Biodiversity Journal , 2012, 3 (4): 281-296

Relict species and the challenges for conservation: the emble - matic case of sicula Di Pasquale, Garfi et Quézel and the efforts to save it from extinction

Giuseppe Garfì 1 & Stéphane Buord 2

1Istituto di Genetica Vegetale, Consiglio Nazionale delle Ricerche, corso Calatafimi 414 - 90129 Palermo, Italy; email: [email protected] 2Conservatoire Botanique National de Brest, 52, allée du Bot - 29200 Brest, France; email: [email protected]

ABSTRACT The foreseen rapid climate changes are thought to represent a major threat for many spe - cies. Owing to that, in the Mediterranean Basin, one the most important area worldwide for biodiversity, a number of taxa are at risk of extinction, especially the endemics and the rarest ones. Within them a particular significance is recognised to the pre-glacial relicts, that are rather conspicuous in the area and represent a valuable heritage for their biogeographical relevance and evolutionary history. Zelkova sicula is one of the most prominent within this flora. To date, it is a very rare species, and due to a number of threatening factors it is on the brink of extinction. In the present paper, we discuss the main topics related to its conservation criti - calities and the ongoing integrated strategies to save it from extinction. Particular emphasis is addressed to assisted colonisation, a “last resort” conservation approach consisting in the esta - blishment of pilot-planting out of the species native range.

KEY WORDS Assisted colonisation; clonality; Life+ EC programme; Sicily; threatened plants

Received 11.05.2012; accepted 20.12.2012; printed 30.12.2012. Proceedings of the 1 st International Congress “Insularity and Biodiversity”, May 11 th -13 th , 2012 - Palermo (Italy)

INTRODUCTION According to the IUCN Red List Categories and Criteria (IUCN, 2001), nine out of the ten Sicilian In the Mediterranean area a number of rare and species therein included are quoted as Critically En - threatened island plants have been recently the ob - dangered (CR) mainly due to their extremely re - ject of a campaign of awareness for their conserva - stricted area and/or the low number of surviving tion (Montmollin & Strahm, 2005). The campaign individuals. Zelkova sicula Di Pasquale, Garfì et was promoted by IUCN in order to mobilize con - Quézel is one of the most renowned and prominent servation practitioners, decision makers and the ge - taxa owed to both its biogeographical relevance and neral public to take actions needed to save from evolutionary history. extinction the most endangered species. Among the First described as a new species to the science fifty species considered, as much as ten were selec - in 1991 (Di Pasquale et al., 1992), Z. sicula is a gla - ted from Sicily and the surrounding islets, so highli - cial relict tree, taking part in the conspicuous con - ghting the notable significance of this region as a tingent of Sicilian relicts plants - e.g. Abies major biodiversity hotspot within the whole Medi - nebrodensis (Lojac.) Mattei, Bupleurum dianthifo - terranen Basin (Quézel & Médail, 2003). lium Guss., Cytisus aeolicus Guss. ex Lindl., Erica 282 GIUSEPPE GARFÌ & S TÉPHANE BUORD

sicula Guss., Petagnaea gussonei (Sprengel) Rau - etc.) has caused a lot of damages on insular biodi - schert, Pseudoscabiosa limonifolia (Vahl) Devesa, versity. Currently, islands figure amongst the most Thymus nitidus (Guss.) Jalas, etc. - that notably con - threatened territories on the earth. In this way, 2017 tribute to the world evolutionary inheritance, and out of over 7000 plant species of the Caribbean hot - remarkably significant for conservation of plant di - spot are threatened or even disappeared. Similarly, versity (Petit et al., 2005). among 3334 Polynesian and Micronesian species, In the present paper we outline an overview 926 are currently threatened (Brooks et al., 2002). about the special meaning of biodiversity in insular The recession of natural insular habitats is even environments, with some remarks on relict species more informative. The original forest which cove - and their vulnerability particularly in the Mediter - red Mauritius currently represents just 5% of the ranean. Within this issue, the case of Z. sicula , as total area of the island. In Madagascar, human oc - an outstanding representative of a relict and most cupation led to a diminution of 90% of the original threatened flora, will be discussed especially with forest in only 200 years. respect to the main topics related to its conservation criticalities and the ongoing strategies to take it Peculiarity and viability of the Mediterra - away from the brink of extinction. nean Basin flora

The five biggest Mediterranean biomes, i.e. Me - BIODIVERSITY, RELICT SPECIES AND diterranean Basin, California, Mediterranean Chile, THREATS IN INSULAR ENVIRONMENTS South Africa and Southwest Australia, count 50, 48, 50, 68 and 75% of endemic species respectively Biodiversity hotspots: the preponderance of (Médail & Quézel, 1997). With 5000 islands and insular environments and their vulnerability small islets, the Mediterranean Basin is one of the biggest insular sets in the world. There are more Conservation International identified 34 priority than 25000 superior plants according to Quézel zones for conservation. These hotspots are concer - (1985) and about 30000 species and subspecies ac - ning only 2.3% of earth’s area but gather more than cording to Greuter (1991). 50% of plant and 45% of animal species of the pla - net. They all are threatened by human activities. For This biodiversity is primarily due to the particu - the most part, these hotspots are made, totally or lar climatic conditions, habitat heterogeneity and partially, of islands and archipelagos, such as New different origins of the flora, which can be divided Zealand, East Melanesia, Polynesia, Micronesia, into three main biogeographic groups (Quézel Japan, Philippines, Indonesia, Sri Lanka, Madaga - 1985, 1995): a native species group, a southern af - scar and Indian Ocean islands, Caribbean islands, finity species group and a non-Mediterranean Ho - Mediterranean Basin islands, etc.. larctic-Eurasiatic group. Insular species are witnesses of a unique evo - In addition, geological, palaeogeographical and lutionary history. The endemism rate in insular en - historical factors have helped to create highly di - vironments is much higher than in continents. For verse environments and the insular mountain or iso - example, the Hawaiian archipelago counts 90% of lated edaphic systems generally appear to be major endemic species, whereas 50% of vascular plants endemic centres (Gómez-Campo et al., 1984). are endemic to Mauritius and 93% to Madagascar, Comparing the vascular flora of each of the above which contains as much as 8000 endemics. Given mentioned Mediterranean biomes, the circum-Me - these endemism rates, insular biodiversity repre - diterranean one shows the highest taxonomic ri - sents a very important part of world biodiversity, chness although the degree of endemism varies which has no link with the small area covered by from 50% (Quézel, 1985) to 59% (Greuter, 1991). these islands. Planetary insular environments are particularly Relict species and insularity in the Mediterranean fragile. Since the sixteenth century and European expansion, the impact of human activities (agricul - Regarding young islands, the isolation, the poor ture, urbanisation, introduction of invasive species, number of pioneer elements, the presence of unoc - Relict species and the challenges for conservation: the emblematic case of Zelkova sicula 283

