The marine benthic flora of Cyprus remains poorly explored, as only a few studies have been carried out until today. Den Hartog (1972) was the first to report a marine plant from Cyprus, the Lessepsian seagrass Halophila stipulacea (Forsskål) Ascherson, followed by Lipkin (1975), who also focused on seagrasses of the island. Prud’homme van Reine (1982) reported two brown algal species [Sphacelaria rigidula Kützing and Sphacelaria cirrosa (Roth) C. Agardh] from Cape Pyla. A more detailed study was provided by Cirik et al. (2000), who included numerous marine plant records from the northern coasts. Taşkın et al. (2008) published a list of alien algae of the northern coasts of the island. More recently, the same authors provided a detailed catalog of seaweeds from the northern coasts (Taşkın et al. 2013). Later on, two alien green algae – Caulerpa racemosa and Caulerpa taxifolia var. distichophylla – were also recorded from the Cypriot coasts (Argyrou et al. 1999, 2003, Çiçek et al. 2013; Aplikioti, personal communication). Finally, scattered records of marine plants from Cyprus can also be found in a few studies dealing either with other groups of marine biota (Hadjichristophorou et al. 1997, Russo 1997, Katsanevakis et al. 2009) or with the use of macroalgae as bioindicators (Stavrou and Orfanidis 2012). All these studies cover only a fraction of the total coastline and different habitats of Cyprus, which is mostly due to the unresolved political situation prevailing over almost four decades, constituting a significant obstacle to more comprehensive marine biodiversity studies and conservation efforts for the island’s inshore marine communities.
Over the last decade, numerous surveys of marine plants of Cyprus have been conducted by the authors, within the framework of the TOTAL Foundation-sponsored project “Brown algal biodiversity and ecology in the Eastern Mediterranean Sea”, the implementation of the Water Framework directive (WFD, 2000/60/EC), and via personal collections. In this paper, we provide a comprehensive and updated checklist of green, brown, and red macroalgae of the island based on both literature data and personal collections.
Materials and methods
The study areas
Field work was performed at several coastal sites around Cyprus (Figure 1): in the years 2003–2004 at Akamas (35°2′32.60″N/32°16′35.60″E) and Liopetri (34°57′38.70″N/ 33°53′50.51″E); in summer 2007 and 2008 at Liopetri; in spring 2012 at Akamas, Cavo Greco (34°57′39.47″N/ 34°4′50.12″E), Famagusta (35°10′N/33°55′E), Karpasia (35°41′N/34°35′E), Kyrenia (35°20′N/33°17′E), Liopetri and Varosha (35°07′22″N/33°57′26″E), and in late summer 2013 at Zenobia wreck (34°53′6″N/33°39′5″E) and northern Akamas (35°04′N°/32°19′E). Sampling was carried out by free diving in rocky midlittoral and upper sublittoral levels (0–3 m depth) and by scuba diving down to 42 m depth. All specimens were collected by destructive sampling (picking or scraping the macroalgae off the substratum). The material collected was preserved in 4% buffered formalin/seawater and/or mounted on Bristol paper, pressed, air dried, and prepared as herbarium specimens.
In the laboratory, specimens were observed under dissecting or compound microscopes. When necessary, they were sectioned manually with a razor blade. In several cases, permanent material was prepared as microscope slides using Karo™ corn syrup (ACH Food Companies, Memphis, TN, USA). Herbarium specimens have been deposited in the East Mediterranean Seaweed Herbarium at the Department of Botany, Faculty of Biology, University of Athens (Greece), and in the seaweed herbarium at the Faculty of Arts and Sciences, Department of Biology, Celal Bayar University (Manisa, Turkey). For nomenclature purposes, the following taxonomic databases were used: Index Nominum Algarum (Silva 2014) and AlgaeBase (Guiry and Guiry 2014).
Reference sources used
Marine macroalgal taxa reported in scientific journals and conference proceedings have been critically reviewed from present-day taxonomic and nomenclatural aspects, taking into account the on-line data provided by Silva (2014) and Guiry and Guiry (2014). On the other hand, technical reports, Bachelor and Master dissertations have not been considered here as they lack a rigorous peer review process in their preparation.
