Aquatic Invasions (2022) Volume 17, Issue 3: 353–373
CORRECTED PROOF

Research Article

Alien species of the Romanian and Bulgarian Black Sea coast:state of knowledge, uncertainties, and needs for future research
Raluca I. Băncilă1,2,*, Marius Skolka2, Petya Ivanova3, Victor Surugiu4, Kremena Stefanova3, Valentina Todorova3and Argyro Zenetos5
1 “Emil Racoviţă” Institute of Speleology of Romanian Academy of Science, 13 Septembrie Road, No. 13, 050711, Bucharest, Romania
2 Ovidius University Constanț a , Faculty of Natural and Agricultural Sciences, Constanța 900470, Romania

3 Institute of Oceanology – Bulgarian Academy of Sciences, First May Street 40, P.O. Box 152, Varna 9000, Bulgaria
4 “Alexandru Ioan Cuza” University of Iași, Faculty of Biology, Bulevardul Carol I, No. 20A, RO-700507 Iași, Romania

5 Institute of Marine Biological Resources and Inland Waters, Hellenic Centre for Marine Research, 19003, Anavyssos, Greece*Corresponding author
E-mail: bancila_ralucaioana@yahoo.com

Citation: Băncilă RI, Skolka M, Ivanova P,
Surugiu V, Stefanova K, Todorova V,
Zenetos A (2022) Alien species of the
Romanian and Bulgarian Black Sea coast:state of knowledge, uncertainties, andneeds for future research. Aquatic
Invasions 17(3): 353–373, https://doi.org/10.
3391/ai.2022.17.3.02

Received: 11 February 2022
Accepted: 5 April 2022
Published: 24 June 2022
Thematic editor: Charles Martin
Copyright: © Băncilă 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
In order to assist the implementation of the European policies on Invasive Alien
Species (IAS Regulation) and mitigate the impact of alien species that threaten themarine ecosystem services and biodiversity, accurate lists of alien species per
European Member State are required. Although inventories of marine alien species
and relevant information about them have been reported for the Black Sea marine
region of Romania and Bulgaria, a validated list of alien species for the two countries
is still lacking. In this paper we (i) propose a validated list of the marine alien species
occurring in the Romanian and Bulgarian Black Sea regions, and (ii) address errors,
gaps and uncertainties associated with listing alien species from the marine watersof the two countries. The list of alien species includes 37 species for Romania and26 for Bulgaria, with the highest number of alien species belonging to the phylum
Arthopoda for both countries. The majority of alien species have been classified as
successfully established in the marine waters of both countries. Thirteen alien species
were classified as invasive in Romania whilst eight alien species were classed as
invasive in Bulgaria. The historical overview indicates that the number of alien
species has steadily increased over the last 50 years both in Romania and Bulgaria.
The results of our study provide the baseline list and information for addressing
marine alien species at a national level and a starting point for selecting theinvasive alien species for risk assessment towards an effective implementation of
the IAS Regulation. In conclusion, this study provides supporting information for
implementing measures to tackle the introduction of alien species in the western regionof the Black Sea. These measures are needed to build an early warning, prevention,and control of invasive alien species in the Black Sea, a unique and fragile ecosystem.
Key words: marine species, cryptogenic, crypto-expanding, species listing

Introduction
Alien species (i.e., species that certainly have been introduced throughhuman activity) pose a serious threat to marine ecosystem services andbiodiversity (Wallentinus and Nyberg 2007; Katsanevakis et al. 2014). A
worldwide increase of the annual rate of first records of alien species hasBăncilă et al. (2022), Aquatic Invasions 17(3): 353–373, https://doi.org/10.3391/ai.2022.17.3.02

