BioInvasions Records (2019) Volume 8, Issue 3: 500–504

CORRECTED PROOF

Rapid Communication First record of the land bicolor (Graff, 1899) (Platyhelminthes, Tricladida, ) in Greece

Katerina Vardinoyannis* and Giorgos Alexandrakis Natural History Museum of Crete, University of Crete, Knossou Av. 71409, Irakleio, Crete, Greece Author e-mails: [email protected] (KV), [email protected] (GA) *Corresponding author

Citation: Vardinoyannis K, Alexandrakis G (2019) First record of the land planarian Abstract Caenoplana bicolor (Graff, 1899) (Platyhelminthes, Tricladida, New alien are added every year to the European fauna. Although there are a Continenticola) in Greece. BioInvasions few indigenous terrestrial in , only one species has been recorded Records 8(3): 500–504, https://doi.org/10. so far in Greece. For the first time, an alien species, Caenoplana bicolor, is 3391/bir.2019.8.3.04 recorded on the island of Crete. This finding suggests the need for control measures Received: 6 March 2019 to prevent impacts from this bioinvasion. Accepted: 20 May 2019 Published: 25 July 2019 Key words: alien species, East Mediterranean, , terrestrial flatworm Handling editor: Ana Luisa Nunes Thematic editor: Stelios Katsanevakis Introduction Copyright: © Vardinoyannis and Alexandrakis Terrestrial (Tricladida: Terricola) constitute a poorly understood This is an open access article distributed under terms of the Creative Commons Attribution License group of free-living flatworms (Mateos et al. 1998); the group contains (Attribution 4.0 International - CC BY 4.0). about 910 species of flat or cylindrical , 4–600 mm in length, that OPEN ACCESS. typically live in tropical jungles or temperate wooded areas and can survive only in moist soil environments (Sluys 2016). The European fauna of land planarians includes very few species compared to other continents (Jones 1998). Data on terrestrial planarians of Europe has been summarized by Minelli (1977) and Jones (1998). By far the most common and widespread indigenous species in Europe and the Mediterranean area is the rhynchodemid terrestris (O. F. Müller, 1773) (Minelli 1977; Jones 1998; Mateos et al. 1998; Ball and Reynoldson 1981). Terrestrial flatworms in Greece have not been studied at all and only M. terrestris has been reported by Arndt (1934) from the island of Crete. Later on, Minelli (1977) and Jones (1998) included the island of Crete in the distribution range of this species. However, in the databases of Fauna Europaea (https://fauna-eu.org/cdm_dataportal/taxon/9b40a829-11e4-4494- 968d-7aa6dbfe6ecf) and GBIF (https://www.gbif.org/species/4416151), both accessed in February 2019, there are no records of terrestrial flatworms from Greece. Land planarians have been reported as alien species in soils throughout the world and, among those, some species are considered to be successful

Vardinoyannis and Alexandrakis (2019), BioInvasions Records 8(3): 500–504, https://doi.org/10.3391/bir.2019.8.3.04 500 First discovery of Caenoplana bicolor in Greece

Figure 1. View of Vryses square with Plane trees and the Vrysianos stream, western Crete, where C. bicolor was found.

invaders (Breugelmans et al. 2012; Mazza et al. 2016; Sluys 2016). In total, 18 alien flatworm species have been reported in 13 European countries (Álvarez-Presas et al. 2014; Justine et al. 2014 and references therein; Mazza et al. 2016; Sluys 2016). In this work, we present the first finding of the alien flatworm Caenoplana bicolor (Graff, 1899) from the island of Crete and suggest a potential route of its introduction.

Materials and results In October 2018, during a field trip in West Crete, two terrestrial flatworms were found in the main square of the village Vryses. The animals were found during daylight hours on the trunk of a Plane tree (Platanus orientalis L.) by the Vrysianos stream (Figure 1), which runs through the main square of the village (35.375827°N; 24.200994°E; Figure 2). Western Crete is more humid and wet than the eastern part of the island. Rainfalls occur from late autumn until mid-spring, and at the village of Vryses the mean annual rainfall is 800–1000 mm (Pennas 1977; http://meteosearch. meteo.gr/stationInfo.asp). Information about Greek terrestrial Platyhelminthes was thoroughly researched both in scientific journals and relevant web pages, i.e. earthling nature https://earthlingnature.wordpress.com/library/tricladida-database/ and the Kawakatsu website http://www.riverwin.jp/pl/. The identification of the specimens was based on shape, size and pattern of their bodies, and was confirmed by Dr. R. Sluys, a leading expert on this taxonomic group. Animals were photographed alive with a Progres Gryphax camera attached to a Zeiss Stemi 508 stereo-microscope. The two specimens

