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Marine Pollution Bulletin 202 (2024) 116389 Available online 26 April 2024 0025-326X/© 2024 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/). Plasticlusters: A marine litter microhabitat in a marina of Tunisia, N Africa Juan Sempere-Valverde a , b , c , * , Pablo Saenz-Arias a , Anastasiia Martynova b , c , d , Ons Benzarti e , f , Ramla Bouhlel e , f , Carlos María L´ opez Fe de la Cuadra a , Jos´ e Manuel Guerra-García a , Sahar Chebaane g , h a Laboratorio de Biología Marina, Departamento de Zoología, Facultad de Biología, Universidad de Sevilla, Avda Reina Mercedes 6, 41012 Sevilla, Spain b Biological and Environmental Sciences and Engineering (BESE), King Abdullah University of Science and Technology (KAUST), Thuwal 23955-6900, Saudi Arabia c Red Sea Research Center (RSRC), King Abdullah University of Science and Technology (KAUST), Saudi Arabia d Computational Bioscience Research Center (CBRC), King Abdullah University of Science and Technology (KAUST), Saudi Arabia e Research Laboratory LR14ES06 “Bioresources: Integrative Biology and Valorization”, Higher Institute of Biotechnology of Monastir, Avenue Tahar Hadded, BP 74, 5000 Monastir, Tunisia f Association Notre Grand Bleu (NGB, NGO), Monastir, Tunisia g MARE - Marine and Environmental Sciences Centre/ARNET - Aquatic Research Network, Regional Agency for the Development of Research, Technology and Innovation (ARDITI), Funchal, Portugal h Faculdade de Ciˆ encias, Universidade de Lisboa, Campo Grande Ed. C1, 1700 Lisboa, Portugal ARTICLE INFO Keywords: Non-indigenous species Marinas Plastic debris Artificial habitat Floating substrata ABSTRACT Plastic debris is a significant and rapidly developing ecological issue in coastal marine ecosystems, especially in areas where it accumulates. This study introduces “plasticlusters”, a new form of floating debris agglomeration found in the Yasmine Hammamet marina (Tunisia, North-Africa), loosely attached to pontoon ropes around the water surface level. The analysis of two samples revealed that they were formed primarily by average 2.11 mm polystyrene fragments, 3.43 mm fibers, 104 mm polypropylene and polyethylene sheets, and 122 mm decomposing seagrass leaves. They were inhabited by several taxa, including at least 2 cryptogenic and 5 nonindigenous species (NIS). Unlike other plastic formations, plasticlusters provide a novel and potentially temporal microhabitat to fouling assemblages due to their loose and unconsolidated structure which, combined with marinas being NIS hubs, could enhance NIS dispersion. The results of this study raise concerns about the combined ecological effects of debris accumulation and biocontamination inside marinas. 1. Introduction Marine litter is one of the most important and rapidly developing global environmental issues, with the litter accumulated in the sea floor and surface being expected to double in the following decades (Ioakeimidis et al., 2017). Non-biodegradable plastics constitute a significant proportion of floating litter in oceans worldwide, with >90 % of marine litter items being plastic, although this percentage is reduced to <50 % in shallow coastal areas (Ioakeimidis et al., 2017). In the areas where litter accumulates, it interacts with the biota through physical and chemical processes and modifies the habitat characteristics. This can negatively impact native communities and favor the prevalence of tolerant and opportunistic species (Deudero and Alomar, 2015; Garcia- Vazquez et al., 2018; Shruti et al., 2023a). Therefore, it is important to describe, characterize, and catalogue these litter agglomerations, along with their impacts on marine communities to understand extent of this ecological phenomenon and as basis for developing management strategies. The persistence of plastic litter has led to an increase in rafting debris, which can be dispersed long distances through ocean currents and accumulate in oceanic gyres and marine basins, such as the Mediterranean Sea (Eriksen et al., 2014). Plastic litter can harbor a diverse array of marine biota, including microorganisms, seaweeds, and several invertebrate taxa, particularly sessile mollusks, bryozoans, crustaceans, annelids, and hydrozoans (P´ ovoa et al., 2021). In some cases, motile species have been reported to be attached to floating debris in association with the previously established sessile community (Bergmann et al., 2015). Therefore, plastic is an important dispersal vector for marine * Corresponding author at: Laboratorio de Biología Marina, Departamento de Zoología, Facultad de Biología, Universidad de Sevilla, Avda Reina Mercedes 6, 41012 Sevilla, Spain. E-mail address: [email protected] (J. Sempere-Valverde). Contents lists available at ScienceDirect Marine Pollution Bulletin journal homepage: www.elsevier.com/locate/marpolbul https://doi.org/10.1016/j.marpolbul.2024.116389 Received 15 January 2024; Received in revised form 12 April 2024; Accepted 15 April 2024
