The rapid increase in the arrival of tropical-origin species into the Levant region has dramatically changed local ecosystems. Non-indigenous species are known for their ability to utilize available ecological niches and in some events expand their non-native niche over time. Here, as an example of such expansion, we report on a massive colonization by the non-indigenous solitary ascidian, Microcosmus exasperatus (Heller, 1878), on soft bottoms along the Mediterranean coast of Israel. While this tropical-origin species is well-known for its ability to form dense aggregations on rocky substrates and artificial structures, only limited reports exist from soft-bottom habitats. In September 2022, a massive settlement of M. exasperatus was sighted on the sandy bottom (15–22 m depth) in front of Mikhmoret, Israel. M. exasperatus had settled on miniature “islets” of hard substrates, such as polychaete tubes, shells, or pebbles. By October, the population had reached a peak density, with a mean of 1.8±1.3 individuals m^-2 (±95% confidence interval for the mean). Longshore visual surveys by towed divers revealed similar populations scattered along the central Israeli coast. Monthly compass surveys monitoring the population density, revealed a gradual population decline during late fall and winter, leading to a complete eradication in February 2023, probably due to a severe winter storm. No population was detectable throughout the spring but in August 2023 a few specimens were again detected on the sandy bottom, albeit at densities several orders of magnitude lower than the previous year. It is postulated that the ephemeral colonization of soft-bottom areas serves as “stepping stones” for the species’ dispersal into new habitats, potentially amplifying its invasive potential. Long-term monitoring across a more comprehensive depth range will reveal whether the observed massive colonization was a singular event or a recurring phenomenon that had previously remained unnoticed.

Tunicates, marine bioinvasion, suspension feeding, soft bottom, lessepsian invasion, epifauna

The global dispersion and distribution of non-indigenous species are of worldwide concern. In the Mediterranean Sea, as of the early 2020s, a comprehensive inventory has identified the establishment of over 500 non-indigenous species (Zenetos et al. 2022). Their distribution exhibits a notable concentration in the eastern Mediterranean basin, primarily attributed to the ongoing influx of Indo-Pacific species through the Suez Canal (Por 1978; Koukouras et al. 2010; Tzomos et al. 2012; Galil et al. 2018). Anthropogenic activities, including maritime traffic, canals, and aquaculture, are principal vectors for the introduction and subsequent dispersal of non-indigenous marine species (Minchin et al. 2009). During the dispersal phase, anthropogenic vectors operate together with natural vectors, such as current-driven larval dispersion, the active or passive movement of adult individuals, and the translocation of adult sessile organisms together with the substrate to which they are attached (Johnson and Carlton 1996; Johnson and Padilla 1996; Shefer et al. 2004; Bryan et al. 2012; Præbel et al. 2013; Ivkić et al. 2019).

Ascidians (Chordata, Ascidiacea) are sessile suspension feeders with a global distribution in all marine environments (Shenkar and Swalla 2011). Some species are highly invasive and are able to impact aquaculture facilities (MacNair 2005; Clarke and Therriault 2007), and reduce local biodiversity (Coutts and Sinner 2004). Typically, non-indigenous ascidians initially colonize harbors and marinas, where they thrive on artificial surfaces, possibly due to lower competition for space (Lambert and Lambert 1998; Shenkar and Loya 2009; López-Legentil et al. 2015).

Soft-bottom inhabiting ascidians are well-documented around the globe in low-energy environments (Allen 1953; Macginitie 1955; Sanders 1960; Millar 1962; Dragovich and Kelly 1964; Tatian et al. 1998; Yakovis et al. 2005; Rimondino et al. 2015). Although reports of soft-bottom ascidians and “ascidian bottoms” habitats are common from the western Mediterranean and the Adriatic Sea (Harant and Vernieres 1933; Parenzan 1959; Pérès et al. 1964; Monniot 1965; Turon 1988; El Lakhrach et al. 2012; Ramos-Espla et al. 2013; Arroyo et al. 2021), their occurrence has been scarce and notably less studied in the eastern Mediterranean, where only a few instances have been documented (Voultsiadou et al. 2011). Observations in the Levant basin are also scarce (Stamouli et al. 2022), and we are not aware of any report of “ascidian bottoms” from the exposed Israeli coastal shelf.

