ANNALES Ser. hist. nat. 11 2001 2 (25) review article UDC 574.5(262.3-17] received: 15. 10. 2001 A SURVEY OF THE INTRODUCED NON-INDIGENOUS SPECIES IN THE NORTHERN ADRIATIC SEA Martin,i ORLANDO BONACA National Institute- of Biology, Marine Biology Station, SS-6330 Piran, FornaCe 41 ABSTRACT A synthesis of non-indigenous species being introduced to the northern Adriatic Sea, based on literature records and unpublished information, is given. Thirty-five introduced species were recorded, twenty-six animals and nine algae. The majority of them have been introduced with vessels, for aquaculture purposes (also as accompanying species) or through the Suez Canal (the so-called Lessepsian migrants). The fate of these species is unpredictable not only in the northern Adriatic, but in the entire Mediterranean Sea. Key words: non-indigenous species, introduction, northern Adriatic Sea RESOCONTO DELLE INTRODUZIONI D! SPECIE NON-INDIGENE NELL'ADRIATICO SETTENTRIONALE SINUS! L'articolo riporta un resoconto delle introduztoni di specie marine nnn-indigene ned'Adriático settentrionale, ba-sato su dad di letieratura ed information! non ancora pubblicate. In 'ótale e stala regístrala la presenza di tren-tacinque specie alloctone, ventisei deüe quali appartenenti al regno anímale e nove a quello vegetale. La maggio-ranza di esse é stata introdotta con le navi, importa ta per la maricoltura (con rispettive specie accompagna tnci) o attraverso if Canale di Suez (migranti Lessepsiatv). La sorte di tali specie appare imprevedibile non solo nel-I'Adriático settentrionale, ma nell'intero hacino Mediterráneo. Parole chiave: specie non-indigene, introduzioni, Adriático settentrionale 149 ANNALES • Ser. hist. nat. • 11 2001 ■ 2 (25) Martina ORLANDO BON'ACA: A SURVtY O* THC INTROOUCCD NON-INDIGENOUS SPECIES .... 1 49-1 SB INTRODUCTION The introduction of species to habitats outside their native ranges is a growing problem due to the unexpected impacts these species might cause on indigenous species and ecosystems (Nolan, 1994; Gollasch & Leppakoski, 1999). Nowadays, it is quite impossible to predict how a species will behave when it is introduced into a new environment. Because of this unpredictability every effort should be made to prevent or at least to monitor the introduction of species from an ecosystem into another (Verlaque, 2001). Marine non-indigenous species (also called introduced, non-native, alien, or exotic organisms) are mostly transported intentionally for aquaculture purposes or unintentionally with marine traffic (Zibrowius.. 1994; Gollasch & Leppakoski, 1999). Ships provide habitats for a large variety of organisms due to (heir transport of ballast water, sediments in ballast tanks and hull fouling (Gollasch & Leppakoski, 1999). Compared to the substantial body of knowledge gathered on terrestrial species introductions, data on the dynamics of marine species introduction remain very scarce. Relatively comprehensive inventories of marine flora and fauna are too recent for us to be able to identify in them the species that were probably introduced, without the risk of error being unacceptably high. Often, the authors of inventories have not specified that certain mentioned .species were probably introduced, mostly because they feel that this assumption is too hypothetical (Ribera & Boudoirresque, 1995). In the northern Adriatic Sea, only a minor research about the presence of non-native species has been carried out (De Mitt & Vio, 1998), but scientists have recorded cases of introductions of non-indigenous species that could badly affect local ecosystems. However, some information about non-indigenous species in this area is known from the reports by Lipej (2000), l.ipej & Makovec (2000), Lipej eta!. (2000) and Orlando (2001). David (1999) provided a review of the existing regulations for the accidental introduction of species with ballast waters. The aim of this paper is to compile the checklist of non-indigenous marine animals and