Non-indigenous species likely introduced by shipping into the Adriatic Sea

Highlights

• 127 NIS were identified as likely introduced by shipping into the Adriatic Sea.

• Half of listed NIS were probably introduced by boat hull fouling.

• Majority of NIS were classified as established.

• Increasing number of touristic vessels may intensify new introductions.

Abstract

By the intensification of maritime traffic, shipping could become one of the most likely pathways of introduction of non-indigenous species (NIS) in the Adriatic Sea. In this paper we provided an updated list of NIS introduced into Adriatic Sea by shipping as pathway, the most likely vectors of introduction, country of first detection, year, origin, establishing success and invasive characteristics. In total, 127 NIS were identified as the most probably introduced by maritime shipping into the Adriatic Sea. Rhodophyta, Arthropoda and Annelida represents almost 50% of all the listed species. The highest number of NIS introduced likely by shipping has been identified for period from 2001 to 2010 year. More than 73% of NIS listed for the first time in the Adriatic Sea were recorded in Italy. Half of listed NIS (50%) were probably introduced by external ship’s vector i.e. boat hull fouling (BHF). Majority of these species were classified as established. Screening of the potential risk of NIS being invasive in the Mediterranean and Adriatic Sea has not been done systematically, and for the most of NIS has never been performed. Increased number of sailing, motor recreational boats and cruise ships, lack on solutions for biofouling suppression and lack on regulations for anchoring may intensify NIS introductions by shipping as the most probable pathway into Adriatic Sea. That could become serious threat for native biodiversity and natural heritage, and it needs to be taken seriously by all relevant organisations and stakeholders.

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.