Biological Conservation 158 (2013) 37–49

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Biological Conservation

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Review

European ash (Fraxinus excelsior) dieback – A conservation biology challenge

Marco Pautasso a,⇑, Gregor Aas b, Valentin Queloz c, Ottmar Holdenrieder c

a Centre d’Ecologie Fonctionnelle et Evolutive (CEFE), UMR 5175 CNRS, 34293 Montpellier, Franceb Ecological-Botanical Gardens, University of Bayreuth, 95440 Bayreuth, Germanyc Forest Pathology and Dendrology, Institute of Integrative Biology (IBZ), ETH Zurich, 8092 Zurich, Switzerland

a r t i c l e i n f o

Article history:Received 1 May 2012Received in revised form 15 August 2012Accepted 22 August 2012Available online 28 November 2012

Keywords:Assisted migrationBiodiversity lossDecline of common speciesEmerging diseasesForest pathologyFungal pathogensGeographical geneticsInvasion biologyRiparian woodlandTree breeding

0006-3207/$ - see front matter � 2012 Elsevier Ltd. Ahttp://dx.doi.org/10.1016/j.biocon.2012.08.026

⇑ Corresponding author.E-mail address: marco.pautasso@cefe.cnrs.fr (M. P

a b s t r a c t

Common ash (Fraxinus excelsior) is a keystone tree species throughout temperate Europe whose futureexistence is threatened by an emerging invasive fungal disease. Ash dieback, which first appeared in Polandin the 1990s, has rapidly spread to most eastern, central and northern European countries. The causal agentof the disease, the ascomycete Hymenoscyphus pseudoalbidus (anamorph Chalara fraxinea), was recentlydescribed as a new species. Given that the disease lethally affects ash trees of all age classes, and thatash tree mortality levels are high, F. excelsior and the many organisms dependent on ash trees are underthreat. Based on a literature survey, we provide an overview of the present knowledge on ash dieback, iden-tify practical recommendations and point out research needs. The observation of relatively resistant indi-vidual ash trees (although at very low frequency) calls for a rapid germplasm collection effort to establish abreeding program for resistance or tolerance to the disease. Ash trees that appear to be tolerant to the path-ogen should not be felled, unless they pose an unacceptable risk to people’s security. Given that the path-ogen does not form propagules on wood, and given the importance of deadwood for biodiversityconservation, dead and dying ash trees should be left in the forest. Landscape pathology and genetic toolscan be used to reconstruct the dispersal pathways of H. pseudoalbidus and to identify environmental fea-tures associated with variation in disease severity, so as to better predict the further development of theepidemic. Observations on differences in susceptibility of various ash species are needed to locate the geo-graphic origin of the pathogen and to identify Fraxinus species which might be used for resistance breedingor even replacement of F. excelsior. Conservation biologists, landscape managers, restoration ecologists,social scientists and tree geneticists need to engage with forest pathologists and the various stakeholdersthroughout the distributional range of F. excelsior so as to tackle this pressing conservation challenge.

� 2012 Elsevier Ltd. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 382. The characteristics and importance of common ash . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 383. Common ash dieback in Europe: a short history . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 394. Ash dieback: a major threat to European biodiversity. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 415. Ash dieback: research needs and recommendations for forest management. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 41

5.1. Reconstruct the invasion routes of H. pseudoalbidus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 415.2. Slow the further spread of the pathogen . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 425.3. Make use of available genetic diversity studies to guide surveys for genetic tolerance. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 425.4. Retain ash trees that are still only lightly/moderately damaged by the pathogen . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 435.5. Learn from other breeding programs to develop ash tree tolerance against H. pseudoalbidus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 435.6. Find common ground with rare plant reintroduction programs and assisted migration debates . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 435.7. Identify ash species tolerant against H. pseudoalbidus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 43

6. Conclusions. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 44Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 45References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 45

ll rights reserved.

autasso).

38 M. Pautasso et al. / Biological Conservation 158 (2013) 37–49

1. Introduction

Common ash (Fraxinus excelsior L.) is a major charismatic treespecies in Europe (ranging from Iran to Ireland, from southernScandinavia to northern Spain; Wardle, 1961; Kárpáti, 1970). Ashis a flexible species which can be found over a range of growingconditions (from riparian to mountain and steep slope stands, frompioneer to mature and old-growth woodland, from nutrient-rich topoorer soils; Scurfield, 1959; Roloff and Pietzarka, 1997; Marigoet al., 2000; Stöhr and Lösch, 2004; Ferrazzini et al., 2007; Dufourand Piégay, 2008). Its drought tolerance and frost sensitivity wouldhave made ash a tree species potentially favoured by the expectedclimate warming and drying (Percival et al., 2006; Scherrer et al.,2011). It occurs as an admixed tree species in various forest com-munities, but rarely attains dominance (Ellenberg, 2010). Commonash trees are important for the functioning and conservation of for-est ecosystems throughout much of Europe.

Common ash is now threatened in much of its distributionalrange by an emerging fungal disease caused by the ascomyceteHymenoscyphus pseudoalbidus (see below). This review aims to pro-vide an overview about common ash conservation management byintegrating current knowledge on ash ecology and the new disease.The review provides (1) a summary of the features and importanceof common ash, (2) a short history of the dieback currently affect-ing this species through a large part of its distributional range, (3)reasons to believe that this dieback will have repercussions for theconservation of European biodiversity, and (4) an overview of re-search needs in relation to the epidemiology of the pathogen andthe potential consequences of ash dieback for biodiversity. The lit-erature review was conducted at the end of 2011 in Web of Science(all databases), Google Scholar, Scopus and CABI Abstracts usingkeywords such as ‘‘Fraxinus’’, ‘‘Fraxinus excelsior’’, ‘‘ash dieback’’,‘‘Chalara fraxinea’’, and ‘‘Hymenoscyphus pseudoalbidus’’. The list ofcited references within relevant papers was scanned for furtheruseful articles, and new papers citing the retrieved literature werechecked.

