1 ANNALES · Ser. hist. nat. · 27 · 2017 · 1 short scientifi c article DOI 10.19233/ASHN.2017.01 received: 2016-12-23 UNUSUAL EXPANSION OF LAURENCIA OBTUSA (HUDSON) J.V. LAMOUROUX IN THE ZAMBRATIJA BAY (NORTHERN ADRIATIC SEA) Martina ORLANDO-BONACA Marine Biology Station, National Institute of Biology, SI-6330 Piran, Fornače 41 E-mail: martina.orlando@nib.si Roberto ODORICO SHORELINE Soc.Coop., AREA Science Park, IT-34149 Trieste, Padriciano 99 e-mail: roberto.odorico@shoreline.it ABSTRACT The paper reports an unusual expansion of the red alga Laurencia obtusa in shallow waters of the Zambratija Bay (northern Adriatic Sea). The large population of L. obtusa was never observed during underwater surveys conducted in recent years. In this area, benthic communities dominated by brown algae from the genus Cystoseira were present. The authors therefore assume that some environmental factors have probably changed and have favoured the extension of this red alga. The hypothesis for this phenomenon takes into account the possibility that the establishment of the invasive green alga Caulerpa cylindracea in the Zambratija bay has had a negative impact on native macroalgal assemblages. Key words: Laurencia obtusa, monospecifi c population, Zambratija Bay, Adriatic Sea ESPANSIONE INSOLITA DI LAURENCIA OBTUSA (HUDSON) J.V. LAMOUROUX NELLA BAIA DI ZAMBRATTIA (ADRIATICO SETTENTRIONALE) SINTESI L’articolo riporta un’insolita espansione dell’alga rossa Laurencia obtusa in acque poco profonde della baia di Zambrattia (Adriatico settentrionale). Ampi popolamenti di L. obtusa non sono mai stati osservati durante le indagini subacquee effettuate negli ultimi anni. In quest’area erano presenti comunità bentoniche dominate da alghe brune del genere Cystoseira. Gli autori pertanto suppongono che alcuni fattori ambientali siano cambiati e abbiano favorito l’estensione di quest’alga rossa. L’ipotesi per questo fenomeno prende in considerazione la possibilità che l’insedia- mento dell’alga verde invasiva Caulerpa cylindracea nella baia di Zambrattia abbia avuto un impatto negativo sulle associazioni macroalgali autoctone. Parole chiave: Laurencia obtusa, popolamento monospecifi co, baia di Zambrattia, mare Adriatico 2 ANNALES · Ser. hist. nat. · 27 · 2017 · 1 Martina ORLANDO-BONACA & Roberto ODORICO: UNUSUAL EXPANSION OF LAURENCIA OBTUSA (HUDSON) J.V. LAMOUROUX IN THE ..., 1–6 INTRODUCTION The red alga Laurencia obtusa (Hudson) J.V. Lam- ouroux is commonly found in the Adriatic Sea, from the northern to the central and southern part of the basin (Avčin et al., 1973, 1974; Matjašič et al., 1975; Giaccone, 1978; Munda, 1979; Vukovič, 1980, Gómez Garreta et al., 2001; Antolić et al., 2011; Curiel et al., 2012). The species usually grows on rocky substrata moderately exposed to wave actions in the lower me- diolittoral belt, and with other photophilous taxa in the association Cystoseiretum crinitae Molinier 1958 in the upper infralittoral belt (Giaccone et al., 1994). However, it was found also on rocky outcrops in the lower infralit- toral and circalittoral belts in the northern Adriatic Sea (Curiel et al., 2012). According to the available literature, L. obtusa was never found forming dense and extended monospecifi c populations in the Adriatic Sea. However, dense stands of Laurencia species were reported for the Florida Bay (Zieman et al., 1989) and for the Gulf of Siam in the South China Sea (Latypov, 1986). The aim of the present paper is to report the fi nding of a dense monospecifi c population of L. obtusa in the Zambratija Bay (northern Adriatic Sea) and to discuss the possible factors that led to this phenomenon. MATERIAL AND METHODS The Zambratija Bay is located in the northwestern part of the Istrian peninsula, near Cape Savudrija, in Croatia (Fig. 1). The sea bottom is predominantly rocky, locally mixed sandy-rocky (Sladonja & Banovac-Kuča, 2014). A recent study concerning the reduction of chlorophyll a concentrations in a wider area, consistent with the decrease in concentrations of phosphate and ammonia (Solidoro