Aquatic Invasions (2022) Volume 17, Issue 3: 308–352
CORRECTED PROOF

Review

Bioinvasion impacts on biodiversity, ecosystem services, and human healthin the Mediterranean Sea
Konstantinos Tsirintanis1, Ernesto Azzurro2,3, Fabio Crocetta3, Margarita Dimiza4, Carlo Froglia2, Vasilis Gerovasileiou5,6,
Joachim Langeneck7, Giorgio Mancinelli8,9,10, Antonietta Rosso10,11, Nir Stern12, Maria Triantaphyllou4, Konstantinos
Tsiamis13, Xavier Turon14, Marc Verlaque15, Argyro Zenetos16 and Stelios Katsanevakis1,*
1 Department of Marine Sciences, University of the Aegean, Lofos Panepistimiou, 81100 Mytilene, Greece; 2 CNR-IRBIM, National Research Council.

Institute of Biological Resources and Marine Biotechnologies, Ancona, Italy; 3Department of Integrative Marine Ecology, Stazione Zoologica Anton
Dohrn, I-80121 Naples, Italy; 4Faculty of Geology & Geoenvironment, National and Kapodistrian University of Athens, Panepistimioupolis 15784,
Athens, Greece; 5Department of Environment, Faculty of Environment, Ionian University, 29100 Zakynthos, Greece; 6Hellenic Centre for Marine
Research (HCMR), Institute of Marine Biology, Biotechnology and Aquaculture (IMBBC), 71500 Heraklion, Greece; 7Department of Biology, Universityof Pisa, 56126 Pisa, Italy; 8Department of Biological and Environmental Sciences and Technologies (DiSTeBA), University of Salento, SP LecceMonteroni, 73100 Lecce, Italy; 9National Research Council – Institute of Marine Biological Resources and Biotechnologies (CNR-IRBIM), 71010
Lesina (FG), Italy; 10CoNISMa, Consorzio Nazionale Interuniversitario per le Scienze del Mare, 00196 Roma, Italy; 11Department of Biological,
Geological and Environmental Sciences, University of Catania, 95129 Catania, Italy; 12Israel Oceanographic and Limnological Research, National
Institute of Oceanography, Haifa 31080, Israel; 13Vroutou 12 Athens, 11141, Greece; 14Centre for Advanced Studies of Blanes (CEAB, CSIC), 17300
Blanes, Catalonia, Spain; 15Aix Marseille University and Université de Toulon, CNRS, IRD, Mediterranean Institute of Oceanography (MIO), UM 110,
Marseille, France; 16Institute of Marine Biological Resources & Inland Waters (IMBRIW), Hellenic Centre for Marine Research (HCMR), 16452,
Argyroupolis, Greece*Corresponding author
E-mail: stelios@katsanevakis.com
Citation: Tsirintanis K, Azzurro E,
Crocetta F, Dimiza M, Froglia C,
Gerovasileiou V, Langeneck J, Mancinelli G,
Rosso A, Stern N, Triantaphyllou M,
Tsiamis K, Turon X, Verlaque M, Zenetos A,
Katsanevakis S (2022) Bioinvasion
impacts on biodiversity, ecosystemservices, and human health in the
Mediterranean Sea. Aquatic Invasions
17(3): 308–352, https://doi.org/10.3391/ai.
2022.17.3.01

Received: 20 December 2021
Accepted: 19 May 2022
Published: 5 July 2022
Thematic editor: Charles Martin
Copyright: © Tsirintanis et al.
This is an open access article distributed under termsof the Creative Commons Attribution License(Attribution 4.0 International - CC BY 4.0).

OPEN ACCESS.

Abstract
Biological invasions have become a defining feature of marine Mediterranean
ecosystems with significant impacts on biodiversity, ecosystem services, and humanhealth. We systematically reviewed the current knowledge on the impacts of marine
biological invasions in the Mediterranean Sea. We screened relevant literature andapplied a standardised framework that classifies mechanisms and magnitude of impacts
and type of evidence. Overall, 103 alien and cryptogenic species were analysed, 59 ofwhich 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 basedon experimental studies. Our assessment allowed us to create an inventory of 88 alienand cryptogenic species from 16 different phyla with reported moderate to highimpacts. 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 ofcombined negative and positive impacts on biodiversity referred to community-level
modifications. Overall, more positive than negative impacts were reported on ecosystemservices, but this varied depending on the service. For human health, only negative
impacts were recorded. Substantial variation was found among Mediterranean ecoregionsin 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.

Key words: alien species, cryptogenic, effects, experiments, expert judgement,
modelling, systematic review

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Introduction
The rate of human-mediated introduction of species to new areas is highand accelerating all over the world (Seebens et al. 2017; Pyšek et al. 2020),
with heavy and rising associated economic costs (Diagne et al. 2021).
Modern biological invasions constitute a unique form of global environmental
change, profound enough to surpass natural drivers of selection anddispersal, creating novel biological communities that would have neveremerged through natural processes (Ricciardi 2007). In the ecologicaldomain, the integration of novel species in the ecosystems can generate
fundamental alterations to the structure of native communities andecosystem functioning (e.g., Vitousek et al. 1996; Kideys 2002; Pranovi etal. 2006; Galil 2007; Ehrenfeld 2010; Vilà et al. 2011; Katsanevakis et al.
2014a; Howard et al. 2019), often with detrimental losses of native
biodiversity (e.g., Clavero et al. 2009; Sala et al. 2011; Harper and Bunbury
2015; Bellard et al. 2016; Doherty et al. 2016; García-Gómez et al. 2020).
The provision of ecosystem services can also be strongly affected by the
impacts of biological invasions (Vilà et al. 2010; Katsanevakis et al. 2014a;
Vilà and Hulme 2017; Castro-Díez et al. 2019). Furthermore, invasive
species pose a threat to human health through a variety of mechanisms
such as pathogen transmission, intoxication, and envenomation (Schaffner
et al. 2013; Hulme 2014; Galil 2018; Peyton et al. 2019; Bédry et al. 2021).
Recent works highlighted that biological invasions can also have positive
outcomes (Katsanevakis et al. 2014a; Vimercati et al. 2020), for example bycreating novel ecosystems that may support native biodiversity and ecosystem
functioning (Hobbs et al. 2009; Schlaepfer et al. 2011; Evers et al. 2018),
providing ecosystem services (Katsanevakis et al. 2018; Apostolaki et al.
2019), and contributing to human well-being (Shackleton et al. 2019; Sfriso
et al. 2020). The positive impacts of alien species are dependent on societal
perception and different cultural values and motivations (Simberloff et al.
2013) and are commonly underestimated (Katsanevakis et al. 2014a).
Nevertheless, their study is receiving increasing attention (Vimercati et al.
2020) and, in some cases, alien species can even constitute targets forprotection and conservation (Schlaepfer et al. 2011; Mačić et al. 2018).
Impact assessment (including both negative and positive impacts ofbiological invasions) is an important but challenging process aiming toquantify the magnitude of changes and prioritise management and mitigationof undesired effects (Parker et al. 1999; Kumschick et al. 2012; Ricciardi etal. 2013; Simberloff et al. 2013; Ojaveer et al. 2015). The utilisation ofconceptual frameworks that classify in a standard way the effects of alien
species on ecosystems is essential in the process (Blackburn et al. 2011;
Bacher et al. 2018). Katsanevakis et al. (2014a) assessed the impacts ofmarine alien species on biodiversity and ecosystem services utilising aframework that emphasised the robustness of the reported evidence andTsirintanis et al. (2022), Aquatic Invasions 17(3): 308–352, https://doi.org/10.3391/ai.2022.17.3.01

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Figure 1. Mediterranean Sea ecoregions (sensu Spalding et al. 2007). The present review covered
all seven Mediterranean ecoregions.

the ecological mechanisms of negative and positive impacts on bothbiodiversity and ecosystem services. Blackburn et al. (2014) proposed aclassification framework of impact magnitude levels for a series of
ecological mechanisms through which alien species impact individuals,
populations, and communities. Difficulties that hinder impact assessments,
such as a wide range of taxonomic groups, various types of affected
habitats, estimation of impact magnitude, and spatial quantification of
impacts, can be overcome through the application of such schemes(Kumschick et al. 2015; Katsanevakis et al. 2016; Nentwig et al. 2016;
Galanidi et al. 2018).
The Mediterranean Sea is a hotspot of biodiversity with a high level ofendemism (Coll et al. 2010). It is divided into seven marine ecoregions(Figure 1), each with a distinct suite of oceanographic and topographic
features and relatively homogeneous species composition (Spalding et al.
2007). In addition, the Mediterranean is a hotspot of biological invasions,particularly throughout its eastern part, having the highest number of
introduced species than any other sea region of the world (Costello et al.
2021). In the same easternmost sectors, under a rapid warming trend,
many thermally-sensitive native populations have collapsed in the past few
decades (Yeruham et al. 2015; Rilov 2016; Albano et al. 2021) and in somecases alien species are the only ones that can sustain ecosystem functions.
Hence, a shift in conservation strategies from protecting native biodiversity
to protecting ecosystem functions (thus also including some alien species
as conservation targets) has been recently proposed (Katsanevakis et al.
2020a).
Approximately 1,000 species are estimated to have been introduced inMediterranean ecoregions (Zenetos et al. 2010, 2012), with more than half
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having established populations (Galil et al. 2016; Zenetos et al. 2017;
Zenetos and Galanidi 2020) and exhibiting an accelerating rate ofestablishment success during recent years (Zenetos et al. 2022). Biologicalinvasions in the Mediterranean have caused large-scale biogeographic
modifications, range shifts of native species, population declines or even
local extinctions (Galil 2007; Edelist et al. 2013; Katsanevakis et al. 2014a).
Previous assessments of the spatial variation of impacts in the Mediterranean
Sea indicated strong spatial heterogeneity, not significantly correlated toalien species richness (Katsanevakis et al. 2016). As the situation changes
fast, with many new alien species becoming invasive and expanding rapidly
in the last few years (e.g., Dimitriadis et al. 2020; Zenetos and Galanidi2020), and as new knowledge accumulates, a regular reassessment of
impacts is important to adequately inform management measures.
With the purpose to update the current knowledge on invasive alienmarine species’ impacts on Mediterranean ecosystems, a new systematic
literature review was conducted building upon the work of Katsanevakis et al.
(2014a). To accomplish this, we compiled and assessed published available
information on alien and cryptogenic species impacts to: (i) identify
impactful species for biodiversity, ecosystem services, and human health,
updating previous knowledge, (ii) assess the magnitude and mechanisms of
their impacts, and their variability across Mediterranean Sea ecoregions,and (iii) propose an inventory of the impactful marine alien species of theMediterranean Sea.

