Larval Settlement on Marine Surfaces: The Role of Physico-Chemical Interactions

A special issue of Journal of Marine Science and Engineering (ISSN 2077-1312). This special issue belongs to the section "Marine Biology".

Deadline for manuscript submissions: closed (31 May 2022) | Viewed by 29799

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Guest Editor
Department of Biology, University of Padova, via Ugo Bassi 58/B, 35131 Padova, Italy
Interests: marine ecotoxicology; marine biofouling; antifouling systems; marine invertebrate immune system; comparative immunobiology; immunotoxicity; embryotoxicity; evolutionary biology of tunicates

Special Issue Information

Dear Colleagues,

The ecological succession of the fouling community in coastal marine ecosystems depends on interactions among organisms and hard substrate. The primary fouling is formed of organisms that settle mainly on virgin surfaces. The secondary fouling is represented by organisms that need fouling for their settlement and growth. In all cases, there is a very close relationship between larval settlement and type of substrate.

In this Special Issue, I call for reviews and original research papers that pay attention to various aspects of the evaluation of marine larval settlement on both natural and artificial surfaces, pro-fouling and anti-fouling systems enclosed, with the growing interest in eco-engineering for coastal ecosystem preservation.

Results on inter- and intraspecific competition for substrate; the dominance of invasive species; the effects of color, roughness, wettability, hydrophilicity, oleophilicity, and nanostructure of the substrate; tolerance to repellent substances; and the morphology of adhesive structures are welcome.

Assoc. Prof. Francesca Cima
Guest Editor

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Keywords

  • Larval settlement
  • Hard-substrate community
  • Biofouling
  • Marine invertebrates
  • Substratum preference
  • Artificial surfaces
  • Invasive species selection

Published Papers (13 papers)

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Editorial

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3 pages, 185 KiB  
Editorial
Larval Settlement on Marine Surfaces: The Role of Physico-Chemical Interactions
by Francesca Cima
J. Mar. Sci. Eng. 2023, 11(4), 859; https://doi.org/10.3390/jmse11040859 - 19 Apr 2023
Viewed by 699
Abstract
Biofouling is the association of sessile aquatic organisms that rapidly settle on artificial hard substrata, thereby posing a large problem worldwide since its growth often causes severe damage to submerged structures [...] Full article

