Original scientific article	UDC 582.26:581.524.2(262.3)
Received: 2010-09-20
NEW RECORDS OF NON-INDIGENOUS ALGAL SPECIES IN SLOVENIAN COASTAL WATERS
Martina ORLANDO-BONACA Marine Biology Station, National Institute of Biology, SI-6330 Piran, Fornace 41, Slovenia E-mail: martina.orlando@mbss.org
ABSTRACT
New records of non-indigenous algal species in Slovenian coastal waters are presented. The red alga Asparagop-sis armata Harvey (Falkenbergia rufolanosa phase) and the green alga Codium fragile subsp. fragile (Suringar) Hariot were collected in shallow waters in the period of the last five years. The author discusses the presence of other non-native algal species in the northern Adriatic and the importance of some vectors of introduction.
Key words: non-indigenous algal species, Slovenian coastal waters, northern Adriatic Sea
NUOVE SEGNALAZIONI DI SPECIE ALGALI NON-INDIGENE IN ACQUE COSTIERE SLOVENE
SINTESI
L'articolo riporta nuove segnalazioni di specie algali non-indigene in acque costiere slovene. L'alga rossa As-paragopsis armata Harvey (fase Falkenbergia rufolanosa) e l'alga verde Codium fragile subsp. fragile (Suringar) Hariot sono state raccolte in acque poco profonde negli ultimi cinque anni. L'autrice discute sulla presenza di altre specie alloctone nell'Adriatico settentrionale e l'importanza di alcuni vettori d'introduzione.
Parole chiave: specie algali non-indigene, acque costiere slovene, Adriatico settentrionale
INTRODUCTION
In the last three decades, at least 40 non-indigenous marine species have been recorded in the northern Adriatic Sea, among them 14 species of introduced mac-rophytes (reviews in Orlando-Bonaca, 2001 and Krmac, 2009; additional data in Curiel et al., 2002). Different authors have documented the presence of four non-indigenous algal species in Slovenian waters.
In 1991, the tetrasporophyte (Falkenbergia rufola-nosa phase) of the red alga Asparagopsis armata Harvey was recorded for the first time in Slovenian coastal waters and in the northern Adriatic (M. Richter, pers. comm.). Six years later, gametophyte plants were recorded in Croatian waters near Senj (M. Richter, pers. comm.). This species originates from Australia and/or New Zealand and it was introduced to the Mediterranean Sea unintentionally with oysters (Ribera & Bou-douresque, 1995). The presence of the alga in Slovenian coastal waters was reported also by Battelli (2000).
In 1992, the presence of Codium fragile subsp. fragile (Suringar) Hariot (as Codium fragile subsp. tomentosoides (van Goor) P.C. Silva) was noticed for the first time by Munda (1992). The finding of the subspecies in Slovenian coastal waters was confirmed in the following years (Munda, 1993; Battelli & Vukovic 1995; Battelli, 1996, 2000). This green alga originates in the Pacific Ocean around Japan and it spread remotely either as an associated unintentional introduction attached to shellfish as oysters, attached to ships' hulls or as spores in ballast tanks. Ribera & Boudouresque (1995) reported that the presence of the subspecies in the Mediterranean Sea was firstly confirmed in French waters in 1950. Subsequently it appeared at both near and distant sites, with no apparent link to either the direction of the currents or the distance.
In 1995, the filamentous tetrasporophyte - Trailliella "pink cotton wool" phase of the red alga Bonnemaisonia hamifera Hariot was found in Slovenian coastal waters (M. Richter, pers. comm.). This species originates in the Pacific and was probably introduced with shellfish from Japan (Gollasch, 2006).
In 1998, the green alga Ulva scandinavica Bliding was recorded for the first time in Slovenian coastal waters and in the Adriatic Sea (Battelli & Tan, 1998). Before that, the species that originates from Sweden and Norway was recorded in the Mediterranean Sea only on the West and South coast of Italy (Battelli & Tan, 1998).
The aim of this paper is to provide new data about the presence of the introduced algae in Slovenian coastal waters. The current state of the non-indigenous algal species in the area is also discussed.
