21-25 • BGCI • 2015 • BGjournal • Vol 12.2 21

Introduction

Specimens of Zelkova spp., whichmay be up to 1,000 years old,found in places of worship and

contemplation in eastern Asia, giveevidence to the ancient and closerelationship of people with these trees.Likewise, traditional herbal medicine,household items and other objects madefrom various parts of the tree, aretestimony to the strong cultural andsocio-economic values and customsassociated with this genus.

Relict trees

Zelkova species form part of the Arcto-Tertiary relict flora that covered largeparts of the northern hemisphere during

the Caenozoic Era (some 55 – 2.5 millionBP). Fossil discoveries attributed to thegenus, dating back more than 50 millionyears, give proof of the plant’s oncewider, circumboreal occurrence. Todaythe highly disjunct distribution of the sixextant species – Z. sicula, Z. abelicea, Z.carpinifolia, Z. schneideriana, Z. sinicaand Z. serrata – from the Mediterraneanover to the Caucasus and East Asia,make this genus a fascinating subject forphylogenetic and biogeographic studiesto advance the understanding ofevolutionary processes.

Zelkova (Ulmaceae)

Z. siculaZ. abelicea

Z. carpinifolia

Z. serrataZ. sinica

Z. schneideriana

Conservation challenges of Zelkova sicula and Z. abelicea – two Mediterranean narrow endemics

WHITHER RARE RELICT TREES IN A CLIMATE OF RAPID CHANGE?

Authors: Joachim Gratzfeld, Gregor Kozlowski, Laurence Fazan, Stéphane Buord, Giuseppe Garfì,Salvatore Pasta, Panagiota Gotsiou, Christina Fournaraki, Dimos Dimitriou

Zelkova serrata. Buddhist shrine, Hita,Japan. (S. Bétrisey)

Shepherd’s crooks (‘Katsouna’) madefrom Zelkova abelicea. Omalos, Crete. (G. Kozlowski)

Zelkova zelkovifolia. Pliocene.Willershausen, Germany. (H. R. Siegel)

Global distribution of Zelkova spp. Map by Natural History Museum Fribourg, Switzerland

Unfortunately, the relict nature of thegenus is no recipe for survival in a rapidlytransforming environment. As elsewherein the world, habitat loss,overexploitation, fast changing climaticconditions and many other drivers ofchange exert high pressure on remainingnatural Zelkova populations, especiallythe two Mediterranean species, Z. siculaand Z. abelicea. These species occur inexceptionally isolated and fragmentedlocations. Among the rarest trees in theworld, they require specific managementapproaches combining a set of integratedin and ex situ conservation measures.

Zelkova sicula – one of the raresttrees in Sicily and in the world

Within the genus, Z. sicula Di Pasq., Garfì& Quézel has a particularly remarkableposition. Discovered in 1991 (Di Pasqualeet al., 1992), this narrow endemic isknown from only two locations. Bothpopulations cover an area of occupancyof less than one hectare and include afew hundred small trees each. Occurringbetween 350 and 450 m above sea level

on the north-eastern slopes of the IbleiMountains (south-eastern Sicily), thepopulations are found in open forestcommunities with other tree species suchas Quercus suber, Q. virgiliana, Oleaeuropaea var. sylvestris, Pyrus spinosaand Calicotome infesta.

Staying alive in a changingclimate

Several of the morphological and lifetraits of Z. sicula can be interpreted asthe result of a long-lasting process ofadaptation to a rather suboptimalenvironment. Unlike the other Zelkovaspecies, Z. sicula is a shrub or a smalltree. Characteristic for plants at the limitof their distribution range, this habit ismost likely a response to water shortagein the current habitat. The location ofboth populations restricted to the bottomof gullies and along narrow streams,suggests that these micro-habitats play akey role in enabling the species towithstand drought. Nonetheless, extremeenvironmental hazards, such asprolonged drought can cause moderateto severe damage, ranging from witheringof leaves to dieback of branches andstems. What is more, rising habitatfragmentation and livestock grazingrepresent major further threats to bothpopulations. Due to its rarity, Z. sicula hasbeen included as Critically Endangered(CR) on the IUCN Red List of ThreatenedSpecies.

Two populations – two clones:two individuals?

Recent studies (Christe et al., 2014b)suggest that Z. sicula has been subject tosevere isolation and geneticimpoverishment. Fructification is irregularand seeds are most probably sterile dueto its triploidy. Regeneration relies onvegetative mechanisms such as rootsuckering and layering; as a result,individuals in both geneticallyimpoverished but distinct populations areassumed to be of clonal origin; hence,each population could be regarded as asingle individual. This, in addition to theextended geographic isolation, has mostlikely caused a sharp decline in gene flowand a decrease in intra-specific geneticvariability. On the other hand, clonalityand vegetative reproduction are adding afurther trait of uniqueness to this speciesin the genus Zelkova; as with Lomatiatasmanica (Proteaceae) – known from asingle, clonal population estimated to beseveral ten thousands of years old (Lynchet al., 1998), each Z. sicula populationcould potentially represent a manythousand year-old genetic unit.