In the Anthropocene, with most of the shelf area being routinely trawled, soft-bottom benthic macrofauna communities predominantly comprise infauna, including annelids, crustaceans, mollusks, echinoderms, and other phyla, albeit often in lower abundances (Warwick and Clarke 1993; Olsgard and Somerfield 2000; Labrune et al. 2008). In soft-bottom habitats, the benthos faces challenges such as limited organic resources, continuous sedimentation, and abrasion by loose particles (Bonsdorff et al. 1996; Chou et al. 2004). The structure, spatial distribution, and biomass of these communities are tightly coupled to environmental variables (Saulnier et al. 2019; Foulquier et al. 2020), with anthropogenic and natural disturbances contributing to modifying both the soft-bottom habitats and their macrobenthic populations (Warwick and Clarke 1993; Bourcier 1996; Sparks-McConkey and Watling 2001). In nearshore regions, characterized by elevated wave energy levels relative to deeper areas, the consequential sediment instability leads to reduced levels of both species’ abundance and diversity (Dolbeth et al. 2007; Martins et al. 2013).

Microcosmus exasperatus (Heller, 1878) (Family: Pyuridae) is a solitary ascidian with a global distribution, primarily in tropical and subtropical waters, and is considered non-indigenous to the Mediterranean Sea (Nagar and Shenkar 2016). Turon et al. (2007), revealed a very restricted distribution of this species in the eastern Mediterranean basin, attributed to introductions via the Suez Canal. It was first documented along the Israeli coastline in 2003, both on artificial substrates and in the natural rocky reefs (Shenkar 2008; Shenkar and Loya 2009).

Marine non-indigenous species are often characterized by opportunistic life-history traits alongside a versatile habitat preference (Belmaker et al. 2013; Safriel 2013; Cardeccia et al. 2018). Upon introduction into a new environment, non-indigenous species typically exploit available niches (Givan et al. 2017), which may not completely represent their ecological niche (Strubbe et al. 2015). Certain non-indigenous species may nonetheless manage to expand their realized niche in the new environment over time (Pack et al. 2022; Iseli et al. 2023). The observed colonization of the non-indigenous solitary ascidian, M. exasperatus, on soft-bottom areas along the Mediterranean coast of Israel (Fig. 1), offers an example of such niche expansion. We investigated the distribution of M. exasperatus along the shallow Israeli soft-bottom areas over an annual cycle, and discuss the potential effects of this niche expansion.

Figure 1. 

Microcosmus exasperatus aggregations on the soft bottom in front of Mikhmoret (17 m bottom depth) and settlement substrate: (A) Aggregation of three specimens covered in sand (top view); (B) aggregation of at least six specimens with hydrozoans epibionts (side view); (C) The polychaete A. vesiculosum and its tube, used as settlement substrate for M. exasperatus.

Throughout the course of this study, M. exasperatus settlements were observed in five of the seven locations surveyed (using either compass or towed-diver surveys) along the Israeli coastline: Mikhmoret, Dor-Habonim nature reserve, Gdor nature reserve, Poleg, and Tel-Aviv (see Suppl. material 1: table S1).

Monthly compass surveys revealed maximal mean population densities during the fall season in front of Mikhmoret (1.8 ± 1.3 individuals m^-2, mean ± 95% confidence interval) at a bottom depth of >15 m. A continuous decline in this population was observed throughout the winter, marked by significant reductions following major storm events. Notably, the population had been completely eradicated from the sampling site by January 2023 and no specimens were detected there during the winter and subsequent spring months. In the following late summer (August – September 2023), a small number of specimens was observed at the sampling site, with mean densities close to zero, greatly differing from the high densities of the previous year (Table 1 and Fig. 4).

Figure 4. 

Microcosmus exasperatus population density and significant wave height measurements throughout the sampling period. The boxplots visually convey the distribution of M. exasperatus density, with black dots denoting individual samples and red triangles denoting outliers. The dashed line and filled dots present the monthly maximum significant wave height values. The numbers on top of the boxplots represent the number of belts surveyed each month Wave data courtesy of the Israel Oceanographic and Limnological Research.

The towed-diver surveys revealed that the massive colonization of M. exasperatus was not limited to the Mikhmoret area but, rather, had spread in a patchy manner throughout the survey area, from Tel Aviv in the south to Dor in the north (Figs 5, 6b). Similarly, large-scale surveys confirmed that the seasonal trend in density observed in the compass surveys was also not limited to the Mikhmoret area but, rather, extended to all locations where ascidians had previously been observed (Fig. 6c), peaking during the fall months and subsequently declining throughout the winter until becoming absent from these locations, with no specimens detected during the subsequent spring surveys (data not shown). Towed-diver survey data also reveal that M. exasperatus was exclusively found at depths below 10 meters, with a notably higher presence observed at bottom depths of 17 to 20 meters (Fig. 6a).

