Modeling macroalgal forest distribution at Mediterranean scale : present status, drivers of changes and insights for conservation and management

Macroalgal forests are one of the most productive and valuable marine ecosystems, but yet strongly exposed to fragmentation and loss. Detailed large-scale information on their distribution is largely lacking, hindering conservation initiatives. In this study, a systematic effort to combine spatial data on Cystoseira C. Agardh canopies (Fucales, Phaeophyta) was carried out to develop a Habitat Suitability Model (HSM) at Mediterranean scale, providing critical tools to improve site prioritization for their management, restoration and protection. A georeferenced database on the occurrence of 20 Cystoseira species was produced collecting all the available information from published and grey literature, web data portals and co-authors personal data. Data were associated to 55 predictor variable layers in the (ASCII) raster format and were used in order to develop the HSM by means of a Random Forest, a very effective Machine Learning technique. Knowledge about the distribution of Cystoseira canopies was available for about the 14% of the Mediterranean coastline. Absence data were available only for the 2% of the basin. Despite these gaps, our HSM showed high accuracy levels in reproducing Cystoseira distribution so that the first continuous maps of the habitat across the entire basin was produced. Misclassification errors mainly occurred in the eastern and southern part of the basin, where large gaps of knowledge emerged. The most relevant drivers were the geomorphological ones, followed by anthropogenic variables proxies of pollution and urbanization. Our model shows the importance of data sharing to combine a large number of spatial and environmental data, allowing to individuate areas with high probability of Cystoseira occurrence as suitable for its presence. This approach encourages the use of this modeling tool for the prediction of Cystoseira distribution and for supporting and planning conservation and management initiatives. The step forward is to refine the spatial information of presence-absence data about Cystoseira canopies and of environmental predictors in order to address species-specific assessments.peer-reviewe

The role of grazers in early-life stages of Cystoseira sensu lato can be crucial in the restoration of marine forests

Grazing is one of the most important biological factors controlling the abundance of early-life stages of fucoids and one of the major issues when restoring marine forests. Benthic macroinvertebrates (e.g., sea urchins) and fish shape and regulate benthic macroalgal communities from polar to tropical regions and can be responsible for regime shifts leading to the predominance of turfs and/or barren grounds. However, other herbivores (i.e., mesograzers) could also significantly participate in the grazing, especially on early-life stages, hampering the persistence and capacity of Cystoseira sensu lato populations to recover after major disturbances and being a cause of failure of restoration actions. We performed experiments in the field and in mesocosm in order to investigate the herbivory pressure and the effects of different grazers on recruits of Cystoseira compressa. The results highlight that non-strict herbivorous invertebrates, such as Clibanarius erythropus, Cerithium vulgatum, and Idotea balthica, graze on recruits of Cystoseira s.l. spp., with I. balthica showing the highest consumption rate. We concluded that biotic factors such as herbivory, which affect key life stages, can be crucial for the conservation of Cystoseira s.l. forests and need to be better understood and considered on a case-by-case basis when planning restoration actions

The structure of Mediterranean rocky reef ecosystems across environmental and human gradients, and conservation implications

Historical exploitation of the Mediterranean Sea and the absence of rigorous baselines makes it difficult to evaluate the current health of the marine ecosystems and the efficacy of conservation actions at the ecosystem level. Here we establish the first current baseline and gradient of ecosystem structure of nearshore rocky reefs at the Mediterranean scale. We conducted underwater surveys in 14 marine protected areas and 18 open access sites across the Mediterranean, and across a 31-fold range of fish biomass (from 3.8 to 118 g m22). Our data showed remarkable variation in the structure of rocky reef ecosystems. Multivariate analysis showed three alternative community states: (1) large fish biomass and reefs dominated by non-canopy algae, (2) lower fish biomass but abundant native algal canopies and suspension feeders, and (3) low fish biomass and extensive barrens, with areas covered by turf algae. Our results suggest that the healthiest shallow rocky reef ecosystems in the Mediterranean have both large fish and algal biomass. Protection level and primary production were the only variables significantly correlated to community biomass structure. Fish biomass was significantly larger in well-enforced no-take marine reserves, but there were no significant differences between multi-use marine protected areas (which allow some fishing) and open access areas at the regional scale. The gradients reported here represent a trajectory of degradation that can be used to assess the health of any similar habitat in the Mediterranean, and to evaluate the efficacy of marine protected areas

