BioInvasions Records (2015) Volume 4, Issue 1: 9–16 Open Access doi: http://dx.doi.org/10.3391/bir.2015.4.1.02 © 2015 The Author(s). Journal compilation © 2015 REABIC Research Article It was only a matter of time: occurrence of Caulerpa taxifolia (Vahl) C. Agardh var. distichophylla (Sonder) Verlaque, Huisman and Procaccini in the Maltese Islands (Chlorophyta, Ulvophyceae, Caulerpaceae) Patrick J. Schembri1*, Jacqueline Barbara1, Alan Deidun2, Edwin Lanfranco3 and Sandro Lanfranco1 1Department of Biology, University of Malta, Msida MSD2080, Malta 2Physical Oceanography Unit, University of Malta, Msida MSD2080, Malta 3Institute of Earth Systems, University of Malta, Msida MSD2080, Malta E-mail: [email protected] (PJS), [email protected] (JB), [email protected] (AD), [email protected] (EL), [email protected] (SL) *Corresponding author Received: 18 August 2014 / Accepted: 24 November 2014 / Published online: 15 December 2014 Handling editor: Darren Yeo Abstract A new alien species of Caulerpa, corresponding morphologically to Caulerpa taxifolia (Vahl) C. Agardh var. distichophylla (Sonder) Verlaque, Huisman and Procaccini, already known from Turkey, Sicily, and Cyprus, was first discovered in Malta in June 2013. The original record was of but a few fronds, and surveys made during winter at the same site did not locate any plants. A survey conducted during July 2014, however, located two patches of the alga occupying a total area of ca 125m2 in the 4–6m depth range, with a mean frond density of 276.3 (± 51.21 SD) per m2. Also in July 2014, two patches with a total of 520 fronds in an area of 0.37m2 at 14–15m depth were found at a second site ca 7.4 km along-coast distance from the first site. The alien algae formed part of a photophilic assemblage growing on rock in clearings adjacent to Posidonia oceanica (Linnaeus) Delile stands. The most likely source of the Maltese populations is Sicily, and the most likely vector is recreational and/or commercial shipping. Key words: alien species, invasive species, Malta, Sicily, Caulerpa cylindracea, photophilic algae, Posidonia oceanica Introduction J.V. Lamouroux, and C. ollivieri Dostál, which may, however, be a dwarf ecotype of C. prolifera The genus Caulerpa within the family Caulerpaceae (UNEP/IUCN/GIS Posidonie 1990). includes coenocytic chlorophytes with stolons In the Mediterranean, Caulerpa achieved great that spread horizontally over the substratum, notoriety when, in 1984, the alien species anchored by means of rhizoids. At intervals, the Caulerpa taxifolia (Vahl) C. Agardh was reported stolons give rise to upright photosynthetic from inshore waters off Monaco, apparently an fronds. The AlgaeBase database currently lists escape from the aquaria of the local Oceanographic some 92 taxonomically valid taxa at specific and Museum (Meinesz and Hesse 1991; Jousson et al. infraspecific level within the genus (Guiry 2014); 1998). From Monaco, this aquarium strain, which however, the taxonomy is confused as a number was subsequently shown to be genetically different of species complexes exist, and some species from the ancestral wild-type native to northeastern have variable morphology that is determined Australia (Meusnier et al. 2004), spread westwards primarily by environmental conditions. The genus (France, Spain, the Balearic Islands) and eastwards has a pan-tropical/pan-subtropical distribution (Italy, Croatia) as well as south to Tunisia with highest species richness in southern (Meinesz et al. 2001). The Tunisian population Australia (Guiry 2014); a few species occur in seems to represent a second, independent, temperate waters including the two indigenous introduction (Meusnier et al. 2004). Dramatically Mediterranean species, C. prolifera (Forsskål) dubbed the ‘killer alga’ by the media because of 9 P.J. Schembri et al. its invasive nature and because of concern about southeast Turkey (Cevik et al. 2007), and a year its potential displacement, or at least degradation, later the same form was recorded from the coasts of indigenous Mediterranean species, especially of Sicily (Cormaci and Furnari 2009; Meinesz et seagrass (Meinesz 1999; see review by Boudou- al. 2010); more recently it has been found in resque et al. 2009), this species gave rise to both Cyprus (Çiçek et al. 2013). Morphological and public interest on the impact of alien species on molecular studies have shown this gracile form native ecosystems, and to scientific research on to be different from the aquarium strain of its origin, ecology and impact as well as on Caulerpa taxifolia, and very close to the Australian methods of control. Paradoxically, the sudden species, Caulerpa distichophylla Sonder (Jongma spread of a second introduced species of et al. 2013); however, molecular