Materials and methods
List of assessed species
A list of targeted taxa for impact assessments was compiled, including
marine alien and cryptogenic species flagged as of “High Impact” in theEuropean Alien Species Information Network (EASIN; Katsanevakis et al.
2012) or as high-impact or invasive in recently published reviews (e.g.
Otero et al. 2013; Katsanevakis et al. 2014a; Karachle et al. 2017; Galanidi etal. 2018; Zenetos et al. 2018; Peyton et al. 2019; Tsiamis et al. 2020). Basedon their expert knowledge, the authors added to the list further invasive
species not previously considered by EASIN or the aforementioned
reviews. Diatoms, dinoflagellates and other microalgae were not includedin the initial species list, based on Gómez (2008, 2019) who argued about
the difficulties and uncertainties in defining the native distribution of suchspecies. Tsiamis et al. (2021) have agreed that there are large gaps inknowledge on unicellular plankton species and that more work is neededon marine non-indigenous phytoplankton species in Europe before tagging
any phytoplankton species as alien. In total, 103 alien and cryptogenic
species belonging to 16 different taxonomic groups were assessed for theirimpacts on biodiversity, ecosystem services, and human health in the
Mediterranean Sea.
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Literature review
A bibliographical review was performed for each targeted species, using the
Scholar Google search engine, as it includes grey literature (i.e. technicalreports, PhD and MSc theses, and conference proceedings) in addition topeer-reviewed journal articles. Species previously assessed by Katsanevakis
et al. (2014a) were updated by searching for more recent publications(between 2013 and March 2021), whereas the bibliographic search was
performed without chronological restrictions for those species notpreviously assessed. For each species, eligible documents were those withthe following set of keywords (anywhere in the article): <species name>
AND “impact” AND “Mediterranean”. The search provided 62,043 articles(sum of the articles found for each separate species search) but included
duplicates as some articles covered more than one target species. Potentiallyeligible papers to be included in the review were initially screened based on
their titles and abstracts; for those that passed the initial screening, the fulltext was reviewed. At a later stage, taxonomic experts further enriched thelist of selected studies with additional documents that had not been foundthrough the literature search. In total, 593 studies that included relevant
information on negative or positive impacts of alien and cryptogenic
species were retained for the analysis.
From each retained paper, the following information was extracted andcoded: DOI/link; short reference; year of publication; Mediterraneanecoregion (according to Spalding et al. 2007; Figure 1); species name andphylum following WoRMS (WoRMS Editorial Board 2021); and reported
negative or positive impact on biodiversity, ecosystem services, and humanhealth, type of evidence, mechanism of impact, magnitude of impact andecosystem engineer type, if relevant (the latter two only for impacts on
biodiversity). Only impacts referring to the Mediterranean Sea were
included; potential impacts, e.g. based on evidence in non-Mediterranean
regions, were not considered.

Framework for impact assessment
Type of evidence refers to the robustness of the methodological approachthat was applied to assess the impact. As such, the robustness of the reported
evidence was classified into six different types corresponding to three strengthof evidence categories (Katsanevakis et al. 2014a, 2016). The six evidence
types were: (i) manipulative experiments and (ii) natural experiments (highstrength of evidence), (iii) direct observations, (iv) modelling, (v) non–experimental-based correlations (medium strength of evidence), and(vi) expert judgement (low strength of evidence). Manipulative experiments
are field or laboratory experiments that include treatments/control andrandom selection of experimental units. In natural experiments, theexperimental units (i.e. controls or impacted areas) are selected by nature
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Figure 2. Main mechanisms through which marine alien species impact biodiversity (sensu
Katsanevakis et al. 2014a). Red background refers to negative impacts and green backgroundrefers to positive impacts.

(i.e. not randomly). Direct observations are direct raw measurements of
the impact about which there is no doubt (e.g. fouling in aquaculture or on
fishing gear, new commodities in fish markets). Modelling refers tomodelled consequences on biodiversity, ecosystem services and humanhealth derived from ecosystem models. Non-experimental-based correlations
refer to significant correlations between the targeted species and theinvestigated impact, but not based on an experimental design for datacollection (e.g. there was a negative correlation between the biomass of analien predator and the biomass of its native prey). Expert judgement is aqualitative or semi-quantitative assessment that relies on the empiricalknowledge of experts based on the species’ traits or the reported impact ofsimilar or the same species in a different geographical region.
Each reported impact was linked to the underlying mechanism.
Mechanisms of impact were classified according to Katsanevakis et al.
(2014a), with some additions (see Figure 2 for biodiversity; Figure 3 forregulating and maintenance ecosystem services; Figure 4 for cultural,
provisioning ecosystem services, and human health). The impact magnitude
was classified following the five-level classification proposed by Blackburn
et al. (2014), i.e. minimal, minor, moderate, major, and massive (Table 1),
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Figure 3. Main mechanisms through which marine alien species impact regulating andmaintenance ecosystem services (sensu Liquete et al. 2013). Red background refers to negative
impacts while green background refers to positive impacts. The classification of impacts on
ecosystem services was based on Katsanevakis et al. (2014a).

considering also Volery et al. (2020). The selection of marine ecosystemservices classification was based on Liquete et al. (2013), who proposed aclassification of 14 marine ecosystem services grouped as “provisioning”,“regulating and maintenance”, and “cultural” (Table 2). Ecosystem engineers
were categorised into four different types: structural, chemical, light engineers,and bioturbators (Wallentinus and Nyberg 2007; Berke 2010; Katsanevakis
et al. 2014a; Figure 5).

Analyses
In addition to descriptive statistics, contingency table analyses wereconducted to quantify the degree of association between selected pairs ofvariables. The hypothesis of independence between such pairs was tested
via chi-square tests. To avoid having cells with < 5 observations, certain
categories within each variable were grouped. Hierarchical cluster analysis,using Euclidean distance and square-root transformation of the number ofimpact records by each mechanism for each species, was performed todetermine the similarities of the analysed species in terms of themechanisms of their impacts for both negative and positive records.
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Figure 4. Main mechanisms through which marine alien species impact provisioning, cultural
ecosystem services (sensu Liquete et al. 2013) and human health. Red background refers tonegative impacts while green background refers to positive impacts. The classification of
impacts on ecosystem services was based on Katsanevakis et al. (2014a), with the exception of
categories marked with an asterisk (*) that are new.

To test the hypothesis that the magnitude of reported impacts on
biodiversity increases with the residence time, i.e. the number of years
passed since the first detection of the species in the Mediterranean Sea, we
followed two different approaches. In the first approach, a one-way
ANOVA was conducted with the maximum reported magnitude of impact
on biodiversity for each species as the categorical factor and the residence
time as the dependent variable. Levene’s test was applied to test homogeneityof variances, and Tukey’s honestly significant difference (HSD) procedure
for multiple range tests. In the second approach, we created an impact
score in which for each species all reports of impacts were summed up in aweighted sum with varying weights depending on the magnitude of impact:
massive 4; major 3; moderate 2; minor 1; minimal 0. The relationshipbetween the impact score and the residence time of each species wasinvestigated with a linear regression approach. All analyses were conductedusing Statgraphics Centurion XVI.
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Table 1. Impact magnitude classification levels with criteria description (adapted from Blackburn et al. 2014, considering also
Volery et al. 2020), referring to both negative and positive impacts.
Impact magnitude

Criteria description

MinimalNo effect on fitness of native species; negligible impact on native species due to competition, predation,parasitism, toxicity, bio-fouling, food provision or control of another invasive species; no effects on
ecosystem processes and ecosystem functioning; no chemical, physical or structural impact on theecosystem (not an ecosystem engineer).

Minor

Impact on individual of a native species due to competition, predation, parasitism, toxicity, bio-fouling, foodprovision, or control of another invasive species without substantial population changes; minor impact on
ecosystem processes and ecosystem functioning with no related population changes; any environmental or
habitat alterations in chemical, physical or structural characteristics do not result in population changes.

Moderate

Native species population changes due to competition, predation, parasitism, toxicity, bio-fouling, foodprovision or control of another invasive species but without changes in community composition; or impact
on ecosystem processes and ecosystem functioning resulting in population declines/increases but nosubstantial change in species composition; or ecological engineering, resulting in population
declines/increases but no substantial change in community composition.

Major

Changes in community composition through local or global extinction (negative) or re-establishment(positive) of at least one native species, because of competition, predation, parasitism, toxicity, bio-fouling,food provision or control of another invasive species; impact on ecosystem processes and ecosystem
functioning resulting in species composition changes; or ecological engineering, resulting in change incommunity composition. Major magnitude applies when under the hypothetical scenario of the alien species
extinction, the induced changes are considered as reversible within 10 years or within 3 generations of theextinct/re-established native taxon/ -a, whichever is longer.

Massive

Same conditions as in “major” magnitude, but changes are considered as irreversible under the hypotheticalscenario of the alien species extinction, within 10 years or within 3 generations of the extinct/re-establishednative taxon/-a.

Results
Impact matrix
The 593 studies on the 103 alien and cryptogenic species resulted in 1,343
records of negative and positive impacts on biodiversity, ecosystemservices, and human health (Table 3). A detailed description of impacts foreach species is given in the online Supplementary material Appendix 1.
Among the analysed taxa, Osteichthyes was the most numerous group(24 species), followed by Mollusca (17 species), and Arthropoda(Crustacea) (14 species), whereas 25 macroalgae were analysed, belonging
to Rhodophyta (12 species), Chlorophyta (8 species), and Ochrophyta(5 species). Biodiversity was impacted by 70% of the studied species (72taxa; Table 3), whereas the remaining ones (30%) showed no reported
impacts on biodiversity. Only 3% of the studied species had only positiveeffects on biodiversity, whereas 27% had only negative ones. In most cases(40%) the studied species impacted biodiversity both negatively and positively.
Among the 72 species impacting biodiversity, 38 represented ecosystemengineers that caused alterations to the studied ecosystem as bioconstructors(structural engineers), regulators of light penetration (light engineers),
modifiers of the chemical matrix of the environment (chemical engineers),
and bioturbators (Table 3). Most ecosystem engineers were macroalgae(phyla Ochrophyta, Chlorophyta, and Rhodophyta) and Mollusca.
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Table 2. The applied marine ecosystem services classification scheme, with a description of each service (sensu Liquete et al. 2013).
Ecosystem service

Category

Description

Food provision

Provisioning

Provision of biomass from the marine environment for humanconsumption. This includes all industrial, artisanal andrecreational fishing activities and aquaculture.

