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Habitat and benthic diversity in the bay of Bagnoli and surrounding areas (Gulf of Naples, Italy): A historical baseline for environmental restoration
Marine Environmental Research 157 (2020) 104925
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Habitat and benthic diversity in the bay of Bagnoli and surrounding areas (Gulf of Naples, Italy): A historical baseline for environmental restoration �s Vega Ferna �ndez, Luigi Musco, Maria Cristina Gambi * Martina Gaglioti, Toma Stazione Zoologica Anton Dohrn, Dept. of Integrative Marine Ecology, Villa Comunale, 80121, Napoli, Italy
A R T I C L E I N F O
A B S T R A C T
Keywords: Macrobenthos Habitat distribution Seagrasses Biodiversity Historical records Gulf of Naples Mediterranean sea
The aim of the study is to provide a synthesis on the biodiversity of zoobenthic species and benthic habitat distribution of Site of National Interest (SNI) of Bagnoli-Coroglio (Gulf of Naples, Tyrrhenian Sea, Italy), which represents one of the priority areas selected at National level for habitat restoration, and is located within the Gulf of Pozzuoli (a large Bay at the northern part of the Gulf of Naples). The work provides a dataset, covering the entire Gulf of Pozzuoli, and obtained consulting several sources of information, from historical to recent publications, and grey literature, aimed at the production of a check-list of species, and reconstruction map of the main marine habitats, in order to achieve a synoptic overview of the historical and recent zoobenthic fauna, as well as distribution of habitats, in order to serve as reference point for any future restoration plan in the area. Relevant information regarding the study area was found in 67 out of more than 250 sources consulted. Overall, 813 species of benthic organisms were recorded, summing up a total of 1006 records. Among them, 148 species were reported in the pre-industrial period (prior to 1911), 361 species during the industrial period (from 1911 to 1991), and 381 species in the course of the post-industrial period (from 1992 up to the present day). No dif ferences in biodiversity or distribution of individual species were directly attributable to the industrial activities in the study area. Such a finding is possibly due to different sampling effort among periods and lack of quan titative data for the majority of the recorded taxa. A mosaic of various habitat and biocoenoses were documented in the zones (shallow and deep hard bottoms, soft-bottoms with different sediment types, seagrass meadows). An overall reduction of the cover and a higher habitat fragmentation was documented for seagrass meadows (mainly Posidonia oceanica) over time. Given that regression of this seagrass species is common in a much wider extent than that covered by the study area, the trend here observed is probably due to multiple impacts from different human activities, including the industrial one at the Bagnoli SNI. The present study highlights that the SNI area is placed in a wider area representing a mosaic of different habitat types, which can provide donor populations of both habitat formers (sponges, gorgonians, scleractinians, bryozoans and mollusks), and seagrasses. These or ganisms are potentially relevant in implementing restoration measures aimed to improve the ecological status of this post–industrial area.
1. Introduction Coastal areas are subjected to land-borne influences and exposed to intense human pressures (Halpern et al., 2008). As a result, coastal areas experience rapid change worldwide. This is notably the case in closed and semi-enclosed basin, like the Mediterranean Sea (Coll et al., 2011). Despite its relatively small extentions, coastal areas are densely popu lated, shipping lanes convey nearly a third of the world traffic, and both land and marine resources are heavily exploited since millennia. Such a suite of factors often results in substantial environmental impact
(Micheli et al., 2013). In particular, localities where industrial activities settled, often served by nearby industrial and commercial harbors, inherited multiple impacts and widespread contamination for decennia. Long-running industrial facilities sometimes represent extreme exam ples of habitat degradation. For this reason, those areas provide us with the challenge of implementing measures aimed at restoring the original native habitats once the impact is reduced or eliminated. The dismissed industrial area of Bagnoli-Coroglio, located in the Gulf of Naples (Tyrrhenian Sea, Italy) (Fig. 1), was mainly devoted to steel production (brownfield in Fig. 1). It is actually a highly polluted area
* Corresponding author. E-mail address: [email protected] (M.C. Gambi). https://doi.org/10.1016/j.marenvres.2020.104925 Received 18 November 2019; Received in revised form 5 February 2020; Accepted 15 February 2020 Available online 20 February 2020 0141-1136/© 2020 Elsevier Ltd. All rights reserved.
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center. The aim of the present study is to provide a synthesis on available of data on benthic habitats and macrozoobenthos of the area, by consulting several sources of information ranging from grey literature to scientific publications. The acquired information would represent a database aimed at the production of a check-list of species and the identification of the main benthic communities and habitat. Several maps of the main marine habitats were also produced in the past, from not-georeferenced historical maps to more recent georeferenced data. Using these maps would allow to achieve a synoptic overview and a state of the art of the historical and recent information about habitat community, and species distribution intended to represent reference points for the imple mentation of restoration programs in the area.
and inserted within one of the 39 Sites of National Interest (SNI) due to high concentrations of PAHs and heavy metals in the sediments (Mor roni et al., 2020). As such, it deserves priority in habitat restoration and environmental remediation initiatives (Musco et al., 2017). Sediment toxicity affects large part of the sea bottom in the area (Morroni et al., 2020), with direct effects on the resident biota associated with sedi ments (Bertocci et al., 2019; Gambi et al., 2020; Tangherlini et al., 2020) and potential effects on species inhabiting rocky shores (Ruocco et al., 2020; Chiarore et al., 2020; Liberti et al., 2020; Limatola, 2020). The long-term accumulation of xenobiotic contaminants in this area deter mined the persistence of environmental degradation over decades since the period of industrial activities in the area, which spanned from early 1910s to 1991. There, chronic pollution represents a threat for human health, biodiversity and ecosystem functioning. Environmental reme diation practices coupled to restoration plans (EU Restoration Agenda) in this area are aimed at revert the environmental degradation and give back a healthy ecosystem to the local population. The ABBaCo project (“Sperimentazioni pilota finalizzate a restauro Ambientale e Balneabilit� a del SIN Bagnoli-Coroglio”). In particular is contributing to the development of new approaches for the removal and remediation of contaminated sediments and habitat restoration of impacted habitats. The first objective of the project in fact, includes the identifications of the benchmark of the environmental status of the area through analysis of historical data aimed at the identification of key species and habitats (Musco et al., 2017). The area of the SNI of Bagnoli-Coroglio is located within the Gulf of Pozzuoli (a large Bay in the northern part of the Gulf of Naples) (Fig. 1). This zone, due also to its vicinity with the town of Naples, historically represents one of the best studied and known coastal areas of Italy and the Mediterranean Sea. This is due to the presence of scientific In stitutions, such as the Stazione Zoologica Anton Dohrn (since 1872) and others (Universities, CNR) which are involved in marine investigations since more than one century and half (Groeben, 2002). The area is quite complex from the historic, geomorphological and ecological points of view. In fact, the Bagnoli area is close to two marine protected areas, which represent also submarine archaeological parks, the Gaiola and the Baia MPAs (instituted since 2000) (Russo et al., 2008), and is adjacent to the small Nisida island, an inactive volcano which is under protection and surveillance since 1933 due to the presence of a juvenile detention
2. Study area Although the study area defined in the context of the SNI and ABBaCo project is limited to the seabed in front of the former industrial pole of Bagnoli-Coroglio (Fig. 1), adjacent areas of the Gulf of Naples and Pozzuoli were considered for the purpose of characterizing zoo benthic diversity and benthic habitat distribution. Data on the coastal lagoons included in the area (Lucrino, Averno Miseno and Fusaro lakes) were not considered due to their brackish water characteristics, or since they lay outside the area (Fusaro). To document the presence of species of ecological importance and conservation interest (i.e. habitat formers) the historical survey was also extended along the south-eastern side to following locations: Nisida, Gaiola, and Capo Posillipo, as well as Capo Miseno, Baia, and Bacoli along the northwestern side (Fig. 1). Such arrangement was intended to document the occurrence of habitats and species occurring also in the surrounding areas of the SNI, which could act as donors for restoration purposes within the SNI, but could also give further insights on the most probable habitats and species historically present in the SNI. Based on the work of geomorphological characterization of the study area by De Pippo et al. (2002), and a subsequent study by Fasciglione et al. (2016), the seabed in front of the former brownfield and steel in dustrial pole (Fig. 1) is characterized to a large extent by sediments (sand of volcanic origin and mud) with the sporadic presence of some topographically unspoiled rocky outcrop, and by man-made structures
Fig. 1. Map of the study area of the Gulf of Pozzuoli. The area boxed with the line is strictly the SNI zone, included within the Pozzuoli Gulf and the Gulf of Naples. The Pozzuoli town and the Gaiola MPA and Cape Posillipo are also indicated. 2
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like docks, piers, and bridges along the coast. The actual rocky bottoms are limited to the islet of Nisida and its small internal bay named Porto Paone, and also to the small promontory called “La Pietra” (“the Stone”) up to the pier of the port of Pozzuoli-Rione Terra. Recent information on the geomorphological characteristics of the study area can be found in the cartography and morphometric analysis of the Bay of Pozzuoli (Somma et al., 2016). A Geological Map of Italy produced by the Cam pania Region Geological Service (Fedele et al., 2017) is also available and provides a detailed view on the geomorphological characteristics of the sea bottom in front of the islet of Nisida.
were produced based on the historical mapping by Funk (1927), rein terpreted by Puri et al. (1964) and Colantoni et al. (1982), and by Parenzan (1956) on Zosteracee; data (not georeferenced) were digitized and geo-referenced, to EPSG 4326: WGS 84 reference system utilizing QGIS v.2.18.15 and Google Earth Pro. The MATTM map (2004) was the only source already available as GIS file. Bionomic habitat maps from Casola et al. (2005) and Gamulin-Brida (1965) of Porto Paone (Nisida) hard bottoms were also acquired from printed material and digitized and geo-referenced with the same afore mentioned program. No habitat maps were available for the pre-industrial period (prior 1910).