algae found in the northern Adriatic Sea. Data were collected from different sources such as bibliographical references and scientific citations, information available at specific web sites, and information obtained by other researchers and naturalists. MODALITY OF INTRODUCTION OF SPECIES According to Boalch (1994), introductions of non-indigenous species can be divided into natural introductions (which may be temporary or permanent), accidental introductions by man (brought in with other or- ganisms, by ships or other vectors or brought in for research or commerce and subsequently escaping), or purposeful introductions. Natural introduction (like in the Mediterranean the natural invasion of species through the Straits of Gibraltar) are frequently the result of local changes in environmental conditions, so that a species normally occurring outside the considered area can extend its range and move into it These types of introductions do no? appear to be harmful. Accidental introductions are much more numerous- The most ancient vector of species introduction is certainly the transportation on the ships' hulls of fixed (fouling) or non-fixed (clinging) Species (Ribera & Sou-douresque, 1995). Fouling concerns small-sized species and large species whose life history includes a microscopic stage. Since 1972, antifoultng paints of ships have generally contained the highly toxic tributyltin (TEST) (Gollasch & Leppakoski.. 1999). This substance has considerably reduced the number of fouling organisms, but in some areas, like harbors or shipyards, the accumulation of the TBT prevents the reproduction of several gastropod species and also some algae seem to be affected (Gollasch & Leppakoski, 1999). Therefore, in the beginning of the 1990s the use of TBT was banned for boats smaller than 25 m (Gollasch & Leppakoski, 1999). Carlton & Celler (1993) note that ballast water is the least selective means of transportation of species from the ecological and taxonomic points of view, and it is a vector that has no equivalent on land- The survival time in ballast water for some species may exceed 18 days (Salt, 1992), so thai many of these organisms are still alive after their intercontinental voyage at the time of deba Hasting. Many scientists who are using marine non-native species fail to take the elementary precautions required to prevent the escape of these organisms from their cultures, e.g. some laboratories dispose through their own direct outfalls sites for seawater. The survival capacity of such species in fresh water is also poorly known (Ribera & Boudouresque, 1995). Some economically important alien species have been introduced intentionally for aquaculture purposes, with consequent accidental introduction of accompanying species (Zibrowius, 1994; Ribera & Boudour-esque, 1995; Gollasch & Leppakoski, 1999). With a few exceptions, the importation, sale and possession of marine species are not subject to any specific regulations. Some companies offer in their catalogues also the invasive marine aigae Caulerpa taxifolia and Sargassum muticum (Ribera & Boudouresque, 1995). The migration of the Red Sea species through the Suez Canal has added by far the greatest number of newcomers in the Mediterranean Sea. With the inauguration of the Suez Canal in 1869, a remarkable fauna! and floral movement started. Hundreds of species are still traversing the canal arid settling in the Mediterra- 150 ANNALES Ser. hist. nai. 11- 2001 • 2 (25) Manilla ORLANDO BOM*CA: A SUHVtYOi THE INTRODUCED NON-IN'DtC.EN'OUS SPEClfS , 149-158 jlean in a process called "Lessepsian migration1, after Ferdinand Marie de Lesseps, the French engineer who h«iIt the canai (Caiil, 1994} There are four successive phases in the introduction of a species (Ribera & Boudouresque, 1995), first of all the arrival of a few specimens of an exotic species that does not automatically imply its naturalization. During the settlement phase, the species constitute populations of individuals