All taxa have been grouped in four categories: accepted, pending confirmation of their presence, excludenda, and inquirenda. Taxa are listed alphabetically for each group (green, brown, red algae) in order to make their detection easier. The locations at which each taxon was found in the present study are given. Previous literature records are also provided for each taxon.
In total, 151 marine macroalgae were identified from all of our sampling expeditions (Table 1), including 30 green algae (Ulvophyceae), 53 brown algae (Phaeophyceae), and 68 red algae (Rhodophyta). Among our collections, 7 green, 9 brown, and 14 red macroalgae are reported for the first time from Cyprus, raising the total number of seaweed species recorded in Cyprus to 313 taxa (53 green, 90 brown, and 170 red algae – see Table 1).
Taxa pending confirmation of their presence
Aglaothamnion pseudobyssoides (P.L. Crouan et H.M. Crouan) Halos
The single record by Taşkın et al. (2013), which lacks description or illustration, should be confirmed as this species is not known to occur elsewhere in the Mediterranean Sea.
Botryocladia skottsbergii (Børgesen) Levring
In the absence of a detailed description, the single record by Taşkın et al. (2013) should be confirmed, as this species is not known to occur in the Mediterranean Sea.
Centroceras clavulatum (C. Agardh) Montagne
According to Won et al. (2009), Mediterranean records of Centroceras clavulatum are misidentifications of Centroceras gasparrinii (Meneghini) Kützing and/or Centroceras micracanthum Kützing, while Centroceras clavulatum is restricted to the Pacific Ocean. Consequently, the Cypriot records of Centroceras clavulatum by Cirik et al. (2000) and Taşkın et al. (2013) most probably belong to another taxon and require re-examination.
Ceramium cupulatum Womersley
This species does not occur in the Mediterranean Sea and the single record by Taşkın et al. (2013) from Cyprus should be confirmed as neither description nor illustration was provided.
Cladophora patentiramea (Montagne) Kützing
This green alga was reported by Argyrou (2000) from southern Cyprus based on a doubtful identification. However, according to Hoek et al. (2000) Cladophora patentiramea could represent calm-water plants of Cladophora coelothrix, while according to Kraft (2007: 85) C. patentiramea should belong to a highly variable species complex with imprecise taxonomic distinctions.
Codium tomentosum Stackhouse
This species does not seem to occur in the Eastern Mediterranean Sea (Furnari et al. 1999), and we agree with Athanasiadis (1987) that numerous records of Codium tomentosum are probably misidentifications of Codium vermilara (Olivi) Delle Chiaje. Therefore, the single Cypriot record by Cirik et al. (2000) should be treated as debatable, pending new documented records.
Colpomenia peregrina Sauvageau
A small thallus was encountered during our samplings at the upper rocky sublittoral zone in Cavo Greco in 2012. Owing to the lack of reproductive structures we prefer to cite our specimen with reservations.
Gayliella taylorii (E.Y. Dawson) T.O. Cho et S.M. Boo
Taking into account the revision of the newly erected genus Gayliella T. O. Cho, L. McIvor et S. M. Boo (Cho et al. 2008), the single Cypriot record by Cirik et al. (2000); as Ceramium taylorii E.Y. Dawson) should be re-examined.
Polysiphonia kampsaxii Børgesen
The single record by Cirik et al. (2000) should be confirmed as the occurrence of this species in the Mediterranean is doubtful (Gómez Garreta et al. 2001).
Ulva lactuca Linnaeus
Despite numerous Mediterranean records, including the Cypriot ones (Russo 1997, Taşkın et al. 2013), its occurrence in the Mediterranean Sea needs to be confirmed (Gallardo et al. 1993). It should be noted that the molecular identity of the holotype does not match that of N. European specimens that have since been assigned to this binomial (Butler 2007). Molecular analyses by Wolf et al. (2012) mention that old specimens from the Adriatic Sea should be assigned to Ulva rigida.
Anadyomene rhizoidifera A.B. Joly et S. Pereira
In the absence of description and illustrations, the record by Cirik et al. (2000) should be excluded from the Cypriot flora, as this species does not occur elsewhere in the Mediterranean Sea.