Research

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20 pages, 5330 KiB  
Article
Searching for the Origin and the Differentiation of Haemocytes before and after Larval Settlement of the Colonial Ascidian Botryllus schlosseri: An Ultrastructural Viewpoint
by Francesca Cima
J. Mar. Sci. Eng. 2022, 10(7), 987; https://doi.org/10.3390/jmse10070987 - 19 Jul 2022
Cited by 4 | Viewed by 1669 | Correction
Abstract
The colonial ascidian Botryllus schlosseri possesses an innate immunity, which plays fundamental roles in its survival, adaptability, worldwide spread and ecological success. Three lines of differentiation pathways of circulating haemocytes are known to be present in the haemolymph, starting from undifferentiated haemoblasts: (i) [...] Read more.
The colonial ascidian Botryllus schlosseri possesses an innate immunity, which plays fundamental roles in its survival, adaptability, worldwide spread and ecological success. Three lines of differentiation pathways of circulating haemocytes are known to be present in the haemolymph, starting from undifferentiated haemoblasts: (i) the phagocytic line (hyaline amoebocytes and macrophage-like cells), (ii) the cytotoxic line (granular amoebocytes and morula cells) and (iii) the storage cell line (pigment cells and nephrocytes). Many questions remain about their origin, and thus, observations during various stages of development were undertaken in this study. Haemocytes were detected beginning from the early tailbud embryo stage. Haemoblasts were always present and morula cells were the first differentiated haemocytes detected. In both the next stage, just before hatching, and the swimming tadpole larva stage, hyaline amoebocytes and pigment cells were also recognisable. Some morula cells containing active phenoloxidase migrated from the haemolymph into the tunic after having crossed the epidermis, and this behaviour could be related to the preparation of a defensive function for spatial competition. During larval metamorphosis, macrophage-like cells appeared with their phagosomes positive to acid phosphatase activity and containing apoptotic cells from tail tissue degeneration. After metamorphosis, in the filter-feeding oozoid stage, nephrocytes involved in nitrogen catabolism finally appeared. In both the subendostylar sinus and the peripheral blind-sac vessels (ampullae), clusters of haemoblasts were recognisable, some of which showed incipient specialisations, considering the hypothesis of the presence of putative niches of haemolymph stem cells. Full article
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18 pages, 2520 KiB  
Article
Settlement of Bivalve Spat on Artificial Collectors (Net Bags) in Two Commercial Mussel Parks in the North-Western Adriatic Sea
by Tihana Marčeta, Maria Gabriella Marin, Valentina Francesca Codognotto and Monica Bressan
J. Mar. Sci. Eng. 2022, 10(2), 210; https://doi.org/10.3390/jmse10020210 - 05 Feb 2022
Cited by 5 | Viewed by 1693
Abstract
Among aquaculture activities, shellfish culture is considered more sustainable and beneficial in terms of food security. Currently, only a few bivalve species are reared and there is a need to explore the possibility to introduce new candidates for shellfish farming. Due to the [...] Read more.
Among aquaculture activities, shellfish culture is considered more sustainable and beneficial in terms of food security. Currently, only a few bivalve species are reared and there is a need to explore the possibility to introduce new candidates for shellfish farming. Due to the lack of information on bivalve recruitment in the North-Western Adriatic Sea, in this study, the possibility to collect natural spat of commercial species was investigated. Artificial collectors (net bags) were deployed in two sites, Pellestrina and Caleri (North-Western Adriatic Sea), within two commercial mussel parks, during the spring–summer and summer–autumn periods. At both sites, collectors were placed at a distance of 1 m from each other, from 5 to 14 m depth. The influence of season, site and depth on bivalve recruitment was inspected and the presence of invasive species was also evaluated. In all, 28 bivalve taxa were found, and a higher settlement rate was observed in summer–autumn compared to the spring–summer period. Mytilus galloprovincialis, Flexopecten glaber, Mimachlays varia and Aequipecten opercularis were the most abundant species in spring–summer. In the summer–autumn period, in both sites analysed, a very high quantity of Anadara transversa and F. glaber were found. Indeed, these species were dominant at Pellestrina and Caleri, respectively. Another non-indigenous species, Arcuatula senhousia, was also detected. Relevant amounts of Pectinidae spat, F. glaber in particular, were collected and the optimal depth range for the scallop spat collection was found to be between 8 and 14 m. Our results highlight the relevant potential of Pectinidae spat collection along the North-Western Adriatic coasts, even though the presence of invasive species needs to be monitored. Full article
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17 pages, 5467 KiB  