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been reported for the last 200 years, 37% of first records referring to theperiod 1970 to 2014 (Seebens et al. 2017). Although the rate of introductionof new alien species in European Seas has slowed down over the last few
years (Korpinen et al. 2019), the European Seas still hold the highest
number of alien species worldwide (Tsiamis et al. 2018). To tackle the issueof alien species, a specific target, i.e., the Aichi Target 9, has been approved
under the Strategic Plan for biodiversity (2011–2020), adopted by theconference of parties at the Convention on Biological Diversity (CBD) in2010. The Aichi Target 9 aimed that by 2020 identification of invasive alien
species and their introduction pathway(s) are prioritized. Moreover, theEuropean Union (EU) adopted the Marine Strategy Framework Directive(MSFD) (Directive 2008/56/EC), which specifically aims to protect themarine ecosystem across Europe and to achieve Good Environmental
Status (GES) by 2020, alien species being treated as a distinct Descriptor(i.e., D2) of GES. Furthermore, the EU Regulation 1143/2014 on Invasive
Alien Species has also been adopted aiming at the prevention andmanagement of the introduction and spread of invasive alien species. To
assist the implementation of specific legal instruments on Invasive Alien
Species (IAS) and mitigate the impact of alien species, accurate lists of alien
species, per each European Member State and marine region as defined by
MSFD, are required (Tsiamis et al. 2019). However, an evaluation ofreported alien species prior to 2012 revealed geographical bias in sampling
efforts associated with the reporting regions (Tsiamis et al. 2019) anderrors in the listing of alien species (Zenetos et al. 2017). For example,
updates of lists of alien species in the marine waters of Greece (PancucciPapadopoulou et al. 2005; Zenetos et al. 2009, 2011, 2018, 2020a) revealed
that these lists suffer from a variety of errors. The errors included taxonomic
issues (i.e., synonyms and species misidentification), erroneous reports,
misclassification of native or natural range expansion species as alien species(Zenetos et al. 2018; Gómez 2019). Recurrent updates of inventories ofalien species from the Mediterranean region (Zenetos et al. 2005, 2008, 2010,2012, 2017; Zenetos and Galanidi 2020) have shown similar inaccuracies.
Since these biases and errors might have serious consequences on thepolicy information and management of biological invasions (McGeoch etal. 2012), reporting updated and accurate lists of alien species is cruciallyneeded. Shipping through the release of ballast water has been identified as
the major and often the primary vector for introduction of alien species
into the Black Sea. The ballast water management convention (BWMC,
IMO 2004), which provides a set of management tools for ballast waters,
entered into force in 2017. To adequately implement the BWMC and to
reduce the number of ballast-transported alien species addressing theuncertainties associated with the identification, distribution, andpathway(s)/vector(s) of introduction of alien species is an important step.
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The Black Sea is the largest anoxic body of water in the world (Bronfman
1995), with only 10% of its total water volume suitable for aquatic organisms(Andrussov 1918; Zenkevich 1963; Zaitsev and Mamaev 1997). It is an
isolated sea connected to the Mediterranean Sea only through narrow
Turkish Straits. Such particular conditions make the Black Sea a uniqueand fragile ecosystem, with low biodiversity, but with high biologicalproductivity. It hosts nearly 800 phytoplankton species, 2000 invertebrates,and 200 fish species (Zaitsev and Alexandrov 1998). However, the BlackSea is a recipient of alien species from several donor regions (i.e., North
Atlantic, East Atlantic-Mediterranean, West Pacific, South-East Asia,
South-West Pacific, Indo-Pacific) (Zaitsev et al. 2004; Tsiamis et al. 2018).
Studies on the invasion of alien species showed that the native biota of theBlack Sea are severely threatened by alien species (Kideys 2002; Gomoiu etal. 2002; Seebens et al. 2017). Moreover, due to its geographical position,
being a sea surrounded by land, the survival and establishment of marine
alien species into the Black Sea might be amplified by climatic change.
Increase of the mean annual water temperature might make the Black Sea
environment more favorable or suitable to certain alien species, i.e.,
warmer waters better matching the thermal tolerance of alien species orcertain alien species could invade based on climate change. The climaticchallenge enhancing the survival and establishment of marine alien species
has been already acknowledged for the Mediterranean Sea, another semienclosed sea, which is currently considered a true hotspot of marine
bioinvasions (Mannino et al. 2017). The increase in the temperature of theMediterranean waters’ accounts for introduction of Erythrean species fromthe Suez Canal and the ingression of the Atlantic thermophilic species into
the Mediterranean through the Gibraltar Strait (Mannino et al. 2017). It isalso worth mentioning that since 2000, an intensification of penetration of
species from the Mediterranean Sea into the Black Sea has been reported(Shalovenkov 2020). Thus, the warming of the Black Sea might be responsible
for the increase of invasion of Mediterranean species into the Black Sea,
through the Turkish Straits, the so-called process of “Mediterranization” of
the Black Sea (Puzanov 1965).
Despite the global increase of the number of alien species, the number ofalien species reported from the Black Sea in recent assessments varies
greatly. For instance, the assessment performed by Zaitsev et al. (2002)
reported 41 alien species, the study carried out by Aleksandrov (2015)
listed 261 alien species, whilst Shalovenkov (2019), in a recent publicationon the alien species invasion in the Black Sea, reported 180 alien species. By
contrast, a search in 2020 in the AquaNIS database (AquaNIS, Editorial
Board 2015) for the Black Sea region returned 293 alien and cryptogenic
species. These discrepancies make the information about the alien species
in the Black Sea ambiguous and difficult to interpret. Although thereported number of alien species is not particularly high, due to the specificBăncilă et al. (2022), Aquatic Invasions 17(3): 353–373, https://doi.org/10.3391/ai.2022.17.3.02

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List and information on alien species in the western Black Sea regionhydrological and environmental conditions of the Black Sea, some of them
have developed mass populations, causing significant changes to native
species communities and in the overall ecological properties of the sea(Kideys 2002). For example, the comb jelly Mnemiopsis leidyi A. Agassiz,
1865, a ctenophore originating from the eastern coast of the United Statesand introduced accidentally to the Black Sea reached enormous biomass
levels (up to 4.6 kg m-2) in the summer of 1989, devastating the food chainof the whole Black Sea basin (Shiganova et al. 2001). Their voracious feeding
led to a significant decrease of the abundance of small pelagic fish species
and to an order of magnitude lowering of zoopankton abundance.
Moreover, geographical biases are evident in the Black Sea, such that more
research has been conducted in the central and eastern part of the BlackSea, with important contribution from Russia (see Boltachev and Karpova
2014; Revkov 2016; Shalovenkov 2017, 2020), Turkey (see Serdar andÖzcan 2018) and Georgia (see Vadachkoria et al. 2020), than in the westernpart of the Black Sea. Therefore, a reviewed list of alien species is essential
prior to any risk assessment underpinning early warning, prevention andcontrol methods of invasive alien species in the Black Sea.
The East and South European Network for Invasive Alien Species(ESENIAS), a regional network established in 2011 by the European
Environment Agency, Ministry of Environment and Water of Bulgaria,
Bulgarian Academy of Sciences, is an important initiative for assessing
alien species in the Black Sea countries. One of the main activities of
ESENIAS, supported throughout the ESENIAS-TOOLS and the largest
project implemented by ESENIAS countries, was to compile a common listof alien species in the Balkan region (i.e., ESENIAS countries) (Trichkova
et al. 2017). Although marine alien species in some taxonomic groups werereported as part of ESENIAS scientific outcomes (e.g., Karachle et al. 2017),
an accurate inventory based on recent updates and scientific validation of
the obtained data still needs to be done.
In this paper we aim to present a reviewed, updated, and validated list ofalien species from the marine regions of Romania and Bulgaria, both BlackSea ESENIAS countries. The list will serve as a baseline towards theimplementation of recent invasive species policies, both internationallyand at the level of EU countries. Furthermore, we propose to address theuncertainties associated with the identification, distribution, andpathway(s)/vector(s) of introduction of alien species into Bulgarian andRomanian marine waters.

