Research Article |
Corresponding author: Margarita Arianoutsou ( marianou@biol.uoa.gr ) Academic editor: Sven Jelaska
© 2023 Margarita Arianoutsou, Chloe Adamopoulou, Pavlos Andriopoulos, Ioannis Bazos, Anastasia Christopoulou, Alexandros Galanidis, Eleni Kalogianni, Paraskevi K. Karachle, Yannis Kokkoris, Angeliki F. Martinou, Argyro Zenetos, Andreas Zikos.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Arianoutsou M, Adamopoulou C, Andriopoulos P, Bazos I, Christopoulou A, Galanidis A, Kalogianni E, Karachle PK, Kokkoris Y, Martinou AF, Zenetos A, Zikos A (2023) HELLAS-ALIENS. The invasive alien species of Greece: time trends, origin and pathways. NeoBiota 86: 45-79. https://doi.org/10.3897/neobiota.86.101778
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The current paper presents the first effort to organize a comprehensive review of the Invasive Alien Species (IAS) of Greece. For this purpose, a database was developed with fields of information on the taxonomy, origin, ecology and pathways of introduction of terrestrial, freshwater and marine species. Our database includes a) taxa in the Union’s list that are present in Greece, b) taxa already present in Greece and considered to be invasive, and c) taxa highly likely to enter Greece in the next 10 years and become invasive. The Database served as the starting point for the compilation of the National List of Alien Invasive Species (HELLAS-ALIENS) in compliance with the EU Regulation 1143/2014. Overall, the HELLAS-ALIENS comprises 126 species, i.e. 32 terrestrial and freshwater plant species, 14 terrestrial invertebrates, 28 terrestrial vertebrates, 30 freshwater fishes and invertebrates and 22 marine species. Terrestrial invertebrates, birds and mammals are mainly of Asiatic origin. Most of the terrestrial plants have their native geographical distribution in the Americas (North and South). Most of the freshwater invertebrates and fishes are of North American origin, while the majority of the marine species are of Indo-Pacific origin. The first records of IAS concern terrestrial plant species, and date back to the 19th century, while those in freshwater and marine ecosystems seem to have been systematically recorded some decades later. Regarding the pathways of introduction, most of the taxa arrived in Greece or are expected to arrive through escape from confinement and unaided. The majority of the terrestrial, freshwater and marine species have been evaluated as of High-risk for the indigenous biodiversity and only 3% of the species listed have been evaluated of Low-risk. Our results provide an important baseline for management and action plans, as required by the priorities set by the European Union through the Biodiversity Strategy for 2030.
European Union, Invasive Alien Species Regulation, pathways of introduction, risk assessments, temporal trends
Biological invasions are a major threat to biodiversity, ecosystem services, the economy and human health (
New introductions of alien species have been accelerated in recent decades by the rapid globalization, urbanization and intensification of human activities (
Databases are important for gathering, sharing and disseminating information on alien species, fundamental for management, scientific and educational purposes (
At the country scale, the ELNAIS network and database (
The European Regulation 1143/2014 encompasses the list of IAS of Union Concern. The EU Regulation (hereafter referred to as the IAS Regulation) requires EU Member States to compile their national lists of IAS and carry out a comprehensive analysis and prioritization of the pathways of introduction and spread of IAS of Union concern. Greece initiated its alignment with the Regulation in February 2021 after an open call for tenders which rendered a project to the research group comprised of the authors of the current work. It was soon realized that any effort to compile a list of IAS should be supported by a database, with all important information on species origin, traits, status, habitat, pathways of introduction, potential impacts and geographical distribution.
The current work reports on the compilation of the Greek national list of IAS (HELLAS-ALIENS), along with their time trends, origin, principal pathways of introduction, and assessment of the risk they might impose.
Compilation of the national list of IAS of Greece (hereafter HELLAS-ALIENS) was based on the following criteria:
Taxa considered to be included in HELLAS-ALIENS were plants of the terrestrial environment (those of freshwater included), terrestrial vertebrates and invertebrates, freshwater fishes and invertebrates and marine organisms. Cryptogenic species were not considered.