Water storage and provision

Provisioning

Provision of water for human consumption and other uses. In themarine environment, these uses are mainly associated with coastallakes, deltaic aquifers, desalination plants, industrial coolingprocesses, and coastal aquaculture in ponds and raceways.

Biotic materials and biofuels

Provisioning

Provision of biomass or biotic elements for non-food purposes,
including medicinal (e.g. drugs, cosmetics), ornamental (e.g.
corals, shells) and other commercial or industrial purposes, suchas fishmeal, algal or plant fertilisers, and biomass to produce
energy or biogas from decomposing material.

Water purification

Regulating and maintenance Biochemical and physicochemical processes involved in theremoval of wastes and pollutants from the aquatic environment,
including treatment of human waste, dilution, sedimentation,
trapping or sequestration (e.g. of pesticide residues or industrial
pollution); bioremediation; oxygenation of “dead zones”,
filtration and absorption; remineralisation; and decomposition.

Air quality regulation

Regulating and maintenance Regulation of air pollutant concentrations in the lower
atmosphere.

Coastal protection

Regulating and maintenance Natural protection of the coastal zone against inundation anderosion from waves, storms or sea level rise by biogenic andgeologic structures that disrupt water movement and thus stabilise
sediments or create protective buffer zones.

Climate regulation

Regulating and maintenance The ocean acts as a sink for greenhouse and climate active gasses,
as inorganic carbon is dissolved into the seawater and used bymarine organisms, a percentage of which is sequestered; perennial
large algae and higher plants can store carbon for longer periods.

Weather regulation

Regulating and maintenance Influence on the local weather conditions, e.g. the influence ofcoastal vegetation and wetlands on air moisture and, eventually,on the saturation point and cloud formation.

Ocean nourishment

Regulating and maintenance Natural cycling processes leading to the availability of nutrients inseawater for the production of organic matter.

Lifecycle maintenanceRegulating and maintenance The biological and physical support to facilitate the healthy anddiverse reproduction of species; this mainly refers to themaintenance of key habitats that act as nurseries, spawning areas
or migratory routes.

Biological regulation

Regulating and maintenance Biological control of pests. The control of pathogens especially inaquaculture installations, the role of cleaner fish in reefs,
biological control on the spread of vector borne human diseases,
and the control of invasive species.

Symbolic and aesthetic values

CulturalThis is about the exaltation of senses and emotions by seascapes,
habitats or species, and values put on coastal natural and culturalsites, and on the existence and beauty of charismatic habitats andspecies such as corals or marine mammals.

Recreation and tourism

CulturalOpportunities that the marine environment provides for relaxationand entertainment, including coastal activities such as bathing,sunbathing, snorkelling, SCUBA diving, and offshore activities
such as sailing, recreational fishing, and whale watching.

Cognitive effects

CulturalInspiration for arts and applications (e.g. architectural designs
inspired by marine shells, medical applications replicating marineorganic compounds), material for research and education (e.g. as
test organisms for biological experiments), information andawareness (e.g. respect for nature through the observation ofmarine wild life).

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Figure 5. Ecosystem engineer types with impacts on biodiversity (both negative and positive).

Food provision (commercial and recreational fishing, aquaculture) was
the most impacted ecosystem service, with 33 species causing negative
impacts, 18 positive impacts, and 14 both (Table 3). Osteichthyes were thetaxonomic group including the highest number of species with an impact
on food provision (19 species). All impacts caused by macroalgae (in total
15 species) on this service were negative. The cultural ecosystem service of“cognitive effects” had the second-highest number of impactful species,
with most of the studied taxa affecting this service positively, as they
constituted model species for biomonitoring or in vitro research studies.
Among regulating and maintenance services, “life-cycle maintenance” and“climate regulation” were affected by the highest number of species.
Human health impacts were all negative, caused by 9 species.

Impacts on biodiversity
More negative than positive impacts on biodiversity were reported, with468 records (78%) against 129 (22%) (Figure 6A). Caulerpa cylindracea was
the invasive species for which most negative impacts on biodiversity werereported, with 53 cases. This chlorophyte of Australian origin thrives in avariety of habitats, depths and environmental conditions, and negatively
affects species and communities in multiple ways (see Appendix 1). The
species is widespread in the Mediterranean and so are its effects on
biodiversity. Womersleyella setacea and Lophocladia lallemandii followedin terms of negative impact records. These invasive rhodophytes form dense
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Table 3. Impact Matrix: Negative (red) and positive (green) impacts of marine alien and cryptogenic species on biodiversity andecosystem services of the Mediterranean. Colour indicates strength of evidence (vivid colours for high strength of evidence,
medium for medium strength, pale colours for low strength). For species without reported impacts or minimal impacts grey cells
are depicted for biodiversity and blank cells for ecosystem services and human health. Type of evidence is indicated for each
impact: Manipulative Experiments, E; Natural Experiments, N; Direct Observations of impact, O; Modelling, M; nonexperimental-based Correlations, C; Expert Judgement, J. (Cr): Cryptogenic species.

Human health

HealthCognitive benefits

Recreation and tourism

Biological regulation

Symbolic and aesthetic values

CulturalLifecycle maintenanceJ

Weather regulation

J

Ocean nourishment

Air quality regulation

Regulating and maintenance

Water purification

Water Storage and provision

Biotic materials and biofuels

Food provision

Ecosystem engineer

Provisioning

Climate regulation

Haplosporidium pinnae (Cr)Impact on marine ecosystem services and human healthCoastal protection

Alien Species
Cercozoa

Impact on species / communities

Minimal / No impact

Impact on biodiversity

NOJ

Foraminifera
Amphistegina lobifera

CJ

J

O

NJ

Ochrophyta
Chrysonephos lewisii
Rugulopteryx okamurae

O

O

NOCJ

NO

N

O

Sargassum muticum

J

OCJ

O

O

Stypopodium schimperi

OJ

OJ

O

Undaria pinnatifida

J

O

O

ENOMCJ

NOCJ

ENOJ

J

J

EJ

ENOJ

ENOJ

NO

OJ

J

J EJ

EJ

N

N

O

J

J

J

O

NO

J

J

J

J
O

J

O

O

O

O

O

O

O

OJ

EJ

O

EJ

J

O
J

EJ

Chlorophyta
Caulerpa cylindracea
Caulerpa taxifolia
Caulerpa taxifolia var. distichophylla

J

ENOMJ EJJJ

J EOCJ

NJ

J

J

J

J

O

O

O

O

O

O

J

C

O

O

J

Cladophora patentiramea
Codium arabicum
Codium fragile subsp. fragile

J
OJ

O

Codium parvulum

J

Halimeda incrassata

N

OJ

EO

O

J

J

J

J

O
N

N

Rhodophyta
Acrothamnion preissii

ENOCJ

OJ

O

O

Agarophyton vermiculophyllum

CJ

NOJ

NO

O

Antithamnion nipponicum

J

Asparagopsis armata

EJ

Asparagopsis taxiformis

EOCJ

J

J

J

J

J

O O

O

J

J

J

J

J

CJ

O
O

OCJ

OC

O

J

N

J

J

EJ
EJ

Bonnemaisonia hamifera
Galaxaura rugosa

J

O

O

Ganonema farinosum (Cr)
Grateloupia turuturu
Lophocladia lallemandii

J

OJ

O

O

ENOCJ

NOCJ

NO

J

J

ENOCJ

NOC

OC

OJ

J

O

OC

J

J

J

J

J

OJ

J

J

J

J

J

ENOJ

J

J

J

J

J

Polysiphonia morrowii
Womersleyella setacea

J

Tracheophyta
Halophila stipulacea

C

O

J

J

NJ

C

Porifera
Paraleucilla magna

EJ

O

Cnidaria
Macrorhynchia philippina

OJ

Oculina patagonica (Cr)OCJ

Rhopilema nomadica

OJ

O

O
E

J
O

J
O

J

J

J

O

OCJ

J

E
CJ

OJ

Ctenophora
Mnemiopsis leidyi

ENC

J

O

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Bioinvasions impacts in the Mediterranean Sea

Table 3. (continued).
Bryozoa
Amathia verticillata (Cr)E

Tricellaria inopinata

J

O

O

O
OJ

Mollusca
Anadara kagoshimensis

J

OJ

OJ

J

J

J

Anadara transversa

ECJ

OJ

OJ

EOJ

J

J

Arcuatula senhousia

EOCJ

EOCJ

EOCJ

OJ

NOCJ

OCJ

Brachidontes pharaonis

ECJ

ECJ

J
O

Bursatella leachii (Cr)

O

J

J
J
EJ

J

J

J

O

J

J

J

J

O

Chama pacifica

J

Conomurex persicus

J

OJ

E

OJ

O

C

O

CJ

J

EC

Crepidula fornicata
Dendostrea cf. folium
Fulvia fragilis

J

Magallana/Crassostrea species

EOJ

OJ

OCJ

O

O

O

J
O

EJ ECJ

J

N

J

J

J

J

J

MJ

M MJ

J

J

J

J

J

J

J

J

J

J

J

Mya arenaria
Petricolaria pholadiformis
Pinctada radiataOO

Rapana venosa

J

EC

O

Ruditapes philippinarum

CJ

Spondylus spinosus

CJ

OJ

O

OJ

EOJ

EO

EO

ENOCJ EOCJ

O

OJ

O

O

ENJ
J

NC

Annelida: Polychaeta
Ficopomatus enigmaticus
Hydroides elegans

EN
O

O

Arthropoda: Crustacea
Acartia (Acanthacartia) tonsa (Cr)Callinectes sapidus

C

N

EOCJ

Dyspanopeus sayi

E

Erugosquilla massavensis

CJ

OJ

O

CJ

OJ

O

E

O

EC

Matuta victor
Metapenaeus monoceros

MCJ

Metapenaeus stebbingiO

Paracerceis sculpta

J

M

CJ
O

Penaeus aztecus

E

O

Penaeus pulchricaudatus

OMJ

M

Penaeus semisulcatus

OM

M

Percnon gibbesi (Cr)O

Portunus segnis

OJ

J

O

EC

O

OC

NCJ

O

EC

Rhithropanopeus harrisii
Echinodermata
Diadema setosum

J

Synaptula reciprocans
Chordata: Ascidiacea
Botrylloides violaceus
Botrylloides diegensis
Ciona robusta

