Biodiversity Data Journal : Taxonomic Paper
Print
Taxonomic Paper
Ascidiacea (Chordata: Tunicata) of Greece: an updated checklist
expand article infoChryssanthi Antoniadou, Vasilis Gerovasileiou§, Nicolas Bailly§
‡ Department of Zoology, School of Biology, Aristotle University of Thessaloniki, Thessaloniki, Greece
§ Institute of Marine Biology, Biotechnology and Aquaculture, Hellenic Centre for Marine Research, Heraklion, Greece
Open Access

Abstract

Background

The checklist of the ascidian fauna (Tunicata: Ascidiacea) of Greece was compiled within the framework of the Greek Taxon Information System (GTIS), an application of the LifeWatchGreece Research Infrastructure (ESFRI) aiming to produce a complete checklist of species recorded from Greece. This checklist was constructed by updating an existing one with the inclusion of recently published records. All the reported species from Greek waters were taxonomically revised and cross-checked with the Ascidiacea World Database.

New information

The updated checklist of the class Ascidiacea of Greece comprises 75 species, classified in 33 genera, 12 families, and 3 orders. In total, 8 species have been added to the previous species list (4 Aplousobranchia, 2 Phlebobranchia, and 2 Stolidobranchia). Aplousobranchia was the most speciose order, followed by Stolidobranchia. Most species belonged to the families Didemnidae, Polyclinidae, Pyuridae, Ascidiidae, and Styelidae; these 4 families comprise 76% of the Greek ascidian species richness. The present effort revealed the limited taxonomic research effort devoted to the ascidian fauna of Greece, which is attributed to the lack of experts and low sampling effort. Therefore, major knowledge gaps on the ascidian diversity of Greece occur and further research in this field is needed.

Keywords

Sea-squirts, Aplousobranchia, Phlebobranchia, Stolidobranchia, Aegean Sea, Levantine Sea, Ionian Sea, eastern Mediterranean

Introduction

The class Ascidiacea (phylum Chordata, subphylum Tunicata) is globally represented by over 2,800 marine species (Shenkar and Swalla 2011, Shenkar et al. 2016b). Ascidians have been identified as a distinct zoological group since the ancient times; Aristotle was the first who described these peculiar animals, "Téthya", as the most extraordinary ones having a completely hidden body inside a leathery shell attached on rocks and with two openings some distance apart (Voultsiadou and Vafidis 2007). Their taxonomic classification proved to be challenging for zoologists. As members of the subphylum Tunicata, their close affinity to vertebrates has been recently confirmed by phylogenomic studies (Delsuc et al. 2006). Furthermore, the original classification of Lahille (1886), which classified the ascidian species into the orders Aplousobranchia, Phlebobranchia, and Stolidobranchia according to the structure of the branchial sac, is supported by molecular phylogeny and is currently accepted by most taxonomists (Shenkar and Swalla 2011). However, there are still different views on the placement of several families into orders, and the phylogenetic relationships within the ascidians remain fuzzy (Turon and López-Legentil 2004, Moreno et al. 2008, Pérez-Portela et al. 2009, Tsagkogeorga et al. 2009, Shenkar et al. 2016a).

The first list of Mediterranean ascidians (Pérès 1958, Pérès 1967) reported 132 species; since then, the relevant scientific research increased leading to 229 ascidian species at present (Coll et al. 2010, Shenkar and Swalla 2011). Most records are from the western Mediterranean (165 species), where much more effort has been devoted as opposed to the eastern basin, from which only 86 species have been reported (Koukouras et al. 1995). Among Mediterranean ascidians, 103 exclusive species are included and the entire basin has been recognized as an area of endemism, at least for this specific taxonomic group (Naranjo et al. 1998, Moreno et al. 2014).

In the Greek seas, however, only scattered records of ascidian species were available, either in relevant faunistic accounts (e.g. Hartmeyer 1904, Monniot and Monniot 1974, Koukouras and Siamidou-Efremidou 1978) or in general ecological publications (e.g. Pérès and Picard 1958, Kiseleva 1963, Vamvakas 1971). Koukouras et al. (1995) published the first checklist of the Aegean Ascidiacea, covering also the eastern Mediterranean basin and the Black Sea. So far, this work was the only comprehensive systematic account on the Greek ascidians, combining primary data with an exhaustive literature review. After this publication, a number of studies have been conducted covering various aspects of ascidian biology, such as population dynamics (Panagiotou et al. 2007, Panagiotou et al. 2008, Vafidis et al. 2008), reproduction (Panagiotou et al. 2008, Vafidis et al. 2008), fisheries (Antoniadou and Vafidis 2008), and ecology in general (Morri et al. 1999, Antoniadou et al. 2006, Antoniadou et al. 2013, Sini et al. 2014) or focusing on ascidian associations with other invertebrates (Voultsiadou et al. 2007, Voultsiadou et al. 2010). This research effort has led to some new records of ascidian species in the Aegean Sea (i.e. Morri et al. 1999, Sini et al. 2014), in parallel with additional biodiversity records (Thessalou-Legaki et al. 2012) and the presence of non-indigenous species (Kondilatos et al. 2010, Katsanevakis et al. 2014).