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Distribution of Z. sicula (red colour). Mapby Natural History Museum Fribourg,Switzerland

Z. sicula. Population of Ciranna, Sicily. (G. Garfì)

Young tree of Z. sicula developing by rootsuckering. (G. Garfì)Z. sicula micro-habitat.(G. Garfì)

Z. sicula leaf withering. (G. Garfì)

Rescue trials in progress

Since 2011, a major project fundedthrough the European Commission EC LifeProgramme (http://www.zelkovazione.eu/)is implementing a range of integrated inand ex situ conservation actions in theareas of knowledge and monitoring, activeconservation, expertise, andeducation/awareness and communication.To date, a number of key milestones havebeen achieved, including the exclusion ofgrazing through fencing and a sustainablemanagement plan involving formalagreements with local stakeholders, aswell as the legal protection of the targetspecies through the enactment of aCouncillor’s Decree by the RegionalDepartment of Environment.

The recent successful development ofprotocols for in vitro and in vivovegetative multiplication is a further majorstep towards effective in and ex situconservation, with the poor intra-specificvariability in the species facilitating theestablishment of the field collections.

Z. sicula in vitro rooted plantlet. (A. Carra)

Introduction to otherecosystems?

Securing viable populations in situnevertheless remains the mainconservation challenge. Introduction toother ecosystems is being studied toestablish further populations in newlocations. These have been identifiedusing the guidelines for ‘assistedcolonisation’ (Brooker et al., 2011), andbuild on paleo-ecological data andobservations of specimens grown underdifferent ex situ conditions which revealthe growth potential of Z. sicula intoactual trees (Garfì et al., 2011; Garfì andBuord, 2012). These findings suggest thatmore humid and cooler climaticconditions typical to montane mixeddeciduous forests with Fagus, Acer,deciduous Quercus, etc. may offer a

better match for the ecologicalrequirements of Z. sicula. Thisconservation approach is applied as the‘last resort’ for narrow endemics confinedto very specialised habitats andincreasingly encroached upon byunfavourable environmental conditions.

Zelkova abelicea – a Cretanpersisting against all the odds

Zelkova abelicea (Lam.) Boiss. is the onlyendemic tree of the east-Mediterraneanisland of Crete. The species is found inopen, mountain forest communities

between 900 and 1,800 m above sealevel, where it grows in mixed stands withAcer sempervirens, Quercus cocciferaand occasionally Cupressussempervirens. Populations of Z. abeliceaoccur in all four main mountain rangesincluding Levka Ori, Psiloritis, Dhikti andThripti. Primarily, they occupy north-facing slopes and areas around dolines(sinkholes) with adequate and relativelyconstant water supply, but the species isalso found near river beds and gullies,where moisture tends to remain close tothe surface during the dry summer period.

Threatened and fragmentedpopulations

More than 40 populations of Z. abeliceaare known, mainly in Levka Ori (ca. 30)and in the Dhikti Mountains (ca. 10). Onlytwo populations occur in the PsiloritisMountains, and one small population inthe Thripti Mountains. This fragmenteddistribution occurred already prior to themodern, botanical exploration of Crete(ca. 300 years ago) and forms part of alively debate whether Crete was everdominated by continuous woodland

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Bosco Pomieri, Madonie Mountains, 1340 masl, a potential introduction site.(G. Garfì)

Z. abelicea, Omalos, Crete. (J. Gratzfeld)

before the arrival of man. To date, it is notresolved if the fragmented pattern of Z.abelicea populations is the result ofanthropogenic habitat transformation or ifits occurrence always consisted of apatchy distribution (Kozlowski et al., 2014).

Recent studies confirm however, that allpopulations are subject to threats fromovergrazing and browsing (goats andsheep), as well as from soil erosion,drought and fires. As a result, all standsof Z. abelicea are dominated by dwarfedand heavily browsed individuals. Thishabit is especially pronounced inrelatively small and isolated populations(e.g. in Thripti where there are no largetrees at all). This is of great concern toconservation as only fully developedtrees are able to flower and produce fruits(Fazan et al., 2012; Kozlowski et al.,2014). Z. abelicea has been included asEndangered (EN) on the IUCN Red List ofThreatened Species.

