The northern Adriatic continental shelf hosts many mesophotic biogenic reefs, arrayed on the sedimentary bottom (see the ‘‘NorthernAdriatic_Reefs’’ compilation at the Marine Geoscience Data System, MGDS¹); and characterized by very heterogenous benthic assemblages (Ponti et al., 2011; Falace et al., 2015). Despite the great spatial variability of their benthic communities, these reefs can be considered as peculiar coralligenous “banks” (sensu Ballesteros, 2006) ranging in size from a few to thousands square meters and distributed between 15 and 40 m depth, where twilight conditions occur due to high water turbidity, with a mean light attenuation at the bottom of 1–2% of the surface irradiance (Ponti et al., 2011). The coralligenous reefs are among the richest, most diverse, and threatened habitats in the Mediterranean Sea. They are considered a “hot spot” of species diversity, shaped by bioconstruction and erosion processes, geological events, human impacts, and climate changes (Ballesteros, 2006). Coralligenous assemblages are exposed to anthropogenic disturbances (Claudet and Fraschetti, 2010; Coll et al., 2010, 2012) such as nutrient enrichment (e.g., Gennaro and Piazzi, 2011; Piazzi et al., 2018), increases in water turbidity and sediment deposition rates (e.g., Balata et al., 2005; Mateos-Molina et al., 2015), invasion by non-indigenous species (e.g., Piazzi and Balata, 2008; de Caralt and Cebrian, 2013), mechanical damages by anchoring, fishing nets and divers frequentation (e.g., Bavestrello et al., 1997; Hinz, 2017), and by climate change-related disturbances like exceptional storms (Teixido et al., 2013), acidification and thermal anomalies (Martin and Gattuso, 2009; Turicchia et al., 2018; Garrabou et al., 2019).

Coralligenous reefs dynamic results from the interplay between the building activities, mainly by the multi-stratified accretion of the encrusting calcareous rhodophytes (ECRs), and physical and biological eroding processes (Cerrano et al., 2001; Ingrosso et al., 2018). The biogenic reef accretion and its persistence over time depend on the predominance of the bioconstruction over dissolution and bioerosion processes (Garrabou and Ballesteros, 2000; Cerrano et al., 2001).

ECRs are the major builders of Mediterranean coralligenous reefs, contributing to limestone deposition. However, many sessile invertebrates with calcified skeletons (e.g., scleractinian corals, bryozoans, serpulid polychaetes, and bivalves) also play an important role in the bioconstruction process of the coralligenous reef by increasing and consolidating the limestone structure (Ballesteros, 2006; Ingrosso et al., 2018).

On the other hand, bioerosion is a widespread ecological process that acts at different spatial and temporal scales. It can alter habitat structure and destroy consolidated hard substrate (Davidson et al., 2018). Internal bioerosion (sensu Neumann, 1966) is generally due to a suite of endolithic organisms, including both microborers (<100 μm large) and macroborers (>100 μm; Tribollet and Golubic, 2011). Usually, the bioerosion processes on new substrates show a temporal succession that begins with microborers, settling within 1 year (Tribollet and Golubic, 2005; Färber et al., 2015; Grange et al., 2015), and continue with macroborers, which become dominant after 2–3 years (Bromley et al., 1990; Casoli et al., 2016b,2019). Macroborers comprise various organisms from a wide range of taxonomic groups, including sponges (e.g., Rosell and Uriz, 2002; Calcinai et al., 2011), polychaetes (e.g., Hutchings, 2008; Casoli et al., 2019), sipunculids (e.g., Risk et al., 1995; Gherardi and Bosence, 2001), and bivalves (e.g., Schiaparelli et al., 2005; Casoli et al., 2016b).

Most of the few long-term experiments to simultaneously measure both bioconstruction and bioerosion processes have been conducted in tropical habitats (e.g., Silbiger et al., 2014, 2016). Although some medium- and long-term field experiments on bioerosion processes have been carried out also in the Mediterranean Sea (Bromley et al., 1990; Casoli et al., 2016b,2019; Färber et al., 2016), these processes have never been investigated on coralligenous reefs of the northern Adriatic Sea, whose formation and maintenance of the diversity are poorly known. The purpose of this study is to shed light on the bioconstruction and bioerosion processes taking place in the main coralligenous reef typologies occurring in the northern Adriatic continental shelf.