Marine Pollution Bulletin 202 (2024) 116389 2 non-indigenous species (NIS) across and within biogeographical regions, contributing to the phenomenon of marine bioinvasions (Astudillo et al., 2009; Bravo et al., 2011; Bergmann et al., 2015; Fernandez et al., 2022). Due to physical and chemical degradation processes, plastic debris can be a source of chemicals like polychlorinated biphenyls and bisphenol A, which can either leach into the environment or enter animal tissues when organisms, like grazers and filter feeders, ingest them (Sendra et al., 2021; Pitacco et al., 2022). These harmful substances can then magnify along the food web and induce physio-ecological effects, such as endocrine-disruption, reproductive disorders, increased risk of diseases or death (Derraik, 2002; Bergmann et al., 2015; De-la-Torre et al., 2021). These chemicals can also be transferred from macro-plastic items to the fouling assemblages inhabiting them, as has been observed in mussels inhabiting expanded polystyrene, which accumulate hexabromocyclododecanes (flame retardants) from the plastic substrates (Jang et al., 2016). Floating plastic litter is removed from the sea surface through various means, including stranding on shorelines, sinking into the depths, or being ingested by aquatic animals (Bergmann et al., 2015; Deudero and Alomar, 2015; Alomar et al., 2016). At the sea bottom, litter tends to accumulate in areas with low water circulation, as underwater canyons and caves (Pham et al., 2014; Bergmann et al., 2015). Plastic items can also be deposited with the sediment, be buried along shorelines, and incorporate in sedimentary composites, such as plastitones (Santos et al., 2022; Wang and Hou, 2023). These can be agglutinations of sediments, debris and melted or burned plastic addressed as plastiglomerates (Corcoran et al., 2014) and anthropoquinas (Fernandino et al., 2020). In rocky shorelines, plastic can adhere to rocks forming plasticrusts (Gestoso et al., 2019), bind with tar to form plastitar (Domínguez-Hern´ andez et al., 2022), and burn or melt, aggregating and forming pyroplastics (Turner et al., 2019). Moreover, plastic can interact with the benthic assemblages, where it can entangle and accumulate as plastisessiles (Ellrich et al., 2023a). Coastal ecosystems are among the most polluted areas in the marine environment, with the density of coastal marine litter being related to the distance of the nearest population center (Gabrielides et al., 1991). Among coastal habitats, artificial shorelines are often hotspots of marine litter and other forms of organic and inorganic pollution (Fernandez et al., 2022; Ros et al., 2023). For instance, artificial structures, such as breakwaters, can capture and accumulate marine litter and debris in the hollows among boulders (Aguilera et al., 2016, 2023; Masi´ a et al., 2021); and artificial materials, such as concrete and rusting metals, can incorporate and accumulate plastic debris, forming plasticoncretes and plastimetals (Ellrich et al., 2023a). Harbors, including ports and recreational marinas, are among the most polluted artificial coastal habitats, as they are generally associated to urban agglomerations and host intense and diverse human activities (Fernandez et al., 2022; Sempere-Valverde et al., 2023). Moreover, harbors often encapsulate water bodies, which reduces water renovation, concentrating and increasing pollutants prevalence (Masi´ a et al., 2021). Ultimately, these different forms of pollution contribute to shape the biological assemblages in harbor areas and contribute to increase biological pollution by favoring the prevalence of tolerant, opportunistic, and non-indigenous species (Fernandez et al., 2022; Ros et al., 2023). Inside harbors, floating structures such as pontoons and buoys have