cupied ecological niches and a natural selection Mediterranean plants and conservation issues lower than in the continent are major ways of spe - ciation. More insular refuges are likened to arks Conservation strategies represent a crucial issue protecting their biota from extinction during hostile in the Mediterranean biome because this area, events (Terborgh, 1992). which represents only 2% of the world’s surface, In the Mediterranean, small islets have served houses 20% of the world’s total floristic richness as natural laboratories of plant evolution while large (Médail & Quézel, 1997). Many of these Mediter - islands have contributed to the conservation of mid - ranean insular species are currently threatened. dle Tertiary flora with a high degree of endemism Despite the long history of botany in the Medi - (Greuter, 1995). In this context, the high rate of en - terranean, there is a lack of species distribution and demism results from the very complicated natural abundance maps which hinders effective conserva - (i.e. tectonic, geologic and climatic) history since tion and management of local botanical heritage. the middle Tertiary (Quézel, 1985; 1995). Due to The assessment of the Mediterranean Islands Flora the moderate direct impact of the Quaternary gla - (Delanoë et al., 1996) suggests that a significant ciations, especially the Würm (Debrandt-Passard, proportion of the islands flora is under threat. 1986), several zones have acted as refuges (Hewitt, Crete, followed by the Balearics, has the highest 1999; 2000). Thus, more favourable thermal condi - percentage (11%) of plants endangered at a global tions and plenty of conservative microhabitats level. The Maltese flora has the highest percentage (cliffs, nunataks, etc.) have helped to preserve nu - (28%) of plants threatened at the local level reflec - merous elements from a Tertiary palaeoflora (Mé - ting the pressure on the island’s habitat. The publi - dail & Verlaque, 1997). cation of the IUCN Top 50 Mediterranean Island Accordingly, we can distinguish two kinds of Plants (Montmollin & Strahm, 2005), albeit not an endemics: palaeo-endemics, i.e. ancient vestiges of exhaustive check-list, has the merit to draw the ge - taxa that were once widespread, and neo-endemics, neral public’s attention to some of the most endan - that have evolved only recently. The presence of gered plant species, stressing particular situations paleo-endemic trees is also remarkable, particularly and conservation needs. on larger islands, and includes fir species Abies ne - In the Mediterranean, the destruction of habitats brodensis and A. cepholonica Loudon in Sicily and due to a long and ancient human presence led to Cephalonia respectively, Zelkova sicula in Sicily their extreme rarefaction and a drastic diminution of and Z. abelicea (Lam.) Boiss. in Crete, Quercus al - their populations. The low altitude zones are most nifolia Poech and Cedrus brevifolia (Hook.f.) affected, particularly coastal areas, rocky grasslands A.Henry in Cyprus (Barbero et al., 1995). and damp ecosystems, but the risks now extend Relict plants, especially trees, as having been throughout all sectors due to the increase of human able to survive impressive environmental changes activities. As mentioned in Olivier et al. (1995), en - over millions of years, are of great concern for their demics regression in Mediterranean area is primarily valuable contribution in improving understanding due to the destruction of favourable habitats due to of past and recent biogeographical and evolutionary urban development, roads, etc. and by direct human processes (Kozlowski et al., 2011). Moreover, in the impact (agricultural and forestry exploitations, wil - frame of forecasted climate changes, some elements dfires, trampling). The biotic threats (concurrence could have a role in the future establishment of of exotic species, competition with woody species), novel ecosystems with new species combinations, together with biological weakness (e.g. low repro - thanks to their aptitude in niching strategy, as re - ductive efficiency, genetic erosion, ineffective di - ported for several relict taxa in the forests of Geor - spersal) are traditionally considered less important, gia (Transcaucasia) (Denk et al., 2001). On the although recent research on plant conservation ge - other side, human-induced future climate scenarios netics acknowledges to the latter a much higher si - could reveal quite catastrophic for many of these gnificance (Kramer & Havens, 2009). elements, acting as the “last nail in the coffin for To face with these major threats, numerous pro - ancient plants” (Connor, 2009). Hence, any effort tective actions must be taken immediately through should be made to improve the perspective of their appropriate management of indigenous populations conservation. and scientific studies undertaken to analyze popu - 284 GIUSEPPE GARFÌ & S TÉPHANE BUORD