Article
Effects of Exposure to Trade Antifouling Paints and Biocides on Larval Settlement and Metamorphosis of the Compound Ascidian Botryllus schlosseri
by Francesca Cima and Roberta Varello
J. Mar. Sci. Eng. 2022, 10(2), 123; https://doi.org/10.3390/jmse10020123 - 18 Jan 2022
Cited by 4 | Viewed by 1846
Abstract
To evaluate the effects of antifouling paints and biocides on larval settlement and metamorphosis, newly hatched swimming larvae of the compound ascidian Botryllus schlosseri, a dominant species of soft-fouling in coastal communities, were exposed to (i) substrata coated with seven antifouling paints [...] Read more.
To evaluate the effects of antifouling paints and biocides on larval settlement and metamorphosis, newly hatched swimming larvae of the compound ascidian Botryllus schlosseri, a dominant species of soft-fouling in coastal communities, were exposed to (i) substrata coated with seven antifouling paints on the market containing different biocidal mixtures and types of matrices and (ii) sea water containing various concentrations of eight biocidal constituents. All antifouling paints showed high performance, causing 100% mortality and metamorphic inhibition, with ≥75% not-settled dead larvae. All antifouling biocides prevented the settlement of larvae. The most severe larval malformations, i.e., (i) the formation of a bubble encasing the cephalenteron and (ii) the inhibition of tail resorption, were observed after exposure to metal and organometal compounds, including tributyltin (TBT) at 1 μM (325.5 µg L−1), zinc pyrithione (ZnP) at 1 μM (317.7 µg L−1), and CuCl at 0.1 μM (98.99 µg L−1), and to antimicrobials and fungicides, including Sea-Nine 211 at 1 μM (282.2 µg L−1) and Chlorothalonil at 1 μM (265.9 µg L−1). The herbicides seemed to be less active. Irgarol 1051 was not lethal at any of the concentrations tested. Diuron at 250 μM (58.2 mg L−1) and 2,3,5,6-tetrachloro-4-(methylsulphonyl)pyridine (TCMS pyridine) at 50 μM (14.8 mg L−1) completely inhibited larval metamorphosis. These results may have important implications for the practical use of different antifouling components, highlighting the importance of their testing for negative impacts on native benthic species. Full article
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13 pages, 3600 KiB  
Article
Morphological Study and 3D Reconstruction of the Larva of the Ascidian Halocynthia roretzi
by Lucia Manni, Federico Caicci, Chiara Anselmi, Virginia Vanni, Silvia Mercurio and Roberta Pennati
J. Mar. Sci. Eng. 2022, 10(1), 11; https://doi.org/10.3390/jmse10010011 - 24 Dec 2021
Cited by 4 | Viewed by 3457
Abstract
The swimming larva represents the dispersal phase of ascidians, marine invertebrates belonging to tunicates. Due to its adhesive papillae, the larva searches the substrate, adheres to it, and undergoes metamorphosis, thereby becoming a sessile filter feeding animal. The larva anatomy has been described [...] Read more.
The swimming larva represents the dispersal phase of ascidians, marine invertebrates belonging to tunicates. Due to its adhesive papillae, the larva searches the substrate, adheres to it, and undergoes metamorphosis, thereby becoming a sessile filter feeding animal. The larva anatomy has been described in detail in a few species, revealing a different degree of adult structure differentiation, called adultation. In the solitary ascidian Halocynthia roretzi, a species reared for commercial purposes, embryogenesis has been described in detail, but information on the larval anatomy is still lacking. Here, we describe it using a comparative approach, utilizing 3D reconstruction, as well as histological/TEM observations, with attention to its papillae. The larva is comparable to those of other solitary ascidians, such as Ciona intestinalis. However, it displays a higher level of adultation for the presence of the atrium, opened outside by means of the atrial siphon, and the peribranchial chambers. It does not reach the level of complexity of the larva of Botryllus schlosseri, a phylogenetically close colonial ascidian. Our study reveals that the papillae of H. roretzi, previously described as simple and conform, exhibit dynamic changes during settlement. This opens up new considerations on papillae morphology and evolution and deserves to be further investigated. Full article
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16 pages, 556 KiB  
Article
Naturally Occurring Rock Type Influences the Settlement of Fucus spiralis L. zygotes
by William G. Ambrose, Jr., Paul E. Renaud, David C. Adler and Robert L. Vadas
J. Mar. Sci. Eng. 2021, 9(9), 927; https://doi.org/10.3390/jmse9090927 - 26 Aug 2021
Cited by 3 | Viewed by 1724
Abstract
The settlement of spores and larvae on hard substrates has been shown to be influenced by many factors, but few studies have evaluated how underlying bedrock may influence recruitment. The characteristics of coastal rock types such as color, heat capacity, mineral size, and [...] Read more.
