In recent years, seascape ecology rapidly developed as the marine-centric counterpart of the landscape ecology (Turner, 1989; Ray, 1991; Wedding et al., 2011; Bell and Furman, 2017; Pittman et al., 2018), emerging as a new and interdisciplinary science for marine sustainability studies (Pittman et al., 2021). Its applications allow for the exploration of the multi-scale linkages between ecological structure, function, and change in marine environments using a spatially explicit and quantitative approach, with potential to inform management and conservation practices (Pittman et al., 2021). As in the case of the landscape ecology, main focuses are the study of seascape composition (i.e., what and how much is present of each habitat or cover type) and configuration (i.e., the spatial structure or the arrangement of the spatial elements). Changes in configuration are expected to cause changes in ecological functions (Turner, 1989; Turner and Gardner, 2015), hence the importance to assess the relationships between spatial patterns and ecological processes and/or services occurring in the seascape. To do so, seascape ecology has inherited numerous metrics designed to quantify spatial properties in landscapes and analyze spatial patterns (O’Neill et al., 1988; McGarigal, 2002; Cushman et al., 2008; Turner and Gardner, 2015). Their application has proven useful also in the marine realm (Boström et al., 2011; Wedding et al., 2011), especially in coastal seascape research (Bell and Furman, 2017).

So far, the research interest of seascape ecologists has mainly focused on benthic seascapes (Zajac et al., 2000; Brown et al., 2011; Proudfoot et al., 2020), with a number of applications in nearshore and shallow water areas (Pittman et al., 2004; Boström et al., 2011). The attention to coastal seascapes gained momentum along with the research on coastal and marine ecosystem services, which in most cases are provided and therefore more appropriately evaluated and managed at the entire seascape scale (Barbier, 2012; Barbier, 2017). Coastal seascape ecology has been investigating several subtidal and intertidal biogenic habitats across different spatial scales (Robbins and Bell, 1994; Garrabou et al., 1998; Fonseca et al., 2002; Boström et al., 2011; Pittman and Brown, 2011; Furman et al., 2015; Parnell, 2015; Staveley et al., 2017). Among these, marine bioconstructions are of peculiar interest as they modify the biophysical properties of the seascape through their long-lasting and three-dimensional structures that serve as a secondary substrate for the colonization by other marine organisms (Ingrosso et al., 2018). It could be expected that the higher the complexity, size, and stability of these formations, the greater the positive effects on species number and diversity (McCoy and Bell, 1991; Sebens, 1991). Complexity can be defined as “the absolute abundance (per unit area or per unit volume) of individual structural components” for a certain scale of investigation (McCoy and Bell, 1991) and is an important feature of seascape configuration. As such, complexity assessments are used in both two- and three-dimensional seascape analyses. In the case of marine bioconstructions, shape complexity is most commonly investigated relatively to their three-dimensional structure (Burns et al., 2019; Price et al., 2019; Pascoe et al., 2021; Ventura et al., 2021; Carlot et al., 2023), which influences the heterogeneity and therefore the number of microhabitats provided. Irregularities such as holes and crevices provide surfaces with different microclimatic conditions (e.g., humidity, light exposure) and/or shelter from predators compared to the surrounding environment, influencing the number of species that can coexist and resulting in characteristic assemblages of species.

In the Mediterranean Sea, seascape ecology studies on biogenic habitats focused mainly on seagrass meadows (Gatti et al., 2012; Pagès et al., 2014; Pace et al., 2017; Abadie et al., 2018; Rodil et al., 2021) and coralligenous formations (Garrabou et al., 1998; Bracchi et al., 2017; Sini et al., 2019) with many other marine habitats yet to be explored. It is the case of the vermetid reefs, a carbonatic bioconstruction built by the synergistic activity of the encrusting red alga Neogoniolithon brassica-florida and gregarious gastropods belonging to the genus Dendropoma (Safriel, 1966), namely D. cristatum, D. anguliferum, D. lebeche (Templado et al., 2015), and an undescribed one in the Ionian Sea (Calvo et al., 2009). These formed a cryptic complex of species (Templado et al., 2015) under the name of Dendropoma petraeum, which was recently disentangled by Templado et al. (2015).

