Spirobranchus tetraceros (Schmarda, 1861), originally described from New South Wales, Australia, was later reported as a widely distributed succesful species of Indo-Pacific origin, including as Lessepsian migrant to the Mediterranean, until evidence has accumulated that the nominal taxon is a large complex of morphologically similar species. Specimens of Spirobranchus cf. tetraceros recently discovered in the Western Mediterranean (Valencia, Spain) morphologically resembled those of S. multicornis from the Red Sea rather than S. tetraceros sensu stricto from Australia. However, genetic studies proved that sequences of the introduced specimens match neither those of the S. tetraceros morphotype from warm temperate Australia (NSW) nor those of S. multicornis from the Red Sea. Subsequently, Kupriyanova et al. (2022) designated a neotype of S. tetraceros from New South Wales supported by DNA sequence data and demonstrated that several species of the S. tetraceros complex exist in Australia alone. This study examined several populations of the S. tetraceros complex world-wide in search of the source population for the Western Mediterranean invader and demonstrated its identity with S. arabicus widely distributed in the Persian (Arabian) Gulf.

non-indigenous species, introduced, species complex, cyt-b, 18S, Red Sea, Persian (Arabian) Gulf, cryptic invasion

Completed in 1869, the Suez Canal connects the Red Sea and the Mediterranean Sea thus joining two biogeographical areas with very different faunas: the Red Sea province of the tropical Indo-West Pacific and the subtropical Levant Basin of the warm-temperate Atlantic Mediterranean (Briggs 1974; Por 1978). These regions have been partially separated since the early Miocene (ca. 20 Ma) and completely separated since the Miocene (13.5 Ma ago) (Harzhauser et al. 2007). Joining these seas by the Suez Canal resulted in a mostly unidirectional faunal migration from the Red Sea to the eastern Mediterranean (Levant Basin) that was termed “Lessepsian migration” (Por 1978). The Red Sea colonizing species thus became “Lessepsian migrants” and the Levant area inhabited by these migrants was termed the “Lessepsian province” (Por 1990). The phenomenon of Lessepsian migration is well documented and numerous Red Sea taxa have established in the Levant Basin (reviewed by Galil 2023).

The hypothesis that a non-indigenous species in the Levant Mediterranean is a Lessepsian migrant is supported when sequential settlement of Indo-West Pacific or Red Sea species in the Levant Basin can be tracked from the source area to the colonized Mediterranean area—including records from within the Suez Canal (Steinitz 1968; Por 1978). An alternative explanation for the presence of a non-native population in the Mediterranean lacking records from the Suez Canal is that it was transported by ships, including ships passing through the Suez Canal (see Zibrowius 1979). Whether a newly found non-indigenous taxon is an expansion of contiguous populations (a Lessepsian migrant sensu Por 1978) or it is derived from a ship-translocated invasive population is not possible to know without population genetics studies. Thus, both Lessepsian migrant step-wise populations and alien ship-translocated populations of the same Indo-West Pacific species may be present in the Levant Basin.

A well-known example of a migrant to the Mediterranean from the Red Sea is the nominal polychaete taxon Spirobranchus tetraceros (Schmarda, 1861) (Serpulidae, Annelida). The first Levant record (Lebanon) of this species dates from 1965 (Laubier 1966). Since that time the taxon has been recognized as the Lessepsian migrant with the most records from within the Suez Canal and the one having the earliest and the widest Levant distributions (Ben-Eliahu 1991; Ben-Eliahu and ten Hove 1992; Ben-Eliahu and ten Hove 2011; Çinar 2013). Around the turn of the century, Ben-Eliahu and Fiege (1996) stated that of all polychaete Lessepsian migrants, only S. tetraceros has reached as far west as Rhodes, Greece. Spirobranchus tetraceros established a foothold in Alexandria Mediterranean waters to the extent that it outcompeted the previously dominant serpulid, Hydroides elegans (Selim et al. 2005). The species was collected in 2016 from Siracusa (Sicily), which led to the suggestion that S. tetraceros is undergoing a westward expansion (Ulman et al. 2017). In the western Mediterranean, the first established population of S. tetraceros was reported by Palero et al. (2020) with specimens collected during 2015–2017 representing the first country record for Spain (Valencia Port).

