Bioinvasion impacts on biodiversity, ecosystem services, and human health in the Mediterranean Sea

Este artículo contiene 45 páginas, 20 figuras, 5 tablas.Biological invasions have become a defining feature of marine Mediterranean ecosystems with significant impacts on biodiversity, ecosystem services, and human health. We systematically reviewed the current knowledge on the impacts of marine biological invasions in the Mediterranean Sea. We screened relevant literature and applied a standardised framework that classifies mechanisms and magnitude of impacts and type of evidence. Overall, 103 alien and cryptogenic species were analysed, 59 of which were associated with both negative and positive impacts, 17 to only negative, and 13 to only positive; no impacts were found for 14 species. Evidence for most reported impacts (52%) was of medium strength, but for 32% of impact reports evidence was weak, based solely on expert judgement. Only 16% of the reported impacts were based on experimental studies. Our assessment allowed us to create an inventory of 88 alien and cryptogenic species from 16 different phyla with reported moderate to high impacts. The ten worst invasive species in terms of reported negative impacts on biodiversity include six algae, two fishes, and two molluscs, with the green alga Caulerpa cylindracea ranking first. Negative impacts on biodiversity prevailed over positive ones. Competition for resources, the creation of novel habitat through ecosystem engineering, and predation were the primary reported mechanisms of negative effects. Most cases of combined negative and positive impacts on biodiversity referred to community-level modifications. Overall, more positive than negative impacts were reported on ecosystem services, but this varied depending on the service. For human health, only negative impacts were recorded. Substantial variation was found among Mediterranean ecoregions in terms of mechanisms of impact and the taxonomic identity of impacting species. There was no evidence that the magnitude of impact increases with residence time. Holistic approaches and experimental research constitute the way forward to better understanding and managing biological invasions.The present study was supported by the Hellenic Foundation for Research and Innovation (H.F.R.I.) under the “First Call for H.F.R.I. 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”; Project Number: HFRI-FM17-1597; Katsanevakis et al. 2020b). FaCr was partially funded by the project PO FEAMP CAMPANIA 2014-2020 (DRD n.35 of 15th March 2018). XT obtained partial funding from project MARGECH (PID2020-118550RB, MCIN/AEI/10.13039/501100011033) from the Spanish Government. AR received grants from the University of Catania through “PiaCeRi-Piano Incentivi per la Ricerca di Ateneo 2020–22 linea di intervento 2”.Peer reviewe

Pinna nobilis in the Greek seas (NE Mediterranean): on the brink of extinction?

The Mediterranean endemic fan mussel Pinna nobilis is suffering an ongoing basin-scale mass mortality event (MME) since 2016. As most Mediterranean populations have collapsed, the species has been declared as Critically Endangered in the IUCN Red List of threatened species. In an effort to track the progress of the MME and provide updated information on the status of the species in the Greek seas, data collected through dedicated surveys and opportunistic assessments during 2019 and 2020 have been compiled. During surveys conducted at 258 sites, a total of 14,589 fan mussels were recorded, of which 81.1% were dead. Of the remaining 2,762 live individuals, 256 were juveniles. Two marine areas that still sustain living populations were identified, namely Kalloni Gulf (Lesvos Island), and Laganas Bay (Zakynthos Island). The inner part of Kalloni Gulf appears to maintain the largest surviving population of the species in the eastern Mediterranean, with an abundance estimate of 684,000 individuals (95% confidence interval: 322,000-1,453,000). Solitary, potentially resistant, scattered individuals were recorded at several sites. Other previously abundant populations that had been assessed in the past, specifically those of Lake Vouliagmeni (Korinthiakos Gulf), Souda Bay (Crete) and Gera Gulf (Lesvos Island) with a total of ~350,000 individuals, have now been wiped out. Our results document the collapse of most P. nobilis populations throughout the Greek seas. The MME has progressed substantially between early 2019 and mid-2020, as indicated by the increase in mortality at sites consecutively monitored multiple times. This work highlights the urgent need for continuous monitoring of surviving populations and calls for immediate implementation of an effective protection and management strategy that will ensure the persistence of surviving individuals and the production of resistant offspring