O

Clavelina oblonga

O

Didemnum vexillum

O

EC

O

Herdmania momus
Microcosmus squamiger

CJ
OC

C

O

Polyandrocarpa zorritensis
Styela plicata

E

OJ

E

E

E

E

ENC

Chordata: Osteichthyes
Alepes djedabaO

Apogonichthyoides pharaonis
Atherinomorus forskalii

OJO

Decapterus russelliO

Dussumieria elopsoides

O

Etrumeus golanii
Fistularia commersonii

O
NOM

M

MJ OM

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Bioinvasions impacts in the Mediterranean Sea

Table 3. (continued).
Herklotsichthys punctatusO

Lagocephalus sceleratus

OMJ

OMJ

Nemipterus randalli

CJ

J

O

C

O

OJ
NC

Parexocoetus mento
Parupeneus forsskali

C

Pempheris rhomboidea

OMJ

Plotosus lineatus

CJ

Pterois miles

O

Sargocentron rubrumOC

Saurida lessepsianus

MJ

J

J
O

OJ
J

J

J

OJ

O
J

Scomberomorus commerson

O

N

O

Siganus luridus

ENMCJ MJ

J

J

J

O

J

J

J

EJ

J

J

J

OJ

Siganus rivulatus

ENMCJ MJ

J

J

J

O

J

J

J

EJ

J

J

J

J

Sphyraena chrysotaenia

CO

Torquigener flavimaculosus

J

Upeneus moluccensis

NC

C

O

Upeneus pori

NC

C

O

Figure 6. A) Number of impact records that resulted from the review analysis to impact
biodiversity. Number of impact records by mechanism through which alien species impacted
biodiversity B) negatively or/ and C) positively.

algal turfs that overgrow other species and alter ecologically important
habitats, with negative implications in benthic communities. Althoughwidespread in the Mediterranean, their effects were mainly reported fromthe western Mediterranean ecoregion. Apart from macroalgae, the mollusc
Brachidontes pharaonis and the fishes Siganus luridus and Siganus rivulatus
were the species with most negative impact records among the studied
taxa. The Erythrean B. pharaonis is an old invader of the Mediterranean,
with a wide range of distribution, but it did not exhibit an alarming
invasive behaviour until the late 1990s. Subsequently, its populations
exploded in many eastern Mediterranean localities, becoming dominant inshallow rocky reef platforms with extremely high densities, outcompeting
native species and shaping community composition (see Appendix 1). The
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Figure 7. Mosaic chart of mechanisms of negative impacts on biodiversity for the studied
different phyla.

Lessepsian invaders Siganus spp. dominate fish communities in many partsof the eastern Mediterranean and have caused detrimental losses on
Mediterranean macroalgal communities through their herbivory (seeAppendix 1 for more information).
Caulerpa cylindracea was also the species most reported for its positive
impacts, with 12 records, followed by B. pharaonis and the serpulid
Ficopomatus enigmaticus. Although the dense populations of C. cylindracea
constitute a nuisance for the majority of native biota, it can also facilitate
several other species, from seagrasses to invertebrates. Brachidontes pharaonis
has acquired a functional role in Mediterranean ecosystems and contributes
significantly as a structural ecosystem engineer, as a filter-feeder that
reduces turbidity and increases light penetration, and as a food source fornative biota. Ficopomatus enigmaticus is a reef-building structural engineer
that provides novel habitat for many benthic taxa.
Negative impacts were caused by a variety of mechanisms (Figure 6B, C;
Figure 7), significantly differing in frequency by taxonomic group (chi-square
test; keeping the three most frequent mechanisms and grouping all others;
keeping the six most frequent taxonomic groups and grouping all others;
p < 0.001). Competition for resources was the most reported mechanism ofnegative impacts with almost 250 records, followed by the creation of novel
habitat, and predation (Figure 6B). This was the case for most studied
phyla except Chordata (Osteichthyes), Annelida (Polychaeta), and Cercozoa(Figure 7). Osteichthyes caused negative impacts mostly by preying on
native biota. Hydroides elegans and F. enigmaticus, the two studied alienpolychaetes, mainly affected other species through the creation of novel
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Figure 8. Geographical variation of the A) negative and B) positive mechanisms of impact on
biodiversity by Mediterranean ecoregion and of analyzed alien phyla with C) negative and D)
positive impacts on biodiversity per Mediterranean ecoregion. The size of the pie charts reflects
the number of reported cases (the inset indicates the minimum and maximum sizes).

habitat. This was also an important mechanism of negative impacts for
macroalgae such as L. lallemandii, C. cylindracea, Caulerpa taxifolia andmolluscs such as B. pharaonis, and Spondylus spinosus. Haplosporidium
pinnae, the sole representative of Cercozoa, has been associated with thedisease that has caused the extinction of the endemic bivalve Pinna nobilis
from almost the entire Mediterranean Sea, except for a small number ofrefugia. The creation of novel habitat was the most common mechanism of
positive impacts on biodiversity accounting for 65% of the reported
positive cases (Figure 6C). Species such as F. enigmaticus, S. spinosus, thebivalves of the genus Magallana/Crassostrea (see the notes in the Appendix 1
for the taxonomic status of the genus), and the rhodophyte Asparagopsis
armata create novel habitats that support a variety of species.
Analysis of impacts by ecoregion revealed that interspecific competitionis the most important mechanism generating negative impacts on biodiversity
in all Mediterranean ecoregions (Figure 8A); nevertheless, the frequency ofthe various mechanisms significantly differed by ecoregion (chi-square
test; keeping the three most frequent mechanisms—competition, creationof novel habitat, predation—and grouping all others; p < 0.001). The creationof novel habitat was the second most reported negative impact mechanism
in western and central Mediterranean ecoregions. On the contrary, predation
was the second most impactful mechanism in the eastern Mediterraneanecoregions (Figure 8A). The frequency of the mechanisms of reported
positive impacts also differed by ecoregion (chi-square test; keeping thetwo most frequent mechanisms and grouping all others; excluding ecoregions
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with < 5 records; p = 0.008). Structural ecosystem engineers that create
novel habitats were the main contributors to positive impacts in all
Mediterranean ecoregions, except for the Levantine Sea where positive
impacts of food provision slightly exceeded the creation of novel habitat(Figure 8B). Food provision to native biodiversity was also important in
the western Mediterranean and the Ionian Sea (Figure 8B).
There was significant variation in the taxonomic composition of thespecies that caused negative impacts on biodiversity among ecoregions(chi-square test; keeping the five most reported phyla and grouping allothers; p < 0.001) (Figure 8C). In the western Mediterranean, the mostreported negative impacts were caused by invasive Rhodophyta andChlorophyta, whereas in the Levantine and the Aegean Sea by Osteichthyes,
and in the Adriatic Sea by Mollusca (Figure 8C). Caulerpa cylindracea, L.
lallemandii, W. setacea, C. taxifolia, and Acrothamnion preissii were among
the chlorophytes and rhodophytes with negative effects in the western
Mediterranean whereas, in the Levantine Sea, B. pharaonis, S. luridus andS. rivulatus were the species with the most recorded impacts. Siganus
luridus was also the species that accounted for most of the recorded
negative impacts in the Aegean Sea. Negative impacts caused by Crustacea
had an important share of total impacts in the Tunisian plateau/Gulf of
Sidra, the Levantine, and the Ionian Sea, but they had little relevance in thewestern Mediterranean and the Alboran Sea (Figure 8C). The Alboran Sea
has been plagued by the negative impacts of the brown alga Rugulopteryx
okamurae, a recent invader that has caused detrimental effects on local
ecosystems (see Appendix 1 for more information).
There was also significant variation in the taxonomic composition of thespecies that caused positive impacts on biodiversity among ecoregions(chi-square test; keeping only the three ecoregions with the highest
number of records and the four mostly reported phyla, grouping all others;
p = 0.01). Macroalgae constituted the bulk of positive impact records forthe western Mediterranean, the Alboran Sea, and the Tunisian plateau/Gulfof Sidra and had an important share in total reported positive impacts
from the Adriatic and the Ionian Sea (Figure 8D). Mollusca ranked first interms of reported positive impacts in the Levantine and the Adriatic Sea
and had an important share in the western Mediterranean and the Aegean
Sea. As creators of novel habitats, Polychaeta contributed to positive
impacts in the Aegean, Ionian, Adriatic Sea, and western Mediterranean(Figure 8D). Furthermore, some Osteichthyes were reported to have positive
impacts on biodiversity, because of their role in the novel trophic webs, but
only in the Levantine Sea.
“Major” was the most reported impact magnitude category for both
negative and positive impact records (Figure 9). Nevertheless, the frequencyof impact magnitudes substantially differed between negative and positive
impacts, with “major” impacts having a significantly higher frequency in
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Figure 9. Proportion of impact magnitude categories of negative (left column) and positive(right column) impacts on biodiversity.

positive than negative impacts (chi-square test; excluding minimal andmassive magnitude categories due to their low frequencies; p = 0.011).
Overall, 61% of negative impacts and 74% of positive impacts wereclassified as major; no positive impacts of massive magnitude were reported.
The frequency of the categories of magnitude of impact significantly
differed among taxonomic groups (chi-square test; disregarding minimaland massive magnitude categories due to their low frequencies, combining
phyla with a small number of records together; p < 0.001). Major negative
impacts were the primary magnitude category recorded for Rhodophyta,
Chlorophyta, Ochrophyta, Mollusca, Polychaeta, Cnidaria, Foraminifera,
Ascidiacea, and Bryozoa (Figure 10A). Massive negative impacts were only
recorded for Osteichthyes (Siganus spp.), Cercozoa (H. pinnae), andOchrophyta (R. okamurae) (Figure 10A). Moderate and minor impacts
were the most reported for Crustacea. Although the number of records ofpositive impacts was lower than that of negative impacts, they followed asimilar pattern regarding impact magnitude (Figure 10B), with significant
differences among taxonomic groups (chi-square test; combining phylawith a small number of records together; p = 0.011).
There was no evidence that the magnitude of impact increases withresidence time. The average residence time of introduced species did not
differ by the maximum reported magnitude of negative (ANOVA; p = 0.947)
or positive (ANOVA; p = 0.300) impacts. The slope of the linear regression
between the residence time of introduced species and the negative impact
score did not differ significantly from zero (p = 0.985), and the intercept(i.e. the average score ± S.E.) was 11.3 ± 3.3 (Figure 11). The slope remained
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Figure 10. Impact magnitude of A) negative and B) positive impacts on biodiversity per
phylum of alien species analysed..

