Biological Flora of the British Isles: Fraxinus Excelsior

Journal of Ecology doi: 10.1111/1365-2745.12566

BIOLOGICAL FLORA OF THE BRITISH ISLES* No. 281

List Vasc. Pl. Br. Isles (1992) no. 123, 2, 1 Biological Flora of the British Isles: Fraxinus excelsior

Peter A. Thomas*,† School of Life Sciences, Keele University, Staffordshire ST5 5BG, UK

Summary 1. This account presents information on all aspects of the biology of Fraxinus excelsior L. (Ash) that are relevant to understanding its ecological characteristics and behaviour. The main topics are presented within the standard framework of the Biological Flora of the British Isles: distribution, habitat, communities, responses to biotic factors, responses to environment, structure and physiology, phenology, floral and seed characters, herbivores and disease, history, and conservation. 2. Fraxinus excelsior is a large forest tree, native throughout the main islands of Britain and much of mainland Europe. Seedlings are shade tolerant, but adults are not so it tends to be an intermediate successional species, invading gaps in mixed stands rather than forming extensive pure stands. Ash grows on a wide range of soils but is commonest on nutrient-rich soils with a high base status and pH > 4.2, and is at its best on dry calcareous screes and fertile alluvial soils. 3. Fraxinus excelsior is trioecious or subdioecious with male, hermaphrodite and female flowers and trees. Seed production is prolific with periodic higher producing mast years. Seeds are primarily wind-dispersed, but they can float and be moved considerable distances along waterways. Germina- tion is delayed by dormancy until usually the second spring after being shed. 4. Ash is tolerant of drought, but intolerant of spring frosts and so is predicted to fare well under current climate change scenarios, and indeed has recently been expanding in range in Europe. How- ever, ash health and survival is currently seriously compromised by ash dieback caused by the fungus Hymenoscyphus fraxineus (Chalara fraxinea) that has the potential to kill all but a very few resistant trees. Moreover, the emerald ash borer beetle Agrilus planipennis, a serious pest of ash species in N. America, has reached Europe (though not yet the British Isles) and poses an equally if not more serious long-term threat to ash. Key-words: ash dieback, climatic limitation, communities, conservation, ecophysiology, emerald ash borer, geographical and altitudinal distribution, germination, mycorrhiza, reproductive biology, soils

Ash. Oleaceae. Fraxinus excelsior L. (F. coriariifolia Schee- and female trees (Wallander 2001; Tal 2006). Flowers in leis) is a deciduous tree with a narrow crown, 12–18 m tall short axillary panicles of > 100 flowers, opening before the and exceptionally reaching 43 m, often reduced to a shrub in leaves, purplish, devoid of perianth. Hermaphrodite flowers exposed positions. Bark grey, smooth in young trees, fur- consist of one ovary and two inferior purple stamens: protog- rowed in mature trees. Buds black, terminal 5–10 mm long. ynous and self-fertile (Morand-Prieur et al. 2003; FRAXI- Leaves opposite, although one leaf of a pair may be displaced GEN 2005). In male flowers, ovary abortive; in female vertically by up to 16 mm or, more rarely, can be missing flowers, anthers abortive or rudimentary. Syncarpous ovary (Boodle 1915), to 30 cm long, pinnate, typically < 5000 mm2 contains four ovules but usually only one (rarely two) is fer- (Grime, Hodgson & Hunt 2007) with up to thirteen sessile, tilized. Fruit a samara about 3–4 cm long, pale brown when opposite leaflets, glabrous or nearly so, exstipulate. Leaflets ripe. usually c. 7 cm, lanceolate to ovate, apiculate to acuminate, Fraxinus is a circumpolar genus of the Northern Hemisphere serrate. Trioecious or subdioecious with male, hermaphrodite with 43 species (Wallander 2008) that are unreliably separable

*Nomenclature of vascular plants follows Stace (2010) and, for non-British species, Flora Europaea. This account supersedes that by Wardle (1961). †Correspondence author. E-mail: [email protected]

© 2016 The Authors. Journal of Ecology © 2016 British Ecological Society 2 P. A. Thomas even by chloroplast DNA barcoding protocols (Arca et al. I. Geographical and altitudinal distribution 2012). Fraxinus excelsior and F. angustifolia are native to Eur- ope. Fraxinus excelsior ssp. coriariifolia, distinguished only by Native throughout most of the British Isles, including the its variably pubescent shoots and leaves, found in Romania, north-west of Scotland (Fig. 1). It is absent on the smaller Turkey, Caucasus and northern Iran, has been recognized by islands of the north and west, and is not considered to be Yaltirik (1978) and others. Fraxinus excelsior var. diversifolia native on the Hebrides, Orkney or Shetland (Wardle 1961) Aiton has variably deeply serrate or incised leaves, seemingly nor the Isles of Scilly (Rackham 2014). occurring naturally through the range of F. excelsior (Hatch Fraxinus excelsior is native throughout mainland Europe 2007). Fraxinus excelsior ssp. oxycarpa (M. Bieb. ex Willd.) (Fig. 2), occurring in 64% of European territories (Grime, Wesm. (F. excelsior ssp. excelsior var. oxycarpa (M. Bieb. ex Hodgson & Hunt 2007), and its natural range largely coincides Willd.) Fiori & Paol.) is now considered to belong to F. angus- with that of Quercus robur. Ash natively reaches its most tifolia and is recognized as ssp. oxycarpa. Hatch (2007) lists a northern point of 63° 40’ N in Norway and 61° N on the Baltic bewildering number of cultivars. coast. It extends eastwards to the Volga River basin in western Fraxinus excelsior is common on soils with high base sta- Russia (Wallander 2008). In southern Europe, F. excelsior is tus, and often dominant or nearly so on calcareous soils. In replaced in the most Mediterranean climates by F. angustifolia. Great Britain, ash is the second most abundant tree species in In Spain, ash extends into the northern mountains but is absent small woodland patches (< 0.5 ha) after the native Quercus from central and southern parts of the Iberian Peninsula and N. spp. (Maskell et al. 2013) and the third most abundant in Africa. It is also absent from Iceland. large areas of high forest (Forestry Commission 2003). There are estimated to be 2.2 million individual ash trees outside of II. Habitat woodland in Great Britain, most in England (1.8 million) sur- passed only by native oaks. Most ash trees tend to be small (A) CLIMATIC AND TOPOGRAPHICAL LIMITATIONS (>40% between 21 and 50 cm DBH); there are very few veteran ash trees (Maskell et al. 2013) although some coppiced The northern limit of ash coincides with January isotherms of ash stools can reach a great age. 0 °C (Dobrowolska et al. 2011) due to its susceptibility to