a generally higher abundance and diversity of NIS than non-floating and soft substrata, which increases their prevalence and dispersal risk (Connell, 2000, 2001; Leclerc et al., 2019; Saenz-Arias et al., 2022; Sempere-Valverde et al., 2024). Structures such as ropes provide important additional settling surfaces deeper in the water column (Tempesti et al., 2023). Like the floating structures, ropes can support diverse communities with a significant biomass of ascidians and bryozoans, which are faunistic taxa that exhibit a high proportion of NIS in marinas (Lambert and Lambert, 1998; Mari´ c et al., 2017; Tempesti et al., 2023). In this context, this study aims to describe a new form of debris agglomeration entangled to the ropes of a marina in Tunisia (North Africa). We hypothesize that (1) these structures are composed by the agglomeration of low-density plastics and organic material, (2) serve as habitat for sessile and motile fouling organisms, and (3) can host NIS, which could be particularly concerning due to their potential to facilitate the spread of NIS and contribute to marine bioinvasions. By testing these hypotheses, we hope to contribute to the growing body of Fig. 1. A: Location of Yasmine Hammamet marina, in Tunisia, North Africa, indicating the weather stations at Enfidha/El Mhedba (E =36 ◦04 ′ 00.1”N, 10◦27 ′ 00.0 ″ E) and Kelibia (K =36◦51 ′ 00.0”N, 11◦04 ′ 59.9 ″ E), the area where the debris agglomerations were observed (A1) and the location in which samples were collected (S = 36◦22 ′ 20.2”N, 10◦32 ′ 40.8 ″ E). B: Picture of a debris agglomeration (plasticluster) as seen from the pontoons. J. Sempere-Valverde et al.
Marine Pollution Bulletin 202 (2024) 116389 3 knowledge on the ecological impacts of marine plastic pollution and provide valuable insights for policymakers, conservationists, and other stakeholders involved in the environmental management of marinas and other harbor areas. 2. Material and methods 2.1. Location of debris agglomerations The marina Yasmine Hammamet, operational since 2001, plays a significant role in the economic activity of the Gulf of Hammamet, which is under intense touristic and urbanization pressure. However, the structure has also promoted some environmental problems, such as algal biomass accumulation and increased erosion in nearby beaches (Hellal, 2009; Saïdi et al., 2022). Water temperature in this region varies from 10.3 to 29.8 ◦C and salinity ranges from 37.1 to 38.8 ‰. Inside the marina, these values range from 16.2 to 28.9 ◦C and 36.1 to 37.8 ‰, respectively (Elgharsalli et al., 2015 and references therein). The debris agglomerations under study were found within a 60 m radius in a relatively sheltered area inside the marina (Fig. 1A). They were loosely attached to ropes hanging from the marina’s floating pontoons at the water surface level (Fig. 1B), and were present on unused ropes in empty moorings, but absent from ropes hanging from boats or in use by moored boats (SC and JS-V Obs.). To better understand the water surface conditions that may have contributed to the formation of the agglomerations under study, we collected daily average wind speed and direction data from meteostat.ne t. This data was sourced from the weather stations at Enfidha/El Mhedba and Kelibia, situated 40 km southwest and 56 km north-northeast of Hammamet, respectively (see Fig. 1A). The selected timeframe was 8 weeks before the observation of the agglomerations. This timeframe was determined by considering previous studies on life history of Cheilostomatida bryozoans (time from recruitment until maturity, see Keough, 1986; Kvach et al., 2019 and references therein). which allowed us to Fig. 2. Characteristics of Plastic Particles Analyzed with FTIR from sample S1. S1_A and S1_B =Polypropylene Transparent Sheets; S1_C =Polystyrene White Expanded Foam Fragments. Polymers were identified using the Hummel Polymer Sample Library. J. Sempere-Valverde et al.
Marine Pollution Bulletin 202 (2024) 116389 4 Fig. 3. Characteristics of Plastic Particles Analyzed with FTIR from sample S2. S2_A =Polypropylene Transparent Sheet; S2_B =Polyethylene Transparent Sheets; S2_C =Polyethylene Transparent Sheets; S2_D =Polystyrene White Expanded Foam Fragments. Polymers were identified using the Hummel Polymer Sample Library, Aldrich Condensed Phase Sample Library and HR Nicolet Sampler Library. J. Sempere-Valverde et al.