lation viability. Among these native species, the re - unexpectedly discovered in the same mountainous lict species such as Z. sicula are priorities for con - massif (Fig. 2) (Garfì et al., 2011). As the former servation because they represent millions years of one, it includes a few hundreds stems, once again evolution. distributed over a limited area of about 0.5 hectares, in quite similar environmental conditions. In the conservation perspective, such extraordinary occur - ZELKOVA SICULA : FROM FOSSILS TO A rence surely contributed to reduce the level of threat LIVING PLANT for this species, but at the moment it was not enough to allow a reduction of risk level adopting Until 1991 the genus Zelkova Spach was known IUCN categories. to Sicily only through fossil records (Béguinot, Included among the family of , the 1929) and nobody before that time would have su - genus Zelkova is currently represented by six spe - spected the existence of living trees in the island. cies, whose worldwide distribution is quite frag - At present-day Z. sicula (Fig. 1) is a very rare spe - mented: three taxa, Z. serrata (Thunb.) Makino, Z. cies exclusive from South-Eastern Sicily, belonging schneideriana Handel-Mazzetti and Z. sinica C. K. to a genus which became extinct in the whole con - Schneid., are widely spread in the lush forests of tinental Europe during the Quaternary Glacial Age. Eastern Asia, and one, Z. carpinifolia (Pall.) Dippel, Up to very recent times the Sicilian species was is common in Transcaucasia, whereas the last two, known to consist worldwide of only a single popu - Z. sicula and Z. abelicea , are narrow endemics to lation (hereinafter referred as ZS1) of about 250 the Mediterranean islands of Sicily and Crete, re - trees, included in a small area less than 0.4 hectares spectively (Denk & Grimm, 2005). within the Bosco Pisano, in the Iblei Mts. At the end In the ecological point of view, some differences of 2009 a second population (hereinafter ZS2) was may be outlined among all taxa. Z. sicula is the only species relatively able to face Mediterranean sum - mer drought stress. It grows in the thermo-(-meso) Mediterranean bioclimate, within sclerophyllous sparse communities dominated by Quercus suber L., Olea europaea var. sylvestris (Miller) Brot and Q. virgiliana (Ten.) Ten.; its biogeographically clo - sest relative Z. abelicea lives in areas with fresh mi - croclimate and good water balance (N-facing slopes, small valleys, dolines), at elevations bet - ween 850 and 1,800 m a.s.l., within supra- and oro- Mediterranean mixed discontinuous woody stands with Acer sempervirens L., Quercus coccifera L. and occasionally Cupressus sempervirens L. (Bar - bero & Quézel, 1980; Egli, 1997). Finally, the four Asian species mostly thrive under a humid and warm-temperate climate, where rainfall usually ex - ceeds 1000 mm/yr and can rise up to 2000-2500 mm/yr (cf. Garfì et al., 2011). Additional aspects distinguish the Sicilian spe - cies. Both populations are currently restricted to gullies bottom and streamsides. Furthermore, in contrast to its relatives, usually represented by me - dium to tall trees, Z. sicula in population ZS1 cur - rently exhibits an explicit shrubby growth form (maximum height 2.5 m), with many plants stunted and a general poor conservation; in population Figure 1. Branchlet of Zelkova sicula . ZS2, which can enjoy of a bit more favorable water Relict species and the challenges for conservation: the emblematic case of Zelkova sicula 285

Figure 2. Current distribution map of Zelkova sicula (see text for abbreviations). supply, the overall conditions look much better in Age, caused the progressive rarefaction from n or - terms of health and vigour, either at tree as well as thern to southern latitudes of the less cold-resistant at population level, with many plants that can attain elements. The Italian peninsula, among others, pla - the height of 5-6 m (Fig. 3) (Garfì et al., 2011). In - yed in this regard a major role of refuge allowing deed, a few individuals cultivated ex-situ in less the persistence at Valle di Castiglione (Central constraining environmental conditions (no water Italy) of the last Zelkova remnants until 31000 stress, milder temperature, partial shadowing) re - years B.P. After that time, according to Follieri et vealed a growth potential of veritable trees. In ac - al. (1986), the genus Zelkova became definitively cordance with that it is suggested that in the past the extinct from the whole continental Europe. Only in species was probably more widespread in fresher the two Mediterranean Islands of Crete and Sicily, and more humid environments. where glaciations effects were less severe, the two Suc h an assumption is quite consistent with the endemics Z. abelicea and Z. sicula survived until data issuing from palaeobotanical investigations, showing Zelkova remains within floristic assem - the present-day (Quézel et al., 1993), tolerating blages dominated by deciduous broadleaved trees, more or less efficiently the summer drought stress from several European localities up to the Late of the current Mediterranean climate. Pleistocene (e.g. Follieri et al., 1986; Garfì, 1996; According to recent investigations (Fineschi et De Paola et al., 1997). Actually, the genus Zelkova al., 2002; Christe et al., in press), Z. sicula is gene - belongs to a hygro-mesothermic floristic unit tically depauperated and seems to have had a hi - which was very common in the luxuriant Tertiary story of severe isolation. It is suspected to be a forests throughout the Northern Hemisphere. In species of hybrid origin and its parents are sugge - Eurasia, climate changes occurred since the late sted to be close to Z. abelicea and Z. carpinifolia Pliocene/early Pleistocene with the onset of the I ce ancestral species. This is rather consistent with re - 286 GIUSEPPE GARFÌ & S TÉPHANE BUORD