Fig. 1. The distribution of Fraxinus excelsior in the British Isles. Each dot represents at least one record in a 10 km square of the National Grid. (●) native 1970 onwards; (s) native pre-1970; (+) non-native 1970 onwards; (x) non-native pre-1970. Mapped by Colin Harrower, Biological Records Centre, Centre for Ecology and Hydrology, mainly from records collected by members of the Botanical Society of the British Isles, using Dr A. Morton’s DMAP software.

24° 0° 24° 48° 72° 58°

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Fig. 2. The distribution of Fraxinus excelsior in Europe. Redrawn from Wardle (1961) and Weissen et al. (1991), taken from Marigo 500 km et al. (2000). late spring frosts and the cold, short growing season. Kollas, south-facing slopes. In unshaded habitats, the species was Korner€ & Randin (2013) recorded a mean growing season recorded as slightly more frequent on north-facing slopes temperature of 13.0 °C and a minimum growing season of (Grime, Hodgson & Hunt 2007). 192 days with a minimum of 1614 annual growing degree- Ash is generally a lowland species in Britain, reaching < days (accumulated mean daily temperatures > 5 °C) at the 275 m in Co. Leitrim and Co. Sligo, Ireland (Barrington & northern limit of ash in Sweden (57–59 °N). Usually, how- Vowell 1884–1888), 450 m on limestone in mid-Wales and the ever, if the period of spring frosts is removed when growth is Black Mountains of South Wales (Wardle 1961; Kerr 1995) minimal, the growing degree-days fall to a subsequent mini- with a maximum altitude of 585 m in Britain (Grime, Hodgson mum of 1100 day °C (Sykes, Prentice & Cramer 1996). & Hunt 2007), descending to around 300 m as Rassal Ash- Below this, ash is not competitive. wood, Wester Rodd, the most northerly ash woodland in Bri- Kollas, Korner€ & Randin (2013) compared growing condi- tain (Michael Proctor, personal communication), generally tions at the northern end of its range with those of ash at its ascending higher than Quercus spp. but lower than Fagus syl- highest occurrence in the western and eastern Swiss Alps vatica (Kerr 1995). Its greatest altitude is in Central Europe, (1165–2160 m). They found that ash at altitude needed a reaching 1650 m in the Swiss Alps and Pyrenees (Besnard & longer growing season than at its northern limit (201–214 Carlier 1990), 1750 m in the French Alps (Carcaillet & Brun compared to 192 days) but coped with a lower mean growing 2000) and 2200 m in northern Iran (FRAXIGEN 2005). season temperature (10.9–11.2 °C compared to 13.0 °C) and fewer growing degree-days (1250–1403 compared to 1614). (B) SUBSTRATUM Spring temperatures appear to be the primarily limiting factor with altitude. Lenz et al. (2013) found that the distribution Ash grows on a wide range of soils, particularly those under- and phenology of eight of the deciduous tree species investi- lain by calcareous rocks such as chalk, oolite, limestone and, gated just below the treeline in the Swiss Alps, including ash, in England and Wales, Old Red sandstone (Wardle 1961). In matched most closely to spring temperatures rather than mini- the British Isles and other western parts of its range, ash is mum winter or summer temperatures between 1931 and 2011. abundant both on shallow dry calcareous soils and also on At the eastern edge of its natural range, winter temperatures moist, well-drained and fertile alluvial soils (Marigo et al. are not crucial since due to winter hardening ash can survive 2000; Dufour & Piegay 2008). Calcareous soils include those temperatures as low as À27 °C (Till 1956); the limits to over marl, limestone and bare chalk (Locket 1946; Weber- growth in the east and south are undoubtedly due to hot sum- Blaschke et al. 2008) including active scree to almost vertical mers and moisture deﬁcit. limestone outcrops (Merton 1970) since seedlings are able to Ash can grow on slopes up to 80°, although Grime, Hodg- recover from damage and burial (Wardle 1959); on less son & Hunt (2007) record it as marginally more common mobile sites, ash may be accompanied by hazel which it soon between 20 and 40°. In shaded areas, young trees are frequent overtops. Ash tends to colonize the more stable larger scree on both northern and southern slopes but only abundant on at the bottom of slopes ﬁrst and then progress uphill. Its pref-