Materials and methods
To compile the list of alien species from Black Sea marine regions ofRomania and Bulgaria we: (i) performed a comprehensive screening of theliterature (i.e., peer reviewed and indexed and non-indexed papers, PhD
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theses, grey literature) published by December 2021 (in time interval 1912
to 2021) and (ii) accessed the data archived in the Hellenic Centre forMarine Research / European Environment Agency database and available
on that date. For Bulgaria, additional data (not yet published nor included
in relevant databases) was obtained from fieldwork surveys carried out in
Varna Bay during the spring-summer-autumn season between 2015 and2016 (ESENIAS project). As a result, our data include the first records, i.e.,
certain species reported for the first time during the sampling within theframework of ESENIAS project. The compiled list of species based on the
bibliographic and field work surveys was checked against the AquaNIS
database (AquaNIS, editorial Board 2015) and the Global Register ofIntroduced and Invasive Species (GRIIS) list. The additional species registeredin the AquaNIS database and/or GRIIS list as alien or cryptogenic species,
were added to the starting list. To avoid uncertainties associated withnomenclature for each species we checked its status according to theWorld Register of Marine Species (WoRMS Editorial Board 2020). Whenneeded, species names were corrected taxonomically in agreement with
WoRMS, and synonyms and alternate representations were provided(WoRMS status in Supplementary material Tables S1–S3).
Local experts were invited to check for possible errors, to validate thespecies on the list, and to suggest exclusions of species from the list. They
were also asked to explain the reason for exclusion. For example, thespecies were excluded because they were extinct species (e.g., Verruca
spengleri Darwin, 1854), misidentified species (e.g., Oithona brevicornis
Giesbrecht, 1891 misidentification of Oithona davisae Ferrari F.D. & Orsi,
1984), native species (e.g., Vaucheria dichotoma f. marina Hauck, 1884),
species expanding their range through natural means (e.g., Bolinopsis vitrea(L. Agassiz, 1860), and species that cannot survive in high salinity marine
waters such as freshwater species or species that are occasionally found inslightly brackish estuarine habitats (e.g., Umbra krameri Walbaum, 1792).
All species that fit these exclusion criteria were removed from the initial list.
For the species retained on the refined list we first gathered data on
species status as follows: alien, cryptogenic and crypto-expanding. Cryptogenic
is a term that includes species that cannot be assigned with certainty toeither native or introduced species in their occurrence area (Carlton 1996).
Crypto-expanding is a recent term (Zenetos et al. 2020b), first introducedin the ESENIAS-tools project (Trichkova et al. 2017) and adopted by
Tsiamis et al. (2021). This term was used for species with an unclear arrival
or introduction pathway(s)/vector(s). For example, a crypto-expanding
species refers to a species that either arrived through natural range
expansion from another area, as it is the case of some species from theMediterranean Sea which arrived in the Black Sea via the Turkish Straits,
or were introduced through human activity. Thus, in the context of theBlack Sea invasions the term crypto-expanding serves our purpose betterBăncilă et al. (2022), Aquatic Invasions 17(3): 353–373, https://doi.org/10.3391/ai.2022.17.3.02

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when dealing with uncertainties in alien species listing than the term
cryptovectic (Carlton and Ruiz 2005). As defined by Carlton and Ruiz
(2005) cryptovectic species are species for which the pathway(s)/vector(s)is unknown, which means that several vectors (polyvectism) move thespecies along the same or different multiple routes causing its occurrence
in a new region. We also did not consider the widely accepted term
secondary introduction. The term is intended for species which were initiallyintroduced in a new region through human mediated translocation andfrom where they might continue to spread by natural or anthropogenic
mechanisms (i.e., species introduced in the first instance to the Russiancoast of the Black Sea that arrives to Romanian and Bulgarian shores). This
is not the case for either cryptogenic or crypto-expanding species. Second, we
gathered data on the species native distribution range, i.e., the distributional
range where the species is considered native. For species validated as alien,
we further classified their native distribution based on the global marine
biogeographic realms proposed by Spalding et al. (2007). We assigned
multiple realms to a species if the native distribution of that species
covered more than one marine realm. For one alien species, i.e., Polydora
cornuta Bosc, 1802, the native distribution range is unknown. Third, we
gathered data on species first sighting or collection date (year or range ofyears); if the precise first sighting or collection date was not mentioned in
the source article, we used the before symbol “<” and the year in which thesource article was published. Finally, we gathered data on species establishment
success. Following the terminology and classification of Blackburn et al.
(2011), Zenetos et al. (2018, 2020a) species were assigned to one of thefollowing four categories: (i) established (a species with at least one selfmaintaining population currently occurring in the wild); (ii) invasive (anestablished species with rapid expansion of its distribution range and highprobability to negatively affect the native biodiversity of the invaded
ecosystem and its services; (iii) casual (a species reported based on one orvery few individuals and with not yet proved ability to spread or reproduce
in its occurrence area); (iv) unknown (a species with currently no available
information on the establishment success, due to incomplete documentationof its abundance or distribution range, or unconfirmed occurrence in aparticular location where it has been previously recorded or reported forthe first time).
For the species classified as alien we also gathered data on: (i) the mostplausible primary pathway(s)/vector(s) of introduction, in accordance with
CBD classification (CBD 2014), and (ii) the certainty of introduction
pathway(s)/vector(s) assignment. Since the terms pathway and vector areused frequently in the text, for more clarity we use herein bothinterchangeably. Pathway would be an adequate term and the ideas
surrounding the term vector are included in our use of the term pathway
and vice-versa. According to CBD classification the pathways of alienBăncilă et al. (2022), Aquatic Invasions 17(3): 353–373, https://doi.org/10.3391/ai.2022.17.3.02