sults of Nakagawa et al. (1998), which point out sponse to the hardiness of a changing environment that fossils, formerly referred by palaeobota - throughout the geologic times, and then the survival nists to as Z. carpinifolia , most likely might instead of the species until present-day; ii) on the other side, be attributed to Z. sicula . Whatever the case, it since clonal recruitment implies absence of gene re - seems quite alike that such harsh and complex vi - combination and then strong genetic impoveri - cissitudes could be invoked as responsible of mu - shment, it hugely diminishes populations’ viability, tations resulting in the current triploid caryotype of raising vulnerability to any external adversity. In the Z. sicula , which differs in this regard, too, from all same time, clonality adds a further element of ex - its diploid relatives (Garfì, 1997a). This is very rare ceptionality to such an emblematic species. If future within the angiosperms and further emphasizes the investigations would reveal that both two current great concern of this species. disjunct stands are entirely clonal populations, this In the whole, the aforementioned issues finally could mean that, as for Lomatia tasmanica (Linch highlight the extreme importance of this taxon for et al., 1998), each of them is a very old organism, both studies of conservation biology and the recon - even aged many thousand years, therefore beco - struction of historical biogeography of the genus ming among the oldest living plant individuals (!) Zelkova (Kozlowski & Gatzfeld, in press). known to date. In any case, the lack of functional seeds strikin - gly enhances the risk of extinction of the species as WHY IS Z. SICULA SO VULNERABLE? it surely involves major difficulties in propagating CURRENT CONSERVATION AND THREATS it, both for in-situ and ex-situ conservation actions. Designing efficient protocols for in-vitro and in-vivo At present a variety of causes threaten a satisfac - vegetative multiplication is to be considered an ir - tory conservation or, what is more, the survival it - replaceable goal for any efforts of active and effi - self of Z. sicula . Some factors are strictly depending cient conservation. In this regard, propedeutic on its biology, others on different exogenous agents. investigations about the residual genetic diversity A general review can be summarized as follows. need to be carried out in order to conserve as much as possible intra-specific variability. Unsuccessful sexual regeneratio n Anthropic disturbance and habitat degradation The fructification of Z. sicula is quite irregular (Garfì, 1997a), as already known for its Cretan re - According to current knowledge (Garfì et al., lative Z. abelicea (Egli, 1997). In the Sicilian spe - 2011), Z. sicula is supposed to be a species thriving cies it seems usually coinciding with the rainiest in typical forest habitat. Heavy human pressure (grazing, wildfires, past silvicultural over-exploi - winter years and has been most often observed on tation), in addition to the foreseen climate deterio - the same, very few trees. Moreover, according to ration are responsible of its current habitat current knowledge (Garfì, 1997b) seeds seem ste - degradation, as involving failure in natural regene - rile due to its triploid conditions. Therefore, at pre - ration of forest species and the further impoveri - sent-day regeneration is exclusively depending on shment in forest composition and structure. vegetative mechanisms such as root suckering and Wildfires represent a major hazard in the whole layering (Fig. 4). forest area. In the past large patches of forest cover Consequently, in both populations most trees are have been destroyed or severely damaged by wil - very probably of clonal origin. This situation, in ad - dfires, whereas very recently fire injuries have dition to the long geographic isolation, most likely even directly concerned the population ZS2. Their involved severe decline in gene flow and a rapid de - origin is usually to be related to human activities. crease of intra-specific genetic variability (Fineschi As in many Mediterranean areas, since ancient et al., 2002; 2004; Christe et al., in press). The su - times fire has represented a kind of very “primi - spected predominance of clonality could have con - tive”, but extremely deleterious method of land ma - trasting implications: i) on the one side it can nagement and in the last years it has become also a represent the mechanism that assured the perpetua - means of social claim. The general consequences tion of a successful genotype differentiated in re - could be the simplification of the ecosystem and Relict species and the challenges for conservation: the emblematic case of Zelkova sicula 287

Figure 3. Population of Zelkova sicula from site Contrada Ciranna (ZS2) with trees 5-6 m high. Figure 4. Vegetative pro - pagation through root suckers. Figure 5. Withered following summer water stress in August 2011. Figure 6. Massive proliferation of epicormic short shoots due to browsing (a) and detail of a decapitated tip (b). Figure 7. Sclerophillous species diffusion at site Bosco Pisano (ZS1) after grazing exclusion. Figure 8. Fencing and irrigation plant built at site Bosco Pisano (ZS1) within actions of the LIFE project Zelkov@zione. 288 GIUSEPPE GARFÌ & S TÉPHANE BUORD

landscape mosaic, with a decrease of ecosystem nescence and shedding of leaves have been most functions. The habitats suffering the greatest risk frequently noticed, whereas in case of abrupt dehy - are those directly related to Z. sicula (i.e. 9330 - dration leaves withered and died but remained atta - Quercus suber forests, and 6220 - Pseudo-steppe ched. Sometimes, severe increasing water stress with grasses and annuals of the Thero-Brachypo - also leads to the death of twigs and branchlets, or dietea), but the other habitats could be also concer - even of the entire stem. The plants can recovery in ned at various extent. Reiterated events can involve the following season, but repeated episodes of stress the definitive loss of most vulnerable species and along more than one single year involve the death the selection of fire-resistant taxa. Notwithstanding of trees (Garfì et al., 2002). For instance, in summer its great ability of resprouting after an injury, Z. si - 2007 the entire population ZS1 suffered very severe cula for its rarity and punctiform distribution could water stress and demographic follow-up enabled to easily disappear as a consequence of repeated wil - assess that almost 20% of trees have died. dfires at short intervals. Furthermore, recent trends in climate changes at As far as concerns grazing, historical data te - global scale depict scenarios characterised by an in - stify that it has been one of the main types of local crease in summer drought, both in terms of less land use. Its pressure became heavier since the last rainfall amount and duration and raise of tempera - sixty-years period, after land abandonment and the ture. Major detrimental effects can then be expected migratory flows abroad of local population that made possible the settlement of transhumant gra - for the conservation of the species in the nature ziers originating from the mountainous area of (Allen et al., 2010; Borghetti et al., 2012). Northern Sicily (Garfì & Di Pasquale, 1988; Di Pa - squale & Garfì, 1989). Potential inter-specific competition In contrast to fire, in some particular cases (e.g. for the habitat 6220 - Pseudo-steppe with grasses Some years after its discovery, the population and annuals of the Thero-Brachypodietea) grazing ZS1 was fenced in order to protect it against brow - is considered a promoting factor for plant richness. sing. During the years following the exclusion of However, it must be kept in mind that in the area of grazing disturbance, Z. sicula experienced a rather interest it has been in the time a formidable cause remarkable growth increase. But in the same time of forest ecosystem degradation. Such an issue must progressive succession processes were observed be carefully evaluated in the conservation planning in its habitat: vegetation communities’ patterns perspective, especially in a region like Sicily where began to change and woody species cover became forest cover has been destroyed on large areas since more and more relevant. Xerophilous taxa, such the antiquity. The great worry is that in the next fu - as Calicotome infesta (C. Presl) Guss ., Pyrus spi - ture the unregulated way this practice is currently nosa Forssk., Phillyrea latifolia L., Sarcopoterium carried out can notably enhance the destruction of spinosum (L.) Spach and some trees like Quercus the last remnants of “natural” forest patches of this suber , Q. virgiliana and Celtis australis L. began part of Sicily. In the specific case of Z. sicula , brow - to spread (Fig. 7). sing is proved responsible of severe growth sup - On the one side such positive dynamic trend is pression (Fig. 5), flowering inhibition and even expected to improve in the long period the global death of trees, already hardly weakened by a con - habitat stability and ecosystem functions. On the straining environment (Garfì, 1997b). other side, such processes are believed to be able to trigger in the short period inter-specific competition Summer water stress at the expense of Z. sicula , which surely cannot ex - press a comparable adaptive and growth ability of Due to its incomplete adaptation to the Medi - typical Mediterranean xerophilic species. terranean climate seasonality, since its discovering This could entail problems of decrease or even Z. sicula has suffered periodical summer drought survival of the species of concern, so that a perio - stress (Fig. 6), and several evidences indicate simi - dical monitoring of both populations should be re - lar occurrences also in past times (Garfì et al., quired in order to assess the demographic trends 2002). Water stress cause moderate to severe injury and population resilience and get information for to the peripheral parts of the crown. Premature se - conservation management. Relict species and the challenges for conservation: the emblematic case of Zelkova sicula 289