© 2016 The Authors. Journal of Ecology © 2016 British Ecological Society, Journal of Ecology 4 P. A. Thomas erence for fertile soils is reflected in its requirement in main- the north-west by Fraxinus excelsior–Sorbus aucuparia– land Europe for soils with a base saturation of >20–30% Mercurialis perennis woodland (W9). In the lowland Fraxi- (>50% is optimal for young ash) and a C:N ratio of <15–20 nus–Acer–Mercurialis woodland, ash, Acer campestre and (Weber & Bahr 2000b; Pinto & Gegout 2005; Walthert, Pan- Corylus avellana are diagnostic species and, to a lesser natier & Meier 2013). Indicators for good ash soils are Mer- extent, oak (Quercus robur in the SE) on heavier soils and curialis perennis, Allium ursinum, Urtica dioica, Circaea locally abundant patches of Tilia cordata or Carpinus betulus. lutetiana, Festuca rubra, Arrhenatherum elatius, Dactylis Almost pure ash woods are common on chalk in the south- glomerata and Poa trivialis (Popert 1950a; Grime, Hodgson east, particularly the South Downs (Wardle 1961). The shrub & Hunt 2007). layer is typified by Crataegus monogyna in the north-west, Ash grows best on moist soils where the winter water-table being replaced by C. laevigata in the south-east. The field is between 40 and 100 cm below the surface (Kerr & Cahalan layer tends to be very variable, particularly because many 2004), but it will grow well on wet, periodically inundated stands of this woodland type have been coppiced in the past, soils along brooks and springs (Diekmann 1996) providing resulting in an unnaturally high abundance of understorey there is a shallow layer of seasonally well-drained soil for species. Nevertheless, the field layer is typified through the establishment (Wardle 1961). Ash is thus absent from solige- range of this community by the presence of Mercurialis nous or topogenous mires. Ash is less common on brown perennis and, at least in the drier subcommunities, a high earths, calcareous mulls (Merton 1970) and compacted soils abundance of Hyacinthoides non-scripta and, to a lesser (Popert 1950b) including alluvial areas that have compact extent, Circaea lutetiana, Geum urbanum and Viola spp. In gravel layers that the roots cannot penetrate. Its occurrence on the south-east and up into the east Midlands and East Anglia, such soils is often due to planting or other management aid- these woodlands are dominated by the Primula vulgaris–Gle- ing its survival (Dobrowolska et al. 2011). choma hederacea subcommunity. However, slight increases Fraxinus excelsior is usually absent on acidic soils where in surface gleying due to soil clay content, slope changes or the pH of the surface soil is lower than 4.2 (Puri 1948; War- soil compaction, lead to the Anemone nemorosa and then the dle 1959, 1961), and Pearsall (1938) noted ash dying at pH more open Deschampsia cespitosa subcommunities, often 3.8. Juveniles tend to be most abundant between pH 6.0 and with all three subcommunities forming a local mosaic. The 8.0 (Grime, Hodgson & Hunt 2007). The upper limit is species-poor Hedera helix subcommunity is more typical of recorded by Puri (1950a,b) as pH 8-9. Ash may, however, be highly humid conditions created by neglected coppice or present in acidic areas, including lead mine spoil (Grime, dense plantations and in the more oceanic south-west. To the Hodgson & Hunt 2007), where the soil has been sufficiently north-west, the Geranium robertianum subcommunity enriched in bases by percolating water or soil mixing. Young becomes commonest, particularly on rendzina soils on steep soils on acidic rock, such as those in rock crevices or semi- slopes, typified by its occurrence on the limestone scree of consolidated scree slopes, may also support ash (Wardle Yorkshire and the Derbyshire Dales. The canopy can be 1961). almost pure ash, sometimes associated with a higher frequency of Ulmus glabra and Acer pseudoplatanus. Lack of water and instability of the scree lead to an impoverished field III. Communities layer dominated by G. robertianum and isolated tussocks of Fraxinus excelsior is an important street tree in a variety of Arrhenatherum elatius (Wardle 1961). On steeper slopes with cities in the Northern and Southern Hemispheres (Davies downwash leading to deep, moist, free-draining colluvium, et al. 2007; Sjoman,€ Ostberg€ & Buhler€ 2012; Breuste 2013). this is replaced by the Allium ursinum subcommunity. In Ash also has a long history as a hedgerow tree in France, the older, less disturbed woodlands, the rare Teucrium scorodonia British Isles (Rackham 1995) and up into southern Sweden subcommunity is typically found in the Wye Valley and Der- (Sarlov€ Herlin & Fry 2000). In Great Britain, ash was byshire. recorded as the most common ‘standard’ hedgerow tree spe- The upland ash woodland, Fraxinus–Sorbus–Mercurialis,is cies, closely followed by Quercus spp.; both were almost an still dominated by F. excelsior and Corylus avellana but with order of magnitude more abundant than the next most com- less of a continental influence and so Tilia spp. and Acer mon species Acer pseudoplatanus (Maskell et al. 2013). It campestre are replaced by Betula pubescens and, particularly was estimated that the length of woody linear features (hedge- in the north, Sorbus aucuparia (Jackson & Sheldon 1949; rows and lines of trees) composed of ash in Great Britain was Gordon 1964). This community is characteristic of constantly 98 900 km with most of this (86 100 km) found in England moist base-rich brown soils of valley heads in the upland (Maskell et al. 2013). Ash is also frequently found as an fringes with cool (mean annual maximum temperature important pioneer species along stone and earth walls, railway <26 °C), moist (annual precipitation >1200 mm) conditions embankments and cuttings on base-rich soil (Rishbeth 1948; (Rodwell 1991) and is thus commonest on the Carboniferous Wardle 1961; Pollard 1973; Shimwell 1999). Limestone of the Pennines across into the Burren of County Ash forms two major woodland types in the British Isles. Clare (Foot 1871; Braun-Blanquet & Tuxen 1952; Ivimey- Base-rich soils of lowland Britain are dominated by Fraxinus Cook & Proctor 1966), including in the grikes of limestone excelsior–Acer campestre–Mercurialis perennis (W8; Rodwell pavement. It also occurs on the Jurassic limestones of 1991) that is replaced in the cooler and wetter conditions of the North York Moors and on the Cambrian and Jurassic

