On the presence of a species of Batophora J. Agardh, 1854 (Chlorophyta: Dasycladales) in Formentera, Balearic Islands Enric BALLESTEROS SHNB Ballesteros, E. 2020. On the presence of a species of Batophora J. Agardh, 1854 (Chlorophyta: Dasycladales) in Formentera, Balearic Islands. Boll. Soc. Hist. Nat. Balears, 63: 109-117. ISSN 0212-260X. e-ISSN 2444-8192. Palma (Illes Balears). We report on the presence of a species of the genus Batophora in Estany des Peix (Formentera, Balearic Islands). The alga was first detected in spring 2020 when it bloomed in the northern side of the lagoon. According to morphological and reproductive characters the species has been tentatively identified as Batophora occidentalis var. largoensis (J.S. Prince and S. Baker) S. Berger and Kaever ex M.J. Wynne, although genetic confirmation is needed. Shipping seems the most plausible pathway of introduction. The sudden and rapid proliferation of Batophora in Estany SOCIETAT D’HISTÒRIA NATURAL DE LES BALEARS des Peix points to an invasive behaviour of this alga. A future monitoring of the evolution of the invasion is highly recommended. Keywords: Batophora; alien species; Formentera; Balearic Islands; Mediterranean Sea. SOBRE LA PRESÈNCIA D’UNA ESPÈCIE DE BATOPHORA J. AGARDH, 1854 (CHLOROPHYTA: DASYCLADALES) A FORMENTERA, ILLES BALEARS. Donem a conèixer la presència d’una espècie del gènere Batophora a l’Estany des Peix (Formentera, Illes Balears). L’alga ha estat detectada per primera vegada durant la primavera de l’any 2020, quan ha crescut espectacularment a la riba nord de l’estany. En base a caràcters morfològics i reproductius, l’alga ha estat temptativament identificada com a Batophora occidentalis var. largoensis (J.S. Prince i S. Baker) S. Berger i Kaever ex M.J. Wynne, tot i que són necessaris estudis genètics posteriors per a confirmar-ho. El transport involuntari per vaixells sembla la forma més plausible d’introducció. La sobtada i ràpida proliferació de Batophora a l’Estany des Peix apunta cap a un comportament invasor de l’alga. Es recomana el seguiment de l’evolució de la invasió d’aquesta espècie. Paraules clau: Batophora; espècie introduïda; Formentera; Illes Balears; Mediterrània. ENRIC BALLESTEROS: Centre d’Estudis Avançats de Blanes-CSIC, Acc. Cala sant Francesc 14, 17300 Blanes, Girona, Spain. ([email protected]) Recepció del manuscrit: 22-11-2020; revisió acceptada: 2-12-2020; publicació online: 3-12-2020. . Introduction greatest number of introduced species (Boudouresque and Verlaque, 2002a). Macrophytes are a key component of The Mediterranean Sea is a hot spot for Mediterranean coastal habitats as they introduced and invasive marine species provide shelter and food for a wide range of (Galil, 2000; Boudouresque, 2008) and at organisms living on rocky bottoms but also the world scale is the sea harbouring the on seagrass meadows (Boudouresque, 110 Boll. Soc. Hist. Nat. Balears, 63 (2020) 2004; Rodríguez-Prieto et al., 2013). of the lagoon, close to the entrance (38º 43’ Several species of macrophytes have been 56” N, 1º 24’ 51.3” E). Notes regarding the introduced into the Mediterranean, distribution of the previously unnoticed changing the seascape and compromising alga and the accompanying species along a the current functioning of ecosystems when shore length of 150 m were obtained. they become invasive (Boudouresque, Several specimens were photographed 2008). The estimated number of introduced (Olympus TG6 camera) and collected for macrophyte taxa ranges between 80 and later description in the laboratory. 