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Plant Diversity and Biogeography of the Aegean Archipelago: A New Synthesis

Maria Panitsa1, Anna Kagiampaki2 and Kostas Kougioumoutzis1

1Division of Plant Biology, Department of Biology, University of Patras, GR-26504 Patras, Greece. E-mail: [email protected] 2Region of Crete, Directorate of Environment and Spatial Planning, GR-71201 Irakleion Crete, Greece. E-mail: [email protected]; [email protected]

ABSTRACT The Aegean archipelago is one of the largest archipelagos in the world and has long fascinated biogeographers due to its high environmental heterogeneity, complex palaeogeography, high di- versity and endemism. In this study, prominence has been given to the plant diversity and bio- geography of the Aegean area. After describing the phytogeographical aspects in the Aegean ar- chipelago from the first division in phytogeographical areas, the current widely used subdivisions to the recent aspects of the Aegean phytogeographical classification, a synoptic analysis of the Aegean plant diversity is presented focusing on the Aegean endemics, the range-restricted plant taxa, the single island endemics, the protected plant taxa and the most Critically Endangered ones. Plant diversification and speciation in the Aegean and factors driving them, as revealed by molecular studies, are discussed briefly. The ruderal, alien and invasive plant taxa richness has al- so been mentioned. Emphasis is also given to small islands and islets plant species diversity. Fac- tors affecting plant species richness in the Aegean, such as the long-lasting human presence, cli- mate, area, elevation, habitat diversity, isolation, geological substrate and structure are discussed on the basis of different biogeographical studies concerning the Aegean area.

AEGEAN, THE GREAT ARCHIPELAGO IN THE MEDITERRANEAN HOTSPOT The Mediterranean Basin constitutes the second largest hotspot at global scale and the largest among the world's five Mediterranean-climate regions (Critical Ecosystem Partnership Fund, 2017). The Mediterranean biome, although representing only 2% of the world’s surface area, contains 20% of the total plant species richness (Médail & Quézel, 1997) and regarding plant endemism, 10% of the world’s plants occur in the Mediterranean region (Blondel, Aronson, Bodiou, & Bœuf, 2010).The European part of the Mediterranean Basin, rich in islands, is one of the world’s major centres of plant diversity, as 10% of all known higher plants are found there (Médail & Quézel, 1997). Multiple factors, such as tectonic movement, earthquakes and volcanic activities and the near-desiccation of the sea during the Messinian Salinity Crisis, have created an ensemble of highly heterogeneous

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224 Plant Diversity and Biogeography of the Aegean Archipelago: A New Synthesis

habitats with diverse topographies, soil types ranean, located in the southern Cyclades, as it is and microclimates related to altitude, slope ex- found on the edge of two tectonic plates: the posure and precipitation (Blondel et al., 2010). African plate and the Aegean-Anatolian mi- The Mediterranean Basin owes its’ topo- croplate (for a thorough review on the SAVA, graphical complexity largely to the numerous is- see Kougioumoutzis & Tiniakou, 2014, and ref- lands that vary in size and are scattered around erences therein). the Mediterranean Sea. The Aegean Archipela- The palaeogeographical history of the go alone consists of more than 8,000 islands Aegean is relatively recent and rather complex. and islets, being one of the largest archipelagos The fragmentation of Ägäis (the present-day in the world (Triantis & Mylonas, 2009). Every Aegean, a then continuous large landmass) island is unique in terms of geographical and started during the Middle and Upper Miocene topographical features, e.g., position, size, alti- (Creutzburg, 1966; Dermitzakis, 1990). The tude, geodiversity, origin, geohistorical process- Aegean’s phytogeographical compartmentaliza- es and many more (Tzanoudakis & Panitsa, tion (Figure 1) coincides largely with the 1995). Enduring human impact is combined Aegean’s palaeogeographical history and its with the geographical features in larger islands evolution during the later stages of the Neo- to shape the insular flora (Greuter, 1975a, b; gene and the Quaternary. Two main distribu- Whittaker & Fernández-Palacios, 2007); this is tional and (palaeo-)geographical barriers exist especially true for the Aegean islands, since, in the Aegean Archipelago: the Mid Aegean nearly 45% of the present Aegean flora has Trench (MAT) and the North Aegean Trench reached the Aegean Islands owing to human ac- (NAT). The formation of the MAT plays a critical tion in prehistoric or early historic times role in shaping the Aegean’s biogeographical (Greuter, 1979). patterns; this ancient and predominant barrier, Crete and southern and central Greece are a- which has also affected animal distribution pat- mong the 10 principal plant diversity core areas terns (e.g. Poulakakis et al., 2014), is stronger in within the Mediterranean Basin hotspot (Médail its southern and geologically older tip, since it & Quézel, 1999). The Aegean Archipelago, lying distinctively separates Crete from Karpathos, at the crossroads of three biogeographical re- the central Aegean and the Peloponnisos. The gions, namely Europe, Asia and Africa (Triantis & MAT does deserve some merit regarding the Mylonas, 2009), and constituting a considerable phytogeographical separation of the central biogeographic barrier between the Balkan and Aegean from the east Aegean, yet its power ap- Anatolian Peninsulas, thus triggering the diver- pears to be diminishing in a S-N axis. In the gence of European and Asian taxa (e.g. Sobiera- north Aegean, the plant distribution patterns jska et al., 2016; Crowl et al., 2015; Mazur et al., have been shaped by the interplay between the 2018) has long fascinated biogeographers (Turill, MAT and the NAT, with the latter gradually re- 1929), due to its high environmental and topo- placing the former as it heads towards the graphical heterogeneity, complex palaeogeo- northern Greek mainland. The NAT constitutes graphical history, as well as high diversity and an impregnable barrier: the North Aegean Is- endemism (Strid, 1996). All the above render it lands have very low affinities with the Aegean an ideal stage for research in biodiversity, evolu- islands situated south of the NAT. Additionally, tion, ecology and biogeographical studies and as the isolation of Crete from Peloponnisos after such, the Aegean archipelago has the potential the Messinian Salinity Crisis and the separation to become a model study area globally, espe- of Karpathos’ island group from Rodos in the cially for land-bridge, continental islands (Sfen- Pliocene were also very important geological thourakis & Triantis, 2017). events that created dispersal barriers (Lymber- Most of the Aegean islands are of continental akis & Poulakakis, 2010). Besides, Quaternary origin, except those belonging to the South sea-level oscillations, as well as plate tectonic Aegean Volcanic Arc (SAVA), one of the most dynamics have influenced the current biogeo- significant geological structures of the Mediter- graphical structure of the Aegean (e.g. Celli- 14_Layout 1 6/9/2018 11:20 ππ Page 225