A decision-support framework for the restoration of Cystoseira sensu lato forests

Macroalgal forests characterised by species of the genus Cystoseira sensu lato form important shallow coastal rocky habitats in the Mediterranean Sea. These forests support a high biodiversity and provide important ecosystem services and societal benefits. Currently these habitats are often in a poor condition in many areas, due to loss and degradation from both anthropogenic and climate stressors. Restoration has recently moved to the forefront of the United Nations and European Union agendas to reverse this trend, particularly in the last decade with the implementation of various international policies. However, this has been in the form of generic targets (e.g., restoration of 30% of degraded habitats by 2030) and has not been linked to specifically what habitat or species to restore, where and how. Initial targets have been missed, new targets are expected through the proposed EU Nature Restoration Law, but overall guidance is still lacking. There are few specific guides to marine habitat restoration limited to mostly seagrass, corals and shellfish. As a priority action for the recovery of coastal marine ecosystems a decision-support framework has been developed for the restoration of Mediterranean macroalgal forests, comprising a stepwise decision tree with additional descriptions of key elements to be considered for a restoration action. The decision tree includes steps concerning current and historical forest presence, site local condition assessment and choice of actions. Key considerations include restoration implementation (competence, society and support, finance and governance), success evaluation (at the target species and the ecosystem level) and long-term management. The framework builds on existing work on Cystoseira s.l. restoration, the work carried out in the EU AFRIMED project, but also on principles and guidelines in place for both generic and specific marine habitats. The work reported here has involved the expertise of scientists and information from stakeholders. Gaps were identified and recommendations were made, dealing with stressors, coordinating and networking stakeholders, integrating top down policy and bottom up initiatives, funding of restoration actions, establishing synergies between restoration, conservation and marine spatial planning and finally communication and publicity

Unpublished Mediterranean and Black Sea records of marine alien, cryptogenic, and neonative species