born in situ. This phase may results in a naturalization of the species. Once naturalized, the introduced species starts the expansion phase, trying Vo occupy the whole biotope and the whole of the geographical range to which it may have access. The persistence phase, the last one, may takes two forms: the decline followed by stabilisation at a lower level than the maximum attained during the expansion phase, or a plateau close to the maximum attained. A species is considered introduced when it has satisfied many criteria (Ribera & Boudouresque, 1995). The most important are that the species is new in the area in question and that there is a geographical discontinuity between its new station and the species' known range (Ribera & Boudouresque, 1995). INTRODUCED FAUNA According to the available data, twenty-six non-indigenous animal species are known to occur in the northern Adriatic Sea (Tab. 1). The increase of marine traffic between the Mediterranean Sea and the Far East that has followed the opening of the Suez Canal, and the import of Indo-Pacific Mollusea for aqitaculture purposes, have facilitated the diffusion in the northern Adriatic Sea of twelve exotic species (De Min & Vio, 1998). According to De Min & Vio (19935, the chemical-physical conditions such as those of some subtropical or tropical estuary areas have promoted the colonization of seven non-native species (Rapana venosa (Fig. 1), Bursatella leachii, Scapbarca inaequivalvis, Musculista senhousia, Xenostrobus secures. Tapes philippinaium, Crassosirea gigas} and of five occasional, too (Strombus decorus, Brachydontes pharaonis, Perna picta, Pinctada radiata, Saccostrea commercial is (the reproduction of this species in the Venice Lagoon has failed)). A tropical species of Nudibrarschia (Gastropoda) Halgerda sp. has been found at the southern tip of Cres island (Quarnero archipelago) at the end of July 1986, which is also the first record of any Halgerda species in the Mediterranean (Turk, 2000). The author supposes that the most probable vector of introduction for this species is ballast water. There are also some records about the presence of exotic. Decapoda (Crustacea) in the northern Adriatic Sea (CIESM, 2000): Caltinectes danae, Callinectes sapi-dus, Dyspanopeus sayi and Rhithropanopeus barrisii. Fig. 1/5/. T; Rapana venosa. (Photo/Loto: T. Makovec) In 1987, the Copepoda (Crustacea) Acart/a tonsa was recorded for the first time in the northern Adriatic in the Lagoon of Scardovari (Occhipinti, 2000). Since then it has supplanted the native congeneric Acartia margalefi iri the Venice Lagoon and in the Po River Delta (Occhipinti, 2000). The circumtropical barnacle lialanus trigonus (Crustacea) was probably introduced as a fouling organism, and was first recorded in the Adriatic Sea near Trieste (Relini, 1968). In Croatian coastal waters it has been found near Rovinj and Pula (Igic, 1982) and in the Ri-jeka Bay (Zavodrtik, 1998; Zavodnik & KovaCic, 2000). In the coastal wetlands of the northern Adriatic the fish Cambusia atfinis has been found, introduced in relation to the problems with mosquitoes (Leiner et al., 1995, Markets, 1999). Because of their aggressive behaviour, tnosquitofish may negatively affect populations of small native fish through prédation and competition (Nico& Fuller, 2000). Fig. 2/SI. 2: Ticopomatus enigmaticus. (Photo/Foto: T. Makovec) 151 ANNALES • Ser. hist. nat. 11 -2001 -2 (25) Martina ORLANDO 80NACA- A SURVEY OF THE INTRODUCED NON-INDIGENOUS SPECIES ..... MS-15H in the Sečovlje Salina Landscape Pati", the Poly-chaeta Ficopomatus enigmaticus (Fig. 2) (Avčin, 1984) was recorded. This species originates from the Southern Hemisphere and it has probably been introduced on ships' hulls and commercial mollusc shells (Thorp, 2000). In 1995, the Siphonophora (Hydrozoa) Muggiaea atlantica, a representative of the Atlantic fauna, was found for the first time in the Adriatic Sea off Dubrovnik (Gamu)in & KrSinic, 2000). The species