Improper use of plants or parts of them the Sicilian Regional Authority of Public Forests - AFDRS, the Institute of Plant Genetics of the Italian Considering the peculiarities of Z. sicula (e.g. National Research Council - IGV-CNR, the National its ancient origin, its troubled history throughout the Botanic Conservatory of Brest - France - CBNB, geological periods, its rarity) since its discovery a and Legambiente, an Italian environmental associa - special interest has arisen about it from a rather va - tion) within the frame of the LIFE+ EC programme, riegated multitude of people, such as scientists, en - specially conceived for the conservation of nature vironmentalists, common tourists, plants collectors, and biodiversity in the EU territory. bonsai producers, nurserymen, etc.. Small to large The project, named “Zelkov@zione - Urgent ac - groups of people, usually not controlled by any of - tions to rescue Zelkova sicula from extinction” ficial guide or surveillance, during their visits scam - (http://www.zelkovazione.eu/) was funded in 2011 per everywhere in the area causing soil subsidence, and, given its evident relevance with the internatio - overall injuries to vegetation and even involuntary nal initiative, a sharing relationship was soon esta - trampling of small Zelkova plants. Moreover, the blished with it. The project aims to ensure the last four categories of visitors are the most dange - survival of Z. sicula through in-situ and ex-situ con - rous since they often gather parts of plants as sou - servation integrated actions to be carried out along venir and, especially the bonsai lovers, even uproot almost five years. It entails four comprehensive to - young plantlets for their collections. pics all related each other (Table 1): i) knowledge and monitoring, ii) active conservation, iii) exper - Although not a priority cause, like for Z. abeli - tise and communication, and iv) education/aware - cea from Crete (Egli, 1997), this kind of distur - ness. Some short remarks can help catching the bance/misuse could reveal detrimental for fundamentals of the project strategy. conservation since responsible for reduction of po - pulations’ size and, given its rarity, significantly in - Collecting information for conservation planning crease the risk of extinction. Albeit a conspicuous literature already exists (cf. reference list), much still need to be understood AN INTEGRATED STRATEGY FOR THE both in terms of basic knowledge and issues to ad - CONSERVATION OF Z. SICULA dress conservation. The viability of Z. sicula is a preliminary information required to correctly plan As previously outlined the entire genus Zelkova conservation policy. In this regard the first step to is a taxon of special concern. Accordingly, in recent assess the current status of the target species invol - years it has deserved a particular interest within the ves the inventory and mapping of all discrete trees scientific community and conservationists (BGCI, (i.e. single/multiple trees or shoots apparently ori - 2010; Kozlowski et al., 2011). This resulted in a ginating from spatially distinct stumps), in addition global conservation plan, set out into three main to the implementation of a georeferenced database complementary goals (Kozlowski & Gratzfeld, in including biometric data (stem height and diame - press): i) conservation, comprising elaboration of ter), phenological features (e.g. flowering trees, an action plan, proposing concrete recovery and/or fruiting), individual vigour, past damages (water reintroduction measures, etc.; ii) basic and applied stress, biotic disturbances), microsite characteristics research, including molecular phylogeny, phylogeo - and spatial distribution patterns. Periodical monito - graphy, population genetics, population structure, ring will allow appraising the demographic trends genetic comparison of wild populations with ex-situ of the target species and the forest stand dynamics collections, etc.; iii) public awareness and outreach, with the aim to prevent inter-specific competition involving development of travelling exhibitions, and phenomena following disturbance suppression. organisation of national and international conferen - Genetic investigations are propaedeutic to any ces and seminars to exchange knowledge and share actions of multiplication, in order to detect residual conservation expertise. In parallel, a specific project genetic variability, if existing, and allow conserva - entirely addressed to the conservation of the Sicilian tion of the most diverse genotypes. Vegetative pro - species was presented by a composite partnership pagation through in-vivo and in-vitro techniques is (i.e. the Sicilian Department of Environment - DRA, an immediate successive step. 290 GIUSEPPE GARFÌ & S TÉPHANE BUORD

Type of actions Involved activities Expected results 1.Updated inventory of both ZS1 and ZS2 popula - •Improvement of knowledge about the biology and the tions, including the position of each tree trough sub- ecology of the target species metric GPS device, the implementation of a •Evaluate the viability of Zelkova populations and pre- georeferenced database with biometric, biological vent any inter-specific competition phenomena follo - Knowledge/ and micro-topographic attributes wing disturbance elimination Monitoring 2.Monitoring of both the target species demographic •Evaluation of the residual genetic diversity in order to trends and the forest community dynamics in current preserve the as highest as possible rate of variability and future populations •Contribute to a more efficient conservation planning 3.Genetic investigations 4.Definition of an efficient in-vitro and in-vivo ve- getative propagation protocol for the target species