2. The characteristics and importance of common ash

The current distribution of F. excelsior is shaped by the followingfactors (Wardle, 1961; Marigo et al., 2000; Myking, 2002; Glenzet al., 2006):

� a northern boundary due to winter cold and a southern oneshaped by summer drought;� an intermediate status between a pioneer species and a perma-

nent forest component;� shade tolerance as a sapling, but light demand as a mature tree;� avoidance of nutrient-poor soils and acidic soils with pH < 4.2;� low competitivity against beech on sites with growing condi-

tions optimal for beech.

According to recent phylogenetic analyses, F. excelsior is one of43 Fraxinus species occurring in temperate and subtropical regionsof the northern hemisphere (Wallander, 2008). The closest rela-tives of F. excelsior are F. angustifolia, F. platypoda, F. mandshuricaand F. nigra (Wallander, 2008). Interspecific hybrids from natureare known for F. excelsior x F. angustifolia (Fernandez-Manjarreset al., 2006; Gérard et al., 2006a,c) and at least a few successfulcontrolled crosses with F. excelsior were reported for F. americanaand F. pennsylvanica (Santamour, 1981). There is little agreementabout genetic differentiation of ash trees at different sites (e.g.,moist vs. dry conditions; Höltken et al., 2003; Hebel et al., 2006;Dacasa-Rüdinger et al., 2008; see also Marchin et al., 2008 forF. americana).

The mating system of common ash is a continuum from puremale (producing pollen) to pure female individuals (producingseeds) with differing degrees of hermaphroditism in between(FRAXIGEN, 2005; Wallander, 2008; Bochenek and Eriksen, 2011).It appears however that ash might be subdioecious or functionallydioecious (Wallander, 2001; FRAXIGEN, 2005). Both pollen andseeds (contained in samaras) are mainly wind-dispersed (Baclesand Ennos, 2008; Floran and Mihalte, 2010), but seeds can alsodisperse along watercourses and survive in water for several weeks(Dacasa-Rüdinger and Dounavi, 2008). Fruit fall is distributedthroughout the winter/spring (Gardner, 1977), but fruit productionvaries from year to year (Tapper, 1992). This variation is balancedby seed viability for 2–3 years (Wardle, 1961). The embryo insideripe seeds is only partly developed at the time of dispersal andthe seeds remain dormant for one vegetation period (sometimesfor two or more) before germinating (Dacasa-Rüdinger andDounavi, 2008). Common ash trees can reach an age of 300 yearsand heights of 40 m, with 45 m reported from an exceptional standin the West Carpathians (Hultén, 1941; Holeksa et al., 2009).Common ash stands and scattered trees are usually regeneratednaturally, but there is some use of ash seedlings from tree nurseries.

Common ash has long played important socio-cultural, eco-nomic and ecological roles (Dumont, 1992; Scheer, 2001; Bellet al., 2008):

� according to Norse mythology, Yggdrasil is the great ash treeholding the universe together with its mighty roots andbranches (Marzell, 1925; James, 1968);� the proto-language of Indo-Europeans is thought to have had a

word for ash tree, which implies that Indo-Europeans are likelyto have originated from a region where ash trees were present(Gamkrelidze and Ivanov, 1990);� it has been long known that some species of ash trees (mainly F.

ornus, but also F. excelsior) exude a sugary substance (manna),but ash bark may also have unrecognized medical potential.Linnaeus wrote in 1735 that the bark of ash trees has anti-malarial properties, and indeed a recent study reported thatbark extracts of F. excelsior inhibit the in vitro growth of asexualstages of Plasmodium falciparum (Aydin-Schmidt et al., 2010);� common ash is a ring-porous, noble hardwood. Its timber is in

high demand because of its properties (elastic, hard, resistantto pressure) which make it very valuable for the production offurniture, veneer, flooring, composite wood, tool handles andsport equipments (Pliura and Heuertz, 2003; Ballian et al.,2008; Bell et al., 2008; Krackler et al., 2010). However, the eco-nomic importance of common ash is difficult to assess, becausehardwoods other than beech are usually combined in foreststatistics;� leaf-hay harvesting from ash trees provided fodder for livestock

in wooded rural areas during drought, and this practice has leftimportant legacies from a nature conservation point of view(Haas, 2002). Pollarded ash trees are iconic elements of manyEuropean landscapes and provide invaluable, yet declining hab-itat for rare epiphytic lichens (Moe and Botnen, 1997; Jüriadoet al., 2009a; Paltto et al., 2011).

Whereas both in North America and in Asia 20 Fraxinus speciesare present, in Europe F. excelsior is one of just three Fraxinus spp.(Wallander, 2008), a confirmation of the impoverished flora ofEurope compared to other continents. Genetic studies of chloro-plast DNA have shown relatively high genetic differentiationamong F. excelsior populations (Fig. 1), suggesting a separate recol-onization history from different refugia (Iberia, the Apennines, theEastern Alps and the Balkans), whereas nuclear DNA markersshowed relatively low differentiation among populations, suggest-ing high levels of pollen flow (Heuertz et al., 2004a). However, in a

Fig. 1. Chloroplast DNA variation of F. excelsior in Europe, showing the influence of the recolonization from ice-age refugia in Southern and Eastern Europe on currentcommon ash genetic diversity (from Heuertz et al., 2004a).

M. Pautasso et al. / Biological Conservation 158 (2013) 37–49 39

comparison among 23 tree species native to Norway, the geneticresources of F. excelsior were assessed as vulnerable, because ofits scattered distribution and relatively limited gene flow amongpopulations (Myking, 2002). Ash phenology shows high variabilityamong neighbouring trees, with differences up to 2 weeks in thestarting date of flowering, leaf-unfolding and leaf-fall in contiguoustrees (Wardle, 1961; Tapper, 1992).