arrived to the northern Adriatic in 199G, reached a high density in July 1997, followed by its mass extinction a month later (Gamulin & Kriinic, 2000). Other introduced species in the northern Adriatic Sea are (Cognetii, 1994; Occhipinti Ambtogi, 1994); the Arrt-phipoda (Crustacea) Echinogammarus pungentoides, the isopoda (Crustacea) Paraceneis sculpta. the Bryozoa Tri-cellaria inopinata, and the Gastropoda Littorina saxatilis. The data presented in the paper of Arbulla et al. (2000) was not taken in consideration, because there were a lot of uncertainties regarding the non-native species. Tab. 1: Nort'indigenous fauna in (be northern Adriatic Sea. Tab. 1: Tujerodna favna v severnem Jadranu. INTRODUCED FLORA Nine species of introduced rriacrophytes are known from the northern Adriatic Sea (Tab. 2). Nowadays, the most notorious introduced alga in the whoie Mediterranean Sea is the tropical alga Cauierpa taxifolia (rig. 3), which has been displayed over the last fifteen years in tropical aquaria at tile Oceanographic Museum in Monaco, its accidental introduction into the natural environment dates from 1984 (Meinesz & l lesse, 1991). The first record of the alga in the Adriatic Sea was in Start Grad Say (Hvar Island, Croatia) in the summer of 1994 (Zuljevic & Antolic:, 1998). Few months later divers spotted the aSga in Malinska, Island of Krk (Zuljevic' & An to I ic!, 1998). The third and last recording was in October 1996 on the northwest side of Dolin Island in the Barbat Channel (Zuljevic & Antolic, 1998). It was estimated that the alga had been brought into the areas of the Stari Grad Bay and Malinska Harbour in 1991 and into the Barbat Channel in 1995 (Span et al., 1998; ZuijeviC & Antofid, 1998). The site in Malinska was only partially eradicated while the site in the Barbat Channel was eradicated in total (Zuljevic & Antolic, 1998). Taxa Class Origin Vector First record Source Acartia tonsa Crustacea Indo-Pacific aquaculture 1987 Occhipinti ¡20001 Bafanus (tigonus Crustacea Circumtropical shipping 1968 Za vodnik (1998) Rrachydontes phuraonis Bivalvia Indo-Pacific Lessepsian introduction 1996 De Min & Vio (1998) Bursatella leachii Gastropoda Circumtropical Lessepsian introduction 1986 De Min & Vio (1998) Callinectes danae Crustacea Western Atlantic ? 1961 C1ESM (2000) CaHinectes sapidus Crustacea Western Atlantic ballast waters 1949 CIESM (2000) Cmssostrea gigas Bivalvia Japan aquacullure 196'? De Min & Vio (1998) Dyspanopeus sayi Crustacea N-W Atlantic ballast waters 1992 CIESM (2000) ichinogammarus pungen- Crustacea / aquaculture ; Cognetti (1994) Ficopomattis enrgmaticus Polychaeta Australia ? > Avčin (1984) Gambusia affinis Osteichrhyes Central America purposeful introduction 1936 Leinerefa/. (1995) Halgerda sp. Gastropoda Indo-Pacific ballast waters 1988 Turk (2000) Littorina saxatilis Gastropoda Atlantic 1792 Occhipinti Anibrogi (1994) A tuggiaes atlantica Hydrozoa Atlantic ? 19% Gamulin KrSiniC (2000) Musculista senhousia Bivalvia indo-Pacific Lessepsian introduction 1986 De Min & Vio (1998) Paraceneis sculpta Crustacea ? } ? Cognetti {1994] Pcma picta Bivalvia Atlantic shipping 1996 De Min & Vio (1998) Pinctada radiata Bivalvia Indo-Pacific Lessepsian introduction 1996 De Min & Vio (1998) Rapana venosa Gastropoda japan shipping 1973 De Min & Vio (1998) R h ithropa nopens lis r ris i i Crustacea N-W Atlantic ballast waters 1994 CIESM (2000) Saccostiva commerc ta tis Bivalvia Australia aquaculture 1980 De Mirt & Vio (1998) Scapharca inaequivalvis Bivalvia Judo-Pacific ballast waters 1969 De Min & Vio (t 998) Strombus decows Gastropoda Indian Ocean shipping 1996 De Min & Vio 0998) Tapes phitippiriarum Bivaivia Indo-Pacific aquaculture 1983 De Min & Vio (1998) Tried!arîa inopinata Bryozoa Indo-Pacific 7 1982 Occhipinti Ambrogi (1994) Xenostrobus securis Bivalvia Australia shipping 1992 De Min & Vio (1998) 152 ANNALES Ser. hist. nni. Il - 2001 • 2 (25) M.ifMn.-! ORLAÏ-.T'O BONACA-A SURVEY Of THE INTRODUCED NONMNOfCFNOUS SPECIES . ! 