First Record of the Invasive Alien Species Rugulopteryx okamurae (Phaeophyceae, Dictyotales) along the Eastern Coast of Sicily (Italy, Mediterranean Sea): Is It Ready to Expand into the Ionian Sea?

Abstract

The Mediterranean Sea is a hotspot for the introduction of non-indigenous species. Among them, invasive alien species can seriously affect the areas they colonize, not only by altering the marine food webs and community structure, but also by harming certain economic activities, such as fishing, tourism, aquaculture and marine infrastructure. Rugulopteryx okamurae is a brown macroalga considered the fourth most harmful species among the 10 most invasive species reported in the Mediterranean; in fact, it has recently been included in the list of invasive alien species of Union concern due to its serious impact on biodiversity and socioeconomic implications. This species was reported for the first time in the Mediterranean in 2002 in Thau Lagoon (France), introduced by the aquaculture of the Japanese oyster Magallana gigas. Since then, this species has spread in both the Mediterranean and Atlantic Ocean with a strong invasive behavior, particularly along the Strait of Gibraltar. Rugulopteryx okamurae was also recently reported for the first time in Italian waters, in the Gulf of Palermo (Sicily). In this study, we report a record of this species further to the east, in the Ionian Sea, where it has not previously been recorded, and provide possible explanations of the spreading and arrival routes in this area. The rapid expansion of R. okamurae is raising concerns; thus, in order to safeguard native communities, it is crucial to keep monitoring this invasive species so that it is possible to regularly update its distribution and follow up on its spread dynamics in the Mediterranean basin.

1. Introduction

The Mediterranean Sea has been considered a hot spot for the invasion of non-indigenous species (NIS) (synonyms: alien, exotic, non-native, allochthonous and introduced) due to the intense maritime traffic and the communication of two water bodies with different biogeographical natures [1]. Invasive alien species (IAS) are a category of established NIS which have already spread or are spreading, or have demonstrated the ability to spread elsewhere, causing adverse effects within invaded regions [2]. From an economic point of view, IAS are responsible for the reduction of fisheries and losses in aquaculture, tourism and marine infrastructure [3]. Moreover, they can threaten human health [3] and cause serious ecological impacts by modifying the habitat they invade, displacing native species and altering food webs and community structure [4]. For these reasons, species invasions are considered one of the greatest threats to native biodiversity [5].

Seaweeds account for 40% of all the IAS reported in the European Union and thus represent one of the major threats to biodiversity and good ecosystem functioning in coastal habitats [6]. In the list of the 10 most invasive species in the Mediterranean Sea, the first 6 are macroalgae [7]: Caulerpa cylindracea Sonder, Womersleyella setacea (Hollenberg) R.E. Norris, Lophocladia trichoclados (C. Agardh) F. Schmitz, Rugulopteryx okamurae (E.Y. Dawson) I.K. Wang, W.J. Lee & H.S. Kim, Acrothamnion preissii (Sonder) E.M. Wollaston and Caulerpa taxifolia (M. Vahl) C. Agardh. Of these six species, R. okamurae, the fourth in terms of harmfulness, was included in the list of invasive alien species of Union concern (EU N° 1143/2014) due to its serious impact on biodiversity and the socioeconomic implications of its rapid spread and establishment [8].

