Cyanobacteria of Greece: an annotated checklist

Spyros Gkelis; Iordanis Ourailidis; Manthos Panou; Nikos Pappas

doi:10.3897/BDJ.4.e10084

Biodiversity Data Journal : Taxonomic Paper

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Taxonomic Paper

Cyanobacteria of Greece: an annotated checklist

Spyros Gkelis^‡, Iordanis Ourailidis^‡, Manthos Panou^‡, Nikos Pappas^‡

‡ Department of Botany, School of Biology, Aristotle University of Thessaloniki, Thessaloniki, Greece

Corresponding author:

Academic editor: Vasilis Gerovasileiou

Received: 04 Aug 2016 | Accepted: 24 Aug 2016 | Published: 01 Nov 2016

This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Citation: Gkelis S, Ourailidis I, Panou M, Pappas N (2016) Cyanobacteria of Greece: an annotated checklist. Biodiversity Data Journal 4: e10084. https://doi.org/10.3897/BDJ.4.e10084

Abstract

Background

The checklist of Greek Cyanobacteria was created in the framework of the Greek Taxon Information System (GTIS), an initiative of the LifeWatchGreece Research Infrastructure (ESFRI) that has resumed efforts to compile a complete checklist of species reported from Greece. This list was created from exhaustive search of the scientific literature of the last 60 years. All records of taxa known to occur in Greece were taxonomically updated.

New information

The checklist of Greek Cyanobacteria comprises 543 species, classified in 130 genera, 41 families, and 8 orders. The orders Synechococcales and Oscillatoriales have the highest number of species (158 and 153 species, respectively), whereas these two orders along with Nostocales and Chroococcales cover 93% of the known Greek cyanobacteria species. It is worth mentioning that 18 species have been initially described from Greek habitats. The marine epilithic Ammatoidea aegea described from Saronikos Gulf is considered endemic to this area. Our bibliographic review shows that Greece hosts a high diversity of cyanobacteria, suggesting that the Mediterranean area is also a hot spot for microbes.

Keywords

blue-green algae, Cyanophyceae, bacteria, microorganisms, Aegean Sea, freshwater, marine, checklist, biodiversity, Mediterranean

Introduction

The history of natural science is directly linked to Greek civilization, since the older written references to plants, animals, and algae are found in the Homeric Epics dating back to the 8^th century BC; the first record of algae in the Western literature appears in Homer’s Iliad: “the dark waves uprear their heads and scatter their sea-wrack (phycos) in all directions” [Iliad IX.1 translated by Batler (1998)]. The Greek philosopher, and first marine biologist, Aristotle, who has established scientific knowledge for many animal and plant taxa (see Voultsiadou 2007) reported “red snow” in 4^th century BC: “after lying for some time, snow turns slightly red” (Historia Animalium 552b8 translated by Peck 1970); this is considered as one of the oldest records of snow algae [unicellular Chlorophyta, like Chlamydomonas or Chloromonas according to Duval et al. (1999)].

In modern times, research on Greek microflora, Cyanobacteria included, started in the 20^th century with the studies of freshwater algae by Stanković (1931) and Skuja (1937). In the subsequent two decades, no published work in microflora can be traced until the limnological survey by Ananiadis (1956). During the 1960s Konstantinos Anagnostidis performs two extensive studies of Cyanobacteria from thermal springs (Anagnostidis 1961) and sulphur-communities (Sulphuretum) in marine and freshwater habitats of Greece (Anagnostidis 1968). These taxonomic studies revealed the occurrence of a great number of cyanobacteria taxa, led to the description of several new species (e.g. Geitlerinema apolloniae Anagnostidis, 2001; Leptolyngbya phormidioides (Anagnostidis) Anagnostidis & Komárek, 1988; Pseudanabaena lonchoides Anagnostidis, 1961; Pseudophormidium battersii (Gomont) Anagnostidis, 2001; Borzia periklei Anagnostidis in (Anagnostidis and Komárek 1988)), and were later widely used to establish the modern classification system of Cyanobacteria (Anagnostidis and Komárek 1985, Anagnostidis and Komárek 1988, Anagnostidis and Komárek 1990, Komárek and Anagnostidis 1986, Komárek and Anagnostidis 1989). Although a lot of the valuable taxonomic, ecological, and biogeographical information recorded in Anagnostidis' monographs is now contained in the “Süsswasserflora von Mitteleuropa” series (Komárek 2013, Komárek and Anagnostidis 1999, Komárek and Anagnostidis 2005, Komárek 2013), many details of his work remain unavailable to the broader scientific community since they were published in Greek.