128 according to different authors Specimens were maintained alive and (Boudouresque and Verlaque, 2002a, transported in sealed plastic bags devoid of 2002b; Cormaci et al., 2004; Zenetos et al., water to the laboratory. Once in the lab, 2012), with a high percentage of invasive or specimens were maintained in a close potentially invasive species (Boudouresque circuit seawater aquarium. Description was and Verlaque, 2002b; Zenetos et al., 2010). performed using a Wild M8 Heerbrugg The arrival of new species into the stereomicroscope and a Zeiss Axioplan Mediterranean Sea is worth mentioning light microscope. Photographs were because they can become a nuisance for the obtained using an Olympus TG3 camera. ecosystems they colonize. Even if a Vouchers have been deposited at the complete and successful eradication of an Herbarium of the University of Girona introduced marine species is very unlikely, (HGI 20826). its control is feasible (Boudouresque, 2008) and, therefore, early warnings are Results important. Here we report on an early detection of a green alga into a lagoon During our visit to Estany des Peix, a environment at the island of Formentera species corresponding to the genus (Balearic Islands, Western Mediterranean), Batophora was clearly distinguishable as with the intention of engaging (a) a the dominant species in the northern shores monitoring of its future extension, (b) a of the lagoon, just after the channel that study on its effects in the habitats, and (c) connects the lagoon to the open sea. the assessment of a possible control of the Although we did not make any extensive invasion. survey, our samples were collected close to shore, in the upper infralittoral zone, always Material and Methods above 60 cm depth. Other species were present in the same habitat, such as the The presence of a previously unnoticed, green algae Dasycladus vermicularis dominant alga in the northern shores of (Scopoli) Krasser, Caulerpa prolifera Estany des Peix, a lagoon located in the (Forsskål) J.V. Lamouroux, Acetabularia north-western part of Formentera (Balearic acetabulum (L.) P.C. Silva and several Islands) (38º 43’ 33” N, 1º 24’ 45” E) was species of the genus Cladophora Kützing, communicated by Daisee Aguilera in late the brown algae Padina pavonica (L.) October 2020, after the detection by José Thivy and Dictyota mediterranea Alejandro Figueiras Pérez in May 2020. A (Schiffner) G. Furnari and the red alga visit to the site was performed in November Polysiphonia opaca (C. Agardh) Moris and 6th, 2020. A snorkelling survey was made in De Notaris. the shallowest waters of the northern side E. Ballesteros, Presence of Batophora (Chlorophyta: Dasycladales) in Formentera 111 Fig 1. Habit of the plants growing over rubble Fig. 2. A: Habit of one sterile surrounded by two (A) and dead seagrass leaves of Posidonia fertile stalks; fertile areas are easily noticeable at oceanica (B). the tip of the stalks by its dark green colour. B: Fig. 1. Aspecte de les plantes creixent sobre Close-up of the fertile upper part of the stalk, pedruscall (A) i sobre fulles mortes de Posidonia holding the dark green, spherical gametophores. oceanica (B). Fig. 2. A: Aspecte d’un tal·lus estèril envoltat de dos de fèrtils; les àrees fèrtils són fàcils de The description of the collected distingir pel seu color verd fosc. B: Detall d’una specimens is as follows. Thallus formed by part superior fèrtil amb els gametòfors esfèrics creeping rhizoids and large numbers of de color verd fosc. simple, green to reddish brown, cylindrical stalks arising from them (Fig. 1, A and B). from the proximal to the distant nodes, the Rhizoids are attached to rocks, rubble, terminal 3-5 nodes very thin, hair-like (Fig. decomposing seagrass leaves or any kind of 3A). Whorls separated 0.8-1.2 mm from artificial substrate (ropes, plastic). Stalks each other in the medium part of the stalk, clothed with soft whorls of six to ten lateral more densely packed in the upper and ditrichotomous branchlets, together forming lower layers (0.5 to 0.6 mm between a fuzzy cylinder 5-6 mm in diameter, 40-50 whorls). The basal, older, whorls lose their mm long (Fig. 2A). Main axis of the stalks terminal nodes (mainly in reproductive measure 450 to 600 m in diameter and the stages) in the lower 7-15 mm of the stalk proximal node of the whorl branchlets (Fig. 2A). Reproductive stalks bear densely packed gametangia into spherical to slightly measures 600-700 m long and 140-180 ellipsoidal structures called gametophores m in diameter (Fig. 3A). Each