To enrich spatio-temporal information on the distribution of alien, cryptogenic, and neonative species in the Mediterranean and the Black Sea, a collective effort by 173 marine scientists was made to provide unpublished records and make them open access to the scientific community. Through this effort, we collected and harmonized a dataset of 12,649 records. It includes 247 taxa, of which 217 are Animalia, 25 Plantae and 5 Chromista, from 23 countries surrounding the Mediterranean and the Black Sea. Chordata was the most abundant taxonomic group, followed by Arthropoda, Mollusca, and Annelida. In terms of species records, Siganus luridus, Siganus rivulatus, Saurida lessepsianus, Pterois miles, Upeneus moluccensis, Charybdis (Archias) longicollis, and Caulerpa cylindracea were the most numerous. The temporal distribution of the records ranges from 1973 to 2022, with 44% of the records in 2020–2021. Lethrinus borbonicus is reported for the first time in the Mediterranean Sea, while Pomatoschistus quagga, Caulerpa cylindracea, Grateloupia turuturu, and Misophria pallida are first records for the Black Sea; Kapraunia schneideri is recorded for the second time in the Mediterranean and for the first time in Israel; Prionospio depauperata and Pseudonereis anomala are reported for the first time from the Sea of Marmara. Many first country records are also included, namely: Amathia verticillata (Montenegro), Ampithoe valida (Italy), Antithamnion amphigeneum (Greece), Clavelina oblonga (Tunisia and Slovenia), Dendostrea cf. folium (Syria), Epinephelus fasciatus (Tunisia), Ganonema farinosum (Montenegro), Macrorhynchia philippina (Tunisia), Marenzelleria neglecta (Romania), Paratapes textilis (Tunisia), and Botrylloides diegensis (Tunisia).Stelios Katsanevakis, Michail Ragkousis, Maria Sini, Markos Digenis and Vasilis Gerovasileiou were supported by the Hellenic Foundation for Research and Innovation (HFRI) under the “First Call for HFRI Research Projects to support Faculty members and Researchers and the procurement of high-cost research equipment grant” (Project ALAS – “ALiens in the Aegean – a Sea under siege” (Katsanevakis et al. 2020b); Project Number: HFRI-FM17-1597). Konstantinos Tsirintanis was co-financed by Greece and the European Union (European Social Fund-ESF) through the Operational Programme “Human Resources Development, Education and Lifelong Learning”, 2014-2020, in the context of the Act “Enhancing Human Resources Research Potential by undertaking a Doctoral Research” Sub-action 2: IKY Scholarship Programme for PhD candidates in the Greek Universities. Maria Zotou was supported by the project “Coastal Environment Observatory and Risk Management in Island Regions AEGIS+” (MIS 5047038), implemented within the Operational Programme “Competitiveness, Entrepreneurship and Innovation” (NSRF 2014-2020), co financed by the Hellenic Government (Ministry of Development and Investments) and the European Union (European Regional Development Fund, Cohesion Fund). Razy Hoffman was supported by Yad-Hanadiv Foundation, through the Israel Society of Ecology and Environmental Sciences and Israel Nature and Parks Authority, an integrated program for establishing biological baselines and monitoring protocols for marine reserves in the Israeli Mediterranean Sea (Grant #10669). Tatiana Begun, Adrian Teaca and Mihaela Muresan were supported by the European Union’s Horizon 2020 BRIDGE-BS project under grant agreement no. 101000240. Fiona Tomas was supported by the project “Invasion of the tropical alga Halimeda incrassata in the Balearic Islands: ecology and invasion dynamics (AAEE119/2017)”, funded by the Vicepresidencia y Consejería de Innovación, Investigación y Turismo del Govern de les Illes Balears, with support from the European Union and FEDER funds, and the project “Una nueva alga invasora en el Mediterráneo: invasibilidad, detección y erradicación del alga tropical Halimeda incrassata (INVHALI)”, funded by the Fundación Biodiversidad, del Ministerio para la Transición Ecológica y el Reto Demográfico. Simonetta Fraschetti, Laura Tamburello, Antonia Chiarore were supported by the project PO FEAMP 2014-2020 - DRD n. 35/2019, “Innovazione, sviluppo e sostenibilità nel settore della pesca e dell'acquacoltura per la Regione Campania” (ISSPA 2.51) and the EU EASME - EMFF (Sustainable Blue Econ-omy) Project AFRIMED (http://afrimed-project.eu/, grant agreement N. 789059). Carlos Jimenez, Louis Hadjioannou, Vasilis Resaikos, Valentina Fossati, Magdalene Papatheodoulou, and Antonis Petrou were supported by MedPan Small Projects, Mava, and LIFE-IP. Louis Hadjioannou, Manos L. Moraitis and Neophytos Agrotis received funding from the European Union’s Horizon 2020 research and innovation program within the framework of the CMMI/MaRITeC-X project under grant agreement No. 857586. Ernesto Azzurro was supported by the project USEIt - Utilizzo di Sinergie operative per la gestione integrata specie aliene Invasive in Italia, funded by the research programme @CNR. Antonietta Rosso and Francesco Sciuto were supported by the University of Catania through “PiaCeRi-Piano Incentivi per la Ricerca di Ateneo 2020–22 linea di intervento 2.” This is the Catania Paleoecological Research Group contribution n. 484. Diego K. Kersting was supported by the Beatriu de Pinós programme funded by the Secretary of Universities and Research (Government of Catalonia) and the Horizon 2020 programme of research