MATERIAL AND METHODS
The Slovenian coastal sea covers the southern part of the Gulf of Trieste. It is a shallow semi-enclosed gulf with a maximum depth of ca. 33 m in waters off Piran. Its coastline is approximately 46.7 km long. The Slovenian coastal area is affected by freshwater inflows and local sources of pollution, mostly anthropogenic impacts such as intensive farming, sewage outfalls, and mari-culture (Francé & Mozetic, 2006; Mozetic et al., 2008; Grego et al., 2009). Many activities such as urbanisation and massive tourism have modified the natural shoreline (Turk, 1999).
From 2006 to 2010, benthic macroalgae were sampled in the upper-infralittoral belt (depth range from 1 to 4 m) in at least 51 sites selected in order to assess the ecological status of macroalgal communities, as required by the European Water Framework Directive 2000/ 60/EC (WFD) (Orlando-Bonaca et al., 2008; Orlando-Bonaca & Lipej, 2009). Additionally, macroalgae were sampled from the water surface down to 10 m of depth in order to characterize benthic habitat types (Lipej et al., 2007, 2008). These studies were broadened in the last years, as required by the Marine Strategy Framework Directive 2008M/ES (Orlando-Bonaca et al., 2010a, 2010b).
Collected samples were placed in plastic bags and the material was transported to the Marine Biology Station of the National Institute of Biology for analysis. Species identification of macroalgae was carried out in the laboratory in accordance with Ribera et al. (1992), Gallardo et al. (1993), Battelli (1996), Gomez Garreta et al. (2001), and Bressan & Babbini (2003).
RESULTS AND DISCUSSION
Two non-indigenous algal species were collected in Slovenian coastal waters in the past five years. Samples of C. fragile subsp. fragile were collected twice (Tab. 1). In summer 2006, a single thallus was found at 3 m of depth at the Cape of the Piran peninsula, during regular monitoring sampling (Orlando-Bonaca et al., 2008). In 2007, 2008 and 2009, the alga was not present in any sample. In August 2010, the subspecies was found to be much more abundant (average density 4 thalli m-2) in the same site, along a coastal segment 50 m long, in a depth range from 1 to 1.5 m. Various unidentified red filamentous algae were growing epiphytically on thalli (Figs.1, 2). The subspecies could be considered as established in this area; however, it is too early to evaluate its potentially damaging impact on the native algal associations.
Tab. 1: Records of non-indigenous algal species in Slovenian coastal waters from the period of the last 5 years. Tab. 1: Podatki o tujerodnih vrstah alg v slovenskih obalnih vodah iz obdobja zadnjih 5 let.
Species	Sampling site	Date	Depth (m)	Average density (thalli m"2)
Codium fragile subsp. fragile	Cape Piran	24.07.2006	3.0	a single thallus
	Cape Piran	25.08.2010	1.5	4
Asparagopsis armata	Marina Izola	26.06.2008	1.0	3
	Cape Ronek	02.09.2008	1.0	2
Fig. 1: Codium fragile subsp. fragile in the summer 2010 at the Cape of the Piran peninsula. (Photo: L. Lipej) Sl. 1: Codium fragile subsp. fragile poleti 2010 na rtu Piranskega polotoka. (Foto: L. Lipej)
Fig. 2: Herbarium specimen of C. fragile subsp. fragile collected in the summer 2010. (Photo: M. Orlando-Bonaca) Sl. 2: Herbarijski primerek C. fragile subsp. fragile, nabran poleti 2010. (Foto: M. Orlando-Bonaca)
In the Italian part of the Gulf of Trieste, C. fragile subsp. fragile was firstly reported by Godini & Avanzini (1988). Nowadays, the subspecies is commonly found in the northern area of the Gulf (Duino-Sistiana sampling sites) as reported in Falace (2000) and Ceschia et al. (2007). Scheibling and Gagnon (2006) provide clear evidence that competitive interactions with large, canopy-forming brown algae can limit the growth of C. fragile subsp. fragile on the Atlantic coast of Nova Scotia (Canada) but, once established, Codium meadows inhibit the re-establishment of native canopy-forming species. Molecular genetics analyses of widely distributed populations of subsp. fragile and of herbarium samples suggest that this is the only invasive form among the recognized subspecies of C. fragile (Provan et al., 2008).