For the selected taxa, contextual/relative information (available until November 2021) was collected and inserted in an exhaustive database, supporting and complementing the HELLAS-ALIENS. The structure of the database is given in Table
Category of information | Information |
---|---|
Taxonomy | Scientific name of species, genus, family, order, class |
Alien status | Invasive, potentially invasive, established, casual, unknown |
Origin | (non-exhaustive) Asian, American, Australian (for terrestrial and fresh water taxa), Circumtropical, Western Indo-Pacific (for marine taxa) |
Year of first observation in the wild | When available |
Pathway | Based on the |
Impact | Health, Economy, Natural Ecosystems, other ecosystem services (e.g., fisheries, tourism) |
Geolocation | Coordinates (WGS84), Region, Sea, Locality, Natura 2000 site, Island, Mountain |
Taxa specific traits | (non-exhaustive) in plants: Growth form, life form, pollination mode, flowering period, fruit type, dispersal mode |
(non-exhaustive) in birds: General guilds (e.g. birds of prey, landbirds, parakeets etc.), nest type, diet | |
Habitat | EUNIS, when available till level 2 ( |
References | Full reference of the bibliographic sources used for the compilation of information |
Comments | When applicable |
For the classification of species with respect to their pathways of introduction into a new area, the Convention on Biological Diversity scheme (
For filling the fields of the database various sources have been used: extensive literature reviews and peer-reviewed publications, existing databases [e.g. FishBase (
For species’ nomenclature, the most updated and widely accepted sources were used. In particular, the terrestrial plants’ nomenclature followed mostly the World Flora Online (
For the risk assessments (RAs) of taxa a mixed approach, based on the EU risk assessment framework that is compiled with the EU Regulation 1143/2014 and was developed under the “Study on Invasive Alien Species – Development of risk assessments to tackle priority species and enhance prevention” (
Overall, the HELLAS-ALIENS comprises 126 species, allocated in five general groups corresponding to terrestrial and freshwater plants (32 species), terrestrial invertebrates (14 species), terrestrial vertebrates (28 species), freshwater fishes and invertebrates (30 species) and marine species (22 species) (see Species List in Suppl. material
Of the 32 plant species of the HELLAS-ALIENS, 18 are considered invasive in Greece (Acacia saligna, Acer negundo, Ailanthus altissima, Azolla filiculoides, Bidens frondosa, Carpobrotus edulis, Cotula coronopifolia, Datura stramonium, Heliotropium curassavicum, Ludwigia grandiflora, Ludwigia peploides, Nicotiana glauca, Opuntia ficus-indica, Oxalis pes-caprae, Paspalum distichum, Phytolacca americana, Robinia pseudoacacia and Solanum elaeagnifolium) (
Twelve out of the 14 terrestrial invertebrate species included in the HELLAS-ALIENS are present in the country. These are ten insects (Aedes albopictus, Cydalima perspectalis, Halyomorpha halys, Harmonia axyridis, Linepithema humile, Paysandisia archon, Rhynchophorus ferrugineus, Solenopsis geminata, Xylotrechus chinensis, Xylotrechus stebbingi), one acari (Tetranychus evansi), and one platyhelminth (Caenoplana bicolor). Two species considered during the HS process as highly likely to arrive in the country were also included in the list, namely Bursaphelenchus xylophilus (the pine wood nematode or pine wilt nematode) and Megachile sculpturalis (the giant resin bee). One of the terrestrial invertebrate species of the HELLAS-ALIENS, Solenopsis geminata (fire ant) was included in the latest version of the EU list.
Terrestrial vertebrate species of the HELLAS-ALIENS included 28 species of amphibians, reptiles, birds, and mammals.
Three amphibians have been included: Lithobates catesbeianus, (American bullfrog), included in the EU list and well established in Crete, Xenopus laevis, (African clawed frog), a recent addition in the EU list that has casual occurrences in urban parks and Triturus carnifex, (Italian crested newt), that is highly likely to invade the country within the next ten years.