Marine Pollution Bulletin 202 (2024) 116389 5 make a gross estimation of the studied agglomerations age. 2.2. Samples collection and processing The litter agglomerations were observed on August 21st, 2021, by a team of researchers (SC, RB, OB, and JS-V) during a non-indigenous species (NIS) survey conducted in the marina of Hammamet. Recognizing these structures as potential novel habitats, the team photographed the debris agglomerations and collected two samples (S1 and S2). Samples were collected by pulling out the ropes from the water and gently removing the material from the rope surface by hand. Samples were stored in ethanol 70 % for later examination. In the laboratory, samples were sieved through a 0.5 mm mesh to retain associated macrofauna and debris. Debris items were identified and classified into three distinct categories: regular and irregular white balls, threads and filaments (fibers), white and transparent films, and organic materials (seagrass leaves). Films and seagrass leaves were directly counted, while smaller items abundance (balls and fibers) was estimated under the stereoscope by counting the items present in a 20 ml subsample of the total sample volume. Items size was estimated by measuring the longest distance for a random selection of 20 items from each category. Fouling sessile and motile species were identified and quantified using magnification, optical microscopy, and Scanning Electron Microscopy, and with local literature and taxonomic guides for reference (e.g., Chabbi et al., 2010; Vieira et al., 2013; Del Pasqua et al., 2018; Chebaane et al., 2019; Temiz et al., 2023). 2.3. Plastic polymer analyses Random pieces of suspected plastics were placed in a glass petri dish and submerged in approximately 5 ml of 30 % H 2 O 2 . The samples were left at 60 ◦C overnight, extracted from the petri dish, rinsed with MilliQ water and left to dry at room temperature (25 ◦C). Polymer identification was performed using Nicolet iS10 Fourier Transform Infrared Spectroscopy (FTIR) in attenuated total reflection (ATR) mode. All spectra were collected in the 4000–600 cm −1 range at a resolution of 4 cm −1 with 16 scans per object. The acquired polymer spectra were identified using the OMNIC Spectra Library. 3. Results The loose aggregations of debris (plasticlusters) were found in late summer, after two months characterized by low wind speeds in the Table 1 Number of items found in each sample (S1 and S2), number of items to which maximum length was measured, and their average size in millimeters and standard deviation values. Count (S1) Count (S2) N measured Av. size [mm] (±SD) PS white fragments a >150 >400 20 2.11 (±1.01) Small fibers a >40 >100 20 3.43 (±3.10) PS and PP sheets 4 16 20 104 (±40.43) P. oceanica leaves 0 7 7 122 (±56.93) a The number of smaller items was estimated by counting items in a 20 ml subsample; PS =polystyrene; PP =polypropylene. Fig. 4. A: the plasticlusters described in this study were formed around ropes, at and above water level, and were composed by plastic fragments, sheets, fibers, organic biomass and fouling organisms; B: these formations were stratified, with plastic foams and fibers in the top area, and big plastic sheets, fibers and seagrass leaves directly below water. Cradoscrupocellaria bertholletii was found in the top area (C), while species such as Botrylloides cf. niger (D) and Symplegma brakenhielmi (E) were present under the water surface. J. Sempere-Valverde et al.
Marine Pollution Bulletin 202 (2024) 116389 6 studied region (Supplementary Fig. S1). During this period, prevalent daily averages ranged from 6 to 20 km/h and reached a maximum of 18 km/h in Kelibia and 30 km/h in Enfidha/El Mhedba by the second week of July. Eastward winds were prevalent in Enfidha/El Mhedba, within the Gulf of Hammamet, while the wind direction in the cape of Kelibia ranged from northwest to south-southeast. Plasticlusters were formed by an aggregation of debris and fouling biomass. Analyzed items, acquired polymer types and FTIR spectra are presented separately for sample S1 (Fig. 2) and S2 (Fig. 3). Large film- and sheet-like particles were identified as polypropylene (PP) and polyethylene (PE), while irregular sponge-like (foam) particles were all identified as polystyrene (PS). A few particles subjected to ATR-FTIR crumbled when pressed on the diamond ATR crystal and/or did not show any identifiable signal and therefore their spectra are not presented here. The inorganic material forming the plasticlusters was