The tetrasporophyte of A. armata was collected in summer 2008 on limestone breakwater boulders of the Marina Izola (Tab. 1, Fig. 3). The alga was present along a coastal segment 20 m long. In the same year, some more thalli of the species were found at Cape Ronek on a sandstone terrace. The alga was not found during the last two years.
In 1978, A. armata was firstly reported for the Gulf of Trieste (Giaccone, 1978). Nowadays, the tetrasporophyte of the species is reported to be commonly found in Italian waters of the Gulf of Trieste (mostly in Mira-mare, Barcola and Aurisina sites) (Falace, 2000). However, the CIESM Atlas of Exotic Macrophytes in the Mediterranean Sea (2009) defines the species as "infrequent" for the Adriatic Sea.
B. hamifera has never been never found in any mac-roalgal sample collected by the Marine Biology Station. Falace (pers. comm.) has not found the species in the Italian part of the Gulf of Trieste. Anyhow, the CIESM Atlas of Exotic Macrophytes (2009) reports on one local record of the species in the Italian part of the Gulf (which is also the only record for the Adriatic Sea), but the bibliography is currently not available. It is therefore impossible to confirm the presence of this red alga in Slovenian waters.
The presence of U. scandinavica was not reconfirmed for Slovenian coastal waters. Moreover, it has never again been reported for the Mediterranean Sea after the publication of Battelli & Tan (1998). Some authors reported its presence on the Atlantic coasts of France, Portugal and Spain (Diaz-Tapia & Bárbara, 2005; Dizerbo & Herpe 2007; Araujo et al., 2009). But according to AlgaeBase (Guiry & Guiry, 2010) and WoRMS (Appeltans et al., 2010) registers, this name is currently regarded as a taxonomic synonym of Ulva rigida C. Agardh.
Although just two non-indigenous algal species appear nowadays to be established in Slovenian coastal waters, it is reasonable to expect the list to expand in the near future. Other non-indigenous algal species were found to be well established in the northern Adriatic, and they could easily reach the Slovenian Sea, both from Italian and Croatian waters. In the years from 1992 to 1994, three invasive algae, Undaria pinnatifida (Harvey) Suringar, Sargassum muticum (Yendo) Fensholt, and
Fig. 3: Herbarium specimen of Asparagopsis armata collected in the summer 2008. (Photo: M. Orlando-Bonaca) SI. 3: Herbarijski primerek Asparagopsis armata, nabran poleti 2008. (Foto: M. Orlando-Bonaca)
Antithamnion pectinatum (Montagne) J.Brauner were recorded in the Venetian Lagoon (Curiel et al., 1994, 1995, 1996, 1998). These seaweeds were introduced into European waters along with Crassostrea gigas, in the late 1960s (Critchley et al., 1983; Rueness, 1989). They quickly colonized the hard substrata in the Venetian Lagoon, competing very well with indigenous species, due to their efficient reproduction mechanisms (Curiel et al., 1998). In 1996, a brown alga from the genus Sorocarpus was first recorded in the Mediterranean Sea, again in the Venetian Lagoon (Curiel et al., 1999). Some years later, Curiel et al. (2002) reported the finding of Polysiphonia morrowii Harvey, and Desmarestia willii Reinch (as Desmarestia confervoides (Bory de Saint-Vincent) M. E. Ramirez & A. F. Peters) in the same area. Moreover, in 2000 Lomentaria hakodatensis Yendo, known from China, Japan and Korea, was found in the Venetian Lagoon (Curiel et al., 2006). The last record concerns Ac-rothamnion preissii (Sonder) E.M. Wollaston, originating from Western Australia, that was collected in July 2007 in the Marano and Grado Lagoon (Falace et al., 2009).