3. Materials and methods
4. Results
A review of the relevant information available at the library of the Stazione Zoologica Anton Dohrn in Naples (SZN) was conducted, focusing on zoobenthic invertebrates and benthic habitats. This encompassed monographs of the Fauna and Flora of the Gulf of Naples, summarized by Lo Bianco (1909), activity report of the SZN, database of the SZN zoological collection, datasheets of the Archive Moncharmont (Archivio Moncharmont, 1965-1985; Gambi et al., 2013), and scientific literature on general studies conducted within the Gulf of Naples including data from the study area. Ancillary information was retrieved from the library of the University of Naples Federico II, and by consul ting iconographic sources at the SZN historical archive (historical cartography, photographic material, watercolors) as well as recent cartography (CARG-Campania Region documents and geomorpholog ical maps from CNR-ISMAR; Fedele et al., 2017). This compilation allowed to summarize sources written in different languages (mainly Italian, German and French) and give a synthetic access to this hidden literature to a wider audience. The benthic taxa which represent habitat formers and engineering species, as well as species of high natural heritage value were grouped, and their diversity and distribution patterns in the studied area checked in order to highlight possible pattern in space and/or time. The following groups of habitat formers were considered: tubicoulous polychaetes (sabellids, serpulids and other tube formers in softbottoms), encrusting cirripeds, anthozoans, molluscs (bivalves including some perforators and vermetids), bryozoans, porifers (massive and arborescent), and tunicates (solitary ascidians). Seagrasses (Pos idonia oceanica and Cymodocea nodosa) were also considered during the data gathering process. A database was compiled from data obtained through bibliographic source and updated for taxonomic classification according to WORMS (2019). In order to highlight possible changes due to the presence of the brownfield, the data have been grouped in three time periods: PreIndustrial (from 1850 to 1910); Industrial (from 1911 to 1991); and Post-Industrial (from 1992 to present). The geographical information on species occurrence provided by the majority of the historical sources proved to be insufficient, in this case, coordinates were inferred by centering the locations indicated in the sources (e.g. Pozzuoli, Bagnoli, Nisida). As regards the available carthographic information on habitat, we decided to include in this contribution the maps realized before 1991 (end of the industrial activities in the Bagnoli-Coroglio SNI), since they are not easily available for the audience, with the exception of the soft–bottoms biocoenosis map of Casola et al. (2005); this represent the first available data on community distribution in sediment habitat of the Bagnoli area (the subsequent map by Fasciglione et al., 2016 mostly overlapping the former one was not considered). We also decided to include the most recent map of the seagrasses, performed in 2002–2003 by Ministry of the Environment (MATTM, 2004), since this map was not available in the literature. Finally, the presence of P. oceanica remains in the cores of the study by Gabellini et al. (2005) were mapped over the biocoenoses map by Casola et al. (2005), to overlap sediment type s/biocoenoses with evidence of possible ancient occurrence of Posidonia in the area. Distribution maps of seagrasses (P. oceanica and C .nodosa)
The number of scientific studies carried out in the study area since the end of the nineteenth century indicates its high ecological relevance. Useful data and information on the study area were found in 67 sources (see Table S2) out of more than 250 sources consulted. Available in formation was very heterogeneous both qualitatively and quantitatively. Detailed geographic information, as well as habitat and depth, was generally lacking beyond generic toponyms in most of the species re cords. In addition, most of the papers, especially those focused on tax onomy, only report qualitative data and could be considered for the occurrence of the species only. Overall, for the considered extended area (From Capo Posillipo- Gaiola to Capo Miseno and the entire Gulf of Pozzuoli) and the three periods considered, 813 macro-benthic organ isms were recorded, for a total of 1006 records; 148 species are reported for the pre-industrial period, 361 for the industrial period, 381 for the post-industrial one (see Table S1 in Supplementary material). The following Phyla were recorded: Porifera, Cnidaria, Annelida, Nermertea, Plathelminthes, Mollusca, Arthropoda (Crustacea, Picnogonida), Bryo zoa, Echinodermata, Tunicata and Chordata. Most of the groups and benthic organisms reported were macrobenthic taxa. However, a few papers dealing with meiofauna were also considered (Bürger, 1895; Chappuis, 1938; Boaden, 1965; Polese et al., 2018). Comparing the three time periods in the whole record, there is a poor correspondence of species among across time in the study area: 27 species were common between the pre-industrial and the industrial periods; 9 between the pre-industrial and post-industrial periods, and 41 between the industrial and post-industrial period. There were not species in common to all the three considered periods. 4.1. Habitat formers A total of 109 habitat-former species, plus two engineering sea grasses were recorded. Among habitat formers the list includes con spicuous species, rare, and of high ecological relevance, such as the sponges Geodia cydonium (abundant at the Fumosa bank off Baia) (Saggiomo and Petrillo, 2008), Calyx nicaensis (reported in a cave at Capo Miseno), and Axinella spp. (along the Nisida islet). Some species are typical of the Coralligenous habitat such as the gorgonians Eunicella spp. and Paramuricea clavata, as well as the scleractinia Astroides caly cularis are reported along the Nisida rocky cliffs (Table S1) (Bacci, 1946), while the large bivalve Pinna nobilis is documented with only a few records associated to P. oceanica meadows, also within the Paone harbor (Nisida island). It is worth noting the occurrence of a highly diversified ascidian fauna composed of solitary species, which probably constituted a facies in the deepest soft bottoms of the Pozzuoli Bay (Salfi, 1931, and several records in the Archive Moncharmont 1965–1985). Such formations were never documented during the post-industrial period. Instead, tubicolous polychates (such as, Owenia fusiformis, several Sabellidae and Terebellidae) were recorded as the habitat for mers in soft bottoms during post-industrial period (Bioservice Report, 2003; Casola et al., 2005).
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4.2. Alien species
were inhabited by arpacticoid copepod Trigriopus fulvus (reported as Harpacticus fulvus), and the decapod Pachygrapsus marmoratus. In the midlittoral zone (the area defined between low and high tide) there were abundant barnacles of the species Chtamalus stellatus, the gastropods Patella rustica (reported as P. lusitanica), Patella aspera, Phorcus turbinatus (reported as Monodonta turbinata) the chiton Leprochitona caprearum (reported as Middeldorfia caprearum), the anemone Actinia equina, and the crab P. marmoratus and Eriphia verrucosa (reported as E. spinifrons). At the entrance of the bay, small specimens of Mytilus galloprovincialis and Mytilaster minimus (reported as Brachyodontes minimus) were observed. In the infralittoral zone, photophilic algae were dominant, among them a facies of Dictyopteris membranacea, and other common species such as Dictyota dichotoma, and the brown seaweed Cystoseira abrotanifolia. Among the invertebrates, ophiurans resulted abundant, and other species, such as the anemone Anemonia viridis (reported as A. sulcata), the starfishes Coscinasteria tenuispina and Martasterias gla cialis and the sea urchin Paracentrotus lividus were also present. Sponges, such as Spongia officinalis and Petrosia ficiformis were also common. Among the photophilic algae, nitrophilic algae, (i.e. indicators of organic enrichment), were also observed, especially Ulva rigida (indi cated as U. lactuca), and the brown alga Hypnea musciformis. Some “enclaves” (inclusions) of species typical of the pre-Coralligenous and Coralligenous habitats were also present in the shaded areas favoring sciaphilous organisms, such as the macroalgae Halimeda tuna, Flabellia petiolata (reported as Udotea petiolata) several species of Peyssonnelia spp. However, the coralligenous community and habitat was not actu ally present. The cnidarian Cornularia cornucopiae, ascidians such as Halocynthia papillosa and Microcosmus sulcatus were also present. The seafloor of Porto Paone was also characterized by soft bottom biocoenoses and seagrasses (see below). As regard the distribution of hard bottom biocoenoses for the postindustrial period, some information was obtained from the cartog raphy produced both by Russo et al. (2005b) and Simeone et al. (2016) as part of a study carried out on behalf of the Gaiola Marine Protected Area. The cartography also involved the external coasts of Nisida, which showed infralittoral photophilic algae, and limited outcrops of cor alligenous assemblages (gorgonians, sponges, bryozoans).