Figure 11. Regressions of negative (left) or positive (right) impact scores in relation to residence time (years since first detection)for each of the assessed species.

statistically not different from zero even when three influential points(with leverage values greater than five times that of an average data point)
were removed (p = 0.529). Similarly, the slope of the linear regression
between the residence time of introduced species and the positive impact
score did not significantly differ from zero (p = 0.215), and the intercept(i.e. the average score ± S.E.) was 2.2 ± 1.0 (Figure 11). The slope remained
statistically not different from zero even when three influential points(with leverage values greater than five times that of an average data point)
were removed (p = 0.057).
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Figure 12. Overview of negative and positive impacts on ecosystem services and human health.

Impacts on ecosystem services
Overall, 685 negative and positive impact records were found to affectprovisioning, regulating/maintenance, and cultural ecosystem services,with 312 negative and 373 positive records in total, whereas for humanhealth 61 negative and no positive impacts were recorded. Most impact
records on provisioning services were recorded for food provision, with
116 negative and 188 positive records (Figure 12). Negative impacts prevailed
over positive for regulating/maintenance services. Still, for several
regulating and maintenance services (climate regulation, water purification,
coastal protection, and biological regulation) more positive than negative
impacts were reported (Figure 12). Among regulating/maintenance services,
lifecycle maintenance was the one with the highest number of recorded
negative impacts. No impact records were found for weather regulation.
For the cultural services “aesthetic values” and “recreation and tourism”,
70 negative and only 6 positive impact records were reported. On the other
hand, for “cognitive effects” records, positive impacts prevailed by 114
records against only 12 cases of negative impacts.
The frequency of the mechanisms of reported negative impacts onprovisioning ecosystem services significantly differed by ecoregion (chisquare test; keeping the four most frequent mechanisms and excluding theAlboran Sea; p < 0.001). Fouling shellfish, gear, and equipment of aquaculture
facilities was the primary mechanism of negative impacts on provisioning
services in the Adriatic Sea, the Ionian Sea, and the western Mediterranean(Figure 13A). Entanglement in nets was the most important mechanism in
the Levantine and the Alboran Sea, with a considerable contribution tonegative impacts on provisioning services throughout the Mediterranean
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Figure 13. Geographical variation of the A) negative and B) positive mechanisms of impact onprovisioning ecosystem services by Mediterranean ecoregion and of analyzed alien species
phyla with C) negative and D) positive impacts on provisioning services per Mediterraneanecoregion. The size of the pie charts reflects the number of reported cases (the inset indicatesthe minimum and maximum sizes).

(Figure 13A). Predation was also a primary mechanism of negative
impacts, especially in the eastern Mediterranean. From the analysis of
positive impacts by ecoregion on provisioning services (Figure 13B), it
became obvious that the Levantine Sea was the main beneficiary, due to
new commodities for local fisheries. Most positive impacts were recordedin this ecoregion and significantly declined westwards (Figure 13B).
Among all mechanisms positively impacting provisioning services acrossMediterranean ecoregions, “new commodities” were by far the mostimportant.
The taxonomic synthesis of the species that negatively impacted
provisioning services differed significantly among ecoregions (chi-square
test; keeping the four most frequent phyla and merging all the others;
excluding the Alboran Sea; p < 0.001) (Figure 13C). Ascidians were themajor group of negative impacts in the western Mediterranean, with animportant contribution also in the Adriatic Sea (Figure 13C). This is due tospecies such as the alien ascidians Styela plicata and Clavelina oblonga that
commonly foul farmed shellfish and aquaculture equipment. Molluscs(Pinctada radiata), bryozoans (Tricellaria inopinata), and sponges(Paraleucilla magna) also foul aquaculture facilities, introducing negative
effects on production. Cnidaria and Osteichthyes were the main groups
that impacted provisioning services in the Levantine Sea (Figure 13C). The
invasive jellyfish Rhopilema nomadica formed massive swarms that becamea nuisance for the local fisheries due to entanglement in nets and for water
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supply for local power plants and desalination facilities due to blocking of
intake pipes. The fish Lagocephalus sceleratus was also a major pest for
fisheries in the Levantine and the Aegean Sea due to its predation on thecatch and the damage caused to fishing gear. Alien crustacean species werealso reported to negatively impact the provision of food across multiple
ecoregions (Figure 13C). The alien crabs Callinectes sapidus and Portunus
segnis interfered with local fisheries in multiple Mediterranean ecoregions
by preying on the catches and by getting entangled in nets. Alien shrimps
such as Metapenaeus monoceros and Penaeus pulchricaudatus have been
associated with population declines of the commercially important native
shrimp Penaeus kerathurus (see Appendix 1).
The main contributors of positive impacts on food provision were alien
Osteichthyes and Crustacea, with positive impact records substantially
increasing eastwards (Figure 13D). Several alien fish such as Nemipterus
randalli, Scomberomorus commerson, Sphyraena chrysotaenia, Saurida
lessepsianus, Upeneus spp., Siganus spp. and crustaceans such as
P. pulchricaudatus, and Metapenaeus spp. are marketed in many
Mediterranean countries. Callinectes sapidus is collected and sold in thenorthern Adriatic and Ebro Delta (Spain) where it is an appreciated shellfish.
Mollusc species, such as those of the genus Magallana/Crassostrea, Ruditapes
philippinarum, and Conomurex persicus have historically contributed tofood provision as new commodities in various Mediterranean ecoregions.
Degradation of habitats was the primary mechanism of negative impacts
on regulating services, mainly recorded in the western Mediterranean andaffecting life-cycle maintenance (Figure 14A). Posidonia oceanica meadowsand coralligenous communities are marine habitats with a fundamentalrole in the functioning of Mediterranean ecosystems and the conservationof marine life. Invasive Rhodophyta such as W. setacea, A. preissii, andL. lallemandii have the potential to degrade such ecosystems (Figure 14C)
through the formation of dense algal turfs that epiphytise Posidonia
meadows and homogenise the diversity and complexity of coralligenous
communities, degrading their state and negatively affecting the life they
support (see Appendix 1). Such habitats are also vulnerable to the invasion
by C. cylindracea that negatively affects many keystone species. Furthermore,
the recent Ochrophyta invader R. okamurae can displace native species,
monopolise shallow communities, and even cause community shifts incoralligenous communities.
Positive mechanisms of impact on “regulating and maintenance” ecosystemservices were much less reported (Figure 14B). Carbon sequestration
overall accounted for most positive impacts either through the formationof shells or via primary production. Such positive contributions to climatechange were attributed to Mollusca, Foraminifera, and Tracheophyta(Figure 14D). Shell-forming organisms such as the foraminiferan Amphistegina

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Figure 14. Geographical variation of the A) negative and B) positive mechanisms of impact onregulating and maintenance ecosystem services by Mediterranean ecoregion and of analyzed
alien species phyla with C) negative and D) positive impacts on regulating and maintenanceservices per Mediterranean ecoregion. The size of the pie charts reflects the number of reported
cases (the inset indicates the minimum and maximum sizes).

lobifera or the bivalves R. philippinarum and Arcuatula senhousia form
dense aggregations that constitute banks of carbon storage in the marine
environment, since their shells contain carbonate. Meadows of the alien
seagrass Halophila stipulacea are also considered carbon sinks (seeAppendix 1).
The Levantine Sea was the Mediterranean ecoregion with most studiesof impacts on cultural ecosystem services (Figure 15A, B). The negative
effects in the Levantine were primarily caused by Chlorophyta, Ochrophyta,
and Rhodophyta (Figure 15C) through decomposing macroalgal material
that washed ashore. Seaweed drifts of Codium parvulum, Codium arabicum,
Galaxaura rugosa, and Stypopodium schimperi have regularly occurred in
the eastern Mediterranean during recent decades, disturbing local activities
and tourism and degrading the aesthetic value of the coast. Large anddense macroalgal thalli of Sargassum muticum and Undaria pinnatifida
have sometimes become a nuisance in Adriatic lagoons, hindering navigation.
In the Levantine Sea, R. nomadica massive swarms have also hindered
tourism profits as they pose a threat to swimmers and deter tourists fromvisiting the coast.
On the other hand, alien species have offered materials for research on
potential pharmaceutical products and biomonitoring services, which are
the main positive impacts reported on cultural services (Figure 15B), withfrequencies that were not found to differ significantly among ecoregions(chi-square test; excluding the Alboran Sea; p = 0.136). Many molluscs andTsirintanis et al. (2022), Aquatic Invasions 17(3): 308–352, https://doi.org/10.3391/ai.2022.17.3.01

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Figure 15. Geographical variation of the A) negative and B) positive mechanisms of impact on
cultural ecosystem services by Mediterranean ecoregion and of analyzed alien species phylawith C) negative and D) positive impacts on cultural services per Mediterranean ecoregion. The
size of the pie charts reflects the number of reported cases (the inset indicates the minimum andmaximum sizes).

crustaceans such as S. spinosus, P. radiata, and Penaeus semisulcatus, andthe foraminiferan A. lobifera, have been used effectively as biomonitoring
species for marine pollution (Figure 15D; see Appendix 1).

Impacts on human healthReported impacts on human health were only negative. The great majorityof this evidence came from the Levantine Sea (Figure 16A) and was primarily
related to stinging and poisoning/intoxication caused by only 9 species
belonging to Osteichthyes, Cnidaria, and Echinodermata (Figure 16B),
namely: L. sceleratus, Torquigener flavimaculosus, Plotosus lineatus, P. miles,
S. luridus, S. rivulatus, Macrorhynchia philippina, R. nomadica, and Diadema
setosum. Such unwanted accidents are sometimes described in the scientific
literature. For example, in the eastern Mediterranean, severe intoxications
and cases of death were attributed to the consumption of L. sceleratus,
which contains in its tissues a paralytic neurotoxin called tetrodotoxin that canbe lethal for humans. Rhopilema nomadica has caused a vast number ofhospitalizations of swimmers and fishers in the Levantine Sea due to its painful
stings. The long-spined sea urchin D. setosum poses a threat for swimmersin the eastern Mediterranean where it can be found at high densities inshallow waters, as its spines contain venom and may inflict painful stings.