1.Building an efficient system of fencing •Improving the protection in the nature against disturbance 2.Setting up of an emergency irrigation system from grazing or improper collecting of plant material 3.Massive production of multiplication material of •Attenuation of summer water stress episodes for the po- Z. sicula and native forest species pulation ZS1 4.In-situ plantation of the target species and establi- •Reinforcement of the current populations of Z. sicula shment of 5 new populations, 2 within the current •Increase the number of population in the nature and test habitat and 3 in supposed more favourable bioclima- the feasibility of uncommon conservation approach as Active tic conditions “assisted colonization” conservation 5.Plantation of native forest species on about a 10 ha •Habitat enforcement/rehabilitation in order to create a area including the current site of ZS1 more suitable ecological environment, through recove- 6.Ex-situ cultivation of at least 200 trees from both ring the as highest as possible ecosystem functionality ZS1 and ZS2, at the CCG and CBNB under controlled situation and in reasonably fast times 7.Prompting formal procedures to release a regional •Securing through ex-situ conservation the as highest as administrative Act for the legal protection of Z. si - possible genetic diversity in public conservation centres cula and the SCI Bosco Pisano •Recognition of the status of protected species at re - gional/national level and starting of the procedure for 8.Starting of formal procedures for the inclusion of its ackowledgement as priority species (sensu Habitat Z. sicula in the list of priority species of the Habitat Directive) Directive •Implementation of a standard normative procedure for protection of all threatened species in public/private lands 1.Implementation of operative conservation plan- •Applying site-dedicated concrete conservation mea- ning according to the rules proposed in the Ma - sures according to the Management Plan “Monti nagement Plan “Monti Iblei” Iblei” 2.Drawing of a grazing management plan for the •Involving the competent local Forest Authority to Bosco Pisano to attenuate the pressure on the con- improve surveillance and protection of the species cerned habitat according to the rules proposed in and habitat through active policy Expertise/ the Management Plan “Monti Iblei” •Realisation of a communication network among pu- Communication 3.Planning of special operative procedures for blic bodies, stakeholders, schools, etc., in order to wildfires prevention share and monitor experience and results 4.Activation of training activities for local people (e.g courses for naturalistic guides) to improve knowledge and introduce young people to the la- bour market 1.Establishing a permanent round-table among •Removing/reducing principal economic/social type partnership, public authorities, no-profit organi - threats for the species and habitat by involving au - sations and local stakeholders to monitor the pro- thorities, organizations and stakeholders cedures of LIFE+ project. •Involving local people in efforts to improve local 2.Carrying out of campaigns of awareness and di- economy on green tourism Education/ vulgation on the specific project and the general •Improving the didactic value of the CCG, with be- Awareness problem of conservation of biodiversity neficial feed-back on the territory in regards to public 3.Realisation of a dedicated website to inform and awareness about the global problem of biodiversity divulgate objectives, procedures, monitoring, conservation feed-backs and results •Prompting local awareness and information about the problems of loss of biodiversity

Table 1. Main activities foreseen in the LIFE+ project “Zelkov@zione”. Relict species and the challenges for conservation: the emblematic case of Zelkova sicula 291

The active actions: habitat rehabilitation, as - servations on cultivated trees, a more humid envi - sisted colonisation and legal protection ronment (e.g. supra-Mediterranean or montane fo - rest habitats dominated by Fagus , Acer , Carpinus , Active conservation mainly includes a number Taxus , deciduous-type Quercus etc.) (Fig. 9) is in - of concrete measures directly in the field, in addition ferred to better match with the ecological require - to traditional ex-situ conservation. Outright actions ments of Z. sicula . as fencing against grazing/misuse disturbances and A similar approach, in which an endangered the setting up of an emergency irrigation system species is introduced outside of its historically (Fig. 8), can contribute to eliminate or significantly known native range, is quite uncommon in actions reduce some of the most flagrant threats. of plant rescue. Actually just in the last few years More indirect interventions will concern the pre - a lively debate has arisen on this subjects (for a re - sent habitat. As formerly mentioned, the optimal ha - view see Brooker et al., 2011), especially fostered bitat of Z. sicula is assumed to be typical forest, by the increasing recognition of the likely inability with complex floristic composition and structure. of many species to cope with rapid climate war - In contrast, the current habitat is heavily degraded ming (Thomas, 2011). Many terms have been pro - due to long-lasting human pressure. Therefore the posed to indicate this approach of moving species recovery of ecosystem functions involving actions at risk from their current locations to those areas of reinforcement and rehabilitation needs to be pur - expected to be suitable for their growth under fu - sued in order to (re-)create a more suitable ecologi - ture climate change scenarios, but the most com - cal environment for the target species. The action mon used is “assisted colonisation” (Hunter, 2007; will be exclusively based on the employ of native Brooker et al., 2011). forest species, produced from multiplication mate - Although some conservationists (Ricciardi & rial collected in the same forest area. Moreover, it Simberloff, 2008) remain very critic in this regard, will be performed according to the modern princi - assisted colonisation is invoked as the “last resort” ples of naturalistic silviculture and water saving when other conservation strategies have been pro - (minimize the impact of preparatory works and con - ved to be ineffective or are highly prone to fail. serve as soon as possible the existing vegetation This is specially true for narrow endemics confi - cover, employ native and tree species, use of ned to very specialised habitat (isolated mountain, hydrogels, i.e. polyacrylates of very high molecular single lake, unique geo-pedologic substratum) that weights binding water up to 400 times their mass, are surrounded by environments fundamentally that can prolong the survival of trees under water unsuitable for them which became insurmountable stress up to 300%). barriers (Thomas 2011; Brooker et al., 2001). Ge - Particular attention will be also paid to the plan - netic patterns are as much as detrimental, since ge - ting patterns, by favouring the creation of hedge - netic erosion can limit short-term resilience, rows and the random distribution of various size evolutionary potential for adaptation, and long- plant groups in the aims to obtain a variety of habi - term survival of plant species in the face of rapid tats and fauna feeding sources. Restoration will also environmental change (Kramer & Havens, 2009). involve the removal of exotic tree groups ( Eucalyp - It is extremely paradigmatic the example of Tor - tus spp. and Cupressus spp.) introduced near ZS1 reya taxifolia Arn., from Florida, that since the fif - population during past afforestations. ties of the last century suffered an inexplicable At the population level, new plantings in the dieback up to the present number of about 500 current sites are aimed to enlarge and reinforce the trees (Barlow & Martin, 2004), therefore having current stands. But one of the greatest efforts of the been the object of intensive planting outside its project consists in the introduction and establi - original range. shment of novel populations in new sites, three of In the case of Z. sicula we can account several which selected in areas supposed to be more suita - reasons to refer to assisted colonisation, especially ble for the species. In fact, according to results of when related to future climate model of rapid war - recent investigations (Garfì et al., 2002; 2011), pa - ming (Allen et al., 2010; Borghetti et al., 2012). Fir - laeoecological data (e.g. Béguinot A., 1929; Follieri stly, we must consider its propagation ability, that et al., 1986; De Paola et al., 1997) and personal ob - even at the genus level is not quite performing. For 292 GIUSEPPE GARFÌ & S TÉPHANE BUORD