dominated by plastics (Table 1), with white PS fragments being the most abundant, and PE and PP sheets the biggest items. Plastics were accompanied with biogenic material, which were identified as the calcareous and noncalcareous tubes of Sedentaria, such as Ficopomatus enigmaticus (Fauvel, 1923) and Branchiomma bairdi (McIntosh, 1885), and decomposing seagrass leaves. The plasticlusters had a stratified composition with two different levels (Fig. 4A and B). Above the water level, white plastic fragments and fibers were covered by diatomaceous biofilm and entangled with filamentous algae and colonies of the branching bryozoan Cradoscrupocellaria bertholletii (Audouin, 1826) (Fig. 4C; Fig. 5). Just at and a few centimeters below the water level, the ropes were covered by relatively big transparent sheets, up to 20 cm in length, which were entangled with seagrass leaves. This stratum hosted the fouling ascidians Botrylloides cf. niger Herdman, 1886 and Symplegma brakenhielmi (Michaelsen, 1904) (Fig. 4D and E), and the Sedentaria Branchiomma bairdi (McIntosh, 1885). Further below the water level, the ropes of the marina were colonized by these and other fouling species, including bioconcretions of Schizoporella errata (Waters, 1878), ascidians such as Microcosmus squamiger Michaelsen, 1927 and Styela plicata (Lesueur, 1823), and the oyster Pinctada radiata (Leach, 1814). A total of 12 taxa were identified from samples, including at least 5 NIS and 2 cryptogenic species (Table 2). Samples had a total solid volume of 155 ml (S1) and 335 ml (S2), and hosted 6 and 8 sessile taxa, respectively. For the associated fauna, S1 hosted 4 individuals from 4 semi-sessile and motile taxa (0.026 ind./ml), and S2 hosted 21 individuals from 7 taxa (0.063 ind./ml). Filamentous algae, diatoms and spirorbids were present on the surface of the clusters material, and these were colonized by sponges, mytilids, calcareous polychaetes, branched bryozoans, and colonial ascidians (Fig. 4; Fig. 5). Polychaetes were Fig. 5. Scanning Electron Microscopy (SEM) pictures for the plasticlusters. A: Polystyrene Styrofoam® sphere (see this figure; Fig. 6); B: spirorbid shell on a fiber; C: Cradoscrupocellaria bertholletii zooidal chambers (ooecium with porous ectooecium was observed for some zooids); D: Sycon sp. sponge covered with diatoms; E: Amphora sp. and Nitzschia sp. diatom species on the surface of a 2 mm polystyrene particle. Table 2 List of sessile, semi-sessile and motile taxa and their presence-absence or abundance (X =Presence; Numbers =number of individuals; Blank =absence) in the plasticluster samples S1 (155 ml) and S2 (335 ml). Most sessile taxa were presented as presence-absence due to the impossibility of measuring their abundance or volume, as they were mostly fragmented or attached and merged to inorganic items. Non-indigenous species (NIS) and cryptogenic species are accompanied with superscript numbers to indicate the references used to determine their status. Taxa marked with asterisks were photographed with Scanning Electron Microscopy (see Fig. 4). Major taxa Sessile taxa Status S1 S2 Chlorophyta Green filamentous algae Unknown X X Bacillariophyceae Diatoms* Unknown X X Ceramiales Ceramium sp. Unknown X Leucosolenida Sycon sp.* Unknown 1 Sabellida Spirorbidae* Unknown X X Ficopomatus enigmaticus (Fauvel, 1923) NIS a 4 Cheilostomatida Cradoscrupocellaria bertholletii (Audouin, 1826)* Cryptogenic b, c X X Savignyella lafontii (Audouin, 1826) Cryptogenic d X Stolidobranchia Botrylloides cf. niger Herdman, 1886 Cryptogenic e X X Symplegma brakenhielmi (Michaelsen, 1904) NIS f,g X Order Semi-sessile and motile taxa Status S1 S2 Mytilida Juvenile of Mytilus sp. Unknown 1 3 Sabellida Branchiomma bairdi (McIntosh, 1885) NIS f,h 6 Phyllodocida Nereididae undet. Unknown 1 8 Syllidae undet. Unknown 1 1 Amphipoda Juvenile of Caprella scaura Templeton, 1836 NIS f,i 1 Elasmopus rapax A. Costa, 1853 Cryptogenic j, k 1 Isopoda Paranthura japonica Richardson, 1909 NIS f,l 1 Tanaidacea Chondrochelia savignyi (Kroyer, 1842) Cryptogenic m 1 a Png-Gonzalez et al. (2023). b Vieira et al. (2013). c Souto et al. (2023). d Lezzi et al. (2018). e Temiz et al. (2023). f Tempesti et al. (2020). g Ramos-Espl´ a et al. (2020). h Del Pasqua et al. (2018). i Chebaane et al. (2018). j Marchini and Cardeccia (2017). k Navarro-Barranco et al. (2023). l Marchini et al. (2014). m Since this species is widely distributed, its native area is still under discussion (WoRMS, 2024). J. Sempere-Valverde et al.