Rugulopteryx okamurae (urn:lsid:algaebase.org:taxname:91743) is a brown macroalga belonging to the order Dictyotales Bory; it is native to the western Pacific Ocean and distributed in the temperate waters of the Philippines, Taiwan, China, Korea and Japan, where it can be found at a depth of between 0.5 and 15 m [9,10]. This species is characterized by a dichotomously branched thallus with a medulla one cell thick centrally and two to three cells thick near the margins [10,11]. In the Mediterranean Sea, R. okamurae was first recorded in 2002 in Thau Lagoon (France), where it was accidentally introduced into a farm of Japanese oyster Magallana gigas (Thunberg, 1793). From 2002 to 2009, R. okamurae established self-sustaining populations in this lagoon; however, it did so without displaying invasive behaviors [11]. In 2013, this species was spotted for the first time in the open sea at Agde (France) [12]. Subsequently, between 2015 and 2016, the species was reported on both sides of the Mediterranean–Atlantic junction, in Ceuta (the African coast of the Strait of Gibraltar) [13] and Tarifa [14]. Since then, this species has spread both towards the Mediterranean Sea and the Atlantic Ocean, colonizing extensive areas of the Strait of Gibraltar, along the southern regions of Spain [14,15], by going as far as the Bay of Alicante (eastern Spain) [16]. In 2018, it was reported for the first time in Cabo Negro and Tangier (Morocco) [17] and in Marseille (France) [18]. In 2023, R. okamurae also reached Italy, in Palermo (Tyrrhenian Sea, first Italian record) [8] and Bari (Adriatic Sea) [19]. Moreover, this species was also reported in different locations of the Atlantic Ocean, such as the Azores [20], Madeira [21], the Canary Islands [22] and along the southern coast of Portugal [23].

Rugulopteryx okamurae shows a strong invasive behavior in many colonized areas due to its high vegetative proliferation and dispersal, including in adverse environmental conditions [24]. As with many species of the same family, R. okamurae presents a diplobiontic isomorphic life cycle [8]. In the invaded areas, this species is usually present all year round as a sporophyte, and it maintains and establishes new populations through fragmentation, vegetative propagules and/or asexual monospores [10,14,25]. From each propagule of R. okamurae, a new clonal individual can be generated, whether the thallus that produces it is fixed to the substrate or free in the water column [26]. Indeed, this species usually expands as detached thalli which can be dispersed by currents or by human vectors, such as fishing or maritime transport [26], and finally accumulate along the shore or on the sea bottom, forming a new population [27,28].

In the Alborán Sea, R. okamurae was observed from the intertidal zone to a depth of 50 m [14], with a higher density and cover percentage at greater depths [29,30]. In the invaded areas, this species can cover 80–100% of the seabed, causing the disappearance of many native macroalgae and invertebrate species [29]. As an example of this, recently, in a Mediterranean coralligenous habitat, a regression was observed of the gorgonian species Paramuricea clavata (Risso, 1827) and the calcareous seaweed Mesophyllum expansum (Philippi) Cabioch & M.L. Mendoza, concurrently with the expansion of R. okamurae [31]. Beyond the serious impacts to Mediterranean biodiversity, this species is causing huge socioeconomic costs to certain human activities, such as fishing and tourism, with losses of millions of euros across various sectors [26]. Fishing is the economic sector most affected by the invasion of this species, with an economic impact of EUR 0.8 × 10⁶ in nine months [32]. This could be related to the feeding inhibitory substances contained in R. okamurae thalli, which can reduce its palatability and are harmful for many species [17].

Rugulopteryx okamurae has already caused major concerns in Spain and Morocco [8]. For that reason, it is crucial to keep monitoring the expansion of this species in the Mediterranean Sea. In this study, we report a further record of this species in Sicily, in the Ionian Sea, where R. okamurae has not previously been reported, and provide possible explanations of the spreading and arrival routes in this area.

2. Materials and Methods

Two sterile drifting specimens of R. okamurae were collected for the first time on 24 March 2024 during a dive at the “Acque Fredde” site (Acireale, Catania) (37°38′15.7″ N–15°10′52.1″ E) along the Ionian coast of Sicily (Italy) (CAT 2247) (Figure 1). After the first discovery, another sampling activity was performed at the same site, on 23 May 2024. On this occasion, given the difficulty in distinguishing in situ Rugulopteryx okamurae from other similar species, collections of Dictyotaceae were carried out at different depths (3, 7, 9, 18 and 30 m) to investigate the possible depth range of the species at the study site. Depth and temperature (14 °C in March and 17 °C in May) were measured using a Suunto D6i underwater computer. The samples were sorted in the laboratory under a stereoscopic Zeiss microscope. R. okamurae was only found at 30 m depth, where three sterile specimens were collected (CAT 2248).