and innovation of the European Union under the Marie Sklodowska-Curie grant agreement No 801370. Francesco Tiralongo was supported by the AlienFish project of Ente Fauna Marina Mediterranea (Scientific Organization for Research and Conservation of Marine Biodiversity, 96012 Avola, Italy), a citizen science project for monitoring and studying rare and non-indigenous fish in Italian waters. Adriana Vella, was supported by funds through the BioCon_Innovate Research Excellence Grant from the University of Malta awarded to her. Noel Vella was supported by REACH HIGH Scholars Programme-Post Doctoral Grant for the FINS project. Some of the records provided by Victor Surugiu were obtained during surveys carried out within the framework of the project “Adequate management of invasive species in Romania, in accordance with EU Regulation 1143/2014 on the prevention and management of the introduction and spread of invasive alien species”, SMIS 2014+ 120008, coordinated by the Romanian Ministry of Environment, Water and Forests in partnership with the University of Bucharest (2018–2022). Alan Deidun and Alessio Marrone were supported by the “Spot The Alien” citizen science campaign for the monitoring of the Alien species in the Maltese archipelago and by the Interreg Italia-Malta Harmony project. The authors from the National Institute of Biology (Slovenia) acknowledge the financial support of the Slovenian Research Agency (Research Core Funding No. P1-0237) and of the Ministry of Agriculture, Forestry and Food (project “Survey of the species richness and abundance of alien species in the Slovenian Sea”). Emanuele Mancini and Fabio Collepardo Coccia were supported by the project PO-FEAMP 2014-2020 “BIOBLITZ: research, knowledge and participation for the sustainable management of marine resources (BioBlitz Blu 2020)” coordinated by CURSA for MIPAAF, the Italian Ministry of Agricultural, Food and Forestry Policies, Measure 1.40 - Protection and restoration of biodiversity and marine ecosystems and compensation schemes in the context of sustainable fishing activities. Daniele Grech was supported by the PO-FEAMP 2014-2020 project ECOGESTOCK “Approccio ECOsistemico per la tutela e la GEStione delle risorse biologiche e STOCK ittici nelle acque interne”, the citizen science project Progetto Fucales: chi le ha viste? and the Paralenz Every dive counts sponsor. Jamila Rizgalla was supported by the project Snowball for the monitoring of alien species in Libyan waters له اهتفش له اهتدطصا ؟) have you seen it have you fished it?). Gerasimos Kondylatos and Dimitrios Mavrouleas were supported by the project “EXPLIAS” (MIS (ΟΠΣ): 5049912), design and piloting methods of commercial exploitation of invasive alien species with a view to contributing to their population control, coordinated by the National Technical University of Athens with the collaboration of the Hellenic Centre for Marine Research and the University of the Aegean and co-founded by Greece and the European Union. G. Kondylatos and Savvas Nikolidakis were supported by the project “SAMOS” (ID CODE: 32.2072004/001), a study for a submarine productive park in Marathokampos of Samos. Paraskevi K. Karachle, Aikaterini Dogrammatzi, Giorgos A. Apostolopoulos, Kassiani Konida and Melina Nalmpanti were supported by the project “4ALIEN: Biology and the potential economic exploitation of four alien species in the Hellenic Seas”, funded by NRSF 2017-2020 (MIS (ΟΠΣ): 5049511). Fabio Crocetta and Riccardo Virgili were partially funded by the project PO FEAMP Campania 2014–2020, DRD n. 35 of 15th March 2018, Innovazione, sviluppo e sostenibilità nel settore della pesca e dell’acquacoltura per la regione Campania, Misura 2.51, WP5, Task 5.5 Presenza e distribuzione di specie non indigene del macrozoobenthos e del necton in Campania. Michel Bariche was partially funded by the University Research Board of the American University of Beirut (DDF 103951/2592). Constantinos G. Georgiadis, Dimitra Lida Rammou, Paschalis Papadamakis and Sotiris Orfanidis were supported by the MSFD monitoring program. Sonia Smeraldo was supported by the MPA-Engage project, led by the Institute of Marine Sciences of the Spanish National Research Council and funded by the Interreg MED program. Evgeniia Karpova acknowledge that the publication of this article was in part carried out within the framework of the state assignment of the FRC IBSS “Patterns of Formation and Anthropogenic Transformation of Biodiversity and Bioresources of the Azov– Black Sea Basin and Other Regions of the World Ocean” (No. 121030100028-0). Elena Slynko’s work was carried out within the framework of a State Assignment no. 121051100109-1 of IBIW RAS. Manuela Falautano and Luca Castriota were supported by ISPRA citizen science campaigns for the monitoring of alien species through the dedicated institutional project ([email protected]). María Altamirano was supported by the project RUGULOPTERYX funded by Fundación Biodiversidad-Ministerio para la Transición Ecológica y el reto Demográfico (Spain) and the project UMA20-FEDERJA-006 with support from the European Union and FEDER funds and Junta de Andalucía. Records provided by L. Mangialajo were collected in the framework of projects funded by the Pew Charitable Trust, by the European Commission (AFRIMED, http://afrimed-project.eu/, grant agreement N. 789059) and by the Académie 3 de l’Université Côte d’Azur (projet CONVOST).Peer reviewe