3. Common ash dieback in Europe: a short history

A major emerging disease is now threatening common ashthroughout most of its distributional range (Kowalski andHoldenrieder, 2009a). The current ash dieback was first observedin North-Eastern Poland at the beginning of the 1990s, withoutidentification of its cause (Przybyl, 2002). Widespread dieback ofmature ash trees has been reported also before, e.g. from the USA(Tobiessen and Buchsbaum, 1976; Houston, 1981; Castello et al.,1985) and Britain (Hull and Gibbs, 1991), but the current levelsof ash mortality dwarf previous observations and all developmen-tal stages from saplings to trees are now affected. Initially, it washypothesized that frost or drought may have caused the diebackin Poland (Pukacki and Przybyl, 2005). Although both abiotic fac-tors may have predisposed ash trees to the dieback (Tulik et al.,2010), it is now clear that a fungus is the primary causal agent(Kowalski and Holdenrieder, 2009a; Schumacher et al., 2010;Kräutler and Kirisits, 2012).

By the time the pathogen was identified as a new anamorphicspecies, Chalara fraxinea (Kowalski, 2006), ash tree mortality hadbeen observed throughout Poland (Gil et al., 2006) and then inneighbouring countries (in order of report: Lithuania, Latvia,Sweden, Germany, the Czech Republic, Denmark, Slovakia, Belarus,Estonia, and Austria; Schumacher et al., 2007; Halmschlager and

Kirisits, 2008; Jankovsy and Holdenrieder, 2009; Dehnen-Schmutzet al., 2010; Timmermann et al., 2011; Fig. 2). Ash dieback has nowreached Slovenia (Ogris et al., 2009), Norway (Talgø et al., 2009),Hungary (Szabo, 2009; Koltay et al., 2012), Finland (Rytkönenet al., 2011), Switzerland (Engesser et al., 2009; Fig. 3), north-eastern France (Husson et al., 2011), north-eastern Italy(Ogris et al., 2010), Belgium (Chandelier et al., 2011), Croatia(Timmermann et al., 2011) and the Netherlands (Anon, 2010). Re-cently, the pathogen was also detected in UK tree nurseries (BritishEcological Society, 2012; Goudet and Piou, 2012).

Disease symptoms range from necrotic leaf spots to bark can-kers associated with xylem necroses and wilting, eventually lead-ing to tree death. The dieback starts with ascospore infection ofleaves. Ascospores are produced during summer in apothecia onleaf remnants from the previous year on the ground and dispersedby wind (Kowalski and Holdenrieder, 2009b; Timmermann et al.,2011; Gross et al., 2012; Kirisits et al., 2012). Leaf infection is fol-lowed by necrotic lesions spreading along the rachis into the shoot,cankering, wilting and dieback of shoots and wood discoloration(Kowalski and Holdenrieder, 2008; Bakys et al., 2009; Kräutlerand Kirisits, 2011). Shoot and stem infection is a dead end for thepathogen, because generally no apothecia are formed on these sub-strata. Spores of the anamorphic state, in contrast, only act as sper-matia and do not seem to be involved in the infection process(Gross et al., in press).

Although the anamorphic state C. fraxinea was at first linkedmorphologically to the ascomycete Hymenoscyphus albidus, a sap-rotrophic and potentially endophytic leaf colonizer which has longbeen observed in Europe without causing disease (Kowalski andHoldenrieder, 2009b), further molecular investigations showedthat the teleomorph of C. fraxinea is indeed a previously unde-scribed cryptic species (which was named H. pseudoalbidus; Quelozet al., 2011). A survey in Denmark showed that the recent

Fig. 2. Distributional range of F. excelsior (blue, from EUFORGEN) and of ash dieback due to C. fraxinea (red). Darker red colours indicate earlier national observation of thedieback. The map only represents presence/absence of the dieback in a country: no inference on H. pseudoalbidus occurrence at local scales should be drawn from it. Thepathogen has been recently reported also from plant nurseries in England and a recently planted woodland in Scotland (British Ecological Society, 2012; Webber and Hendry,2012).

Fig. 3. Records of F. excelsior stands with dieback due to H. pseudoalbidus in Switzerland, 2008–2011 (maps from Wald, Schnee und Landschaft (WSL) Research Institute,Birmensdorf, CH). The figure shows that the pathogen population has not just been expanding, but that it expanded very rapidly (in 2 years, from a few reports to a wholeregion affected). The figure also shows the importance of natural barriers (the Ticino canton is still not affected, thanks to the protecting influence of the Alps).

40 M. Pautasso et al. / Biological Conservation 158 (2013) 37–49

expansion of H. pseudoalbidus has resulted in H. albidus becoming arare species, possibly because the two fungi occupy the same niche(McKinney et al., in press).

The disease has not just spread over long distances, but has rap-idly caused high levels of ash tree mortality in all age classes. Forexample, in Denmark ash dieback was first observed in 2003, be-came common by 2005 (particularly on young stands), by 2008

was reported as extensive on about one third of all monitoredash trees and by 2009 was affecting ash trees of all ages in all partsof the country (Lorenz et al., 2008; Skovsgaard et al., 2010;McKinney et al., 2011). Similar observations were made inSwitzerland (Fig. 3). In Sweden, although F. excelsior trees makeup about 1% of the standing tree volume (Fischer and Lorenz,2011), ash decline is felt as a major threat given the cultural value

M. Pautasso et al. / Biological Conservation 158 (2013) 37–49 41

and landscape aesthetics role of ash trees in the southern part ofthe country (for climatic reasons, ash is not present in northernSweden). In 2009, about one fourth of ash trees in southern Swe-den was reported as dead or severely damaged (Fischer et al.,2010). F. excelsior has been declared to be under threat in Swedenand included in 2010 as ‘vulnerable’ in the Red List of that country(Pihlgren et al., 2010; Stenlid et al., 2011).

