Multiple impacts of microplastics can threaten marine habitat-forming species.


Journal

Communications biology
ISSN: 2399-3642
Titre abrégé: Commun Biol
Pays: England
ID NLM: 101719179

Informations de publication

Date de publication:
30 03 2021
Historique:
received: 26 05 2020
accepted: 03 03 2021
entrez: 31 3 2021
pubmed: 1 4 2021
medline: 6 8 2021
Statut: epublish

Résumé

Microplastics are recognised as a potential global threat to marine ecosystems, but the biological mechanisms determining their impact on marine life are still largely unknown. Here, we investigated the effects of microplastics on the red coral, a long-lived habitat-forming organism belonging to the Corallium genus, which is present at almost all latitudes from shallow-water to deep-sea habitats. When exposed to microplastics, corals preferentially ingest polypropylene, with multiple biological effects, from feeding impairment to mucus production and altered gene expression. Microplastics can alter the coral microbiome directly and indirectly by causing tissue abrasions that allow the proliferation of opportunistic bacteria. These multiple effects suggest that microplastics at the concentrations present in some marine areas and predicted for most oceans in the coming decades, can ultimately cause coral death. Other habitat-forming suspension-feeding species are likely subjected to similar impacts, which may act synergistically with climate-driven events primarily responsible for mass mortalities.

Identifiants

pubmed: 33785849
doi: 10.1038/s42003-021-01961-1
pii: 10.1038/s42003-021-01961-1
pmc: PMC8010021
doi:

Substances chimiques

Microplastics 0
Polypropylenes 0
Water Pollutants, Chemical 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

