., Reference Bullard, Lambert, Carman, Byrnes, Whitlatch, Ruiz, Miller, Harris, Valentine, Collie, Pederson, McNaught, Cohen, Asch, Dijkstra and Heinonen2007; Lambert, Reference Lambert2009; Carman & Grunden, Reference Carman and Grunden2010). It fouls heavily on aquaculture establishments such as mussel and oyster cages (Lambert, Reference Lambert2009). Its current distribution pattern indicates that it is a temperate species and can tolerate a temperature range between −2 and 28 °C (Bullard et al., Reference Bullard, Lambert, Carman, Byrnes, Whitlatch, Ruiz, Miller, Harris, Valentine, Collie, Pederson, McNaught, Cohen, Asch, Dijkstra and Heinonen2007; Valentine et al., Reference Valentine, Carman, Dijkstra and Blackwood2009; Ordóñez et al., Reference Ordóñez, Pascual, Fernández-Tejedor, Pineda, Tagliapietra and Turon2015). Water temperatures above 8–10 °C are required for colony growth (Kleeman, Reference Kleeman2009). Its occurrence in the Mediterranean Sea suggests its capability to adapt to warmer waters. The maximum thermal limit of this species was known to be 24 °C (Bullard et al., Reference Bullard, Lambert, Carman, Byrnes, Whitlatch, Ruiz, Miller, Harris, Valentine, Collie, Pederson, McNaught, Cohen, Asch, Dijkstra and Heinonen2007), but Ordóñez et al. (Reference Ordóñez, Pascual, Fernández-Tejedor, Pineda, Tagliapietra and Turon2015) proved that it can sustain temperature 28 °C in the Mediterranean Sea. It prefers salinities above 26 psu (Bullard & Whitlatch, Reference Bullard and Whitlatch2009).

In the study area, the surface temperature near the bluefin tuna cage system was 15 °C (December), but it increases to 26 °C in the summer period in the area (Eryilmaz & Yücesoy-Eryilmaz, Reference Eryilmaz and Yücesoy-Eryilmaz2016). It was only found on cage nets only, and there has been no observation at the moment that this species also colonizes natural substrata. It has a vertical distributional pattern on the cage nets which goes down to 35 m depth. It colonizes nets from surface down to 16 m, after that, nets were fouled only by a brown alga species. This vertical distribution might be associated with the thermocline that usually develops around 15–20 m depth in the region in the summer period (Eryilmaz & Yücesoy-Eryilmaz, Reference Eryilmaz and Yücesoy-Eryilmaz2016).

The vector for introduction

The sexual reproduction of the species generates short-lived lecithotrophic tadpole larvae that have a short distance dispersal ability (meters to kilometres) (Fletcher et al., Reference Fletcher, Forrest and Bell2013). Translocation by human activities explains its sudden appearances in distant locations in the world's oceans (Lambert, Reference Lambert2009). Kleeman (Reference Kleeman2009) categorized its dispersal by larval release or fragmentation from adult colonies as natural processes (current and hitchhiking) and human vectors (hull fouling, ballast water/sea chests, fishing and dredging, and aquaculture). Its presence in the Gulf of Maine and France was explained by imports of large quantities of the Pacific oyster [Magallana gigas (Thunberg, 1793)] from Japan and other invaded areas (Dijkstra et al., Reference Dijkstra, Harris and Westerman2007). In the Ebro Delta, it might have been introduced to the area as epifauna with the oyster spat from the French Atlantic coast (Ordóñez et al., Reference Ordóñez, Pascual, Fernández-Tejedor, Pineda, Tagliapietra and Turon2015). Shipping was considered to be a possible vector for its introduction to the other invaded area in the Mediterranean Sea, the Lagoon of Venice (Tagliapietra et al., Reference Tagliapietra, Keppel, Sigovini and Lambert2012).