In our dataset only three alien invertebrate species occurred in the considered area: the two sabellid polychaetes Branchiomma luctuosum, B. boholense and the opistobranch mollusk Anteaeolidella cacaotica (re ported as Aeolidella takanosimensis) (Table 1S). The former two species are established while the latter is considered casual and never recorded after Schmekel (1968). No studies on their impact are available in the areas as well as in the entire Gulf of Naples. The few other conspicuous alien species in the area are macroalgae, outside the scope of our work. However, among them only Caulerpa cylindracea and Asparagopsis armata are reported to have an invasive habit in the area (Buia et al., 2001; Papa and Russo, 2010) and may have a potential impact on the local communities, although no studies are available on this subject. 4.3. Hard bottoms The major source of information on hard bottoms, which covers the whole study area during the industrial period, was the monograph by Funk (1927) focusing on marine macrophytes. This work also summa rizes previous historical works and provides the first distribution of P. oceanica meadows. The most conspicuous hard bottom zone is the Nisida island and its inlet Porto Paone, which is the crater of the ancient vol canic edifice. Porto Paone, despite its limited extension and depth, held a complex mosaic of biocoenoses (photophilic algae, nitrophilous algae, C. nodosa, P. oceanica meadow, soft bottoms, precoralligenous and coralligenous (Fig. 2) and a remarkable benthic biodiversity (140 spe cies Gamulin-Brida, 1965; Table S1). The paper by Gamulin-Brida (1965, in French) accounted for a detailed list of organism and com munities, and also represents an ante-litteram example of application of SCUBA diving visual census techniques. The Porto Paone inlet has a maximum length and a width of 225 m and 185 m, respectively, and a maximum depth of 15 m. The above mentioned author divided the area into 8 sectors to take into account the ecological differences in light exposure, and the differences with respect to the connection with the open sea. Among the hard bottom biocoenoses the work listed those typical of supralittoral rock, characterized by Littorina neritoides, Ligia italica and Chtamalus depressus. Some “reef pools” with variable salinity
Fig. 2. Distribution of benthic biocenoses within Porto Paone (Nisida islet) (georeferenced after Gamulin-Brida, 1965). 4
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Biocoenosis of muddy sands in calm areas (SVMC) constituted the most extensive habitat of the MPA, down to 15 m. The SVMC biocenosis appeared enriched with fragments from submerged Roman artefacts and exoskeletons of benthic organisms, and presented elements of the SGCF biocenosis (sands and gravels under the influence of bottom currents), and elements of the SFBC biocoenosis (well calibrated fine sand) near the Lucrino lake. The soft bottoms were covered by the green alga C. prolifera mixed with the alien congeneric C. cylindracea. Meadows and semi-prairies of C. nodosa, mixed with the SVMC and SFBC biocoenoses, were mainly observed in the area in front of Lake Lucrino, between 3 and 7 m depth.
4.4. Soft-bottoms Information on macrozoobenthic fauna from soft bottom habitats were available in Gamulin-Brida (1965), which highlighted the presence of sandy bottoms about 20 m from the rocky cliff. Beyond that distance, soft bottoms patches appeared mixed with vegetated ones dominated by either P. oceanica and C. nodosa seagrasses with peculiar associated communities. Following the classification of Bellan-Santini et al. (1994), the part of the bottom between fine sediments and the rocky cliff was characterized by the biocoenosis of sand and gravel under the influence of the bottom currents (SGCF). The large bivalve Pinna nobilis was here documented in the channels among patches of P. oceanica. Data on benthic populations and biocoenosis associated with soft bottoms during the post-industrial period was provided by the Bioservice Report (2003) and summarized in Casola et al. (2005) (Fig. 3). In such work, 307 taxa and five biocoenoses were identified: i) the biocoenosis of well-calibrated fine sands (SFBC), which extends along the coastal strip between Lido delle Sirene and Bagnoli at depths between 3 and 8 m; ii) the biocenosis of muddy sands of calm fashion (SVMC), in the superficial area between the “Lido delle Sirene” and the isthmus connecting Coro glio to the island of Nisida at less than 5 m depth; iii) the biocoenosis of coastal debris (DC) between 25 and 40 m depth; iv) the biocenosis of coastal terrigenous mud (VTC), at 50 m depth; v) a transition ecotonal assemblage localized between the SFBC and the DC biocoenoses char acterized by the coexistence of species typical of the surrounding bio coenoses. Furthermore, the seagrass C. nodosa appeared interspersed with the green alga Caulerpa prolifera in correspondence of the SVMC biocoenosis. This community/biocoenosis characterization and species composition was confirmed by subsequent survey carried out on the area in 2005 and summarized in Fasciglione et al. (2016). A characterization of the habitat of the submerged Park of the Baia MPA was also available (Russo et al., 2005a, 2008). The area is largely characterized by a mosaic of patches of soft bottoms and submerged archaeological remains of Roman origin. The occurring biocoenoses were photophilous algae (AP), which was present on the top of sub merged Roman ruins, while sciophilous populations were observed in the cavities and more shaded walls within the same structures.
4.5. Seagrasses and their habitat Information on occurrence and distribution of seagrasses, mainly P . oceanica, in the study area was available in the monumental work by Funk (1927), in his compendium on marine macrophytes. Collection was based on direct sampling on hard bottoms and dredge sampling for seagrasses, and other plant formations, indicated by the author as fibrous and calcareous algae (Fig. 4). This map is not well referenced in space, and sampling locations were originally figured as individual points (Table II in Funk, 1927). These points were extrapolated as a map by Puri et al. (1964) and later redrawn by Colantoni et al. (1982). We integrated all these information in Fig. 4, including the macroalgl dis tribution, in consideration of their important role as habitat former and their potential role in structuring the local fauna. P. oceanica extended from the outer side of the islet of Nisida facing Capo Posillipo to the sea bottom between Capo Posillipo and Gaiola. While the calcareous algae reported, probably correspond to the coralline beds later reported in the Gulf of Pozzuoli by other authors. The fibrous algae indicated by Funk (1927) probably were conspicuous erect and arborescent algae, perhaps Fucales or Sargassaceae, observed in both historical and recent times in the same zone (Buia et al., 2013) (Fig. 4). A first quantification of the extent of seagrasses (Zosteracee) was provided by Parenzan (1956), who estimated that Zosteracee (mainly P. oceanica) covered 2106 square meters in the area between Capo Miseno and Nisida (Fig. 4). P. oceanica occurred within the SNI north to
Fig. 3. Distribution of benthos sampling stations on soft bottom inside the SNI of Bagnoli and benthic biocenosis (revised and georeferenced after Casola et al., 2005). 5
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Fig. 4. Georeferenced re-elaboration of Posidonia oceanica distribution and other macrophytes, according to Funk (1927) e elaborated by Puri et al. (1964); and distribution of Zosteracee (mainly Posidonia oceanica) from Parenzan (1956).
the piers, up to the external pier of the Pozzuoli harbour, in front of Porto Paone, and in the outer side of Nisida and Capo Posillipo (Fig. 4). It is also worth to mention that Parenzan (1956) listed Zostera marina among seagrasses, but this species was never recorded in subsequent surveys. It could be hypothesized that this record of Z. marina could in fact refer to C. nodosa, which is very common in the zone. Also, in the survey of Parenzan (1956), sampling was carried out indirectly by dredging, and spatial distribution was not well referenced. Therefore,
comparisons of the seagrass maps by Funk (1927) and Parenzan (1956) with the more recent geo-referenced map by MATTM (2004) should be done with caution. The distribution of seagrasses was also studied in the aforementioned work of Gamulin-Brida (1965) inside Porto Paone, reporting large part of the inlet as colonized by P. oceanica and C. nodosa, mixed with rocky outcrops covered by photophilic algae and patches of unvegetated sediment. P. oceanica was then present mainly in the southern part of
Fig. 5. Elaboration of the mapping of seagrasses (Posidonia oceanica and Cymodocea nodosa) performed in the period 2002–2004 on the Campanian coast, and relative to the Gulf of Pozzuoli (MATTM, 2004). 6
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communities and habitats, thereby providing a reference baseline for defining restoration objectives. As expected from a historical dataset, all the historical information, except some of the most recent works, lacked quantitative data and precise geographical references. As a result, the pattern of distribution of the majority of the species appeared frag mentary both in space and time. However, combining different infor mation sources reduced uncertainty and allowed to track a relevant pattern of change in distribution over time for some species (e.g., seagrasses). From an historical point of view, considering the huge dataset collected, spanning from mid-1800 to present time, we attempted to compare the data according to the industrial activity in the area. How ever, the fact that few species were contemporary present during the three periods considered, and that there were no studies on community and habitat mapping in the pre-industrial period, did not allow to relate and quantify temporal changes in biodiversity or in habitat distribution, except, to some extent, for the seagrasses. The biodiversity recorded in the period prior the industrialization of Bagnoli (prior 1911; 148 spe cies) suffered from an evident bias linked to a minor number of studies and therefore relatively weak sampling effort. This is evident if compared with the diversity observed during the industrial period (1911–1991; 361 species), with benthic fauna almost doubled and a modest overlapping of species with the previous period (27 species in common) probably due to a larger number of studies in respect to the past. In fact, the industrial period coincided with and intense and pro ductive periods of marine research, especially held by the Stazione Zoologica of Naples, and mainly focused on taxonomy, faunistic and first ecological surveys, due to eminent zoologists, such as Bacci, Salfi, Sar� a, Cognetti, Ryland, Tortonese, Parenzan, and Moncharmont. The postindustrial period is characterized by research weakly focused on tax onomy, but more oriented on ecology, with large scale survey and georeferenced mapping, including investigations aimed at evaluating anthropogenic impacts. Although the species recorded in this last period is the highest of the whole data set (381), it only shares 41 species with the industrial period and 9 with the pre-industrial one. In addition, the majority of species of the recent period (over 300) were recorded in two surveys on the soft-bottoms (Bioservice Report, 2003; Casola et al.,
Porto Paone between 5 and 6 m depth, and a detailed list of epiphytic and motile organisms associated to the leaf canopy was provided by this author (see Table 1S). During the post-industrial period, C. nodosa was reported for the areas located northwest of the bay of Porto Paone, where the sediment contained the largest proportion of organic matter and mud. Russo et al. (2005a, 2008) reported C. nodosa extent, as well as isolated patches of P. oceanica, in front of the Baia MPA, such as off Lake Lucrino and opposite to Punta Epitaffio. The map of distribution of seagrasses in Campania and Calabria re gions (MATTM, 2004) (Fig. 5) shows the distribution of both C. nodosa, and P. oceanica mixed with C. nodosa, limited to the west slope of the promontory of Capo Miseno up to Bacoli. In addition, there were some isolated patches of P. oceanica and C. nodosa in the innermost portion of the Gulf of Pozzuoli between 25 and 30 m depth. A mosaic of P. oceanica and dead matte has been found deeper between 30 and 35 m in front of the islet of Nisida. Finally, the sampling sites described of Gabellini et al. (2005) were georeferenced and plotted. The resulting map (Fig. 6), based on sediment cores and grabs, revealed the occurrence of P. oceanica rhizomes and residues of dead matte in the sediment from the southernmost portion of the SNI, as well as along the rocky coasts of the northern side, and near the port of Nisida. 5. Discussion The study area here considered, which encompassed the BagnoliCoroglio SNI and adjacent zones (Gulf of Pozzuoli), is one of the best known in the Gulf of Naples due most likely to its accessibility, long tradition for bathing and hydrothermal facilities, and transformation in one of the main sites of industrial development in Italy. Here it is re ported the occurrence of 813 species, for a total of 1006 records, in the SNI and its neighborhoods during three periods of time roughly span ning 160 years. The area represents also the best known within the Gulf of Naples and with the highest biodiversity also for the macrophytes (macroalgae and seagrasses) (Funk, 1927; Buia et al., 2013). The synthesis of species and habitats here presented provides a synoptic view of the biodiversity, and the distribution of benthic