HELLAS-ALIENS includes five reptile species. Trachemys scripta, (pond slider), a species of Union concern and Podarcis siculus, (Italian wall lizard) are already established in the country. The Italian wall lizard is native to some parts of Europe, but it is considered invasive in others, with potentially significant impacts on the native herpetofauna (
Twelve bird taxa are included in the HELLAS-ALIENS. Three bird species with casual presence status in Greece have been included in the catalogue because they are EU-listed (Acridotheres tristis, Alopochen aegyptiaca and Threskiornis aethiopicus). Four bird taxa already established in Greece have been considered and included in the list, as they are threatening biodiversity (Alectoris rufa, Branta canadensis, Phasianus colchicus [non subsp. colchicus] and Psittacula krameri). The species Myiopsitta monachus (Monk Parakeet), well established in Attica, was also selected for the HELLAS-ALIENS following the recommended management approach (
In total, eight species of mammals were included in the HELLAS-ALIENS. Of those, seven are also included in the EU list. Two of them, the coypu, Myocastor coypus, and the racoon, Procyon lotor, are already established in Greece; three species (Ondatra zibethicus, Nyctereutes procyonoides, and Tamias sibiricus) have casual occurrences in the country; Herpestes javanicus has not yet arrived in Greece but was selected through the HS exercise. The species Callosciurus finlaysonii is present in the country only as a pet. Finally, the American mink, Neovison vison, though not of Union concern, is well established in Northwest Greece with already recorded impacts on native biodiversity (
The freshwater species of the HELLAS-ALIENS include 16 invertebrates and 14 fish species. With respect to the invertebrates, 12 species are well-established invasive or potentially invasive, while four more, i.e., Dreissena polymorpha (Zebra mussel), Pomacea maculata (Giant applesnail), Procambarus clarkii (the Red swamp crayfish) and Procambarus virginalis (Marmorkrebs) were added to the list following the HS procedure. Three freshwater invertebrate species, the established Pacifastacus leniusculus (American signal crayfish), and the crayfish species P. clarkii and P. virginalis currently not present in the wild, are included in the EU list.
As far as freshwater fishes are concerned, 12 species are currently present in the wild, while two more, Perccottus glenii (Chinese sleeper) and Ameiurus melas (the Black bullhead), were added to the list following the HS procedure as they are expected to invade Greek freshwater ecosystems. Lepomis gibbosus (Pumpkinseed) and Pseudorasbora parva (Stone moroko), established in Greece, are included in the EU List, while the also established and widespread Eastern mosquitofish Gambusia holbrooki was included in the EU list as recently as July 2022. Of the two species that are likely to arrive and invade, P. glenii is included in the EU list, while A. melas was included in the EU list in July 2022.
With respect to the marine species of the HELLAS-ALIENS, five are plants, nine are invertebrates and eight are fishes. Currently, the only marine species in the EU list are the Plotosus lineatus (striped catfish) and Rugulopteryx okamurae (brown seaweed). Although several marine species were proposed and risk assessed, none was approved for entering the EU list. Among the proposed ones it is worth mentioning two fishes, namely the silver-cheeked toadfish Lagocephalus sceleratus and the lionfish Pterois miles as well as the blue crab Callinectes sapidus and the rapa whelk Rapana venosa. The three former species are well established, with a wide distribution in the Greek seas whereas R. venosa has been sporadically reported in North Greece (
The origin of all taxa is presented in Fig.
Treemap graphical representation of HELLAS-ALIENS taxa origin. Colours of tiles are consistent within each group of organisms. A terrestrial taxa B freshwater taxa C marine taxa. C-IP: Central Indo-Pacific; W-IP: Western Indo-Pacific; CT: Circumtropical; T-NP: Temperate Northern Pacific; T-NWP: Temperate Northern Western Atlantic; TR-A: Tropical Atlantic; T-AA: Temperate Australo-Asia.
Most of the plants have their native range in the Americas (North and South), followed by those of Asian and African origin (Fig.
Most of the freshwater species, both invertebrates (88%, 14 taxa) and fishes (72%, 10 taxa), are of North American and, secondarily, of Asian origin (Fig.
As far as the marine species are concerned, the vast majority of all taxa are of Indo-Pacific origin (Fig.
The year of the first record in the wild has been detected for all 100 taxa currently present in the country. Data is available for 54 terrestrial species, 24 freshwater species and 22 marine species. The rate of introduction of new IAS records shows a rapid increase during the last two decades (Fig.
Number of new invasive alien species reported during the 1830–2021 period from Greece (blue) and cumulative number of species (red).