The systematic research on Greek Cyanobacteria started in the 1980s with a series of publications on cyanobacterial taxonomy and species composition (Anagnostidis and Economou-Amilli 1978, Anagnostidis and Economou–Amilli 1980, Anagnostidis et al. 1981, Anagnostidis et al. 1982, Overbeck et al. 1982, Anagnostidis et al. 1983, Anagnostidis and Pantazidou 1985, Anagnostidis and Pantazidou 1988a, Anagnostidis and Pantazidou 1988b, Anagnostidis and Pantazidou 1988c, Hindak and Moustaka 1988, Anagnostidis et al. 1988a, Anagnostidis and Pantazidou 1991a, Anagnostidis and Pantazidou 1991b, Anagnostidis and Roussomoustakaki 1991, Tryfon 1996), as well as on population dynamics (Moustaka-Gouni 1988, Moustaka-Gouni and Nikolaidis 1990, Moustaka-Gouni and Nikolaidis 1992, Tafas and Economou-Amilli 1997, Tryfon et al. 1997, Montesanto et al. 1999, Moustaka-Gouni et al. 2000, Temponeras et al. 2000, Vardaka et al. 2000) regarding both the freshwater and marine waterbodies. The recent research on cyanobacterial diversity in Greece comprises polyphasic or multidisciplinary studies of cyanobacteria strains (Gkelis et al. 2005b, Lamprinou et al. 2011, Lamprinou et al. 2013a, Lamprinou et al. 2013b, Gkelis et al. 2015b, Gkelis and Panou 2016, Bravakos et al. 2016), natural populations (Moustaka-Gouni et al. 2009, Moustaka-Gouni et al. 2010, Papadimitriou et al. 2013, Gkelis and Zaoutsos 2014, Gkelis et al. 2014, Gkelis et al. 2015a), as well as ecological works (e.g. Lamprinou et al. 2009, Katsiapi et al. 2011, Katsiapi et al. 2012).

Despite the increased research efforts, knowledge of diversity and distribution of Cyanobacteria in Greece is still inconsistent since no list on local cyanobacterial flora has ever been published. Modern biodiversity research faces an ever increasing rate of data generation and efforts are made to structure, aggregate, link and process these data in a meaningful way (Koureas et al. 2016). Currently, the Greek Taxon Information System (GTIS), an initiative launched by the LifeWatchGreece Research Infrastructure (ESFRI), is resuming efforts to compile a database of all species reported from Greece; a prerequisite for GTIS is to have checklists for each taxonomic group (Bailly et al. 2016). The aim of this study is to create a checklist of cyanobacterial taxa inhabiting the area of Greece on the basis of the recent taxonomic revisions.

Materials and methods

The Checklist of Greek Cyanobacteria was created in the framework of the Greek Taxon Information System (GTIS), an initiative of the LifeWatchGreece Research Infrastructure (ESFRI) that has resumed efforts to compile a complete checklist of all species reported from Greece (Bailly et al. 2016). In that publication, a methodology is described to produce Preliminary Checklists only. However, in the present case of Cyanobacteria, the status of the list for Greece was quite advanced, and the recent primary literature was exhaustively searched for this work; the present list is thus considered as an updated, annotated, and archived checklist.

The data for this study were collected through extensive search in the scientific literature of the last 60 years. The search was performed in Scopus and Web of Science using the keywords: Greece AND cyanobacteria, Greece AND phytoplankton, Greece AND cyanoprokaryota, Greece AND blue-green algae. Furthermore, the two exhaustive monographs by Anagnostidis (Anagnostidis 1961, Anagnostidis 1968) were studied and the cyanobacterial taxa were recorded. All geographical areas of Greece and all biomes (freshwater, marine, terrestrial, caves etc.) and biotic forms (planktic, benthic, periphytic, endolithic, epizoic etc.) were considered.