431

Références

Hartmann, N. B. et al. Are we speaking the same language? Recommendations for a definition and categorization framework for plastic debris. Environ. Sci. Technol. 53, 1039–1047 (2019).
pubmed: 30608663 doi: 10.1021/acs.est.8b05297
Browne, M. A. et al. Linking effects of anthropogenic debris to ecological impacts. Proc. R. Soc. B. 282, 20142929 (2015).
pubmed: 25904661 doi: 10.1098/rspb.2014.2929 pmcid: 4424639
Wright, S. L., Thompson, R. C. & Galloway, T. S. The physical impacts of microplastics on marine tr: a review. Environ. Pollut. 178, 483–492 (2013).
pubmed: 23545014 doi: 10.1016/j.envpol.2013.02.031
Galloway, T. S., Cole, M. & Lewis, C. Interactions of microplastic debris throughout the marine ecosystem. Nat. Ecol. Evol. 1, 0116 (2017).
doi: 10.1038/s41559-017-0116
Phuong, N. N. et al. Is there any consistency between the microplastics found in the field and those used in laboratory experiments? Environ. Pollut. 211, 111–123 (2016).
pubmed: 26745396 doi: 10.1016/j.envpol.2015.12.035
Lindeque, P. K. et al. Are we underestimating microplastic abundance in the marine environment? A comparison of microplastic capture with nets of different mesh-size. Environ. Pollut. 265, 114721 (2020).
Auta, H. S., Emenike, C. U. & Fauziah, S. H. Distribution and importance of microplastics in the marine environment: a review of the sources, fate, effects, and potential solutions. Environ. Int. 102, 165–176 (2017).
pubmed: 28284818 doi: 10.1016/j.envint.2017.02.013
Paul-Pont, I. et al. Constraints and priorities for conducting experimental exposures of marine organisms to microplastics. Front. Mar. Sci. 5, 252 (2018).
doi: 10.3389/fmars.2018.00252
Isobe, A., Iwasaki, S., Uchida, K. & Tokai, T. Abundance of non-conservative microplastics in the upper ocean from 1957 to 2066. Nat. Commun. 10, 1–13 (2019).
doi: 10.1038/s41467-019-08316-9
Brandon, J. A., Freibott, A. & Sala, L. M. Patterns of suspended and salp‐ingested microplastic debris in the North Pacific investigated with epifluorescence microscopy. LO Lett. 5, 46–53 (2020).
Rochman, C. M. et al. The ecological impacts of marine debris: unraveling the demonstrated evidence from what is perceived. Ecology 97, 302–312 (2016).
pubmed: 27145606 doi: 10.1890/14-2070.1
Law, K. L. Plastics in the marine environment. Annu. Rev. Mar. Sci. 9, 205–229 (2017).
doi: 10.1146/annurev-marine-010816-060409
Kögel, T., Bjorøy, Ø., Toto, B., Bienfait, A. M. & Sanden, M. Micro-and nanoplastic toxicity on aquatic life: determining factors. Sci. Tot. Environ. 709, 136050 (2019).
Hui, M. et al. Microplastics in aquatic environments: toxicity to trigger ecological consequences. Environ. Pollut. 261, 114089 (2020).
Heindler, F. M. et al. Toxic effects of polyethylene terephthalate microparticles and Di(2-ethylhexyl)phthalate on the calanoid copepod, Parvocalanus crassirostris. Ecotoxicol. Environ. Saf. 141, 298–305 (2017).
pubmed: 28365455 doi: 10.1016/j.ecoenv.2017.03.029
Della Torre, C. et al. Accumulation and embryotoxicity of polystyrene nanoparticles at early stage of development of sea urchin embryos Paracentrotus lividus. Environ. Sci. Technol. 48, 12302–12311 (2014).
pubmed: 25260196 doi: 10.1021/es502569w
Balbi, T. et al. Impact of cationic polystyrene nanoparticles (PS-NH2H) on early embryo development of Mytilus galloprovincialis: effects on shell formation. Chemosphere 186, 1–9 (2017).
pubmed: 28759811 doi: 10.1016/j.chemosphere.2017.07.120
Paul-Pont, I. et al. Exposure of marine mussels Mytilus spp. to polystyrene microplastics: toxicity and influence on fluoranthene bioaccumulation. Environ. Pollut. 216, 724–737 (2016).
pubmed: 27372385 doi: 10.1016/j.envpol.2016.06.039
Yu, P., Liu, Z., Wu, D., Chen, M., Lv, W. & Zhao, Y. Accumulation of polystyrene microplastics in juvenile Eriocheir sinensis and oxidative stress effects in the liver. Aquat. Toxicol. 200, 28–36 (2018).
pubmed: 29709883 doi: 10.1016/j.aquatox.2018.04.015
De Sá, L. C., Oliveira, M., Ribeiro, F., Rocha, T. L. & Futter, M. N. Studies of the effects of microplastics on aquatic organisms: what do we know and where should we focus our efforts in the future? Sci. Tot. Environ. 645, 1029–1039 (2018).
doi: 10.1016/j.scitotenv.2018.07.207
Liu, Z. et al. Effects of microplastics on the innate immunity and intestinal microflora of juvenile eriocheir sinensis. Sci. Tot. Environ. 685, 836–46 (2019).
doi: 10.1016/j.scitotenv.2019.06.265
Von Moos, N., Burkhardt-Holm, P. & Köhler, A. Uptake and effects of microplastics on cells and tissue of the blue mussel Mytilus edulis L. after an experimental exposure. Envir. Sci. Tech. 46, 11327–11335 (2012).
doi: 10.1021/es302332w
