Marine ecosystems are often formed by the association of multiple foundation species (sensu Dayton, 1972) with a conjunct impact on the physical and biological structure of the environment. This co-occurrence of foundation species is crucial for the creation and stability of habitats, as well as for their productivity and the whole ecosystem functioning, sustaining the ecosystem services (Angelini et al., 2011).

Where foundation species overlap, their interplay may generate positive interspecific interactions with mutual advantages for their stability, supporting the resilience and the resistance of the whole community against external drivers of changes (Angelini et al., 2015; Thomsen et al., 2018). A cordgrass meadow could facilitate the establishment of a mussel bed on the substrate (Altieri et al., 2007), a biogenic reef may kick-start seagrass and algae recovery (Reusch et al., 1994; Newell and Koch, 2004; Lang and Buschbaum, 2010; Guo and Pennings, 2012), whereas a macrophyte coverage may generate suitable abiotic conditions for the establishment of calcifying organisms (Hendriks et al., 2014; Wahl et al., 2018).

Understanding all these processes is crucial to boosting habitat conservation and restoration (Byers et al., 2006). The consideration of interspecific interactions in restoration plans could enhance the potential to recover lost ecological functions, accelerating ecosystem-structuring processes by a multi-habitat approach (e.g., Lang’at et al., 2013; Derksen-Hooijberg et al., 2018). Only recently restoration studies have incorporated the mechanisms of facilitation among species (Halpern et al., 2007; Renzi et al., 2019).

Designated as one of the most relevant biodiversity hotspots worldwide (Meyers et al., 2000), the Mediterranean Sea hosts many different mixed habitats originated by the overlap of multiple foundation species (e.g., gorgonians and erected sponges within the coralligenous outcrops, mussel beds within the P. oceanica meadows, hermatypic corals and other calcifying bioconstructors within forests of erected macroalgae). Among these bioconstructors, gregarious vermetids of the genus Dendropoma Mörch, 1861, in association with the crustose coralline alga (CCA) Neogoniolithon brassica-florida (Harvey), Setchell and Mason (1943) form ecologically important biogenic structures (called vermetid reef) along the central, the south, and the southeastern rocky coasts of the basin. These bioconstructions may co-create a complex three-dimensional framework with canopy-forming macroalgae (mainly belonging to the genus Cystoseira C. Agardh, 1820), which often fringe the seaward rim of the reef (Ingrosso et al., 2018).

The role of the vermetid reef in sustaining high levels of marine biodiversity, coastal processes, and ecosystems is widely recognized, because this bioconstruction magnifies the horizontal extension and three-dimensionality of intertidal rocky platforms, protects the coasts from physical erosion, regulates sediment transport, and is an important carbon sink, with subsidiary benefits also for humans (Chemello and Silenzi, 2011; Colombo et al., 2013; Milazzo et al., 2016; Ape et al., 2018).

The active protection of this habitat and bioengineering species is advocated in European legislation (Bern Convention European Council, 1979; Barcelona Convention Protocol concerning Specially Protected Areas and Biological Diversity in the Mediterranean, SPA/BD, 1995; Council Directive 92/42/EEC; the IUCN Red List of Mediterranean Habitats, Gubbay et al., 2016). However, during the last decade, living vermetid cover has drastically decreased throughout the Mediterranean rocky shores (Badreddine et al., 2019; Rilov et al., 2020; Bisanti et al., 2022). This collapse is hypothesized to be related to the global climate change and to intensive human coastal exploitation, with severe consequences for the bioconstruction maintenance and cascading effects on the whole rocky intertidal ecosystem (Galil, 2013; Rilov et al., 2020; Albano et al., 2021).

Experimental studies suggest that the future Mediterranean climatic scenario (i.e., the rapid increase of the sea surface temperature and extreme climatic events) will adversely affect the reef-builder Dendropoma sp. at different ontogenetic stages (embryos, early recruits, and adults) and the photosynthetic and calcification performance of the associated CCA, leading to the reef decline (Milazzo et al., 2014; Fine et al., 2016; Alessi et al., 2019; Milazzo et al., 2019). At the same time, the ocean CO₂ enrichment should boost the reef-associated macroalgae with non-linear effects on the community (Celis-Plá et al., 2015; Cornwall et al., 2017; Milazzo et al., 2019).

Within this framework, the implementation of active and coordinated efforts for vermetid reef conservation should be an intergovernmental priority. Planning how to face local vermetid decline by successful restoration strategy should also consider biological interactions and the adoption of a multispecies approach (McAfee et al., 2022).