Vardinoyannis and Alexandrakis (2019), BioInvasions Records 8(3): 500–504, https://doi.org/10.3391/bir.2019.8.3.04 501 First discovery of Caenoplana bicolor in Greece

Figure 2. Map of western Crete and the location of the village Vryses.

have been stored (collection ID: NHMC.62.2) in absolute ethanol (96%) and deposited in the Invertebrate Collection of the Natural History Museum of Crete - University of Crete. The collected specimens belong to the species Caenoplana bicolor (Graff, 1899) (Figure 3A–C); they are dark colored with a large yellow stripe containing two black lines, and the largest specimen was 3.8 cm in length (Figure 3A).

Discussion Caenoplana bicolor is the second species of land planarian to be recorded from Crete (other than the native ), thus Crete hosts one indigenous and one alien planarian species. The island of Crete is the southernmost place where this species has been recorded in Europe and, as stated by de Waart (2016), the species can survive in dry biotopes. This flatworm is native from (Justine et al. 2018), but it has been recorded

Vardinoyannis and Alexandrakis (2019), BioInvasions Records 8(3): 500–504, https://doi.org/10.3391/bir.2019.8.3.04 502 First discovery of Caenoplana bicolor in Greece

Figure 3. Caenoplana bicolor from western Crete. A: largest specimen; B: part of the underside of the body, C: both specimens.

in Spain, , , and the Netherlands (Álvarez- Presas et al. 2014; de Waart 2016; Justine et al. 2014; Sluys 2016). The introduction of alien flatworms into the soils of several countries may significantly affect soil ecosystems, through predation or disruption of components of native ecosystems (Winsor et al. 2004; Álvarez-Presas et al. 2014; Justine et al. 2014; Mazza et al. 2016). As they are top-level predators of soil invertebrates such as , , , isopods and others (Sluys 1999), they might pose a threat to local biodiversity (Breugelmans et al. 2012). This can be even more critical for the invertebrate fauna of the Greek islands, where endemism in certain groups is quite high, e.g. 59% for terrestrial gastropods (Vardinoyannis et al. 2018) and 67.3% for terrestrial isopods (Sfenthourakis and Schmalfuss 2018). Breugelmans et al. (2012) pointed out that the “impacts of introduced exotic terrestrial flatworms may be especially detrimental in islands and archipelagos that support an endemic invertebrate fauna”. Although these specimens were found on the trunk of a native tree in a village, we hypothesize that their presence in Crete is due to the horticultural trade. This is because C. bicolor has also been recorded in Italy, Spain and the Netherlands, which are countries with significant horticultural trade and, in Spain, France and the UK, the species is found in gardens, orchards and plant nurseries (de Waart 2016; Sluys 2016). Introduction of alien species through the horticultural trade has already been suggested for terrestrial gastropods in Greece (Vardinoyannis et al. 2017). Given that bioinvasions may have unpredictable and adverse effects on native plants

Vardinoyannis and Alexandrakis (2019), BioInvasions Records 8(3): 500–504, https://doi.org/10.3391/bir.2019.8.3.04 503 First discovery of Caenoplana bicolor in Greece

and animals (Sluys 2016), we believe that it is important to undertake control measures in order to prevent further spread of this species in Crete.

Acknowledgements

We thank Dr R Sluys for confirming our identification and providing us with useful information on Platyhelminthes, and Dr APMcK Pegman and LM Constantino who also confirmed our findings. We also thank Mina Trikali, librarian in the Natural History Museum of Crete, for her valuable help in literature search. Three anonymous reviewers and the handling editor Dr A. Nunes, provided useful criticism and advice which improved further the manuscript and the English.