4. Ash dieback: a major threat to European biodiversity

The widespread distribution and frequently high local abun-dance of ash does not appear to make it less vulnerable to the die-back. The death of vast numbers of common ash trees is likely tohave major ecological consequences for European biodiversityand forest ecosystems (including tree biomass and thus carbonsequestration), as suggested by other examples of declines of oncecommon tree species (Liebhold et al., 1995; Orwig, 2002; Lovettet al., 2006; Gaston and Fuller, 2008; Gaston, 2011) and removalexperiments (Ellison et al., 2005, 2010).

National surveys show that ash dieback due to H. pseudoalbidusis now occurring over entire countries, for example throughoutPoland (Gil et al., 2006), Denmark (Skovsgaard et al., 2010), Austria(Kirisits, 2011a,b), Slovakia (Kunca et al., 2011) and Germany(Anon, 2011b; Metzler, 2011). It is thus to be expected that the fun-gal pathogen will be able to disperse over the whole distribution ofF. excelsior over the next years (Anon, 2011a), thus affecting coun-tries and regions where ash dieback has not yet been observed(Ireland, northern Spain, western, southern and central France,north-western Italy, Bulgaria, Serbia, Kosovo, Macedonia, Albania,northern Greece, northern Turkey, Ukraine, Moldova, Russia,Georgia, Armenia, Azerbaijan, Iran) (see Fig. 1 and Wardle (1961)for a distribution map of F. excelsior). Also F. angustifolia, a vicariantspecies with a Mediterranean distribution (Gérard et al., 2006b),has been shown to be susceptible to H. pseudoalbidus (Kirisitset al., 2009b, 2010).

Ash dieback poses a major threat to European biodiversity be-cause of the keystone role of F. excelsior in floodplain forest ecosys-tems in Europe. Riparian forests have already been impoverished inrecent years by the loss of many elm (Ulmus spp.), alder (Alnus spp.)and pedunculate oak (Quercus robur) trees, due to Dutch Elm Dis-ease, Phytophthora alni, and various soil-borne Phytophthora spe-cies, respectively (Brasier, 1991; Jung et al., 2000; Thomas et al.,2002; Brasier et al., 2004). The loss of a high proportion of ash treesis likely to have a cascade of ecological effects on ecosystem ser-vices and biodiversity. This is the case not just in riparian wood-lands (Wardle, 1961; Harper et al., 1997; Volk, 2002), but alsowherever ash trees are found, from field margins, hedgerows andscattered trees in agro-ecosystems (Orlowski and Nowak, 2007;Hemery et al., 2010) to parks, gardens and tree avenues in urbanareas (Aksoy and Demirezen, 2006; Tubby and Webber, 2010).

Ash trees have increased in numbers in recent years in oakwoodland, possibly due to the ability of F. excelsior to make use ofgrowing nitrogen inputs (Hofmeister et al., 2004; Amar et al.,2010). Also abandoned grassland is often colonized by ash trees,where F. excelsior acts as a pioneer species in woodland recoloniza-tion (Wardle, 1961; Marie-Pierre et al., 2006). The ecological andphysiological flexibility of ash, and the general rural abandonmentwhich is occurring in marginal and mountainous European areas,have resulted in a general expansion of this tree species over thelast decades (Marigo et al., 2000; Streštík and Šamonil, 2006;Krackler et al., 2010; Dobrowolska et al., 2011). This expansion im-plies that there is now more to lose from ash dieback than if ash hadremained a relatively rare species. Another consequence may bethat the dispersal and population dynamics of H. pseudoalbidus isfacilitated by the higher density of ash trees. A similar phenomenonhappened with elm trees, which were frequently planted

throughout Europe and North America before succumbing toOphiostoma ulmi and O. novo-ulmi and their bark beetle vector.Luckily, elm trees were not completely removed from Europeanlandscapes due to Dutch Elm Disease, but eradication of F. excelsiordue to ash dieback (despite the lack of a vector for H. pseudoalbidus)is still not to be excluded.

One problem is that both for elm and for ash trees we have littleknowledge of how much biodiversity strictly depends on the pres-ence of those tree species, compared to more thoroughly studiedtree species such as Fagus sylvatica (Moelder et al., 2008; Smithet al., 2008; Gandhi and Herms, 2010; Walentowski et al., 2010).There is much evidence showing that many organisms depend onthe presence of trees to survive, from wood-decaying fungi to sapr-oxylic insects, from epiphytic lichens to geophytes and birds(Jarolimek, 1994; Emborg et al., 2000; Lonsdale et al., 2008; Jüriadoet al., 2009b; Chiari et al., 2010; Dahlberg et al., 2010; Thor et al.,2010; Molina et al., 2011). The wood-decaying fungi Peniophoralimitata, Hypoxylon moravicum and H. fraxinophilum are reportedto be specific to F. excelsior (Helfer and Blaschke, 2001). Moreover,308 fungi occurring on F. excelsior (including an unknown numberof host-specific taxa) are listed in the USDA database (http://nt.ars-grin.gov/fungaldatabases/). The arbuscular symbiont(s) of F.excelsior also deserve attention (Turrini and Giovannetti, 2012).In contrast to other Fraxinus species, F. excelsior roots only appearto form arbuscular mycorrhiza but no ectomycorrhiza (Weberand Claus, 2000; Lang and Pohle, 2011; Lang et al., 2011).

For organisms that specifically depend on F. excelsior, the loss ofash trees from entire landscapes would mean the loss of their hab-itat, and thus potentially their extinction. This loss can be predictedon the basis of species-area relationships that have been builtusing as area the abundance of tree species and as species richnessthe number of species of various groups of fungi and insects re-corded on those tree species, provided that those organisms aretree-species dependent and cannot shift to another host (Strongand Levin, 1975; Kennedy and Southwood, 1984; Newton andHaigh, 1998; Brändle and Brandl, 2001; Miller, 2012). This extinc-tion potential has been demonstrated by a Swedish study of theedge effects of ash dieback on the demography and metapopula-tion parameters of a red-listed epiphytic moss Neckera pennata, agood indicator of other threatened bryophytes and lichens(Roberge et al., 2011). Even if such disappearance were to happenafter a certain lag time (due e.g. to the survival of some ash treesfor some years), there is the potential for a major loss of biodiver-sity (Kuussaari et al., 2009).