et al. 2009; Mozetič et al. 2012), underlined the oligotrophication of the whole northern Adriatic basin over the last decade (Mozetič et al. 2010). In September 2016, during a scuba diving survey in the upper-infralittoral belt of the Zambratija Bay, a dense monospecifi c population of L. obtusa were found. The area covered by the species was photographed and fi lmed. Its extension was measured by the use of satellite imagery (Google Earth) and the GIS program Manifold®. Fresh samples were taken to the laboratory of the Marine Biology Station (NIB) in Piran and fi xed in 4% formaldehyde solution. The species identifi cation was made using a stereomicroscope Olympus SZH-ILLK, and a microscope Olympus BX51, and was in accor- dance with Falace et al. (2013) and Rodríguez-Prieto et al. (2013). RESULTS AND DISCUSSION In the middle part of the Zambratija Bay, a dense monospecifi c population of the invasive non-indigenous species Caulerpa cylindracea Sonder was found in 2016, but the record is not new, since the Zambratija Bay is currently considered the northernmost site where the establishment of C. cylindracea was confi rmed earlier (Sladonja & Banovac-Kuča, 2014; Iveša et al., 2015). But at two sites, which can be considered the entrance and the exit points of the bay, a dense monospecifi c population of L. obtusa (Fig. 2) were recorded for the fi rst time. The two sites were characterized by carpets of interwoven thalli of this red alga, where holes made by fi sh species were evident (Fig. 3). In these cavities the presence of blennies was observed, mostly Parablennius tentacularis (Brünnich, 1768) and Parablennius rouxi (Cocco, 1833). The extension of the area covered by L. obtusa was estimated to be about 3215 m2 at site 1 and 11618 m2 at site 2 (Fig. 1), in a depth range from 1.0 m to 2.5 m. When thalli of L. obtusa were manually lifted from the substrate, thalli of Halimeda tuna (J. Ellis & Solander) J.V. Lamouroux were found at the sea bottom. The segments of thalli of this green alga were mostly whitish, which is normal after the release of gametes, when the outer involucres remain light due to the presence of calcium carbonate in cell walls (Lipej et al., 2016). However, in this case the whitish colour of thalli could also be related to the overgrowing by L. obtusa and the consequent reduction of the light that reaches the green alga. Fig. 1: The map of the Zambratija Bay with the sites (1 and 2) where a dense monospecifi c population of Laurencia obtusa were found. Sl. 1: Zemljevid zambratijskega zaliva z označenima lokalitetama (1 in 2), kjer je bila ugotovljena gosta monospecifi čna populacija vrste Laurencia obtusa. 3 ANNALES · Ser. hist. nat. · 27 · 2017 · 1 Martina ORLANDO-BONACA & Roberto ODORICO: UNUSUAL EXPANSION OF LAURENCIA OBTUSA (HUDSON) J.V. LAMOUROUX IN THE ..., 1–6 The wide population of L. obtusa was never ob- served during underwater surveys conducted in recent years. In this area, benthic communities dominated by brown algae from the genus Cystoseira (mainly C. com- pressa (Esper) Gerloff & Nizamuddin)), Padina pavon- ica (Linnaeus) Thivy, and H. tuna were present (pers. obs.). Therefore, we assume that some environmental factors have probably changed and have favoured the extension of this red alga. Our hypothesis for this phenomenon takes into account the possibility that the establishment of the invasive green alga C. cylindracea in the Zambratija bay has had a negative impact on native macroalgal assemblages, as reported by Bulleri et al. (2010). According to Bulleri et al. (2016), the species is able to enhance the competitive ability of algal turfs in respect to canopy-forming and encrusting macroalgae, by the alteration of some abiotic factors, like the en- hanced trapping of sediments. Therefore, the spreading of C. cylindracea in the Zambratija bay, may have led to the disappearance of Cystoseira spp. and other canopy forming macroalgae, with the consequent dense growth of the lower vegetation cover. Such signifi cant changes at the community level may have favoured