Possible Interactions between Invasive Caulerpa Taxa and Native Macrozoobenthos: The Case Study of Favignana Island

Abstract

Biological invasions are widely recognized as a major threat to native biodiversity, ecosystem functioning and services. Amongst the NIS recorded in the Mediterranean Sea, Chlorophyta species belonging to the genus Caulerpa (Caulerpa cylindracea, C. taxifolia and C. taxifolia var. distichophylla) have raised serious concerns due to their potential or ascertained impact on native benthic communities. During surveys carried out to monitor the occurrence and the coverage of Caulerpa species along the coasts of Favignana Island (Egadi Islands Marine Protected Area), we observed variations in C. cylindracea and C. taxifolia coverage and also some large invertebrates overgrown with thalli of both species.

Non-indigenous species (NIS) are widely recognized as one of the main drivers of global change, threatening native biodiversity, ecosystem functioning and services. Under favorable conditions, NIS may become invasive (Invasive Alien Species “IAS”), causing significant environmental impacts, such as biodiversity loss and ecosystem services degradation. The Mediterranean Sea is particularly vulnerable to NIS introduction [1,2], and in recent decades, there has been a rapid increase (estimated to be eight species per year for the whole Mediterranean basin) of NIS with an expansion of tropical and sub-tropical species. The Sicilian islands (the Central Mediterranean Sea, Italy) and all the Marine Protected Areas (MPAs) they host are notably prone to marine biological invasions, due to their strategic position at the crossroads between the South Western and Eastern Mediterranean Sea, by virtue of the intense maritime traffic skirting the region and Lessepsian migrations [3,4,5,6,7,8].

Amongst the NIS recorded in the Mediterranean Sea, Chlorophyta species belonging to the Caulerpa genus (Caulerpa cylindracea Sonder, Caulerpa taxifolia (M. Vahl) C. Agardh and Caulerpa taxifolia var. distichophylla (Sonder) Verlaque, Huisman and Procaccini), which have raised serious concerns due to their potential or ascertained impact on native communities, are actually considered IAS [8,9,10].

Since 2014, surveys have been regularly carried out in the Egadi Islands MPA to monitor the occurrence and the coverage of green algae belonging to the Caulerpa genus [11,12]. The Egadi Islands MPA is the largest Italian MPA, comprising three main islands: Favignana, Marettimo, and Levanzo. The surveys, carried out within the projects Caulerpa cylindracea—Egadi Islands and Aliens in the Sea, showed a wide distribution of C. cylindracea along the coasts of the MPA. In all probability, anchorage activities, and in general maritime traffic, represent an important pathway for the spread of C. cylindracea within the MPA.

On the contrary, the presence of C. taxifolia was punctiform, being recorded only at Bue Marino, Cala Fumere, Praia, Punta Marsala, and Arrè Turino till 2018 ([13,14], authors’ observations). In 2019, the presence of C. taxifolia was observed for the first time at the entrance of Cala San Nicola (37.93012 N, 12.32585 E) (Figure 1).

This site presents a sandy bottom inhabited in the central part by a Posidonia oceanica (L.) Delile meadow. The coast is characterized by sand, calcarenite and a vermetid reef, a bioconstruction built up mainly by the gastropod mollusc Dendropoma cristatum (Biondi, 1859) (Vermetidae) in association with some coralline algae such as Neogoniolithon brassica-florida (Harvey) Setchell et Mason. In August 2021 a survey was carried out within the Cala San Nicola to monitor the distribution of both species, C. cylindracea and C. taxifolia (Figure 2).

Caulerpa cylindracea was observed near the coast, and a decrease in coverage (from values over 50% to a value of about 20%) with respect to previous observations was highlighted [11]. Instead, a significant increase in C. taxifolia (whose patches reached a coverage of about 50%) was registered. The patches of C. taxifolia covered 30% of the rhizomes of P. oceanica, and for the remaining 20%, there was a mixed bottom (sand–rock). Surveys carried out in July 2023 highlighted a further reduction in the coverage of C. cylindracea (from 20% to 5%), which also showed very short thalli (about 2 cm high), together with a consistent reduction in C. taxifolia (from 50% to 5–10%). Many vertebrate and invertebrate species are reported to feed on C. cylindracea, for instance, Oxynoe olivacea (Rafinesque, 1814), Paracentrotus lividus (Lamarck, 1816), Holothuria (Roweothuria) poli Delle Chiaje, 1824, Sarpa salpa (Linnaeus, 1758) and Diplodus sargus (Linnaeus, 1758) [15,16]. It is well known that feeding on C. cylindracea may have negative effects as a consequence of the caulerpin it contains [15,16,17,18]. However, C. cylindracea exhibits great spread and regeneration abilities that allow it to tolerate a wide range of grazing intensities. Indeed, it can easily recover by regenerating from detached fragments of stolons and fronds [19,20].

During the surveys, we also observed several individuals of Holothuria (Holothuria) tubulosa Gmelin, 1791 and only one individual of Holothuria (Roweothuria) poli overgrown with a few thalli of C. cylindracea and C. taxifolia (August 2021, San Nicola, Figure 3 and Figure 4). Both of these holothurians are common and widespread in the coastal areas of the Mediterranean Sea [16], are “continuous” deposit-feeders that can ingest and rework large amounts of sediment, and can have a role in the recycling of seagrass detritus in P. oceanica meadows [21,22].

This finding would suggest a possible interaction for the purposes of camouflage, i.e., animals are hidden by decorating themselves with parts of organisms, some of which being algae [23]. This strategy, costly in terms of time and energy, is well known for Decapoda (Crustacea) and Echinodermata to avoid their predators. Indeed, we also observed individuals of the crab Maja crispata (Risso, 1827) overgrown with C. cylindracea (San Giuseppe, 2017; Figure 4) and individuals of the echinoderm Sphaerechinus granularis (Lamarck, 1816) covered by a few thalli of C. cylindracea (Figure 5).

Decoration in majid species is well known; some of them showed a preference for macroalgae and also opportunistic behavior by using what is available at the site [24]. Since Caulerpa taxa contain toxic substances which discourage predators, we hypothesize that a passive mutualistic interaction may be established between Caulerpa taxa and their hosts. In particular, it is possible that the host uses Caulerpa both as camouflage and as a deterrent for predators, while Caulerpa uses the host as a pathway of secondary spread to invade new areas inhabited by both native macroalgal communities and P. oceanica meadows.

However, selectivity in camouflage has been demonstrated, suggesting that decoration behavior is a more complex process than is generally recognized. Animals that cover themselves with natural substrates can increase their protection by selecting items that are defended against larger omnivorous consumers [25]. McLay (2020) also proposed the hypothesis of the evolution of masking, from passive to active camouflage [26].

Moreover, it is known that some crabs also use organisms decorating their body as a food store, whose ingestion rate is highest when they are deprived of other sources of food [27]. These observations highlight the need for regular monitoring activity on NIS, particularly in MPAs, to have accurate and regularly updated information on their current distribution, spread dynamics and strategies, abundance, and pathways of introduction. In this respect, Citizen Science activities could significantly improve the efficacy of monitoring plans.