Particularly threatening from a biodiversity conservation pointof view is the loss of ancient ash trees (Denzler, 1998; Pautassoand Chiarucci, 2008; Rackham, 2008; Lindbladh and Foster, 2010;Stagoll et al., 2012), but also young F. excelsior trees are importantfor some threatened species (e.g. the butterfly Euphydryas maturna;Freese et al., 2006). Common ash is also a key species supportingland mollusc diversity (Rüetschi, 1999). The biodiversity loss dueto ash dieback would happen on top of all other biodiversity lossesalready taking place in Europe (e.g. due to habitat fragmentation,degradation and shift, as a consequence of agricultural intensifica-tion, urban sprawl and densification, in relation to air, water andsoil pollution, and following climate changes; Jenouvrier andVisser, 2011; MacLean and Wilson, 2011; Seidl et al., 2011;Balmford et al., 2012; Driscoll et al., 2012).

5. Ash dieback: research needs and recommendationsfor forest management

5.1. Reconstruct the invasion routes of H. pseudoalbidus

Landscape ecology tools can be used to study the spatio-temporal distribution and development of ash dieback over a range

42 M. Pautasso et al. / Biological Conservation 158 (2013) 37–49

of scales. This may enable to assess whether there are differencesin disease incidence and severity among regions, and, in that case,whether there are environmental features that can help predict ashdieback development (Holdenrieder et al., 2004; Xu et al., 2009;Chadfield and Pautasso, 2012; Xhaard et al., 2012). Spatial analysisshould take advantage of the genetic tools now available to detectH. pseudoalbidus (Ioos et al., 2009; Chandelier et al., 2010; Johans-son et al., 2010; Ioos and Fourrier, 2011). Sensitive markers tostudy the genetic variability of the pathogen in space and timeare now available (Bengtsson et al., 2012; Gross et al., 2012; Krajet al., 2012). A major genetic study of C. fraxinea in all affectedcountries would provide insights about how the pathogen hasmoved and how it is likely to further disperse. Useful insightsmay also be obtained from spatially explicit simulations integrat-ing information about host distribution, realistic features of thetree nursery network and the effect of control policies (Harwoodet al., 2009).

5.2. Slow the further spread of the pathogen

Slowing down the expansion of ash dieback is difficult given thenatural long-distance dispersal of fungal spores, which are able toeasily jump landscape patches without the presence of hosts, asdemonstrated by modelling studies (Shaw et al., 2006; Mundtet al., 2009; Wingen et al., in press). However, measures can be ta-ken to avoid additional artificial dispersal of the pathogen, e.g.avoiding the planting of infected ash saplings in woodlands. Forexample, foresters are now advised not to plant ash trees to regen-erate cut woodlands. Also landscaping might act as a dispersalpathway, given that ash dieback due to H. pseudoalbidus has alsobeen reported in tree nurseries (Burgess, 2009; Schumacheret al., 2010; Kirisits and Cech, 2011; Kirisits et al., 2012) and latentinfections can occur on the plants (Kirisits et al., 2012). Given thattree nurseries form a well-connected network of plant shipmentsall over Europe (Menkis et al., 2006; Jeger et al., 2007; Brennet al., 2008; Xu et al., 2009; Dehnen-Schmutz et al., 2010;Moslonka-Lefebvre et al., 2011), they may well have contributedto the rapid long-distance dispersal of the pathogen, which wasobserved over the last years.

5.3. Make use of available genetic diversity studies to guide surveys forgenetic tolerance

There is evidence for reduced susceptibility of some commonash tree individuals to H. pseudoalbidus (Pliura et al., 2011;McKinney et al., 2011). Interestingly, ash trees with early leafsenescence in autumn appear to be less susceptible (McKinneyet al., 2012). This finding is likely to be related to the infectionbiology of the pathogen, which enters trees through their leaves.Reduced susceptibility of some tree individuals is not necessarilydue to host genetic reasons, it could also be in part a random con-sequence of leaf infection occurring far from the stem or by otherpathogens which induce early leaf shedding, e.g. ash mildew(Phyllactinia fraxinea). Variation in ash susceptibility may also bedue to the local absence of secondary parasites, e.g. Armillariaspp. (Bakys et al., 2011). The presence of genetic tolerance to thepathogen would be a major sign of hope for the future of F. excelsiorin Europe. If tolerance is present without a history of co-evolutionbetween host and pathogen (Parker and Gilbert, 2004; Brown andTellier, 2011), it would represent an example of exapted resistance(Newcombe, 1998). There is a need for a major survey throughoutthe distributional range and in each country to establishcomprehensive germplasm collections and to breed for tolerance(Gonzalez-Martinez et al., 2006). This not just to identify lesssusceptible ash individuals, but also to make sure that the genetic

material then used to breed for tolerance captures populationgenetics patterns of ash trees throughout Europe, e.g.

� excess of homozygosity (which could be useful for local adapta-tion and has been observed in parts of Bulgaria, France,Germany and Italy; Heuertz et al., 2001; Morand et al., 2002;Hebel et al., 2006; Ferrazzini et al., 2007);� local differentiation among tree populations due to a patchy

distribution of suitable habitat (islands in Finland; Höltkenet al., 2003), but an absence of local differentiation in the caseof habitat fragmentation due to deforestation in Scotland(Bacles et al., 2005);� a clear longitudinal subdivision at the European scale (due to

the ice age recolonization from different refugia; Heuertzet al., 2004a,b; Fig. 1);� isolation by distance (populations tend to be similar if close

geographically; Heuertz et al., 2006).