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species introduction in European Seas are: (i) corridor (COR) (e.g.,
movement of alien species via canals); (ii) escape from confinement (EC)(e.g., aquaculture); (iii) transport stowaway (TS) (e.g., moving of live alien
species by maritime transport via ballast water and sediments, bio-foulingof water vessels and dredging, angling or fishing equipment); (iv) release innature (REL) (e.g., intentional introduction of live alien species forfishing); (v) transport contaminant (TC) (unintentional movement of live
pests, through international trade); (vi) unaided (UNA) (e.g., naturaldispersal of invasive alien species that have been introduced by different
pathways). We defined four certainty levels (Katsanevakis et al. 2013) as
follows: (i) level “1” which corresponds to a very high certainty (i.e., thepathway was documented), (ii) level “2” refers to a medium certainty (i.e.,
the pathway is very likely), (iii) level “3” attributed to low certainty (i.e., thepathway is likely), and (iv) level “4” assigned to unknown pathway.
To show how the number of new records reported since 1970 for thealien, crypto-expanding, and cryptogenic species varied in time (MSFD
descriptor D2, criterion D2C1) we grouped the number of new reports per
six-year time intervals and calculated the cumulative number of species
over time. The chi-square (χ2) test was used to test for significant differences
between countries and among categories (i.e., alien, crypto-expanding andcryptogenic species) of the taxonomic affiliation, establishment success,origin, variation in new records reported over time, and introduction
pathway(s). All the graphics in the manuscript were generated using the
package ggplot2 in R, version 3.5.1. (R Core Team 2022).

Results
The literature search generated 218 references from the year 1912 to 2021
(see Table S4). The initial list included 194 species, out of which 43 species
were suggested by the local experts to be excluded from the list (see Table S1for detailed information about them including reason for exclusion), 38
species were validated as alien (Table 1 and Table S2) and a total of 113
species were classified as crypto-expanding, cryptogenic, and data deficient(Table S3). There was a nonsignificant difference in the overall number ofalien, cryptogenic and crypto-expanding species between the two countries(χ2 = 4.6709, df = 2, P = 0.096). When each country was consideredseparately, the validated list of alien species included 37 species for
Romania and 26 for Bulgaria, respectively (Table 1 and Table S2 for detailed
information). Eleven alien species were exclusive to Romania, while fromall 26 alien species present in Bulgaria only one was not shared with Romania.
Furthermore, 29 cryptogenic and 72 crypto-expanding species were
documented for Romania while for Bulgaria we found 22 cryptogenic, 28
crypto-expanding, and 6 data deficient species. Eleven cryptogenic and 46
crypto-expanding species were exclusive to Romania and four cryptogenic,Băncilă et al. (2022), Aquatic Invasions 17(3): 353–373, https://doi.org/10.3391/ai.2022.17.3.02

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Table 1. The validated list of alien species recorded in the Black Sea marine region of Bulgaria (BG) and Romania (RO) (seeTable S2 for detailed information about them) and their establishment success following the terminology and classification ofBlackburn et al. (2011), and Zenetos et al. (2018, 2020a): casual (cas), established (est), invasive (inv), and unknown (unk).
PhylumTaxon

SpeciesAnnelida

Polychaeta
Polychaeta
Polychaeta
Polychaeta
Polychaeta
Polychaeta
Polychaeta
Oligotrichea
Ascidiacea
Ascidiacea
Nuda
Tentaculata
Hydrozoa
Anthozoa
Cirripedia
Cirripedia
Cirripedia
Copepoda
Copepoda
Decapoda
Decapoda
Decapoda
Decapoda
Decapoda
Decapoda
Decapoda
IsopodaBivalvia
Bivalvia
Bivalvia
Bivalvia
Bivalvia
Gastropoda
Gastropoda
Phaeophyceae
Bacillariophyceae
Bacillariophyceae
PiscesAlitta succinea (Leuckart, 1847)
Amphiglena mediterranea (Leydig, 1851)
Dipolydora quadrilobata (Jacobi, 1883)
Ficopomatus enigmaticus (Fauvel, 1923)
Laonome xeprovala Bick & Bastrop, in Bick et al. (2018)
Polydora cornuta Bosc, 1802
Streblospio gynobranchiata Rice & Levin, 1998
Eutintinnus lusus-undae (Entz, 1885)
Molgula manhattensis (De Kay, 1843)
Styela clava Herdmann, 1881
Beroe ovata Bruguière, 1789
Mnemiopsis leidyi A. Agassiz, 1865
Calyptospadix cerulea Clarke, 1882
Diadumene lineata (Verrill, 1869)
Amphibalanus amphitrite (Darwin, 1854)
Amphibalanus eburneus (Gould, 1841)
Chthamalus stellatus (Poli, 1791)
Acartia tonsa Dana, 1849
Oithona davisae Ferrari F.D. & Orsi, 1984
Alpheus dentipes Guérin, 1832
Callinectes sapidus Rathbun, 1896
Eriocheir sinensis H. Milne Edwards, 1853
Eurypanopeus depressus (Smith, 1869)
Hemigrapsus sanguineus (De Haan, 1835)
Palaemon macrodactylus Rathbun, 1902
Rhithropanopeus harrisii (Gould, 1841)
Sphaeroma walkeri Stebbing, 1905
Anadara kagoshimensis (Tokunaga, 1906)
Arcuatula senhousia (Benson, 1842)
Magallana gigas (Thunberg, 1793)
Crassostrea virginica (Gmelin, 1791)
Mya arenaria Linnaeus, 1758
Corambe obscura (A.E. Verrill, 1870)
Rapana venosa (Valenciennes, 1846)
Desmarestia viridis (O.F. Müller) J.V. Lamouroux, 1813
Lauderia pumila Castracane, 1886
Thalassiosira nordenskioeldii Cleve, 1873
Planiliza haematocheila (Temminck & Schlegel, 1845)

Ciliophora
Chordata
Ctenophora
Cnidaria
Arthropoda

Mollusca

Ochrophyta
Chordata

BG
est
inv
inv
inv

inv
inv
unk
est
cas
est
est
est
est
est
cas
est
inv
cas
est
inv
est
inv
unk
est
unk
est