225 Plant Diversity and Biogeography of the Aegean Archipelago: A New Synthesis

FIGURE 1 ¡ Phytogeographical divisions of the Aegean. Black discontinuous lines delimit the 13 floristic re- gions of Greece according to the “Flora Hellenica” project, where the map originates from (Strid, 1996). The Flo- ra Hellenica regions of the Aegean are: NAe: North, WAe: West, EAe: East, Kik: Cyclades, ΚΚ: Crete – Karpathos complex. Red lines and regions’ names in red indicate the phytogeographical division by Rechinger and Rechinger-Moser (1951). Blue lines delimit Cardaegean. Green lines are the regions defined by Kougioumoutzis et al. (2017); NMI: the northernmost module consisted by the islands of Thasos and Samothraki together with north mainland Greece (NE). SMI: Evvoia and the western part of South Aegean island arc are grouped together with the southern parts of mainland Greece. CAE: Central Aegean module consisted of the Cyclades together with Northern Sporades and Limnos. NE-AE: North-Eastern Aegean module extending from Lesvos to Kos. SE-AE: Southeast Aegean module consisted by the complexes of Rodos, Karpathos, Nisyros, Tilos, Symi and Chalki. KR: the separated phytogeographical region of Kriti. Bold red discontinuous line: Rechinger’s line, generally coincid- ing with the Mid Aegean Trench (MAT). 14_Layout 1 6/9/2018 11:20 ππ Page 226

226 Plant Diversity and Biogeography of the Aegean Archipelago: A New Synthesis

nese et al., 2009; Kougioumoutzis, Simaiakis, & Aegean islands due to human-mediated disper- Tiniakou, 2014; Simaiakis et al., 2017). Finally, sal comprise the anthropophytic element of the the spatial configuration of the Aegean Archi- Aegean flora (Greuter, 1975a, b, 1979). pelago during the last glacial maximum and/or earlier glacials, has had a strong and detectable impact on the plant species’ distribution and PHYTOGEOGRAPHICAL ASPECTS evolutionary patterns, as in the Nigella arvensis AND DIVISIONS IN THE AEGEAN complex (Strid, 1970; Comes, Tribsch, & Bit- ARCHIPELAGO tkau, 2008; Comes & Jaros, this volume) and the Brassica cretica complex (Edh, Widén, & First division of the Aegean in Ceplitis, 2007). For more information concern- phytogeographical areas ing the palaeogeography of the Aegean, see The modern botanical exploration of the Chapter 1. Aegean Islands dates back to the late 18th cen- The intriguing geological history of the tury (see Lack & Mabberley, 1999). The substan- Aegean has been a major factor in the area’s tial plant distribution data collected by pioneer phytogeographical patterns creation (e.g. Crowl botanists working in the Aegean enabled Turrill et al., 2015). During the Pliocene, when the cli- (1929) to first divide the area in six phytogeo- matic conditions changed from fairly humid to graphical regions. Nearly two decades later, dry, the geographical and/or elevational range Karl-Heinz Rechinger from the Natural History of many plant species has changed and there Museum of Vienna, based on his extensive plant was a spatial isolation among populations locat- collections during his six field trips in the wider ed on different areas, resulting in subsequent Aegean area between 1927-1942, first ad- genetic divergence (Thompson, 2005). Many dressed the phytogeographical peculiarities of studies concerning the flora, endemism and the Aegean (e.g., Kykladenfenster, i.e., the ab- phytogeography in the Aegean region have sence of several taxa from the central Aegean been published (among others, Greuter, 1972, that are present in the Greek mainland and in 1975b; Runemark, 1971; Snogerup, 1967; the East Aegean Islands). By combining his own Snogerup & Snogerup, 1987; Carlström, 1987; records with those by other botanists, such as Strid, 1970, 1972, 1996, 2016a, b; Christo- Dörfler’s from Crete, Hedenborg’s from Rodos doulakis, 1996; Panitsa, Tzanoudakis, Triantis, & and Ade’s from Tilos and Karpathos, Rechinger Sfenthourakis, 2006; Panitsa, Tzanoudakis, & published several monumental works: “Flora Sfenthourakis, 2008, Georghiou & Delipetrou, Aegaea” (Rechinger, 1943a), “Contributions to 2010; Bittkau & Comes, 2005, 2009; Comes et the Cretan flora” (Rechinger, 1943b) and “Flora al., 2008; Crowl et al., 2015; Kougioumoutzis, Aegaea Supplementum” (Rechinger, 1949), fol- Tiniakou, Georgiou & Georgiadis, 2014, 2015; lowed by the “Features of plant distribution in Kougioumoutzis, et al., 2017; Strid & Tan, 2017) the Aegean” (Ι-ΙΙΙ) (Rechinger, 1950). documenting the presence of endemic relict Τhe criteria which led Rechinger to the im- species with a long paleobotanical history and print of theexplicit phytogeographical division of with no close relatives in the current flora as al- the Aegean had been: i) the distribution range so of endemic species that evolved compara- of non-endemic plant taxa, which are restricted tively recently and chiefly by non-adaptive radi- to certain parts of the Aegean such as several ation (Runemark, 1969, 1970, 1971). Evolution- Anatolian (Aristolochia hirta, Centaurea urvillei, ary older plant taxa that already occurred in the Fritillaria bithynica), North-African (Medicago Aegean islands they now inhabit long before heyniana, Lycium schweinfurthii, Zygophyllum these became isolated from the adjacent main- album) and Balkan elements (e.g. Paeonia pere- land, consist the relict element of the Aegean grina), ii) the contrast of some taxa being ab- flora; species that migrated from the adjacent sent from certain areas, whereas they are wide- mainland constitute the telechorous or migrato- ly distributed in other ones (Kykladenfenster), ry element and species that reached several iii) the proportion of endemism as a feature of 14_Layout 1 6/9/2018 11:20 ππ Page 227