An important finding from this point of view is the recent rec-ognition that F. excelsior may have survived the last ice age innorthern refugia (as far north as Scotland; Sutherland et al.,2010). Surveys for ash tolerance to dieback should thus considernot just the traditional glacial refugia (e.g., the Balkans; Jarniet al., 2011) because of the high genetic and morphological vari-ability found there, but also ash populations at other boundariesof its distributional range. The importance of both rear and frontrange edges for tree genetic diversity is also suggested by the highlevels of genetic differentiation found for Ulmus laevis in Finland(Vakkari et al., 2009) and for Austrocedrus chilensis at its northernrange boundary in Patagonia (Arana et al., 2010). Although thereis still debate in the sampling effort level and the specificity ofprimers necessary to survey/make use of the genetic diversity ofF. excelsior (Boshier and Stewart, 2005; Harbourne et al., 2005;Miyamoto et al., 2008; Arca et al., 2012), it is clear that identifyingtolerance to H. pseudoalbidus and then planting a few ash clonesthroughout Europe would not be a solution. Resistance to the path-ogen can be overcome and the maintenance of high levels of genet-ic diversity is needed to face other impending challenges such asglobal warming, more frequent extreme events and other ashpathogens (Burley and Kanowski, 2005; Kaminska and Berniak,2009; Pautasso, 2009, 2012; Orlikowski et al., 2011). Currently,H. pseudoalbidus shows a low allelic diversity, which is typical ofintroduced organisms (Gross et al., 2012). Additional pathogenintroductions might occur, which would increase the genetic flex-ibility of the pathogen. Therefore, restoration activities should aimfor the selection of a genetically diverse population of ashes show-ing quantitative rather than qualitative resistance.

Preliminary results to assess heritability in ash tolerance to H.pseudoalbidus infection are appearing. In a progeny trial at threelocations in Lithuania, ten Lithuanian and 14 European F. excelsiorpopulations were found to show high heritability (�0.40) in toler-ance to H. pseudoalbidus infection, even if only 10% of individualtrees survived after 8 years (Pliura et al., 2011). In a Danish study,most tested ash trees were highly susceptible to H. pseudoalbidus,with only an estimated 1% with the potential of producing off-spring with less than 10% of crown damage under the current dis-ease pressure (Kjær et al., 2012). The question arises of whetherthis expected very low survival applies throughout the distribu-tional range of ash (Kessler et al., 2012). In terms of population via-bility, 1% of survival would have been even more problematic if ashhad been a rare species. However, in stands where ash is abundantthe inoculum of H. pseudoalbidus may build up more easily thusleading to density-dependent tree mortality. To guide surveys fortolerance, we need to know whether the disease is spreadingeverywhere regardless of ash density or whether isolated ash treesare less affected than ash trees located close to many ash trees.

M. Pautasso et al. / Biological Conservation 158 (2013) 37–49 43

Suitable data from forest inventories are generally lacking, becauseash has traditionally been surveyed together with other deciduoustree species. Surveys targeted to Fraxinus (within and outside for-ests) are needed.

5.4. Retain ash trees that are still only lightly/moderately damaged bythe pathogen

In order for the identification of tolerant trees to be possible,ash trees that are still only lightly/moderately affected by the path-ogen should be given a chance to survive. This is all the more so gi-ven that expected survival of ash trees is very low (�1%; Kjær et al.,2012; but see Kessler et al., 2012). Ash pollen and seed dispersal infragmented landscapes has been shown to occur up to distances ofmore than three kilometers (Bacles et al., 2006; Bacles and Ennos,2008), thus emphasizing the importance of retaining ash treespotentially tolerant to the pathogen to allow the species to recoverfrom the dieback. Removing from affected forests all ash trees (aswas recently done in Japanese larch (Larix kaempferi) plantationsaffected by Phytophthora ramorum in Britain; Brasier and Webber,2010) would make it impossible to identify which ash trees are tol-erant and for a new generation of ash to develop. A similar reactiontook place during the 1950s against chestnut blight in Italy, wheremany ancient chestnut orchards were lost not because of the dis-ease (which was weakening due to hypovirulence), but becauseof people’s exaggerated perception of the chestnut blight threat(Pezzi et al., 2012).

Removing all infected ash trees would also exacerbate the lossof biodiversity due to ash tree mortality, as this would happenall at once over whole forests and landscapes (Foster and Orwig,2006; Michalcewicz and Ciach, 2012). Also considering the key roleof deadwood for ecological processes and many endangered organ-isms (Lassauce et al., 2011), and the widespread dearth of dead-wood in European forests due to forest management (Verkeriet al., 2011), dead and dying ash trees should be left in the forest,unless they pose a risk to security of forest workers and visitorsdue to falling decaying branches (Bieker et al., 2010). Dead ashtrees do not pose an epidemiological risk because stem infectionis normally a dead end for the fungus and sporulation normallyhappens on infected ash leaves only. Herbivore control measuresmay make sense to reduce browsing damage of ash saplings bydeer and other herbivores, so that any ash trees resistant to thepathogen may be given a chance to make such resistance visible.Control measures against bark beetles are debatable, because theash bark beetles (Hylesinus crenatus, H. oleiperda and Leperesinusvarius) normally do not attack very young trees which constitutethe main material for selection against disease susceptibility(Skovsgaard et al., 2010; Bakys et al., 2011; Kunca et al., 2011; Lenzet al., 2012; Pfister, 2012).

5.5. Learn from other breeding programs to develop ash tree toleranceagainst H. pseudoalbidus

Breeding programs similar to the one needed for ash in Europehave been developed e.g. for American chestnut (Castanea dentata)against chestnut blight (due to the ascomycete Cryphonectriaparasitica; Anagnostakis, 2012; Dalgleish and Swihart, 2012), forelm trees (Ulmus spp.) against Dutch Elm Disease (Santini et al.,2012), for white pines (Pinus spp.) against Cronartium ribicola (Kinget al., 2010), for Douglas fir against Armillaria ostoyae (Cruickshanket al., 2010), and for Fraxinus spp. in North America (due to thedieback caused by the emerald ash borer Agrilus planipennis;Widrlechner, 2011). Breeding programs against ash dieback shouldlearn from those experiences (Sharma et al., 2009; Alexander andLee, 2010; Koch et al., 2010a; Ingwell and Preisser, 2011), e.g.