Country

RO
est
cas
inv
inv
est
inv
inv
est
est
est
inv
inv
est
inv
cas
est
est
est
est
est
est
est
cas
est
inv
est
inv
cas
est
est
inv
inv
inv
est
est
est
inv

two crypto-expanding and three data deficient species to Bulgaria,
respectively. Forty-four species, i.e., 18 cryptogenic, 26 crypto-expanding
and three data deficient species, were shared by both countries (Table S3).
We found a significant difference in the number of species among thetaxonomic groups for both countries (Romania: χ2 = 82.905, df = 24, P < 0.001;
Bulgaria: χ2 = 56.388, df = 20, P < 0.001). The highest number of alien
species belonged to the phylum Arthopoda, whilst the phylum Myzozoa
was the best represented for both cryptogenic and crypto-expanding species
in both counties (Figure 1). The chi-square test also revealed significant
differences in the establishment success among alien, cryptogenic andcrypto-expanding species in both counties (Romania: χ2 = 25.495, df = 4,
P < 0.001; Bulgaria: χ2 = 42.023, df = 6, P < 0.001). Most of the alien andBăncilă et al. (2022), Aquatic Invasions 17(3): 353–373, https://doi.org/10.3391/ai.2022.17.3.02

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Figure 1. Number of alien, crypto-expanding, and cryptogenic species per taxonomic group from the Black Sea marine region of
Bulgaria (BG) and Romania (RO), respectively.

Figure 2. The establishment success (following the terminology and classification of Blackburn et al. (2011), Zenetos et al. (2018,2020a): casual (cas), established (est), invasive (inv), and unknown (unk), of the alien, crypto-expanding and cryptogenic species
from the Black Sea marine region of Bulgaria (BG) and Romania (RO), respectively.

cryptogenic species were classified as established according to theestablishment success in both countries (Figure 2). Thirteen alien speciesclassified as invasive occurred in Romania whereas only eight in Bulgaria,
respectively (Figure 2). The majority of crypto-expanding species had selfsustaining established populations in Romania and on the contrary in
Bulgaria where an unknown establishment success was reported for all ofthem (Figure 2).
The results showed that the origin of alien species based on the classificationof global marine biogeographic realms proposed by Spalding et al. (2007)
did not differ significantly between Romania and Bulgaria (χ2 = 13.856,
df = 20, P = 0.838). For both countries the majority of alien species
originated from the Atlantic Ocean followed by Pacific and Indo-Pacificbiogeographic realms (Figure 3). Alien species with native ranges in the
Arctic Ocean and Australia were less represented (Figure 3). Most cryptoexpanding and cryptogenic species listed from Romania have had an
obscure origin as they are nowadays regarded as cosmopolitan while mostof the crypto-expanding and cryptogenic species listed from Bulgaria
originated from the Atlantic Ocean (Table S3).
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Figure 3. Native distribution ranges of the alien species depicted per marine biogeographic
realms following Spalding et al. (2007), from the Black Sea marine region of Bulgaria (BG) andRomania (RO), and from both countries’ (BG + RO) region, respectively.

Figure 4. The number of new reported records since 1970 at six-year time intervals (bars) and the cumulative number of species(lines) for alien, crypto-expanding, and cryptogenic species from the Black Sea marine region of Bulgaria (BG) and Romania(RO), respectively.

We found a significant difference in the number of new records reported
since 1970 among the defined six-year time intervals for Romania (χ2 =25.57, df = 14, P = 0.029) but not for Bulgaria (χ2 = 19.133, df = 14, P = 0.159).
Figure 4, that shows the introduction history of the alien, crypto-expanding,Băncilă et al. (2022), Aquatic Invasions 17(3): 353–373, https://doi.org/10.3391/ai.2022.17.3.02

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List and information on alien species in the western Black Sea region

Figure 5. The introduction pathway(s) of alien species from the Black Sea marine region of
Bulgaria (BG) and Romania (RO), and from both countries’ (BG + RO) region, respectively.
The pathway classification follows the Convention on Biological Diversity (2014): corridor(COR), escape from confinement (EC), transport-stowaway (TS), release in nature (REL), andunaided (UNA).

and cryptogenic species reported since 1970 per six-year intervals, indicatedthat: (i) the number of alien species has steadily increased over the last 50
years for both Romania and Bulgaria; (ii) there is a steep increase ofreported crypto-expanding species in the time interval 1994–2011 forRomania, and (iii) there is an important increase of reported cryptoexpanding species in the time interval 2006–2011 for Bulgaria.
The chi-square test indicated that the introduction pathway(s) of alien
species differ significantly between the two countries (χ2 = 48.093, df = 10,
P < 0.01). Transport-stowaway was the most important pathway of arrival
for species listed as alien in both countries (Figure 5). A significant numberof alien species were introduced by two pathways. For them, the Transportstowaway was the main introduction pathway and natural dispersal, i.e.,
unaided introduction, was less important (Figure 5). Concerning the certainty
of introduction pathway(s) the majority of alien species were clearly
associated to a specific pathway at the time of introduction or the most
likely pathway could be inferred. Consequently, certainty levels of “1” and“2”, respectively, were assigned to introduction pathway(s) of more than
89% of the species (Table S2).

Discussion
We propose a validated list of alien, cryptogenic and crypto-expanding in
the western Black Sea region, i.e., Bulgarian and Romanian Black Sea region.
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List and information on alien species in the western Black Sea region