Lee, K., Shim, W. J., Kwon, O. Y. & Kang, J. Size-dependent effects of micro polystyrene particles in the marine copepod Tigriopus japonicus. Environ. Sci. Technol. 47, 11278–11283 (2013).
pubmed: 23988225 doi: 10.1021/es401932b
Cole, M., Lindeque, P., Fileman, E., Halsband, C. & Galloway, T. S. The impact of polystyrene microplastics on feeding, function and fecundity in the marine copepod Calanus helgolandicus. Environ. Sci. Technol. 49, 1130–1137 (2015).
pubmed: 25563688 doi: 10.1021/es504525u
Sussarellu, R. et al. Oyster reproduction is affected by exposure to polystyrene microplastics. Proc. Natl Acad. Sci. USA 113, 2430–2435 (2016).
pubmed: 26831072 doi: 10.1073/pnas.1519019113 pmcid: 4780615
Galloway, T. S. & Lewis, C. N. Marine microplastics spell big problems for future generations. PNAS 113, 2331–2333 (2016).
pubmed: 26903632 doi: 10.1073/pnas.1600715113 pmcid: 4780651
Katija, K., Anela Choy, C., Sherlock Rob, E., Sherman Alana, D. & Robison, B. H. From the surface to the seafloor: how giant larvaceans transport microplastics into the deep sea. Sci. Adv. 3, e1700715 (2017).
Mouchi, V. et al. Long-term aquaria study suggests species-specific responses of two cold-water corals to macro-and microplastics exposure. Environ. Pollut. 253, 322–329 (2019).
pubmed: 31323615 doi: 10.1016/j.envpol.2019.07.024
Cole, M., Lindeque, P., Halsband, C. & Galloway, T. S. Microplastics as contaminants in the marine environment: a review. Mar. Pollut. Bull. 62, 2588–2597 (2011).
pubmed: 22001295 doi: 10.1016/j.marpolbul.2011.09.025
Sagarin, R. D. et al. Between control and complexity: opportunities and challenges for marine mesocosms. Front. Ecol. Environ. 14, 389–396 (2016).
doi: 10.1002/fee.1313
Levin, L. A. et al. Environmental influences on regional deep-sea species diversity. Annu. Rev. Ecol. Evol. Syst. 32, 51–93 (2001).
doi: 10.1146/annurev.ecolsys.32.081501.114002
Bruckner, A. W. Advances in management of precious corals in the family Corallidae: are new measures adequate? Curr. Opin. Environ. Sustain 7, 1–8 (2014).
doi: 10.1016/j.cosust.2013.11.024
Bruckner, A. W. Rate and extent of decline in Corallium (pink and red coral) populations: existing data meet the requirements for a CITES Appendix II listing. Mar. Ecol. Prog. Ser. 397, 319–332 (2009).
doi: 10.3354/meps08110
Ardila, N. E., Giribet, G. & Sanchez, J. A. A time-calibrated molecular phylogeny of the precious corals: reconciling discrepancies in the taxonomic classification and insights into their evolutionary history. BMC Evol. Biol. 12, 1–12 (2012).
doi: 10.1186/1471-2148-12-246
Hall, N. M., Berry, K. L. E., Rintoul, L. & Hoogenboom, M. O. Microplastic ingestion by scleractinian corals. Mar. Biol. 162, 725 (2015).
doi: 10.1007/s00227-015-2619-7
Allen, A. S., Seymour, A. C. & Rittschof, D. Chemoreception drives plastic consumption in a hard coral. Mar. Pollut. Bull. 124, 198–205 (2017).
pubmed: 28743368 doi: 10.1016/j.marpolbul.2017.07.030
Savinelli, B. et al. Microplastics impair the feeding performance of a Mediterranean habitat-forming coral. Mar. Envir. Res. 155, 104887 (2020).
doi: 10.1016/j.marenvres.2020.104887
Lamb, J. B. et al. Plastic waste associated with disease on coral reefs. Science 359, 460–462 (2018).
pubmed: 29371469 doi: 10.1126/science.aar3320
Grasshoff, M. Die Flachwasser-Gorgonarien von Europa und Westafrika-(Cnidaria, Anthozoa) (1992).
van de Water, J. A. et al. Spirochaetes dominate the microbial community associated with the red coral Corallium rubrum on a broad geographic scale. Sci. Rep. 6, 27277 (2016).
pubmed: 27263657 pmcid: 4893704 doi: 10.1038/srep27277
Morohoshi, T., Ogata, K., Okura, T. & Sato, S. Molecular characterization of the bacterial community in biofilms for degradation of poly (3-hydroxybutyrate-co-3-hydroxyhexanoate) films in seawater. Microbes Environ. 33, 19–25 (2018).
pubmed: 29386425 pmcid: 5877338 doi: 10.1264/jsme2.ME17052
Lenhoff, H. M. & Heagy, W. Aquatic invertebrates: model systems for study of receptor activation and evolution of receptor proteins. Annu. Rev. Pharm. Toxicol. 17, 243–25842 (1977).
doi: 10.1146/annurev.pa.17.040177.001331
de Oliveira Soares, M. et al. Microplastics in corals: an emergent threat. Mar. Pollut. Bull. 161, 111810 (2020).
doi: 10.1016/j.marpolbul.2020.111810
Farrell, P. & Nelson, K. Trophic level transfer of microplastic: Mytilus edulis (L.) to Carcinus maenas (L.). Envir. Poll. 177, 1–3 (2013).
doi: 10.1016/j.envpol.2013.01.046
Cole, M. et al. Microplastic ingestion by zooplankton. Environ. Sci. Technol. 47, 6646–6655 (2013).
pubmed: 23692270 doi: 10.1021/es400663f
SAPEA, Science Advice for Policy by European Academies. A Scientific Perspective on Microplastics in Nature and Society. https://doi.org/10.26356/microplastics (SAPEA, 2019).