Figure 5. 

Spatial distribution of Microcosmus exasperatus settlements along the sandy seabed (see Suppl. material 1: table S2). The red dots denote the presence of M. exasperatus and the green lines represent bathymetry, with each line indicating a depth interval of 10 meters.

Figure 6. 

Spatio-temporal occurrence of Microcosmus exasperatus in the towed-diver surveys (October 2022 – February 2023). (A) Depth, (B) Locations, and (C) Seasons. The Y-axis values are expressed as the fraction of the transect in which M. exasperatus was observed (1 = 100%); Error bars signify a confidence interval of 95%.

In September 2022, massive colonizations by M. exasperatus on sandy bottom areas (15–22 m depth) were observed, extending for at least 65 kilometers along the Israeli coastline. This marks the first report of sandy-bottom colonization of M. exasperatus in the Levant.

Turon et al. (2007) revised the distribution of Microcosmus squamiger (Michaelsen, 1927) and M. exasperatus in the Mediterranean. According to their revision, the first confirmed record of M. exasperatus in the Mediterranean occurred in 1998 in Tunisia (Méliane 2002). Since then, the species has also been reported from Lebanon, Turkey, Israel, Cyprus, and from additional locations in Tunisia (Bitar et al. 2007; Shenkar 2008; El Lakhrach et al. 2012; Ramos-Espla et al. 2013; Gewing et al. 2016). The only previous reports of this species’ settlement on soft bottom were documented in the Gulf of Gabès, Tunisia, using SCUBA and bottom trawling (El Lakhrach et al. 2012; Ramos-Espla et al. 2013) and in Lebanon, where it was found attached to Caulerpa taxifolia (M.Vahl) C.Agardh 1817 (Ramos-Espla A, pers. comm.). It remains uncertain as to whether the massive colonization event reported here from along the Israeli coast is a recent seasonal phenomenon, but it is certainly the first time the species has been observed during fall surveys of the soft bottom in front of Mikhmoret (Israel) that have been conducted since 2007 (Yahel, unpublished data).

Various ascidian species and even different species within the Microcosmus genus have demonstrated the ability to utilize isolated areas of rigid substrate within soft-bottom habitats for settlement (Monniot 1968; Arroyo et al. 2021). However, these prior occurrences have not been perceived as events of niche expansion. M. exasperatus was first recorded along the Israeli coastline in 2003. It was observed both in the natural rocky reefs and on artificial substrates and became quickly established all along the coastline (Shenkar and Loya 2009). The current report of its colonization in soft-bottom habitats constitutes an important niche expansion, 20 years after its first report. This sequence of events may reflect the establishment of the species in Tunisia, initially reported on an artificial substrate in 1998 (Méliane 2002) and subsequently documented on the natural soft bottom of the Gulf of Gabes, 14 years later (El Lakhrach et al. 2012; Ramos-Espala 2013).

The only earlier account we are aware of pertaining M. exasperatus on a soft bottom is that by El Lakhrach et al. (2012) who reported a maximum density of 0.031 individuals m^-2 (313.5 individuals ha^-1) for M. exasperatus in Tunisia, two orders of magnitude lower than the population seasonal peak (1.8 ± 1 individuals m^-2) reported here. This substantial difference led us to characterize the current observation as “massive colonization”. Populations of M. exasperatus on hard substrates in Israel exhibited considerably higher maximum densities than soft-bottom populations (21.5 individuals m^-2; Nagar and Shenkar 2016). Analogous to the hard-bottom population, the density of the soft-bottom population experienced a decline over the winter, but with no significant recovery following improved environmental conditions. The observed collapse of the soft-bottom population suggests that it is not yet firmly established. Although the causes behind the latter’s niche expansion remain unclear, the potential impacts of this expansion should be duly considered.

In July 2023, following a seven-month absence, a new settlement of M. exasperatus was observed on the mooring line at the study site. Subsequently, in August and September 2023, a few specimens were discovered settling on empty shells on the soft bottom in two distinct locations: one within the study site itself and another approximately one kilometer to the south. These subsequent settlement events reinforce the notion that this settlement ability is not a sporadic occurrence but a genuine and previously undocumented feature of M. exasperatus in the invaded area.