The settlement of spores and larvae on hard substrates has been shown to be influenced by many factors, but few studies have evaluated how underlying bedrock may influence recruitment. The characteristics of coastal rock types such as color, heat capacity, mineral size, and free energy have all been implicated in settlement success. We examined the influence of naturally occurring rock types on the initial attachment of zygotes of the brown alga Fucus spiralis Linnaeus 1753. We also assessed the dislodgment of zygotes on four bedrock types after initial attachment in laboratory experiments using wave tanks. Settling plates were prepared from limestone, basalt, schist, and granite, found in the region of Orrs Island, Maine, USA. The plate surfaces tested were either naturally rough or smooth-cut surfaces. We measured the density of attached zygotes after 1.5 h of settlement and subsequently after a wave treatment, in both winter and summer. The pattern of initial attachment was the same on natural and smooth surfaces regardless of season: highest on limestone (range 7.0–13.4 zygotes/cm2), intermediate on schist (1.8–8.5 zygotes/cm2) and basalt (3.5–14.0 zygotes/cm2), and lowest on granite (0.8–7.8 zygotes/cm2). Patterns of survivorship following the wave treatment were similar to those of initial settlement with the mean survivorship varying from 60.1% (SE = 3.8) (limestone, smooth substrate) to 31.8% (SE = 0.59) (granite, natural substrate), and with the highest mean survival on limestone, basalt, and schist, and the lowest on granite. Our results suggest that rock type has a significant effect on zygote attachment and persistence. Patterns of attachment were the same on smooth and rough surfaces, indicating that surface roughness is not the predominant factor controlling the difference in successful attachment among rock types. Other properties of bedrock, possibly grain size, surface free energy, or chemical interaction with the adhesives used by the zygotes, directly affect the attachment of these algal propagules. These results suggest that patterns of benthic community structure could be determined in part by the distribution of bedrock types. Full article
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14 pages, 3812 KiB  
Article
The Application of UVC Used in Synergy with Surface Material to Prevent Marine Biofouling
by Kailey N. Richard, Kelli Z. Hunsucker, Harrison Gardner, Kris Hickman and Geoffrey Swain
J. Mar. Sci. Eng. 2021, 9(6), 662; https://doi.org/10.3390/jmse9060662 - 15 Jun 2021
Cited by 12 | Viewed by 2988
Abstract
Biofouling is problematic for the shipping industry and can lead to functional and financial setbacks. One possible means of biofouling prevention is the use of ultraviolet-C (UVC) light. Previous studies have investigated UVC with marine coatings, but the synergistic effect with color and [...] Read more.
Biofouling is problematic for the shipping industry and can lead to functional and financial setbacks. One possible means of biofouling prevention is the use of ultraviolet-C (UVC) light. Previous studies have investigated UVC with marine coatings, but the synergistic effect with color and surface material, specifically reflectance, has yet to be determined. This study comprised three parts: UVC and color (red vs. white), UVC and reflectance (stainless steel vs. polycarbonate), and UVC and exposure intervals (weekly intervals and 10 min intervals). There was no variance in the biofouling communities for colored surfaces when exposed to 254 nm UVC. Reflectance studies demonstrated that the surface material plays a role in biofouling settlement. Stainless steel panels had significantly greater macrofouling settlement than polycarbonate, specifically among encrusting bryozoan, tubeworms, and tunicate communities. Panels of both surface materials exposed to indirect UVC significantly differed from controls and those exposed directly to UVC. Exposure intervals were also found to reduce biofouling settlement especially with long frequent intervals (i.e., 10 min/day). UVC can be utilized on various colored surfaces and different surface types, but the effectiveness in preventing biofouling is ultimately determined by the duration and frequency of UVC exposure. Full article
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8 pages, 4070 KiB  
Communication
A Vital Staining Practice That Discerns Ancestry within Groups of Settling Larvae of a Brooding Coral
by Dor Shefy, Nadav Shashar and Baruch Rinkevich
J. Mar. Sci. Eng. 2021, 9(6), 616; https://doi.org/10.3390/jmse9060616 - 03 Jun 2021
Cited by 6 | Viewed by 2309
Abstract
Xenogeneic and allogeneic encounters following aggregated and clustered settlements of coral larvae (planulae) may carry important ecological consequences in shaping coral reefs’ communities. However, larval settlement behaviors and settlement location choices in the presence of conspecifics or heterospecifics have not been examined in [...] Read more.