Figure 9. View of the Bosco Tassita (Nebrodi Mts.) as an example of possible (re-)introduction area of Zelkova sicula according to assisted colonisation instance, it has been suggested that the extant di - sound and show that an apparently ‘unnatural’ in - stribution of Z. carpinifolia is probably also due to tervention might even decisively contribute to save the rather inefficient dispersal mechanisms that may a species from extinction. have hindered its expansion from Pleistocene refu - Traditional living ex-situ collection is also con - gia to Holocene alluvial plains in the Colchic lo - templated. At least 200 trees from both popula - wlands (Denk et al., 2001). The situation of the tions will be cultivated at the CCG and the CBNB, Sicilian species is even more dramatic, given its in order to secure the species and conserve the as ineffectiveness to regenerate through seeds that highest as possible genetic diversity, according to makes its dispersal impossible over long distances. the recommendations of Kozlowski et al. (2011). In addition, its current area is extremely isolated The actuation of legal protection is the last but and fragmented, being separated from supposed not the least issue of concrete actions. At present in - more suitable habitats (e.g. the Nebrodi Mountain deed Z. sicula does not yet enjoy for any legal/for - Range, Northern Sicily) by vast lowlands. Moreo - mal measure of safeguard. Therefore different ver, as mentioned by some papers (Jackson & actions are addressed to both the sites and the spe - Hobbs, 2009; Brooker et al., 2011), palaeoecologi - cies. Formal procedures are prompted for the reco - cal data can provide important information on past gnition of SCI ITA090022 “Bosco Pisano” (site of occurrence of the species and/or the plant commu - ZS1) as a Special Area of Conservation (SAC) nity it took part to, then encouraging our transloca - sensu Habitat Directive 92/43, and to enlarge the tion projects. This should be rather innovative for perimeter of SCI ITA090024 “Cozzo Ogliastri” in the Mediterranean area, and in case of success, such order to include the site ZS2, situated in its close an action would confirm that our assumptions are proximity. In parallel, as the target species is not Relict species and the challenges for conservation: the emblematic case of Zelkova sicula 293

comprised either in the Annex II or IV of the Habi - gional level, organisation of periodic meetings and tat Directive, the Italian Ministry of Environment workshop on the aims and advancement of the pro - will be requested through the DRA to include it in ject in public venues. The events will allow to con - the list of “priority” species (in danger of disappea - tinuously evaluate the “state of the art” and to ring, needing particularly strict protection). illustrate the final results. At regional/national level the main goal is to The organization of a generalist network will aim obtain also the acknowledgement of the status of at sharing the project actions among public authori - protected species through the adoption by the DRA ties, no-profit institutions and local stakeholders in - of a normative document (Councilor’s Decree) volved in the conservation issues of critically containing appropriate measures that will ensure endangered species. Finally, the realisation of a pro - the legal protection of the target species and its ha - ject-dedicated website will serve to inform and dis - bitat. This will represent the first step to serve for seminate as much as possible objectives, procedures, the implementation of a standard normative proce - monitoring, feedbacks and results of the project. dure for protection of all threatened species in pu - blic/private areas. CONCLUSIONS Capitalizing knowledge and expertise and developing public awareness In the frame of the foreseen rapid climate chan - ges at world level, and in the Mediterranean in par - Knowledge and expertise as well as actions in ticular, many plant species unable to cope with the field cannot disregard the need of divulgation unsuitable environment are doomed to become ex - of the results in order to increase public awareness. tinct. Insular endemics and relict taxa are the most The implicated and ongoing expertise will encom - threatened, especially those suffering for habitat de - pass as key outcome the implementation of an ope - struction and biological weakness (e.g. low repro - rative conservation planning for the areas of ductive efficiency, genetic erosion, ineffective concern according to the rules proposed in the Ma - dispersal). In this regard Z. sicula represents a quite nagement Plan “Monti Iblei” (ARTA, 2009), al - paradigmatic conservation case, which must face to ready compiled within the Regional Management very challenging tasks. Plans of SCI and ZSP. This will directly lead to the As a general rule, priorities for biodiversity con - drawing of a site-dedicated management plan for servation management should be of two kinds: i) grazing and the wildfires prevention, aiming to at - priorities for extensive areas where high biological tenuate the pressure on the habitat and reduce the diversity has accumulated over long periods of geo - major anthropogenic threats. Accordingly, the com - logical time and ii) priorities for distinctive areas petent local Forest Authority will be involved in im - with high endemism. Because of the small extent proving surveillance and protection of the species and high concentration of unique taxa, the risk of and habitat through an active policy. rapid and irreversible loss of biodiversity is high The establishment of a permanent communica - and important ecosystem functions may also rapidly tion network among conservationists, public bodies, be lost. Biogeography has an important role to play stakeholders, protected areas managers, etc. is a in this process of conservation, but much more kno - complementary goal in order to share and monitor wledge is required about the habitat preferences of experience and results. Additionally, the actuation species and their response to habitat fragmentation of training activities are foreseen for local people resulting from increasing development pressures (e.g. courses for naturalistic guides) to improve and climate change. knowledge and stimulate the dissemination of an Landscape ecology will play an increasingly im - environmental consciousness. portant role, providing the spatial context within Dedicated campaign of awareness and divulga - which to select ecologically important sites for pro - tion on both the specific project issues and the ge - tection, for monitoring change and for identifying neral problem of biodiversity conservation will be sites for habitat restoration and relict species (re-)in - promoted through media, educational programmes troduction. Among all, one of the most intriguing in primary and secondary schools at local and re - and challenging strategy surely must be referred to 294 GIUSEPPE GARFÌ & S TÉPHANE BUORD