the unusual formation of monospecifi c stands of L. obtusa. Addition- ally, Bulleri et al. (2016) reported that at pristine sites, the prevention of the re-invasion of C. cylindracea on experimental cleared plots, had favoured the recovery of canopy-forming and encrusting macroalgae. However, in order to test this hypothesis, other sites along the Istrian coast, where the establishment of C. cylindracea was already confi rmed (Sladonja & Banovac-Kuča, 2014; Iveša et al., 2015), should also be surveyed in the nearby future. This is needed to verify all the changes in the composition and density of native macroalgal assemblages. ACKNOWLEDGEMENTS The authors would like to thank dr. Monica Moras and her students Elisabetta Borlina, Antonio Callegaro, Giacomo Cattaruzza, Elena Del Pup, Anthea Isola, Veronica Mariuz, Stefania Mazzega, Francesco Porracin Fig. 2: Details of the apical portion of Laurencia obtusa; scale bar: 5 mm (photo: Martina Orlan- do-Bonaca). Sl. 2: Podrobnosti apikalnega dela vrste Laurencia obtusa; velikostna lestvica: 5 mm (foto: Martina Orlando-Bonaca). 4 ANNALES · Ser. hist. nat. · 27 · 2017 · 1 Martina ORLANDO-BONACA & Roberto ODORICO: UNUSUAL EXPANSION OF LAURENCIA OBTUSA (HUDSON) J.V. LAMOUROUX IN THE ..., 1–6 from the Liceo Scientifi co Vendramini (Pordenone, Italy) that collaborated in the fi eld work during their summer campus. Special thanks go to Milijan Šiško for the prepa- ration of Figure 1, and to two anonymous reviewers for their suggestions and comments. The fi rst author acknowledges the fi nancial support from the Slovenian Research Agency (research core funding No. P1-0237). Fig. 3: A dense monospecifi c population of Laurencia obtusa were found in the Zambratija Bay (northern Adriatic Sea) in September 2016. The holes in the carpet of interwoven thalli were made by fi sh species, mainly blennies (photo: Monica Moras). Sl. 3: Gosta monospecifi čna populacija vrste Laurencia obtusa, opažena v zambratijskem zalivu (severni Jadran) septembra 2016. Rove v preprogi steljk so naredile ribe, predvsem babice (foto: Monica Moras). 5 ANNALES · Ser. hist. nat. · 27 · 2017 · 1 Martina ORLANDO-BONACA & Roberto ODORICO: UNUSUAL EXPANSION OF LAURENCIA OBTUSA (HUDSON) J.V. LAMOUROUX IN THE ..., 1–6 NENAVADNO RAZŠIRJANJE ALGE LAURENCIA OBTUSA (HUDSON) J.V. LAMOUROUX V ZAMBRATIJSKEM ZALIVU (SEVERNI JADRAN) Martina ORLANDO-BONACA Marine Biology Station, National Institute of Biology, SI-6330 Piran, Fornače 41 E-mail: martina.orlando@nib.si Roberto ODORICO SHORELINE Soc.Coop., AREA Science Park, IT-34149 Trieste, Padriciano 99 e-mail: roberto.odorico@shoreline.it POVZETEK Avtorja poročata o nenavadnem razširjanju rdeče alge Laurencia obtusa v plitvinah zambratijskega zaliva (severni Jadran). V zadnjih letih nista nikoli imeli priliko opazovati velike populacije te alge. V tem predelu so prevladovale rjave alge iz rodu Cystoseira. Avtorja domnevata, da so spremembe v okoljskih dejavnikih verjetno spodbudile razširjanje te rdeče alge. Ta hipoteza vključuje možnost, da je do tega pojava prišlo zaradi naselitve invazivne zelene alge Caulerpa cylindracea v zambratijskem zalivu, ki je imela negativen vpliv na samoniklo skupnost makroalg. Ključne besede: Laurencia obtusa, monospecifi čna populacija, zambratijski zaliv, Jadransko morje 6 ANNALES · Ser. hist. nat. · 27 · 2017 · 1 Martina ORLANDO-BONACA & Roberto ODORICO: UNUSUAL EXPANSION OF LAURENCIA OBTUSA (HUDSON) J.V. LAMOUROUX IN THE ..., 1–6 REFERENCES Antolić, B., A. Špan, A. Žuljević, V. Nikolić, I. Grubelić, M. Despalatović & I. Cvitković (2011): A checklist of the benthic marine macroalgae from the eastern Adriatic coast: III. Rhodophyta 1: Ceramiales. Acta Adriatica, 52(1), 67-86. Avčin, A., I. Keržan, L. Kubik, N. Meith-Avčin, J. Štirn, P. Tušnik, T. Valentinčič, B. Vrišer & A. Vukovič (1973): Akvatični ekosistemi v Strunjanskem zalivu I.: preliminarno poročilo. V: Akvatični sistemi v Strun- janskem zalivu I: skupno delo. Prispevki k znanosti o morju. Inštitut za biologijo univerze v Ljubljani, Morska biološka postaja Portorož, 