Griffithsia devoniensis Harvey
The single record by Cirik et al. (2000) should be excluded as the occurrence of this North Atlantic species in the Mediterranean Sea is rather doubtful (Gómez Garreta et al. 2001).
Uronema confervicola Lagerheim
Reported by Cirik et al. (2000), this freshwater green alga should be excluded from the marine flora of Cyprus.
Caulerpa racemosa var. turbinata (J. Agardh) Eubank – uvifera (C. Agardh) J. Agardh
Caulerpa racemosa var. turbinata (J. Agardh) Eubank is currently considered as a synonym of Caulerpa chemnitzia (Esper) J.V. Lamouroux, while C. racemosa var. uvifera (C. Agardh) J. Agardh is currently considered as a synonym of C. racemosa (Forsskål) J. Agardh (Belton et al. 2014). Thus, we state that the taxon C. racemosa var. turbinata (J. Agardh) Eubank – uvifera (C. Agardh) J. Agardh, reported from Cyprus by Verlaque et al. (2000), should be considered as taxon inquirendum.
Laurencia obtusa var. laxa (Turner) Ardissone and Laurencia papillosa var. subsecunda Kützing
Both reported by Cirik et al. (2000) but without description and illustrations, are both uncertain records, while their taxonomic identity should be clarified.
In total, nine marine benthic algae of Cyprus are currently considered as alien species, including three green algae, one brown alga, and five red algae (Table 1). Among them, Hypnea spinella is reported for the first time from Cyprus.
Cirik et al. (2000) reported 135 taxa of marine seaweeds at specific and infraspecific level from Cyprus northern coasts. Later on, Taşkın et al. (2013) cited 242 seaweeds, again from the northern coasts of Cyprus. The 30 new taxa reported in the present study, combined with the aggregation and revision of all literature records concerning the seaweeds of Cyprus as a whole, raise the total number of Cyprus seaweeds recorded to 313 taxa (53 green, 90 brown, and 170 red algae). Still, there is no doubt that this number is an underestimate, as most parts of the island and particularly the deeper parts of the euphotic benthos remain totally unexplored. Also, nothing is known about fungal, oomycete, and other eukaryotic pathogens of seaweeds in Cyprus waters, despite their likely considerable ecological impact – a recent survey in the Aegean Sea (the area closest to Cyprus where such work has been conducted) has resulted in records of Eurychasma dicksonii (E.P. Wright) Magnus, Anisolpidium sphacellarum (Kny) Karling and Anisolpidium ectocarpii Karling in a region previously totally unexplored in this respect (Strittmatter et al. 2013). Therefore, additional surveys are crucial for further exploration of the marine benthic flora of Cyprus.
We are grateful to Paraskevi Louizidou and Savvas Michailides for sampling assistance and to Konstantina Kafa for producing the map of Cyprus with the sampling localities. We are also indebted to the Total Foundation (Paris) for its support to this study. We also wish to thank Erol Adalıer and the Deep Dive Diving Center for sampling assistance. Special thanks are due to Kate Clerides for providing support to this consortium of marine scientists and phycologists, enabling them to conduct and publish this study.