With this regard, canopy-forming macroalgae are known to influence the recruitment of sessile and reef-forming marine invertebrates in multiple ways (e.g., barnacles, Leonard (1999); mussels, Moreno (1995) and Bégin et al. (2004); oysters, Shelamoff et al. (2019) and McAfee et al. (2021)). Macroalgal canopies, indeed, represent valuable biogenic refugia for benthic organisms, especially in highly dynamic environments as the intertidal (Watt and Scrosati, 2013a; Watt and Scrosati, 2013b), allowing abiotic stress amelioration, the alteration of predator–prey interactions (Ware et al., 2019) and increasing the niche availability for the associated biota (Bulleri et al., 2016).

This study aims to assess the effect of canopy-forming algae on the settlement success of the central-Mediterranean vermetid reef-builder Dendropoma cristatum (Biondi 1859) on artificial discs that can be transferred and used to restore other vermetid reefs. We expect that vermetid settlers positively respond to the canopy presence, taking advantage of the macroalgal influence on the surrounding habitat. Furthermore, the influence of the macroalgal canopy on the temperature and understory algal colonization was also examined, to detect eventual features at the vermetid settlement surface that may co-vary with the canopy presence and affect the reef-builder settlement.

In our study, the intertidal macroalgal canopy does not obstruct the vermetid input on the artificial discs and it seems to positively affect the settlement of the considered reef-forming species.

Indeed, Dendropoma cristatum settlers were found on all the artificial substrates employed for the experiment, with increasing abundance in the presence of a coverage of macroalgal canopy, where they resulted 1.70-fold more abundant compared to the uncovered settlement discs. This biological facilitation may be explained by a habitat improvement by the canopy instead of the occurrence of a spatial variability in the vermetid post-larvae supply. Indeed, the experiment was conducted within an area where the D. cristatum adult density was homogeneous, guaranteeing a comparable local output of settlers among the sites where the geopolymer discs were deployed.

Peculiar sub-canopy conditions may regulate the mechanism by which vermetids positively respond to the erect macroalgae presence. In particular, this study highlights a negative control by the canopy on the understory algal colonization on the artificial settlement discs and on the environmental temperature in the proximity of the reef surface where D. cristatum settlement naturally occurs.

Macroalgal canopies are documented to inhibit the understory vegetation by a multiplicity of dynamics (e.g., by reducing the understory light, Connell (2003); by frond abrasion, Irving and Connell (2006); by altering the local hydrodynamic regime, O’Brien and Scheibling (2018)), and the reduction of the understory algal coverage is positively associated with the increase in settlement and recruitment of sessile invertebrates (Bégin et al., 2004; Shelamoff et al., 2019; McAfee and Bishop, 2019; McAfee et al., 2021). Interestingly, a negative association between the understory algal colonization and the vermetid settlement emerged also from our study. On the geopolymer discs, erected algae and turf settled within the same vermetid shelters (with a likely antagonistic role against the vermetid settlement), and their abundance was suppressed by the macroalgal canopy, increasing the availability of uncolonized refuges for the reef-builder attachment. By contrast, the coralline algae encrustation was well-developed also under the macroalgal canopy, where it colonized the disc surface, remaining outside the vermetid burrows.

Furthermore, according to Catalán et al. (2023), the algal assemblage under the canopy seems to be highly homogeneous, being mainly dominated by the encrusting red algae and the epilithic biofilm.

The slightly cooler temperature measured at the settlement surface under the macroalgal canopy is positively associated with the vermetid settlement. Changes in the temperature may significantly affect the survival of organisms living in the intertidal (Somero, 2010), especially if sedentary and sessile as reef-builder vermetids. Furthermore, thermal stress dampening by the macroalgal canopy has been recognized as one of the major benefits for the intertidal biota, generating a more favorable habitat for the community establishment and functioning (Bertness et al., 1999; Leonard, 1999; Coombes et al., 2013; Umanzor et al., 2017; Ørberg et al., 2018; Sarà et al., 2021).

At the reef scale, the temperature has been hypothesized as a factor that may control the settlement of D. cristatum (Franzitta et al., 2016), although a gap of knowledge persists about the thermal sensitivity of this reef-builder over its life cycle. This information would be essential to forecast the consequences of the expected temperature rise on this species and on the reef persistence at the Mediterranean scale.