The list represents the baseline information for addressing marine alien
species on a national level and a coherent and representative list for future
updating. Moreover, the list serves as a starting point towards an effective
implementation of MSFD (D2C1: trends in introduction) as well as forselecting the invasive alien species for risk assessment and inclusion on theUnion list (EU IAS Regulation). Concerning the validation of previously
reported alien species the present study revealed: (i) errors in listing ofalien species, (ii) changes in the alien status and/or establishment successof alien, cryptogenic and crypto-expanding species, and (iii) gaps in thescientific literature associated with reporting of alien species. This suggeststhat both the opinion of local experts (Crocetta et al. 2017) and filling gaps
in the knowledge of alien species are essential to define future research
priorities and focus conservation efforts.
As highlighted in previous works (Zenetos et al. 2017), the main reasonsfor excluding species from the initial list, species that failed to be classified
as alien, cryptogenic or crypto-expanding included: (i) synonymizing ofexisting taxa (i.e., Mugil soiuy Basilewsky, 1855, which is synonymous with
Liza haematocheila (Temminck & Schlegel, 1845) and for which the new
accepted name is Planiliza haematocheila (Temminck & Schlegel, 1845);
Peridinium quinquecorne T.H.Abé, 1927 which is synonymous with
Protoperidinium quinquecorne (Abé, 1927) Balech, 1974 and for which the
new accepted name is Blixaea quinquecornis (Abé) Gottschling, 2017;
Distephanus speculum var. octonarius (Ehrenberg) Jørgensen, 1899
synonym of Octactis octonaria (Ehrenberg) Hovasse, 1946; Oxyphysis
oxytoxoides Kofoid, 1926 synonym of Phalacroma oxytoxoides (Kofoid)
F.Gomez, P.Lopez-Garcia & D.Moreira, 2011; Rhizosolenia calcar-avis
Schultze, 1858 synonym of Pseudosolenia calcar-avis (Schultze)
B.G.Sundström, 1986; Glenodinium gymnodinium Penard, 1891 synonymof Naiadinium polonicum (Woloszynska) Carty, 2014; Fogedia finmarchica(Cleve & Grunow) A.Witkowski, D.Metzeltin & Lange-Bertalot, 1997 synonymof Navicula finmarchica (Cleve & Grunow) Cleve, 1895), (ii) erroneous
reports (i.e., Acrochaetium leptonema (Rosenvinge) Børgesen, 1915, Kylinia
rosulata Rosenvinge, 1909, Asterionellopsis glacialis (Castracane) Round,
1990, Pteria hirundo (Linnaeus, 1758), Bacteriastrum hyalinum Lauder, 1864,
Lepas sp., Neptunea arthritica (Valenciennes, 1858), which never occurredin any of the Romanian or Bulgarian Black Sea regions), (iii) species
misidentification (i.e., O. brevicornis, a misidentification of O. davisae;
Alexandrium affine (H. Inoue & Y. Fukuyo) Balech, 1995, for which
description does not correspond to that of individuals collected from its
native range; Ruditapes philippinarum (A. Adams & Reeve, 1850), most likely
a misidentification of Polititapes aureus (Gmelin, 1791), (iv) misclassificationof native species as alien (i.e., Blackfordia virginica Mayer, 1910, Prorocentrum
cordatum (Ostenfeld) J.D. Dodge, 1976, V. dichotoma f. marina, Pseudosolenia
calcar-avis (Schultze) B.G. Sundström, 1986, Ulva lactuca Linnaeus, 1753,
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Acrochaetium mahumetanum G. Hamel, 1927, and Prionace glauca(Linnaeus, 1758) – all were previously reported as alien but currently are
regarded as native species), and (v) inclusion of freshwater species inmarine species lists (i.e., Lepomis gibbosus (Linnaeus, 1758), Pseudorasbora
parva (Temminck & Schlegel, 1846), U. krameri, Lithognathus mormyrus(Linnaeus, 1758), Naiadinium polonicum (Woloszynska) Carty, 2014, Urnatellagracilis Leidy, 1851 and Podonevadne trigona ovum (Zernov, 1901)). Several
species were excluded from the list because they involved extinct species(i.e., V. spengleri), natural range expansion species (i.e., B. vitrea, Sphyrna
zygaena (Linnaeus, 1758) and Chelon labrosus (Risso, 1827)) and species
not validated by local experts (i.e., Erythrocladia irregularis Rosenvinge,
1909, Hildenbrandia crouaniorum J. Agardh, 1851, and Hillea fusiformis(J. Schiller) J. Schiller, 1925, which proved to be AquaNIS miss-reports).
Also, data deficient species could not be assigned to any of the previous
categories due to lack of data, i.e., unsubstantiated records with nodescription or photos of species and taxa of unresolved taxonomic status.
The refined list of alien species recorded in Romanian Black Sea region
proposed here comprised 37 species. This number is lower in comparison
with the number of species (i.e., 49 species) listed in the last inventory of
Skolka and Preda (2010). Since then, five new species – Hemigrapsus
sanguineus (De Haan, 1835 [in De Haan, 1833–1850]), Eurypanopeus
depressus (Smith, 1869), O. davisae, Amphiglena mediterranea (Leydig, 1851),
Alitta succinea (Leuckart, 1847) and Laonome xeprovala Bick & Bastrop, inBick et al., 2018 – have entered the list (Micu et al. 2010a, b; Zinevici et al.
2011; Timofte and Tabarcea 2012; Petrescu et al. 2016; Surugiu and Capa
2020; Teacă et al. 2021), whereas many have been excluded following the
aforementioned criteria. We refer to species that changed their status fromalien to cryptogenic (i.e., Teredo navalis Linnaeus, 1758, Amphibalanus
improvisus (Darwin, 1854), Einhornia crustulenta (Pallas, 1766), Thalassiothrix
mediterranea var. pacifica Cupp, 1943) or to crypto-expanding (i.e., Pontella
mediterranea (Claus, 1863), Mecynocera clausi Thompson I. C., 1888,
Neocalanus gracilis (Dana, 1852), Euterpina acutifrons (Dana, 1847), Triconia
dentipes (Giesbrecht, 1891), T. minuta (Giesbrecht, 1893), Oncaea mediterranea(Claus, 1863), Calocalanus tenuis Farran, 1926, C. pavoninus Farran, 1936,
Agetus flaccus (Giesbrecht, 1891), A. typicus Krøyer, 1849, Corycaeus clausi
Dahl F., 1894, Urocorycaeus furcifer (Claus, 1863), Microsetella rosea(Dana, 1847), Ctenocalanus vanus Giesbrecht, 1888, C. pavo (Dana, 1852),
C. plumulosus (Claus, 1863), Clausocalanus arcuicornis (Dana, 1849),
Paracalanus nanus Sars G.O., 1925, P. aculeatus Giesbrecht, 1888,
Mesocalanus tenuicornis (Dana, 1849), and Neocalanus gracilis (Dana, 1852)).
Surprisingly, there are no studies that provide an inventory of all marine
alien species for the Bulgarian Black Sea region. The refined list of 26 alien
species we came up with here, is the first comprehensive list (i.e., including
all taxonomic groups) of marine alien species for this region. SeparateBăncilă et al. (2022), Aquatic Invasions 17(3): 353–373, https://doi.org/10.3391/ai.2022.17.3.02