The pathways followed by the IAS of the HELLAS-ALIENS per environment are shown in Fig.
CBD principal introduction pathways for invasive species of Greece per environment. T: terrestrial; F: freshwater; and M: marine taxa.
Most of the terrestrial and freshwater plant taxa (27 taxa) have entered, or are expected to enter, Greece through escape from confinement (See Suppl. material
Most of the invasive terrestrial vertebrates in Greece have escaped from confinement and this pathway seems to apply also to the species that are expected to enter the country in the next 10 years. Only 17% of the vertebrates enter the country through natural dispersal across borders (Suppl. material
The majority of the terrestrial invertebrates (67%) have arrived as contaminants in transport pathways such as Xylotrechus chinensis, followed by transport-stowaway (17%) e.g., Aedes albopictus (Suppl. material
Six freshwater invasive invertebrates out of the 16 included in the HELLAS-ALIENS have been introduced through the transport – contaminant pathway (37.5%), six species (37.5%) have entered or are expected to enter unaided, while four species (25%) have escaped or are expected to escape from confinement. Seven freshwater invasive fishes (50%) have entered or are expected to enter the inland water ecosystems of the country unaided. Three species (21.4%) have been unintentionally introduced as transport-contaminants during commercial fish stockings, two species (14.3%) have escaped from confinement from aquaculture units and two species (14.3%) have been released in nature for sport fishing (Oncorhynchus mykiss) and biological control of mosquitoes (Gambusia holbrooki) respectively (Suppl. material
Regarding the IAS of the marine environment, all fish species (100%) have arrived unaided (Suppl. material
Out of the 126 taxa, 63% (79 taxa) were evaluated as of High-risk, 34% (43 taxa) as of Medium-risk and only 3% (4 taxa) as of Low-risk. High-risk taxa form the majority in all three environments (terrestrial, freshwater, and marine), with 65%, 60%, and 59% of taxa respectively (Fig.
In the High-risk RA category, 37 taxa have entered or are expected to enter Greece through escape from confinement, while 29 taxa have arrived or are expected to arrive in Greece unaided. In the Medium-risk RA category, 18 taxa entered, or are expected to enter, Greece through escape from confinement, 14 taxa have reached or are expected to reach Greece unaided, and 13 taxa have contaminated, or are expected to contaminate unintentionally, transferred commodities. All taxa using corridors as a pathway category (exclusively terrestrial plants) are of High-risk (Fig.
Grouped bar chart representing percentage of taxa per Risk Assessment category across different environments.
Alluvial diagram showing the distribution of introduction pathways across impact categories for all taxa. Nodes on the left represent different CBD principal pathways and nodes on the right the classification of taxa by Risk Assessment categories. Same colour between pathway and risk assessment nodes indicates that all taxa using the specific pathway are exclusively classified in the particular impact category.
The scope of the EU 1143/2014 Regulation is to prevent new arrivals and the establishment of IAS in the member states. Consequently, the compilation of national lists and prioritization of their pathways of introduction are of high importance for managing biological invasions. The current study provides a solid scientific base to meet these requirements.
The rate of introductions varied over time, with the number of new IAS arrivals increasing after 1970. Similarly, the introduction rate of species follows a sharp increase after the same period. Records for terrestrial taxa seem to predominate. This could reflect the emphasis placed on monitoring the terrestrial environment, the fact of more frequent introductions in this environment, or the fact that the effects of invasions are more easily detected. Unfortunately, studies on biological invasions in both aquatic and terrestrial environments are rather sparse, so there is not much comparison possible within this field.