© 2016 The Authors. Journal of Ecology © 2016 British Ecological Society, Journal of Ecology Fraxinus excelsior 5 limestones on Skye. This community thus varies from high petraea–Betula pubescens–Dicranum majus woodland (W17) forest in more sheltered areas, with occasional Ulmus glabra but is usually restricted to areas of nutrient- or base-enriched and Acer pseudoplatanus, through to scrub of C. avellana, soil. B. pubescens and S. aucuparia with scattered emergent ash On very wet, base-rich soils, Fraxinus excelsior is com- on upland sites or those with thin soils. The field layer mon, though not abundant, in moderately eutrophic fen peat tends to be similar in composition to its southern counter- carr supporting Alnus glutinosa–Carex paniculata woodland part. Undoubtedly, this community was formerly much more (W5), particularly in the drier Phragmites australis and Lysi- common in cool oceanic areas now converted to agricultural machia vulgaris subcommunities. Growth of ash is often poor use. North of the Midlands, the two ash woodland types but greatly improved with drainage (Kassas 1951). Ash is less interdigitate with the Fraxinus–Acer–Mercurialis on drier frequent in the closely related Salix cinerea–Betula and warmer lower reaches of valleys and the Fraxinus–Sor- pubescens–Phragmites australis woodland (W2) undoubtedly bus–Mercurialis in damper, higher altitude areas. Upland due to the absence of the large C. paniculata tussocks that, in ash woodlands tend to be fairly uniform in composition the Alnus–Carex carr, provide drier establishment niches for although in areas where grazing is restricted, especially ash and other trees. With the build-up of peat, this woodland where water is abundant, the typical subcommunity gives type is invaded by alder to create eutrophic Alnus glutinosa– way to the more-open, species-rich Crepis paludosa sub- Urtica dioica woodland (W6), and ash does become more fre- community. quent but is still uncommon and much less so than in the Ash woodlands abut a number of other woodland types. more base-rich Alnus–Fraxinus–Lysimachia woodland. Ash is In the lowlands, on the driest, most base-rich soils, Fagus also present but extremely uncommon in the moderately sylvatica and, to a degree, Taxus baccata become important acidic conditions of Betula pubescens–Molinia caerulea competitors and the ash woodlands can be regarded as seral woodland (W4) and then only on the drier Dryopteris stages towards Taxus baccata (W13) or Fagus sylvatica– dilatata–Rubus fruticosus and Juncus effusus subcommunities. Mercurialis perennis (W12) woodland. In Taxus woodland, Ash saplings are also a component of a number of scrub ash persists only as an occasional canopy tree in the Mercu- types on lowland base-rich soil. It is the commonest large rialis subcommunity. Ash is more abundant in the Fagus– woodland tree found in the lowland Crataegus monogyna– Mercurialis woodland, especially in the moister Mercurialis Hedera helix scrub (W21). On deeper, neutral soils, and thus perennis subcommunity, where it persists as a frequent inva- often on abandoned agricultural and urban land, ash saplings der of gaps. Not surprisingly, on the less base-rich soils of can be a rare component of Rubus fruticosus–Holcus lanatus Fagus sylvatica–Rubus fruticosus woodland (W14), ash is (W24) that can be seral to base-poor Fagus–Rubus and Quer- only present as very occasional canopy trees that may be cus–Pteridium–Rubus woodlands, or on base-rich soils, Fraxi- the survivors of woodland invaded by beech. However, Watt nus–Acer–Mercurialis woodland. Moderately acidic soils (1925) also suggests that the heavy shade of beech allows supporting Pteridium aquilinum–Rubus fruticosus underscrub ash to establish in the absence of competition with herba- (W25), often seral to Quercus–Pteridium–Rubus woodland, ceous vegetation, and these seedlings readily grow into gaps may also contain very occasional saplings of ash. when released. As Wardle (1961) noted, F. excelsior occupies similar habi- On less base-rich soils, tending towards brown earths, oak tats in mainland Europe to those found in the British Isles, increases in dominance leading to Quercus robur–Pteridium but pure ash woodlands are less common. Communities simi- aquilinum–Rubus fruticosus woodland (W10). Here, ash nor- lar to Fraxinus–Acer–Mercurialis and Fraxinus–Sorbus–Mer- mally has only an occasional presence but can be locally curialis are found as Tilio-Acerion forests of slopes, screes abundant on fairly acidic but fertile soils such as in East and ravines across Europe, in particular the south-west, pri- Anglia. However, in the Acer pseudoplatanus–Oxalis ace- marily on calcareous rocks, including limestone pavement, tosella subcommunity of the wetter north-west, ash can be as but also siliceous rocks (Natura 2000 codes 9180 and 8240; frequent as in Fraxinus–Acer–Mercurialis woodland but in Commission of the European Communities 2007). Dominant lower abundance. On the wettest, moderately base-rich sites, species are ash, Acer pseudoplatanus, Ulmus glabra and Tilia especially on flushes and springs, Fraxinus–Acer–Mercurialis cordata. Ash woods are, however, rare since past manage- is invaded by alder leading to Alnus glutinosa–Fraxinus ment has tended to favour trees such as Fagus sylvatica and excelsior–Lysimachia nemorum woodland (W7) although ash conifers (Angiolini, Foggi & Viciani 2012). can remain common in the canopy. Dictated by soil moisture, As in the UK, ash is also found in European beech forests the ash, oak and alder woodlands can form a small-scale on calcareous substrates, particularly around the Baltic, classi- mosaic on the landscape. The analogous zonations in the fied as Fagus sylvatica–Fraxinus excelsior–Stachys sylvatica north are Fraxinus–Sorbus–Mercurialis, Quercus petraea– (Diekmann et al. 1999) and in Carpathian beech forests, Den- Betula pubescens–Oxalis acetosella (W11) and Alnus–Fraxi- tario glandulosae-Fagetum (Jezdrzejczak 2013). Ash is gener- nus–Lysimachia woodlands, though due to the colder ally uncommon in these forests, mixed with Acer conditions ash is only an occasional presence in the Quercus- pseudoplatanus, Prunus avium and Ulmus glabra either as Betula-Oxalis woodland and much rarer than in the southern canopy or subcanopy trees. These communities extend up into Quercus–Pteridium–Rubus woodland. On acidic soils in the mountainous areas with calcareous rocks such as Lonicero north-west, ash is found as a very occasional tree in Quercus alpinenae-Fagetum dominated by beech with ash and Acer