The taxonomic status of the recorded cyanobacterial taxa was checked and updated, where necessary, to the currently accepted taxonomically species using Komárek and Anagnostidis (1999), Komárek and Anagnostidis (2005), Komárek (2013), and the AlgaeBase (Guiry and Guiry 2016). The species were classified to suprageneric taxa according to the latest taxonomic revisions on the basis of polyphasic methods (Komárek et al. 2014, Komárek 2016). Not valid species, species of unclear taxonomic status, and species transferred to other phyla were excluded from the list. Also, infraspecific taxa that are not valid or need revision were not included in the list. The first publication mentioning a taxon's occurrence in Greece and the original name used in that record is given under Notes and Nomeclature, respectively.

Data resources

Notes:

Notes:

Xenococcus schousboei Thuret in Bornet & Thuret, 1880

Nomenclature:

Xenococcus schousboei

Notes:

Anagnostidis and Golubic 1966

Xenotholos kerneri (Hansgirg) M. Gold-Morgan, G. Montejano & J. Komárek, 1994

Nomenclature:

Xenococcus kerneri

Notes:

Anagnostidis and Golubic 1966

Yonedaella lithophila (Ercegovic) Umezaki, 1962

Nomenclature:

Sphaeronema lithophilum

Notes:

Anagnostidis 1968

Analysis

A total of 543 species and 85 infraspecific taxa have been found in Greece up to date. The species are classified in 130 genera, 41 families, and 8 orders. The orders Synechococcales and Oscillatoriales have the highest number of species (158 and 153 species, respectively), whereas these two orders along with Nostocales and Chroococcales cover 93% of the known Greek cyanobacteria species (Fig. 1). The families Oscillatoriaceae, Leptolyngbyaceae, Microcoleaceae, and Chroococcaceae have the highest number of species (>30 each) (Fig. 2a); the genera Phormidium, Leptolyngbya, Oscillatoria, Chroococcus, Aphanocapsa, and Gloeocapsa have the highest number of species (>15 each) (Fig. 2b). Fourteen species were found to include 85 infraspecific taxa (Table 1); those infraspecific taxa were not included in the checklist. Furthermore, 21 species recorded in Greece are not valid or of uncertain taxonomic status (Table 2) and were not included in the checklist.

Table 1.

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List of infraspecific cyanobacterial taxa known to occur in Greece. For each taxon the first publication mentioning its occurrence in Greece is given.