Grouping of species according to the mechanisms of their impacts
Species with impacts on biodiversity, ecosystem services, and humanhealth were grouped by hierarchical cluster analysis according to their
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Figure 16. Geographical variation of A) mechanisms of negative impact and the responsible B)
phyla causing the impacts on human health by Mediterranean ecoregion.

Figure 17. Hierarchical cluster dendrogram of alien and cryptogenic species (Cr: cryptogenic) based on the mechanisms ofreported impacts on biodiversity, ecosystem services and human health. Coloured frames (red, green, blue, light blue) indicate thefour major groups species of the dendrogram. Included species are numbered as follows: 1) Acartia (Acanthacartia) tonsa (Cr), 2)
Acrothamnion preissii, 3) Agarophyton vermiculophyllum, 4) Alepes djedaba, 5) Amathia verticillata (Cr), 6) Amphistegina
lobifera, 7) Anadara kagoshimensis, 8) Anadara transversa, 9) Antithamnion nipponicum, 10) Arcuatula senhousia, 11) Asparagopsis
armata , 12) Asparagopsis taxiformis, 13) Atherinomorus forskalii, 14) Brachidontes pharaonis, 15) Bursatella leachii (Cr),16) Callinectes sapidus, 17) Caulerpa cylindracea, 18) Caulerpa taxifolia, 19) Caulerpa taxifolia var. distichophylla, 20) Chamapacifica, 21) Chrysonephos lewisii, 22) Ciona robusta, 23) Cladophora patentiramea, 24) Clavelina oblonga, 25) Codium
arabicum, 26) Codium fragile subsp. fragile, 27) Codium parvulum, 28) Conomurex persicus, 29) Decapterus russelli,30) Diadema setosum, 31) Didemnum vexillum, 32) Dussumieria elopsoides, 33) Dyspanopeus sayi, 34) Erugosquilla massavensis,35) Etrumeus golanii, 36) Ficopomatus enigmaticus, 37) Fistularia commersonii, 38) Fulvia fragilis, 39) Galaxaura rugosa,40) Grateloupia turuturu, 41) Halimeda incrassata, 42) Halophila stipulacea, 43) Haplosporidium pinnae (Cr), 44) Herdmania
momus, 45) Herklotsichthys punctatus, 46) Hydroides elegans, 47) Lagocephalus sceleratus, 48) Lophocladia lallemandii,49) Macrorhynchia philippina, 50) Magallana/Crassostrea species, 51) Metapenaeus monoceros, 52) Metapenaeus stebbingi,53) Microcosmus squamiger, 54) Mnemiopsis leidyi, 55) Nemipterus randalli, 56) Oculina patagonica (Cr), 57) Paracerceis
sculpta, 58) Paraleucilla magna, 59) Parupeneus forsskali, 60) Pempheris rhomboidea, 61) Penaeus aztecus, 62) Penaeus
pulchricaudatus, 63) Penaeus semisulcatus, 64) Percnon gibbesi (Cr), 65) Pinctada radiata, 66) Plotosus lineatus,
67) Polyandrocarpa zorritensis, 68) Portunus segnis, 69) Pterois miles, 70) Rapana venosa, 71) Rhopilema nomadica, 72) Ruditapes
philippinarum, 73) Rugulopteryx okamurae, 74) Sargassum muticum, 75) Sargocentron rubrum, 76) Saurida lessepsianus,77) Scomberomorus commerson, 78) Siganus luridus, 79) Siganus rivulatus, 80) Sphyraena chrysotaenia, 81) Spondylus spinosus,
82) Styela plicata, 83) Stypopodium schimperi, 84) Torquigener flavimaculosus, 85) Tricellaria inopinata, 86) Undaria
pinnatifida, 87) Upeneus moluccensis, 88) Upeneus pori, 89) Womersleyella setacea.

similarity of mechanisms of reported impacts, resulting in 4 major groups(Figure 17).
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The first cluster (red colour in Figure 17) included six alien macroalgae,
namely C. cylindracea, W. setacea, L. lallemandii, R. okamurae, A. preissii,
and C. taxifolia. A high number of negative impact records was reported
for each of these species, with competition for resources being the mostcommon mechanism of impact. A high number of impact records was also
reported on ecosystem services through the mechanism of degradation ofimportant habitats, with 84 negative cases on 8 different services. These
species also constitute ecosystem engineers that mainly impacted otherspecies negatively (34 records) rather than positively (21 records) throughthe creation of novel habitat.
The second cluster (green colour in Figure 17) was formed by 26 species
that were grouped together primarily due to their positive impact on foodprovision, being new commodities. All these species, mainly crustaceans,fishes, and two molluscs, contributed to 91% of the overall positive impacts
on food provision by new commodities. Among them, the alien shrimps
M. monoceros, P. pulchricaudatus, and P. semisulcatus were the species
with the highest number of positive reports as new commodities, but also
some competitive negative impacts on native shrimp species and thus
exhibited a high similarity. The alien fishes N. randalli, Saurida lessepsianus,
Upeneus spp., the alien molluscs C. persicus and R. philippinarum, and thealien crab P. segnis formed a subgroup within this cluster following thesame pattern of reported mechanisms of impact but with a lower
frequency. Predation (including grazing) was also a mechanism of negative
impact characteristic for some species of this cluster, such as theherbivorous fish Siganus spp., the omnivorous crab C. sapidus, and thepiscivorous fish F. commersonii.
The third major cluster (blue colour in Figure 17) included alien molluscs
such as B. pharaonis, Chama pacifica, and Magallana/Crassostrea species,
the alien polychaetes F. enigmaticus and H. elegans, the alien macroalgae
Asparagopsis spp. and U. pinnatifida, and the cryptogenic hexacoral Oculina
patagonica. A high number of impacts on biodiversity was recorded forthese species, mainly through the mechanisms of competition and thecreation of novel habitat (both negative and positive for the latter) as
structural ecosystem engineers.
The final cluster (light blue colour) was delineated by 45 species with
394 impact records. Thirty-six species of this cluster had less than 10
records each. Competition for resources was the most common mechanismof impact with 59 records, caused by 33 of the 46 species of the cluster.
Fouling species with negative impacts on aquaculture followed as the second
most common mechanism. Such species with both competition and foulingimpacts were the ascidians Styela plicata, Clavelina oblonga, and Didemnum
vexillum, the bivalve P. radiata, the sponge P. magna, and the bryozoan
T. inopinata. Most species with negative impacts on human health werealso included in this cluster. Diadema setosum, M. philippina, P. lineatus, andP. miles were grouped together with high similarity as stinging species.
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Figure 18. Type of evidence of the analysed impact records on biodiversity, ecosystemservices and human health. The numbers on top of the bars indicate the sample size (number ofreported cases) for each category.

Type of evidence
Only 16% of impact records were experimental (9% were based on
manipulative and 7% on natural experiments; Figure 18). Moreover, manyof the experimental studies were in vitro experiments on alien species
extracts and compounds. Most of the taxa studied by experimental studies
were Chlorophyta and Rhodophyta. Overall, direct observation was themost common type of evidence accounting for 40% of all records. Reported
impacts on provisioning ecosystem services were almost exclusively basedon direct observations (Figure 18). Fouling on aquaculture facilities,
entanglement in nets, and new commodities in the fisheries and fish
markets are undoubtedly direct impacts and as such were classified as
direct observations. For biodiversity records, direct observations referredto the creation of novel habitat, apparent competitive interactions such as
overgrowth of sessile organisms, predation impacts derived from stomach
content analysis, and massive mortalities. Expert judgement and nonexperimentally based correlations accounted for 32% and 9% of impact
records, respectively (Figure 18), the former being dominant for “regulating
and maintenance” ecosystem services. Modelling overall accounted for
only 2% of the records.
The western Mediterranean and the Alboran Sea exhibited the highest
percentages of experimental studies assessing negative impacts on biodiversity,
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Figure 19. Geographical variation of type of evidence for negative (A) and (B) positive impacts
on biodiversity across Mediterranean ecoregions.

followed by the Adriatic and the Ionian Sea (Figure 19A). Much lessexperimental studies were recorded in the Aegean and the Levantine Sea.
Instead, expert judgement was the main type of evidence in these
ecoregions, as well as in the Adriatic and the Ionian Sea. The western
Mediterranean and the Adriatic Sea were the ecoregions with the highest
proportion of experimental studies for positive impacts on biodiversity(Figure 19B). Most impact reporting through modelling studies for both
negative and positive impacts was from the Levantine Sea (Figure 19A, B).

Inventory of high impact species in the Mediterranean Sea
An inventory of impactful species, based on both negative and positive
reported impacts on biodiversity, ecosystem services and human health, is
proposed in Table 4 and includes 88 species. Of the 103 assessed species, 15
were excluded from this inventory due to the complete absence of impact
records or the reporting of only minor impacts. For three included species
there was only weak evidence for their impact, based on expert judgement.
Based on their negative impacts score on biodiversity, a list of the ten worst
invasive species was compiled (Table 5). Caulerpa cylindracea ranked first,
followed by W. setacea and L. lallemandii. Macroalgae dominated in thelist of the ten worst invasives (6 species), followed by fishes and bivalve
molluscs (2 species each).