Fig. 6. Distribution of Posidonia oceanica in core sample stations on soft bottom inside the SNI of Bagnoli (after Gabellini et al., 2005), superimposed on the benthic soft-bottom biocenoses (after Casola et al., 2005). 7
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2005; Fasciglione et al., 2016). Therefore, the taxonomic diversity and information amongst the three periods is not homogeneous. Based on the present dataset it is not possible to highlight any difference in the pattern of biodiversity or the distribution of individual species and habitats along the considered period of time and its possible relationship with industrial activity and impact on the area. Therefore, we suspect that the intrinsic limits of the historical information here reported, could be the same for other areas of the Gulf of Naples, which account for similar amount and quality of historical information. Such information may have a strong potential, but it can suffer from the same constraints herein observed when compared with more recent data. However, the majority of the species (especially those from hard bottoms and P. oceanica meadows) occurs at the Nisida islet and inside Porto Paone probably due to the complex geomorphology of the area. Moreover, Nisida and Posillipo Cape represented two of the main areas for sam pling and collection of marine organisms, as documented in the SZN Zoological Collection and the Archive Moncharmont (1965-1985). The presence of the penitentiary institute in the Nisida islet, and the conse quent restricted access to this area since the early 1800s, probably favored the maintenance of nearly pristine conditions at Porto Paone, which was characterized by a complex mosaics of different habitat patches, as documented by Gamulin-Brida in 1965 (see Fig. 2). This area deserves special attention and it should be further surveyed in order to better understand the temporal dynamics of biodiversity in the SNI. Such an area, as well as the external Nisida cliffs, might be considered suitable as donor sites for future restoration initiatives within the SNI. In fact, the maps reported in this work might be valuable benchmarks for assessing the restoration success in the area, especially those produced for soft-bottoms fauna and communities, which are very accurate and useful for future assessment of these habitats (Casola et al., 2005; Fas ciglione et al., 2016). The historical maps of distribution of P. oceanica and C. nodosa meadows should be considered with caution. However, they help to visualize the progressive reduction of the overall covering of meadows from larger and continuous areas documented by Funk (1927) and Parenzan (1956), to smaller, more fragmented patches in the most recent period (MATTM, 2004) and mostly observed outside the SNI area, albeit remains of P. oceanica dead matt inside the sediment cores sampled within the SNI (Gabellini et al., 2005), suggest that P. oceanica was probably present also within the SNI. It is plausible that the overall reduction and fragmentation of seagrass cover, resulted from a suite of different human impacts, including the industrial pollution (e.g., coastal reclamation and development, organic pollution, fishing, anchoring, etc.). In fact, multiple human impact on benthic habitats was recently detected in the area (Bertocci et al., 2019), albeit shallow hard bottom communities appeared resilient and therefore adapted to the harsh local conditions (Pellecchia et al., 2020). In conclusion, this synthesis highlights that the impacted SNI area hosted a diversified zoobenthic fauna and a complex mosaic of different coastal habitat (seagrasses, shallow and deepwater hard bottoms, a va riety of soft bottom habitats). In case of rehabilitation of the area with dredging of contaminated sediments and cessation of additional forms of human impact, the remnant populations of ecologically relevant or ganisms (sponges, gorgonians, scleractinians, bryozoans and molluscs, and seagrasses) of this or neighboring areas might still have the potential to became donor populations for the restoration measures.
list of the species with additional information on their records, shape files of the GIS maps). Ethical approval No use of animals or plants were included in this paper based entirely on a literature synthesis. Declaration of competing interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. Acknowledgements We are grateful to Dr. Claudia Di Somma and all the library staff of the SZN for their help and collaboration in consulting the historical literature as well as other historical documents related to the study area. MG was supported by a fellowship provided by the SZN. This study was supported by the project ABBaCo funded by the Italian Ministry for Education, University and Research (grant number C62F16000170001). Appendix A. Supplementary data Supplementary data to this article can be found online at https://doi. org/10.1016/j.marenvres.2020.104925. References Archive Moncharmont, 1965-1985. Archive (More than 5,000 Paper Sheets) Complite by Prof. Ugo Moncharmont when Was Hired as Responsible of the Zoology Dept. Of the Stazione Zoologica, and Acquired in Digital Form by the Library and Public Archive of the Stazione Zoologica in Naples (see Gambi et al., 2013). Bacci, G., 1946. Ricerche sulle zoocenosi bentoniche del Golfo di Napoli. I La secca di Benda Palummo. Pubblicazioni della Stazione Zool. Napoli 20 (2), 158–178. Boaden, P.J., 1965. Interstitial fauna from Porto Paone. Pubblicazioni della Stazione Zool. Napoli 34 (2), 235–239. Bürger, O., 1895. Die Nemertinen des Golfes von Neapel und der Angrenzenden MeeresAbschnitte. Monographie Fauna und Flora des Golfes von Neapel, vol. 22. Bellan-Santini, D., Lacaze, J.-C., Poizat, C., 1994. Les biocenoses marines et littorales de Mediterran�ee. Synth� ese, menaces et perspectives. Museum National Histoire Naturelle Paris. Collection Patrimoines Nat. 19, 1–246. Bertocci, I., Dell’Anno, A., Musco, L., Gambi, C., Saggiomo, V., Cannavacciuolo, M., Lo Martire, M., Passarelli, A., Zazo, G., Danovaro, R., 2019. Multiple human pressures in coastal habitats: variation of meiofaunal assemblages associated with sewage discharge in a post-industrial area. Sci. Total Environ. 655, 1218–1231. Bioservice Report, 2003. Rapporto finale di Attivit� a “Analisi dei popolamenti macrozoobentonici di fondo mobile ai fini della definizione di un quadro di riferimento per le valutazioni di impatto ambientale nelle aree marine costiere (Regione Campania rif. 170/97). Buia, M.C., Gambi, M.C., Terlizzi, A., Mazzella, L., 2001. Colonization of C. racemosa along the southern Italian coast: I. distribution, phenological variability and ecological role. In: Gravez, V., Ruitton, S., Boudouresque, C.F., Le Direac’h, L., Meinesz, A., Scabbia, G., Verlaque, M. (Eds.), Proceedings of the Fourth International Workshop on Caulerpa Taxifolia, Marseille, France, pp. 352–360. Buia, M.C., Chiarore, A., Mulas, M., Porzio, L., 2013. Historical changes in algal diversity in the Gulf of Naples. In: Ozhan, E. (Ed.), MEDCOAST Proceedings, Marmaris Turkey, 30 October- 3 November 2013, pp. 837–846. Casola, E., Lanera, P., Magnifico, G., Plastina, N., Scardi, M., Valiante, L.M., Vinci, D., 2005. Carta bionomica dei fondali antistanti l’ex stabilimento siderurgico Italsider (Bagnoli, Napoli). Biol. Mar. Mediterr. 12 (1), 244–247. Chappuis, P.A., 1938. Sub e Hanpacticoiden aus sud-Italien. Bull. Soc. Sci. Cluj 9, 153–181. Chiarore, A., Musco, L., Bertocci, I., Gallo, A., Cannavacciuolo, A., mutalipassi, M., Caramiello, D., Giomi, F., Fusi, M., Danovaro, R., Munari, M., 2020. Sea urchin chronicles. The effect of oxygen super-saturation and marine polluted sediments from Bagnoli-Coroglio Bay on different life stages of the sea urchin Paracentrotus lividus. Mar. Environ. Res. (this issue). Colantoni, P., Gallignani, P., Fresi, E., Cinelli, F., 1982. Patterns of Posidonia oceanica (L.) Delile beds around the island of Ischia (Gulf of Naples) and adjacent waters. Mar. Ecol. 3 (1), 53–74. Coll, M., Piroddi, C., Albouy, C., Ben Rais Lasram, F., Cheung, W.W.L., et al., 2011. The Mediterranean Sea under siege: spatial overlap between marine biodiversity, cumulative threats and marine reserves. Global Ecol. Biogeogr. 21 (4), 465–480. De Pippo, T., Donadio, C., Pennetta, M., Terlizzi, F., Valente, A., Vecchione, C., Vegliante, M., 2002. Seabed morphology and pollution along the Bagnoli coast
Authors’ contribution All Authors conceived the paper. MG and MCG performed the work; MG performed all the GIS maps; MCG wrote the initial Ms with feedback and comments of all Authors. Data availability The individual raw data used to support the findings of this study are available from the corresponding author upon request (complete check8
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Habitat and benthic diversity in the bay of Bagnoli and surrounding areas (Gulf of Naples, Italy): A historical baseline for environmental restoration �s Vega Ferna �ndez, Luigi Musco, Maria Cristina Gambi * Martina Gaglioti, Toma Stazione Zoologica Anton Dohrn, Dept. of Integrative Marine Ecology, Villa Comunale, 80121, Napoli, Italy
A R T I C L E I N F O
A B S T R A C T
Keywords: Macrobenthos Habitat distribution Seagrasses Biodiversity Historical records Gulf of Naples Mediterranean sea
The aim of the study is to provide a synthesis on the biodiversity of zoobenthic species and benthic habitat distribution of Site of National Interest (SNI) of Bagnoli-Coroglio (Gulf of Naples, Tyrrhenian Sea, Italy), which represents one of the priority areas selected at National level for habitat restoration, and is located within the Gulf of Pozzuoli (a large Bay at the northern part of the Gulf of Naples). The work provides a dataset, covering the entire Gulf of Pozzuoli, and obtained consulting several sources of information, from historical to recent publications, and grey literature, aimed at the production of a check-list of species, and reconstruction map of the main marine habitats, in order to achieve a synoptic overview of the historical and recent zoobenthic fauna, as well as distribution of habitats, in order to serve as reference point for any future restoration plan in the area. Relevant information regarding the study area was found in 67 out of more than 250 sources consulted. Overall, 813 species of benthic organisms were recorded, summing up a total of 1006 records. Among them, 148 species were reported in the pre-industrial period (prior to 1911), 361 species during the industrial period (from 1911 to 1991), and 381 species in the course of the post-industrial period (from 1992 up to the present day). No dif ferences in biodiversity or distribution of individual species were directly attributable to the industrial activities in the study area. Such a finding is possibly due to different sampling effort among periods and lack of quan titative data for the majority of the recorded taxa. A mosaic of various habitat and biocoenoses were documented in the zones (shallow and deep hard bottoms, soft-bottoms with different sediment types, seagrass meadows). An overall reduction of the cover and a higher habitat fragmentation was documented for seagrass meadows (mainly Posidonia oceanica) over time. Given that regression of this seagrass species is common in a much wider extent than that covered by the study area, the trend here observed is probably due to multiple impacts from different human activities, including the industrial one at the Bagnoli SNI. The present study highlights that the SNI area is placed in a wider area representing a mosaic of different habitat types, which can provide donor populations of both habitat formers (sponges, gorgonians, scleractinians, bryozoans and mollusks), and seagrasses. These or ganisms are potentially relevant in implementing restoration measures aimed to improve the ecological status of this post–industrial area.