Species	Infraspecific epithet	Reference
Anabaena torulosa	var. tenuis	Anagnostidis 1961
Anabaena oscillarioides	fa. circinalis	Anagnostidis 1968
Aphanothece microscopica	fa. endophytica	Anagnostidis 1968
Entophysalis deusta	st. solentioides	Anagnostidis 1968
	st. dermatocarpoides	Anagnostidis 1968
	st. dermocarpoides	Anagnostidis 1968
	st. gloeocapsoides	Anagnostidis 1968
	st. hormathonematoides	Anagnostidis 1968
	st. hyelloides	Anagnostidis 1968
	st. pleurocapsoides	Anagnostidis 1968
	st. tryponematoides	Anagnostidis 1968
	st. typicus	Anagnostidis 1968
Gloeocapsa biformis	st. derm. col. ralfsianus	Anagnostidis 1968
	st. derm. magma	Anagnostidis 1968
	st. dermochrous	Anagnostidis 1968
	st. nannocytosus	Anagnostidis 1968
	st. perdurans	Anagnostidis 1968
	st. punctatus	Anagnostidis 1968
Gloeocapsa compacta	st. perdurans	Anagnostidis 1968
	st. lam. col. magma	Anagnostidis 1968
	st. lam. col. typicus	Anagnostidis 1968
	st. lam. coloratus	Anagnostidis 1968
	st. nannocytosus	Anagnostidis 1968
	st. perdurans	Anagnostidis 1968
	st. simplex	Anagnostidis 1968
Gloeocapsa kützingiana	st. lam. col. magma	Anagnostidis 1968
	st. lam. coloratus	Anagnostidis 1968
	st. perdurans	Anagnostidis 1968
	st. rupestris	Anagnostidis 1968
Gloeocapsa sanguinea	st. col. alp. magma	Anagnostidis 1968
	st. col. alp. ralfsianus	Anagnostidis 1968
	st. col. ralfsianus	Anagnostidis 1968
	st. lam. col. alp. magma	Anagnostidis 1968
	st. lam. col. alpinus	Anagnostidis 1968
	st. lam. col. magma	Anagnostidis 1968
	st. lam. coloratus	Anagnostidis 1968
	st. perdurans	Anagnostidis 1968
	st. simplex	Anagnostidis 1968
Mastigocladus laminosus	fa. oscillariodes subfa. subrecta	Anagnostidis 1961
	fa. oscillariodes subfa. circinata	Anagnostidis 1961
	fa. oscillariodes subfa. spiroides	Anagnostidis 1961
	fa. pseudanabaenoides	Anagnostidis 1961
	fa. pseudanabaenoides subfa. subrecta	Anagnostidis 1961
	fa. pseudanabaenoides subfa. circinata	Anagnostidis 1961
	fa. pseudanabaenoides subfa. spiroides	Anagnostidis 1961
	fa. lyngbyoides	Anagnostidis 1961
	fa. lyngbyoides subfa. subrecta	Anagnostidis 1961
	fa. lyngbyoides subfa. circinata	Anagnostidis 1961
	fa. phormidioides	Anagnostidis 1961
	fa. phormidioides subfa. subrecta	Anagnostidis 1961
	fa. phormidioides subfa. circinata	Anagnostidis 1961
	fa. plectonematoides	Anagnostidis 1961
	fa. symplocoides	Anagnostidis 1961
	fa. anabaenoides	Anagnostidis 1961
	fa. anabaenoides subfa. subrecta	Anagnostidis 1961
	fa. anabaenoides subfa. circinata	Anagnostidis 1961
	fa. anabaenoides subfa. spiroides	Anagnostidis 1961
	fa. nostocoides	Anagnostidis 1961
	fa. aulosiroides	Anagnostidis 1961
	fa. stigonematoides	Anagnostidis 1961
	fa. microchaetoides	Anagnostidis 1961
	fa. tolypotrichoides	Anagnostidis 1961
	fa. scytonematoides	Anagnostidis 1961
	fa. typica	Anagnostidis 1961
	fa. typica subfa. normalis	Anagnostidis 1961
	fa. typica subfa. brachytrichoides	Anagnostidis 1961
	fa. pallidus	Anagnostidis 1961
	fa. oscillariodes	Anagnostidis 1961
	fa. chroococcoides	Anagnostidis 1961
	fa. pleurocapsoides	Anagnostidis 1961
Nostoc punctiforme	var. populorum ¹	Anagnostidis and Economou-Amilli 1978
Pseudanabaena articulata	fa. ²	Anagnostidis 1968
Pseudanabaena lonchoides	fa. circinata	Anagnostidis 1961
	fa. crassior	Anagnostidis 1968
	fa. tenuis	Anagnostidis 1968
Scytonema myochrous	st. crustaceus	Anagnostidis 1968
	st. petalonema	Anagnostidis 1968
	st. petalonema	Anagnostidis 1968
	st. petalonema	Anagnostidis 1968
	st. typicus	Anagnostidis 1968
Siphononema polonicum	st. chamaesiphonoides	Anagnostidis 1968
	st. juvenilis	Anagnostidis 1968
	st. scopulonematoides	Anagnostidis 1968
	st. stigonematoides	Anagnostidis 1968
Synechocystis aquatilis	var. minor	Anagnostidis 1961

¹ The current taxonomic status is Nostoc punctiforme fa. populorum

² The author does not identify a certain forma

Table 2.

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List of cyanobacterial taxa known to occur in Greece with uncertain or not valid taxonomic status. For each taxon the publication mentioning its occurrence in Greece and the current taxonomic status is given.