227 Plant Diversity and Biogeography of the Aegean Archipelago: A New Synthesis

some parts of the Aegean and iv) the existence 4. The East Aegean, deemed as the phytogeo- of several vicariant taxa (Rechinger, 1943b, graphical border between Europe and Asia, 1950; Rechinger & Rechinger-Moser, 1951). characterized by a large number of Anatolian Rechinger’s line generally coincides with the plant taxa. Mid Aegean Trench (MAT) and has long been re- 5. The Central Aegean, viz. the Cyclades island garded as a very strong biogeographical bound- group, which lacks a relatively large number ary, largely due to the scarce occurrence of Ana- of species otherwise distributed along the tolian floristic elements west of this line.Indeed, rest of the archipelago. for some species complexes (e.g., Juniperus 6. The South Aegean island arc (SAIA), consti- phoenicea aggr.,and the Roucela clade in east- tuted an island bridge between mainland ern Mediterranean Campanulaceae), the Greece and Anatolia. It included Crete, the Aegean Sea separating the Balkan and Anatolian largest and highest Greek island. Peninsulas poses as a considerable biogeo- The western and easternpart of SAIA were graphical barrier between Europe and Asia thought to be more strongly connected – in acting in a similar way to the Strait of Gibraltar floristic terms – with the adjacent mainland: the in the western Mediterranean basin, thus trig- Peloponnisos and Asia Minor, respectively. First gering the divergence of European and Asian and foremost, the Kythira island group is one of taxa and indicating the important role of the the most floristically and phytogeographical lyin- Aegean Sea in the diversification of these close- triguing Aegean mini-archipelagos (Tzanoudakis, ly related taxa (e.g. Sobierajska et al., 2016; Panitsa, Trigas, & Iatrou, & 2006); not only it Crowlet al., 2015; Mazur et al., 2018). Neverthe- shares several plant taxa with Peloponnisos less, Rechinger’s line seems to represent a (Rechinger, 1967; Strid, 1996; Trigas, Tsiftsis, rather weaker than previously thought biogeo- Tsiripidis, & Iatrou, 2012), but also an almost graphical barrier, since the central Aegean acts equal number of taxa occur there, as well as in as a transitional biogeographical zone between Crete (Rechinger, 1967). Furthermore, Rodos Asia and Europe, filtering the distribution of constituted the cornerstone between the phyto- taxa originating from mainland Greece, Anato- geographical regions of South and East Aegean, lia, Crete and the northern Aegean (Kou- because it held a dual phytogeographical position gioumoutzis et al., 2017). between those two regions (Rechinger, 1967). Both Turill and Rechinger noticed the abrupt phytogeographical differences between the Cy- clades and the East Aegean Islands, drew the Current widely used phytogeographical phytogeographical line dividing Asia from Eu- subdivisions of the Aegean rope (i.e. Rechinger’s line) and laid the founda- Flora Europaea, based on Rechinger’s data, as tions of the Aegean’s prevailing phytogeographi- well as other more recent in-depth studies such cal subdivision (Rechinger & Rechinger-Moser, as those of Turland, Chilton, and Press (1993), 1951). The consequent phytogeographical re- Jahn and Schönfelder (1995), and the Flora Hel- gions of the Aegean were: lenica project (Strid & Tan, 1997), consider Crete 1. The West Aegean, comprising numerous and the insular complex of Karpathos as a dis- species occurring in mainland Greece; these tinctive phytogeographical unit. plant assemblages were an amalgamation of Furthermore, a double phytogeographical the east Mediterranean, the Balkan and the role is attributed to the central part of the South south European floristic elements. Aegean Arc, namely Antikythira, Crete and the 2. The North Aegean, that comprised a zone in Karpathos complex by Greuter (1971); Not only which many taxa reached the southernmost they belong to the South Aegean region, but al- limit of their geographical distribution. so they are related with Cyclades, all together 3. The Northeast Aegean, constituted by taxa constituting the part of the Aegean which is phy- of eastern distribution (mostly Anatolian togeographically more isolated from the conti- plant taxa). nental landmass. Greuter (1971) had named this 14_Layout 1 6/9/2018 11:20 ππ Page 228

228 Plant Diversity and Biogeography of the Aegean Archipelago: A New Synthesis

region “Cardaegean” (“Kardägäis” in German), module SMI, Evvoia and the western part of i.e. “heart of the Aegean”. Runemark (1971) South Aegean Arc are grouped together with added the island of Ikaria to “Cardaegean”. Τhe the southern parts of mainland Greece (Pelo- “Cardaegean” is mainly characterized by: (a) a ponnisos: Pe, and Sterea Hellas: StE). Ιn the unique endemic element, namely endemics oc- Central Aegean module (CAE), the Cyclades are curring exclusively in the Cretan area and in the grouped together with Northern Sporades and southern and central Cyclades (Greuter, 1975b), Limnos. North-Eastern Aegean module (NE-AE) (b) the lack of species which spread during the extends from Lesvos to Kos. The Southeast Pleistocene, (c) small species numbers except for Aegean module (SE-AE) is formed by the com- Crete, (d) a large number of anthropochorous plexes of Rodos, Karpathos, Nisyros, Tilos, Symi species, and (e) a significant relict element and Chalki, while Crete is a separated phytogeo- (Greuter, Pleger, & Raus,1983). graphical region (KR). The delimitation of these The South Aegean floristic element, correlat- six Aegean biogeographical regions is in almost ed to the South Aegean Arc reflects the east to complete harmony with the archipelago’s west migration during the Miocene and the palaeogeographical evolution from the middle “Cardaegean” element (the Cretan area and the Miocene to the end of the Pleistocene. The bio- South and Central Kik) and the palaeogeograph- geographical barriers of the mid-Aegean trench ical situation during the Pleistocene (Greuter, and the North Aegean trench seem to have in- 1971, 1975b). fluenced plant distribution patterns, and the In the frame of the Flora Hellenica project, phytogeographical subdivision of the Aegean, Greece was divided in 13 phytogeographical re- both locally and regionally, is similar to the gions (Strid, 1996, Strid & Tan, 1997). Five of Aegean’s past and contemporary climatic diffe- these regions (NAe: North Aegean, WAe: West rentiation (Kougioumoutzis et al., 2017). Aegean, EAe: East Aegean, Kik: Central Aegean- Cyclades, and KK: Crete-Karpathos) spread in the Aegean archipelago (Figure 1). This subdivi- Molecular studies for plant sion is principally a practical one (Strid, 2000) diversification and speciation and it is widely accepted and used in most of in the Aegean the floristic and phytogeographical studies. Es- Recent molecular studies (Bittkau & Comes, 2005; pecially concerning the Aegean, it also demon- Edh et al., 2007) support the theory that plant di- strates phytogeographical borders, based upon versification and speciation in the Aegean region is Rechinger (1943, 1950), whose aspects proved driven mainly by random (genetic drift) rather to be exceptionally precise, even on the basis of than adaptive differentiation among isolated po- contemporary enriched floristic data from the pulations (Runemark, 1969; Strid, 1970; Snogerup, Aegean (Strid, 1996, 2000). Gustafsson, & von Bothmer, 1990; Thompson, 2005). Cellinese et al. (2009) showed that most Cretan Campanula species were present in the is- Recent aspects of the Aegean lands at the time of their isolation, and very little phytogeographical classification long-distance dispersal to Crete and diversification Building upon the aforementioned phytogeo- within Crete has occurred since then. Τhey con- graphical subdivision, Kougioumoutzis et al. cluded that endemism is probably driven by loss of (2017) presented the most recent biogeographi- species on the mainland after island isolation and cal classification of the Aegean archipelago. Via that species on the islands may have been more a network optimization approach, six large high- widespread in the past, but they are now restrict- ly linked subgroups of islands and plant taxa ed to often inaccessible areas, probably as a result (biogeographical modules) were identified in of human pressure. Crowl et al. (2015) stated that the Aegean (Figure 1). The northernmost mod- the evolutionary history and current distributional ule (NMI) consists of Thasos and Samothraki to- patterns of endemic Roucela complex (Campanu- gether with north mainland Greece (NE). In laceae: Campanula) are the result of both disper- 14_Layout 1 6/9/2018 11:20 ππ Page 229