Vermetid reefs are found at the tide level in rocky shores and can have different morphologies, from simple and thin crusts to broad platforms expanding seawards (Laborel, 1987; Antonioli et al., 1999). Other shapes can result from differential erosive processes, such as the mushroom-like pillars, micro-atolls, and islands (Safriel, 1966; Antonioli et al., 1999). Platforms represent the most complex among the vermetid reef structures (Milazzo et al., 2016), on which the characteristic outer reef, inner edge, and cuvette can be identified ( Figure 1 ). The outer reef is the biologically active part of the reef, dense with living Dendropoma individuals. It grows upwards and seawards as a crevices-rich and complex structure, often exceeding 50 cm of thickness (Chemello and Silenzi, 2011). The inner edge is a small Dendropoma encrustation that can be found at the boundary between the platform and the rocky shore, acting as a superior delimiter of the reef. Compared to its outer counterpart, the inner edge is thinner, mostly vertically developed, and with less dense Dendropoma abundances. Enclosed by the two margins is the zone of the cuvettes, shallow depressions no deeper than 50 cm that form small pools in low tide and calm water conditions (Molinier and Picard, 1953).

Considering the structural features of the vermetid reefs, a coastal seascape in which they are densely present is supposed to have higher structural complexity and heterogeneity levels compared to seascapes in which they are absent. With their three-dimensional and seaward-expanding structure, vermetid reefs support high biodiversity levels (Safriel and Ben-Eliahu, 1991), providing additional space and microhabitats, reduction of physical disturbances, refuge from predation, and a nursery habitat for many benthic and fish assemblages (Goren and Galil, 2001; Chemello and Silenzi, 2011). In addition to benefitting marine biodiversity, the presence of the vermetid reefs in the coastal seascape provides many valuable ecosystem services such as coastal protection, carbon sequestration, and sediment transport regulation (Milazzo et al., 2016).

Despite such ecological importance to Mediterranean coastal seascapes, vermetid reefs are a poorly known and neglected habitat (Picone et al., 2022), whose persistence is at risk. Threatened by a high anthropogenic pressure and the global climate change, local declines and even local losses have been observed and reported in the eastern and central areas of the Mediterranean Sea (Galil, 2013; Badreddine et al., 2019; Bisanti et al., 2022). Ocean warming and acidification negatively impact early life stages of D. cristatum, thus impairing the building of new reef surface (Alessi et al., 2019). In addition, considering the slow growth rate of Dendropoma, sea level rise is likely one of the most threatening pressures to these bioconstructions (Milazzo et al., 2016). The projected sea level rise under future emissions scenarios (Cooley et al., 2022) would likely lead to the submergence of the reefs, entailing the loss of their structures and key functions in the intertidal zone, with detrimental effects on biodiversity as well as ecosystem services provided. The non-living structures of the submerged reefs would likely continue playing a role in supporting biodiversity in deeper waters, but their original contribution to the structural complexity of the seascape as well as their unique ecological role would be lost.

To our knowledge, no study so far has characterized a coastal seascape with vermetid reefs (hereafter “vermetid reefscape”) through the landscape ecology lens. Such approach would provide new insights on the structural properties of the vermetid reefs and set a reference baseline for future studies. In this paper, we provide a first characterization of a vermetid reefscape using landscape ecology metrics, and quantitatively assess the degree of its contribution to the structural complexity of the coastal seascape.

Among the three classes in the seascape, the outer reef was the one with the highest total edge value (5,785.6 m) and, at the same time, the lowest class area (1,040 m²). Excluding the sea class, the outer reef accounted for only 3.9% of the total seascape. Opposite are the results of the edge-area metrics for the coast class, which had the lowest total edge (2,248.6), but the highest area (23,710 m²), representing 89.3% of the seascape. The platform class was, therefore, the second highest class in terms of both total edge (3,511.8 m) and area (1,803 m², 6.8%). Accordingly, the highest edge density value was reached by the outer reef (0.12 m/m²), followed by the platform (0.07 m/m²) and the coast (0.05 m/m²) classes ( Table 3 ). In line with these results, the value of the area-weighted perimeter-area ratio for the outer reef class was the highest (55,618), almost three times the platform value (19,544), and more than thirty times compared to the coast (1,479). Aggregation metrics showed the outer reef as the patchiest (NP = 679; PD = 14,193) as well as the most fragmented (i.e., reduced area and smaller patches) class in the seascape (SPLIT = 208,449), followed again by the platform (NP = 103; PD = 2,153; SPLIT = 9,615) and the coast (NP = 7; PD = 146; SPLIT = 4.1). Finally, the same pattern occurred in the case of the landscape shape index, which identified the outer reef as the most geometrically complex among the classes in the seascape (LSI = 44.8), followed by the platform, and the coast ( Table 3 ). The analysis at the landscape level revealed the reef coast seascape (RC) to have higher values than the no-reef coast (NRC) in all the area-edge, shape, and aggregation metrics applied ( Table 3 ). The natural logarithm ratios of the metrics selected for the comparison of the RC and NRC seascapes were all positive, ranging from 0.1 (CA) to 0.87 (ED) ( Figure 5 ). In particular, compared to the NRC scenario, the RC seascape had 12% more coastal area, while the edge density, area-weighted perimeter-area ratio, and landscape shape index were 139%, 90%, and 66% higher, respectively. The Wilcoxon signed rank test revealed a statistically significant effect of the vermetid reefs presence on the coastal total edge (z = 3.9, p < 0.005), with a large effect size (r = 0.74). Total edge values in the RC seascape were significantly higher than in the NRC scenario, with the median score for the RC seascape being 21.9 compared to 8.5 for the same seascape without the vermetid reefs ( Figure 6 ).