� taking into account genotype x environment interactions;� considering that resistance to a given pathogen should not

imperil other aims such as resistance to drought;� avoiding basing recommendations on single/a few resistant tree

individuals;� making use of conserved functional domains of disease-

resistance genes among different plant species;� exploring the option of introgression breeding (in analogy with

the American chestnut program, discovering the origin of thepathogen would be important);� taking advantage of citizen science to increase the effectiveness

and efficiency of surveys to identify potentially tolerant treeindividuals.

A difficulty in achieving durable ash tolerance against H.pseudoalbidus is that the pathogen appears to be morphologicallyvariable and to be reproducing sexually (Kowalski and Bartnik,2010; Bengtsson et al., 2012; Gross et al., 2012), which would im-ply that tolerance, if based on a narrow genetic basis, might be rap-idly overcome.

5.6. Find common ground with rare plant reintroduction programs andassisted migration debates

Similar lessons can be learnt from plant species reintroductionprograms, where the following measures appear to increase thelikelihood of success (Albrecht et al., 2011; Godefroid andVanderborght, 2011; Godefroid et al., 2011):

(a) targeting protected/managed sites rather than the wholelandscape;

(b) transplanting seedlings rather than sowing seed (but thismay not be the case for ash; Jinks et al., 2006);

(c) using a high rather than low number of reintroducedindividuals;

(d) taking material from diverse and stable source populations;(e) monitoring long-term reintroduction success; and(f) basing decisions on geographical patterns in the genetic var-

iation of the species to be reintroduced.

A breeding and reintroduction program for common ash wouldneed to find common ground also with current debates on novelecosystems (Carroll, 2011; Araújo et al., 2011; Hewitt et al.,2011; Hobbs et al., 2011) and the need for assisted migration ofplant species that are likely not to be able to migrate fast enoughto cope with the expected climate shifts (Seabrook et al., 2011;Weeks et al., 2011). Assisted migration activities to enable plantspecies to cope with rapid climate change could result in the inad-vertent movement of plant pathogens (Brasier, 2008; MacLeodet al., 2010; Garbelotto and Pautasso, 2012).

5.7. Identify ash species tolerant against H. pseudoalbidus

One potential intervention which could make sense in the ex-treme case of widespread disappearance of common ash is itsreplacement with other ash species (e.g. F. pennsylvanica, whichshows invasive behaviour in several European floodplain forests;Schmiedel, 2010). Such wholesale species replacements may leadto opposition from conservation biologists but may well have tohappen anyway over this century due to rapid climate shifts(Kou et al., 2011; Ruiz-Labourdette et al., 2012; Zhu et al., 2012).Fraxinus species showing no or only little disease expression afterinfection may have coevolved with the pathogen and thereforeindicate the geographic origin of H. pseudoalbidus.

Several Asian and American ash species planted in Europe wereonly little or moderately affected by the disease (F. mandshurica, F.

Fig. 4. Four basic scenarios for the further development of ash dieback in Europe,based on future levels of pathogen dispersal and host susceptibility. If both areconsistently high, host disappearance may take place. If pathogen dispersal islimited, high host susceptibility may matter less. Should instead common ashsusceptibility be limited in some regions, the impact of the dieback would be lessdevastating. Each scenario can be considered for various regions and countries, aswell as for the whole distribution of common ash. Further dimensions to beconsidered are the conduciveness of the environment to disease, as well as humanactions to prevent further worsening of the dieback.

44 M. Pautasso et al. / Biological Conservation 158 (2013) 37–49

americana, F. pennsylvanica; Drenkhan and Hanso, 2010) orappeared to be resistant after wound inoculation (F. chinensis,F. bungeana, F. latifolia, F. pennsylvanica, F. velutina; Aas andHoldenrieder, unpubl.). The European F. ornus, which is closelyrelated to the Asian F. bungeana, appears to be resistant againstnatural infection, but developed limited necrotic lesions after arti-ficial inoculation (Kirisits et al., 2009a; Kräutler and Kirisits, 2012).In contrast, the American black ash (F. nigra), which is closely re-lated to F. mandshurica, is very susceptible. This pattern suggestsan origin of the pathogen in Asia, as already suspected by Quelozet al. (2011). However, these observations are based on a smallnumber of trees and provide only circumstantial evidence for resis-tance or tolerance of these species. Therefore, careful monitoring ofexotic ash species in the presence of disease on surrounding F.excelsior (and F. angustifolia; Kirisits et al., 2009b; Kräutler andKirisits, 2012) is needed.

In addition, ash species tolerant to the disease might be candi-dates for introgression breeding with F. excelsior. Hybridisation ofF. excelsior with other ash species, combined with subsequentintrogression breeding might be a feasible, yet time consumingway to achieve ash tolerance to the pathogen (Fritz et al., 1999;Koch et al., 2010b). Unfortunately, experience with other pathosys-tems shows that very few resistant host genotypes may result fromthis approach (e.g. Vigouroux and Olivier, 2004; Solla et al., 2005;Jacobs, 2007).