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List and information on alien species in the western Black Sea region

taxonomic group inventories for Bulgarian Black Sea region have been
published, i.e., inventories of invertebrate marine species (Hubenov 2014,2015) and fish species (Yankova 2016). Hubenov (2014) reported a total of
31 alien invertebrate marine species and Yankova (2016) reported six alienfish species. Several species of invertebrates and fish which have beenclassified as alien by Hubenov (2014) and Yankova (2016), are currently
regarded as cryptogenic (i.e., A. improvisus, Hesionides arenaria Friedrich,
1937, Streblospio shrubsolii (Buchanan, 1890), Streptosyllis varians Webster& Benedict, 1887, T. navalis, Pomatoschistus marmoratus (Risso, 1810) andP. bathi Miller, 1982) or crypto-expanding (i.e., T. minuta, Sardinella aurita
Valenciennes, 1847, Sphyraena sphyraena (Linnaeus, 1758)). However,P. marmoratus, which was mentioned from the Black Sea as P. microps
leopardinus (Nordmann, 1840) (Bănărescu 1964), is a subspecies of P. microps(Krøyer, 1838). Bănărescu (1964) reported the subspecies as native to the BlackSea and mentioned it as naturally occurring at the Romanian Black Sea coast.
We found that most of the alien species were either established orinvasive in the Romanian Black Sea region. Since 2010 (Skolka and Preda2010), there was a substantial change compared to the present days in theestablishment success of alien species from casual to established (i.e.,
Calyptospadix cerulea Clarke, 1882, Crassostrea virginica (Gmelin, 1791),
Magallana gigas (Thunberg, 1793), Sphaeroma walkeri Stebbing, 1905,
Palaemon macrodactylus Rathbun, 1902, Callinectes sapidus Rathbun, 1896
and Styela clava Herdman, 1881) and from established to invasive (i.e.,
M. leidyi, Beroe ovata Bruguière, 1789, Polydora cornuta Bosc, 1802,
Corambe obscura (A. E. Verrill, 1870), Planiliza haematocheila (Temminck& Schlegel, 1845), Rhithropanopaeus harrisii (Gould, 1841)). We also
report four new invasive alien species in Black Sea region of Romania (i.e.,
Dipolydora quadrilobata (Jacobi, 1883), Diadumene lineata (Verrill, 1869),
Streblospio gynobranchiata Rice & Levin, 1998, and L. xeprovala), andchanges in the establishment success of two cryptogenic species, i.e.,
Einhornia crustulenta (Pallas, 1766) from casual (Skolka and Preda 2010)
to established. The observed increase in the success of establishment andinvasion of alien and of species that might be alien, is most likely the resultof the increase in habitat degradation (Spear et al. 2013) and international
trade (Westphal et al. 2008). Also, since the second half of the 20th century
marine invasions are being amplified by the increase in use ofnon‐biodegradable plastics. Billions of tons of plastics are deposed at theland‐sea interface creating rafts that last for decades and permit more
species to be transported as passengers far longer and further (Carlton et al.
2017). After World War II global shipping expanded dramatically andmany thousands of species are transported around the world as stowaways
in ballast water (Carlton and Geller 1993) and contaminants of transported
goods to regions that are increasingly favorable to new invasions due toclimate warming.
Băncilă et al. (2022), Aquatic Invasions 17(3): 353–373, https://doi.org/10.3391/ai.2022.17.3.02

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Concerning the Bulgarian Black Sea region, although Hubenov (2014,2015) reported nine alien invasive species of invertebrates (i.e., M. leidyi,
B. ovata, Ficopomatus enigmaticus (Fauvel, 1923), P. cornuta, D. quadrilobata,A. improvisus, Rapana venosa (Valenciennes, 1846), Anadara kagoshimensis(Tokunaga, 1906), and Mya arenaria Linnaeus, 1758), and Yankova (2016)
five alien invasive species of fish (i.e., Sparus aurata Linnaeus, 1758, S. aurita,
P. marmoratus, Sarpa salpa (Linnaeus, 1758), and P. bathi), in our study
local experts classified eight invertebrate species (i.e., M. leidyi, B. ovata,F. enigmaticus, P. cornuta, D. quadrilobata, R. venosa, A. kagoshimensis
and M. arenaria) as alien invasive species, while all alien fish species wereclassified either as cryptogenic (i.e., P. marmoratus and P. bathi) or cryptoexpanding (S. aurata, S. aurita, and S. salpa), having established populations
or an unknown establishment success. Amphibalanus improvisus, reported
by Hubenov (2014, 2015) as an alien invasive species in the Black Sea
region of Bulgaria, was reassigned by the local experts in this study as anestablished cryptogenic species.
We found that the vast majority of alien, cryptogenic and cryptoexpanding species have their native distribution in the Atlantic Ocean anda significant proportion in the Pacific and Indo-Pacific regions both for
Romanian and Bulgarian Black Sea marine regions. The result is in linewith other studies which have addressed the native distribution ofEuropean alien species. The Atlantic, Pacific and Indo-Pacific regions
represented important realms of alien species recorded in the main
European Seas (Tsiamis et al. 2018). On the other hand, the connection of
the Black Sea with the Mediterranean Sea, where many alien Indo-Pacificspecies have entered the Mediterranean Sea via Suez Canal (Zenetos andGalanidi 2020), is worth mentioning. Very few alien, cryptogenic andcrypto-expanding species were native to the Arctic or Sea of Azov, most
likely due to climatic differences.
Trends in the introduction of alien species clearly showed that there wasa steady increase in the number of introduced alien species in marine
regions of both Romania and Bulgaria over the last 50 years. Previous
studies evaluating the dynamics of introduction of alien species to Europe
indicated that the number of newly reported alien species over the past
century is generally increasing in the marine environment (Richardson andPyšek 2008). This increase partly reflects new introductions and is partly
due to the progress in conducting inventories of alien species for manytaxonomic groups. There was also strong evidence that the number ofcrypto-expanding and cryptogenic species recorded in the recent decades
in the marine regions of Romania and Bulgaria, respectively, sharply
increased until 2011. In the time interval 2012–2017 the number of
introduced species clearly decreased with only one report in the last four
years, i.e., L. xeprovala from the Romanian marine region (Teacă et al.
2021). The most recent record of a non-native species in the Black Sea wasBăncilă et al. (2022), Aquatic Invasions 17(3): 353–373, https://doi.org/10.3391/ai.2022.17.3.02

