BioInvasions Records (2013) Volume 2, Issue 3: 177–184 Open Access doi: http://dx.doi.org/10.3391/bir.2013.2.3.01 © 2013 The Author(s). Journal compilation © 2013 REABIC

Research Article

Alien marine macrophytes in transitional water systems: new entries and reappearances in a Mediterranean coastal basin

Antonella Petrocelli1*, Ester Cecere1 and Marc Verlaque2 1 Institute for the Marine Coastal Environment (IAMC) – CNR, Talassografico “A. Cerruti”, Taranto, Italy 2 Aix-Marseille University, Mediterranean Institute of Oceanography (MIO), Marseille cedex 9, France E-mail: [email protected] (AP), [email protected] (EC), [email protected] (MV) *Corresponding author

Received: 20 March 2013 / Accepted: 17 July 2013 / Published online: 24 July 2013

Handling editor: Frédéric Mineur

Abstract

Three alien macrophytes, Ascophyllum nodosum, peregrina and Polysiphonia morrowii, are reported for the first time from the Mar Piccolo of Taranto (southern Italy, ). Two other species, Agardhiella subulata and Codium fragile subsp. fragile that were not, or were sporadically, detected in the basin since their first record in 1987 and 2002, respectively, were also recorded. In the Mar Piccolo, there appears to be a close link between establishment of alien species and the regular import of shellfish for direct sale. To limit the flow of accidental species introductions, a continuous and rigorous control of all the economic activities performed along the coast is recommended through the enforcement of effective laws and an early detection of new introductions. Key words: Ascophyllum nodosum; ; marine macrophytes; Mar Piccolo; Mediterranean Sea; Polysiphonia morrowii; shellfish transfer

shellfish farming (mussels and oysters) was the Introduction main economic activity up to the second half of the 1950's (Caffio 2009). Starting in the 1980's, Transitional water systems (TWS) (i.e. estuaries, to satisfy the increasing market demands, the coastal lagoons) are traditionally exploited for import of shellfish from both Mediterranean and their resources, including fisheries and aquaculture extra-Mediterranean countries began. In 2011 activities (Pérez-Ruzafa et al. 2011). Human and 2012, the destruction of most of mussel pressures in these systems have, in the long term, production of the First Inlet plants (see Figure 1) resulted in degraded water quality, destruction of due to dioxin and PCB contaminations required habitats, a serious depletion of marine biodiversity, massive importations to meet consumer demands. In and (especially in the last 30 years) large 2013, the First Inlet mussel processing plants numbers of invasions by alien species (Lotze et were moved to the near Mar Grande (Figure 1). al. 2006). As far as the Mediterranean Sea is The first alien marine macrophytes were concerned, about 1000 alien marine species are observed in the Mar Piccolo shortly after the listed, of which there are 128 macrophytes onset of shellfish imports in the 1980's and the (Zenetos et al. 2010; 2012). The introduction of number of species detected had increased to 10 alien macrophyte species has been particularly by the end of 2010 (Perrone and Cecere 1994; pronounced into transitional water systems, Cecere and Petrocelli 2009; Gravili et al. 2010; especially in the Western Mediterranean Basin Cecere et al. 2011). Some of alien species were (Zenetos et al. 2010; 2012). recorded sporadically [e.g. Codium fragile The Mar Piccolo of Taranto (Ionian Sea, southern (Suringar) Hariot subsp. fragile, Grateloupia Italy) is a Mediterranean transitional water system minima P.L. Crouan & H.M. Crouan, Osmundea long used for human activities. In particular, oederi (Gunnerus) G.Furnari and Womersleyella

177 A. Petrocelli et al.

Figure 1. The Mar Piccolo of Taranto - Location of monitored stations () and alien marine macrophytes: 1. Agardhiella subulata; 2. Ascophyllum nodosum; 3. Codium fragile subsp. fragile; 4. Colpomenia peregrina; 5. Polysiphonia morrowii. ( ) Location of mussel plants in the First Inlet before 2013 and in the Mar Grande starting from 2013.