Taxon	Reference	Current taxonomic status
Achroonema lentum	Anagnostidis and Economou–Amilli 1980	unclassified below the Kingdom level (Guiry and Guiry 2016)
Achroonema proteiforme	Anagnostidis 1968
Achroonema angustum	Anagnostidis 1968
Achroonema atriculatum	Anagnostidis 1968
Achroonema splendens	Anagnostidis 1968
Achroonema subsalsum	Anagnostidis 1968
Desmanthos thiocrenophilum (?)	Anagnostidis 1968
Pelonema aphane	Anagnostidis 1968
Pelonema cf. subtilissimum	Anagnostidis and Roussomoustakaki 1991
Pelonema pseudovacuolatum	Anagnostidis 1968
Pelonema subtilissimum	Anagnostidis 1968
Pelonema tenue	Anagnostidis 1968
Peloploca ferruginea (?)	Anagnostidis 1968
Peloploca taeniata	Anagnostidis 1968
Peloploca undulata	Anagnostidis 1968
Pleurocapsa crepidinum	Anagnostidis and Golubic 1966	needs revision; possibly a Chroococcidiopsis species (Komárek and Anagnostidis 2005)
Aphanothece nidulans var. nidulans	Hindak and Moustaka 1988	uncertain; Algabase (Guiry and Guiry 2016) contains only two valid A. nidulans varieties: var. longissima Nash and var. thermalis Hansgirg
Hydrocoleus homoeotrichus	Anagnostidis et al. 1983	needs revision; sensu Anagnostidis et al 1983, probably belongs to the Oscillatoriaceae according to trichome structure, and into the genus Blennothrix (Komárek and Anagnostidis 2005)
Achroonema pseudangustum	Anagnostidis and Economou–Amilli 1980	not valid (Guiry and Guiry 2016)
Scolecia filosa	Färber et al. 2015	Ichnotaxa produced by unknown heterotrophic organisms (Heindel et al. 2009)
Gloeocapsa polydermatica	Anagnostidis 1961	Sporotetras polydermatica [Chlorophyta] (Guiry and Guiry 2016)

Figure 1.

Classification of cyanobacteria of Greece in orders.

Figure 2.

Classification of cyanobacteria of Greece in families (a) and genera (b). Only families and genera including more than five species are shown.

Discussion

A thorough review of the relevant literature revealed that 543 species of cyanobacteria have been reported up to date from Greece. The species recorded from this area are classified in 130 genera and 41 families, all of the 8 orders of the class Cyanophyceae (Komárek et al. 2014) being represented. In this checklist we have not included 85 infraspecific taxa mostly from the genera Entophysalis, Gloeocapsa, Mastigocladus, Scytonema, and Siphononema recorded in several habitats such as gulfs, waterfalls, caves, and lakes by Anagnostidis (Anagnostidis 1961, Anagnostidis 1968). In the genus Mastigocladus numerous taxa were described, which do not belong to this genus (Komárek 2013). Among the formae described by Anagnostidis, some are subject to revision [e.g. M. fa. microchaetoides is "surely not Mastigocladus, as it is morphologically similar to Aulosira" according to Komárek (2013)]. The great morphological variability of this chroococcalean and nostocalean species should be further investigated in the future.

A number of species reported in Greece were found to be of not valid or of uncertain taxonomic status: The species Pleurocapsa crepidinum is possibly a Chroococcidiopsis species and needs revision (Komárek and Anagnostidis 2005). The species Hydrocoleus homoeotrichus sensu Anagnostidis et al. (1983), probably belongs to the Oscillatoriaceae and into the genus Blennothrix (Komárek and Anagnostidis 2005) according to its trichome structure. The taxon Aphanothece nidulans var. nidulans found in Lake Volvi (Hindak and Moustaka 1988) is not included either in the Chroococcales volume of Süsswasserflora von Mitteleuropa (Komárek and Anagnostidis 1999) nor in the AlgaeBase (Guiry and Guiry 2016); Algaebase contains only two valid A. nidulans varieties: var. longissima Nash and var. thermalis Hansgirg. Gloeocapsa polydermatica Kützing found in Nigrita hot springs (Anagnostidis 1961) is currently regarded as a taxonomic synonym of the chlorophyte Sporotetras polydermatica (Kützing) I.Kostikov, T.Darienko, A.Lukesová, & L.Hoffmann (Guiry and Guiry 2016). The taxon Scolecia filosa found in microbial bioerosion at an underwater marine site in Peloponnese (Färber et al. 2015) belongs to ichnotaxa produced by unknown heterotrophic organisms (Heindel et al. 2009), not cyanobacteria. The remaining 17 species belong to the family Pelonemataceae; this family, consisting of the genera Achroonema, Pelonema, Peloploca, and Desmanthos, was created to accommodate some colorless bacteria with multicellular filaments (trichomes), which were observed in hypolimnia of lakes and ponds or in sulfur springs (Hirsch 1981). At present, members of this family are considered unclassified below the Kingdom level (Guiry and Guiry 2016).