Davenport, J. & Healy, A. Relationship between medium salinity, body density, buoyancy and swimming in Artemia franciscana larvae: constraints on water column use? Hydrobiologia 556, 295–30142 (2006).
doi: 10.1007/s10750-005-9118-7
Knutsen, T., Melle, W. & Calise, L. Determining the mass density of marine copepods and their eggs with a critical focus on some of the previously used methods. J. Plankton Res. 23, 859–873 (2001).
doi: 10.1093/plankt/23.8.859
Tsounis, G. et al. Diet and seasonal prey capture rates in the Mediterranean red coral (Corallium rubrum L.). Mar. Biol. 149, 313–325 (2006).
doi: 10.1007/s00227-005-0220-1
Reichert, J., Schellenberg, J., Schubert, P. & Wilke, T. Responses of reef building corals to microplastic exposure. Environ. Pollut. 237, 955–960 (2018).
pubmed: 29146203 doi: 10.1016/j.envpol.2017.11.006
Van Woesik, R. Lesion healing on massive Porites spp. corals. Mar. Ecol. Prog. Ser. 164, 213–220 (1998).
doi: 10.3354/meps164213
Cerrano, C. et al. A catastrophic mass‐mortality episode of gorgonians and other organisms in the Ligurian Sea (North‐western Mediterranean), summer 1999. Ecol. Lett. 3, 284–293 (2000).
doi: 10.1046/j.1461-0248.2000.00152.x
Garrabou, J., Perez, T., Sartoretto, S. & Harmelin, J. G. Mass mortality event in red coral Corallium rubrum populations in the Provence region (France, NW Mediterranean). Mar. Ecol. Prog. Ser. 217, 263–272 (2001).
doi: 10.3354/meps217263
Garrabou, J. et al. Mass mortality in Northwestern Mediterranean rocky benthic communities: effects of the 2003 heat wave. Glob. Change Biol. 15, 1090–1103 (2009).
doi: 10.1111/j.1365-2486.2008.01823.x
Martin, C., Corona, E., Mahadik, G. A. & Duarte, C. M. Adhesion to coral surface as a potential sink for marine microplastics. Environ. Pollut. 255, 113281 (2019).
pubmed: 31600700 doi: 10.1016/j.envpol.2019.113281
Glasl, B., Herndl, G. J. & Frade, P. R. The microbiome of coral surface mucus has a key role in mediating holobiont health and survival upon disturbance. ISME J. 10, 2280 (2016).
pubmed: 26953605 pmcid: 4989324 doi: 10.1038/ismej.2016.9
van de Water, J. A., Allemand, D. & Ferrier-Pagès, C. Host-microbe interactions in octocoral holobionts-recent advances and perspectives. Microbiome 6, 64 (2018).
pubmed: 29609655 pmcid: 5880021 doi: 10.1186/s40168-018-0431-6
Louis, Y. D., Bhagooli, R., Kenkel, C. D., Baker, A. C. & Dyall, S. D. Gene expression biomarkers of heat stress in scleractinian corals: promises and limitations. Comp. Biochem. Physiol. C. Toxicol. Pharm. 191, 63–77 (2017).
doi: 10.1016/j.cbpc.2016.08.007
Tarrant, A. M., Reitzel, A. M., Kwok, C. K. & Jenny, M. J. Activation of the cnidarian oxidative stress response by ultraviolet radiation, polycyclic aromatic hydrocarbons and crude oil. J. Exp. Biol. 217, 1444–14536 (2014).
pubmed: 24436378 pmcid: 4006587
Sørensen, J. G., Kristensen, T. N. & Loeschcke, V. The evolutionary and ecological role of heat shock proteins. Ecol. Lett. 6, 1025–1037 (2003).
doi: 10.1046/j.1461-0248.2003.00528.x
Haguenauer, A., Zuberer, F., Ledoux, J. B. & Aurelle, D. Adaptive abilities of the Mediterranean red coral Corallium rubrum in a heterogeneous and changing environment: from population to functional genetics. J. Exp. Mar. Biol. Ecol. 449, 349–357 (2013).
doi: 10.1016/j.jembe.2013.10.010
Elifantz, H., Horn, G., Ayon, M., Cohen, Y. & Minz, D. Rhodobacteraceae are the key members of the microbial community of the initial biofilm formed in Eastern Mediterranean coastal seawater. FEMS Microbiol. Ecol. 85, 348–357 (2013).
pubmed: 23551015 doi: 10.1111/1574-6941.12122
Meron, D. et al. The impact of reduced pH on the microbial community of the coral Acropora eurystoma. ISME J. 5, 51 (2011).
pubmed: 20668489 doi: 10.1038/ismej.2010.102
Maher, R. L., Rice, M. M., McMinds, R., Burkepile, D. E. & Thurber, R. V. Multiple stressors interact primarily through antagonism to drive changes in the coral microbiome. Sci. Rep. 9, 1–12 (2019).
doi: 10.1038/s41598-019-43274-8
La Riviere, M., Roumagnac, M., Garrabou, J. & Bally, M. Transient shifts in bacterial communities associated with the temperate gorgonian Paramuricea clavata in the Northwestern Mediterranean Sea. PLoS ONE 8, e57385 (2013).
pubmed: 23437379 pmcid: 3577713 doi: 10.1371/journal.pone.0057385
Zettler, E. R., Mincer, T. J. & Amaral-Zettler, L. A life in the “plastisphere”: microbial communities on plastic marine debris. Environ. Sci. Technol. 47, 7137–7146 (2013).
pubmed: 23745679 doi: 10.1021/es401288x
Neave, M. J., Apprill, A., Ferrier-Pagès, C. & Voolstra, C. R. Diversity and function of prevalent symbiotic marine bacteria in the genus Endozoicomonas. Appl. Microbiol. Biotechnol. 100, 8315–8324 (2016).