Marine invasive alien species in Europe: 9 years after the IAS Regulation

Biological invasions, resulting from human activities, exert substantial impacts on ecosystems worldwide. This review focuses on marine invasive alien species (IAS) in Europe, examining the current state, proposing strategies to address the problem, and offering recommendations for enhanced management. Effective management of biological invasions relies on accessible, accurate data to inform decision-making. Information systems such as the European Alien Species Information Network (EASIN), Aquatic Non-Indigenous and Cryptogenic Species (AquaNIS), and World Register of Introduced Marine Species (WriMS) provide comprehensive databases on IAS, but their sustainability requires long-term maintenance, continuous updates, and support. Most countries lack specific monitoring programs for marine IAS, and standardization and improvement of monitoring methods are needed. Port monitoring plays a vital role in the early detection of new arrivals, and recent advancements in molecular techniques show promise for effective IAS monitoring. Risk screening tools are commonly employed to rank taxa based on their invasiveness potential in European regions, but variations in protocols can yield inconsistent results. European impact assessments highlight resource competition, novel habitat creation, and predation as primary mechanisms for negative impacts on biodiversity, while the creation of novel habitats represents a key mechanism for positive impacts. Preventing IAS introductions is critical, and measures such as ballast water treatment systems are implemented to reduce the likelihood of marine introductions. However, understanding introduction pathways remains uncertain for many IAS. Eradication and control efforts for marine IAS have limited success, emphasizing the need for enhanced biosecurity measures. Climate change, especially ocean warming, can intensify IAS impacts on native species and ecosystems. In climate change hotspots, some tropical aliens may, however, compensate for the loss of thermally sensitive natives with similar traits. Therefore, it is imperative to consider the interactions between climate change and IAS in developing effective management and conservation strategies. Enhancing IAS management in Europe entails i) securing adequate funding, ii) expanding the list of IAS of Union Concern to adequately cover marine invasions, iii) learning from countries with successful biosecurity practices, iv) sustaining information systems, v) improving monitoring and early warning systems with innovative technologies, vi) enhancing prediction models, vii) conducting integrated impact assessments and mapping cumulative IAS impacts, and vii) considering the potential benefits of IAS in ecosystem functioning and services

Unpublished Mediterranean records of marine alien and cryptogenic species

Good datasets of geo-referenced records of alien species are a prerequisite for assessing the spatio-temporal dynamics of biological invasions, their invasive potential, and the magnitude of their impacts. However, with the exception of first records on a country level or wider regions, observations of species presence tend to remain unpublished, buried in scattered repositories or in the personal databases of experts. Through an initiative to collect, harmonize and make such unpublished data for marine alien and cryptogenic species in the Mediterranean Sea available, a large dataset comprising 5376 records was created. It includes records of 239 alien or cryptogenic taxa (192 Animalia, 24 Plantae, 23 Chromista) from 19 countries surrounding the Mediterranean Sea. In terms of records, the most reported Phyla in descending order were Chordata, Mollusca, Chlorophyta, Arthropoda, and Rhodophyta. The most recorded species was Caulerpa cylindracea, followed by Siganus luridus, Magallana sp. (cf. gigas or angulata) and Pterois miles. The dataset includes records from 1972 to 2020, with the highest number of records observed in 2018. Among the records of the dataset, Dictyota acutiloba is a first record for the Mediterranean Sea. Nine first country records are also included: the alga Caulerpa taxifolia var. distichophylla, the cube boxfish Ostracion cubicus, and the cleaner shrimp Urocaridella pulchella from Israel; the sponge Paraleucilla magna from Libya and Slovenia; the lumpfish Cyclopterus lumpus from Cyprus; the bryozoan Celleporaria vermiformis and the polychaetes Prionospio depauperata and Notomastus aberans from Malta

Search for dark matter produced in association with bottom or top quarks in √s = 13 TeV pp collisions with the ATLAS detector