Various methods allow to compute accretion and bioerosion rates in the field and in the lab, ranging from measuring the change in weight, height, volume, or density of experimental block to impregnating samples with resins to obtain casts or using different X-ray configurations (reviewed in Silbiger et al., 2016). Nowadays, the use of experimental blocks, of the same material or mineralogically similar to the substrate to be studied is the most used approach (Färber et al., 2016; Silbiger et al., 2016). However, separating and measuring the two processes simultaneously is very challenging. For this purpose, imaging methodologies in 3-dimensions (3D) based on computed tomography (CT) are very promising (Rossi et al., 2021). In the present study, the bioconstruction and bioerosion rates and their net balance on the northern Adriatic coralligenous reefs have been investigated in a field experiment using travertine limestone tiles as recruitment panels with two exposure times: 3 and 12 years. Shapes and volumes of the external biological limestone deposits and the internal bioerosion traces were non-destructively identified and measured through high-resolution CT.

In the northern Adriatic coralligenous reefs, the main builders are represented by ECRs, the bivalve Anomia ephippium, serpulid polychaetes, bryozoans, and barnacles. The present study shows that in the first 3 years, albeit sustained by different species compositions, total bioconstruction and its annual rate were almost the same at all sites. The differences between bioconstruction at the different sites become evident by analyzing these processes on a longer time scale. In 12 years, limestone deposited is much greater in the reef characterized by a higher abundance of calcareous algae (MR08) than in the other reefs. At MR08, the annual bioconstruction rate estimated in 12 years is equal to that estimated in 3 years, resulting in an almost constant rate over time. On the contrary, in the other two sites, the annual rates estimated in 12 years were significantly lower than those of the first 3 years. These different bioconstruction performances could be due to the differences in species assemblages inhabiting the study sites (Ponti et al., 2011). Indeed, the tiles deployed at MR08 after 12 years on the top side were totally covered by a thick layer of calcareous algae, mainly Lithophyllum incrustans Philippi, 1837, Mesophyllum sp. and Peyssonnelia sp. (Ponti et al., 2014). This result is consistent with the observations on other Mediterranean coralligenous reefs, whose formation and maintenance are mainly attributed to calcareous algae belonging to the genera Lithophyllum, Lithothamnion, Mesophyllum, Neogoniolithon, and Peyssonnelia (Garrabou and Ballesteros, 2000 and references therein). However, the growth of calcareous algae is complex as it can be characterized by periods of growth and shrinkage due to competitive interactions and disturbance events (Steneck, 1986).

The benthic assemblages at P204 and P213 were characterized by higher abundances of fast-growing species, including algal turfs, that may have outcompeted calcareous algae for space, limiting their settlement and growth, as often occurs in rocky coastal bottoms affected by high rates of sediment deposition (Airoldi, 2003). Space competitors include also serpulid polychaetes, which are important players in developing and maintaining the biogenic reefs (Laborel, 1987; Cocito, 2004; Casoli et al., 2016a). They act as secondary builders by shaping the seafloor and as binders by coating and fastening other tubes or partially filling crevices (Sanfilippo et al., 2013; Gravina et al., 2021). Indeed, serpulid polychaetes were abundant both on the top and bottom sides of the tiles; however, at MR08 after 12 years, on the top side, they were completely overgrown by calcareous algae.

Among the other builders, the solitary vermetid gastropods Thylacodes arenarius were only found after 12 years of exposure at MR08 on the top and bottom sides of the tiles. T. arenarius is a subtidal species that lives on hard substrates in dim light conditions and relatively calm waters (Calvo and Templado, 2005). Usually, individuals are covered by calcareous algae, sponges, bryozoans, and other organisms, and in fact here their shells were entirely overgrown by the ECRs.

Finally, at the site near the coast (P204), the proximity to the donor populations could have favored the settlement of fast calcifying organisms like the non-indigenous oyster, Magallana gigas (Bayne, 1999).

In the northern Adriatic coralligenous reefs, boring sponges represent the main cause of bioerosion. They can penetrate and erode limestone materials such as rocks, corals, and mollusk shells (Glynn and Manzello, 2015). They produce a vast system of branched and interconnected galleries in the substrate and at the same time communicate with the surface through numerous openings. The distribution, abundance, and erosion rates of boring sponges can be affected by environmental factors such as nutrients, temperature, turbidity, light, depth, and pH (e.g., Schönberg, 2008; Calcinai et al., 2011; Nava and Carballo, 2013; Silbiger et al., 2014; Marlow et al., 2018). The activities of boring sponges shape the coralligenous habitats by eroding the substrate and creating shelters for organisms (Cerrano et al., 2001; Calcinai et al., 2015), but at the same time they reduce the mechanical stability of the reef (Scott et al., 1988).