As previously mentioned, terrestrial plants were the first invasive species to be recorded, with some records dating back to the first half of the 19th century. Phytolacca americana (A. Strid, pers. comm. 2022) and Datura stramonium (Bory de Saint-Vincent and Chaubard 1832-33) were the alien species first observed in the wild (ca. 1830). Similar to other studies (e.g.,
All terrestrial vertebrates of the HELLAS-ALIENS were introduced into the wild after 1960, except for the Ring-necked Pheasant, which has been intensively reproduced and released as game during the 20th century all over Greece; yet there is no information on the date and place of its first introduction in the wild (
Regarding the twelve terrestrial invertebrates already present in Greece, all first records are after 2003 with the exceptions of the harlequin ladybird Harmonia axyridis which was introduced intentionally in the early 1990s (
As for the new records of alien freshwater organisms, they seem to have peaked in the period 2000–2010 and, to a lesser degree, in 2010–2020, probably reflecting the increasing negative impacts of globalization on native freshwater biodiversity (
The highest number of new introductions for the marine environment of Greece dates back to the 1990s. While only five IAS had entered the Greek marine waters by 1970, and none in the 1970–1980 period, the trend of new introductions appears to be increasing and culminates in the 1990–2000 period with seven new marine IAS. In the last two studied periods, the number of IAS ranges from four to five per decade. This trend in marine waters follows the pattern observed in the Mediterranean Sea for all new alien species introductions (not only invasive ones).
Temporal trends within taxonomic groups, which constitute the sum for each environment, are observed and can be explained by the different pathways of introductions of species that differ in their ecology. We must note here that the species included in our analysis are in their majority established species that have been evaluated as invasive.
Terrestrial and freshwater plants constitute a large portion of the species comprising the national list of Greece. This is probably because plant species are easier to be studied but also to the fact that plant species are widely used for ornamental purposes, combined with the fact of easily escaping from confinement. The use of exotic plants in landscape improvement and reforestation used also to be a very common practice; hence, these plants could easily escape and expand their distribution and finally become invasive. The current list comprises 32 terrestrial and freshwater plant taxa of which 84% have escaped from confinement. This is in agreement with relevant studies (
Fifteen plant taxa were classified as of High-risk and 16 as of Medium-risk, while only one species (Matricaria discoidea) was classified as of Low-risk. M. discoidea has been present in Greece since 1994 and, although it is considered an invasive species, its populations are spatially limited to specific mountains where they are found mainly at high altitudes, in stony/gravelly places (
Most alien invasive plants in Greece originate from the Americas followed by Asian and African species. This pattern is similar to that observed for all alien plants recorded in Greece (
A published consolidated list of alien terrestrial vertebrates in Greece is missing. According to the HELLAS-ALIENS list, invasive terrestrial vertebrates already present in the wild add approximately 8%, 3%, 2% and 6% to the native amphibians, reptiles, birds and mammals, respectively.
HELLAS-ALIENS contains three terrestrial vertebrate IAS that are native to other parts of Europe and thus cannot be considered for the EU list: Alectoris rufa, Podarcis siculus, and Triturus carnifex. The latter is highly likely to invade the country within the next 10 years as the Horizon exercise performed has shown. Alectoris rufa, has been introduced in the wild as game since at least 1979 (
Another vertebrate worth mentioning in the HELLAS-ALLIENS is Neovison vison, (American mink) which is already established in Northwest Greece (
Importation of pets followed by either their deliberate release or escape from confinement seems to be an important pathway for several terrestrial vertebrates in accordance with the general pattern in Europe (
Twenty-one terrestrial vertebrate species have been assessed as of High-risk, five as of Medium-risk and two of Low-risk for the native biodiversity. High-risk species include, among others, the well-established in Crete Lithobates catesbeianus, (the American bullfrog), a carrier of the lethal chytrid fungus that threatens amphibian populations worldwide (
Most of the terrestrial invertebrates on HELLAS-ALIENS are likely to have detrimental impacts to economic sectors such as agriculture, forestry, the tourism industry and human health (
Updated, relatively recent compilations available for freshwater fishes indicate that alien freshwater fish species of the HELLAS-ALIENS list add approximately 17% to the native freshwater ichthyofauna of Greece (
Invasion by alien species constitutes a leading cause of the rapid global freshwater biodiversity loss (