pubmed: 27557714 pmcid: 5018254 doi: 10.1007/s00253-016-7777-0
Ziegler et al. Coral bacterial community structure responds to environmental change in a host-specific manner. Nat. Commun. 10, 1–11 (2019).
doi: 10.1038/s41467-019-10969-5
Hermabessiere et al. Occurrence and effects of plastic additives on marine environments and organisms: a review. Chemosphere 182, 781–793 (2017).
pubmed: 28545000 doi: 10.1016/j.chemosphere.2017.05.096
Aminot, Y. et al. Leaching of flame-retardants from polystyrene debris: Bioaccumulation and potential effects on coral. Mar. Pollut. Bull. 151, 110862 (2020).
pubmed: 32056644 doi: 10.1016/j.marpolbul.2019.110862
Miller, M. E., Hamann, M. & Kroon, F. J. Bioaccumulation and biomagnification of microplastics in marine organisms: a review and meta-analysis of current data. PLoS ONE 15, e0240792 (2020).
pubmed: 33064755 pmcid: 7567360 doi: 10.1371/journal.pone.0240792
Pabortsava, K. & Lampitt, R. S. High concentrations of plastic hidden beneath the surface of the Atlantic Ocean. Nat. Commun. 11, 1–11 (2020).
doi: 10.1038/s41467-020-17932-9
de la Fuente, R., Drótos, G., Hernández García, E., López, C. & van Sebille, E. Sinking microplastics in the water column: simulations in the Mediterranean Sea. Ocean Sci. 17, 431–453 (2021).
Cerrano, C. et al. Red coral extinction risk enhanced by ocean acidification. Sci. Rep. 3, 1457 (2013).
pubmed: 23492780 pmcid: 3597996 doi: 10.1038/srep01457
Rastelli, E. et al. A high biodiversity mitigates the impact of ocean acidification on hard-bottom ecosystems. Sci. Rep. 10, 1–13 (2020).
doi: 10.1038/s41598-020-59886-4
Le Goff, C. et al. In vivo pH measurement at the site of calcification in an octocoral. Sci. Rep. 7, 1–14 (2017).
Sutherland, A. B. A simple reciprocating apparatus for maintaining long‐term turbidity in biological experiments. Limnol. Oceanogr. Meth. 4, 49–57 (2006).
doi: 10.4319/lom.2006.4.49
Fossi, M. C. et al. Are baleen whales exposed to the threat of microplastics? A case study of the Mediterranean fin whale (Balaenoptera physalus). Mar. Poll. Bull. 64, 2374–2379 (2012).
doi: 10.1016/j.marpolbul.2012.08.013
Fossi, M. C. et al. Fin whales and microplastics: The Mediterranean Sea and the Sea of Cortez scenarios. Environ. Pollut. 209, 68–78 (2016).
pubmed: 26637933 doi: 10.1016/j.envpol.2015.11.022
Tsounis, G. et al. Prey-capture rates in four Mediterranean cold-water corals. Mar. Ecol. Prog. Ser. 398, 149–155 (2010).
doi: 10.3354/meps08312
Cole, M. et al. Isolation of microplastics in biota-rich seawater samples and marine organisms. Sci. Rep. 4, 4528 (2014).
pubmed: 24681661 pmcid: 3970126 doi: 10.1038/srep04528
Quintanilla, E. et al. Local confinement of disease-related microbiome facilitates recovery of gorgonian sea fans from necrotic-patch disease. Sci. Rep. 8, 14636 (2018).
pubmed: 30279438 pmcid: 6168572 doi: 10.1038/s41598-018-33007-8
Hazrin-Chong, N. H. & Manefield, M. An alternative SEM drying method using hexamethyldisilazane (HMDS) for microbial cell attachment studies on sub-bituminous coal”. J. Microbiol. Methods 90, 96–99 (2012).
pubmed: 22561094 doi: 10.1016/j.mimet.2012.04.014
Trygonis, V. & Sini, M. PhotoQuad: a dedicated seabed image processing software, and a comparative error analysis of four photoquadrat methods. J. Exp. Mar. Bio. Ecol. 424, 99–108 (2012).
doi: 10.1016/j.jembe.2012.04.018
Untergasser, A. et al. Primer3—new capabilities and interfaces. Nucleic Acids Res. 40, e115–e115 (2012).
pubmed: 22730293 pmcid: 3424584 doi: 10.1093/nar/gks596
Schmittgen, T. D. & Livak, K. J. Analyzing real-time PCR data by the comparative C
pubmed: 18546601 doi: 10.1038/nprot.2008.73
Danovaro, R. Methods for the Study of Deep-sea Sediments, Their Functioning and Biodiversity (CRC Press, 2010).
Bushnell, BBMap. https://sourceforge.net/projects/bbmap/ (2014).
Corinaldesi, C. et al. High diversity of benthic bacterial and archaeal assemblages in deep-Mediterranean canyons and adjacent slopes. Prog. Oceanogr. 171, 154–161 (2019).
doi: 10.1016/j.pocean.2018.12.014
Callahan, B. J. et al. DADA2: high-resolution sample inference from Illumina amplicon data. Nat. Methods 13, 581 (2016).
pubmed: 27214047 pmcid: 4927377 doi: 10.1038/nmeth.3869
Quast, C. et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 41, 590–596 (2012).
doi: 10.1093/nar/gks1219
Hall, M. & Beiko, R. G. in Microbiome Analysis, Vol. 1849 (eds Beiko, R., Hsiao, W. & Parkinson, J.) 113–129 (Humana Press, 2018).
Bates, D., Mächler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67 https://doi.org/10.18637/jss.v067.i01 (2014).
Anderson, M. J. A new method for non-parametric multivariate analysis of variance. Austral Ecol. 26, 32–46 (2001).