© 2016 The Authors. Journal of Ecology © 2016 British Ecological Society, Journal of Ecology 6 P. A. Thomas pseudoplatanus as co-dominants. Here, ash readily regener- seed sowing (Jinks, Willoughby & Baker 2006) removing ates on open avalanche slides (Fischer, Fischer & Lehnert field layer competition (seedling emergence was 87-92% 2012). On mesotrophic soils, ash is found in the Fagus syl- with herbicide compared to 56% in the control). The effect vatica–Corylus avellana–Galium odoratum community (Diek- of the field layer is species specific. Herbs such as Mercuri- mann et al. 1999), similar to the eastern beechwoods but with alis perennis may prevent ash establishment (Wardle 1959) the addition of Quercus robur and Q. petraea. On deeper even though the light level below can still be c. 33% of full more acidic soils, ash is a component of oak woodlands such sunlight (Gardner 1976). On moist sites, this may be caused as the Quercion robori–petraeae community, as well as forests by damping-off destroying most seedlings within a month of of the Quercetalia pubescenti–petraeae order on coastal dunes their germination (Wardle 1961). On dry sites, those seed- (2180; Commission of the European Communities 2007). lings that survive attacks by predators and parasites during In the Boreo-nemoral zone of Scandinavia, ash is found in their first summer may fail to survive the winter. However, a number of open mesotrophic mixed deciduous forests, once above the field layer, survival can be high. Harmer, including the Quercus robur–Fraxinus excelsior community, Boswell & Robertson (2005) showed that while Rubus spp. and the eutrophic elm-ash communities of Ulmus glabra– may reduce seedling density for 2–3 years, the rapid growth Fraxinus excelsior and Ulmus minor–Fraxinus excelsior of ash in partial shade meant that they were soon clear of where ash tends to be a pioneer (Diekmann 1994). Ash is light competition. found at very low frequency (3%) in the wet lowland Picea Grass species can be particularly problematic for establish- abies forests of north-eastern Europe, but dominating with ment and subsequent growth; seedlings become established Alnus glutinosa and P. abies on eutrophic peat in the commu- only where there are breaks in the sward (Wardle 1961). Bed- nities of Carici elongatae-Alnetum and Carici remotae-Fraxi- ford & Pickering (1919) found annual height growth of sap- netum (Prieditis 1999). lings was increased by 51% when grass was removed. Bloor, Ash is also found in alluvial and riparian forests, such as Leadley & Barthes (2008) found that below-ground competi- eutrophic alder-ash forests of northern Europe (Fraxinus tion was more important than above-ground competition excelsior–Prunus padus and Fraxinus excelsior–Alnus gluti- between ash seedlings and Dactylis glomerata under glass- nosa communities) where ash tends to be a dominant (Diek- house conditions. While shoot competition alone did not mann 1994) and on the eutrophic floodplains of south-east affect seedling growth, root competition reduced the mass of Europe in Ulmo laevis–Fraxinetum oxycarpae (Brullo & seedlings by 58% and height of ash by c. 35% in the first Spampinato 1999). 19 weeks after germination (Bloor, Barthes & Leadley 2008). In arid parts of south-east Europe with shallow calcareous Added N (100 kg N haÀ1 yearÀ1) increased the effectiveness soils, ash and Tilia platyphyllos are an infrequent but some- of Dactylis competition on ash, reducing the biomass of ash times abundant component of xerophytic oak woodlands seedlings by 80% compared to the control (Bloor, Barthes & around the Pannonian basin dominated by Quercus pubescens Leadley 2008). In the absence of root competition, seedlings (91H0; Commission of the European Communities 2007). showed a significant increase in biomass allocation to leaves. Perhaps surprisingly, reducing competition by using herbicide to clear 1 m diameter circles had no effect on any of the trees IV. Response to biotic factors used by Harmer (2001). Ash coppices strongly after felling. Ash is also a prolific Ash seedlings >30 cm tall below the field layer cover may seed former, and its seedlings occur wherever the field layer persist for several years under the shade of 50% canopy cover is reduced in density, whether by overhead shade or by dry- and under severe browsing (Harmer 2001), but in the Der- ness, excessive wetness or instability of the soil (Wardle byshire Dales, all were dead within 3 years of germination 1961). Seedlings and juveniles of ash are shade tolerant and (Gardner 1976). However, once above the field layer, saplings can establish successfully down to c. 2% full sunlight (Gat- may live for many years forming an effective seedling bank. In suk et al. 1980; Marigo et al. 2000). However, the shade Lathkill Dale ash saplings survived for 21–22 (28 maximum) cast by vernal field layer plants is crucial to survival. In years below the ash canopy (Gardner 1976). Mortality was Swedish deciduous woodlands, Tapper (1992a) noted that in highest in the first 2 years and then age independent (Tapper plots where the field layer was classified as ‘dense’, ‘sparse’ 1992a); Harmer, Boswell & Robertson (2005) observed 40– and ‘removed’, the survival of seedlings after 9 years was 50% mortality per year regardless of size. Moderate shading 13.3%, 29.2% and 42.6%, respectively. Height growth per may initially increase seedling growth by reducing competition year was lowest in the dense plots but did not significantly (Helliwell & Harrison 1979) but as saplings become more light differ in the other two (dense 3.9 Æ 2.6 cm (SD), sparse demanding when >50 cm tall (Tapper 1996a), effective 8.2 Æ 5.3 cm, removed 7.5 Æ 5.2 cm). He observed up to increase in height is possible only under conditions approach- 1120 seedlings mÀ2 and this in itself affected survival; in ing full sunlight (Harmer, Kiewitt & Morgan 2012) and young plots with field layer cover, seedlings within 1.5 cm of trees can become increasingly etiolated (Rust & Savill 2000). another survived less well (although there was no difference Wardle (1959) noted that a ‘typical shaded seedling’ was only in the open ‘removed’ plots where light levels were higher). 29.6 cm tall after 14 years, with no branches and so little wood Similarly, establishment in southern England was higher that the stems were prone to break. When gaps appear, ash when competitors were killed by herbicide within 5 days of from the seedling bank can quickly grow into even small gaps

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4 0 0 005 10 15(m) 204 5 10 15 (m) 20

Fig. 3. Profile diagram showing an early successional stage of an Alnus glutinosa–Fraxinus excelsior woodland on the island of Asmansboda in the outer archipelago of Stockholm, Sweden, in 1984 (left) and 1991 (right). All individuals >7 m height are included. Unshaded trees are A. glutinosa and shaded are F. excelsior. The diagram shows a vertical cross section of the tree crowns and the position of their stems (0–4m from the profile). Stems with a broken line denote that major parts of the crown are located outside the profile. From Tapper (1996a).