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the amphipod Melita nitida S.I. Smith in Verrill, 1873, found in 2019 along
the Black Sea coast of Georgia (Copilaș-Ciocianu et al. 2020). This suggests
that, although overall the amount of data increased, the knowledge on the
distribution and the natural dispersal mechanisms is far from being
complete, which leads to confusion regarding the status of many species.
However, we cannot rule out that the reason of a decreasing trend in the
introduction of marine species over the past few years might be thereduced sampling effort for investigating the communities of marine
species in the Black Sea region. For example, R. venosa, ranked as one of
the 100 worst alien species in Europe, and C. sapidus, which is among the
100 worst invasive species in the Mediterranean, are considered forinclusion on the Union list under EU Regulation on invasive alien species.
Recent studies have shown that C. sapidus is spreading on the southerncoast of the Black Sea (Ceylan 2020). Moreover, observations from citizen
scientists of C. sapidus are verified by experts and is promoted as
legitimate. Yet, there are few recent publications on R. venosa (Janssen etal. 2014) and C. sapidus (Uzunova 2016) for the Bulgarian Black Sea andno recent publications for Romania. Publications stemming frominventory and monitoring activities in hot spots of invasive alien species(i.e., ports, lagoons and aquaculture farms) identified per regional sea and
MSFD area are not available in both countries. Moreover, the lack ofstudies documenting the world distribution and vectors for alien species isemphasized by the fact that the true status of many species (i.e., classified
as crypto-expanding and cryptogenic) is still unclear. This adds to thenecessity of taxonomic verification which is dependent on the availabilityof taxonomic expertise. Thus, our study highlights the need for further
studies, including molecular studies, that are able to elucidate the true
status of introduced species in the western Black Sea region, as well as themechanisms of introduction (pathways) and the actual spread of alien
species. Without appropriate, harmonized and integrated data on alien
species, future efforts toward implementation of MSFD instruments may
render ineffective. Nonetheless, the data collected so far allows us to
identify key vectors presumably responsible for the introduction of alien
species in the western Black Sea region.

Conclusions
We present an updated and validated list of alien species for the RomanianBlack Sea region and a first comprehensive list of alien species for the
Bulgarian Black Sea region. This information is essential for future risk
assessment and implementation of biodiversity conservation and management
policies in the western part of Black Sea. The data provided here areparticularly useful for the development of priority lists of invasive alien
species present in marine waters of Romania and Bulgaria. The list supplies
key information to identify species to be included on the Bulgarian andBăncilă et al. (2022), Aquatic Invasions 17(3): 353–373, https://doi.org/10.3391/ai.2022.17.3.02

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List and information on alien species in the western Black Sea region

Romanian national concern lists or/and on the Union list. Also, the resultsof this study open new research directions including future focus on poorly
studied alien species and species reported based on the information
available in AquaNIS with no recent scientifically documented record.
Moreover, our results reveal some disparity in the number of alien species,
species status and establishment success between the Romanian andBulgarian Black Sea regions, which might result from uneven monitoringof alien species in the two countries. This emphasises the need for study ofthe overall distribution of alien species in the Black Sea but also could be
useful information to direct the management efforts of alien species wherepriority is needed and tailor them per Black Sea sector. In conclusion, thisstudy provides supporting information for implementing measures totackle the introduction of alien species in the western region of the BlackSea towards an early warning, prevention and control of invasive alien
species and application of the MSFD directive in the Black Sea, a uniquefragile ecosystem.

Acknowledgements
We thank to Dr. Petr Pyšek and the two anonymous reviewers for their comments on the earlyversion of the manuscript which considerably helped to improve the manuscript. We are also
grateful to Șerban M Sârbu, Adjunct Faculty, California State University Chico for correctionof grammatical errors and improvement of diction. This article is based upon work from COST
Action CA17122, supported by COST (European Cooperation in Science and Technology;
www.cost.eu).

Funding declaration
This work was financially supported by a COST Short Term Scientific Mission, STSM
Fellowship, COST Action (Alien-CSI) CA 17122 “Increasing understanding of alien species
through citizen science” at the Institute of Marine Biological Resources and Inland Waters,
Hellenic Centre for Marine Research (Attica, Greece), granted to RIB.

Authors’ contribution
RIB and AZ conceived the idea of the study. AZ, MS, PI, VS, KS, and VT contributed to datacollecting. RIB and AZ wrote the manuscript with input from VS.

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Supplementary material
The following supplementary material is available for this article:
Table S1. Species to be excluded.
Table S2. List of alien species.
Table S3. List of cryptogenic, crypto-expanding, and data deficient species.
Table S4. References for Tables S1–S3.
This material is available as part of online article from:http://www.reabic.net/aquaticinvasions/2022/Supplements/AI_2022_Bancila_etal_SupplementaryMaterial.xlsx

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