However, Spirobranchus tetraceros sensu stricto was originally described from warm-temperate New South Wales (NSW), Australia and its reported wide distribution was a result of a taxonomic revisionary study by ten Hove (1970) that lumped 22 nominal Spirobranchus taxa world-wide under the oldest available name. This was done following the cosmopolitan species concept dominant at the time (see Hutchings and Kupriyanova 2018). Moreover, the circum(sub)tropical S. tetraceros, as redefined by ten Hove (1970), had been later recognised as a species complex by ten Hove (1994: 113). This notion was directly supported by the first DNA data in Palero et al. (2020) demonstrating that specimens from the S. tetraceros type locality were ge­netically distinct from the western Mediterranean material. Furthermore, the genetic dis­tance between sequences of the specimens from the Red Sea (Gulf of Eilat) and those of the Mediterranean S. cf. tetraceros were large enough to indicate distinct taxa. Thus, the hypothesis that S. cf. tetraceros is a Red Sea species that passively migrated to the Mediterranean and underwent a westward expansion was not supported by the Palero et al. (2020) results.

Most recently Kupriyanova et al. (2022) designated a neotype of S. tetraceros from NSW supported by DNA sequence data and demonstrated that several species of the S. tetraceros complex are found in Australia alone. The authors also resurrected the name S. multicornis (Grube, 1862) for the Red Sea population of S. cf. tetraceros. While the authors showed that S. tetraceros from Australia is not found either in the Red Sea or the Mediterranean, the identity and origin of the western Mediterranean population remained unknown.

The aim of this study was to determine the origin of the introduced established population of S. cf. tetraceros from the Western Mediterranean reported in Palero et al. (2020). We examined several populations of the S. cf. tetraceros complex world-wide in search of the elusive source population.

The study was based on the material of Spirobranchus cf. tetraceros deposited in the Australian Museum (Sydney) and in the Zoological Museum of the University of Tehran (Iran). We added new DNA sequence data (cyt-b and 18S) of the specimens of S. cf. tetraceros from Western Australia, Hong Kong, and South Korea, as well as S. dendropoma Mörch, 1863 from Curaҫao and S. arabicus Monro, 1937 (recently re-described by Pillai (2009)) from Kuwait and Iran (Fig. 1) to the dataset used by Kupriyanova et al. (2022). Specimens used in the study with registration numbers and collection localities are found in Table 1.

Figure 1. 

Map of collection localities for S. arabicus specimens used in this study: 1 – Valencia, Spain; 2 – Crete, Greece; 3 – Al-Doha, Kuwait (29.316667°N, 47.85°E); 4 – Farur, Iran (26.31126°N, 54.48600°E); 5 – Hengam, Iran (26.63221°N, 55.84954°E); 6 -Tiss, Iran (25.34800°N, 60.59780°E); 7 – Ramin, Iran (25.26472°N, 60.75306°E); 8 – Gwatr, Iran (25.16389°N, 61.50222°E).

This genetic study showed that the mysterious specimens from the Spirobranchus tetraceros complex recently introduced to and established in the Western Mediterranean (Crete, Greece, and Spain) belong to S. arabicus, most likely introduced from the Persian (Arabian) Gulf and Gulf of Oman. Palero et al. (2020) suggested that the Mediterranean specimens examined might belong to a yet undescribed species of the S. tetraceros complex. This is clearly not the case, and we refer to this species as S. arabicus following Pazoki et al. (2023), even though the type locality of the latter species is the coast of Oman (Fig. 1), which lies slightly outside the area sampled in this study. Spirobranchus arabicus is very common throughout the Persian Gulf and Gulf of Oman (Pazoki et al. 2023) and is likely to be distributed throughout the West Indian Ocean biogeographical province sensu Toonen et al. (2016).