Therefore, the aim of the present work is to compile an updated checklist of Ascidiacea of the Greek seas. For this purpose, the earlier list compiled by Koukouras et al. (1995) has been extended, updated, and annotated according to the recent literature and taxonomic status.

Materials and methods

The Checklist of Ascidiacea of Greece (Suppl. material 1) was compiled within the context of the Greek Taxon Information System (GTIS). GTIS is an application of the LifeWatchGreece Research Infrastructure (ESFRI) aiming to produce a complete inventory of the Greek biota, by joining relevant efforts. As a first step, the publication of Preliminary Checklists for each taxonomic group has been suggested (Bailly et al. 2016). The present checklist of ascidians has been based on the key-publication of Koukouras et al. (1995), who had compiled the ascidian species list of the Aegean Sea for the first time. In the course of the current study, all recent primary literature was also thoroughly searched and the relevant data were incorporated into the updated species list. New species additions are annotated in the checklist and cited along with the first literature reference reporting their presence in the Greek seas. Non-indigenous species (NIS) are also marked. A cross-checking of all species names and their higher classification was carried through the Ascidiacea World Database, AWD (Shenkar et al. 2016b); the classification followed in the present checklist is the one proposed by the AWD, which contains an updated list of all ascidian species, recursively revised by ascidian taxonomy experts (Shenkar and Swalla 2011).

Checklist of Ascidiacea known to occur in Greek waters

Class Ascidiacea

Material    Download as CSV 

Order Aplousobranchia

Material    Download as CSV 

Family Clavelinidae

Material    Download as CSV 

Clavelina dellavallei (Zirpolo, 1825)

Material    Download as CSV 

Clavelina lepadiformis (Müller, 1776)

Material    Download as CSV 

Family Didemnidae

Material    Download as CSV 

Didemnum amourouxi Lafargue, 1976

Material    Download as CSV 

Didemnum coriaceum (Drasche, 1883)

Material    Download as CSV 

Didemnum drachi Lafargue, 1975

Material    Download as CSV 

Didemnum fulgens (Milne Edwards, 1841)

Material    Download as CSV 

Didemnum granulosum (Drasche, 1883)

Material    Download as CSV 

Didemnum maculosum (Milne Edwards, 1841)

Material    Download as CSV 

Didemnum peyrefittense Brément, 1913

Material    Download as CSV 

Diplosoma listerianum (Milne Edwards, 1841)

Material    Download as CSV 
Notes: 

Recorded by Morri et al. (1999)

Diplosoma spongiforme (Giard, 1872)

Material    Download as CSV 

Lissoclinum perforatum (Giard, 1872)

Material    Download as CSV 
Notes: 

Recorded by Thessalou-Legaki et al. (2012)

Polysyncraton bilobatum Lafargue, 1968

Material    Download as CSV 

Polysyncraton lacazei (Giard, 1872)

Material    Download as CSV 

Trididemnum cereum (Giard, 1872)

Material    Download as CSV 

Trididemnum inarmatum (Drasche, 1883)

Material    Download as CSV 

Family Polycitoridae

Material    Download as CSV 

Cystodytes dellechiajei (Della Valle, 1877)

Material    Download as CSV 

Eudistoma costai (Della Valle, 1877)

Material    Download as CSV 

Polycitor crystallinus (Renier, 1804)

Material    Download as CSV 

Family Polyclinidae

Material    Download as CSV 

Aplidium aegeaensis (Hartmeyer, 1904)

Material    Download as CSV 

Aplidium albicans (Milne Edwards, 1841)

Material    Download as CSV 

Aplidium asperum Drasche, 1883

Material    Download as CSV 

Aplidium conicum (Olivi, 1792)

Material    Download as CSV 

Aplidium elegans (Giard, 1872)

Material    Download as CSV 
Notes: 

Recorded by Sini et al. (2014)

Aplidium nordmanni (Milne Edwards, 1841)