49-15« % • - ; • , >V à m;m Fig. 4/Sl. 4: Asparagopsis armata - Falkenbergia rufola-riosa phase. (Photo/Foto: M. Richter) Fig. 3/Sl. 3: Caulerpa taxifolia. (Photo/Foto: M. Richtcr) The non-indigenous red alga Asparagopsis armata was recorded for the first time in the northern Adriatic, in Slovenian coastal waters, in 1991 (M. Richter, pers. comm.}, but only the tetrasporophyte - Falkenbergia ru-folanosa phase (Fig. 4). Six years later the gametophyte plants were recorded in Croatian waters near Senj (M. Richter, pers. comm.). This species originates from Australia and/or possibly New Zealand and it was introduced to the Mediterranean Sea unintentionally with oysters (Ribera & Boudouresque, 1995). In 1995, the red algae Bonnemaisonia ha mi (era was found in Slovenian coastal waters, but only the filamentous tetrasporophyte - Trailliella "pink cotton wool" phase (M. Richter, pers. comm.) (Fig. 5}. This species originates in the Pacific and was probably introduced with shellfish from japan (Tittley, 2000). The green alga Uiva scandinavica (originating from Sweden and Norway) was recorded for the very first time in the coastal waters of Slovenia in September 1998 {Battel!i & Tan, 1998). It was also the first record of this species in the Adriatic Sea. Before that, U. scandinavica was recorded in the Mediterranean Sea only on the west and south coast of Italy (Batteili & Tan, 1998). Fig. 5/ SI. 5: Bonnemaisonia hamitera - Trailliella phase (Photo/Foto: M. Richter) The presence of Coditim fragile subsp. tomentosoides in the northern Adriatic Sea was noticed for the first time in 1992 (Munda, 1992). Its presence in Slovenian coastal waters was confirmed many times (Munda, 1993; Batteili & Vukovic 1995; Batteili, 1996). This species (Fig. 6) originated in the Pacific Ocean around japan. It spread remotely either as an associated unintentional introduction attached to shellfish as oysters, attached to ships' hulls or as spores in ballast tanks. In the Mediterranean Sea it was reported for the first time in French waters in 1950, and subsequently appeared at both near and distant sites, with no apparent link with either the direction of the currents or the distance (Fig. 7) (Ribera & Boudouresque, 1995). The invasive seaweeds Undaria pinnatifida, Sargas-sum muticum and Antithamnion pectinatirm have been recorded in the Venice Lagoon (Curiel et ai„ 1994; 1995; 199G; 1998). The brown seaweed Sargassum muticum (Fig. 8) was first introduced into France along with C'rassostrea gigas in the late 1960s (Critchley et ai, 1983). The subsequently rapid expansion of the alga has led to a dramatic increase in the number of permanent ANNALES • Ser. hist. liât. 11 ■ 2001 • 2 (25) Martina O P. L AN'DO SONACA: A SURVEY OF THE INTRODUCED NON-iNDlGtNOUS SPtClES ..., 145-158 Fig. 6/SI. 6: Codium fragile. (Photo/Foto: M. Richter) populations along the European Atlantic coast and in the western Mediterranean. Also the introduction of Undaria pinnatifida and Antithamnion pectinatum in European waters was caused by the importation of the Japanese oyster in mariculture (Rueness, 1989). All these species have quickly colonized the hard substrata in the Venice Lagoon, competing with indigenous species, and the lack of potential predators in the colonized area (such as sea urchin Paracentrotus tividus) probably enhances their spread. According to several authors, manual eradication may be ineffectual, due to their efficient reproduction mechanisms and preliminary data showed quick recolonization of the area (Curiel etal., 1998). Recently, another atga from the genus Sorocarpus has been reported for the Venice Lagoon, which is also the first record in the Mediterranean (Curiel et at., 1999). The authors have not made any hypotheses about the origin and the period of arrival of the settlement, due to the lack of knowledge of its distribution in the lagoon area. CONCLUSIONS Although the northern Adriatic Sea is just a small portion of the Mediterranean marine realm, it has been certainly affected by the invasion of non-indigenous species These organisms have been introduced mostiy by shipping, through the Suez Canal or for aquac.ulture purposes. Twenty-six introduced animals and nine algae have been recorded to date. It is quite reasonable to expect that the list will be expanded in the near future. Fig. 7: Chronology of the expansion of Codium fragile in the Mediterranean (modified from Rihera, 1994). Sf. 7: Kronologija širjenja vrste Codium fragile v Sredozemlju (dopolnjeno po Riberi, 1994). 