Marine Pollution Bulletin 202 (2024) 116389 7 relatively abundant at S2, including the semi-sessile NIS Branchiomma bairdi (McIntosh, 1885). Moreover, peracarids were found in both samples, including the NIS Caprella scaura Templeton, 1836 and Paranthura japonica Richardson, 1909. 4. Discussion This study introduces a novel form of clustered floating marine debris, with a distinct structure from those previously characterized in coastal areas (see Shruti et al., 2023b for review). First, the complex structures of plasticlusters, with hollows among their components, allow them to provide a more suitable habitats for fouling organisms than single debris items (Ros et al., 2020; Revanales et al., 2022). Moreover, their loose structure makes them temporary, as they could disaggregate under extreme weather events, such as storms, reducing their likelihood of incorporation into coastal sedimentary dynamics. The ecological implications of these factors include the potential dispersal of species inhabiting the structures, which could be particularly relevant in the case of non-indigenous species (NIS). Therefore, and despite the convenience of a unified plastic vocabulary to facilitate communication among scientists, resource managers, policymakers, and the public (Haram et al., 2020), we introduce the term “plasticlusters” to describe this new category of plasticene structures. We believe that plasticluster is particularly apt, as it refers to a relatively loose agglomeration or ‘cluster’ of items. Plasticlusters differentiate form other plastic formations, such as plastisessiles (Ellrich et al., 2023a), in that plasticlusters are formed as an accumulation of debris, mainly plastic, resulting in a habitat that was not previously present in the area. However, these are not overgrown by sessile fouling, so they are not consolidated with a primary substrate (e. g., rope surface or bedrock) by calcareous invertebrates, but rather colonized by them, which might increase the risk of NIS dispersal. Plasticlusters could be formed on different habitats and with different shapes, and the term could englobe clusters already described, such as litter accumulated in canyons and cavities at the sea bottom (Pham et al., 2014; Bergmann et al., 2015). It could also include floating debris clustered within encapsulated water masses, as it happens when wind accumulates debris in a sector within a marina for a certain period, so they might be colonized by resident species before disaggregating. Refer to Table 3 for a more detailed description of the currently plastic formations described in shoreline areas. The fouling organisms inhabiting the plasticlusters and the weather conditions preceding their detection suggest that the structure was formed by the accumulation of floating plastic debris over a period of weeks (see Fig. 6). Fibers and expanded polystyrene spheres (Styrofoam®) are among the most common meso- and microplastic items in the littoral areas of Tunisia (Abidli et al., 2018), and the clustering of floating debris is a common phenomenon inside ports and marinas, where debris is relatively abundant and can be accumulated by wind and currents (Campbell et al., 2017; Masi´ a et al., 2021; Sempere-Valverde et al., 2023). Plastics can be clustered by surface tension, entanglement, biological growth and binding substances, and these processes are likely to have taken place in the formation of the structures reported in this study. For instance, microplastics tend to coagulate with biogenic particles and aggregate in clusters, to which epiplastic biofilms can contribute by the secretion of extracellular polysaccharides (Michels et al., 2018; Schmitt-Jansen et al., 2022). Like expanded polystyrene, low-density polyethylene and polypropylene are less dense than seawater. As these floating plastics adhere to the plasticluster, surface tension and adsorbed organic substances might have contributed to the binding of items (Fig. 6A); and the growth of macro and microbenthic assemblages would contribute to strengthening the bond between plastic items and increase the uptake of particles (e.g., Fig. 6B). Finally, it is likely that the biggest items are incorporated in later stages, as the increase in size of the structure and the growth of fouling organisms would favor the entanglement of large sheets of plastic and seagrass leaves (Fig. 6C). Marinas are among the most invaded artificial coastal habitats at a Table 3 Comparison of shoreline plastic formations and references used to retrieve Description and Origin. Species dispersal capacity for each formation were determined by expanding De-la-Torre et al. (2021) criteria: taking into account the floatability of the formation (1 =yes; 0 =no), the capacity of the formation