the translocation of species in presumed more sui - Béguinot A., 1929. Illustrazione delle filliti quaternarie table habitats, becoming the “last resort” to face the dei travertini palermitani conservate nel Museo di deleterious impact of forecasted climate deteriora - Geologia della R. Università di Palermo. Archivio tion. Pilot (re-)introductions attempts worth to be Botanico, Bullettino dell’Istituto Botanico di Mo - dena, 5: 143-173. carried out and results could notably contribute to BGCI (Botanic Gardens Conservation International), the present debate concerning the application of as - 2010. Global Survey of ex situ Zelkova collections. sisted colonization, especially for relict species, as Available from http://www.bgci.org/files/survey-zel - a valuable conservation tool for dealing with the kova.pdf threats of a changing world. Borghetti M., La Mantia T., Menozzi P. & Piotti A., 2012. Probabili impatti del cambiamento climatico sulla bio - diversità delle foreste italiane. Forest@ 9: 245-250. ACKNOWLEDGMENTS Brooker R., Britton A., Gimona A., Lennon J. & Little - wood N., 2011. Literature review: species transloca - Authors are grateful to all colleagues of the par - tions as a tool for biodiversity conservation during climate change. Scottish Natural Heritage Commis - tnership of project Zelkov@azione, with special re - sioned Report No.440, 68 pp. gards to Matilde Fiore and Giandomenico Christe C., Kozlowski G., Frey D., Bétrisey D., Mahar - Maniscalco (from DRA), Francesco Carimi (from ramova E., Garfì G., Pirintsos S. & Naciri Y., in press. CNR-IGV), Giancarlo Perrotta (from DRAFD), Sal - Tertiary relict trees show footprints of past intensive vatore Livreri Console and Nicola Corona (from Le - diversification and structuring: the genus Zelkova gambiente), Dominique Dhervé and Catherine (Ulmaceae) in southwest Eurasia. Journal of Biogeo - Gautier (from CBNB), and the respective administra - graphy. tive and technical staff for their invaluable contribu - Connor S.E., 2009. Human impact - the last nail in the tion during all steps of the project implementation. coffin for ancient plants? Journal of Biogeography, The project “Zelkov@zione - Urgent actions to re - 36: 485-486. De Paola M., Franco A., Macchia F. & Forte L., 1997. scue Zelkova sicula from extinction”was co-funded Plant macrofossils in Pleistocenic volcanoclastic de - by the EC LIFE+ Programme, Grant Agreement n. posit near Tursi (Basilicata). In: Atti Giornata di Studi LIFE 10 NAT/IT/000237. in ricordo di Daria Bertolani Marchetti (Formigine, 18 maggio 1996), Aedes Muratoriana, Modena, 319-327. Debrandt-Passard S., 1986. Synthèse géologique du sud- REFERENCES est de la France. Vol. 2. Atlas. Mémories du Recher - ches Géologiques et Minières, 126. Paris. Allen C.D., Macalady A.K., Chenchouni H., Bachelet D., Delanoë O., Montmollin B. & Olivier L., 1996. Conser - McDowell N., Vennetier M., Kitzberger T., Rigling vation of the Mediterranean Island plants. 1. Strategy A., Breshears D.D., Hogg E.H.T., Gonzalez P., Fen - for Action. IUCN, Cambridge, 106 pp. sham R., Zhang Z., Castro J., Demidova N., Lim J.- Denk T. & Grimm G.W., 2005. Phylogeny and biogeo - H., Allard G., Running S.W., Semerci A. & Cobb N., graphy of Zelkova (Ulmaceae sensu stricto) as infer - 2010. A global overview of drought and heat-induced red from leaf morphology, ITS sequence data and the tree mortality reveals emerging climate change risks fossil record. Botanical Journal fo the Linnean So - for forests. Forest Ecology and Management 259: ciety, 147: 129-157. 660–684. Denk T., Frotzler N. & Davitashvili N., 2001. Vegetatio - ARTA 2009. Piano di gestione “Monti Iblei”. nal patterns and distribution of relict taxa in humid http://www.artasicilia.eu/old_site/web/pdg_defini - temperate forests and wetlands of Georgia (Transcau - tivi/definitivi/ddg_provv/ddg_monti_iblei_666_2009. casia). Biological Journal of the Linnean Society, 72: pdf. Accessed 24/12/2012. 287-332. Barbero M. & Quézel P., 1980. La végétation forestière Di Pasquale G. & Garfì G., 1989. Risorse e prelievo pa - de Crète. Ecologia Mediterranea, 5: 175-210. storale nei boschi di Buccheri (sec. XVIII-XX). Qua - Barbero M., Loisel R. & Quézel P. 1995. Les essences derni storici, 72: 901-909. arborées des îles méditerranéennes: leur rôle écolo - Di Pasquale G., Garfì G. & Quézel P., 1992. Sur la pré - gique et paysager. Ecologia Mediterranea, 21: 53-69. sence d’un Zelkova nouveau en Sicile sudorientale Barlow C. & Martin P.S., 2004. Bring Torreya taxifolia (Ulmaceae). Biocosme Mésogéen, 8-9: 401-409. North-Now. Wild Earth Forum, Fall/Winter 2004- Egli B., 1997. A project for the preservation of Zelkova 2005: 52-56. abelicea (Ulmaceae), a threatened endemic tree Relict species and the challenges for conservation: the emblematic case of Zelkova sicula 295

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