154 ANNAL tS • Ser. hist. nat. • 11 • 2001 • 2 (25) Marline! ORLANDO BON AC A ASUKVfY OF THE INTRODUCïD NON-1NDICENOUS SffŒS ... 149-153 Tab. 2: Non-indigenous flora in the northern Adriatic Sea. Tab. 2: Tujerodna flora v severnem Jadranu. Taxa Division Origin Vector first record Source Anlilhaminon peclinatum Rhodophyta Japan aquacuiture 1994 Curie! étal. (1996) Aspamgopsis armata Rhodophyta Australia Gibraltar 1991 Kichter Ioral. comm.) gofW>emaisonia hamifera Rhodophyta Pacific Gibraltar 1995 Richter (oral, comm.) Caulerpa taxifolia C.hlorophyta Pan(ropico be proper to set up an international monitoring programme of ballast waters The exchange of ballast water as far as possible from the roast is nowadays believed to be the most reliable method to minimise the risk of transfer of unwanted organisms (Gol-lasch & Leppakoski, 1999). But if not accompanied with a proper enforcement oi existing national and international legis ations (above ali the articles concerning the transfer of living marine or ganisms), even the best research and monitoring pro grams shall have little chance to control and minimize the introduction of potentially harmful marine non indigenous species. Nowadays, the current legislations appear very inadequate and insufficient (De Klemm, 1994. Verfaque, 2001). ACKNOWLEDGEMENTS ! wish to thank Asst. Prof. Dr. Lovrenc Lipej for his advice and help during the preparation of the paper, Marjan Richter for his information and photos, Dr. Aleksander Vukovic foi sharing with me his knowledge, Ti-homir Makovec for his photos and technical help, and Vladimir Bemetic for his help in the search for the literature. fig. 8/Sl. 8: Sargassum rnuticurn. (Photo/Foto: M. Richter) 155 ANNALES • Ser. hist. nat. ■ 11 ■ 2001 2 (25) Martina ORLANDO BONACA.A SURVEY Of THE INTRODUCED NON-INDIGENOUS SPECKS t <19-1 SB PREGLED VNOSOV TUJERODNIH VRST V SEVERNI JADRAN Martina ORLANDO BONACA Nacionalni institut za biologijo. Morska biotoika postaja, Sl-63i0 Piran, Fornače 41 POVZETEK Avtorica podaja pregled zabeleženih vnosov tujerodnih vrst v severnem Jadranu, temelječem na bibliografskih zapisih ter Se ne objavljenih podatkih. Na tem območju je bilo opaženih petintrideset, alohtonih vrst, od tega devet alg in šestindvajset živali. Med algami je najbolj znana eksotična vrsta Caulerpa taxifolia, ki je bila v severnem Jadranu prvič opažena leta 1994. Mehkužci so najpogosteje vnešene živali. fujerodni morski organizmi se na več načinov nenehno širijo po svetu in tako prihajajo tudi v severno-jadranske vode. Plovba je najpomembnejši vnosni vektor. Strokovnjaki menijo>, da so balastne vode z ekološkega in taksonom-skega vidika najmanj selektiven način prenosa organizmov. Plovila prevažajo organizme tudi na svojem trupu in dnu. Eksotični organizmi vstopajo v Sredozemsko morje tudi skozi Sueški prekop>, ki je bil zgrajen leta 1869. Tretji zelo pomembni vir vnosa tujerodnih vrst pa je marikultura. japonsko ostrigo {Crassostrea gigas) so prvič uvozili v Evropo v šestdesetih letih in nehote z njo pripeljali tudi nekatere vrste alg, kot sta Sargassum muticum in Lindaria pin-natifida, ki se zelo hitro širita na trdih podlagah Beneške lagune. Strokovnjaki se s tujerodnimi vrstami premalo časa ukvarjajo, da bi lahko natančno ocenili njihov vpliv na novo okolje. Večina teh vrst kmalu pogine, tiste, ki pa preživijo, lahko povzročijo ogromno škodo. 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