229 Plant Diversity and Biogeography of the Aegean Archipelago: A New Synthesis

sal and vicariance events (through the Miocene 1995 for references; Bergmeier & Dimopoulos, and onward) mainly driven by rising sea levels and 2001; Bergmeier et al.,2011; Christodoulakis, continental fragmentation. However, Jaros, Trib- 2000; Tzanoudakis et al., 2006, Panitsa & sch, and Comes (2018) concluded that the MAT Tzanoudakis, 1998, 2001, 2010; Panitsa et al., does not seem to have played a vicariant role in 2004; Panitsa, Tzanoudakis, Triantis & Sfen- shaping diversification within Nigella, despite its thourakis, 2006, 2008; Tzanoudakis et al., 2006; importance as a barrier to dispersal and gene flow Snogerup & Snogerup, 2004). in Aegean biota (among others, Runemark, 1980; Small island floras have special features Crowl et al., 2015; Poulakakis et al., 2014; Sfen- (Bergmeier & Dimopoulos, 2001). They may in- thourakis & Triantis, 2017). Hilpold et al. (2014) clude single – islet endemics such as Anthemis concluded that there is a clear relation between glaberrima (Rech. f.) Greuter (Greuter, 1968) oc- geography and the structure of the molecular curring on Agria Gramvousa, off western Crete, data studying phylogeny of species of the genus and is considered as a Critical Endangered Centaurea. Kozlowski, Frey, Fazan, Egli et al. species, included in Annex II of the Directive (2014) mentioned that relict species provide a 92/43/EC of priority for protection, or Allium unique opportunity to understand past and re- platakisii Tzanoud. & Kypriot. found on Pon- cent biogeographical and evolutionary processes tikonisi, an islet between Crete and Antikythira studying Zelkova abelicea (Ulmaceae), one of (Tzanoudakis & Kypriotakis, 1993), and others. the most prominent Tertiary relict trees of the Small islands also host some taxa shared among Mediterranean region, the only tree endemic to them; these are apparently “islet specialist” Crete, and promoted the development of new plant taxa occurring chiefly on islets not more approaches for the improvement of conservation than a few hundred hectares in size (Rechinger strategies for Tertiary relict trees characterized by & Rechinger-Moser, 1951; Runemark, 1969; major local disjunctions. Bosque et al. (2014) not- Höner & Greuter, 1988; Raus, 1989, 1991; Hön- ed that the persistence of the species to climate er, 1990, Panitsa & Tzanoudakis, 2001; Geo- changes seems to be more complicated and multi- rgiou, Panitsa, & Tzanoudakis, 2006). Bergmeier factorial than a linear and plain view of species and Dimopoulos (2003) discussed the relation survival in climate refugial areas, and therefore between the occurrence and proportion of islet calls for a consideration of the processes in future specialist plant taxa and island area, altitude, conservation planning. and grazing. Plant assemblages on these islets Bittkau and Comes (2009), Comes et al. can be locally affected by random events and (2008), Jaros et al. (2018), and Comes and Jaros the irregular plant species distribution patterns (this volume) emphasized the need to investi- can be explained by the reproductive drift ob- gate further biological and landscape features served among the populations of taxa on small and contemporary vs. historical processes in islands (Runemark, 1969). Non-adaptive radia- driving population divergence and taxon diversi- tion is considered the primary evolutionary driv- fication in Aegean plant radiations. er of their small populations (Snogerup, 1967; Runemark, 1970; Strid, 1970). Additionally, reproductive drift is observed Small islands among the populations of taxa on small islands There is no standard threshold to separate small and this phenomenon explains the irregular en- from large islands. Small islands or islets are demism pattern and the presence/absence pat- usually considered those which are not able to tern of some non-endemic species on small is- support permanent human activities. According lands (Runemark, 1969). to Greuter (2001) the smallest of the islets In most archipelagos, as island size decreas- should be prioritized in the nature conservation es, area gradually becomes inadequate for the of the Mediterranean Basin. Many studies con- estimation of species number (Burns, McHardy, cerning small islands of the Aegean area have & Pledger, 2009). The phenomenon termed been published (e.g. see Panitsa & Tzanoudakis, ‘Small Island Effect’, initially mentioned by Pre- 14_Layout 1 6/9/2018 11:20 ππ Page 230

230 Plant Diversity and Biogeography of the Aegean Archipelago: A New Synthesis

ston (1962), is observed when on islands small- change and disturbance that have a significant er than an area’s threshold value, species rich- complicating effect on community dynamics, ness fluctuates due to factors other than area enhancing observed turnover rates. (e.g. Sfenthourakis, 1996; Whittaker, 1998; Lo- molino, 2000; Triantis et al., 2006). Geophysical traits, such as elevation, islets’ AEGEAN PLANT DIVERSITY IN shape and degree of isolation, habitat diversity, GENERAL TERMS – TOTAL PLANT minimum distance from the nearest species pool SPECIES RICHNESS and micro-ecological differences, occasional dis- Uotila (2017) showed that the Aegean area be- turbances and other stochastic events, and hu- longs to one of the floristically well-mapped ar- man interventions, such as grazing and fire, have eas, mainly within the framework of several de- been considered as factors determining how tailed projects: i) the Atlas of the Aegean Flora many and which species are able to maintain (Strid, 2016a, b), ii) the Annotated Checklist of their populations on small islands (e.g Beyhl, the Vascular Plants of Greece (Dimopoulos et 1990; Morrison, 1997, 2002; Bogaert, Salvador- al., 2013, 2016), which recorded the distribution Van, Eysenrode, Impens, & Van Hecke, 2001, of the plant taxa in the 13 floristic regions of Bridges & McClatchey, 2005, Forman, 2006). Greece, the five floristic regions of the Aegean Species richness on small islands may behave included, but also iii) Flora Hellenica (Strid & idiosyncratically, but this does not always lead to Tan, 1997, 2002) and iv) Atlas Florae Europaea, a typical Small Island Effect (Panitsa et al., 2006). a running, long-term program for mapping the A ‘Small Island Effect’ was observed in the cen- distribution of vascular plants in Europe. tral, central – eastern and southern part of the Tzanoudakis and Panitsa (1995), Montmollin Aegean, for islets with an area extent less than and Iatrou (1995), Turland et al. (1993), 1.165 km2 for which the species – area relation- Georghiou and Delipetrou (2010), Kagiampaki ship was the dominant factor determining (2011), Strid (1996, 2006, 2016), and Strid and species richness but significantly weaker, com- Tan (2017) have presented until now the pared to the respective relationship for larger is- progress in plant taxonomical, floristic and phy- lands (Kagiampaki, 2011). Minimum distance togeographical studies concerning Greece or from the nearest large island and disturbance more specifically the Aegean islands and Crete. penetration distance combined with area, man- Since the later publication, eight recently dis- aged to slightly increase the percentage of plant covered plant taxa (5 species, 2 subspecies and species richness explained (Kagiampaki, 2011). one comb. & stat., have been described from Turnover in time has been examined by the Aegean area (Kleinsteuber, Ristow, & Has- Snogerup and Snogerup (1987, 2004) and Panit- sler, 2016; Galanos & Tzanoudakis, 2017; Trigas, sa et al. (2008) providing evidence for rapid Kalpoutzakis, & Constantinidis, 2017; Rätzel, Ris- shifts in species number that may nonetheless tow, & Uhlich, 2017; Kypriotakis, Antaloudaki, & be considered as equilibrial dynamics, as islets Tzanoudakis, 2018; Vladimirov, Dane, Matevski, are able to respond rapidly to environmental & Tan, 2016; Raab-Straube & Raus, 2017).