M. exasperatus colonization of the sandy bottom in the fall of 2022 resulted in massive populations along the Israeli coastline. The source of the larvae that eventually comprised the documented colonization remains obscure. However, several different habitats with known populations of M. exasperatus are located within a short distance (a few kilometers) from the observed sandy-bottom populations. Those habitats include the natural rocky reef, marinas, ports, and artificial structures (Nagar and Shenkar 2016). It is postulated that, consequently, the propagule pressure of M. exasperatus was particularly high, especially during the fall of 2022, when the population reached the highest densities. The fact that this putative propagule pressure did not translate into new settlements or larger populations in the following year suggests that recruitment is not limited by propagule supply, especially in the soft-bottom habitats. Previous studies have suggested that the closure depth (the maximal depth for wave-induced sediment transport) of the Israeli coastline is between 10 and 15 meters (Golik 1997; Bitan and Zviely 2019). However, even a relatively calm winter such as that in 2022, with only one severe storm (February 2022, H_s > 5 m), seems to have significantly impacted the documented population along the coast, potentially via abrasion and dislodgment by the strong bottom currents.

The ability of M. exasperatus to form massive populations on the sandy bottom reveals a potential dispersal pathway for the species. According to Zhan et al.’s (2015) invasion model for ascidians, M. exasperatus is currently at its spread stage in the Mediterranean Sea. The duration of M. exasperatus pelagic dispersal time is estimated to be around three days, from gamete spawning to larval metamorphosis (Shenkar N, unpublished data). Such a period should enable the larvae to disperse tens of kilometers from their origin, even under moderate near-bottom currents (5–15 cm s^-1). The combination of massive settlement over large swathes of the soft-bottom sediment and the extended planktonic larval stage of M. exasperatus, facilitates the use of soft-bottom habitats as “stepping stones” for its dispersal to new areas, given favorable sea and environmental conditions. Such ability significantly enhances its invasive potential in the Levant basin and can extend its dispersal range to across soft-bottom habitats.

Sediment covers the majority of the ocean floor, establishing the soft bottom as the world’s most extensive marine habitat (Snelgrove 1999). Stamouli et al. (2022) noted that there has been a restricted research effort focused on large invertebrate species inhabiting soft-bottom environments in the southeastern Mediterranean. The current discovery of M. exasperatus populations on the soft bottom along the Israeli coast calls for further studies to determine the presence of ascidians in this less explored habitat, in particular the presence of non-indigenous opportunistic species.

The discovery of the ability of the non-indigenous ascidian M. exasperatus to form aggregations on soft-bottom substrates represents a significant increase in its known invasive potential in the Levant basin of the Mediterranean. This ability provides a “stepping stones” dispersal pathway for similar benthic species, which may be able to exploit miniature “islets” of hard substrate in the expansive soft-bottom environment, and hence significantly increase propagule pressure along the coastline during the reproduction seasons. Despite their status as the largest marine habitat globally, the soft-bottom habitats of the southeastern Mediterranean have been overlooked in the context of ascidian ecology.

It remains unclear as to whether the observed massive colonization of the soft bottom in the Levant was a singular event or is a recurring phenomenon that has gone unnoticed to date. It is also unclear as to what depths this phenomenon extends. The dynamics of the soft-bottom environment nonetheless remain a critical determinant of M. exasperatus population persistence, at least within the studied depth range. Given the extensive nature of the soft-bottom habitat and the inherently patchy distribution of M. exasperatus populations, the combination of towed-diver and compass surveys has enabled the acquisition of detailed data and provided a broader perspective of its population dynamics. Long-term monitoring across a more comprehensive depth range is undoubtedly needed in order to fully answer the still unresolved questions.

DBG, AN, GK, AF, OUH, and GY designed the study and participated in field experiments, data analysis, and manuscript preparation. NS participated in the study design and manuscript preparation.

This work was funded by an ISF grant 249/21 and NSF-BSF grant 2017622 to GY.

We thank Barak Cohen, Saar Ariav, Nir Sherer, Liron Michaeli, Maayan Nieger Rachmilevitz, Gal Bicho, Romy Biran, Noa Flatau, Yoav Sagiv, students of the Ruppin Underwater Research Methods Course for the initial observations and participation in the first surveys; To Mr. Reuben Rosenblat, Mrs. Shira Bone, and the teams of the Ruppin Scientific Diving Center and the Mikhmoret Sailing Club for their immense and professional support in the fieldwork; To Mr. Shahar Malamud, without whom this research could not have been conducted; and to Naomi Paz for her editorial assistance.