Material    Download as CSV 

Aplidium pallidum (Verrill, 1871)

Material    Download as CSV 

Aplidium pseudolobatum (Pérès, 1956)

Material    Download as CSV 

Aplidium turbinatum (Savigny, 1816)

Material    Download as CSV 

Aplidium undulatum Monniot & Gaill, 1978

Material    Download as CSV 

Polyclinella azemai Harant, 1930

Material    Download as CSV 

Polyclinum aurantium Milne Edwards, 1841

Material    Download as CSV 
Notes: 

Recorded by Morri et al. (1999)

Pseudodistoma cyrnusense Pérès, 1952

Material    Download as CSV 

Order Phlebobranchia

Material    Download as CSV 

Family Ascidiidae

Material    Download as CSV 

Ascidia colleta Monniot C. & Monniot F., 1970

Material    Download as CSV 

Ascidia mentula Müller, 1776

Material    Download as CSV 

Ascidia muricata Heller, 1874

Material    Download as CSV 

Ascidia salvatoris (Traustedt, 1885)

Material    Download as CSV 

Ascidia virginea Müller, 1776

Material    Download as CSV 

Ascidiella aspersa (Müller, 1776)

Material    Download as CSV 

Ascidiella scabra (Müller, 1776)

Material    Download as CSV 

Phallusia fumigata (Grube, 1864)

Material    Download as CSV 

Phallusia mammillata (Cuvier, 1815)

Material    Download as CSV 

Phallusia nigra Savigny, 1816

Material    Download as CSV 
Notes: 

Recorded by Kondilatos et al. (2010); NIS

Family Cionidae

Material    Download as CSV 

Ciona intestinalis (Linnaeus, 1767)

Material    Download as CSV 

Ciona roulei Lahille, 1887

Material    Download as CSV 
Notes: 

Recorded by Thessalou-Legaki et al. (2012)

Family Corellidae

Material    Download as CSV 

Corella parallelogramma (Müller, 1776)

Material    Download as CSV 

Rhodosoma turcicum (Savigny, 1816)

Material    Download as CSV 

Family Diazonidae

Material    Download as CSV 

Diazona violacea Savigny, 1816

Material    Download as CSV 

Rhopalaea neapolitana Philippi, 1843

Material    Download as CSV 

Family Perophoridae

Material    Download as CSV 

Ecteinascidia turbinata Herdman, 1880

Material    Download as CSV 
Notes: 

Recorded by Monniot (1983)

Perophora listeri Wiegman, 1835

Material    Download as CSV 

Order Stolidobranchia

Material    Download as CSV 

Family Molgulidae

Material    Download as CSV 

Eugyra arenosa (Alder & Hancock, 1848)

Material    Download as CSV 

Molgula appendiculata Heller, 1877

Material    Download as CSV 

Molgula manhattensis (De Kay, 1843)

Material    Download as CSV 

Molgula occulta Kupffer, 1875

Material    Download as CSV 

Family Pyuridae

Material    Download as CSV 

Halocynthia papillosa (Linnaeus, 1767)

Material    Download as CSV 

Herdmania momus (Savigny, 1816)

Material    Download as CSV 
Notes: 

Recorded by Katsanevakis et al. (2014); NIS

Microcosmus claudicans (Savigny, 1816)

Material    Download as CSV 

Microcosmus nudistigma Monniot C., 1962

Material    Download as CSV 

Microcosmus polymorphus Heller, 1877

Material    Download as CSV 

Microcosmus sabatieri Roule, 1885

Material    Download as CSV 

Microcosmus savignyi Monniot, 1962

Material    Download as CSV 

Microcosmus vulgaris Heller, 1877

Material    Download as CSV 

Pyura dura (Heller, 1877)

Material    Download as CSV 

Pyura microcosmus (Savigny, 1816)

Material    Download as CSV 

Pyura squamulosa (Alder, 1863)

Material    Download as CSV 

Pyura tessellata (Forbes, 1848)

Material    Download as CSV 

Family Styelidae

Material    Download as CSV 

Botryllus schlosseri (Pallas, 1766)

Material    Download as CSV 

Botrylloides leachii (Savigny, 1816)

Material    Download as CSV 

Distomus variolosus Gaertner, 1774

Material    Download as CSV 

Polycarpa caudata Monniot C. & Monniot F., 1974

Material    Download as CSV 

Polycarpa fibrosa (Stimpson, 1852)

Material    Download as CSV 

Polycarpa gracilis Heller, 1877

Material    Download as CSV 

Polycarpa pomaria (Savigny, 1816)