Table 1 ¡ Floristic analysis of the 5 Aegean phytogeographical regions. In parentheses, the percentage of the whole Greek flora. Data according to Dimopoulos et al. (2016).

Families Genera Species Subspecies Taxa NAe 145 (78.4) 678 (63.2) 1928 (33.5) 494 (25.1) 1932 (29.2) WAe 146 (78.9) 695 (64.8) 2024 (35.1) 582 (29.5) 2084 (31.5) KiK 136 (73.5) 619 (57.7) 1661 (28.8) 458 (23.2) 1750 (26.4) KK 146 (78.9) 703 (65.5) 2079 (36.1) 571 (29.0) 2214 (33.4) EAe 151 (81.6) 756 (70.5) 2381 (41.3) 660 (33.5) 2520 (38.1) 14_Layout 1 6/9/2018 11:20 ππ Page 231

231 Plant Diversity and Biogeography of the Aegean Archipelago: A New Synthesis

The number of species per surface unit is an togeographical area in the Aegean in terms of important parameter of Aegean vascular plant di- native plant species richness (Figures 3-4). On versity, regarding the conservation of the diversity the other hand, rates of range-restricted ness of the Aegean area (Panitsa & Tzanoudakis, 2010). exceed the respective endemism rates in EAe, Jahn (2003) determined plant species diversity WAe and ΝAe. Moreover, the phytogeographical per unit area by subdividing the island of Crete by region of Kik, which has long been held as floris- means of a grid into 343 unit areas (cells) empha- tically impoverished (but see Kougioumoutzis & sizing that richness in species and endemics are Tiniakou, 2014), emerges as the second richest important criteria for plant protection. Aegean phytogeographical region in terms of Greek and Aegean endemic plant species rich- ness and no longer stands out as the poorest Endemic and range-restricted species Aegean phytogeographical region, regarding na- richness tive plant species richness, thus confirming the Dimopoulos et al. (2013, 2016) noticed that findings by Kougioumoutzis and Tiniakou both the highest and the lowest endemism rate (2014). among the Greek floristic regions are within the Dimopoulos et al. (2013, 2016) mentioned Aegean area. The highest (17.7%) and lowest that range-restricted taxa provide valuable in- (3%) endemism rate is observed in the phyto- formation on the local character, the unique- geographical regions of KK and NAe, respective- ness and relations of the Greek and Aegean flo- ly. KK hosts 392 Greek endemic taxa. KK is thus ra. The Aegean’s range-restricted flora consists the most important endemic hotspot not only in of 893 taxa, 702 of which are Greek endemics the Aegean region, but in the entire Mediter- and 577 of these taxa are found only on one of ranean Basin (Médail, 2017). the 5 Aegean phytogeographical regions (Figure It should be underlined that the vast majority 2). Figure 5 presents habitat preferences of the (62%) of the 740 endemic taxa, are regional en- endemic and range-restricted plant taxa of the demics (occurring in one of the 5 Aegean floris- Aegean area and the differences with the ones tic regions) while 17.7% are Greek endemics of the total Aegean flora. found also on one of the 5 Aegean floristic re- Most of the endemic and the range-restrict- gions (EAe, WAe, Kik, ΝAe or KK). Table 3 pres- ed taxa are plants occurring Mediterranean an- ents the number of common plant taxa of the nual-rich grasslands and phrygana grasslands, whole flora and of the endemic flora among the followed by plants found in grasslands, repre- five Aegean floristic regions. Figure 2 presents senting submediterranean/temperate lowland the percentages of vascular endemic, and en- demic range-restricted plant taxa in each of the Aegean phytogeographical regions of Greece. Figure 3 shows in box plots the Aegean endemic and single island endemic species richness pat- terns in different phytogeographical areas for is- lands with large and small size and Figure 4 presents native, Aegean endemic and single is- land endemic species richness in different phy- togeographical areas. When comparing the pat- terns of endemism and range-restrictedness rates of the Aegean phytogeographical regions, it becomes evident that KK presents a high en- demism rate combined with a high rate of range-restrictedness. The phytogeographical re- FIGURE 2 ¡ Percentages of vascular endemic, endemic gion of KK can be regarded not only as a specia- range-restricted and range-restricted plant taxa in each tion hotspot, but also as the richest island phy- of the 5 Aegean phytogeographical regions of Greece. 14_Layout 1 6/9/2018 11:20 ππ Page 232

232 Plant Diversity and Biogeography of the Aegean Archipelago: A New Synthesis

FIGURE 3 ¡ Aegean endemic and single island endemic species patterns in different phytogeographical areas for islands with large and small size. 14_Layout 1 6/9/2018 11:20 ππ Page 233

233 Plant Diversity and Biogeography of the Aegean Archipelago: A New Synthesis

FIGURE 4 ¡ Native, Aegean endemic and single island endemic species richness in different phytogeographical ar- eas. Abbreviations as in Figure 1. 14_Layout 1 6/9/2018 11:20 ππ Page 234

234 Plant Diversity and Biogeography of the Aegean Archipelago: A New Synthesis

Tzanoudakis et al. (2006) and Panitsa et al. (2004) studied the flora of Antikythira island and the offshore islets of Kythira and Antikythi- ra, and Trigas et al. (2012) showed the conserva- tion importance of Kythira, an island that to- gether with Antikythira and offshore islets, be- long to the phyrogeographical area of Pelopon- nisos (PE) and are not included in the five phy- togeographical areas of the Aegean. Some islands like Evvoia and Samos have a dual role, as they not only host many regional en- FIGURE 5 ¡ Habitat categories represented among all demics, but also numerous Single Island En- taxa, endemic taxa and endemic range-restricted taxa demics (SIE) while other islands such as Crete, of the Aegean area. Abbreviations as in Dimopoulos et Karpathos, Naxos, Amorgos, Ikaria and Rodos can al. (2013, 2016): A: freshwater; C: cliff; G: sub-Mediter- be regarded as genuine hotspots of Aegean en- ranean grassland; H: high mountain; M: coastal/ma- demism and they have acted as speciation cen- rine; P: Mediterranean grassland and phrygana; R: rud- tres and/or refugia for the in situ evolved Aegean eral and agricultural; W: woodland. endemics (Kougioumoutzis et al., 2014, 2017). A large amount (44.4%) of the plant taxa in- cluded in Annexes II, IV & V of the Directive to montane pastures and meadows and then 92/43/EU for the Natura 2000 network are agricultural and ruderal habitats. Specialist found on the Aegean islands. Some of the most plants of high mountains, cliffs, freshwater and prominent members of this list, are islet spe- coastal habitats, although represented in low cialist plant taxa, such as Anthemis glaberrima proportions, are remarkably prominent in the and Silene holzmannii, as well as single island Aegean flora. endemic taxa, such as Bupleurum kakiskalae.