Argyrou, M. 2000. The “Cladophora” phenomenon in the coastal waters of Cyprus. In: (United Nations Environment Programme, ed.) Proceedings of the First Mediterranean Symposium on Marine Vegetation. Regional Activity Centre for Specially Protected Areas, Ajaccio, France. pp. 69–73.Google Scholar
Argyrou, M., A. Demetropoulos and M. Hadjichristophorou. 1999. Expansion of the macroalga Caulerpa racemosa and changes in soft bottom macrofaunal assemblages in Moni bay, Cyprus. Oceanologica Acta 22: 517–528.CrossrefGoogle Scholar
Argyrou, M., J.T. Bayle, C. Rais, A.A. Ramos-Espla, P. Sanchez-Jerez and C. Valle. 2003. Marine vegetation assemblages and benthic bionomy in Cyprus. In: (United Nations Environment Programme, ed.) Proceedings of the Second Mediterranean Symposium on Marine Vegetation. Regional Activity Centre for Specially Protected Areas, Athens, Greece. pp. 229.Google Scholar
Athanasiadis, A. 1987. A survey of the seaweeds of the Aegean Sea with taxonomic studies on species of the tribe Antithamnieae (Rhodophyta). PhD Thesis. University of Göteborg, Sweden. pp. 174.Google Scholar
Belton, G.S., W.F. Prud’homme van Reine, J.M. Huisman, S.G.A. Draisma and C.F.D. Gurge. 2014. Resolving phenotypic plasticity and species designation in the morphologically challenging Caulerpa racemosa-peltata complex (Chlorophyta, Caulerpaceae). J. Phycol. 50: 32–54.CrossrefGoogle Scholar
Cho, T.O., S.M. Boo, M.H. Hommersand, C.A. Maggs, L.J. McIvor and S. Fredericq. 2008. Gayliella gen. nov. in the tribe Ceramieae (Ceramiaceae, Rhodophyta) based on molecular and morphological evidence. J. Phycol. 44: 721–738.Web of ScienceCrossrefGoogle Scholar
Çiçek B.A., O. Kurt, E. Taşkın and M. Öztürk. 2013. First report of Caulerpa taxifolia var. distichophylla (Sonder) Verlaque, Huisman and Procaccini (Caulerpaceae, Chlorophyta) from Northern Cyprus. In: (CIESM Ed.), Proceedings of the 40th CIESM Congress. Marseille, France (in press).Google Scholar
Cirik S., V. Aysel, H.A. Benli, B. Cihangir and A. Ünlüoglu. 2000. Preliminary studies on the marine vegetation of northern Cyprus. TrJFAS 6: 31–40.Google Scholar
Den Hartog, C. 1972. Range extension of Halophila stipulacea (Hydrocharitaceae) in the Mediterranean. Blumea 20: 154.Google Scholar
Furnari, G., M. Cormaci and D. Serio. 1999. Catalogue of the benthic marine macroalgae of the Italian coast of the Adriatic Sea. Bocconea 12: 1–214.Google Scholar
Gallardo, T., A. Gómez Garreta, M.A. Ribera, M. Cormaci, G. Furnari, G. Giaccone and C.F. Boudouresque. 1993. Check-list of Mediterranean Seaweeds, II. Chlorophyceae Wille s.l. Bot. Mar. 36: 399–421.Google Scholar
Gómez Garreta, A., T. Gallardo, M.A. Ribera, M. Cormaci, G. Furnari, G. Giaccone and C.F. Boudouresque. 2001. Check-list of Mediterranean Seaweed. III. Rhodophyceae Rabenh. 1. Ceramiales Oltm. Bot. Mar. 44: 425–460.Google Scholar
Guiry, M.D. and G.M. Guiry. 2014. AlgaeBase. World-wide electronic publication, National University of Ireland, Galway. http://www.algaebase.org; searched on 5 March 2014.
Hadjichristophorou, M., M. Argyrou, A. Demetropoulos and T.S. Bianchi. 1997. A species list of the sublittoral soft-bottom macrobenthos of Cyprus. Acta Adriat. 38: 3–32.Google Scholar
Hoek, C., M. van den and M. Chihara. 2000. A taxonomic revision of the species of Cladophora (Chlorophyta) along the coasts of Japan and the Russian Far-east. Nat. Sci. Mus. [Tokyo] Monogr. 19: 1–242.Google Scholar
Katsanevakis, S., K. Tsiamis, G. Ioannou, N. Michailidis and A. Zenetos. 2009. Inventory of alien marine species of Cyprus. Mediterranean Marine Science 10: 109–133.Google Scholar
Kraft, G.T. 2007. Algae of Australia. Marine benthic algae of Lord Howe Island and the southern Great Barrier Reef, 1. Green algae. Australian Biological Resources Study and CSIRO Publishing: Canberra and Melbourne, pp. 347.Google Scholar
Lipkin, Y. 1975. Halophila stipulacea in Cyprus and Rhodes, 1967–1970. Aquat. Bot. 1: 309–320.Google Scholar
Müller, K.M., K.M. Cole and R.G. Sheath. 2003. Systematics of Bangia (Bangiales, Rhodophyta) in North America. II. Biogeographical trends in karyology: chromosome numbers and linkage with gene sequence phylogenetic trees. Phycologia 42: 209–219.CrossrefGoogle Scholar
Prud’homme van Reine, W.F. (1982). A taxonomic revision of the European Sphacelariaceae (Sphacelariales, Phaeophyceae). Leiden Botanical Series 6: [i-x], 1–293, 660 figs, XXI tables, 6 plates.Google Scholar
Silva, P.C. 2014. Index Nominum Algarum, University Herbarium, University of California, Berkeley. http://ucjeps.berkeley.edu/INA.html, searched on 5 March 2014.