Auteurs

Cinzia Corinaldesi (C)

Department of Materials, Environmental Sciences and Urban Planning, Polytechnic University of Marche, Via Brecce Bianche, Ancona, Italy. c.corinaldesi@univpm.it.

Sara Canensi (S)

Department of Life and Environmental Sciences, Polytechnic University of Marche, Ancona, Italy.

Antonio Dell'Anno (A)

Department of Life and Environmental Sciences, Polytechnic University of Marche, Ancona, Italy.

Michael Tangherlini (M)

Department of Research Infrastructures for Marine Biological Resources, Stazione Zoologica Anton Dohrn, Fano Marine Centre, Fano, Italy.

Iole Di Capua (I)

Stazione Zoologica Anton Dohrn, Villa Comunale, Naples, Italy.

Stefano Varrella (S)

Department of Materials, Environmental Sciences and Urban Planning, Polytechnic University of Marche, Via Brecce Bianche, Ancona, Italy.

Trevor J Willis (TJ)

Department of Integrative Marine Ecology, Stazione Zoologica Anton Dohrn, Fano Marine Centre, Fano, Italy.

Carlo Cerrano (C)

Department of Life and Environmental Sciences, Polytechnic University of Marche, Ancona, Italy.

Roberto Danovaro (R)

Department of Life and Environmental Sciences, Polytechnic University of Marche, Ancona, Italy.
Stazione Zoologica Anton Dohrn, Villa Comunale, Naples, Italy.

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