Each mountain chain representsa separate genetic andconservation unit

Because of the extreme fragmentation,gene flow between distant populations ishighly unlikely, mainly because of thelimited dispersal capacity of seeds. Thiswas confirmed by recent genetic studiesdemonstrating that Z. abeliceapopulations are highly genetically diversewithin and between the four mountainregions (Christe et al., 2014a). Thisindicates on the one hand that thecolonization of Crete by Z. abelicea is veryancient (probably before the earlyMiocene, some 25 million years ago), and,on the other hand, that each mountainchain with Z. abelicea populations shouldbe considered as a separate genetic unit.

Ex situ conservation challenges

In comparison with other Zelkovaspecies, especially those from EasternAsia, Z. abelicea is underrepresented inbotanic garden collections (Kozlowski etal., 2012). In addition, only a very smallportion of the genetic variability in naturalpopulations is found in ex situ collections(Christe et al., 2014b). In fact, allinvestigated individuals cultivated inbotanic gardens and arboreta, originatefrom one single region of the OmalosPlateau (Levka Ori), while the othergenetically distant populations do notappear to be in ex situ collections.

Future ex situ conservation efforts will needto consider the entire genetic diversity ofthe species, whilst avoiding geneticmixture of differentiated populations fromthe four mountain chains, especially whenestablishing field living collections(Kozlowski et al., 2012, 2014).Furthermore, dwarfed and heavily browsedpopulations do not produce seeds.Vegetative propagation is the only optionto establish collections of thesepopulations, enhancing the complexity andcosts of ex situ conservation measures.

In situ conservation challenges

Conventional measures of protection andmanagement, including effectivemethods to limit and/or completelyprevent livestock grazing and browsingshould be implemented by means offencing, and should comprise the entirerange of the genetic diversity of thespecies. Such measures require to bedeveloped in close collaboration with

shepherds and other stakeholders (e.g.local administration, municipalities,national park administration), andaccompanied by long-term scientificsurveys to monitor progress and allowadaptive management.

Ongoing conservation action

Based on the thorough research workundertaken in recent years, aninternational, interdisciplinary andintegrated conservation programme for Z.abelicea has been initiated. Theimplementation of the project is assumedby the Mediterranean Agronomic Instituteof Chania (MAICh) in collaboration withthe Forest Directorate of Chania (FDC) aswell as with forest agencies from otheradministrative regions of Crete.International coordination and scientificsupport is assured by researchers andconservationists from the Universities ofFribourg (Switzerland) and Athens(Greece), Botanic Gardens ConservationInternational (BGCI, United Kingdom) andthe Institute of Biosciences andBioResources of the National ResearchCouncil in Palermo (Sicily, Italy). Amongstothers, new and genetically representativeex situ collections (field living collectionsas well as seed banks) are beingestablished using seeds and vegetativeplant material sampled from all mountainregions where Z. abelicea occurs.Additionally, selected pilot plots havebeen fenced and are regularly monitoredby the team of MAICh and researchersand students of the University of Fribourg.What is more, a range of local andinternational campaigns and public

BGCI • 2015 • BGjournal • Vol 12.2 24

Distribution of Z. abelicea (red colour).Map by Natural History Museum Fribourg,Switzerland

Isolated, shrub habit population of Z. abelicea in the Thripti Mountains,Eastern Crete. (G. Kozlowski)

Seed collections for ex situ conservationof Z. abelicea at the MediterraneanAgronomic Institute of Chania, Crete. (G. Kozlowski)

outreach events have been realized,including scientific seminars, conferencesand exhibitions, accompanied by a seriesof first-rate public outreach materials.

Conclusions

The conservation challenges presented byZelkova spp. have attracted the attentionof researchers, conservation practitionersand horticulturalists in a joint endeavour tosecure the remaining genetic diversity inthe genus. Inspired by this sharedconcern, since 2010, a highlyinterdisciplinary and international researchgroup represented by partners fromEurope, the Caucasus and East Asia havebeen participating in the development andimplementation of an integratedconservation action plan for Zelkova spp.(Kozlowski G. & Gratzfeld J., 2013).

The isolated occurrence and rarity of Z.sicula and Z. abelicea provide an idealcontext to practise integrated conservationaction and serve as models forsafeguarding other threatened species.While the exclusion of grazing pressuresuch as through fencing is the mostpragmatic measure for immediateprotection in the wild, long-term in situconservation efforts need to beimplemented in close collaboration withlocal stakeholders and anchored innational legislation and policy. Systematicscientific evaluations to monitor progressand allow adaptive management will inturn, inform the nature of populationreinforcement programmes and options forpotential introduction to other analogousenvironments in situations where theoriginal habitat has been lost, or no longerprovides a viable option for the speciessurvival. This is especially urgent for Z.sicula, known from only two locations.