Unpublished Mediterranean and Black Sea records of marine alien, cryptogenic, and neonative species

To enrich spatio-temporal information on the distribution of alien, cryptogenic, and neonative species in the Mediterranean and the Black Sea, a collective effort by 173 marine scientists was made to provide unpublished records and make them open access to the scientific community. Through this effort, we collected and harmonized a dataset of 12,649 records. It includes 247 taxa, of which 217 are Animalia, 25 Plantae and 5 Chromista, from 23 countries surrounding the Mediterranean and the Black Sea. Chordata was the most abundant taxonomic group, followed by Arthropoda, Mollusca, and Annelida. In terms of species records, Siganus luridus, Siganus rivulatus, Saurida lessepsianus, Pterois miles, Upeneus moluccensis, Charybdis (Archias) longicollis, and Caulerpa cylindracea were the most numerous. The temporal distribution of the records ranges from 1973 to 2022, with 44% of the records in 2020–2021. Lethrinus borbonicus is reported for the first time in the Mediterranean Sea, while Pomatoschistus quagga, Caulerpa cylindracea, Grateloupia turuturu, and Misophria pallida are first records for the Black Sea; Kapraunia schneideri is recorded for the second time in the Mediterranean and for the first time in Israel; Prionospio depauperata and Pseudonereis anomala are reported for the first time from the Sea of Marmara. Many first country records are also included, namely: Amathia verticillata (Montenegro), Ampithoe valida (Italy), Antithamnion amphigeneum (Greece), Clavelina oblonga (Tunisia and Slovenia), Dendostrea cf. folium (Syria), Epinephelus fasciatus (Tunisia), Ganonema farinosum (Montenegro), Macrorhynchia philippina (Tunisia), Marenzelleria neglecta (Romania), Paratapes textilis (Tunisia), and Botrylloides diegensis (Tunisia).peer-reviewe

Évaluation de l'efficacité des aires marines protégées pour soutenir les petits métiers de la pêche (perspectives écologiques et de gestion de la Méditerranée française)