Xenogeneic and allogeneic encounters following aggregated and clustered settlements of coral larvae (planulae) may carry important ecological consequences in shaping coral reefs’ communities. However, larval settlement behaviors and settlement location choices in the presence of conspecifics or heterospecifics have not been examined in detail, due to a lack of experimental tools. One potential approach is the employment of vital staining of planulae with dyes that do not impair larval metamorphosis processes, are stable for prolonged periods, and do not diffuse to un-labeled counterpart planulae. For these purposes, we examined the use of neutral red (NR) dye, as an identification marker, on the planulae of Stylophora pistillata, a Red Sea branching coral species. To examine possible NR impacts on larval settlement in the presence of conspecific planulae, we followed the settlement ratios of kin, non-kin, and mixed assemblages, as a proxy for metamorphosis success. We found no differences in settlement rates of stained vs. unstained larvae, lack of stain diffusion to other larvae and that NR stain is maintained for more than a week under a still water regimen. Thus, staining with NR may serve as a useful experimental tool, opening new opportunities in studying larval settlement patterns in sessile marine organisms. Full article
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14 pages, 1915 KiB  
Article
Experimental Assessment of a Conducting Polymer (PEDOT) and Microbial Biofilms as Deterrents and Facilitators of Macro-Biofouling: Larval Settlement of the Barnacle Notobalanus flosculus (Darwin, 1854) from Central Chile
by Simone Baldanzi, Ignacio T. Vargas, Francisco Armijo, Miriam Fernández and Sergio A. Navarrete
J. Mar. Sci. Eng. 2021, 9(1), 82; https://doi.org/10.3390/jmse9010082 - 14 Jan 2021
Cited by 3 | Viewed by 2277
Abstract
Maritime enterprises have long sought solutions to reduce the negative consequences of the settlement and growth of marine biofouling (micro- and macro-organisms) on virtually all surfaces and materials deployed at sea. The development of biofouling control strategies requires solutions that are cost-effective and [...] Read more.
Maritime enterprises have long sought solutions to reduce the negative consequences of the settlement and growth of marine biofouling (micro- and macro-organisms) on virtually all surfaces and materials deployed at sea. The development of biofouling control strategies requires solutions that are cost-effective and environmentally friendly. Polymer-based coatings, such as the poly (3,4-ethylenedioxythiophene) (PEDOT) and its potential applications, have blossomed over the last decade thanks to their low cost, nontoxicity, and high versatility. Here, using multiple-choice larval settlement experiments, we assessed the efficacy of PEDOT against the balanoid barnacle Notobalanus flosculus one of the most common biofouling species in Southeastern Pacific shores, and compared results against a commercially available antifouling (AF) coating, and biofilms at different stages of succession (1, 2, 4 and 8 weeks). We show that larval settlement on PEDOT-coated surfaces was similar to the settlement on AF-coated surfaces, while larvae settled abundantly on roughened acrylic and on early-to-intermediate stages of biofilm (one to four weeks old). These results are promising and suggest that PEDOT is a good candidate for fouling-resistant coating for specific applications at sea. Further studies to improve our understanding of the mechanisms of barnacle larval deterrence, as well as exposure to field conditions, are encouraged. Full article
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13 pages, 5245 KiB  
Article
Anatomy and Ultrastructure of the Cyprid Temporary Adhesive System in Two Species of Acorn Barnacle
by Joshua J. Raine, Nick Aldred and Anthony S. Clare
J. Mar. Sci. Eng. 2020, 8(12), 968; https://doi.org/10.3390/jmse8120968 - 27 Nov 2020
Cited by 3 | Viewed by 2505
Abstract
Acorn barnacles are sessile as adults and select their settlement site as a cypris larva. Cyprids are well adapted to exploring surfaces in dynamic environments, using a temporary adhesive secreted from the antennules to adhere during this process. The temporary adhesive and the [...] Read more.
Acorn barnacles are sessile as adults and select their settlement site as a cypris larva. Cyprids are well adapted to exploring surfaces in dynamic environments, using a temporary adhesive secreted from the antennules to adhere during this process. The temporary adhesive and the secretory structures are poorly characterized. This study used serial block-face scanning electron microscopy and three-dimensional modelling to elucidate the anatomy related to temporary adhesion. The temporary adhesive glands of two acorn barnacle species, Balanus amphitrite and Megabalanus coccopoma, were located in the proximal region of the first antennular segment, contrary to previous descriptions that placed them in the more distal second segment. The temporary adhesive systems of these acorn barnacles are therefore similar to that described for the stalked barnacle, Octolasmis angulata, although not identical. Knowledge of the true location of the temporary adhesive glands will underpin future studies of the production, composition and secretion of the adhesive. Full article
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Review