to be colonized by invertebrates (1 =yes; 0 =no), and the relative likelihood of the formation to disaggregate (2 =high; 1 =medium; 0 =low), we categorized the formations into three categories regarding their capacity for invertebrates dispersal: 4 =High; 3 and 2 =Medium; 1 =Low. References in table, De-la-Torre et al. (2021), Furukuma et al. (2022), and Ellrich et al. (2023b) were used to construct fouling composition and dispersal capacity columns. Blank cells =not recorded; PE =polyethylene. Plastic formation Description Origin Fouling taxa Dispersal Capacity Reference Plastiglomerate Geogenic analogues to conglomerates formed by agglutination of sediment, organic material, and molten plastic Plastic debris, burned or melted by the sun, act as cement for aggregates Medium Corcoran et al. (2014) Pyroplastic Amorphous matrix of burned plastic of relatively homogeneous color and with cracks and fractures, pits, and cavities Burned waste during campfires on the beach Serpulids (Spirobranchus triqueter), bryozoans (Electra pilosa) and mollusc eggs Medium Turner et al. (2019) Plasticrust Plastic debris encrusting the intertidal rocky surface Crash of potential packaging materials against rocks by the tidal hydrodynamics Littorinids (Tectarius striatus) Medium Gestoso et al. (2019) Anthropoquinas Sedimentary rocks that contain anthropogenic items, including plastic, cemented with biogenic and siliciclastic material Plastic debris acting as aggregates in sedimentary processes Low Fernandino et al. (2020) Plastitar An agglomerate of tar and mainly microplastics attached to the rock surface Arrival and accumulation of microplastics debris to the coast Medium Domínguez- Hern´ andez et al. (2022) Plastitone Agglutination almost entirely composed of molten plastic High heat conditions melt the plastic, which can fuse with other materials Medium Santos et al. (2022) Plasticoncrete Plastic hardened in concrete Introduction of PE fibres during the hardening of concrete Low Ellrich et al. (2023a) Plastimetal Plastic rusted with metal Plastic rusting with metal in rocky intertidal boulder fields Low Ellrich et al. (2023a) Plastisessiles Plastic attached to benthic substrates by sessile invertebrates Sessile invertebrates incorporating and overgrowing plastic into the benthic assemblages Oysters (Magallana gigas) and serpulids (S. triqueter) Medium Ellrich et al. (2023a) Plasticluster Relatively loose aggregation of plastic debris, forming a cluster over a period of time Plastic and debris clustered by weak forces and supporting biogenic growth Sessile and motile organisms (see Table 2) High Present study J. Sempere-Valverde et al.
Marine Pollution Bulletin 202 (2024) 116389 8 global scale, with floating substrata being characterized by their high NIS abundance (Connell, 2000; Leclerc et al., 2019; Giangrande et al., 2021; Sempere-Valverde et al., 2024). Similarly, plastics have been found to serve as substrata for a wide range of marine organisms, including diatoms, bryozoans, barnacles, ascidians and other invertebrates (Li et al., 2016; Reisser et al., 2014; Subías-Baratau et al., 2022; Tempesti et al., 2023). The plasticlusters in Yasmine Hammamet marina hosted a variety of sessile and motile NIS, including of Paranthura japonica, which is recorded here for the second in Tunisian waters after Tempesti et al. (2016). Plasticlusters had a complex structure at scales relevant to small motile crustaceans and polychaetes, which might have encountered organic resources within the clusters, as well as predation and desiccation refugia. This might be particularly relevant during prolonged emersion times (i.e., when ropes are manipulated). Furthermore, plasticluster composition, structure and volume could affect their colonization by fouling species and could have been responsible of the differences in species composition between the two samples examined. Therefore, further research is needed to understand the plasticlusters formation, colonization, and disaggregation processes inside marinas, and how these interact with fouling assemblages as the heterogeneity increases provided by the plasticlusters on the rope surfaces might not influence their overall species composition and structure (Tempesti et al., 2023). Floating polymers such as polyethylene (PE), polypropylene (PP) and polystyrene (PS) have a hydrophobic nature that can influence the settlement of sessile assemblages (Muthukumar et al., 2011; Pinochet et al., 2020) and promote the adsorption of organic pollutants and metals, increasing their environmental persistence (Thompson et al., 2009; Koelmans et al., 2013). This could affect the ecological performance of the assemblages in confined areas such as marinas. Among marine macro-organisms, benthic invertebrate assemblages may be particularly vulnerable to plastic-related pollution, which can contribute to reduced development, reproduction, growth, feeding and survival, particularly for filter feeders and motile scavengers (D’Alessandro et al., 2018; Messinetti et al., 2018; Naveira et al., 2021; Mason et al., 2022). 