A search for weakly interacting massive particle dark matter produced in association with bottom or top quarks is presented. Final states containing third-generation quarks and miss- ing transverse momentum are considered. The analysis uses 36.1 fb−1 of proton–proton collision data recorded by the ATLAS experiment at √s = 13 TeV in 2015 and 2016. No significant excess of events above the estimated backgrounds is observed. The results are in- terpreted in the framework of simplified models of spin-0 dark-matter mediators. For colour- neutral spin-0 mediators produced in association with top quarks and decaying into a pair of dark-matter particles, mediator masses below 50 GeV are excluded assuming a dark-matter candidate mass of 1 GeV and unitary couplings. For scalar and pseudoscalar mediators produced in association with bottom quarks, the search sets limits on the production cross- section of 300 times the predicted rate for mediators with masses between 10 and 50 GeV and assuming a dark-matter mass of 1 GeV and unitary coupling. Constraints on colour- charged scalar simplified models are also presented. Assuming a dark-matter particle mass of 35 GeV, mediator particles with mass below 1.1 TeV are excluded for couplings yielding a dark-matter relic density consistent with measurements

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

Invasive Fish and Sea Urchins Drive the Status of Canopy Forming Macroalgae in the Eastern Mediterranean

Canopy-forming macroalgae, such as Cystoseira sensu lato, increase the three-dimensional complexity and spatial heterogeneity of rocky reefs, enhancing biodiversity and productivity in coastal areas. Extensive loss of canopy algae has been recorded in recent decades throughout the Mediterranean Sea due to various anthropogenic pressures. In this study, we assessed the biomass of fish assemblages, sea urchin density, and the vertical distribution of macroalgal communities in the Aegean and Levantine Seas. The herbivore fish biomass was significantly higher in the South Aegean and Levantine compared to the North Aegean. Very low sea urchin densities suggest local collapses in the South Aegean and the Levantine. In most sites in the South Aegean and the Levantine, the ecological status of macroalgal communities was low or very low at depths deeper than 2 m, with limited or no canopy algae. In many sites, canopy algae were restricted to a very narrow, shallow zone, where grazing pressure may be limited due to harsh hydrodynamic conditions. Using Generalized Linear Mixed Models, we demonstrated that the presence of canopy algae is negatively correlated with the biomass of the invasive Siganus spp. and sea urchins. The loss of Cystoseira s.l. forests is alarming, and urgent conservation actions are needed

Aliens in the Aegean – a sea under siege (ALAS)

ALAS aims to fill knowledge gaps on the impacts of marine alien species in the Aegean Sea, and support marine managers and policy makers in prioritizing mitigation actions. The project will focus on under-studied alien-native interactions, priority and vulnerable habitats (such as shallow forests of canopy algae and underwater caves), and apply a multitude of approaches. It will apply a standardized, quantitative method for mapping Cumulative IMpacts of invasive Alien species on marine ecosystems (CIMPAL), according to which cumulative impact scores are estimated on the basis of the distributions of invasive species and ecosystems, and both the reported magnitude of ecological impacts and the strength of such evidence. Towards that direction, ALAS will improve our knowledge base and compile the needed information to estimate CIMPAL by (1) conducting a series of field experiments and surveys to investigate the impacts of selected invasive alien species on marine habitats, (2) producing high-resolution habitat maps in the coastal zone, refining the results of previous research efforts through fieldwork, remote sensing and satellite imaging, (3) producing species distribution models for all invasive species, based on extensive underwater surveys for the collection of new data and integrating all existing information. ALAS will incorporate skills and analyses in novel ways and provide high-resolution results at a large scale; couple classic and novel tools and follow a trans-disciplinary approach, combining knowledge from the fields of invasion biology, conservation biology, biogeography, fisheries science, marine ecology, remote sensing, statistical modelling; conduct for the first time in the Aegean Sea a comprehensive, high-resolution analysis of cumulative impacts of invasive alien species; and report results in formats appropriate for decision-makers and society, thus transferring research-based knowledge to inform and influence policy decisions