branchlet (Fig. 2B). Gametophores grouped on the forks 6-7 times, decreasing in diameter 112 Boll. Soc. Hist. Nat. Balears, 63 (2020) Fig. 3. A: Cross section of a sterile stalk showing the central main axis holding a whorl of ten lateral ditrichotomous branchlets, swiftly decreasing in diameter from the proximal to the outer nodes, the last ones becoming hair-like. B: Cross section of a fertile stalk with immature gametophores. C: Cross section of a fertile stalk with mature gametophores. Fig. 3. A: Secció transversal d’un tal·lus estèril on es distingeix un eix principal central amb un verticil de deu branques laterals que es divideixen di- o tricotòmicament i que redueixen el seu diàmetre des de les parts proximals a les més externes, les darreres en forma de pèl. B: Secció transversal d’un tal·lus fèrtil amb gametòfors immadurs. C: Secció transversal d’un tal·lus fèrtil amb gametòfors madurs. mature (Fig. 4, B and C). Biflagellate gametes show an elongated convex form and measure 5x12 m. Discussion Two species are currently recognized inside the genus Batophora: B. oerstedii J. Agardh and B. occidentalis (Harvey) S. Berger and Kaever ex M.J. Wynne. There is much confusion regarding the specific characters that allow the distinction between B. oerstedii and B. occidentalis with contrasting features among authors, even in the reproductive characteristics, the only ones valid to make a proper identification of the species (see: Berger and Kaever, 1992; Gómez-Poot et al., upper (1/4) part of the stalk, with the fertile 2002; Qua-Young et al., 2006; Rodríguez- part of the stalk measuring 9 to 11 mm long Reyes et al., 2018). After a thorough (Fig. 2B). Gametophores mostly attached to revision of the literature, it seems that the the distant part of the proximal node of the main diagnostic character that distinguishes whorl branchlets, only exceptionally to the B. oerstedii from B. occidentalis is the second node (Fig. 3, B and C). When fully position of the gametophores, restricted to developed, gametophores are almost the proximal node in B. occidentalis but spherical, (440)-500-600-(650) m present in the proximal but also on the maximum diameter (Fig. 4A). Gametangia second node in B. oerstedii (Bonotto and are spherical, measuring (60)-65-(70), Lüttke, 1980; Berger and Kaever, 1992). exceptionally 80-87m in diameter when This character would unequivocally identi- E. Ballesteros, Presence of Batophora (Chlorophyta: Dasycladales) in Formentera 113 fy the specimens from Estany des Peix as B. occidentalis. However, a third species was described by Prince and Baker (1984a; 1984b): Batophora largoensis. According to Berger and Kaever (1992) B. largoensis and B. occidentalis crossbreeded and gave a new fertile generation, while B. largoensis did not crossbreed with B. oerstedii (Prince and Baker, 1984b); therefore, B. largoensis was transferred to the entity B. occidentalis as a variety (Berger and Kaever, 1992). The specimens collected in Estany des Peix match with the original description of B. largoensis by Prince and Baker (1984a), although the gametangia of the plants collected in Formentera are larger than those reported in the original description (60 to 87 versus 50 m in diameter). Gametophores are also slightly bigger, although in the range of the original description (Prince and Baker, 1984a) and in the ranges provided by other authors (Littler and Littler, 2000; Dawes and Mathieson, 2008; Rodríguez-Reyes et al., 2018). According to the last revision of the genera Batophora by Rodríguez-Reyes et al. (2018), where the three Batophora entities are compared, our specimens correspond to the variety largoensis because the whorled branchlets are completely deciduous only in a small part of the older fertile stalks and because gametophores are spherical, never ovoid as they usually are in B. occidentalis. Thus, the taxa found in Estany des Peix is most likely Batophora occidentalis var. Fig. 4. A: Mature, nearly spherical gameto- largoensis (J.S. Prince and S. Baker) S. phores holding a great number of densely Berger and Kaever ex M.J. Wynne (Wynne, packed gametangia. B: Detail of gametangia 1998). This variety has been reported so far inside a gametophore. C: Two mature from the Gulf of Mexico (Prince and Baker, gametangia. 