(Fig. 3) readily competing with other broadleaved trees (Tap- hares and moose) in southern Sweden: Quercus robur (85% of per 1996a). In larger gaps, large numbers of hitherto stagnating plants browsed) > Alnus glutinosa > Fagus sylvatica > Tilia seedlings are released. The density of such thickets is eventu- cordata > Prunus avium > Betula pendula > Picea abies > ally reduced by intraspecific competition. Fraxinus excelsior (16% of plants browsed). However, a num- As saplings develop, they rapidly lose their tolerance of ber of other studies have shown ash to be highly susceptible shade and require light levels near full sunlight to grow well. to browsing (Eiberle & Bucher 1989; Gill & Beardall 2001; This difference with age is undoubtedly the reason for the dif- Pepin et al. 2006; McEvoy & McAdam 2008) and to prefer- fering opinion as to degree of shade tolerance of adult ash trees, entially establish within clumps of spiny plants such as some suggesting that ash is as shade tolerant as Quercus spp. Crataegus monogyna (Merton 1970; Grime, Hodgson & (Prentice & Helmisaari 1991) and others that ash is more shade Hunt 2007). As an example, Kullberg & Bergstrom€ (2001) tolerant than Quercus and Acer pseudoplatanus (Ellenberg noted that B. pendula and F. sylvatica were preferred over et al. 1991; Kerr 1995). A number of studies considering ash, while other studies found little browsing on B. pendula mature trees have shown that shade tolerance increases in the (Mysterud, Lian & Hjermann 1999; Bergqvist, Bergstrom€ & following order: Betula pendula < Populus tremula < F. ex- Wallgren 2012) or F. sylvatica (Modry, Hubeny & Rejsek celsior < Tilia cordata = Corylus avellana (Niinemets, Kull & 2004; Gotmark€ et al. 2005) despite all being conducted in Tenhunen 1998; Niinemets & Kull 1999). Scandinavia. Part of this variability is due to how damage Fraxinus excelsior acts as both a pioneer (Halden 1928; is recorded in the different studies since F. sylvatica tended Wardle 1959) with a strong ability to colonize but also as a to lose the leader and one or more laterals, while B. pen- competitor/stress-tolerant competitor (Grime, Hodgson & dula and ash had only lateral branches removed (Kullberg Hunt 2007) able to survive as a permanent forest component. & Bergstrom€ 2001). It is also apparent that browsed seed- The competitiveness of ash against other broadleaved tree lings are often the tallest (Price 1991) and herbivory varies species results from its ability to produce a high density of between seasons; in a study in the UK (McEvoy & McA- seedlings, its rapid growth with very low branch order and its dam 2008), ash was undamaged during February, but lateral high water use efficiency and drought resistance (Rysavy branches were significantly damaged in the following Octo- 1991; Marigo et al. 2000; Rust & Savill 2000). No allelopa- ber. Also important is the susceptibility of individuals to thy or chemical substances from ash leaves have been noted. herbivory. In France, it has been seen that ash trees vary in There is some evidence from southern Sweden that planting the palatability of the bark to the vole Microtus arvalis, ash with a nurse crop of Alnus glutinosa, Betula pendula or possibly related to differences in the concentration of cou- Larix x eurolepis at a total density of 4139 seedlings haÀ1 marin derivatives in the bark (Moraal & Goedhart 1997). was detrimental to ash, it having the lowest survival over Similarly, the bark-sucking insect, Pseudochermes fraxini 10 years (2% compared to 79% in Quercus robur) and the (Kaltenbach) (Hemiptera, Eriococcidae), also responded dif- shortest saplings (0.6 m compared to 3.1 m in Q. robur). ferentially. However, the authors (Lof€ et al. 2014) found evidence of ash Rabbits, hares and sheep attack young plants, although dieback that probably contributed to the poor performance. again they appear less susceptible than other broadleaved Kerr (2003) found little evidence of intraspecific competition trees such as F. sylvatica (Hulden 1941; Bourne 1945; Mer- in monoculture plantations. ton 1970; Gardner 1976). In a variety of grasslands and grazed pastures, while high-intensity grazing reduces establishment (Hester, Mitchell & Kirby 1996; Mottet et al. 2007), Browsing low intensity of grazing may facilitate ash invasion by reduc- Kullberg & Bergstrom€ (2001) give the following order of most ing competition but leaving some areas ungrazed providing to least browsed species by herbivores (particularly roe deer, regeneration niches for ash (Marie-Pierre, Didier & Gerard