The use of a UAV remote sensing sampling technique proved a useful tool to investigate the vermetid reefs from a structural perspective, as in the case of other drone-based applications to marine and coastal habitats, including bioconstructions (Collin et al., 2018; Ventura et al., 2018; Jackson-Bué et al., 2021; Tait et al., 2021; Brunier et al., 2022). Such approaches play an increasingly important role not only in detecting and monitoring changes in and impacts to marine and coastal bioconstructions, especially in the face of the threats posed by climate change, but offer also efficient tools to assess the degree to which such impacts affect the generation of many ecosystem services depending on the structural properties of the biogenic formations.

The methodology used in this study allowed a cost-efficient acquisition of high-resolution spatial data, suitable for the analysis of the role played by the vermetid reefs in modifying the structure of the coastal seascape. The visual identification and manual digitization of the seascape classes resulted in a low-cost and time saving method for the classification of a small-scale seascape characterized by a low number of visually discernible classes. If future studies were to be conducted, for instance, on the algal communities living on the vermetid reefs, different techniques would have to be implemented (e.g., Tait et al., 2021). Spectral information and classification algorithms (e.g., support vector machines (SVM), maximum likelihood) would be required to accurately and efficiently perform image classification, especially in the case of highly diverse seascapes with higher number of classes. These automated approaches would require specific training procedures to reach high levels of accuracy, potentially presenting limitations in their applications in the case of an environment characterized by spectral complexity (Brunier et al., 2022).

The analysis of the vermetid reefscape at the class level showed a clear pattern of increasing edge density, perimeter-area ratio of patches, and patchiness from the coast seaward. These features underpin a higher structural complexity of the vermetid reefs and its two constituting classes, the platform and the outer reef. The latter in particular accounts for only about 4% of the seascape surface, which makes it the least represented class, and is configured as a discontinuous, fragmented, and thin stripe between the platform and the sea. Compared to the platform, the outer edge has a six times higher patch density and a more than twenty times higher splitting index, a metric whose value increases as the class area decreases and is subdivided into smaller patches. The disaggregation of the outer reef was also captured by the high value of the landscape shape index that, together with the area-weighted perimeter-area ratio, indicated the outer reef as the most geometrically complex class overall.

The fragmented nature of the outer reef is a peculiar feature of this class of the vermetid reefscape, whose scattered structure results from the interaction of different factors such as hydrodynamics, type of rocky substrate, and reef growth (Safriel, 1966; Antonioli et al., 1999). Anthropogenic stressors acting on this already but naturally fragmented class could have severe impacts on it, drastically lowering the overall complexity and heterogeneity of the vermetid reef. The high perimeter-area ratio makes this class more exposed to potential threats negatively affecting the vitality of the Dendropoma individuals. Such scenario would be particularly concerning considering the functional role the outer reef plays in building new reef surface and maintaining the whole bioconstruction alive and expanding. An erosion rate not compensated by a sufficient growth of the outer reef would ultimately lead to the collapse of the entire structure as already reported for the Eastern Mediterranean (Galil, 2013).

The outcomes of the analysis performed at the landscape level were consistent to the ones at the class level, showing overall the same patterns. The presence of the bioconstruction in the RC seascape resulted in a longer coastal edge, a more complex geometric shape, and a patchier configuration of the seascape compared to the NRC scenario in which the vermetid reefs are absent. In the RC seascape, the total edge length was more than doubled compared to the NRC scenario, going from 2.3 to 5.4 km, with an increase in coastal area of about only 11%. The role played by the vermetid reefs in increasing the two-dimensional structural complexity of the seascape stems from their high total edge value per unit area, which positively affects metrics based on a length-area ratio such as perimeter-area ratio, edge density, and landscape shape index.