Stavrou, P. and S. Orfanidis S. 2012. Monitoring of macroalgae communities across anthropogenic pressure gradient in Cyprus coasts for Water Framework Directive (2000/60/EC). In: (Hellenic Centre for Marine Research, ed.) Proceedings of the 10th Panhellenic Symposium of Oceanography and Fisheries. Athens, Greece, p. 215.Google Scholar
Strittmatter M., D.G. Müller, C.M.M. Gachon, D.G. Müller, J. Kleinteich, S. Heesch, A. Tsirigoti, C. Katsaros, M. Kostopoulou and F.C. Küpper. 2013. Intracellular eukaryotic pathogens in brown algae in the Eastern Mediterranean Sea, including LSU rRNA data for the oomycete Eurychasma dicksonii. Dis. Aquat. Organ. 104: 1–11.Web of ScienceCrossrefGoogle Scholar
Taşkın, E., M. Öztürk and O. Kurt. 2008. Alien and invasive marine plants of North Cyprus. In: (Çiçek BA, Oniz H, eds.) Proceedings of the 2nd International Symposium on Underwater Research. Eastern Mediterranean University, Famagusta, TRN Cyprus, March 2008, pp. 20.Google Scholar
Taşkın, E., O. Kurt, M. Cormaci, G. Furnari and M. Öztürk. 2010. Two brown algae from the eastern Mediterranean Sea: Microcoryne ocellata Strömfelt and Corynophlaea flaccida (C. Agardh) Kützing. Fresen. Environ. Bull. 19: 892–896.Google Scholar
Taşkın E., M. Öztürk, O. Kurt and S. Ulcay. 2013. Benthic marine algae in Northern Cyprus (Eastern Mediterranean Sea). J. Black Sea/Mediterranean Environment 19: 143–161.Google Scholar
Verlaque M. and C.F. Boudouresque. 1991. Stypopodium schimperi (Buchinger ex Kützing) Boudouresque et Verlaque comb. nov. (Dictyotales, Fucophyceae), algue de Mer Rouge récemment apparue en Méditerranée. Cryptogamie, Algologie 12: 195–211.Google Scholar
Verlaque M., C.F. Boudouresque, A. Meinesz and V. Gravez. 2000. The Caulerpa racemosa complex (Caulerpales, Ulvophyceae) in the Mediterranean Sea. Bot. Mar. 43: 49–68.Google Scholar
Verlaque M., C. Durand, J.M. Huisman, C.F. Boudouresque and Y. Le Parco. 2003. On the identity and origin of the Mediterranean invasive Caulerpa racemosa (Caulerpales, Chlorophyta). Eur. J. Phycol. 38: 325–339.CrossrefGoogle Scholar
Wolf, M.A., K. Sciuto, C. Andreoli and I. Moro. 2012. Ulva (Chlorophyta, Ulvales) biodiversity in the North Adriatic Sea (Mediterranean, Italy): cryptic species and new introductions. J. Phycol. 48: 1510–1521.Web of ScienceCrossrefGoogle Scholar
Won, B.Y., T.O. Cho and S. Fredericq. 2009. Morphological and molecular characterization of species of the genus Centroceras (Ceramiaceae, Ceramiales), including two new species. J. Phycol. 45: 227–250.CrossrefGoogle Scholar