The origin of the vast majority of marine IAS included in the HELLAS-ALIENS was the Indo-Pacific and in particular the west Indo-Pacific. Most marine IAS have entered Greek waters via the Suez Canal, but not directly. Indeed, the impact of the Suez Canal in the introduction of marine aliens has been previously documented (e.g.,
For the marine environment, ten (45% of taxa) and seven (32% of taxa) of High and Medium-risk taxa respectively have arrived unaided. It is worth noting that Penaeus aztecus, the only taxon that has potentially escaped from confinement, is of High-risk, while the pearl oyster Pinctada radiata which has been intentionally released, is of Medium-risk. All marine plants are of High risk. Finally, alien marine taxa add approximately 7% to the native marine biota (
The present study provides a thorough analysis of the IAS of Greece. Our results based on the systematic review of existing literature reveal that a considerably high number of terrestrial plants and freshwater organisms are threatening local biodiversity and may also pose serious problems in the economy and society, as is the case of marine species (
This work has been funded by the Hellenic Ministry of Environment and Energy, project: “Compiling the National Catalogue of Alien Species and Methodology for their Risk Assessments”. Dr Arne Strid is gratefully acknowledged for providing georeferenced data on plant species; Dr Nicholas Koutsikos and Dr Ioannis Karaouzas are acknowledged for assistance in the compilation of the freshwater species’ list, as well as for the provision of georeferenced data on freshwater fish species (N. Koutsikos); Mr Odysseas Froilan Papageorgiou and Dr Rigas Tsiakiris for the provision of their personal observations of the Alectoris rufa and Branta canadensis in the wild, respectively. The following scholars have assisted in the Horizon Scanning exercise: Tim Adriaens (Research Institute for Nature and Forest, INBO Brussels, Belgium), Dimitrios Avtzis (Institute of Forest Research, DEMETRA Hellenic Agricultural Organization), Sandro Bertolino (Dipartimento di Scienze della Vita e Biologia dei Sistemi, Università degli Studi di Torino, Italy), Giuseppe Brundu (Università degli Studi di Sassari, Department of Agricultural Sciences), Martina Carrete (Department of Physical, Chemical and Natural Systems, Universidad Pablo de Olavide, Sevilla, Spain), Vassilios Gerovassiliou (University of the Ionian), Ioannis Karaouzas (Hellenic Centre for Marine Research, Greece), Nicholas Koutsikos (Hellenic Centre for Marine Research, Greece),. Emiliano Mori (Consiglio Nazionale Delle Ricerche, Istituto Di Ricerca Sugli Ecosistemi Terrestri, Sesto Fiorentino, Florence, Italy), Konstantinos Perdikaris (Department of Fisheries, Regional Unit of Thesprotia, Greece), Vladimir Pešić (University of Montenegro, Montenegro), Jodey Peyton (UK Centre for Ecology and Hydrology), Marina Piria (Zagreb University, Croatia), Wolfgang Rabitsch (Environment Agency, Austria), Canella Radea (National and Kapodistrian University of Athens, Greece), Filipe Ribeiro (University of Lisbon, Portugal), Helen Roy (UK Centre for Ecology and Hydrology), Riccardo Scalera (IUCN SSC Invasive Species Specialist Group, Rome, Italy), Elena Tricarico (University of Florence, Italy). Finally, special thanks are due to the two anonymous reviewers for their useful comments and Sven Jelaska, editor, for his valuable and detailed comments to the latest version of the manuscript.
List of HELLAS-ALIENS species
Data type: excel file with a list of species
Explanation note: The file contains the full list of alien invasive species of Greece.
CBD principal introduction pathways for terrestrial invasive alien species of Greece per different categories
Data type: figure
Explanation note: fig. S1: CBD principal introduction pathways for terrestrial invasive alien species of Greece per different categories. The category vertebrates includes amphibians, reptiles, birds and mammals.
CBD principal introduction pathways for freshwater invasive alien species of Greece per different categories
Data type: figure
Explanation note: fig. S2: CBD principal introduction pathways for freshwater invasive alien species of Greece per different categories. The category vertebrates corresponds to fishes.
CBD principal introduction pathways for marine invasive alien species of Greece per different categories
Data type: figure
Explanation note: fig. S3: CBD principal introduction pathways for marine invasive alien species of Greece per different categories. The category vertebrates corresponds to fishes.
Alluvial diagram showing the distribution of introduction pathways across impact categories
Data type: figure
Explanation note: fig. S4: Alluvial diagram showing the distribution of introduction pathways across impact categories. Nodes on the left represent different CBD main pathways and nodes on the right the classification of taxa by Risk Assessment categories. Same colour between pathway and risk assessment nodes indicates that all taxa using the specific pathway are exclusively classified in the particular impact category. A: terrestrial; B: freshwater; C: marine taxa.