Cliona viridis was the dominant agent of erosion into the experimental tiles (up to 28% of the initial volume, on average over 12 years). This species is regarded as one the most abundant and effective borer in the Mediterranean Sea (Rosell et al., 1999; Bertolino et al., 2013), especially in the northern Adriatic mesophotic reefs (Ponti et al., 2011). Species from the Cliona viridis complex commonly displays high bioerosion rates, up to 28 kg m^–2 a^–1 (Schönberg et al., 2017 and references therein). It should be noted that the erosion produced by this species, although increased over time, was substantially the same at all sites. Although many boring sponges can be negatively affected by high sediment deposition and water turbidity, either by preventing settlement, hampering vital physiological function or controlling survivals (Nava and Carballo, 2013; Bell et al., 2015; Marlow et al., 2018), C. viridis seems to be tolerant to high levels of turbidity (<4 m visibility) and sediment deposition (Carballo et al., 1994, 1996; Carballo, 2006). Conversely, Cliona rhodensis was mainly found at MR08, where the water turbidity is on average lower than the other sites (Ponti et al., 2011). That is in agreement with the higher sensitive against turbidity and sedimentation of C. rhodensis than C. viridis (Carballo et al., 1994, 1996).

Burrowing worms, mainly spionids, sabellids, and cirratulids, are usually important in the early stage of erosion (Hutchings, 2008) and appeared to benefit from the substrate modifications provided by encrusting epibenthos (Casoli et al., 2019; Gravina et al., 2019). Although CT images revealed traces of boring polychaetes into the tiles, it was impossible to attribute the marks left to the responsible species. The mean limestone removed by burrowing worms increased with increasing time exposure and was almost the same at all sites. According to previous study, burrowing worms remove fewer amounts of limestone than sponges; however, by burrowing, they modify and weaken the substrate and, because of their short life span, facilitate the bioerosion of other organisms by leaving their burrows vacant for other borers (Hutchings et al., 1992).

Rocellaria dubia is one of the most common endolithic bivalves in the Mediterranean Sea. It prefers horizontal or slightly inclined surfaces and high sediment deposition (Schiaparelli et al., 2003). It can occur in high density both in the natural and artificial substrate (Schiaparelli et al., 2005; Casoli et al., 2016b). It is easily recognizable through its 8-shaped calcareous holes emerging from the substrate. Despite its wide diffusion and ecological importance, its biology and autecology are poorly known. Its planktonic larvae can settle in crevices or holes in the substrate and then efficiently excavate limestone (Morton et al., 2011; Ponti et al., 2015; Casoli et al., 2016b). R. dubia siphons have been observed both on the top and lateral side of the tiles. The mean limestone removed by R. dubia into the experimental tiles varies among the study sites. It was higher at P204 and P213, characterized by high water turbidity and sedimentation rates. That could be related to the tolerance of this species to high sedimentation rates, thanks to its long siphons protected by aragonitic siphonal tubes (Morton et al., 2011) and the possible competition with boring sponges at MR08. Noteworthy, the mean limestone removed did not increase by increasing the exposure time, confirming that R. dubia is a fast borer (Casoli et al., 2016b) and may have reached its maximum density in the first 3 years.

Considering the overall process, the mean bioerosion rate seems to increase over time, and it was higher at MR08. This may be due to the firm establishment of the sedimentation tolerant Cliona viridis boring sponge at all the sites, while at MR08 it may have been further promoted by less sedimentation. This has provided the boring sponge C. rhodensis with suitable habitat. Moreover, the higher abundance of calcareous algae has in turn provided an additional substrate for long-term bioerosion.

In this field experiment, bioconstruction has overcome the bioerosion processes only in the short term (3 years) and only where the calcareous algae find better conditions for settlement and growth. In the relatively long term (12 years), bioerosion equals the bioconstruction processes at all study sites, with a substantially null net result in terms of limestone budget. Although the external volume of the concretion may increase, its interior gradually empties, and the lower structural resistance could lead to subsequent collapses and compactions.

These observations lead to hypothesize in the investigated northern Adriatic coralligenous reefs a steady state, resulting from the net balance between bioconstruction and bioerosion, regardless by their differences in benthic assemblages. However, this result must be taken with caution due to the high variability observed among the individual experimental units, which are small in volume, and the relative shortness of the study period, which, although long for a field experiment, is not comparable with life span of these reefs, estimated in 5–7,000 years (Gordini et al., 2012; Tosi et al., 2017). Furthermore, due to the spatial and temporal scale adopted in the experiment, the results achieved cannot consider the effect of disturbances such as the worsening of environmental conditions or mechanical damage to the reefs caused by trawling that, with some gear, can displace and crumble square meters of reef in seconds.