setacea (Hollenberg) R.E. Norris,]; some formed like features of the Mar Piccolo are mainly due to transitory but well developed populations [e.g. the presence of several submarine freshwater Agardhiella subulata (C. Agardh) Kraft et M.J. springs and a few small rivers entering the two Wynne, Solieria filiformis (Kützing) Gabrielson inlets. The two basins are subject to strong and Undaria pinnatifida (Harvey) Suringar], and human pressures such as urban, industrial, and the final group formed permanent populations agricultural pollution as well as aquaculture, exhibiting fluctuating abundances [e.g. Caulerpa military shipping, and commercial fishing. The racemosa (Forsskål) J. Agardh var. cylindracea salinity ranges from 34.3 to 37.7 while seawater (Sonder) Verlaque, Huisman et Boudouresque, temperature ranges from 7.1°C to 33.6°C Grateloupia turuturu Yamada and Hypnea cornuta (Alabiso et al. 1997). (Kützing) J. Agardh]. However, none of the species From 2011 to winter 2013, seasonal surveys listed ever showed noxious invasive behaviour. were carried out at four stations in the Mar The regular monitoring of the marine flora of Piccolo of Taranto where alien marine species the Mar Piccolo specifically designed to detect were previously observed (Figure 1). Marine alien flora, began in December 2000 and was macrophytes were hand-collected and brought to carried out monthly at four stations until the end the laboratory for study under stereo and light of 2010 (Figure 1). Since 2011, due to the lack microscopes (Leica Microsystems®, Wetzlar, of funds, a seasonal monitoring activity was Germany). Photomicrographs were made using a started. This study reports the detection of new Nikon Coolpix 4500 (Nikon, Tokyo, Japan). non-native macrophytes, plus two species that Afterwards, some thalli were preserved in 2.5% re-appeared, in Mar Piccolo between 2011 and formaldehyde-seawater and others were dried as 2012. voucher specimens that are stored in the Herbarium of the Istituto Sperimentale Talassografico of Taranto (TAR) (Table 1). Materials and methods

The Mar Piccolo of Taranto (40°28'N; 17°15'E) Results (Northern Ionian Sea) is a semi-enclosed embayment showing lagoon-like features. It has Two exotic species, Agardhiella subulata and a surface area of 20.72 km² and is divided by two Codium fragile subsp. fragile, which had not promontories into two smaller basins: the First been observed in the Mar Piccolo since the end Inlet with a maximum depth of 12 m and the of 1990s and 2009, respectively, were found again in Second Inlet which has a maximum depth of 8 m 2011. Three additional exotic species, Ascophyllum (Figure 1). Hard substrates are mostly artificial nodosum (Linnaeus) Le Jolis, Colpomenia peregrina while the natural substrate is sandy near the Sauvageau, and Polysiphonia morrowii Harvey shore and muddy in the central zone. The lagoon- were detected for the first time in 2012.

178 Presence of new alien in a Mediterranean

Table 1. Material deposited in the Herbarium of the Istituto Sperimentale Talassografico of Taranto (TAR).

Species Finding Specimen / photo Agardhiella subulata Mar Piccolo, 13.10.1989 53R TAR Mar Piccolo, 03.12.1989 60R TAR Mar Piccolo, 28.06.2011 135R TAR Mar Piccolo, 24.05.2012 136R TAR, female gametophyte Ascophyllum nodosum Mar Grande, 25.07.2009 44F TAR, specimens unattached Mar Grande, 01.03.2011 51F TAR, specimens unattached Mar Piccolo, 28.05.2012 Photos, specimens attached Colpomenia peregrina Mar Piccolo, 24.04.2012 56F TAR Mar Piccolo, 28.05.2012 Formalin preserved thallus Codium fragile subsp. fragile Mar Piccolo, 16.07.2002 Formalin preserved thallus Mar Piccolo, 25.07.2009 35C TAR Mar Piccolo, 21.07.2011 Formalin preserved thallus Mar Piccolo, 28.05.2012 Formalin preserved thallus Polysiphonia morrowii Mar Piccolo, 21.05.2012 Formalin preserved thallus Mar Piccolo, 26.02.2013 148R TAR

Figure 3. Ascophyllum nodosum. Attached thallus observed in June 2012. Photograph by E. Cecere and A. Petrocelli.