5, 168-216. Avčin, A., N. Meith-Avčin, A. Vukovič & B. Vrišer (1974): Primerjava bentoških združb Strunjanskega in Koprskega zaliva z ozirom na njihove polucijsko pogo- jene razlike. Biol. vestn., 22(2), 171-208. Bulleri, F., D. Balata, I. Bertocci, L. Tamburello & L. Benedetti-Cecchi (2010): The seaweed Caulerpa race- mosa on Mediterranean rocky reefs: from passenger to driver of ecological change. Ecology, 91(8), 2205–2212 DOI 10.1890/09-1857.1. Bulleri, F., F. Badalamenti, L. Iveša, B. Mikac, L. Musco, A. Jaklin, A. Rattray, T. Vega Fernandez & L. Benedetti-Cecchi (2016): The effects of an invasive seaweed on native communities vary along a gradient of land-based human impacts. PeerJ, 4:e1795; DOI 10.7717/peerj.1795. Curiel, D., A. Falace, V. Bandelj, S. Kaleb, C. Solidaro & E. Ballesteros (2012): Species composition and spatial variability of macroalgal assemblages on biogenic reefs in the northern Adriatic Sea. Botanica Marina, 55(6), 625-638. Falace, A., G. Alongi, S. Kaleb & M. Cormaci (2013): Guida illustrata alle alghe del Golfo di Trieste. Daewin Edizioni, Roma, 168 pp. Giaccone, G. (1978): Revisione della fl ora marina del Mare Adriatico. Annuario Parco Marino Miramare, 6(19), 1-118. Giaccone, G., G. Alongi, F. Pizzuto & A.V.L. Cossu (1994): La Vegetazione marina bentonica fotofi la del Mediterraneo, 2: Infralitorale e Circalitorale: proposte di aggiornamento. Bollettino dell’Accademia Gioenia di scienze naturali, 27(346), 111-157. Gómez Garreta, A., T. Gallardo, M.A. Ribera, M. Cormaci, G. Furnari, G. Giaccone & C.-F. Boudouresque (2001): Checklist of the Mediterranean seaweeds. III. Rhodophyceae Rabenh. 1. Ceramiales Oltm. Botanica Marina, 44, 425-460. Iveša, L., T. Djakovac & M. Devescovi (2015): Spreading patterns of the invasive Caulerpa cylindracea Sonder along the west Istrian Coast (northern Adriatic Sea, Croatia). Mar. Environ. Res., 107, 1-7. Latypov, Yu.Ya. (1986): Coral Communities of the Namsu Islands (Gulf of Siam, South China Sea). Mar. Ecol. Progr. Ser., 29, 261–270. Lipej, L., M. Orlando-Bonaca & B. Mavrič (2016): Biogenic formations in the Slovenian sea. Nacionalni inštitut za biologijo, Morska biološka postaja, Piran, 204 pp. Matjašič, J., J. Štirn, A. Avčin, L. Kubik, T. Valentinčič, F. Velkovrh & A. Vukovič (1975): Flora in favna Severne- ga Jadrana, prispevek 1. Slovenska akademija znanosti in umetnosti. Razred za prirodoslovne vede, 54 pp. Mozetič, P., C. Solidoro, G. Cossarini, G. Socal, R. Precali, J. Francé, F. Bianchi, C. De Vittor, N. Smod- laka & S. Fonda Umani (2010): Recent trends towards oligotrophication of the northern Adriatic: evidence from chlorophyll a time series. Estuaries and Coasts, 33, 362-375. Mozetič, P., J. Francé, T. Kogovšek, I. Talaber & A. Malej (2012): Plankton trends and community changes in a coastal sea (northern Adriatic): bottom-up vs. top-down control in relation to environmental drivers. Estuarine, coastal and shelf science, 115, 138-148. Munda, I.M. (1979): Some Fucacean associations from the vicinity of Rovinj, Istrian Coast, Northern Adri- atic. Nova Hedwigia, 31, 607-666. Rodríguez-Prieto, C., E. Ballesteros, F. Boisset, & J. Alfonso-Carrillo (2013): Guía De Las Macroalgas Y Fanerógamas Marinas Del Mediterráneo Occidental. Ediciones OMEGA, Barcelona, 656 pp. Sladonja, B. & V. Banovac-Kuča (2014): New records of Caulerpa cylindracea Sonder (Caulerpales, Chlorophyta) in Istria, Croatia. Annales, Series historia naturalis, 24(2), 115-120. Solidoro, C., M. Bastianini, V. Bandelj, R. Codermatz, G. Cossarini, D. Melaku Canu, E. Ravagnan, S. Salon & S. Trevisani (2009): Current state, scales of variability, and trends of biogeochemical properties in the northern Adriatic Sea. Journal of Geophysical Research, 114, C07S91, doi: 10.1029/2008JC004838. Vukovič, A. (1980): Asociacije morskih bentoških alg v Piranskem zalivu. Biol. vestn., 28(2), 103-124. Zieman, J.C., J.W. Fourqurean & R.L. Iverson (1989): Distribution, abundance and productivity of seagrasses and macroalgae in Florida bay. Bulletin of marine sci- ence, 44 (1), 292-311.