Non-indigenous species likely introduced by shipping into the Adriatic Sea
Introduction
Invasion of non-indigenous species (NIS) become the main generator of biodiversity loss worldwide [12], [53], and one of the major threats to biodiversity in Europe [27], [52]. The intentional or unintentional introduction/translocation of species beyond its natural habitats can result in severe negative impact on nature, human health, and the economy [53], [80].
The Mediterranean Sea represents one of the hotspots of biodiversity [16] and NIS introduction may negatively affect ecosystem structure and function [76]. An increased trend of invasion of NIS in aquatic environments, both freshwater and marine, has been noted from mid-20th century [36], [49], [72], [91]. Similarly, an increase in the number of NIS records has been found in the Mediterranean Sea in the period between 1970 and 2010 [33], [96]. The annual rate of NIS records depends on the habitat and intensity of research efforts, particularly in the Mediterranean Sea where different basins vary greatly in the accessibility to vectors and research activities. Presently, 821 NIS findings have been reported from the Mediterranean Sea, with 613 already well established, and with 208 casual records [96].
According to the EU Regulation on the Prevention and Management of the Introduction and Spread of Invasive Alien Species [25], [26] and the Marine Strategy Framework Directive (MSFD), [24], each member state should monitor and evaluate the pathways of introduction of NIS in order to identify the most common pathway i.e. priority pathway [25], [33]. Presently, several different pathways of introduction were identified for the Mediterranean Sea: (1) aquaculture; (2) shipping; (3) corridors; (4) aquarium trade; and (5) other (live food, bait trade, floating objects, etc) [49], [99]. Shipping is the most likely pathway of introduction for the majority of NIS [28], [3], [34], [49], [99] by which more than half (51.9%) of the marine non-indigenous species were introduced in European Seas [49] and 40% in most Mediterranean countries ([66]. According to projections, global maritime traffic tends to increase by 240–1209% by 2050, which is the reason why shipping growth can have a far greater impact on marine invasions than climate-driven environmental changes. Thus, emerging global shipping networks could increase the risk of global invasion 3–20 times ([77]). Indeed, increasing numbers of touristic recreational boats, particularly on the eastern coast of the Adriatic Sea, have been noted as a consequence of strengthening tourism in the region [51], [64]. Furthermore, the Adriatic Sea possesses many marinas and shores that are major tourist destinations, and it has become an inevitable anchorage for cruise ships [85], certainly increasing the possibility of NIS introductions. Also, the North Adriatic coastal lagoons are under extreme risk of NIS introduction due to its environmental instability, low number of species, aquaculture activities, and the presence of not saturated benthic communities [62], [63], especially the Gulf of Venice, which is the hot spot of NIS introduction in the Adriatic Sea ([59], [68], [99]). Two vectors of NIS introduction by shipping activities were identified: (1) ballast water (BW), and (2) hull fouling (biofouling), (BHF), of which BW became the most important vector in last 20 years [40], [49]. An important step towards managing NIS via shipping was made by Ballast Water Management Convention (BWC) entered into force in September 2017 [44]. However, BWC does not cover any aspect of NIS introduction by biofouling on recreational boats, which are the primary vector of introduction in harbours [28]. Furthermore, MSFD seeks to achieve Good Environmental Status (GES) of EU marine waters and to protect the resource on which marine-related economic and social activities depend. One of the qualitative descriptors for determining GES focuses on the introduction of NIS at levels that do not adversely affect the ecosystems [24]. To minimize the problem, practices to control and manage the introductions of NIS by maritime traffic, may be implemented [10], and regular monitoring of NIS could be established.
Many recently published papers provide information on the NIS introduction in the Mediterranean Sea [8], [29], [33], [47], [66], [68], [81], [96], [98], [99], but a limited number of papers were focused on the Adriatic Sea [57], [69], [81]. Most of papers related to NIS introduction into the Adriatic Sea refer to new records and individual introductions [37], [62] or invasions at a particular site [56], not being focused on introduction pathways. Recently, several papers focused on NIS introduction by shipping into the Adriatic Sea were published but only particular groups of organisms were covered [7], [70]. Also, most of the papers are focused on the Italian coastal area of the Adriatic Sea [81], and yet none provides a comprehensive analysis of NIS likely introduced by shipping into the Adriatic Sea, covering the Adriatic region entirely, including its eastern part.
Data suggests that a total of 190 NIS by all identified pathways were introduced into the Adriatic Sea [99]. However, the most recent data for the Adriatic Sea after the exclusion of questionable and cryptogenic species, suggest that 143 NIS were identified in the Adriatic, but this number covers inventory of alien species located only along the Italian coast [81]. Furthermore, Tsiamis et al. [92] suggest 155 NIS species identified in the Adriatic in total. Because of continuous changes to checklists by updates on species nomenclature, likely date and pathways of introduction, as well as origin and establishment success of individual species, every list could be named a ‘provisional list’ [56], [58], [96].