As elsewhere in the world, ex situconservation of Zelkova faces thechallenge of ensuring geneticallyrepresentative collections, preferably in thecountries of the species’ naturaldistribution, where current ex situ holdingsare still largely inadequate. The complexityof capturing the whole range of a species’genetic variation for ex situ conservation iswell illustrated by the distinct geneticdiversity of Z. abelicea found in each of itsfour main locations of occurrence. Whilethe remoteness and inaccessibility of someof the last remaining natural Zelkovapopulations prevent the broader publicfrom appreciating their grandeur in thewild, ex situ collections at botanic gardensand associated scientific institutions, playa critical role in enhancing environmentalawareness and education. Linking reportsof fossil finds with their extant relatives andnew population discoveries, Zelkova andrelict plants in general, can providecompelling stories to reach out to thewider society. Relict species from ancienttimes not only function as storehouses ofinformation of the Earth’s transformationsover millions of years but also deliver adiverse range of ecosystem services.Though ultimately a matter of societalchoice, their conservation may thereforepresent a vital element in the developmentof future ecosystem managementapproaches, especially in a period ofunprecedented, rapid global change.

References

,Brooker, R., Britton, A., Gimona, A.,Lennon, J. & Littlewood, N. 2011.Literature review: species translocationsas a tool for biodiversity conservationduring climate change. Scottish NaturalHeritage Commissioned Report No.440,68 pages.

,Christe, C., Kozlowski, G., Frey, D.,Bétrisey, S., Maharramova, E., Garfì, G.,Pirintsos, S. & Naciri Y. 2014a. Footprintsof past intensive diversification andstructuring in the genus Zelkova(Ulmaceae) in south-western Eurasia.Journal of Biogeography. 41: 1081-1093.

,Christe, C., Kozlowski, G., Frey, D.,Fazan, L., Bétrisey, D., Pirintsos, S.,Gratzfeld, J. & Naciri Y. 2014b. Do botanic garden collections capturethe genetic variation of wildpopulations? A molecular analysis oftwo relict tree species Zelkova abeliceaand Z. carpinifolia. Biodiversity andConservation 23: 2945-2959.

,Di Pasquale, G., Garfì, G. & Quézel P.1992. Sur la présence d’un Zelkovanouveau en Sicile sudorientale(Ulmaceae). Biocosme Mésogéen, 8-9: 401-409.

, Fazan L., Stoffel M., Frey D., Pirintsos S.& Kozlowski G., 2012. Small does notmean young: age estimation of severelybrowsed trees in anthropogenicMediterranean landscapes. BiologicalConservation 153: 97-100.

,Garfì G., Carimi F., Pasta S., Rühl J. &Trigila S., 2011. Additional insights onthe ecology of the relic tree Zelkovasicula di Pasquale, Garfì et Quézel(Ulmaceae) after the finding of newpopulation. Flora, 206: 407-417.

,Garfì G. & Buord S., 2012. Relictspecies and the challenges forconservation: the emblematic case ofZelkova sicula Di Pasquale, Garfì etQuézel and the efforts to save it fromextinction. Biodiversity Journal, 3 (4): 281-296.

,Kozlowski G., Frey D., Fazan L., Egli B.,Bétrisey S., Gratzfeld J., Garfi G. &Pirintsos S., 2014. Tertiary relict treeZelkova abelicea (Ulmaceae):distribution, population structure andconservation status. Oryx 48: 80-87.

,Kozlowski G., Gibbs D., Huan F., FreyD. & Gratzfeld J., 2012. Conservation ofthreatened relict trees through living exsitu collections: lessons from the globalsurvey of the genus Zelkova(Ulmaceae). Biodiversity andConservation, 21: 671-685.

,Kozlowski G. & Gratzfeld J., 2013.Zelkova – an ancient tree. Global statusand conservation action. NaturalHistory Museum Fribourg, Switzerland,60 pages.

, Lynch A.J.J., Barnes R.W., CambecèdesJ. & Vaillancourt R.E., 1998. GeneticEvidence that Lomatia tasmanica(Proteaceae) Is an Ancient Clone.Australian Journal of Botany 46: 25-33.

Joachim GratzfeldBotanic Gardens ConservationInternational, 199 Kew Road, Richmond, Surrey, TW9 3BW, United Kingdom, joachim.gratzfeld@bgci.org

BGCI • 2015 • BGjournal • Vol 12.2 25

Fenced pilot sites with Z. abelicea. Onthe left: non-fenced and heavily grazedarea. Xeropotamos, Crete. (M. Beffa)

Journal of Botanic Gardens Conservation International

Volume 12 • Number 2 • July 2015

Tree conservation and the role of

botanic gardens