analysis of Caulerpa in the early 1990s, Caulerpa racemosa Caulerpa distichophylla and Caulerpa taxifolia (Forrskål) J. Agardh, did not generate much only revealed slight genetic differences between public interest although it was even more invasive the two, leading Jongma et al. (2013) to consider than C. taxifolia, and spread much further and Caulerpa distichophylla as a gracile variety of faster, and it had the potential for as much, if not Caulerpa taxifolia and to propose the name more, environmental impact (Verlaque et al. Caulerpa taxifolia (Vahl) C. Agardh var. 2000; Verlaque et al. 2004; Piazzi et al. 2005; distichophylla (Sonder) Verlaque, Huisman and Klein and Verlaque 2008; Boudouresque et al. Procaccini. 2009). Although Caulerpa racemosa had been Caulerpa taxifolia var. distichophylla appears present in the Mediterranean since the 1920s, to have been introduced into the Mediterranean Verlaque et al. (2000) showed that the invasive from southwestern Australia and, unlike the already strain was different from the previously recorded present aquarium strain of Caulerpa taxifolia, it populations, and Verlaque et al. (2003) eventually seems to be limited by winter temperatures of identified this invasive strain as Caulerpa less than 15ºC (Jongma et al. 2013). Sicily, there- racemosa var. cylindracea (Sonder) Verlaque, fore, seems to represent the westward and northern Huisman and Boudouresque. This taxon was limit of spread of C. t. var. distichophylla recently elevated to specific rank as Caulerpa (Jongma et al. 2013; Musco et al. 2014). Obviously, cylindracea Sonder, on the basis of molecular there are no thermal limits to its spread south- and morphological evidence (Belton et al. 2014). wards and here we record such a range extension The originally present Mediterranean strains of to the Maltese Islands, which now represents the Caulerpa racemosa, referred to by Verlaque et southernmost station for this relatively new alien al. (2000) and subsequent authors as C. racemosa species in the Mediterranean. var. turbinata (J. Agardh) Eubank + var. uvifera We were alerted to the presence of this species (C.Agardh) J. Agardh, and as C. racemosa var. when, during surveys made in the summer of lamourouxii (Turner) Weber-van Bosse f. requienii 2013 to monitor selected invasive alien species, (Montagne) Weber-van Bosse, were respectively including Caulerpa cylindracea, in Maltese marine assigned by Belton et al. (2014) to a species for protected areas (MPAs) (MEPA 2013) as part of which the oldest available name is Caulerpa an IUCN sponsored project (Otero et al. 2013), six chemnitzia (Esper) J. V. Lamouroux, and to fronds of a gracile Caulerpa previously unknown Caulerpa lamourouxii (Turner) C.Agardh, which from the Maltese Islands were collected together was reinstated as a full species. with other algae from a site on the northeast In addition to these taxa, two additional, alien, coast of the island of Malta. species of Caulerpa have been reported from the Mediterranean: Caulerpa mexicana Sonder ex Material and methods Kützing, limited to the coasts of Israel, Lebanon, Syria and Turkey; and C. scalpelliformis (Brown Systematic surveys for the gracile Caulerpa were ex Turner) C. Agardh, with a similar distribution conducted during November 2013, January 2014, but also with isolated records from Egypt and and July 2014 at the site where the original Turkey (Ukabi et al. 2012; Verlaque et al. in specimen of this species was collected in June press). Both C. mexicana and C. scalpelli-formis 2013, the White Rocks area on the northeast are actually species complexes (Belton et al. coast of the island of Malta (Figure 1), as well as 2014) but the Mediterranean strains have not yet in adjacent areas along the same shore. A second been genetically characterised. site at Exiles in Sliema, also on the northeast In 2006, a gracile form of Caulerpa taxifolia coast of the island of Malta and at some 7.4 km was reported from the Gulf of Iskenderun, along-coast distance from the White Rocks site 10 Occurrence of Caulerpa taxifolia var. distichophylla in Malta Specimens of the gracile Caulerpa and the accompanying flora were collected and transported fresh to the laboratory for examination. Underwater photographs were also taken. The morphometry of the specimens was described through measurement of the diagnostic structural features used by Jongma et al. (2013) to characterise specimens from Sicily. The diagnostic features of a sample of specimens from each site were captured in photographs and micrographs and subsequently measured using the Measurement Tool of ImageJ v. 1.46r (Rasband 1997–2012). Voucher specimens of plants from both Maltese sites have been deposited in the herbarium of the Department