Table 2 ¡ Endemic and range-restricted plant species richness and rates (in parentheses) of the 5 Aegean phyto- geographical regions. Data according to Dimopoulos et al. (2016).

Families Genera Endemic taxa Range restricted All Aegean regions 50 204 740 702 NAe 23 44 57 (3.0) 82 (4.2) WAe 36 101 102 (4.9) 217 (10.4) KiK 27 77 162 (9.2) 169 (9.6) KK 44 160 392 (17.7) 388 (17.5) EAe 31 79 152 (6.0) 259 (10.3)

Table 3 ¡ Number of common plant taxa among the Aegean phytogeographical regions. Above the diagonal, num- bers of common taxa of the whole flora of the regions, below the diagonal numbers of endemic taxa. On the diago- nal, the first number is the endemic taxa and the second is the total taxa per region.

NAe WAe Kik KK EAe NAe 57 1932 1370 1153 1138 1395 WAe 13 202 2084 1310 1298 1332 KiK 12 42 162 1750 1415 1508 KK 6 29 70 392 2214 1577 EAe 14 28 52 51 152 2520 14_Layout 1 6/9/2018 11:20 ππ Page 235

235 Plant Diversity and Biogeography of the Aegean Archipelago: A New Synthesis

Ten of the Top 50 critically endangered Mediter- Thasos 8 SIEs. Kagiampaki, Triantis, Vardinoyan- ranean Island Plants are hosted on seven Aegean nis, and Mylonas (2011) discussed available evi- islands, namely, Crete (Anthemis glaberrima, dence on local endemics in the South Aegean in- Bupleurum kakiskalae, Convolvulus argy- dicating some cases of in situ speciation like en- rothamnos and Horstrissea dolinicola), Evvoia demic mountain flora of the island of Crete, old (Allium calamarophilon and Minuartia dirphya), relics and SIE. Triantis, Mylonas, and Whittaker Kythira (Polygala helenae), Elafonisos (Saponar- (2008) concluded that islands can be considered ia jagelii), Samos (Consolida samia), Skyros and equivalent to biological provinces for single-is- Skyropoula (Aethionema retsina) (Pasta, Perez- land endemics. Graber, Fazan, & Montmollin, 2017). Kallimanis, Panitsa, Bergmeier, and Di- mopoulos (2011) defined palaeo-endemics as Ruderal plant diversity - Alien and reproductively and geographically isolated weeds species without close relatives and neo-en- According to Dimopoulos et al. (2013, 2016) on demics as taxa with many closely related the five Aegean phytogeographical regions rud- species. They found that palaeo-endemic eral plant taxa represent 37-41.6% of the total species richness is correlated only to island flora, 7.5-13% of which are alien taxa. Concern- area and this is also supported by the presence ing their chorology, it is interesting to mention of palaeo-endemic species only on six of the that 1-2.4% are endemics and 1.3-2.7% are largest Aegean islands. On the other hand, range-restricted. Turland, Phitos, Kamari, and they showed that neo-endemics as a propor- Bareka (2004) and Bergmeier (2006) studied the tion of the islands flora, is associated only with distribution and diversity of plants of traditional the islands’ maximum elevation and that neo- agriculture, the weeds of traditional agriculture endemic species richness is also strongly corre- from Crete (KK), and Bergmeier and Strid (2014) lated to island area and diversity of geological from all over Greece, including information for substrate indicating that an island’s habitat the five Aegean phytogeographical regions. heterogeneity is the main environmental driver These authors demonstrated that arable plants of speciation. reflect phytogeographical and bioclimatic differ- Dimitrakopoulos, Memtsas, and Troumbis entiation, in particular along a south–north gra- (2004), Trigas, Iatrou, and Karetsos (2007), Panitsa dient. Galanos (2015) studied the alien flora of et al. (2010), Iliadou, Kallimanis, Dimopoulos, and terrestrial and marine ecosystems of Rodos is- Panitsa (2014) found low association between land (EAe). overall species diversity and endemic species rich- Gritti, Smith, and Sykes (2006) simulating the ness for Greek as also for Aegean vascular plants. vegetation biogeography and dynamics on two Kallimanis et al. (2010) found that the environ- of the main islands of the Aegean (Crete and mental factors driving total plant species richness Lesvos) among others, indicated that the effect and endemic plant species richness differed of climate change alone is likely to be negligible markedly and that there was a lack of correlation and that the rate of ecosystem disturbance was between total species richness and single island the main factor controlling susceptibility to inva- endemic (either neo- or palaeo-endemic) diversity sion, strongly influencing vegetation develop- as a proportion of the islands flora. ment on the shorter time scale. Many alien A significant proportion (42.4%) of the en- plant assemblages on different islands present demic taxa occurring in the Aegean archipelago is an idiosyncratic nature since most alien plants considered Single Island Endemics (SIE).The vast established on Mediterranean islands have the majority (68.4%) of the Aegean endemics regis- potential to become naturalized on more is- tered on one of the 5 Aegean phytogeographical lands and regional ecological surveys may pro- regions. The island of Crete hosts 61.8% of the vide an adequate means to assess this risk SIEs and the island of Evvoia 13.4%. Ikaria, Rodos (Lloret, Médail, Brundu, & Hulme, 2004; Lloret and Samos host 12 SIEs each, Samothraki 9 and et al., 2005; Hulme et al., 2008). 14_Layout 1 6/9/2018 11:20 ππ Page 236

236 Plant Diversity and Biogeography of the Aegean Archipelago: A New Synthesis

FACTORS AFFECTING PLANT SPECIES semblance between the phytogeographical RICHNESS compartmentalization of the Aegean both lo- cally and regionally with the Aegean’s past and Several researchers have addressed the factors present climatic compartmentalization and no- driving the Aegean plant species richness pat- ticed that an island’s network position in the terns. The most prominent of these factors are Aegean seems to be affected also by contrast- discussed below. ing climate regimes and not only by area, eleva- tion and geographical isolation. Iliadou et al. Human presence (2014) discussed the effect of the climate con- cluding that low precipitation and associated Sfenthourakis and Triantis (2017) underlined summer drought stress in the Aegean might that the understanding of the interplay between limit the dominance of competitive common human presence, establishment of exotic species, allowing the persistence of more vul- species and extinction of indigenous biotas, is of nerable threatened species. Kougioumoutzis critical importance.Human influence is long-last- and Tiniakou (2014) showed that mean annual ing in the Aegean as in the whole Mediter- precipitation has a strong negative impact on ranean area and human factor has significantly the endemic species richness in Kik and con- shaped the Aegean flora since synanthropic strains the dispersal of several Greek endemic floristic element reaches 30%-50% of some is- species in the region. land floras and it is the most effective vector for Kougioumoutzis et al. (2014) also indicated long-distance dispersal (Greuter, 1975b, 1979, that despite the long recognized floristic impo- 1995, 2001; Cellinese et al., 2009; Triantis & My- verishment of the Cyclades islands (Kik), some lonas, 2009, Kallimanis et al. 2010, Trigas, Panit- areas are actually plant diversity hotspots and sa, & Tsiftsis, 2013). Kougioumoutzis and Tiniak- that there is a phytogeographical compartmen- ou (2014) suggested that the human factor has talization within the central Aegean, which re- played a major role in shaping the pattern ob- flects two main traits of the area; the palaeo- served in the endemic species present in the Cy- geographical evolution since the Last Glacial clades. Stefanaki and Kokkini (2015) noticed Maximum (ca. 20 ka), as well as the climatic that at least some of the rare species recorded subdivisions of the same islands. Meusel, Kast- exclusively in anthropogenic habitats owe their ner, and Raus (1984) while working in the SE occurrence there to human activity, and Aegean area on Carlina tragacanthifolia, stated Bergmeier and Strid (2014) determined the dis- that its distribution is explained ecoclimatically tribution patterns and the rarity of many wild by favourable warm winter temperatures and plant species of traditional agriculture in Greece extremely hot summer temperatures in a terri- revealing the unique character of the east tory with little rainfall. Aegean arable flora. Human presence and the Another aspect of the role of the climate as a multiplicity of the Aegean geological history are factor affecting plant species richness in the the main factors affecting Aegean island land- Aegean is that climate significantly shapes scapes and their cultural aspects (Panitsa & Di- species richness within plant–pollinator com- mopoulos, 2015). munities (Petanidou et al., 2017).