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17 pages, 356 KiB  
Review
Biocide vs. Eco-Friendly Antifoulants: Role of the Antioxidative Defence and Settlement in Mytilus galloprovincialis
by Costantino Parisi, Jessica Sandonnini, Maria Rosaria Coppola, Adriano Madonna, Fagr Kh. Abdel-Gawad, Emidio M. Sivieri and Giulia Guerriero
J. Mar. Sci. Eng. 2022, 10(6), 792; https://doi.org/10.3390/jmse10060792 - 09 Jun 2022
Cited by 4 | Viewed by 2291
Abstract
Antifoulant paints were developed to prevent and reduce biofouling on surfaces immersed in seawater. The widespread use of these substances over the years has led to a significant increase of their presence in the marine environment. These compounds were identified as environmental and [...] Read more.
Antifoulant paints were developed to prevent and reduce biofouling on surfaces immersed in seawater. The widespread use of these substances over the years has led to a significant increase of their presence in the marine environment. These compounds were identified as environmental and human threats. As a result of an international ban, research in the last decade has focused on developing a new generation of benign antifoulant paints. This review outlines the detrimental effects associated with biocide versus eco-friendly antifoulants, highlighting what are effective antifoulants and why there is a need to monitor them. We examine the effects of biocide and eco-friendly antifoulants on the antioxidative defence mechanism and settlement in a higher sessile organism, specifically the Mediterranean mussel, Mytilus galloprovincialis. These antifoulants can indirectly assess the potential of these two parameters in order to outline implementation of sustainable antifoulants. Full article
12 pages, 2210 KiB  
Review
Substrate Selection of Ascidian Larva: Wettability and Nano-Structures
by Euichi Hirose and Noburu Sensui
J. Mar. Sci. Eng. 2021, 9(6), 634; https://doi.org/10.3390/jmse9060634 - 07 Jun 2021
Cited by 7 | Viewed by 3768
Abstract
Ascidians are marine sessile chordates that comprise one of the major benthic animal groups in marine ecosystems. They sometimes cause biofouling problems on artificial structures underwater, and non-indigenous, invasive ascidian species can potentially and seriously alter native faunal communities. Ascidian larvae are usually [...] Read more.
Ascidians are marine sessile chordates that comprise one of the major benthic animal groups in marine ecosystems. They sometimes cause biofouling problems on artificial structures underwater, and non-indigenous, invasive ascidian species can potentially and seriously alter native faunal communities. Ascidian larvae are usually tadpole-shaped, negatively phototactic, and adhere on substrates by secreting a glue from their adhesive organs. Although larvae often prefer hydrophobic surfaces, such as a silicone rubber, for settlement, hydrophobic materials are often used to reduce occurrence of fouling organisms on artificial structures. This inconsistency may indicate that an attractive surface for larvae is not always suitable for settlement. Micro-scale structures or roughness may enhance the settlement of ascidian larvae, but settlement is significantly reduced by a nano-scale nipple array (or moth-eye structure), suggesting functional properties of similar structures found on the body surfaces of various invertebrates. The substrate preferences of larvae should be one of the important bases in considering measures against biofouling, and this review also discusses the potential uses of materials to safely reduce the impacts of invasive species. Full article
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Other

3 pages, 2754 KiB  
Correction
Correction: Cima, F. Searching for the Origin and the Differentiation of Haemocytes before and after Larval Settlement of the Colonial Ascidian Botryllus schlosseri: An Ultrastructural Viewpoint. J. Mar. Sci. Eng. 2022, 10, 987
by Francesca Cima
J. Mar. Sci. Eng. 2022, 10(9), 1207; https://doi.org/10.3390/jmse10091207 - 29 Aug 2022
Viewed by 668
Abstract
In the original publication [...] Full article
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