It is worth mentioning that 18 of the species included in the list have been initially described from Greek habitats. The marine epilithic Ammatoidea aegea described from Saronikos Gulf (Aegean Sea) (Anagnostidis and Pantazidou 1991a) is considered endemic to this area (Komarek and Anagnostidis 2005). Interestingly, most of these new species were found in rarely sampled habitats, such as caves [e.g. Toxopsis calypsus, Ifinoe spelaea (Lamprinou et al. 2011)], marine coastal rocks [e.g. epilithic Cyanosarcina thalassia (Anagnostidis and Pantazidou 1991b) or endolithic Cyanosaccus aegaeus and Cyanosaccus atticus (Anagnostidis and Pantazidou 1985, Anagnostidis and Pantazidou 1988c)], archaeological sites [e.g. aerophytic, chasmoendolithic Cyanosarcina parthenonensis (Anagnostidis and Pantazidou 1991b)], heliothermal saltwork mats [Cyanothece halobia (Anagnostidis and Roussomoustakaki 1991)], and waterfalls [Phormidium edessae (Skuja 1937)], highlighting the need for further research to reveal the unknown diversity in these environments. A recent study by Bravakos et al. (2016) on cyanobacteria strains isolated from mats of thermal springs of Greece indicates at least six new taxa at the genus level. Furthermore, Konstantinou et al. (2016) report possible new species on cyanobacteria strains isolated from marine sponges from the Aegean Sea, thus corroborating the abundant diversity of lesser-known environments.

To the best of our knowledge, the list of Greek cyanobacteria compiled for the needs of the present study is the first list of both freshwater and marine Cyanophyceae in the Mediterranean. There is another list presenting 327 species from Israel (Tsarenko et al. 2000), but this refers only to the continental part of that country. The Egyptian list (Nassar 2014) contains 19 cyanobacteria species, whereas a phytoplankton checklist from the Eastern Adriatic (Vilicic et al. 2002) contains no cyanobacteria. Other local cyanobacterial lists were published in the past 15 years from continental parts of Europe, e.g. Slovakia, Sweden, Poland, Romania, Ukraine, Slovenia, the Netherlands, and the Czech Republic (Kaštovský et al. 2010 and references therein), as well as a checklist from the Baltic Sea reporting 172 cyanobacterial species (Hällfors 2004). The Czech Republic list comprises 505 species, 392 of which are considered recently present according to Kaštovský et al. 2010. The cyanobacteria checklist of Nepal (Rai et al. 2011) presents 274 species. Therefore, it appears that Greece hosts a comparatively high diversity of cyanobacteria, suggesting that the Mediterranean area is also a hot spot for the “substantially underestimated or unexplored” (Coll et al. 2010) microbes.

Acknowledgements

This paper is dedicated to the memory of Professor Konstantinos Anagnostidis (12 December 1924-9 December 1994), whose pioneer work on cyanobacterial diversity has paved the way for modern cyanobacterial taxonomy and the study of Phycology in Greece.

This study was supported by the LifeWatchGreece Infrastructure, (MIS 384676), funded by the Greek Government under the General Secretariat of Research and Technology (GSRT), ESFRI Projects, National Strategic Reference Framework (NSRF).

SG gratefully acknowledges Prof. Eleni Voultsiadou for critically reading the manuscript, useful suggestions, and fruitful discussions. We thank Dr. Vasilis Gerovasileiou for his support.

Author contributions

SG conceived, designed and supervised this project, and prepared the manuscript. IO and NP collected the data. IO, MP, and SG and built the database.

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Supplementary material

Endnotes