References

Álvarez-Presas M, Mateos E, Tudó Á, Jones H, Riutort M (2014) Diversity of introduced terrestrial flatworms in the Iberian Peninsula: a cautionary tale. PeerJ 2: e430, https://doi.org/ 10.7717/peerj.430 Arndt W (1934) Die Landplanarienfunde in Deutschland. Zoogeographica 2: 375–392 Ball IR, Reynoldson TB (1981) British planarians. Cambridge: Cambridge University Press, 141 pp Breugelmans K, Cardona JQ, Artois T, Jordaens K, Backeljau T (2012) First report of the exotic blue land planarian, (Platyhelminthes, Geoplanidae), on Menorca (Balearic Islands, Spain). ZooKeys 199: 91–105, https://doi.org/10.3897/zookeys.199.3215 de Waart S (2016) Exotische landplatwormen in Nederland (Platyhelminthes: Tricladida). Nederlandse Faunistische Mededelingen 47: 1–10 Jones HD (1998) The African and European land planarian fauna, with an identification guide for field workers in Europe. Pedobiologia 42: 477–489 Justine JL, Gey D, Gros P, Thêvenot J (2014) The invasive New Guinea flatworm manokwari in France, the first record for Europe: time for action is now. PeerJ 2: e297 https://doi.org/10.7717/peerj.297 Justine JL, Winsor L, Gey D, Gros P, Thévenot J (2018) Giant worms chez moi! Hammerhead flatworms (Platyhelminthes, Geoplanidae, spp., spp.) in metropolitan France and overseas French territories. PeerJ 6: e4672, https://doi.org/10.7717/peerj.4672 Mateos E, Giribet G, Carranza S (1998) Terrestrial planarians (Platyhelminthes, Tricladida, Terricola) from the Iberian Peninsula: first records of the family Rhynchodemidae, with the description of a new Microplana species. Contributions to Zoology 67: 267–276, https://doi.org/10.1163/18759866-06704004 Mazza G, Menchetti M, Sluys R, Solá E, Riutort M, Tricarico E, Justine JL, Cavigioli L, Mori E (2016) First report of the land planarian Diversibipalium multilineatum (Makino & Shirasawa, 1983) (Platyhelminthes, Tricladida, Continenticola) in Europe. Zootaxa 4067: 577–580, https://doi.org/10.11646/zootaxa.4067.5.4 Minelli A (1977) A taxonomic review of the terrestrial planarians of Europe. Bolletino Zoologico 44: 399–419, https://doi.org/10.1080/11250007709429278 Pennas P (1977) To Klima tis Kritis [The climate of Crete]. PhD Thesis Aristotle University of Thessaloniki, 105 pp Sfenthourakis S, Schmalfuss H (2018) Biogeography of Greek terrestrial Isopods. In: Sfenthourakis S, Pafilis P, Parmakelis A, Poulakakis N, Triantis K (eds), Biogeography and biodiversity of the Aegean. In honour of Prof. Moysis Mylonas. Broken Hill Publishers Ltd, Nicosia, Cyprus, pp 91–105 Sluys R (1999) Global diversity of land planarians (Platyhelminthes, Tricladida, Terricola): a new indicator-taxon in biodiversity and conservation studies. Biodiversity and Conservation 8: 1663–1681, https://doi.org/10.1023/A:1008994925673 Sluys R (2016) Invasion of the Flatworms. Easily hidden in imported plants, some land flatworms are conquering the world. American Scientist 104: 288–295, https://doi.org/10.1511/2016.122.288 Vardinoyannis K, Tzatzi M, Mylonas M (2017) New arrivals in Greece and Cyprus in Ćmiel. In: Lipińska A, Zając K, Zając R, Cameron RAD (eds), Book of Abstracts of the 8th European Malacological Societies. Krakow, Poland, September 10-14, 2017, p 152 Vardinoyannis K, Parmakelis A, Triantis KA, Giokas S (2018) Land Molluscs in Greece: The Rich, Unique, Diverse, and Unprotected Models. In: Sfenthourakis S, Pafilis P, Parmakelis A, Poulakakis N, Triantis K (eds), Biogeography and biodiversity of the Aegean. In honour of Prof. Moysis Mylonas. Broken Hill Publishers Ltd, Nicosia, Cyprus pp 47–66 Winsor L, Johns PM, Barker GM (2004) Terrestrial planarians (Platyhelminthes: Tricladida: Terricola) predaceous on terrestrial gastropods. In: Barker GM (ed), Natural Enemies of Terrestrial Molluscs. Oxfordshire: CAB International, pp 227–278, https://doi.org/10.1079/ 9780851993195.0227

Vardinoyannis and Alexandrakis (2019), BioInvasions Records 8(3): 500–504, https://doi.org/10.3391/bir.2019.8.3.04 504