1. Introduction Coastal areas are subjected to land-borne influences and exposed to intense human pressures (Halpern et al., 2008). As a result, coastal areas experience rapid change worldwide. This is notably the case in closed and semi-enclosed basin, like the Mediterranean Sea (Coll et al., 2011). Despite its relatively small extentions, coastal areas are densely popu lated, shipping lanes convey nearly a third of the world traffic, and both land and marine resources are heavily exploited since millennia. Such a suite of factors often results in substantial environmental impact
(Micheli et al., 2013). In particular, localities where industrial activities settled, often served by nearby industrial and commercial harbors, inherited multiple impacts and widespread contamination for decennia. Long-running industrial facilities sometimes represent extreme exam ples of habitat degradation. For this reason, those areas provide us with the challenge of implementing measures aimed at restoring the original native habitats once the impact is reduced or eliminated. The dismissed industrial area of Bagnoli-Coroglio, located in the Gulf of Naples (Tyrrhenian Sea, Italy) (Fig. 1), was mainly devoted to steel production (brownfield in Fig. 1). It is actually a highly polluted area
* Corresponding author. E-mail address: [email protected] (M.C. Gambi). https://doi.org/10.1016/j.marenvres.2020.104925 Received 18 November 2019; Received in revised form 5 February 2020; Accepted 15 February 2020 Available online 20 February 2020 0141-1136/© 2020 Elsevier Ltd. All rights reserved.
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center. The aim of the present study is to provide a synthesis on available of data on benthic habitats and macrozoobenthos of the area, by consulting several sources of information ranging from grey literature to scientific publications. The acquired information would represent a database aimed at the production of a check-list of species and the identification of the main benthic communities and habitat. Several maps of the main marine habitats were also produced in the past, from not-georeferenced historical maps to more recent georeferenced data. Using these maps would allow to achieve a synoptic overview and a state of the art of the historical and recent information about habitat community, and species distribution intended to represent reference points for the imple mentation of restoration programs in the area.
and inserted within one of the 39 Sites of National Interest (SNI) due to high concentrations of PAHs and heavy metals in the sediments (Mor roni et al., 2020). As such, it deserves priority in habitat restoration and environmental remediation initiatives (Musco et al., 2017). Sediment toxicity affects large part of the sea bottom in the area (Morroni et al., 2020), with direct effects on the resident biota associated with sedi ments (Bertocci et al., 2019; Gambi et al., 2020; Tangherlini et al., 2020) and potential effects on species inhabiting rocky shores (Ruocco et al., 2020; Chiarore et al., 2020; Liberti et al., 2020; Limatola, 2020). The long-term accumulation of xenobiotic contaminants in this area deter mined the persistence of environmental degradation over decades since the period of industrial activities in the area, which spanned from early 1910s to 1991. There, chronic pollution represents a threat for human health, biodiversity and ecosystem functioning. Environmental reme diation practices coupled to restoration plans (EU Restoration Agenda) in this area are aimed at revert the environmental degradation and give back a healthy ecosystem to the local population. The ABBaCo project (“Sperimentazioni pilota finalizzate a restauro Ambientale e Balneabilit� a del SIN Bagnoli-Coroglio”). In particular is contributing to the development of new approaches for the removal and remediation of contaminated sediments and habitat restoration of impacted habitats. The first objective of the project in fact, includes the identifications of the benchmark of the environmental status of the area through analysis of historical data aimed at the identification of key species and habitats (Musco et al., 2017). The area of the SNI of Bagnoli-Coroglio is located within the Gulf of Pozzuoli (a large Bay in the northern part of the Gulf of Naples) (Fig. 1). This zone, due also to its vicinity with the town of Naples, historically represents one of the best studied and known coastal areas of Italy and the Mediterranean Sea. This is due to the presence of scientific In stitutions, such as the Stazione Zoologica Anton Dohrn (since 1872) and others (Universities, CNR) which are involved in marine investigations since more than one century and half (Groeben, 2002). The area is quite complex from the historic, geomorphological and ecological points of view. In fact, the Bagnoli area is close to two marine protected areas, which represent also submarine archaeological parks, the Gaiola and the Baia MPAs (instituted since 2000) (Russo et al., 2008), and is adjacent to the small Nisida island, an inactive volcano which is under protection and surveillance since 1933 due to the presence of a juvenile detention
2. Study area Although the study area defined in the context of the SNI and ABBaCo project is limited to the seabed in front of the former industrial pole of Bagnoli-Coroglio (Fig. 1), adjacent areas of the Gulf of Naples and Pozzuoli were considered for the purpose of characterizing zoo benthic diversity and benthic habitat distribution. Data on the coastal lagoons included in the area (Lucrino, Averno Miseno and Fusaro lakes) were not considered due to their brackish water characteristics, or since they lay outside the area (Fusaro). To document the presence of species of ecological importance and conservation interest (i.e. habitat formers) the historical survey was also extended along the south-eastern side to following locations: Nisida, Gaiola, and Capo Posillipo, as well as Capo Miseno, Baia, and Bacoli along the northwestern side (Fig. 1). Such arrangement was intended to document the occurrence of habitats and species occurring also in the surrounding areas of the SNI, which could act as donors for restoration purposes within the SNI, but could also give further insights on the most probable habitats and species historically present in the SNI. Based on the work of geomorphological characterization of the study area by De Pippo et al. (2002), and a subsequent study by Fasciglione et al. (2016), the seabed in front of the former brownfield and steel in dustrial pole (Fig. 1) is characterized to a large extent by sediments (sand of volcanic origin and mud) with the sporadic presence of some topographically unspoiled rocky outcrop, and by man-made structures
Fig. 1. Map of the study area of the Gulf of Pozzuoli. The area boxed with the line is strictly the SNI zone, included within the Pozzuoli Gulf and the Gulf of Naples. The Pozzuoli town and the Gaiola MPA and Cape Posillipo are also indicated. 2
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like docks, piers, and bridges along the coast. The actual rocky bottoms are limited to the islet of Nisida and its small internal bay named Porto Paone, and also to the small promontory called “La Pietra” (“the Stone”) up to the pier of the port of Pozzuoli-Rione Terra. Recent information on the geomorphological characteristics of the study area can be found in the cartography and morphometric analysis of the Bay of Pozzuoli (Somma et al., 2016). A Geological Map of Italy produced by the Cam pania Region Geological Service (Fedele et al., 2017) is also available and provides a detailed view on the geomorphological characteristics of the sea bottom in front of the islet of Nisida.
were produced based on the historical mapping by Funk (1927), rein terpreted by Puri et al. (1964) and Colantoni et al. (1982), and by Parenzan (1956) on Zosteracee; data (not georeferenced) were digitized and geo-referenced, to EPSG 4326: WGS 84 reference system utilizing QGIS v.2.18.15 and Google Earth Pro. The MATTM map (2004) was the only source already available as GIS file. Bionomic habitat maps from Casola et al. (2005) and Gamulin-Brida (1965) of Porto Paone (Nisida) hard bottoms were also acquired from printed material and digitized and geo-referenced with the same afore mentioned program. No habitat maps were available for the pre-industrial period (prior 1910).