While the study resolved the identity and the origin of the recent invader into the Westen Mediterranean, several unanswered questions remain about the identity and origin of the species reported as S. tetraceros from the Levantine Basin of the Mediterranean. The most likely hypothesis for this Lessepsian migrant (sensu Por 1978) reaching the Levant Basin through the Gulf of Suez and Suez Canal would be conspecificity with S. multicornis, previously reported (as S. tetraceros) from the Red Sea (e.g., Perry et al. 2018). However, ecological data suggest that the relationship between S. cf. tetraceros from the Suez Canal and S. multicornis from the Red Sea requires further examination. According to Perry et al. (2018), S. multicornis was found to be exclusively associated with live corals in low abundance in the Gulf of Eilat. However, in the Gulf of Suez and the Suez Canal in Egypt S. cf. tetraceros was reported as a massive fouler, settling on artificial substrate as well as on corals (Selim et al. 2005). Moreover, Selim et al. (2005) reported that “S. tetraceros” had replaced Hydroides elegans, a well-known successful invader (Kupriyanova et al. 2023) as the dominant fouling species in Alexandria Harbour (the Mediterranean). At the time that S. cf. tetraceros had become the most abundant serpulid in the harbour on rocks, concrete, and metal surfaces, H. elegans was still dominant on the fouling plates (Ghobashy and Ghobashy 2005). Spirobranchus arabicus specimens were almost always present on the fouling plates in the Persian Gulf and Gulf of Oman, but never formed tube aggregations (Pazoki unpubl. obs.).

The conflicting ecological evidence suggests that more than one species of the S. tetraceros complex might be present in the Red Sea. While the coral-associated S. multicornis examined by Perry et al. (2018) can be a native species restricted in the Red Sea biogeographical province sensu Toonen et al. (2016), the species that thrives as a fouler in the Suez Canal might have been yet another alien introduced to the Red Sea. Further molecular studies are needed to determine whether the fouling S. cf. tetraceros and S. multicornis from the Red Sea have the same origin.

The results of this study suggest an invasion of S. arabicus to the Western Mediterranean with ship-fouling as vector (see Zibrowius 1979) rather than the previously hypothesized westward extension of the Lessepsian migrant such as S. multicornis from the Red Sea via Suez Canal. Thus, the hypothesis of Ben-Eliahu (1991) that S. tetraceros is a Lessepsian migrant crossing the Suez Canal to the Mediterranean by range extension was not supported by our study. However, it is also possible that several species of the S. tetraceros complex have been introduced to the Levant basin of the Mediterranean, both as Lessepsian migrants as well as transported on ship hulls.

In summary, the results of this study call for both an integrative taxonomic world-wide revision of the Spirobranchus tetraceros complex and a large-scale genetic study of S. cf. tetraceros in the Mediterranean. Such a study would help to monitor the Mediterranean region to detect potential cryptic invasions by the members of the apparently large S. tetraceros complex. This is important because worldwide distributed cryptic invaders are particularly difficult to track as they are typically assumed to either be native species or wrongly assigned to other invasive species (Morais and Reichard 2018). The study also stresses the crucial importance of integrative taxonomic studies for understanding of invasion pathways.

EKK: research conceptualization, funding provision, writing – the original draft, review & editing. GD: investigation and data collection, funding provision, writing – review & editing. SP: sampling design and methodology, investigation and data collection, data analysis and interpretation, writing – review & editing. MAK: research conceptualization, investigation and data collection, writing – review & editing.

This study partially funded by Australian Biological Resources Study (ABRS) grant RG18–21 to EKK and by French Government in the frame of the “Investments for the future” Programme IdEx Bordeaux (ANR-10-IDEX- 03-02) to GD.

We are grateful to Dr Harry ten Hove (Naturalis, Leiden, the Netherlands) for sharing his numerous notes and insights on the Spirobranchus tetraceros complex. We thank Dr Ferran Palero for providing unpublished 18S sequences of the S. cf. tetraceros specimens collected from Valencia, Spain. Dr Vasily Radashevsky (Institute of Marine Biology, Vladivostok, Russia) provided specimens of S. cf. tetraceros that he collected in South Korea and Dr Harry ten Hove provided specimens of S. dendropoma that he collected in Curaҫao. Specimens of S. cf. tetraceros from Hong Kong were collected and provided by Dr James Xie (Hong Kong Baptist University). EKK is grateful to Dr Manal Al-Kandari (Kuwait Institute for Scientific Research) who facilitated her visit to Kuwait. SP thanks Drs Reza Naderloo and Hassan Rahimian (University of Tehran, Iran) for their help in the field. We are thankful to three anonymous reviewers for their comments.