6. Conclusions

Thanks to environmental change, globalization, increased long-distance trade and the transport of plants for planting, invasiveorganisms have become a major threat to biodiversity and ecosys-tem services in Europe and elsewhere (Aukema et al., 2010;Holzmüller et al., 2010; Vilà et al., 2010; EFSA PLH, 2011; Esslet al., 2011; Garnas et al., 2011; Keller et al., 2011; Mostowy andEngelstädter, 2011; Fisher et al., 2012; Kenis et al., 2012; Liebholdet al., 2012). H. pseudoalbidus provides a further and vivid exampleof such a threat, which could potentially affect also the muchhigher biodiversity of Fraxinus spp. in North America and China,provided that those ash species are equally susceptible to thepathogen and that the fungus is introduced from Europe, estab-lishes itself, spreads over long distances, and causes a similar levelof tree mortality (APHIS, 2009).

The rapid expansion of the pathogen in all directions fromPoland, together with the fact that the host is very frequently killedby the pathogen, is in favour of considering H. pseudoalbidus as anorganism introduced to Europe (Timmermann et al., 2011; Quelozet al., 2011; Kirisits et al., 2012). In addition, the low allelic richnessdetected using microsatellites confirms an introduction event(bottleneck) (Bengtsson et al., 2012; Gross et al., 2012). This imme-diately raises the question of the origin(s) of the pathogen, which isan important question to answer to avoid the inadvertent intro-duction of additional pathogen strains, to study potential biologicalcontrol options, and to locate potential common ash crossing part-ners for introgression breeding. Given that the pathogen has ex-panded towards the south of Poland and not just towards thenorth, it is difficult to identify a simple role for the recent climatewarming in explaining ash dieback (Alfaro et al., 2010). Neverthe-less it is to be expected that similar phenomena (host shifts, genet-ic recombination, pathogen dispersal) could become morecommon in the future due to the various global changes, thus pro-ducing cumulative effects on tree biodiversity, health and produc-tivity (Slippers et al., 2005; Stenlid et al., 2007; Giraud et al., 2010;Jacob et al., 2010; Pautasso et al., 2010; Gange et al., 2011;Heilmann-Clausen and Læssøe, 2012).

Interdisciplinary research is needed to find solutions to theconservation biology challenge posed by common ash dieback

throughout Europe. Forest pathologists need to work together withconservation biologists, forest and landscape managers, plantbreeders, restoration ecologists, social scientists and tree geneti-cists (Tallmon et al., 2004; McKay et al., 2005; Waring and O’Hara,2005; Laine et al., 2011; McRoberts et al., 2011; Pliura et al., 2011;Brukas and Sallnäs, 2012), so as to:

(1) leave selection to the pathogen and identify (experimen-tally) resistant or tolerant ash individuals;

(2) protect them and release them from competition with otherspecies;

(3) start a breeding program which develops resistance whilstpreserving overall ash genetic diversity and its regional pat-terns of differentiation;

(4) reintroduce resistant/tolerant ash where it has disappeared.

Scenarios should be built to map the potential further develop-ment of ash dieback across Europe, building on (Kass et al., 2011):

� previous studies on regional outbreaks of (exotic) treepathogens;� knowledge about spatial variation in pathogen resistance of

natural plant populations (Laine et al., 2011);� the restrictions in the use of fungicides in forests, as well as the

problems that would derive in nurseries by fungicides maskingsymptoms on infected seedlings (Parke and Grünwald, 2012);� the still limited epidemiological knowledge on H. pseudoalbidus;� the much larger body of research on the ecology of F. excelsior

(which has however been produced without having this newproblem in mind, and is not as large as for other tree speciessuch as e.g. F. sylvatica);� evidence on the current human impacts on European ecosys-

tems (e.g. widespread alteration of floodplains and riparian for-ests; Gurnell et al., 2008);� models of the expected biotic consequences of the expected

shifts in climate, land use and other global change drivers overthe coming decades; and� the perception of the problem by the various stakeholders, as

well as their likely reactions to variation in the factors above(Kelly et al., 2012).

For example, in case of continuing expansion of the pathogenand unabated tree mortality levels, widespread common ashdisappearance can be envisaged. If instead the spread of thepathogen can be slowed down, and pathogen infection does not

Table 1Summary of proposed measures to reduce the threat posed by common ash dieback to F. excelsior and its associated biodiversity (modified from Kirisits et al., 2012).

Option Explanation

Quarantine for ash nurseryseedlings

Ban the trade of ash nursery seedlings from areas already infected (plant passporting and certification schemes are difficult due tolatent infections)

Avoid planting of ash in forests andlandscapes

Planting of infected ash seedlings in forests is likely to have contributed to the rapid spread of the pathogen. Increased ash treedensity in the open landscape might provide stepping stones for the pathogen

Do not remove ash trees fromforests

The chance should be given to resistant or tolerant ash trees to show this feature, so as to make a breeding programme possible.Deadwood is an essential resource for saproxylic organisms

Breeding for resistance/tolerance Make use of the knowledge of common ash genetic diversity to start a breeding programme for resistance/tolerance to thepathogen that will preserve the existing genetic diversity of the host

Inoculum reduction around ancientash trees

Removing ash leaves in autumn around solitary ancient ash trees may help reduce inoculum and thus preserve this importantheritage

M. Pautasso et al. / Biological Conservation 158 (2013) 37–49 45

result in complete tree mortality, a slow recovery of the speciesmay still be possible (Fig. 4). Given the key role that local humanpopulations will have in managing this emerging disease, more ef-fort should be made in disseminating the rapidly increasingamount of research results on H. pseudoalbidus, so that the public,foresters and other stakeholders can base their management deci-sions also on reliable information rather than on emotional re-sponses only (Schraml and Volz, 2009; Gibon et al., 2010; Knightet al., 2011; Carroll, 2011; Mills et al., 2011; Table 1).

Acknowledgements

Many thanks to M. Garbelotto, A. Gross, M. Jeger, L. Paul and J.Webber for insights and discussions, to F. Graf, T. Kowalski and P.Niemz for providing information, to T. Matoni, R. Pakeman andanonymous reviewers for helpful comments on a previous draftand to the French Foundation for Research on Biodiversity (FRB)and the Centre de Synthèse et d’Analyse sur la Biodiversité (CESAB)for supporting this work.

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