2006; Van Uytvanck, Milotic & Hoffmann 2010). Hester, V. Response to environment Mitchell & Kirby (1996) found recruitment of ash into sheep- grazed grassland in Cumbria was greatest in low grazing (A) GREGARIOUSNESS intensity plots (0.6–1.2 sheep haÀ1). Many ash woodlands in Britain arose following reduced grazing in the mid-19th cen- Occasionally as scattered trees, but often in clumps, and tury and after myxomatosis in the mid-1950s (Merton 1970). sometimes ash may form nearly pure stands (Wardle 1961). Complete defoliation of 2-week-old ash seedlings up to 80 days after the cessation of stem elongation resulted in a (B) PERFORMANCE IN VARIOUS HABITATS second flush of growth from the terminal buds (Collin, Badot & Millet 1994; Collin et al. 2000). By contrast, partial defoli- Fraxinus excelsior grows fastest and attains its largest dimen- ation (up to 75%) maintained some apical control and led sions on sites that are fertile and moist but well drained with instead to the release of basal axillary buds. the winter water-table 40–100 cm below the surface (Kerr & Browsing of young ash seedlings results in lower survival Cahalan 2004). In mainland Europe, this can be of sufficiently and growth. Simulated browsing by clipping of seedlings high density and vitality that ash can be considered invasive (originally 30–40 cm tall) twice per year (June and August) leading to ‘fraxinization’ where ash takes over from other over 5 years in southern England reduced height growth competitive species (see FRAXIGEN 2005 and Dobrowolska proportionately more in ash (compared to unclipped plants) et al. 2011 for references). Exposure to strong winds and soil than in F. sylvatica, Q. robur or Acer pseudoplatanus. Stem dryness or compaction reduces the rate of height and diameter diameter growth in ash after 5 years was reduced to 43– growth and the ultimate size of the tree (Wardle 1961), but 35% of the controls (depending upon site). Survival was ash is comparatively wind firm compared to competitor trees reduced from c. 95% in controls to c.58–80% in clipped (Rackham 2014). Under extreme conditions, it remains a ash plants (estimated from a figure), similar to A. pseudo- shrub. Good stands of ash occur over the pH range of 5–8 platanus, while Q. robur and F. sylvatica were unaffected. (Wardle 1961) and it performs poorly on acidic sites. When Similar results have been reported by Eiberle (1975, 1979) grown on acidic sand, seedling establishment is low, and in and McEvoy & McAdam (2008). Conversely, the survival southern Sweden under a canopy of Picea abies partial felling and height growth of ash saplings appears to be less of the spruce did not improve height or diameter growth of affected by grazing and browsing due to biomass loss being newly planted ash seedlings unlike in Fagus sylvatica, Quer- largely restricted to the lateral branches (Diekmann 1994; cus robur and Tilia cordata. Mortality was also significantly Kullberg & Bergstrom€ 2001), and the ability, as noted higher in ash. Ash will sometimes establish on sites with above, for ash to produce new flushes of leaves on heavily compacted clay or very dry soils over chalk, but the seedlings À grazed plots (2.1–3.8 sheep ha 1 – Hester, Mitchell & generally do poorly and do not survive beyond 3–4 years Kirby 1996). (Tabari, Lust & Neirynk 1998). Ashalsoappearstobefairlyimmunetoinsectherbivory. Ash has the advantage in being an early to intermediate suc- Ruhnke et al. (2009) working in a floodplain forest in central Ger- cessional species such that it can persist in both pioneer and many found that ash had the smallest loss of leaf area to insects mature phases of vegetation development (Tapper 1996a; (56/38 mm2 leafÀ1 in 2002/2003) compared to 106/183 mm2 in Emborg, Christensen & Heilmann-Clausen 2000; Einhorn, Acer pseudoplatanus and 127/61 mm2 in Quercus robur. Rosenqvist & Leverenz 2004). So as well as its important role Seeds of ash appear to be relatively unpalatable and were in secondary woods (Scurfield 1959; Merton 1970), ash is also the least preferred out of 12 broadleaved species used in a a frequent component in the canopy of ancient woodland (Pig- trial in southern England by Jinks, Parratt & Morgan ott 1969). Ash benefits from stand opening and is found in (2012). In deciduous woodlands in north-east England, ash moderately disturbed habitats and relatively unproductive, spe- seeds were the least removed (49%) compared to a loss of cies-poor woodland habitats, but also in more species-rich, 68% in Ulmus glabra and 81% in Taxus baccata (Hulme unshaded sites with >15 other species mÀ2 associated with & Borelli 1999). Ash benefited least if seeds were buried <40% abundance of ash (Grime, Hodgson & Hunt 2007). But 1 cm deep; removal was reduced by 31% in ash compared its mid-successional niche does seem to make it intermediate in to 35% in T. baccata and 65% in U. glabra. Ash seeds its reaction to environmental changes; thinning stands in were seen to have a high phenolic content – 14.55% of dry Lithuania by up to 25–35% of volume resulted in an increase mass compared to 11.43% in Q. robur and 4.52% in F. syl- in crown area of ash of >100%, which was small compared to vatica (Hulme & Borelli 1999)- which is known to reduce c. 200% in pioneer species of Populus tremula and Betula pen- seed palatability to small mammals (Jensen 1985). Although dula/B. pubescens, but larger than c. 80% in later successional less predated, it is likely that post-dispersal seed predators Picea abies (Juodvalkis, Kairiukstis & Vasiliauskas 2005). have little influence on seedling density since ash produces Growth of ash tends to be fastest at the bottom of slopes in such a large number of seedlings compared to its competi- colluvial or alluvial soil enriched by down-wash, possibly due tors such as U. glabra and F. sylvatica (Hulme 1996). War- to higher P levels (indicated by the presence of Urtica dioica) dle (1961) notes that earthworms (Annelida, Oligochaeta) and perhaps to a lesser extent due to constancy of water sup- assisted the survival of seeds by dragging them down into ply in dry years (Merton 1970). Seedling establishment can their burrows. be very high along river valleys (Dufour & Piegay 2008) and