pyramidal in shape, with branches tapered at the basis and acuminate to rounded at the apex. These characters agree well with the description of specimens previously found in the region (Perrone and Cecere 1994). Some individuals were irregularly branched due to many regenerations and proliferations caused by heavy grazing. Only Figure 2. Agardhiella subulata. Unattached thallus collected in female and male gametophytes were collected, no June 2011. Photograph by E. Cecere and A. Petrocelli. tetrasporophytes were observed. New findings occurred also in March and December 2012 in the same station. Agardhiella subulata was collected Unattached individuals of Agardhiella subulata in a zone where both local and imported (Rhodophyta, Gigartinales, Solieriaceae) were molluscs are packed before selling (Figure 1). found at 1 m depth in June 2011, entangled with Sparse thalli of Ascophyllum nodosum Gracilaria bursa-pastoris (S.G. Gmelin) P.C. Silva (, Fucales, Fucaceae) were found (Figure 2). Thalli were dark red, very robust, settled on pebbles and fishing nets down to 50 terete throughout, with a diameter of axes up to 5 cm depth in June 2012 (Figure 3). Thalli, greenish mm. Main branches were percurrent, densely and in colour, reached a maximum height of 30 cm, alternately branched to 3–4 orders, sometimes growing together with Amphiroa beauvoisii J.V.

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Figure 4. Codium fragile subsp. fragile. Attached thallus Figure 6. Polysiphonia morrowii. Thallus collected in March observed in July 2011. In the frame, utricles with pointed apex 2012, as an epiphyte on Dictyota dichotoma. In the inset, note the (arrows). Photograph by E. Cecere and A. Petrocelli. pointed branchlets (arrows). Photograph by E. Cecere and A. Petrocelli.

A few thalli of Codium fragile subsp. fragile (Chlorophyta, Bryopsidales, Codiaceae), up to 8 cm high, were observed on a few rocks in July 2011 (Figure 4). Specimens were bottle-green, generally isolated, settled at ca 1 m depth, and free of epiphytes. The presence of mucronate utricles confirmed the identification of the species (Silva 1955). New thalli were observed in May- June 2012. C. fragile subsp. fragile was found in an area where the fish market and several mollusc retail shops were present (Figure 1). Small isolated, brownish and saccate thalli of Colpomenia peregrina (Ochrophyta, , ) were found in March-April 2012 (Figure 5), settled on pebbles, together with Figure 5. Colpomenia peregrina. Attached thallus observed in Amphiroa beauvoisii, Corallina sp., Dictyota April 2012. In the frame, sporangia without cuticle (arrow). dichotoma var. intricata, Lomentaria clavellosa Photograph by E. Cecere and A. Petrocelli. (Lightfoot ex Turner) Gaillon, Padina sp., Scytosiphon lomentaria (Lyngbye) Link and Ulva rigida C. Agardh. No reproductive structures Lamouroux, Corallina sp., Dasya rigidula (Kützing) were present. More aggregated thalli collected in Ardissone and Dictyota dichotoma (Hudson) J.V. April and May 2012 were fertile, with plurilocular Lamouroux var. intricata (C. Agardh) Greville. sporangia without cuticle, which allowed the No reproductive structures were observed. No correct identification (Clayton 1975). No thalli thalli were found during the two following seasonal were observed in June 2012. Colpomenia surveys (August and December). Ascophyllum peregrina was found in a zone characterised by nodosum was found in a zone characterised by the the presence of numerous mussel retail shops as presence of numerous mussel retail shops, and was the case for A. nodosum and P. morrowii where other alien macrophytes (e.g. C. fragile, (Figure 1). G. turuturu, U. pinnatifida) were previously Two tufts of Polysiphonia morrowii (Rhodo- observed (Figure 1). phyta, Ceramiales, Rhodomelaceae), dark red in