3. Materials and methods
4. Results
A review of the relevant information available at the library of the Stazione Zoologica Anton Dohrn in Naples (SZN) was conducted, focusing on zoobenthic invertebrates and benthic habitats. This encompassed monographs of the Fauna and Flora of the Gulf of Naples, summarized by Lo Bianco (1909), activity report of the SZN, database of the SZN zoological collection, datasheets of the Archive Moncharmont (Archivio Moncharmont, 1965-1985; Gambi et al., 2013), and scientific literature on general studies conducted within the Gulf of Naples including data from the study area. Ancillary information was retrieved from the library of the University of Naples Federico II, and by consul ting iconographic sources at the SZN historical archive (historical cartography, photographic material, watercolors) as well as recent cartography (CARG-Campania Region documents and geomorpholog ical maps from CNR-ISMAR; Fedele et al., 2017). This compilation allowed to summarize sources written in different languages (mainly Italian, German and French) and give a synthetic access to this hidden literature to a wider audience. The benthic taxa which represent habitat formers and engineering species, as well as species of high natural heritage value were grouped, and their diversity and distribution patterns in the studied area checked in order to highlight possible pattern in space and/or time. The following groups of habitat formers were considered: tubicoulous polychaetes (sabellids, serpulids and other tube formers in softbottoms), encrusting cirripeds, anthozoans, molluscs (bivalves including some perforators and vermetids), bryozoans, porifers (massive and arborescent), and tunicates (solitary ascidians). Seagrasses (Pos idonia oceanica and Cymodocea nodosa) were also considered during the data gathering process. A database was compiled from data obtained through bibliographic source and updated for taxonomic classification according to WORMS (2019). In order to highlight possible changes due to the presence of the brownfield, the data have been grouped in three time periods: PreIndustrial (from 1850 to 1910); Industrial (from 1911 to 1991); and Post-Industrial (from 1992 to present). The geographical information on species occurrence provided by the majority of the historical sources proved to be insufficient, in this case, coordinates were inferred by centering the locations indicated in the sources (e.g. Pozzuoli, Bagnoli, Nisida). As regards the available carthographic information on habitat, we decided to include in this contribution the maps realized before 1991 (end of the industrial activities in the Bagnoli-Coroglio SNI), since they are not easily available for the audience, with the exception of the soft–bottoms biocoenosis map of Casola et al. (2005); this represent the first available data on community distribution in sediment habitat of the Bagnoli area (the subsequent map by Fasciglione et al., 2016 mostly overlapping the former one was not considered). We also decided to include the most recent map of the seagrasses, performed in 2002–2003 by Ministry of the Environment (MATTM, 2004), since this map was not available in the literature. Finally, the presence of P. oceanica remains in the cores of the study by Gabellini et al. (2005) were mapped over the biocoenoses map by Casola et al. (2005), to overlap sediment type s/biocoenoses with evidence of possible ancient occurrence of Posidonia in the area. Distribution maps of seagrasses (P. oceanica and C .nodosa)
The number of scientific studies carried out in the study area since the end of the nineteenth century indicates its high ecological relevance. Useful data and information on the study area were found in 67 sources (see Table S2) out of more than 250 sources consulted. Available in formation was very heterogeneous both qualitatively and quantitatively. Detailed geographic information, as well as habitat and depth, was generally lacking beyond generic toponyms in most of the species re cords. In addition, most of the papers, especially those focused on tax onomy, only report qualitative data and could be considered for the occurrence of the species only. Overall, for the considered extended area (From Capo Posillipo- Gaiola to Capo Miseno and the entire Gulf of Pozzuoli) and the three periods considered, 813 macro-benthic organ isms were recorded, for a total of 1006 records; 148 species are reported for the pre-industrial period, 361 for the industrial period, 381 for the post-industrial one (see Table S1 in Supplementary material). The following Phyla were recorded: Porifera, Cnidaria, Annelida, Nermertea, Plathelminthes, Mollusca, Arthropoda (Crustacea, Picnogonida), Bryo zoa, Echinodermata, Tunicata and Chordata. Most of the groups and benthic organisms reported were macrobenthic taxa. However, a few papers dealing with meiofauna were also considered (Bürger, 1895; Chappuis, 1938; Boaden, 1965; Polese et al., 2018). Comparing the three time periods in the whole record, there is a poor correspondence of species among across time in the study area: 27 species were common between the pre-industrial and the industrial periods; 9 between the pre-industrial and post-industrial periods, and 41 between the industrial and post-industrial period. There were not species in common to all the three considered periods. 4.1. Habitat formers A total of 109 habitat-former species, plus two engineering sea grasses were recorded. Among habitat formers the list includes con spicuous species, rare, and of high ecological relevance, such as the sponges Geodia cydonium (abundant at the Fumosa bank off Baia) (Saggiomo and Petrillo, 2008), Calyx nicaensis (reported in a cave at Capo Miseno), and Axinella spp. (along the Nisida islet). Some species are typical of the Coralligenous habitat such as the gorgonians Eunicella spp. and Paramuricea clavata, as well as the scleractinia Astroides caly cularis are reported along the Nisida rocky cliffs (Table S1) (Bacci, 1946), while the large bivalve Pinna nobilis is documented with only a few records associated to P. oceanica meadows, also within the Paone harbor (Nisida island). It is worth noting the occurrence of a highly diversified ascidian fauna composed of solitary species, which probably constituted a facies in the deepest soft bottoms of the Pozzuoli Bay (Salfi, 1931, and several records in the Archive Moncharmont 1965–1985). Such formations were never documented during the post-industrial period. Instead, tubicolous polychates (such as, Owenia fusiformis, several Sabellidae and Terebellidae) were recorded as the habitat for mers in soft bottoms during post-industrial period (Bioservice Report, 2003; Casola et al., 2005).
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4.2. Alien species
were inhabited by arpacticoid copepod Trigriopus fulvus (reported as Harpacticus fulvus), and the decapod Pachygrapsus marmoratus. In the midlittoral zone (the area defined between low and high tide) there were abundant barnacles of the species Chtamalus stellatus, the gastropods Patella rustica (reported as P. lusitanica), Patella aspera, Phorcus turbinatus (reported as Monodonta turbinata) the chiton Leprochitona caprearum (reported as Middeldorfia caprearum), the anemone Actinia equina, and the crab P. marmoratus and Eriphia verrucosa (reported as E. spinifrons). At the entrance of the bay, small specimens of Mytilus galloprovincialis and Mytilaster minimus (reported as Brachyodontes minimus) were observed. In the infralittoral zone, photophilic algae were dominant, among them a facies of Dictyopteris membranacea, and other common species such as Dictyota dichotoma, and the brown seaweed Cystoseira abrotanifolia. Among the invertebrates, ophiurans resulted abundant, and other species, such as the anemone Anemonia viridis (reported as A. sulcata), the starfishes Coscinasteria tenuispina and Martasterias gla cialis and the sea urchin Paracentrotus lividus were also present. Sponges, such as Spongia officinalis and Petrosia ficiformis were also common. Among the photophilic algae, nitrophilic algae, (i.e. indicators of organic enrichment), were also observed, especially Ulva rigida (indi cated as U. lactuca), and the brown alga Hypnea musciformis. Some “enclaves” (inclusions) of species typical of the pre-Coralligenous and Coralligenous habitats were also present in the shaded areas favoring sciaphilous organisms, such as the macroalgae Halimeda tuna, Flabellia petiolata (reported as Udotea petiolata) several species of Peyssonnelia spp. However, the coralligenous community and habitat was not actu ally present. The cnidarian Cornularia cornucopiae, ascidians such as Halocynthia papillosa and Microcosmus sulcatus were also present. The seafloor of Porto Paone was also characterized by soft bottom biocoenoses and seagrasses (see below). As regard the distribution of hard bottom biocoenoses for the postindustrial period, some information was obtained from the cartog raphy produced both by Russo et al. (2005b) and Simeone et al. (2016) as part of a study carried out on behalf of the Gaiola Marine Protected Area. The cartography also involved the external coasts of Nisida, which showed infralittoral photophilic algae, and limited outcrops of cor alligenous assemblages (gorgonians, sponges, bryozoans).