Marine protected areas (MPAs) are increasingly being implemented as a fisheries management tool. The continued decline of worldwide capture fisheries gives an impetus for studying how MPAs could sustain fisheries. Despite the growing MPA literature, many ecological effects have remained understudied. This doctoral thesis aimed to examine how MPAs can benefit small-scale fisheries, particularly in the French Mediterranean. Field experiments were conducted in the Cap Roux Fishery Reserve, Saint-Raphaël to determine the effects of protection on adult fish communities, recruitment and adjacent fisheries. Indirect effects of protection were detected, particularly on trophic interactions. Mortality of juvenile fish was higher inside the reserve compared to fished areas as seen from surveys of newly-settled Diplodus sargus in their nursery habitats and a caging experiment using recently-settled Symphodus ocellatus in artificial habitats. The mortality patterns were attributed to higher predation inside the reserve. Stable isotope analyses revealed that fish species with higher trophic levels were caught inside the reserve. Meanwhile, catch yields from experimental fishing were higher inside the reserve than in fished areas but decreased with distance from the center of the reserve. Spillover effect was not observed, which could be explained by several factors: poaching or fishing along the boundary which could offset any gains from protection, reserve size which could be incompatible with natural fish home ranges, and the age of the reserve which could still be young for full biomass recovery. These factors should be considered in the management of the Cap Roux Fishery Reserve.Les Aires Marines Protégées (AMPs) sont de en plus utilisées comme stratégie de gestion de la pêche. Le déclin continuel de la production mondiale des captures de pêche renforce la nécessité d étudier si ces AMPs pourraient permettre d augmenter à nouveau et de soutenir le rendement des pêches. Malgré une littérature croissante sur le thème des AMPs, de nombreux effets écologiques n ont pas encore été suffisamment étudiés pour étayer cela. Cette thèse de doctorat a pour but de déterminer comment les AMPs peuvent bénéficier à la pêche aux petits métiers, plus particulièrement en Méditerranée française. Le travail de terrain a été réalisé au sein du Cantonnement de Pêche du Cap Roux, Saint-Raphaël afin de déterminer les effets de la protection sur les peuplements de poissons adultes, le recrutement des juvéniles et le rendement des pêches effectuées à proximité. Des effets indirects de la protection ont été mis en évidence notamment par l étude des interactions trophiques. Une mortalité des juvéniles de poissons plus importante à l intérieur de la réserve que dans les zones pêchées a été mise en évidence par: (i) des suivis des juvéniles de l année de Diplodus sargus dans les zones de nurseries et (ii) des expériences de caging de juvéniles de Symphodus ocellatus installés sur des substrats artificiels. Cette mortalité a été attribuée à une pression de prédation plus forte à l intérieur de la réserve. Les analyses des isotopes stables a montré que les espèces de poissons avec des niveaux trophiques mesurés plus élevés ont été capturés dans la réserve. Les rendements de captures par pêche experimentale ont été plus élevés à l intérieur de la réserve qu à l extérieur, mais a diminué avec la distance du centre de la réserve. Les retombées de la réserve ne soient pas apparentes à ce jour dans les zones périphériques. Plusieurs facteurs pourraient expliquer cela: (i) le braconnage et la pêche exercée en limite de réserve pourraient masquer les effets positifs de la protection, (ii) la taille de la réserve pourrait être incompatible avec les aires de distribution naturelle des espèces de poissons considérées et enfin (iii) la réserve pourrait être trop jeune pour permettre une augmentation de la biomasse à l extérieur de l AMP. Ces facteurs devraient être pris en considération dans le futur plan de gestion du Cantonnement de pêche du Cap Roux.NICE-BU Sciences (060882101) / SudocSudocFranceF

Sampling of Ostreopsis cf. ovata using artificial substrates: Optimization of methods for the monitoring of benthic harmful algal blooms

In the framework of monitoring of benthic harmful algal blooms (BHABs), the most commonly reported sampling strategy is based on the collection of macrophytes. However, this methodology has some inherent problems. A potential alternative method uses artificial substrates that collect resuspended benthic cells. The current study defines main improvements in this technique, through the use of fiberglass screens during a bloom of Ostreopsis cf. ovata. A novel set-up for the deployment of artificial substrates in the field was tested, using an easy clip-in system that helped restrain substrates perpendicular to the water flow. An experiment was run in order to compare the cell collection efficiency of different mesh sizes of fiberglass screens and results suggested an optimal porosity of 1-3 mm. The present study goes further on showing artificial substrates, such as fiberglass screens, as efficient tools for the monitoring and mitigation of BHABs. (C) 2016 Elsevier Ltd. All rights reserved

Reduction of herbivorous fish pressure can facilitate focal algal species forestation on artificial structures

Coastal areas have been transformed worldwide by urbanization, so that artificial structures are now widespread. Current coastal development locally depletes many native marine species, while offering limited possibilities for their expansion. Eco-engineering interventions intend to identify ways to facilitate the presence of focal species and their associated functions on artificial habitats. An important but overlooked factor controlling restoration operations is overgrazing by herbivores. The aim of this study was to quantify the effects of different potential feeders on Cystoseira amentacea, a native canopy-forming alga of the Mediterranean infralittoral fringe, and test whether manipulation of grazing pressure can facilitate the human-guided installation of this focal species on coastal structures. Results of laboratory tests and field experiments revealed that Sarpa salpa, the only strictly native herbivorous fish in the Western Mediterranean Sea, can be a very effective grazer of C. amentacea in artificial habitats, up to as far as the infralittoral fringe, which is generally considered less accessible to fishes. S. salpa can limit the success of forestation operations in artificial novel habitats, causing up to 90% of Cystoseira loss after a few days. Other grazers, such as limpets and crabs, had only a moderate impact. Future engineering operations,intended to perform forestation of canopy-forming algae on artificial structures, should consider relevant biotic factors, such as fish overgrazing, identifying cost-effective techniques to limit their impact, as is the usual practice in restoration programmes on land