180 Presence of new alien seaweeds in a Mediterranean colour, were collected in March 2012 (Figure 6), drastically declined and probably disappeared. in the same benthic assemblage as C. peregrina. The present occurrence of A. subulata in the Mar Tufts, up to 4 cm high, were characterised by the Piccolo likely resulted from new introductions. uncorticated axes with 4 periaxial cells; unicellular Like in the Lagoon of Venice (Curiel and Marzocchi rhizoids in open connection with the periaxial 2010), the Thau Lagoon (Boudouresque et al. cells, and by the ultimate branchlets sharply 2011) and the Cape Peloro Lagoon (Sicily) pointed at apex. No reproductive structures were (Manghisi et al. 2010), the most likely vector of observed. New thalli were found attached on introduction is the importing of shellfish. sparse pebbles in February 2013. Polysiphonia Ascophyllum nodosum is a cold-temperate morrowii was found in a zone characterised by North-Atlantic species (North America and the presence of numerous mussel retail shops as ) (Guiry and Guiry 2013). Unattached was the case for A. nodosum and C. peregrina thalli of A. nodosum were first observed in the (Figure 1). Mar Grande of Taranto in July 2009, in the vicinity of an experimental aquaculture site for Discussion Crassostrea gigas (Petrocelli and Cecere 2010). The attached individuals discovered in 2012 in Marine alien species can be introduced into new the Mar Piccolo are the first for the Mediterranean environments by means of a variety of vectors. Sea. The only previous European case of One of the most important vectors of introduction is introduction was on the trestles of C. gigas farms the trade in living organisms (Minchin 2007). in the Wadden Sea (Reise 1998). Like in San Indeed, unintentional introduction of marine Francisco Bay, where it was eradicated twice, aliens often happens for hitchhiking species, the species was likely imported as packing which are joined to the target species in various material (Miller et al. 2011). Since its upper, ways, e.g., used as packing material, as epibionts long-term, temperature tolerance does not exceed or hidden between the imported organisms, 24–25 °C (Keser et al. 2005), and the seawater attached to packages, or carried into the palleal temperature in the Mar Piccolo is far higher in cavity of shellfish (Olson 2001). As far as the summer (up to 33.6 °C; Alabiso et al. 1997), its marine macrophytes are concerned, the trade of naturalization seems unlikely. Ascophyllum shellfish (mainly oysters and mussels) is nodosum is itself, however, a potential vector for considered to be a major vector of introduction other non-native macrophytes and invertebrates in Europe and in the Mediterranean Sea (44% (Crawford 2001; Miller et al. 2004). and 46% of the total, respectively) (Wallentinus Codium fragile subsp. fragile is a cold- 2002; Zenetos et al. 2010). Among the temperate North-Pacific species that has been Mediterranean coastal lagoons, the Mar Piccolo introduced worldwide (Provan et al. 2008). The of Taranto, with 13 alien macrophytes, is only oldest European collection dates from 1845 in surpassed by the Thau Lagoon (58 alien species; (Provan et al. 2008), then the species Boudouresque et al. 2011) and the Lagoon of spread along the NE Atlantic coast and into the Venice (37 alien species; Sfriso et al. 2009). Mediterranean Sea. In the mid-1950's, it appeared Agardhiella subulata is commonly distributed along the NW Atlantic coast , in the 1970's in along the eastern coast of the USA, Caribbean New Zealand, and at the end of the last century Sea and Latin America. The species was also in Australia and Chile, where it became a serious reported in India and South Korea (Guiry and pest for aquaculture activities (Provan et al. Guiry 2013). In and the Netherlands, 2008, Bridgwood 2010). Its first introduction A. subulata is considered to be alien and most into the Mediterranean Sea probably dates from likely unintentionally introduced by shellfish the World War II and presumably was due to importation (Farnham and Irvine 1979; Wolff military shipping (Verlaque 1994). In the Mar 2005). In the Mediterranean Sea, it was first Piccolo, since July 2002 when two first attached reported in the Thau Lagoon in 1984 (Ben Maiz thalli were found, C. fragile was observed spora- 1986; misidentified as Solieria chordalis), then dically: in summer 2003, June 2009, July 2011, and in the Mar Piccolo of Taranto at the end of the May and June 2012 (Cecere and Petrocelli 2009, and 1980’s together with Solieria filiformis (Perrone unpublished data). This succession of introduction- and Cecere 1994) - both species being dominant extinction events might be associated with continu- in unattached macrophyte assemblages, mainly ous shellfish importations, as observed near Piran in summer, up to the end of the 1990’s (Cecere (Slovenia) (Orlando-Bonaca 2010). The high sea- et al. 1992). Afterwards, their populations water temperature in summer (up to 33.6°C) might