Material    Download as CSV 

Styela canopus (Savigny, 1816)

Material    Download as CSV 

Styela plicata (Lesueur, 1823)

Material    Download as CSV 

Discussion

A total of 75 species classified, according to AWD, into 33 genera, 12 families and 3 orders, have been reported from the Greek seas. In addition, Ascidia conchilega, Müller, 1776 which is included in AWD and WoRMS databases is a doubtful record for the Greek seas because its original reference for the area is missing and thus it was not included in the list by Koukouras et al. (1995). Aplousobranchia and Stolidobranchia are the most speciose orders with 32 and 25 species, respectively. Aplousobranchia reach 36 species, if the families Diazonidae and Cionidae are included therein instead of Phlebobranchia, as suggested by various ascidian taxonomists based on morphological, developmental, and molecular data (Kott 1990, Turon and López-Legentil 2004, Shenkar and Swalla 2011, Shenkar et al. 2016a) but not currently adopted by AWD. The families Didemnidae (14 species), Polyclinidae (12 species), Pyuridae (12 species), Ascidiidae (10), and Styelidae (9 species) comprised the highest number of species, covering altogether 76% of the Greek ascidian species richness. The first two families have been identified as the most speciose ones across most Mediterranean longitudinal bands (Moreno et al. 2014).

Most ascidian species included in the present checklist were already known as elements of the Greek fauna (Koukouras et al. 1995), while 8 new additions were made in the course of this compilation. These additions include: 4 species of Aplousobranchia, namely Aplidium elegans, Diplosoma listerianum, Lissoclinum perforatum, and Polyclinum aurantium; 2 species of Phlebobranchia, namely Ciona roulei and Ecteinascidia turbinata; and 2 species of Stolidobranchia, namely Herdmania momus and Phallusia nigra. Although the latter species may need additional confirmation because of the identification uncertainty between the 3 darkly pigmented Phallusia species when based on exclusively external features (Vandepas et al. 2015), we consider its presence as valid since it has been reported from the south sector of the Aegean Sea by multiple authors (Kondilatos et al. 2010, Çinar 2014).

The Greek ascidian fauna is mainly composed by species of Atlanto-Mediterranean origin (44.4%) or by endemic species (40.3%), as previously suggested (Koukouras et al. 1995). Among the newly added species, C. roulei is a Mediterranean endemic, whereas Phallusia nigra and Herdmania momus are considered non-indigenous species (NIS) of circum(sub)tropical and Indo-pacific origin, respectively (Gerovasileiou et al. 2016); both species have been probably introduced through shipping (Galil et al. 2016). Another three species, i.e. Molgula occidentalis Traustedt, 1883, Pycnoclavella nana (Lahille, 1890), and Microcosmus exasperatus Heller, 1878, have been recently reported from the Turkish coasts of the Aegean (Çinar 2014); this may imply their presence in the nearby Greek coasts, since they are part of the same ecoregion, the Aegean Archipelago (Spalding et al. 2007) and also part of the Levantine cluster, i.e. areas highly impacted by Erythraean species migration (Galil et al. 2016). Finally, we should mention the presence of Symplegma brakenhielmi (Michaelsen, 1904) in the Turkish levantine coasts (Çinar et al. 2006). Since several non-indigenous ascidians, such as P. nigra and H. momus, have invaded the Greek waters few years after their first record in Turkish waters, it is reasonable to expect them to be reported from south Greece as well, within next few years.

The present updated checklist of Ascidiacea of the Greek seas summarizes the status of the current knowledge. However, a major gap in our knowledge on ascidian diversity of the Greek seas is obvious when the number of species is compared to those known from the western Mediterranean. This can be attributed to two main reasons: (i) the absence of ascidian expertise in Greece and, (ii) the fact that the entire literature on Greek ascidians refers almost exclusively to the Aegean Sea. The necessity for further research on ascidian diversity becomes therefore obvious and expands to the Ionian and Levantine coasts of Greece, from which the ascidian fauna has practically not at all been studied so far.

Acknowledgements

This work 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). We would like to thank Dr. Xavier Turon and anonymous reviewers for their constructive comments.

References

Supplementary material

Suppl. material 1: Checklist of the ascidian fauna (Tunicata: Ascidiacea) of Greece
Authors:  Chryssanthi Antoniadou, Vasilis Gerovasileiou, Nicolas Bailly
Data type:  Taxonomic checklist
Brief description: 

Taxonomic checklist of Ascidiacea known to occur in Greek waters.