Morpho-anatomical observations were carried out on living material that was kept moist and dark in a refrigerator for one week. For microscopic observations, some specimens were observed by a Zeiss Axioplan microscope (Göttingen, Germany). Cross sections were made using a razor blade under a stereoscopic Zeiss microscope. Photographs were taken using a Zeiss Axiocam ICc1 digital camera. Underwater photographs were taken with an Olympus TG-6 underwater camera.

The herbarium specimens (CAT 2247; CAT 2248) are kept at the Herbarium of the Department of Biological, Geological and Environmental Science—Plant Biology Section of the University of Catania (CAT). Herbarium abbreviations follow Thiers [33].

3. Results

3.1. Description of the Observed Specimens

Our specimens matched with the description of Rugulopteryx okamurae reported by Hwang et al. [10] for the Pacific specimens and by Verlaque et al. [34] for the Mediterranean ones.

Thalli showed an erect habit up to 8 cm in length (Figure 2A,B), membranous to the touch, with a non-iridescent yellow-brown color in situ. They were characterized by a dichotomous branching, with a distance between each dichotomy of up to 2 cm in length. The second internode below the apex measured 6 mm distally and 3 mm proximally. The margins of the frond were swollen (Figure 2B). From the base, multicellular, uniseriate, hyaline rhizoids protruded (Figure 3A). Some stolon-like segments were also observed. The apical cells (Figure 3B,C) were lens-shaped, which divided transversely to produce a cuneate subapical cell. The subapical portions of the thallus were up to 3 mm in width, while the basal part was up to 1 mm in width. In cross section, both subapical and median portions of the thallus showed a medulla 1 cell thick centrally and 2–4 cells thick near the margins surrounded by a single layer of small cortical cells (Figure 3D,E). The basal part showed four layers of medullary cells and a single layer of cortical cells (Figure 3F). No reproductive structures were observed.

3.2. Habitat and Distribution

Although sampling was performed at different depths, Rugulopteryx okamurae was only found at 30 m depth. The first time, two thalli were found detached on a sandy substrate; the second time, three thalli were observed attached to a rocky substrate (Figure 2A) covered by sand and gravel, below a rock wall. The substrate where these specimens were collected was covered by other Dictyotaceae [e.g., Dictyota dichotoma (Hudson) J.V. Lamouroux, Padina pavonica (Linnaeus) Thivy, Zonaria tournefortii (J. V. Lamouroux) Montagne], Ericaria zosteroides (C. Agardh) Molinari & Guiry, Sargassum furcatum Kützing and Peyssonnelia spp.

Comparing the specimens collected in the two samplings, those collected in May were taller than those collected in March (6 and 8 cm in length, respectively).

4. Discussion

This study reported a further eastward Mediterranean record of the invasive alien species Rugulopteryx okamurae in the Ionian Sea, where this species has not previously been recorded. This is the third report of this species in Italian waters, following those from the Tyrrhenian [8] and Adriatic Sea [19], suggesting an ongoing process of expansion of this species into the central Mediterranean.

As for other Mediterranean and Pacific records [10,34], even in this study, no reproductive structures of this species were observed. Hwang et al. [10] highlighted that it is usually only sporophytes that occur in the field since they seem to fail to undergo meiosis to form gametophytes. Therefore, this species mainly spreads through vegetative propagation in the form of propagules (e.g., proliferous branchlets arising on the thallus surface), which grow to form new plants [10].

Comparing the found specimens, we observed that those collected in May were larger than those collected in March. This could be a result of the difference in seawater temperature, which was 14 °C in March and 17 °C in May. According to Hwang et al. [10], R. okamurae has its maximum growth period when temperatures exceed 15 °C; however, this does not prevent this species from being in a dormant form all year round. This ability to survive in adverse environmental conditions contributes to the high colonization capacity of this species [24]. Moreover, as was also observed in this study, R. okamurae can live and persist detached from the substrate. As confirmation of this, Mateo-Ramírez et al. [28] observed that unattached thalli of this species from the bathyal areas of the Gulf of Cádiz (258–823 m) were alive and healthy, with high Fv/Fm values even after long periods of continuous darkness. Thus, these thalli can be widely dispersed by currents and accumulate on deep sea bottoms. Indeed, R. okamurae has often been reported in many coralligenous habitats, threatening many habitat-forming species, such as Dendrophyllia ramea (Linnaeus, 1758), Parazoanthus axinellae (Schmidt, 1862), Pentapora fascialis (Pallas, 1766), Myriapora truncata (Pallas, 1766) [30], Paramuricea clavata (Risso, 1827) and Mesophyllum expansum (Philippi) Cabioch & M.L. Mendoza [31].