181 A. Petrocelli et al. explain the failure to naturalize because the precautionary procedures for the shellfish importing species requires a temperature range of 10–24°C are applied the more unintentional introductions for growth and reproduction (Bridgwood 2010). of associated aliens increase (Minchin 2007). In Colpomenia peregrina is a cold-temperate this respect, the importing of live seafood for Pacific species (Asia, North America and Australia) immediate consumption must be looked at more (Guiry and Guiry 2013). At the beginning of the carefully because organisms going directly to 20th century, it was introduced to France via the market are not subjected to the same sanitary import of the American oyster Crassostrea virginica controls that are required for those destined to (Gmelin 1791) (Farnham 1980). Afterwards it aquaculture activities (Chapman et al. 2003). spread throughout Britain, the rest of Europe, This could be the case for the Codium fragile Africa, North and Central America (Guiry and (Suringar) Hariot subsp. atlanticum (A.D. Guiry 2013). In the Mediterranean Sea, it was first Cotton) P.C. Silva, recently discovered at Marina reported in the Thau Lagoon in 1918 (Verlaque of Pisa (Tyrrhenian Sea) where several firms 2001). In the Mar Piccolo, C. peregrina was only import seafood for local restaurants (Petrocelli et observed from March to May 2012, but thalli al. 2012). Relatively simple aquaculture practices were fertile before disappearing in summer, so the already used to eliminate parasites (e.g. hot development of new generations can be expected, water or brine treatments) can markedly reduce as was observed in Japan (Kogame and the risk of macrophyte introduction (Mineur et Yamagishi 1997). al. 2007). Polysiphonia morrowii is a temperate, North- Until now, in the Mar Piccolo of Taranto, no Pacific, species (Japan, China, Korea and Russia) negative impacts due to establishment of alien reported as alien in Australia, New Zealand, and macrophytes have been detected. However, the Europe (Guiry and Guiry 2013). It is very close attention level must remain high because it is to P. senticulosa Harvey, another North Pacific well known that an alien species can become taxon reported from the Northern Europe invasive after a long period of quiescence (Stegenga et al. 2007). No fertile thalli were (Simberloff and Gibbons 2004). Since in the Mar found in the Mar Piccolo but our material was Piccolo of Taranto the importation of shellfish tentatively attributed to P. morrowii because all appears as a major and continuous way of the Mediterranean and NE Atlantic populations introduction of aliens, we recommend: 1. A previously studied belonged to this species continuous monitoring of aliens already observed (Verlaque 2001, Curiel et al. 2002, Geoffroy et in the basin as well as of potential sites of al. 2012). In the Mediterranean Sea, it was first introduction (aquaculture facilities) to early collected in 1997 in the Thau Lagoon and in detect any new entry; 2. A continuous and careful 1999 in the Lagoon of Venice (Verlaque 2001, control of the economic activities performed in Curiel et al. 2002). Its introduction with oyster the basin, punishing the non-observance of the imports from the NW Pacific is the most probable current laws; 3. Information campaigns towards hypothesis. In the Mar Piccolo, P. morrowii was sea-users (e.g. shellfish farmers, fishermen, only observed in March 2012 and February 2013, scuba divers, yachtsmen) and the general public, maybe because its natural growth period is short to acquaint them of the problem and of the best (from February to May in Korea; Kim et al. practices for avoiding unintentional introductions. 2004). Polysiphonia morrowii is considered as potentially invasive (Geoffroy et al. 2012), so a Acknowledgements careful monitoring of the species in the Mar Piccolo is advisable. This study was partially supported by the Research Project These new findings, their proximity with “RITMARE-Italian Research for the sea” financed by the Italian Ministry of Instruction, University and Research. We are indebted shellfish retail shops and the frequent observations to Michèle Perret-Boudouresque for bibliographic assistance. 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