5. Conclusions Plasticlusters represent a novel habitat formed by the aggregation of marine debris inside marinas. They could provide relatively complex structures that might serve as microhabitats for sessile and motile NIS and vectors for their dispersion, as they have the risk of disaggregate into floating plastic items and spread (Campbell et al., 2017; Ibabe et al., 2020; Fernandez et al., 2022). However, this is the first study on plasticlusters and, given the low replication in this initial study, it will be important to continue describing, characterizing, cataloguing and monitoring plasticlusters in harbor areas. Further research is required to fully understand the implications of plasticlusters on fouling assemblages, the ecological consequences of plastic debris in coastal environments and their potential ecological effects in harbor areas. Nonetheless, this research highlights the need to account for plasticlusters during NIS monitoring inside marinas, and to promote management practices to reduce the formation of plasticlusters by regularly removing floating litter from marinas and other coastal habitats. Supplementary data to this article can be found online at https://doi. org/10.1016/j.marpolbul.2024.116389. Funding JSV was supported by a FPI Grant (PRE2018-086266) from Ministerio de Ciencia, Innovaci´ on y Universidades (Project CGL 2017-82739- P) co-financed by ERDF European Union and Agencia Estatal de Investigaci´ on, Gobierno de Espa˜ na. SC was financially supported by a predoctoral grant in the framework of the 2015 ARDITI Grant Programme Madeira 14-20 (Project M1420-09-5369-FSE-000002). This study has benefitted from a Grant for the Use of General Research Services (2022/00000255) by IV Plan Propio de Investigaci´ on y Transferencia de la Universidad de Sevilla. CRediT authorship contribution statement Juan Sempere-Valverde: Writing – original draft, Visualization, Resources, Methodology, Investigation, Funding acquisition, Data curation, Conceptualization. Pablo Saenz-Arias: Writing – review & editing, Validation, Investigation, Data curation. Anastasiia Martynova: Formal analysis, Investigation, Methodology, Software, Visualization. Ons Benzarti: Writing – review & editing, Investigation, Data curation. Ramla Bouhlel: Writing – review & editing, Investigation, Data curation. Carlos María L´ opez Fe de la Cuadra: Writing – review & editing, Validation, Resources. Jos´ e Manuel Guerra-García: Writing – review & editing, Validation, Supervision, Conceptualization. Sahar Chebaane: Writing – review & editing, Validation, Supervision, Resources, Project administration, Methodology, Investigation, Funding acquisition, Data curation, Conceptualization. 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. Fig. 6. Plasticluster agglomerations in the marina of Hammamet. A: Initial accumulation of plastic floating debris on a recently submerged rope, which has not yet been colonized by macrofouling species; B: Growth of fouling on rope surface and among litter (pictures inside and outside water), with a white arrow indicating a colony of Cradoscrupocellaria bertholletii that contributed to the agglomeration of plastics; C: Final stage (inside and outside water), with big sheets of plastic and seagrass leaves entangled under the polystyrene agglomeration area and colonized by filter-feeding organisms. J. Sempere-Valverde et al.
Marine Pollution Bulletin 202 (2024) 116389 9 Data availability Data is available in the article Acknowledgements We would like to thank Atef Ouerghi and the Regional Activity Center for Specially Protected Areas (RAC/SPA) for supporting the fieldwork of this study. We are also grateful to Adnen Kacem and Aziza Hadjhassine, from the Higher Institute of Biotechnology of Monastir, for their assistance in facilitating the processing of samples. Our thanks also extend to the authorities and the Capitainerie de Port Yasmine Hammamet for their help and for granting permission for sampling. Special thanks are due to the three anonymous reviewers for their comments and suggestions, which greatly helped to increase the quality and extent of this manuscript. References Abidli, S., Antunes, J.C., Ferreira, J.L., Lahbib, Y., Sobral, P., El Menif, N.T., 2018. Microplastics in sediments from the littoral zone of the north Tunisian coast (Mediterranean Sea). Estuar. Coast. Shelf Sci. 205, 1–9. 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