Discussion
The number of reported negative impact records on biodiversity wasapproximately four times higher than the number of positive ones.
Analysing the mechanisms of these effects, it was revealed that many alien
species strongly compete for space and resources with native biota (e.g.,
Turon et al. 2007; Fanelli et al. 2015; Manconi et al. 2020) whereas others
act as ecosystem engineers and alter the structure of habitats causing major
negative effects on the local communities (e.g., Rilov et al. 2004; Bedini etal. 2014). Furthermore, intense feeding activities of invasive species cancause the decline of native populations (e.g., Kampouris et al. 2019), withalien grazers even being able to cause massive negative impacts in eastern
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Table 4. Proposed inventory of alien and cryptogenic marine species with reported moderate to high impacts on biodiversity or
ecosystem services or human health. Species whose impact was only reported by expert judgement are marked in light yellow(weak evidence); Cr: For cryptogenic species.
Cercozoa
Haplosporidium pinnae (Cr)Foraminifera
Amphistegina lobifera
Ochrophyta
Chrysonephos lewisii
Rugulopteryx okamurae
Sargassum muticum
Stypopodium schimperi
Undaria pinnatifida
Chlorophyta
Caulerpa cylindracea
Caulerpa taxifolia
Caulerpa taxifolia var. distichophylla
Cladophora patentiramea
Codium arabicum
Codium fragile subsp. fragile
Codium parvulum
Halimeda incrassata
Rhodophyta
Acrothamnion preissii
Agarophyton vermiculophyllum
Antithamnion nipponicum
Asparagopsis armata
Asparagopsis taxiformis
Galaxaura rugosa
Grateloupia turuturu
Lophocladia lallemandii
Womersleyella setacea

Tracheohyta
Halophila stipulacea
Porifera
Paraleucilla magna
Cnidaria
Macrorhynchia philippina
Oculina patagonica (Cr)Rhopilema nomadica
Ctenophora
Mnemiopsis leidyi
Bryozoa
Amathia verticillata (Cr)Tricellaria inopinata
Mollusca
Anadara kagoshimensis
Anadara transversa
Arcuatula senhousia
Brachidontes pharaonis
Bursatella leachii (Cr)
Chama pacifica
Conomurex persicus
Fulvia fragilis
Magallana/Crassostrea species
Pinctada radiata
Rapana venosa
Ruditapes philippinarum
Spondylus spinosus

Annelida: Polychaeta
Ficopomatus enigmaticus
Hydroides elegans
Arthropoda: Crustacea
Acartia (Acanthacartia) tonsa (Cr)Callinectes sapidus
Dyspanopeus sayi
Erugosquilla massavensis
Metapenaeus monoceros
Metapenaeus stebbingi
Paracerceis sculpta
Penaeus aztecus
Penaeus pulchricaudatus
Penaeus semisulcatus
Portunus segnis
Echinodermata
Diadema setosum
Chordata: Ascidiacea
Ciona robusta
Clavelina oblonga
Didemnum vexillum
Herdmania momus
Microcosmus squamiger
Polyandrocarpa zorritensis
Styela plicata

Chordata: Osteichthyes
Alepes djedaba
Atherinomorus forskalii
Decapterus russelli
Dussumieria elopsoides
Etrumeus golanii
Fistularia commersonii
Herklotsichthys punctatus
Lagocephalus sceleratus
Nemipterus randalli
Parupeneus forsskali
Pempheris rhomboidea
Plotosus lineatus
Pterois miles
Sargocentron rubrum
Saurida lessepsianus
Scomberomorus commerson
Siganus luridus
Siganus rivulatus
Sphyraena chrysotaenia
Torquigener flavimaculosus
Upeneus moluccensis
Upeneus pori

Table 5. The ten worst invasive species, based on their negative impact
score (accounting only for impacts on biodiversity). This ranking does notaccount for the spatial extent of impacts but is based on a sum of allreported impacts in the literature, weighted by their magnitudes.
Species
Caulerpa cylindracea
Womersleyella setacea
Lophocladia lallemandii
Brachidontes pharaonis
Siganus luridus
Rugulopteryx okamurae
Caulerpa taxifolia
Siganus rivulatus
Acrothamnion preissii
Spondylus spinosus

Negative Impacts Score
134
80
65
47
44
43
38
38
36
33

Mediterranean ecoregions by depleting rocky reef algal biomass (e.g., Sala
et al. 2011). At the same time, some alien species create novel habitats thatoffer shelter to many other native organisms (e.g., Di Martino et al. 2007;
Munari et al. 2015), constitute new food sources for native predators (e.g.,
Giacoletti et al. 2016; Tiralongo et al. 2021), and contribute to other
ecological functions of the recipient ecosystem (e.g., Sarà et al. 2021).
It is noteworthy that a higher number of positive than negative impacts
were recorded affecting the flow of ecosystem services. Food provision
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appears as the most affected ecosystem service by both positive andnegative impacts. Invasive fish have significantly increased their numbersin the last thirty years, representing today more than half of the totalabundance and biomass of the Levantine fish (Katsanevakis et al. 2018).
Simultaneously, severe population declines in some native fish populations
occurred (Edelist et al. 2013). All surveys that indicated a competitive effectof alien species on commercial native species stocks were supported byweak or modest strength of evidence. There is no strong evidence supporting
the hypothesis of native species population declines exclusively or largely
due to competition with alien species. On the other hand, research has
demonstrated that many species have declined in the Levantine Sea due toclimate change, as the new temperature regime is beyond their thermal
niche (Rilov 2016). Climate change is an important stressor for native biota
and has negatively affected the Mediterranean Sea (Marbà et al. 2015; Rilov
2016; Albano et al. 2021). In the western Mediterranean, shallow waters
have been warming for more than a century with more abrupt positive
trends during the recent decades that have resulted in local sea surface
temperature increases that even exceed 1 °C (Lejeusne et al. 2010) anddeleterious marine heatwaves (Garrabou et al. 2009, 2019, 2022). The
eastern basin was shown to be warming faster (Pisano et al. 2020; Novi etal. 2021), with surface water temperature even exceeding a 3 °C increaseduring the period 1978–2014 in the southeastern regions (Ozer et al. 2017).
Climate change has played a crucial role in the alteration of eastern
Mediterranean ecosystems and the collapse of several species (Rilov 2016;
Albano et al. 2021), but these dramatic changes are better explained as aresult of the combined effects of climate change and biological invasions(Marras et al. 2015; Azzurro et al. 2019; Yeruham et al. 2020). Indeed,
multiple stressors often act in synergy, leading to multiplicative effects(Korpinen et al. 2019; Gissi et al. 2021).
A progressive transition towards a more thermophilic biota is reported
for the global fishery catch for most marine ecosystems (Cheung et al.
2013), and also in the Mediterranean Sea (Tsikliras and Stergiou 2014),
where warm adapted invaders of Indo-Pacific origin are already replacing
native biota (Stergiou et al. 2016 and references therein; Katsanevakis et al.
2018; Albano et al. 2021). Yet, to date many alien species contribute to foodprovision as new commodities (Katsanevakis et al. 2018), especially in theeastern Mediterranean where alien fishes and crustaceans are moreabundant in comparison to the western basin (Katsanevakis et al. 2014b).
Levantine fisheries have even begun to shift their target from deeper toshallower waters where they can catch larger quantities of thermophilicalien species (van Rijn et al. 2020).
Contrary to the general idea that invading alien species are inherently“bad”, a view that is often dependent on social perceptions (Katsanevakis etal. 2014a), the positive effects of tropical invaders are worth exploring in
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detail, especially in the current climate change context. In the Levantine
Sea, the ecological space made available by the shift of temperate species
towards higher latitudes and greater depths cannot be covered byneonatives (sensu Essl et al. 2019) from southern regions, as this is a landlocked basin. In that sense, it can be argued that thermophilic Lessepsianimmigrants entering the Mediterranean through the Suez Canal may
contribute to limiting the loss of ecosystem functions and services. Restoring
the Levantine Sea ecosystems to their previous state before climate change andmassive biological invasions is unrealistic. Except for targeted management
actions for specific species (e.g. P. miles and L. sceleratus), marine
managers in the region need to be adaptive and realistic, understanding
and accepting the role of alien species in the novel marine ecosystems.
Regarding the impacts of invasive species on human health, we observedthat these are mostly limited to the eastern basin. Among the nine species,
only L. sceleratus was found to have an impact in locations west of the
Aegean Sea, and the species has already reached the westernmost end of
the Mediterranean (Azzurro et al. 2020). The actual number of negative
impact cases on human health is probably underestimated because many
non-life-threatening episodes do not require hospitalisation and aretreated by first aid. Such cases are most often not officially reported (Bédry
et al. 2021), especially not by scientific literature. Bédry et al. (2021)
proposed a series of actions to manage the effects of marine biologicalinvasions on human health: i) to reinforce public awareness of the potential
dangers that specific alien species may pose to human health, ii) to train
and prepare professional medical personnel on the physiological effects of
toxic alien species, iii) to establish a regional warning and monitoring
system. In this review, we did not record positive impacts of alien or
cryptogenic species on human health but future research on alien species is
expected to disclose their potential as providers of biomolecules, to be usedby the pharmaceutical industry (e.g. Genovese et al. 2009; Minicante et al.
2016; Dhahri et al. 2020). However, the discovery of new potentially active
molecules is a well-worn argument very often put forward to minimise theproblem of species introductions (a “chestnut” in journalistic terms), but
its validity has only rarely, if ever, been demonstrated and evaluated.
Marine species capable of producing active metabolites are well known
around the world and invasions are not necessary to initiate research andexploitation. The industrial exploitation of such molecules often requires
either aquaculture production or chemical synthesis. So far, to the best of
our knowledge, there are no examples of industrial exploitation ofMediterranean invaders for active molecules.
Biological invasions remain one of the most catastrophic threats to
global biodiversity, but the complexity of their impacts along with theirecological, and socio-economic dimensions are worth exploring in detailand at different scales. Some scientists consider that the origin of a species
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does not make it de facto responsible for negative consequences (Davis etal. 2011) since native species also possess the ecological ability to affectecosystems and cause deleterious impacts under certain conditions. For
example, the coastal rocky reefs of the eastern Mediterranean are
overgrazed by the invasive rabbitfishes Siganus luridus and S. rivulatus(Sala et al. 2011; Giakoumi 2014; Vergés et al. 2014; Yeruham et al. 2020)
but under certain conditions, similar effects can be provoked by nativegrazers (Hereu 2006; Vergés et al. 2009; Bonaviri et al. 2011; Gianni et al.
2017; Tsirintanis et al. 2018; Papadakis et al. 2021), often due to cascading
effects caused by the loss of overfished native predators (Sala et al. 1998). It
should also be highlighted that some of the high-impact species of thecurrent proposed inventory are cryptogenic, meaning that their origin
cannot be completely ascertained. Non-factual perception of alien species
as invasive (i.e. negatively impacting ecosystems and human well-being)neglects a holistic approach to impact assessment and can lead to bias
(Goodenough 2010; Katsanevakis et al. 2014a). Commonly the same species
have both negative and positive impacts on biodiversity, and the overallbalance is hard to assess. For example, the possible facilitation of therestoration of a degraded ecosystem by an invasive alien species like thefacilitation of seagrass seedlings by C. cylindracea in degraded meadows(Ceccherelli and Campo 2002; Pereda-Briones et al. 2018) deserves further
consideration and confirmation by long-term studies evaluating the survival
rate of germlings in dense C. cylindracea meadows. This brings up ecological,
cultural, and socio-economic considerations that complicate decision
making in invasive species management, as changes in host communities
are not always perceived as harmful (Bonanno 2016), and management
decisions need to account for conflicts and trade-offs (Mason et al. 2017).
In this study, we found a clear geographic differentiation in the distributionof reported impacts. For example, predation as a mechanism of impact wasmore important in the Levantine Sea than in the rest of the basin. This isfollowing the higher richness and abundance of invasive fishes thatcharacterise the eastern sectors of the Mediterranean, being introduced
from the Red Sea through the Suez Canal and favoured by the higher
temperatures of the eastern Mediterranean (Katsanevakis et al. 2014b). The
great taxonomic differences of alien species among ecoregions (Zenetos etal. 2012; Katsanevakis et al. 2014b), as well as the significant differences in
impacts among taxonomic groups, revealed in this study, partly explain thevariation detected among Mediterranean ecoregions.
A global effect of alien species invasions is biotic homogenization, theprocess of native biodiversity impoverishment happening simultaneouslywith a proliferation of alien species that results in the expansion ofhomogeneity in terms of genetic, taxonomic and functional diversity with
unclear biodiversity distinctions (Olden et al. 2004 and references therein).
Signs of biotic homogenization are evident in the marine ecosystems of theTsirintanis et al. (2022), Aquatic Invasions 17(3): 308–352, https://doi.org/10.3391/ai.2022.17.3.01