Other three invasive algal species are considered to be established in the Croatian part of the northern Adriatic Sea. The tropical alga Caulerpa taxifolia (M. Vahl) C. Agardh, accidentally introduced from the Oceano-graphic Museum in Monaco into the natural environment (Meinesz & Hesse, 1991), was found in the Adriatic Sea in Stari Grad Bay (Hvar Island, Croatia) and in Malinska (Krk Island) in 1994, and in the Barbat Channel (Dolin Island) in 1996 (Zuljevic & Antolic, 1998). The alga was only partially eradicated from Malinska (Zuljevic & Antolic, 1998). Caulerpa racemosa var. cylin-dracea (Sonder) Verlaque, Huisman & Boudouresque, originating from South-western Australia, is currently considered more dangerous for natural habitats of the northern Adriatic. The first record of the species in the Adriatic dates from 2000 at the Pakleni Islands (Zuljevic et al., 2003). Nowadays, more than 60 affected locations (also in the northern Adriatic) were recorded, with the species changing native macroalgal populations (Despa-latovic et al., 2008). The third invasive species present in Croatian North Adriatic waters is the red filamentous alga Womersleyella setacea (Hollenberg) R.E. Norris.
The seaweed has Indo-Pacific-Carribean origin and was recorded for the first time in the Rijeka Bay in 1997 (Battelli & Arko Pijevac, 2005). Since then, the species has frequently been found in at least 50 Adriatic locations, where its dense monospecific turfs on rocky bottoms are covering native algal assemblages (Despalato-vic et al., 2008).
Nowadays it is well known that marine non-indigenous species are mostly transported intentionally and/ or unintentionally for aquaculture purposes, or unintentionally with marine traffic (transport of organisms in ballast waters, sediments in ballast tanks and hull fouling) (Gollasch & Leppakoski, 1999). Krmac (2009) reported that ballast waters that are released in the Port of Koper mostly originate from Porto Marghera (Venetian Lagoon) where vessels unload the cargo and introduce ballast waters. Subsequently, water from their ballast tanks is released into the Koper Bay when they reload. The possibility of new non-native species introduction into Slovenian waters is therefore still high, since the Venetian Lagoon is considered to be rich in invasive species. From studies concerning the tracking of the invasive species spread, underlying the accurate identification of cryptic taxa, it is evident that the number of taxonomic units involved in bio-invasion is currently underestimated (Provan et al., 2008). As the future of the introduced species is unpredictable, it would be very useful to enforce the international collaboration in the Adriatic, and to constantly update the global data bank on introduced species and receptive habitats.
ACKNOWLEDGEMENTS
The author would like to thank Žiga Dobrajc, Milijan Šiško, Borut Mavric, Lovrenc Lipej, Erik Lipej, Franc Kravos, Aleksander Vukovic, Tihomir Makovec and Marko Tadejevic for their help during the 5 years of fieldwork. Special thanks to Annalisa Falace and Marjan Richter for their precious information, and to Lovrenc Lipej for the photography.
This paper is dedicated to the memory of our wonderful colleague and friend Žiga Dobrajc, who recently tragically passed away.
NOVI ZAPISI O TUJERODNIH VRSTAH ALG V SLOVENSKIH OBALNIH VODAH
Martina ORLANDO-BONACA Morska biološka postaja, Nacionalni inštitut za biologijo, SI-6330 Piran, Fornače 41 E-mail: martina.orlando@mbss.org
POVZETEK
Avtorica podaja pregled novih podatkov o tujerodnih vrstah alg v slovenskih obalnih vodah. Rdeča alga As-paragopsis armata Harvey (faza Falkenbergia rufolanosa) in zelena alga Codium fragile subsp. fragile (Suringar) Hari-ot sta bili v zadnjih petih letih opaženi in nabrani v plitvem morju. Za zdaj sta to edini tujerodni algi, ki sta ustaljeni v slovenskem morju. Avtorica nadalje razpravlja o navzočnosti drugih vrst tujerodnih alg v Severnem Jadranu in o načinih vnosa. Tujerodne vrste bi lahko v slovensko morje prispele iz Beneške lagune, kjer so doslej potrdili navzočnost vsaj 8 vrst tujerodnih alg. Prav tako so 3 druge vrste alg že prisotne ob hrvaški obali v Severnem Jadranu in jih lahko zato upravičeno pričakujemo tudi v slovenskem delu Jadrana.
Ključne besede: tujerodne vrste alg, slovenske obalne vode, Severni Jadran
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