1984a), the Caribbean Sea (Littler and Fig. 4. Gametòfors madurs, pràcticament Littler, 2000), Cuba (Suárez et al., 2014), esfèrics, amb un gran nombre de gametangis al Martinica (Delnatte and Wynne, 2016) and seu interior. B: Detall dels gametangis a the tropical western Atlantic (Wynne, l’interior d’un gametòfor. C: Dos gametangis 2017). Further genetic analyses are required madurs. 114 Boll. Soc. Hist. Nat. Balears, 63 (2020) to confirm our identification following data. Our new finding of Batophora morphological characters. confirms the existence of this genus in the The benthic assemblage that is being Mediterranean. The origin of introduction colonized by Batophora was characterized of Batophora in Estany des Peix remains by Ballesteros et al. (2008) under the name unknown. Macrophytes are the leading “Lagoonal assemblage of photophilic group of introduced organisms in the algae” and corresponds to the habitat western Mediterranean and their main “Sheltered infralittoral rock, well pathway of introduction is shellfish illuminated, without Fucales, with aquaculture followed by shipping and Dasycladus vermicularis and Acetabularia aquarium trade (Verlaque, 2001; acetabulum” (LPRE code 0301030702) Boudouresque and Verlaque, 2002a, 2012; (Templado et al., 2012; Ballesteros and Zenetos et al., 2012; Galil et al., 2018; Cebrian, 2015; Ballesteros, 2019). This Boudouresque et al., 2020). Since there are habitat closely agrees with the one reported no shellfish farms in Estany des Peix and for Batophora spp. by several authors on Batophora is not used in aquaria, the most the tropical and subtropical Atlantic coasts, likely pathway of introduction is shipping, the Caribbean and the Gulf of Mexico: probably via fouling of adult individuals or quiet waters of lagoons, inlets and estuaries via ballast water transporting gametophores (Taylor, 1960; Gómez-Poot et al., 2002; or gametangia. Formentera is a hot spot for Rodríguez-Reyes et al., 2018). In its native luxury yachting, which has been listed as a distribution area, Batophora spp. also pathway for species introductions (Hewitt grows on submerged roots of mangroves, is et al., 2007; Brine et al., 2013; Cecere et very resistant to desiccation and inhabits al., 2016). Several yachts that overwinter in waters with a large range of salinity and the Caribbean come to the Mediterranean nutrients (Littler and Littler, 2000; Marcano Sea in summer (Gui and Russo, 2011; et al., 2014). Rodrigue and Notteboom, 2012). Even that Outside the tropical and subtropical it is not easy that a delicate alga such as eastern Atlantic and adjacent seas, Batophora can survive the Caribbean- Batophora has been reported from Tenerife Mediterranean transfer, yachting seems the (Canary Islands) and Taranto most plausible explanation for the (Mediterranean Sea). Samples collected in a introduction of Batophora in Estany des tide pool from El Médano, Tenerife (Reyes Peix. et al., 1993) were identified as Batophora Batophora was first detected at the oerstedii var. occidentalis (=Batophora entrance of Estany des Peix by José occidentalis) based only in morphological Alejandro Figueiras Pérez on May 2020. characters of sterile individuals and, thus, The alga has progressed fast towards the identification has to be confirmed. The only inner part of Estany des Peix during Mediterranean record of the genus summer and early autumn. The sudden and Batophora comes from Taranto (Apulia, rapid proliferation of Batophora in Estany Ionian Sea, Central Mediterranean) by des Peix points to an invasive behaviour of Botalico, DelleFoglie and Perrone in the alga. In fact, this lagoon harbours other Cormaci et al. (2004), who found some native Mediterranean algae present also in sterile, unidentified specimens. 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