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Mediterranean Sea, as the establishment and advancement of biologicalinvasions in the basin have occurred alongside native biota impoverishment
and losses (Galil 2007 and references therein). In many cases, an impoverishedhomogeneous state has been spread within the Mediterranean basin, throughthe spread and dominance of some alien structural ecosystem engineers(Navarro-Barranco et al. 2018; Morri et al. 2019). The increasing rate of
biological invasions in the Mediterranean and the continuing seawater
warming led to the replacement of endemic populations by mostly
thermophilic Lessepsian species. Hence, the “Mediterranean character” ofthe marine biota progressively declines, contributing to the breakdown of
the regional distinctiveness of the Mediterranean Sea (Ben Rais Lasram andMouillot 2009).
In the current literature review, most studies on impacts on biodiversity
were based on medium and low strength of evidence. In agreement with
Katsanevakis et al. (2014a), the proportion of reported impacts with highstrength of evidence (i.e. manipulative and natural experiments) was low.
These studies were conducted in 13 out of the 22 Mediterranean countries,
with most cases (84%) reported from Italy, Spain, and France (Figure 20A).
The latter are the Mediterranean countries with the higher budget for
research and development (UNESCO 2021) (Figure 20B), reflecting theconnection between research robustness, number of experimental studies,and investment in research and development. Indeed, several studies relatescientific output to national spending on research and development, thenumber of universities in a country, GDP, and English proficiency (Man etal. 2004; Meo et al. 2013; Jamjoom and Jamjoom 2016; Mueller 2016).
Another possible reason for the higher inferential strength of impact
assessment studies in the western Mediterranean countries could be related
to the taxonomic distribution of alien species within the Mediterranean.
There is a higher species richness of alien macroalgae in the western
Mediterranean in comparison to the eastern basin, and the opposite
pattern for alien fish species, which have primarily invaded the eastern
Mediterranean (Katsanevakis et al. 2014b). Our analysis revealed that thevast majority (90%, n = 76) of experimental impact cases on biodiversity
reported from the western Mediterranean and the Alboran Sea assess
impacts caused by alien macroalgae, whereas no experimental study
investigates impacts caused by alien fish. At the same time, experimental
impact records are significantly lower in numbers in the Levantine and the
Aegean Sea and mainly refer to alien fish effects (71%; n = 14). Macroalgae
are sessile organisms, easier to be controlled in confined experimental
treatments, in contrast to mobile organisms such as fish. There is already ahigh level of difficulty in performing underwater experiments to investigate
ecological interactions due to the various factors that affect a diver’s
awareness such as visibility and temperature (O’Brien and Caramanna2017). In addition, species mobility may interfere with the success of an
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Figure 20. A) Number of reported experimental studies included in this review assessing
impacts on biodiversity, per Mediterranean country, B) Total intramural expenditure on Researchand Development (R&D), performed by some Mediterranean countries during 2018, expressedin Purchasing Power Parity dollars (UNESCO 2021).

applied underwater experiment and this fact can explain why experimental
research on alien species is more limited in the eastern Mediterranean,
dominated by mobile species invasions. Similar results were reported by
Kytinou et al. (2020), who reviewed methodological approaches globallythat analyse coastal shelf food webs, and concluded that only 14% of thereviewed studies conducted manipulative or natural experiments, and mostof the studies focused on benthic species and much less on fish. Also,
Thomsen et al. (2014) reviewed aquatic alien species’ experimental impact
assessment surveys within forty years (1972–2012) and found only one
alien marine fish species studied by experiments among more than ahundred different species. The species mobility hypothesis is further
supported by the fact that in the Levantine and the Aegean Sea most of the
impacts were reported by experimental studies on the herbivorous fishes
Siganus spp. with assessments based on the effects on macroalgal
communities, i.e. the sessile food of siganids.
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Furthermore, there are several additional confounding factors that
distort the actual impact patterns, such as paucity of data (Ojaveer et al.
2015), taxonomic impediment (Engel et al. 2021), challenges for assessing
and quantifying the actual impact of particular alien taxa (Carlton 2002;
Simberloff 2011; Davidson and Hewitt 2014; Strayer et al. 2017), and weakinferential strength of evidence (Katsanevakis et al. 2014a). Another aspect
to consider is that the current analysis examines impacts caused by eachalien species separately. Βut species do interact, and their cumulative
impacts are not necessarily additive but can be multiplicative or mitigative(Katsanevakis et al. 2016), also often interacting with other local or global
stressors such as climate change (Gissi et al. 2021). Hence, impacts by alien
species reported in a specific location are not necessarily representative of
the entire ecoregion. As a consequence, spatial patterns herein reported
should be interpreted with caution, as highlighted in other studies reporting
spatial patterns in biological invasions (e.g. Pyšek et al. 2008; Stranga andKatsanevakis 2021).
In addition, the methodological approach of the current impact
assessment framework is performed without chronological restrictions anddepicts the effects of alien and cryptogenic species on biodiversity,
ecosystem services and human health from the moment of the first impact
report of each targeted species until 2021. The temporal variation of
impacts was not taken into account. Still, invasive alien species can regress
after an invasion phase, following a so-called “boom and bust” invasion
pattern, as has been reported for Caulerpa cylindracea, C. taxifolia,
L. lallemandii and S. schimperi (Iveša et al. 2006; Montefalcone et al. 2015;
Dimitriadis et al. 2021; Santamaría 2021). Unfortunately, the literature ofmarine invasions sorely lacks scientific articles showing the evolution of
invaded sites over several decades (Strayer et al. 2017; Ojaveer et al. 2018).
The reason may be due to the functioning of scientific research, i.e. theshort duration of doctoral thesis projects, short-term funding, the need to
publish quickly, the lack of interest of scientific journals and reviewers inwhat seems routine monitoring, and probably also the fact that spectacular
bad news is easier to publish than good news. Hence, it is possible thatsome of the published impacts later declined in magnitude, due to the“boom-and-bust” dynamics of biological invasions. This stresses the need for
repetitive assessments and regular re-evaluation of the impacts of alien species.
We have provided a list of the “ten worst invasive species” in the
Mediterranean, based on reported impacts. Similar lists have been
compiled in the past (e.g. see Streftaris and Zenetos 2006; Katsanevakis etal. 2016) based on different approaches and metrics. Depending on thecriteria applied for impact assessment, different schemes can lead tostrikingly different outcomes (González-Moreno et al. 2019). Hence, anysuch ranking of invasive species should be perceived under the limitations
and assumptions of the analysis that produced it. For example, the present
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study did not account for the spatial distribution of impactful species andthe geographical extent of reported impacts, which for some species can bequite small (i.e. high impact but in a restricted area). Nevertheless, it isremarkable that our inventory of the ten worst invasive species is quite
similar to the respective ranking in Katsanevakis et al. (2016) [theirindicator D3], produced by a quite different approach, i.e. the sum of
cumulative impact scores of the species on marine habitats based on aconservative additive model (CIMPAL) across all 10 × 10 km cells thatcover the entire Mediterranean Sea. Eight of the ten top species are sharedby the two rankings.
We recorded a variety of impacts on biodiversity, ecosystem services andhuman health caused by alien and cryptogenic species. Without forgettingthat all introduced species represent a disturbance to nature by modifying
native ecosystems (Ricciardi et al. 2013), management choices need to be
based on robust evidence. This remains a primary need in the process ofevaluating the effects of alien species in ecosystems. The way forward tointerpret biological invasions and prioritise management actions is toincorporate holistic approaches to alien species impact assessments,
accounting for both positive and negative impacts and socio-ecologicaltradeoffs, and increase the strength of evidence through the implementationof more experimental studies.

Acknowledgements
We thank N. Koukourouvli for her assistance in GIS and Michèle Perret-Boudouresque fordocumentation assistance. We thank the two anonymous reviewers for their comments andsuggestions that significantly contributed to the improvement of the manuscript.

Funding declaration
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 andResearchers 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”.

Authors’ contribution
KTs: research conceptualization, design and methodology, review and data collection, data
analysis, writing the first draft of the manuscript; SK: research conceptualization, design andmethodology, data analysis, supervision, editing and writing; all authors: validating data,
contribution with additional data and taxonomic expertise, interpretation, editing and writing.

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Supplementary material
The following supplementary material is available for this article:
Appendix 1. Species-specific review of the impacts of alien and cryptogenic species on biodiversity, ecosystem services and humanhealth in the Mediterranean Sea, and other related information.
This material is available as part of online article from:http://www.reabic.net/aquaticinvasions/2022/Supplements/AI_2022_Tsirintanis_etal_Appendix.pdf

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