Four large cargo ports are situated in the north-east part of the Adriatic Sea (Trieste, Venice, Koper, and Rijeka) with 100 million tonnes of cargo handled every year [65], together with an increasing number of touristic recreational boats and cruise ships along the eastern Adriatic, increase the possibility of NIS transport and introductions. Although published information is substantial, the information on new introductions is accelerating as research intensifies. Therefore, today the number of introduced NIS into the Adriatic Sea likely by shipping could be much higher than previously identified, and expected intensification of maritime traffic around the Mediterranean [77] could increase its number in the future. Hence it is essential to build the basic presence of NIS to fulfill existing gaps of knowledge about the introduction of NIS in the Adriatic Sea due to the possible growth of maritime activity which has become one of the major threat to native biodiversity.
Accordingly, the focus of this paper is to identify (1) the NIS likely introduced by shipping (Transport-Stowaway) as a pathway covering the entire area of the Adriatic, (2) the NIS introduced likely by Ship/boat BW and Ship/boat BHF as vectors, and (3) first introduction, origin, establishment success and invasive characteristics of NIS introduced by shipping into the Adriatic Sea. The year of first record in the Mediterranean Sea are also provided. The outcomes of this study are expected to provide useful information on NIS for policy makers to prioritise decisions of appropriate management and conservation measures, and to secure biodiversity protection of the Adriatic Sea in future strategies focusing on maritime traffic.
Section snippets
Study area
The Adriatic Sea is a semi-enclosed sea [20], 800 km long and 200 km wide [61], with an average depth of 259.5 m and the maximum depth of 1233 m [4]. The northern part is shallow and rarely exceeds a depth of 100 m [4], with deeper central and southern parts. In the southern Adriatic, Otranto Sill forms the boundary to the Ionian Sea [5]. The western Adriatic shore is relatively unindented, while the eastern shore is the most indented Mediterranean coastline [20]. The western Italian coast of
Results
A total of 127 NIS introduced into the Adriatic Sea by shipping as a pathway were identified (Appendix 1). More than 50% of all listed species belong to three phyla: Arthropoda (29 species), Rhodophyta (21 species) and Annelida (18 species) (Appendix 1; Fig. 1).
The most numerous first introduction records of NIS for the whole Adriatic were found for Italian coastline and represent 73% (93 NIS) of listed species. Within the Croatian territorial sea, 23% (29 NIS) species were found, while the
Discussion
Compared with the other EU marine environments, the Adriatic Sea is recognized as one of the most NIS-impacted seas in the region [99]. A list of NIS records and number of recorded species (EST, CAS) varies from year to year, and the pathway of NIS introduction is usually difficult to identify [34].
In this research, 94 EST and 33 CAS species were identified as NIS introduced into the Adriatic Sea likely by shipping, which represents more than 65% of the total NIS introduced since the last
Conclusion
The presented data show that shipping has become the major pathway in the Adriatic Sea for NIS introduction of most groups of marine organisms, except fishes. Accordingly, an increased number of sailing and motorized recreational boats could be a new significant vector of NIS introduction, and could be prioritized according to area specificity by decision makers and environmental managers. Difficulties in control, lack of solutions for biofouling suppression, and lack of regulations for
Authors information
The authors declare no competing interests, financial or otherwise. Correspondence should be addressed to M. Piria ([email protected]).
Authors contributions
All authors contributed extensively to the work presented in this paper. In particular, M. Slišković and M. Piria designed the study, collected the data and prepared the manuscript. K. Pavičić Ivelja, V. Nerlović, G. Jelić Mrčelić collected the data, analyzed and interpreted the results. A. Gavrilović finalized the article.
Acknowledgements
We express our thanks to dr. Jurica Jug-Dujaković and dr. Steven Van Gorder for their constructive comments during preparation of the manuscript. This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
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2022, Marine Pollution BulletinCitation Excerpt :During last decades, the diffusion of NIS worldwide showed an increase in its magnitude due to the high level of globalization in maritime trading (Seebens et al., 2017). The arrival of NIS into the ports is strictly related to national/international commercial maritime traffic and recreational boating (Carlton and Geller, 1993; Seebens et al., 2013; Slišković et al., 2021). Consequently, the arrival of these species into the marinas is possibly due to the spreading from touristic harbours and other marinas through recreational boating (Clarke Murray et al., 2011; Ferrario et al., 2017; Ulman et al., 2019b).
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