The comparison of the two seascape scenarios through the logarithmic ratios produced positive values indeed, providing a measure of the degree to which the vermetid reefs contribute to the overall structural complexity of the coastal seascape. The logarithmic responses of edge density, perimeter to area ratio, and landscape shape index were from five to almost nine times higher compared to the area increase. These results once again stress the important role played by the vermetid reef formation in shaping the coastal structure, pointing to features other than just the surface of the reef. The additional area provided by the platform in the intertidal zone is indeed pivotal for the ecological role played by the vermetid reefs, offering a diversified substrate made of crests and cuvettes with peculiar microhabitats, which allow the settlement of specific reef communities and the support of high biodiversity levels. Even though the link between platform area and the harboured biodiversity is acknowledged in the literature as the main emergent outcome of the presence of the vermetid reefs, our results showed that the additional area is not their main contribution to the coastal seascape structure. The relatively low coastal area increase (0.1 times) in the RC seascape entailed a 1.4-fold higher coastal total edge, resulting in a seascape characterized by a higher edge density value ( Figure 6 ). The higher values of the perimeter to area ratio and the landscape shape index resulted also from differences in the shape of the vermetid reefscape. The perimeter to area ratio increases as a landscape has more patches with irregular perimeter, while high values of the landscape shape index result from landscapes deviating from a circular shape, with an increase in the amount of internal edges. The two metrics conveyed therefore additional information compared to the edge density, showing that the presence of the vermetid reefs underpinned also higher levels of shape complexity. The results of the Wilcoxon signed rank test confirmed the difference between the two seascapes, showing a statistically significant effect of the presence of the vermetid reefs on the coastal total edge. Moreover, the large effect size (r = 0.74) was consistent with the logarithmic ratio results, showing the high degree to which the vermetid reefs contribute to shaping the coastal seascape.

The loss of the vermetid reefscape as a result of anthropogenic fragmentation and degradation, or even the potential inundation of the reefs according to the sea level rise projections for the next decades (Cooley et al., 2022), would lead to a significantly simpler coastline shape, with a likely less degree of heterogeneity provided to the intertidal zone. Considering the ratio between the current reef growth rate of 0.19 mm/year (Sisma-Ventura et al., 2020) and the sea level rise rate of 1.4 mm/year estimated for the North-Western Sicily (Lo Presti et al., 2022), a scenario of complete inundation of the vermetid reefs is expected to occur between 2060 and 2080. Such changes would increase the competition for space and resources and ultimately lead to lower biodiversity levels (Rilov et al., 2021). In addition, the degradation of the biophysical structures and the ecological functions provided by the vermetid reefscape would involve the loss of many valuable ecosystem services. For instance, simpler, smaller, and more disaggregated patches of vermetid reefs would be less capable of preventing coastal erosion and regulating sediment transport, or acting as seawalls or breakwaters, protecting the coast from currents, waves, and extreme events (Milazzo et al., 2016). Finally, the loss of the outer reef and its living Dendropoma individuals would impair reef growth and prevent their CO₂ sequestration from the atmosphere to build new carbonate structures.

The characterization of marine bioconstructions through their structural properties has been increasing in the recent literature, laying the foundations for the investigation of the links between structure and biodiversity, functions, and services in the marine realm. The seascape approach together with the metrics inherited from the landscape ecology proved a useful set of tools to investigate the role played by the vermetid reefs in shaping the coastal seascape structure, potentially paving the way to applications on other marine bioconstructions.

In conclusion, this paper showed the value of the vermetid reefscape from a structural perspective, pointing to the complexity that would be irreversibly lost at a seascape scale due to the anthropogenic pressures the vermetid reefs will continue facing for the next decades. The study provides a reference for future monitoring and impact assessments on the structure and status of the investigated seascape, representing also a starting point for environmental accounting applications. Future studies on the vermetid reefscape will need to focus on the relationship between the structural complexity and the composition of species assemblages colonizing the reef, investigating the effects of structural changes on the supported biodiversity at different scales. Such investigations would contribute to improving the knowledge on this neglected bioconstruction and its important role in shaping Mediterranean seascapes.

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

FP: Conceptualization, Methodology, Software, Formal Analysis, Investigation, Data Curation, Writing – Original Draft, Visualization. RC: Conceptualization, Writing – Review & Editing, Supervision. All authors contributed to the article and approved the submitted version.