In our dataset only three alien invertebrate species occurred in the considered area: the two sabellid polychaetes Branchiomma luctuosum, B. boholense and the opistobranch mollusk Anteaeolidella cacaotica (re ported as Aeolidella takanosimensis) (Table 1S). The former two species are established while the latter is considered casual and never recorded after Schmekel (1968). No studies on their impact are available in the areas as well as in the entire Gulf of Naples. The few other conspicuous alien species in the area are macroalgae, outside the scope of our work. However, among them only Caulerpa cylindracea and Asparagopsis armata are reported to have an invasive habit in the area (Buia et al., 2001; Papa and Russo, 2010) and may have a potential impact on the local communities, although no studies are available on this subject. 4.3. Hard bottoms The major source of information on hard bottoms, which covers the whole study area during the industrial period, was the monograph by Funk (1927) focusing on marine macrophytes. This work also summa rizes previous historical works and provides the first distribution of P. oceanica meadows. The most conspicuous hard bottom zone is the Nisida island and its inlet Porto Paone, which is the crater of the ancient vol canic edifice. Porto Paone, despite its limited extension and depth, held a complex mosaic of biocoenoses (photophilic algae, nitrophilous algae, C. nodosa, P. oceanica meadow, soft bottoms, precoralligenous and coralligenous (Fig. 2) and a remarkable benthic biodiversity (140 spe cies Gamulin-Brida, 1965; Table S1). The paper by Gamulin-Brida (1965, in French) accounted for a detailed list of organism and com munities, and also represents an ante-litteram example of application of SCUBA diving visual census techniques. The Porto Paone inlet has a maximum length and a width of 225 m and 185 m, respectively, and a maximum depth of 15 m. The above mentioned author divided the area into 8 sectors to take into account the ecological differences in light exposure, and the differences with respect to the connection with the open sea. Among the hard bottom biocoenoses the work listed those typical of supralittoral rock, characterized by Littorina neritoides, Ligia italica and Chtamalus depressus. Some “reef pools” with variable salinity
Fig. 2. Distribution of benthic biocenoses within Porto Paone (Nisida islet) (georeferenced after Gamulin-Brida, 1965). 4
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Biocoenosis of muddy sands in calm areas (SVMC) constituted the most extensive habitat of the MPA, down to 15 m. The SVMC biocenosis appeared enriched with fragments from submerged Roman artefacts and exoskeletons of benthic organisms, and presented elements of the SGCF biocenosis (sands and gravels under the influence of bottom currents), and elements of the SFBC biocoenosis (well calibrated fine sand) near the Lucrino lake. The soft bottoms were covered by the green alga C. prolifera mixed with the alien congeneric C. cylindracea. Meadows and semi-prairies of C. nodosa, mixed with the SVMC and SFBC biocoenoses, were mainly observed in the area in front of Lake Lucrino, between 3 and 7 m depth.
4.4. Soft-bottoms Information on macrozoobenthic fauna from soft bottom habitats were available in Gamulin-Brida (1965), which highlighted the presence of sandy bottoms about 20 m from the rocky cliff. Beyond that distance, soft bottoms patches appeared mixed with vegetated ones dominated by either P. oceanica and C. nodosa seagrasses with peculiar associated communities. Following the classification of Bellan-Santini et al. (1994), the part of the bottom between fine sediments and the rocky cliff was characterized by the biocoenosis of sand and gravel under the influence of the bottom currents (SGCF). The large bivalve Pinna nobilis was here documented in the channels among patches of P. oceanica. Data on benthic populations and biocoenosis associated with soft bottoms during the post-industrial period was provided by the Bioservice Report (2003) and summarized in Casola et al. (2005) (Fig. 3). In such work, 307 taxa and five biocoenoses were identified: i) the biocoenosis of well-calibrated fine sands (SFBC), which extends along the coastal strip between Lido delle Sirene and Bagnoli at depths between 3 and 8 m; ii) the biocenosis of muddy sands of calm fashion (SVMC), in the superficial area between the “Lido delle Sirene” and the isthmus connecting Coro glio to the island of Nisida at less than 5 m depth; iii) the biocoenosis of coastal debris (DC) between 25 and 40 m depth; iv) the biocenosis of coastal terrigenous mud (VTC), at 50 m depth; v) a transition ecotonal assemblage localized between the SFBC and the DC biocoenoses char acterized by the coexistence of species typical of the surrounding bio coenoses. Furthermore, the seagrass C. nodosa appeared interspersed with the green alga Caulerpa prolifera in correspondence of the SVMC biocoenosis. This community/biocoenosis characterization and species composition was confirmed by subsequent survey carried out on the area in 2005 and summarized in Fasciglione et al. (2016). A characterization of the habitat of the submerged Park of the Baia MPA was also available (Russo et al., 2005a, 2008). The area is largely characterized by a mosaic of patches of soft bottoms and submerged archaeological remains of Roman origin. The occurring biocoenoses were photophilous algae (AP), which was present on the top of sub merged Roman ruins, while sciophilous populations were observed in the cavities and more shaded walls within the same structures.
4.5. Seagrasses and their habitat Information on occurrence and distribution of seagrasses, mainly P . oceanica, in the study area was available in the monumental work by Funk (1927), in his compendium on marine macrophytes. Collection was based on direct sampling on hard bottoms and dredge sampling for seagrasses, and other plant formations, indicated by the author as fibrous and calcareous algae (Fig. 4). This map is not well referenced in space, and sampling locations were originally figured as individual points (Table II in Funk, 1927). These points were extrapolated as a map by Puri et al. (1964) and later redrawn by Colantoni et al. (1982). We integrated all these information in Fig. 4, including the macroalgl dis tribution, in consideration of their important role as habitat former and their potential role in structuring the local fauna. P. oceanica extended from the outer side of the islet of Nisida facing Capo Posillipo to the sea bottom between Capo Posillipo and Gaiola. While the calcareous algae reported, probably correspond to the coralline beds later reported in the Gulf of Pozzuoli by other authors. The fibrous algae indicated by Funk (1927) probably were conspicuous erect and arborescent algae, perhaps Fucales or Sargassaceae, observed in both historical and recent times in the same zone (Buia et al., 2013) (Fig. 4). A first quantification of the extent of seagrasses (Zosteracee) was provided by Parenzan (1956), who estimated that Zosteracee (mainly P. oceanica) covered 2106 square meters in the area between Capo Miseno and Nisida (Fig. 4). P. oceanica occurred within the SNI north to
Fig. 3. Distribution of benthos sampling stations on soft bottom inside the SNI of Bagnoli and benthic biocenosis (revised and georeferenced after Casola et al., 2005). 5
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Fig. 4. Georeferenced re-elaboration of Posidonia oceanica distribution and other macrophytes, according to Funk (1927) e elaborated by Puri et al. (1964); and distribution of Zosteracee (mainly Posidonia oceanica) from Parenzan (1956).
the piers, up to the external pier of the Pozzuoli harbour, in front of Porto Paone, and in the outer side of Nisida and Capo Posillipo (Fig. 4). It is also worth to mention that Parenzan (1956) listed Zostera marina among seagrasses, but this species was never recorded in subsequent surveys. It could be hypothesized that this record of Z. marina could in fact refer to C. nodosa, which is very common in the zone. Also, in the survey of Parenzan (1956), sampling was carried out indirectly by dredging, and spatial distribution was not well referenced. Therefore,
comparisons of the seagrass maps by Funk (1927) and Parenzan (1956) with the more recent geo-referenced map by MATTM (2004) should be done with caution. The distribution of seagrasses was also studied in the aforementioned work of Gamulin-Brida (1965) inside Porto Paone, reporting large part of the inlet as colonized by P. oceanica and C. nodosa, mixed with rocky outcrops covered by photophilic algae and patches of unvegetated sediment. P. oceanica was then present mainly in the southern part of
Fig. 5. Elaboration of the mapping of seagrasses (Posidonia oceanica and Cymodocea nodosa) performed in the period 2002–2004 on the Campanian coast, and relative to the Gulf of Pozzuoli (MATTM, 2004). 6
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communities and habitats, thereby providing a reference baseline for defining restoration objectives. As expected from a historical dataset, all the historical information, except some of the most recent works, lacked quantitative data and precise geographical references. As a result, the pattern of distribution of the majority of the species appeared frag mentary both in space and time. However, combining different infor mation sources reduced uncertainty and allowed to track a relevant pattern of change in distribution over time for some species (e.g., seagrasses). From an historical point of view, considering the huge dataset collected, spanning from mid-1800 to present time, we attempted to compare the data according to the industrial activity in the area. How ever, the fact that few species were contemporary present during the three periods considered, and that there were no studies on community and habitat mapping in the pre-industrial period, did not allow to relate and quantify temporal changes in biodiversity or in habitat distribution, except, to some extent, for the seagrasses. The biodiversity recorded in the period prior the industrialization of Bagnoli (prior 1911; 148 spe cies) suffered from an evident bias linked to a minor number of studies and therefore relatively weak sampling effort. This is evident if compared with the diversity observed during the industrial period (1911–1991; 361 species), with benthic fauna almost doubled and a modest overlapping of species with the previous period (27 species in common) probably due to a larger number of studies in respect to the past. In fact, the industrial period coincided with and intense and pro ductive periods of marine research, especially held by the Stazione Zoologica of Naples, and mainly focused on taxonomy, faunistic and first ecological surveys, due to eminent zoologists, such as Bacci, Salfi, Sar� a, Cognetti, Ryland, Tortonese, Parenzan, and Moncharmont. The postindustrial period is characterized by research weakly focused on tax onomy, but more oriented on ecology, with large scale survey and georeferenced mapping, including investigations aimed at evaluating anthropogenic impacts. Although the species recorded in this last period is the highest of the whole data set (381), it only shares 41 species with the industrial period and 9 with the pre-industrial one. In addition, the majority of species of the recent period (over 300) were recorded in two surveys on the soft-bottoms (Bioservice Report, 2003; Casola et al.,