The present finding of R. okamurae could be related to the hydrodynamic regime of the study area, influenced by the tidal currents of the Strait of Messina and the upwelling currents of the Ionian Sea [35], which provide the deeper environments of this site with lower temperatures and make it richer in nutrients. This favors the growth of R. okamurae, which is now likely to compete with other canopy-forming species present in that area (e.g., Ericaria zosteroides, Sargassum furcatum) [36,37]. Although R. okamurae has a tolerance for high temperatures, this species shows a preference for colder waters, having so far shown an invasive behavior especially in the coldest regions of the Mediterranean Sea (e.g., Gulf of Lion, Alborán Sea, Sicily Channel) [38].

According to Bellissimo et al. [8], there are two main explanations for the arrival of R. okamurae in Sicily: transport by currents and/or through anthropogenic activities, such as maritime transport or fishing or recreational activities. Accordingly, even in this case, two main hypotheses can be suggested for the path of arrival of R. okamurae in the Ionian Sea. The first one refers to the most recent report of this species along the coast of Bari (Italy, Southern Adriatic Sea) [19]. One branch of the Atlantic Water (AW) current penetrates the Adriatic Sea and is partly associated with the formation of the Adriatic Deep Water in the southern part of the subbasin, while the remainder of the current continues northwards and mixes with the runoffs of the Po and other rivers. When the AW exits the Adriatic Sea, it continues its path along the southern tip of the Italian peninsula, arriving along the Ionian coast of Sicily [39]. Therefore, it is possible that R. okamurae could have been transported from the previously known population at the coast of Bari to the eastern coast of Sicily by the AW exiting the south Adriatic Sea.

Another potential path of arrival could be linked to the arrival of the thalli of this species mediated by anthropogenic vectors, such as commercial transports and recreational and professional fishing [8,28]. R. okamurae thalli can often remain entangled in trawl nets or hooked into longlines or trammel nets, which frequently clogs the nets [40]. This is most likely the route by which this species arrived in Palermo (northern coast of Sicily, Tyrrhenian Sea). Indeed, in this area, R. okamurae was first found near an important port, which is the destination of fishing activities carried out in other Rugulopteryx-invaded areas of the Mediterranean (e.g., Marseilles) [8]. It is probable that, as in the case of Palermo, R. okamurae could have arrived on the eastern coast of Sicily through anthropogenic vectors since the study area is located near the small port of Santa Tecla (Acireale), which is used for fishing and tourist boats.

On the northern coast of Sicily, according to Bellissimo et al. [8], R. okamurae is at the beginning of its invasion. The area is already negatively affected by anthropogenic pollution, which might somewhat hinder the species’ establishment and further distribution. In relation to the present study, it is not yet possible to assess the invasiveness status of R. okamurae, given the low number of thalli of this alien species found in the study area. Nevertheless, since this species was not present in this area until very recently [37], it is crucial to keep monitoring R. okamurae in this area, as it could represent a future threat for the native canopy-forming species [36]. As has already been observed, R. okamurae is able to thrive in Mediterranean conditions, endangering key ecosystems [30].

5. Conclusions

In the present study, we documented a further eastward record of R. okamurae in the Central Mediterranean, which is considered a gateway for the eastern part of the basin. Due to its strong invasive behavior, this alien species could continue to threaten the native flora and fauna and cause serious economic impacts to other Mediterranean areas. Further observations will therefore be carried out at the studied site and in surrounding areas to monitor its possible expansion into the Ionian Sea. These data are essential for management and mitigation plans of R. okamurae as well as for improving the protection and conservation of native communities, as they make it possible to anticipate the further expansion of this species in the Mediterranean Sea.