The benthic assemblages of the northern Adriatic coralligenous reefs are characterized by high spatial heterogeneity and relatively low temporal variability (Ponti et al., 2011). Multiple interacting abiotic and biotic factors are affecting the structure of these communities over space and time. The spatial distribution of the three main types of benthic assemblages found has been related to geographic and environmental variables, like distance from the coast, depth, water turbidity, and sediment load (Ponti et al., 2011; Curiel et al., 2012; Falace et al., 2015). However, settlement and recruitment processes, related to the reproduction strategies, dispersive capacity, and distance of the donor populations, play a fundamental role in structuring these communities (Fava et al., 2016). Moreover, these reefs are impacted by various anthropogenic disturbances like dystrophic crises mostly related to eutrophication (Kollmann and Stachowitsch, 2001; Zuschin and Stachowitsch, 2009; Tomasovych et al., 2017), and intense trawling activities and littering (Pranovi et al., 2000; Melli et al., 2017). Ultimately, the long-time persistence and development of these biogenic reefs rely on the dynamics between bioconstruction and bioerosion processes. When the activities of boring organisms exceed the actions of builders, these reefs risk a shift from builder-dominant to a boring-dominant, leading to an unbalance of net accretion, as already occurred in many tropical coral reefs (e.g., Rose and Risk, 1985; Ward-Paige et al., 2005; Marulanda-Gómez et al., 2017).

The present study provides the first baseline knowledge on the bioerosion and bioconstruction dynamics over space and time in the northern Adriatic Sea coralligenous reefs. This was achieved by coupling a field experiment with high-resolution computed tomography, which allows to investigate the interior of the substrates in a non-destructive way offering new opportunities and novel perspectives on ecological researches (Gutierrez et al., 2018). The method applied is very promising, however there is room for improvement. Manual segmentation of CT 3D models can be time-consuming and challenging, and semi/automated methods, like those realized by Titschack et al. (2015) and Färber et al. (2016), should be further implemented to separate and distinguish interconnected empty spaces putatively due to different species based on the corresponding traces. The procedure could be achieved using supervised machine learning algorithms and methods for shape recognition and segmentation (Rossi et al., 2021).

The experimental material adopted (i.e., travertine) can influence the bioconstruction and bioerosion rates (Calcinai et al., 2008). Travertine is a porous limestone characterized by natural fractures, which made the experiment more realistic. However, as suggested by Silbiger et al. (2016), an initial scan of the experimental tiles would have been preferable to quantify the volume of the natural fractures and their role as a possible preferential corridor for borer organisms.

The ichnotaxonomy approach, originally developed as a hierarchical classification system for fossil traces, poses some limits when applied to investigate current bioerosion processes. Ichnogenera and ichnospecies identification are often tricky because the pattern of erosion morphology may have been affected by the microtexture of the calcareous substrates (e.g., Calcinai, 2004; Calcinai et al., 2008), and the traces made by different organisms were often merged into a network of connected cavities, a likely consequence of several generations of traces of endoliths (Färber et al., 2016).

However, combining CT and morphological taxonomy on sampled organisms made it possible to attribute different bioerosion traces (ichnotaxa) to the boring species. Six out of the nine identified ichnotaxa were attributed to 3 living species. It was acknowledged that Cliona viridis and C. rhodensis could produce different traces, depending on their ontogenetic phase.

Manipulative field experiments using artificial substrates (e.g., travertine) that resemble natural ones, combined with CT technology, allow exploring the mechanisms underlying the formation and maintenance of biogenic reefs. However, much of these processes remain to be investigated, especially in coralligenous and other temperate reefs typologies. With an increasing number of coralligenous reefs being subjected to anthropogenic disturbances in the Mediterranean Sea (Micheli et al., 2013; Bevilacqua et al., 2018), the balance between bioconstruction and bioerosion may be changed in favor of erosion with severe consequences for their conservation.

The implementation of experimental and innovative approaches could help the design of appropriate conservation strategies of coralligenous habitats in the Mediterranean Sea that are characterized by long-lived species, high spatial variability, and limited temporal changes (Teixidó et al., 2011) and are among the most vulnerable habitats (Ponti et al., 2021) to the current increases of anthropogenic disturbances and climate change.

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

ET and MP: conceptualization, formal analysis, and writing original draft. ET, MP, MB, and BC: investigation. MA, MM, and AS: resources. ET: visualization. MA, MP, and ET: funding acquisition. All authors: writing—review and editing.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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