According to the interview by workers in bluefin tuna farming, this species first appeared in the area in nearly 5 years ago (2018), so its introduction to the area can be explained by three possible means. (1) Bluefin tuna trade is being held between Japan and Türkiye. Possibly due to the tax advantage, the Japanese merchant ship arrives in Malta and anchors there. A Maltese ship sails to Türkiye to convey farm-harvested fish to the Japanese ship. This invasive species may have primarily introduced to Malta by the Japanese ship and secondarily to Türkiye by the Maltese ship. (2) Bluefin tuna specimens breeding in the cage systems in Ildır Bay are fished off the coasts of Cyprus or Malta, and transferred to the area in nets slowly hauled by ships. Although this species has not yet been recorded in either Malta or Cyprus, the invaded areas in the western Mediterranean and Adriatic Sea by this species are close to Malta and colonies attached to nets or ships may have transferred this species to the region. (3) Another possibility is leisure yachting activity. The İzmir Peninsula is one of the favourite destination of yacht tourism. Many leisure yachts from the Mediterranean and other regions sail to Ildır Bay, nearby the bluefin tuna cages are located, and colonies as a part of foulers on hulls of ships might have been translocated to the area. However, workers in sea-bream and sea-bass cage farming in the area told us that this species do not exist on their nets, indicating its local colonization and its introduction via the bluefin tuna transportation. It is unknown at this stage if this species has invaded natural or other artificial substrata (docks, pier, pontoons, etc.) in the area.

Impacts

Didemnum vexillum is an aggressive and rapidly growing colonial ascidian (Bullard et al., Reference Bullard, Lambert, Carman, Byrnes, Whitlatch, Ruiz, Miller, Harris, Valentine, Collie, Pederson, McNaught, Cohen, Asch, Dijkstra and Heinonen2007). It forms dense encrusting mats with lobes in the introduced areas and is capable of changing or modifying habitats. It has a strong competitive ability, commonly overgrowing several sessile species including other ascidians, sponges, macroalgae, cnidarians, bryozoans, mussels, polychaetes, and crustaceans (Bullard et al., Reference Bullard, Lambert, Carman, Byrnes, Whitlatch, Ruiz, Miller, Harris, Valentine, Collie, Pederson, McNaught, Cohen, Asch, Dijkstra and Heinonen2007). It is capable of increasing their sizes 6–11 times in just 15 days (Valentine et al., Reference Valentine, Carman, Blackwood and Heffron2007a). On Georges Bank, off the coast of New England (USA), 50–90% surfaces of area within a 230 km² were covered by this species (Bullard et al., Reference Bullard, Lambert, Carman, Byrnes, Whitlatch, Ruiz, Miller, Harris, Valentine, Collie, Pederson, McNaught, Cohen, Asch, Dijkstra and Heinonen2007). The species smothered marked sized Perna canaliculus (Gmelin, 1791) mussels in New Zealand within 14 days (in summer) (Coutts & Sinner, Reference Coutts and Sinner2004). It clogged syphons and caused condition loss or even death of mussels. Didemnum vexillum does not specifically attach itself to artificial substrata, but also colonizes natural habitats, having dramatic effects on native biota by altering habitat complexity and structure (Mercer et al., Reference Mercer, Whitlatch and Osman2009), and adversely affecting economically important activities such as fishing and aquaculture (Bullard et al., Reference Bullard, Lambert, Carman, Byrnes, Whitlatch, Ruiz, Miller, Harris, Valentine, Collie, Pederson, McNaught, Cohen, Asch, Dijkstra and Heinonen2007; Valentine et al., Reference Valentine, Collie, Reid, Asch, Guida and Blackwood2007b). It poses a major economic threat to the mussel farms located along the northern Adriatic coasts and lagoons (Tagliapietra et al., Reference Tagliapietra, Keppel, Sigovini and Lambert2012).

In the eastern Mediterranean, this species solely occurred on nets of bluefin tuna cages and entirely outcompeted the native fouler, the mussel Mytilus galloprovincialis Lamarck, 1819 (interview with workers in bluefin tuna farming), which was regarded as a previous pest for the farm because of clogging mesh's eye openings. It seems that this species does not have a profound effect on the tuna fish breeding activity, as the breeding period is almost 6 months in the area (caging in June and harvesting in December or January). After harvesting tuna fish, nets are removed from the cage and underwent to cleaning. This species changed the cleaning procedure of nets in the farming. Normally, when mussels are attached, nets go to net washing device for cleaning. However, as the didemnid attaches nets firmly, nets cannot be adequately cleaned up by net washing machines, thus they are laid on the ground in the sun and retain there until they are completely dried out. It then detaches from nets easily and if required nets are subjected to antifouling paintings.