Climate Area, elevation and habitat diversity Climatic differentiations within the Aegean Area and elevation are the major drivers of have an impact on both the plant distribution plant diversity patterns in the Aegean (Panitsa and species richness patterns, as well as on the Trigas, Iatrou, & Sfenthourakis, 2010; Kallimanis diversification patterns in the region (Kou- et al., 2011) and they have a high significance in gioumoutzis et al., 2014; Crowl et al., 2015). the differentiation of the Aegean plants (Tri- Kougioumoutzis et al. (2017) indicated the re- gaset al., 2013; Steinbauer et al., 2016; Kou- 14_Layout 1 6/9/2018 11:20 ππ Page 237

237 Plant Diversity and Biogeography of the Aegean Archipelago: A New Synthesis

gioumoutzis et al. 2014, 2017; Kougioumoutzis the whole Mediterranean area (Médail & Ver- & Tiniakou, 2014). laque, 1997). Cliffs are a conspicuous feature of Kagiampaki et al. (2011) provided evidence the Aegean landscape, as also of the Mediter- that species richness and area are strongly relat- ranean, and probably played an important role ed for the South Aegean total vascular species as a refuge, particularly maritime cliffs and richness, endemism and richness of each plant those with a southerly exposure (Thompson, family. Delipetrou and Georghiou (2010) found 2005). In cliffs, Thompson (2005) mentioned the than in insular regions there is a predominance fact that obligatory chasmophytes may have of local endemics restricted to or occurring at the persisted alongside with plants characteristic of thermo-Mediterranean zone, which decreases as contemporary garrigues, phrygana, and maquis the coverage in high mountain sincreases (e.g. KK vegetation during the glacial maxima (Davis, and NAe). 1951; Snogerup, 1971). On the Cyclades, the Concerning the island of Crete, SIE species present endemic flora grows almost exclusively richness has a unimodal pattern to elevational in habitats that are inaccessible to man and his gradient with a peak at 1,500 m a.s.l. that is domestic animals (Snogerup, 1985). This phe- holding steady when individual Cretan moun- nomenon according to Runemark (1971) is at- tains are considered, indicating that the hump- tributed to the less competitive nature of the shaped pattern of SIE is not an artefact of in- endemic Aegean flora against such kind of pres- creasing heterogeneity of the SIE species com- sure; most endemic species do not belong to a position with increasing altitude among the Cre- climax community and do not grow in the habi- tan mountains (Trigas et al., 2013). The latter tat which is most suitable for them, but only in authors however also noticed that subendemic habitats where they are permitted to grow by species richness, show a monotonic decrease stronger competitors (Runemark, 1971). along the elevation gradient. These results are Rechinger (1965) stated that Aegean endemics further supportedby endemic species densities are mainly ancient mountain endemics with dis- along the elevation gradient and they are obvi- tribution areas older than the current land/sea ously not affected by taxon-specific traits, since distribution, since the present-day Aegean Is- numerous plant families and genera are repre- lands were mountain-tops in the geological sented in all endemic species groups averaging past. Indeed, the Aegean limestone cliffs very taxon-specific patterns. often harbour endemic taxa (Tzanoudakis et al., Panitsa et al. (2010), found that habitat di- 2006). As Snogerup (1995) states, Kalamos versity, of which elevation is another dimension, Peninsula in Anafi, is among the most important is the main factor affecting floristic richness, to- cliff refugia in the Aegean, as more than one- tal and most of the endemics levels (including third (37.8%) of the endemic flora of Anafi is lo- single island endemics), on East Aegean islands cated there (Kougioumoutzis, Tiniakou, Geor- except the Aegean endemics which are better giou, & Georgiadis, 2012) at elevations below predicted by elevation. They also noted that ele- 500 m a.s.l.; including many rare endemic taxa, vation can be considered also a dimension of such as Campanula laciniata and Sternbergia habitat diversity for plants, since higher islands greuteriana. This phenomenon can be also ob- offer a greater variety of habit at types across served in many other Cycladic Islands, such as which endemic plants are not normally distrib- Amorgos (Snogerup, 1995). uted. Legakis and Kypriotakis (1994) concluded Cliffs, screes, rocky and other habitats with that the combination of altitude and climate high stress level are dominated of stress tolera- creates high habitat diversity in Crete, which tors and correlated to the abundance of en- partly justifies the high endemism on the island demics (Kypriotakis & Tzanoudakis, 2001; and Kagiampaki et al. (2011) showed that habi- Tzanoudakis et al., 2006; Trigas, Iatrou, & Panit- tat diversity alone is sufficient in describing the sa, 2008; Panitsa et al., 2010; Panitsa & Kon- number of South Aegean endemics. topanou, 2017, etc.) and this is also the case for Topographic and geological heterogeneity 14_Layout 1 6/9/2018 11:20 ππ Page 238