Differences up to 6°C were revealed among the temperatures registered at the same time across the two habitat types. During the whole experiment, the highest temperature on the bare reef was 2.45°C higher than the highest temperature recorded under the macroalgal canopy. During the diurnal low tides, the canopy coverage reduced the average environmental temperature of 0.32°C and modulated the temperature oscillation when the reef was exposed to the air. This narrow temperature difference among habitat types may plausibly deter the vermetid settlement. A similar temperature variation, indeed, affects the D. cristatum reproductive performance in terms of the size and the number of embryos per egg capsule (Alessi et al., 2019).

The macroalgal canopy might buffer the thermal stress for settling vermetids when the reef is under direct sun irradiance, lowering temperature fluctuations and peaks at the substrate, as in our study. However, this is just an aspect of the influence of canopy-forming algae on microclimatic conditions along the intertidal vermetid reef and additional studies should focus on other near-surface features associated with heat. Extreme desiccation conditions documented along the Sicilian coasts during the summer 2022, due to prolonged reef aerial exposure, are suggested as possible triggers for vermetid mortality (Bisanti et al., 2022). The study of macroalgal canopy as biogenic refugia against these prolonged periods of physiological stress needs a higher concern, weighting the full potential of natural canopy-forming algae to ameliorate the rising climatic stress at the reef-scale.

Further studies on the physiology of the juvenile vermetid snails may clarify if their settlement competence is affected by the environmental temperature, if they undergo higher post-settlement mortality in the hotter environment or if they selectively discriminate among settlement sites, confirming that, in addition to biological cues (e.g., the presence of CCA, Spotorno-Oliveira et al. (2015), and the epilithic biofilm, La Marca et al. (2018)), also physical stress might drive the settlement of reef-builder vermetids.

Although our experiment has been carried out in the field under multiple sources of variability and did not directly test the effect of the temperature on the settlement dynamics of D. cristatum, our results might corroborate the role of the environmental temperature as a limiting factor during the early life stages of different benthic invertebrates and also foundation species (Storch et al., 2011; Webster et al., 2011; Lathlean et al., 2013; Byrne et al., 2017; Huggett et al., 2018; Lang et al., 2023).

The macroalgal canopy may have a control on further abiotic and biotic factors that have not been considered at this step of our research. It is also plausible that it protects the newly settled snails against physical disturbances, contextually enhancing the environmental quality for the reef-builder vermetids in multiple ways (e.g., by shading the substrate and contrasting the development of sediment-entrapping understory turf assemblage, Connell et al. (2014); by reducing the competition with other benthic organisms removed by the mechanical canopy whiplash and benthic sweeping, Beermann et al. (2013) and Shelamoff et al. (2019)). Furthermore, extending the spatial-temporal setup of our investigation may also reveal if the facilitative effect provided by the canopy may depend on the local environmental context or if it is generalizable to other reef areas and if other biological interactions may succeed during the following stages of the vermetid colony development.

From a practical perspective, the use of modular and relatively small substrates (i.e., the geopolymer discs) is instrumental in deploying these artificial settlement units where the environmental context fits the initial step of the vermetid colonization (e.g., close to the macroalgal canopy at their settlement stage), avoiding more expensive and alternative solutions to artificially enhance the early vermetid recruitment. Moreover, the implementation of these rock-like D. cristatum colonized units is central for moving a vermetid group to selected sites and for rebuilding a self-sustaining population of reef-forming organisms, avoiding the transplantation of adults and overcoming the limited dispersal ability of these reef-builder gastropods (Calvo et al., 1998; Galil, 2013).

The efforts for the protection of the co-occurring vermetid reefs and canopy-forming macroalgae may, therefore, represent an opportunity to increase the effectiveness of actions focused on one single habitat, contributing to the conservation of the intertidal ecosystem at a wider scale. This multi-habitat approach (McAfee et al., 2022), moreover, is fundamental to strengthening the framework for the achievement of the UN Decade on Ecosystem Restoration goals (UN Resolution 73/284; Waltham et al., 2020) and is in line with the recent Nature Restoration Law (European Commission, 2022), which aims at implementing national restoration plans through measures that support the connectivity between habitats.

The raw data supporting the conclusions of this article will be made available by the authors, without undue reservation.

The manuscript presents research on animals that do not require ethical approval for their study.

EM, FA, AR, VM, and SM conceived this research; EM wrote the manuscript, with a contribution from AR, VM, and FA. ED provided the technical support for the geopolymer disc production. EM, AR, VM, MS, FA, and MM conducted the fieldwork; EM conducted the laboratory analysis; EM and AR performed the data analysis; AR, VM, FA, and SM contributed to the manuscript revision and discussion. SM provided funds to support the experiment. All authors commented on the first draft of the manuscript. All authors contributed to the article and approved the submitted version.