Porto Paone between 5 and 6 m depth, and a detailed list of epiphytic and motile organisms associated to the leaf canopy was provided by this author (see Table 1S). During the post-industrial period, C. nodosa was reported for the areas located northwest of the bay of Porto Paone, where the sediment contained the largest proportion of organic matter and mud. Russo et al. (2005a, 2008) reported C. nodosa extent, as well as isolated patches of P. oceanica, in front of the Baia MPA, such as off Lake Lucrino and opposite to Punta Epitaffio. The map of distribution of seagrasses in Campania and Calabria re gions (MATTM, 2004) (Fig. 5) shows the distribution of both C. nodosa, and P. oceanica mixed with C. nodosa, limited to the west slope of the promontory of Capo Miseno up to Bacoli. In addition, there were some isolated patches of P. oceanica and C. nodosa in the innermost portion of the Gulf of Pozzuoli between 25 and 30 m depth. A mosaic of P. oceanica and dead matte has been found deeper between 30 and 35 m in front of the islet of Nisida. Finally, the sampling sites described of Gabellini et al. (2005) were georeferenced and plotted. The resulting map (Fig. 6), based on sediment cores and grabs, revealed the occurrence of P. oceanica rhizomes and residues of dead matte in the sediment from the southernmost portion of the SNI, as well as along the rocky coasts of the northern side, and near the port of Nisida. 5. Discussion The study area here considered, which encompassed the BagnoliCoroglio SNI and adjacent zones (Gulf of Pozzuoli), is one of the best known in the Gulf of Naples due most likely to its accessibility, long tradition for bathing and hydrothermal facilities, and transformation in one of the main sites of industrial development in Italy. Here it is re ported the occurrence of 813 species, for a total of 1006 records, in the SNI and its neighborhoods during three periods of time roughly span ning 160 years. The area represents also the best known within the Gulf of Naples and with the highest biodiversity also for the macrophytes (macroalgae and seagrasses) (Funk, 1927; Buia et al., 2013). The synthesis of species and habitats here presented provides a synoptic view of the biodiversity, and the distribution of benthic
Fig. 6. Distribution of Posidonia oceanica in core sample stations on soft bottom inside the SNI of Bagnoli (after Gabellini et al., 2005), superimposed on the benthic soft-bottom biocenoses (after Casola et al., 2005). 7
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2005; Fasciglione et al., 2016). Therefore, the taxonomic diversity and information amongst the three periods is not homogeneous. Based on the present dataset it is not possible to highlight any difference in the pattern of biodiversity or the distribution of individual species and habitats along the considered period of time and its possible relationship with industrial activity and impact on the area. Therefore, we suspect that the intrinsic limits of the historical information here reported, could be the same for other areas of the Gulf of Naples, which account for similar amount and quality of historical information. Such information may have a strong potential, but it can suffer from the same constraints herein observed when compared with more recent data. However, the majority of the species (especially those from hard bottoms and P. oceanica meadows) occurs at the Nisida islet and inside Porto Paone probably due to the complex geomorphology of the area. Moreover, Nisida and Posillipo Cape represented two of the main areas for sam pling and collection of marine organisms, as documented in the SZN Zoological Collection and the Archive Moncharmont (1965-1985). The presence of the penitentiary institute in the Nisida islet, and the conse quent restricted access to this area since the early 1800s, probably favored the maintenance of nearly pristine conditions at Porto Paone, which was characterized by a complex mosaics of different habitat patches, as documented by Gamulin-Brida in 1965 (see Fig. 2). This area deserves special attention and it should be further surveyed in order to better understand the temporal dynamics of biodiversity in the SNI. Such an area, as well as the external Nisida cliffs, might be considered suitable as donor sites for future restoration initiatives within the SNI. In fact, the maps reported in this work might be valuable benchmarks for assessing the restoration success in the area, especially those produced for soft-bottoms fauna and communities, which are very accurate and useful for future assessment of these habitats (Casola et al., 2005; Fas ciglione et al., 2016). The historical maps of distribution of P. oceanica and C. nodosa meadows should be considered with caution. However, they help to visualize the progressive reduction of the overall covering of meadows from larger and continuous areas documented by Funk (1927) and Parenzan (1956), to smaller, more fragmented patches in the most recent period (MATTM, 2004) and mostly observed outside the SNI area, albeit remains of P. oceanica dead matt inside the sediment cores sampled within the SNI (Gabellini et al., 2005), suggest that P. oceanica was probably present also within the SNI. It is plausible that the overall reduction and fragmentation of seagrass cover, resulted from a suite of different human impacts, including the industrial pollution (e.g., coastal reclamation and development, organic pollution, fishing, anchoring, etc.). In fact, multiple human impact on benthic habitats was recently detected in the area (Bertocci et al., 2019), albeit shallow hard bottom communities appeared resilient and therefore adapted to the harsh local conditions (Pellecchia et al., 2020). In conclusion, this synthesis highlights that the impacted SNI area hosted a diversified zoobenthic fauna and a complex mosaic of different coastal habitat (seagrasses, shallow and deepwater hard bottoms, a va riety of soft bottom habitats). In case of rehabilitation of the area with dredging of contaminated sediments and cessation of additional forms of human impact, the remnant populations of ecologically relevant or ganisms (sponges, gorgonians, scleractinians, bryozoans and molluscs, and seagrasses) of this or neighboring areas might still have the potential to became donor populations for the restoration measures.
list of the species with additional information on their records, shape files of the GIS maps). Ethical approval No use of animals or plants were included in this paper based entirely on a literature synthesis. Declaration of competing interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. Acknowledgements We are grateful to Dr. Claudia Di Somma and all the library staff of the SZN for their help and collaboration in consulting the historical literature as well as other historical documents related to the study area. MG was supported by a fellowship provided by the SZN. This study was supported by the project ABBaCo funded by the Italian Ministry for Education, University and Research (grant number C62F16000170001). Appendix A. Supplementary data Supplementary data to this article can be found online at https://doi. org/10.1016/j.marenvres.2020.104925. References Archive Moncharmont, 1965-1985. Archive (More than 5,000 Paper Sheets) Complite by Prof. Ugo Moncharmont when Was Hired as Responsible of the Zoology Dept. Of the Stazione Zoologica, and Acquired in Digital Form by the Library and Public Archive of the Stazione Zoologica in Naples (see Gambi et al., 2013). Bacci, G., 1946. Ricerche sulle zoocenosi bentoniche del Golfo di Napoli. I La secca di Benda Palummo. Pubblicazioni della Stazione Zool. Napoli 20 (2), 158–178. Boaden, P.J., 1965. Interstitial fauna from Porto Paone. Pubblicazioni della Stazione Zool. Napoli 34 (2), 235–239. Bürger, O., 1895. Die Nemertinen des Golfes von Neapel und der Angrenzenden MeeresAbschnitte. Monographie Fauna und Flora des Golfes von Neapel, vol. 22. Bellan-Santini, D., Lacaze, J.-C., Poizat, C., 1994. Les biocenoses marines et littorales de Mediterran�ee. Synth� ese, menaces et perspectives. Museum National Histoire Naturelle Paris. Collection Patrimoines Nat. 19, 1–246. Bertocci, I., Dell’Anno, A., Musco, L., Gambi, C., Saggiomo, V., Cannavacciuolo, M., Lo Martire, M., Passarelli, A., Zazo, G., Danovaro, R., 2019. Multiple human pressures in coastal habitats: variation of meiofaunal assemblages associated with sewage discharge in a post-industrial area. Sci. Total Environ. 655, 1218–1231. Bioservice Report, 2003. Rapporto finale di Attivit� a “Analisi dei popolamenti macrozoobentonici di fondo mobile ai fini della definizione di un quadro di riferimento per le valutazioni di impatto ambientale nelle aree marine costiere (Regione Campania rif. 170/97). Buia, M.C., Gambi, M.C., Terlizzi, A., Mazzella, L., 2001. Colonization of C. racemosa along the southern Italian coast: I. distribution, phenological variability and ecological role. In: Gravez, V., Ruitton, S., Boudouresque, C.F., Le Direac’h, L., Meinesz, A., Scabbia, G., Verlaque, M. (Eds.), Proceedings of the Fourth International Workshop on Caulerpa Taxifolia, Marseille, France, pp. 352–360. Buia, M.C., Chiarore, A., Mulas, M., Porzio, L., 2013. Historical changes in algal diversity in the Gulf of Naples. In: Ozhan, E. (Ed.), MEDCOAST Proceedings, Marmaris Turkey, 30 October- 3 November 2013, pp. 837–846. Casola, E., Lanera, P., Magnifico, G., Plastina, N., Scardi, M., Valiante, L.M., Vinci, D., 2005. Carta bionomica dei fondali antistanti l’ex stabilimento siderurgico Italsider (Bagnoli, Napoli). Biol. Mar. Mediterr. 12 (1), 244–247. Chappuis, P.A., 1938. Sub e Hanpacticoiden aus sud-Italien. Bull. Soc. Sci. Cluj 9, 153–181. Chiarore, A., Musco, L., Bertocci, I., Gallo, A., Cannavacciuolo, A., mutalipassi, M., Caramiello, D., Giomi, F., Fusi, M., Danovaro, R., Munari, M., 2020. Sea urchin chronicles. The effect of oxygen super-saturation and marine polluted sediments from Bagnoli-Coroglio Bay on different life stages of the sea urchin Paracentrotus lividus. Mar. Environ. Res. (this issue). Colantoni, P., Gallignani, P., Fresi, E., Cinelli, F., 1982. Patterns of Posidonia oceanica (L.) Delile beds around the island of Ischia (Gulf of Naples) and adjacent waters. Mar. Ecol. 3 (1), 53–74. Coll, M., Piroddi, C., Albouy, C., Ben Rais Lasram, F., Cheung, W.W.L., et al., 2011. The Mediterranean Sea under siege: spatial overlap between marine biodiversity, cumulative threats and marine reserves. Global Ecol. Biogeogr. 21 (4), 465–480. De Pippo, T., Donadio, C., Pennetta, M., Terlizzi, F., Valente, A., Vecchione, C., Vegliante, M., 2002. Seabed morphology and pollution along the Bagnoli coast
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