238 Plant Diversity and Biogeography of the Aegean Archipelago: A New Synthesis

are among the most important factors promot- mountain isolation is not the main isolating fac- ing species richness globally (Whittaker & Fer- tor. Island isolation is expected to affect endem- nández-Palacios, 2007; Sfenthourakis & Triantis, ic species richness, and probably its relationship 2009) and locally (Kougioumoutzis & Tiniakou, to altitude, in a rather complex way (Trigas et 2014). Sfenthourakis and Panitsa (2011) also al., 2013). Kougioumoutzis et al. (2014), through showed that diversity at the whole-island scale the network biogeographical analysis of the is shaped mainly by heterogeneity among local central Aegean archipelago, confirmed the communities in small Aegean islands. The palaeogeographical and climatic compartmen- Choros model (Triantis, Mylonas, Lika, & Vardi- talization of the Cyclades (Kik) and showed that noyannis, 2003) provides about the same pre- the flora of the Cyclades (Kik) has not yet diction of endemics richness as the habitat di- reached the relaxation phase. This region may versity alone for the east Aegean small islands act as an ecogeographical filter for the distribu- (Panitsa et al., 2006) but it was most efficient in tion of several plant lineages across the Aegean shaping the number of south Aegean endemics Sea, while there seems to be a N–S-oriented (Kagiampaki et al., 2011). biogeographical barrier fundamental for both Trigas et al. (2013) evaluated drivers affecting plants and animals in the Aegean corresponding patterns along the elevational gradient on the is- to the palaeogeographical situation during the land of Crete, focusing on elevation, area, geo- middle Ionian (Kougioumoutzis et al., 2017). metric constraints (MDE), Stevens’ elevational Panitsa et al. (2010) indicated that the occur- Rapoport effect and the post-isolation uplift of rence of local endemics might be attributed ei- the Cretan mountains. They concluded that the ther to in situ speciation in environmentally di- response of plant species to environmental gra- verse localities or to the extinction of formerly dients on continental island systems are deter- more widespread species from nearby regions, mined by a combination of factors, each one due to the pronounced and repeated environ- with different intensity and duration of influence mental changes during the Pleistocene, to post- depending largely on historical parameters. glacial human-mediated disturbance, or even to Panitsa, Koutsias, Tsiripidis, Zotos, and Di- random relaxation processes. mopoulos (2011) describe an integrated GIS- Steinbauer et al. (2016) found an increase in based methodology for conservation value as- speciation caused by the isolating effect of to- sessment using the traditional species-based pography and suggested that the importance of and a habitat-based multi-criteria evaluation in isolation for speciation is consistent with the in- 49 small Aegean islands emphasizing the criteria crease in percent endemism with elevation of diversity, rarity, naturalness, replaceability around the world. Weigelt and Kreft (2013), and threat on each habitat type in combination quantifying island isolation, mentioned that al- with the number of significant plant taxa. Ka- though the distance to the nearest mainland is giampaki et al. (2011) examined habitat diversi- an adequate and easy-to-calculate measure of ty, based on a transformation of Southern isolation, accounting for stepping stones, large Aegean Indicator Values data (Böhling, Greuter, islands as source landmasses, climatic similarity & Raus, 2002) on light, temperature, moisture and the area of surrounding landmasses in- and soil salinity, considered some major opera- creases the explanatory power of isolation for tive factors which characterize plant habitats. species richness. Relationship of total and en- demic plant species richness of the Aegean is- lands with distance from nearest in habited is- Isolation land and from nearest mainland have been ex- The labyrinthine palaeogeographical and geo- amined in many studies (e.g. Iliadou et al., logical history of the Aegean archipelago has 2014; Panitsa et al., 2001, Tzanoudakis et al., strongly affected plant species distribution pat- 2006; Panitsa & Tzanoudakis 2001, 2010; Kalli- terns (e.g., Kougioumoutzis et al., 2017). On manis et al., 2010, 2011; Kagiampaki et al., long isolated continental islands like Crete, 2011; Kougioumoutzis & Tiniakou, 2014). 14_Layout 1 6/9/2018 11:20 ππ Page 239

239 Plant Diversity and Biogeography of the Aegean Archipelago: A New Synthesis

Geological substrate and structure GENERAL CONCLUSIONS Iliadou et al. (2014) stated that the number of Studies on biota of the Aegean islands have pro- Greek endemics and the number of threatened vided useful insights into several crucial ques- species appear to be strongly correlated to geo- tions in biogeography, ecology and evolutionary logical diversity in the Aegean islands. Trigas and biology (Sfenthourakis & Triantis, 2017). The Iatrou (2006) indicated the strong link of endem- whole Aegean archipelago, characterized as a ic taxa of Evvoia (WAe) to a specific geological natural laboratory for biodiversity, biogeography substrate (43.6% of the local endemic taxa are and evolution by many researchers, has a com- exclusively distributed on limestone) and also fo- plex geological and palaeogeographical history cused on the isolated serpentine areas of Evvoia that varies among its phytogeographical areas, which are of special phytogeographical interest, and a different combination of factors of vari- in particular with respect to their position at the able intensity and duration time that drives pat- southeastern periphery of the whole system of terns of its impressive plant species richness serpentine areas in the Balkans that represent and endemism. The question concerning factors an ancient core of speciation and act likewise as affecting plant species richness in the Aegean an important refugial habitat for relict elements has some answers, also revealed in the present (Stevanović, Tan, & Petrova, 2007). review, showing differences among the different Aegean phytogeographical areas, but the puzzle Kougioumoutzis and Tiniakou (2014) when remains incomplete. Whittaker, Fernández-Pala- studying islands of the SAVA, stated that geodi- cios, Matthews, Borregaard, and Triantis (2017) versity is an important factor in shaping plant suggested that the combination of increasing species diversity in the Cyclades, while mean an- application of molecular tools with advances in nual precipitation, human population density and functional trait biology holds promise for un- maximum elevation were significant predictors of locking many of the unresolved questions in the Greek endemics present in the Cyclades. longer-term (eco-evolutionary) island biogeog- Dimopoulos, Raus, Mucina, and Tsiripidis raphy. (2010) suggested that the formation of local Additionally, when considering biodiversity pioneer vegetation on the volcanic islands is conservation (from the species to the ecosys- not solely controlled by the age of the substrate tem and landscape levels), island ecosystems, (‘maturation’ of the communities through satura- strongly influenced by a diversity of global en- tion of their local species pools), but it is also un- vironmental changes related to land-use prac- der strong control of factors such as the distri- tices, climate change, sea level rise, fires and bution of ashes after the recent volcanic erup- biological invasions, provide significant chal- tions, and the chemical and physical proper- lenges and offer opportunities for a rapid ad- ties (e.g. nutrient content) of the soils formed vance of our understanding on fundamental by the deposition of the ashes. Karadimou, aspects of human relationships with nature Kallimanis, Tsiripidis, and Dimopoulos (2015) and of conservation strategies (Borges et al. and Karadimou, Tsiripidis, Kallimanis, Raus, 2018; Medail, 2017; Whittaker et al., 2017; and Dimopoulos (2016) found that different Whittaker & Fernández-Palacios, 2007; Nogué mechanisms play a leading role in community et al., 2017). Since human influence is ex- assembly at different scales, studying the tremely intense also on Aegean island ecosys- mechanisms driving community assembly be- tems, priority in conservation strategies should tween volcanic Aegean islands of different age be given in education and sensitization of local and history of vegetation development and in- population sto environmental issues and par- vestigating the relationship between trait- ticularly to the special value of Aegean islands based Functional diversity and area, the Func- as places that house unique components of tional Diversity - Area Relationship (FDAR) us- global biodiversity and, also as crucial parts of ing plant diversity data. our natural and cultural heritage. 14_Layout 1 6/9/2018 11:20 ππ Page 240

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