© 2016 The Authors. Journal of Ecology © 2016 British Ecological Society, Journal of Ecology Fraxinus excelsior 9 fastest growth in girth is found in these slope bottom sites or south-east Germany grew the slowest in first four years (reaching up to 3.22 m girth on deep alluvium) and also in and were c.20–25% shorter than UK material. plateau top trees but since these are often beside roads or The leaves of Sorbus aucuparia are known to decompose walls they tend to be much shorter. In neglected coppice on more rapidly than ash, while Acer pseudoplatanus, Betula pen- good sites, ash coppice can be vigorous enough to overtop dula, Castanea sativa and Fagus sylvatica decompose more and kill standard oaks (Rackham 2003). Although it attains its slowly (Sydes & Grime 1981b; Bjørnlund & Christensen 2005; greatest size on fertile soils, ash has its highest densities and Rajapaksha et al. 2013). The low C:N ratio (14–28) and low has its maximum ecological impact on sites that are less lignin content make ash litter readily decomposable (Ruhnke favourable for growth, principally on relatively infertile cal- et al. 2009; Jacob et al. 2010; Holzwarth, Daenner & Flessa careous soils where individuals can be reduced to stunted 2011; Langenbruch, Helfrich & Flessa 2012). Usually by June trees or shrubs (Wardle 1961; Grime, Hodgson & Hunt only petioles (including the rachis) are left which can persist 2007). Such sites are one of the few habitats where ash can for many years, with implications for ash dieback (IX(C)). Lea- form almost pure stands (Halden 1928; Hulden 1941; Wardle chates from fresh ash litter have been stated to strongly inhibit 1959; Jahn 1991). On scree or steep slopes, stems can have a germination and seedling growth of other tree species, most j-shaped base or even be prostrate due to instability on mobile likely due to the high concentrations of minerals released from surfaces and subsequent adventitious rooting along the under- the rapidly decomposing litter (Rajapaksha et al. 2013); Nyk- side of the trunk (Merton 1970). Slowest radial growth is vist (1959) found 22% of air-dried litter mass was leached found on shallow, dry stony ground rather than scree (Ausse- within 24 h. The lack of an effect on ash may give it a competi- nac & Levy 1992; Marigo et al. 2000), reaching a top height tive advantage facilitating the establishment of large cohorts. In after about 20 years and dying when <4–5 m tall (Merton Denmark, soil respiration was highest under ash (2.09 Æ 0.16 1970). On deep, water-retentive soils in Belgium, regeneration (SE, n = 3) lmol mÀ2 sÀ1) compared to that under Quercus of ash has been found to be as dense as 150 000 trees haÀ1, robur, A. pseudoplatanus and F. sylvatica (1.27 Æ 0.09 while on dry, south-facing slopes it can be <12 700 lmol mÀ2 sÀ1 in the latter) and so ash stands had least litter trees haÀ1 (Tabari, Lust & Neirynk 1998). and highest carbon turnover rates in the organic layer (Oostra, Munch€ & Dieterich (1925) identified two forms of ash in Majdi & Olsson 2006; Vesterdal et al. 2012). This was partly Germany: ‘water ash’ on moist, fertile alluvial soils and attributed to the higher soil temperatures (1 °C warmer than the ‘limestone ash’ on thinner, drier limestone soils. Ash from coolest), low leaf area index (3.6 m2 mÀ2) but also higher these habitats have indeed been found to differ in wood prop- earthworm populations. Higher turnover in the organic layer erties (see references in Weiser 1964), water uptake (Carlier, was balanced by higher C stocks in the mineral soil Peltier & Gielly 1992) and flood tolerance (Jaeger et al. (79.5 t haÀ1) (Vesterdal et al. 2008). Somewhat ironically, 2009). They also differ morphologically in that the midribs deeper litter layers appear to benefit ash. Ash seedling biomass and main lateral veins of the former are thickly covered with in their first year in Acer pseudoplatanus and Quercus spp. hairs, compared to being nearly glabrous in the latter (Wardle woodland was positively correlated with the depth of tree litter 1961). However, it is apparent that these are really two ends (tested up to 600 g mÀ2 dry mass), possibly because the litter of a continuous spectrum in which provenance and site fac- hid seeds from predators (Sydes & Grime 1981a). This helps tors play an important role (Kleinschmit et al. 1996). Cundall, explain the abundant regeneration of ash below F. sylvatica Cahalan & Connolly (2003) found significant differences (see Interaction of ash with elm, sycamore and beech below). between British provenances for height after 2 years in a Edmondson et al. (2014) investigated soil organic carbon nursery under optimum conditions, and after 5 years, 60% of beneath long-established trees in urban parks in Leicester with variation in growth was attributed to site, 24% due to prove- mown grass and found that carbon was highest under ash nance and 6.5% by provenance x site interaction. However, (median of 26 kg mÀ2, mainly at 40–100 cm depth) com- the lack of genetic differentiation between populations identi- pared to 19 kg mÀ2 under Acer spp., 14 kg mÀ2 under Quer- fied in VIII(C) can weaken provenance variation depending cus robur and 15 kg mÀ2 under just grass. Enrichment by upon the populations chosen, such that Boshier & Stewart ash can be attributed to its greater root mass than Q. robur (2005), working with reciprocal transplants of seed between and Acer pseudoplatanus (Kerr & Cahalan 2004) and its pref- eight woodlands across the range of ash in England and erence for the clay-rich soils in the parks. Wales, found no geographical pattern in growth performance Ash generally thrives under interspecific competition, but based on origin. Similarly in mainland Europe, Kleinschmit performance can vary depending upon other species. It was et al. (1996) found little variation in growth or morphology found in southern Sweden that ash seedling densities were across German populations of ash while Baliuckas et al. higher in deciduous woodlands than in stands including coni- (1999), who grew ash from across a wider range of Europe in fers (Gotmark€ et al. 2005), and Strestil & Sammonil (2006) a common garden in Uppsala, found that at that scale tree found faster growth of ash seedlings in the Czech Republic in height was negatively correlated with latitude and longitude Fageto–Quercetum illimerosum than in the Carpineto–Acere- with trees from northern latitudes and eastern longitudes tum saxatile community. On good sites, Kerr (2003) found lit- being the shortest. Cundall, Cahalan & Connolly (2003) in tle evidence of intraspecific competition and in monoculture forestry provenance trails planted in the UK found that ash plantations, ash increased in height, diameter and stem vol- from the continental climates of Romania, the Czech Republic ume with a decrease in spacing from 4.86 to 0.77 m between

© 2016 The Authors. Journal of Ecology © 2016 British Ecological Society, Journal of Ecology 10 P. A. Thomas trees although Kuehne et al. (2013) found that wider spacing not abundant when the older ash stands were regenerating c. of >15 m led to greater diameter and with more biomass in 80–200 years ago, but was abundant when the later stands branches. Survival can be better at wide spacing (Espahbodi were regenerating c.85–125 years ago (Merton 1970). The et al. 2003). In forestry plantations in France, the mean height balance may also be swayed in favour of the less shade-tol- growth of ash in the first 10 years (80 cm yearÀ1) was gener- erant ash by it being less browsed by large mammals than ally higher than other species grown under similar conditions: sycamore (Linhart & Whelan 1980). Cerm ak & Mrkva Acer pseudoplatanus c. 56 cm, Quercus rubra 30–80 cm, (2006) in the Czech Republic observed that browsing pri- Juglans nigra 30–70 cm, J. regia 30–50 cm, Prunus avium marily by roe dear led to an increase in the proportion of c. 38 cm yearÀ1 (Le Goff, Colin-Belgrand & Muller 1993; ash saplings (>2 m tall) from 51% in 2002 to 67% in 2005 Balandier & Marquier 1998; Balandier & Dupraz 1999). In a at the expense of sycamore (reduced from 40% to 15% over north-east France stand with ash trees up to 17 cm dbh, Le the same period). Kerr (1995) also points out that ash and Goff & Ottorini (1996) noted that competitive status (defined sycamore have a tendency to produce abundant seed in as the ratio of crown length to total tree height) was linearly alternate years favouring one species or the other depending and positively correlated with tree girth and height. Basal area upon when openings in the canopy occur, fostering the was linearly correlated with foliage biomass and with bole maintenance of both species. volume increments. The most dominant trees had more foli- Ash has traits that in some ways make it competitively age and so grew faster. superior to beech (Rust & Savill 2000; Saxe & Kerstiens 2005). Meißner et al. (2012) showed that ash has a greater plasticity in where it can take water from the soil. In mixed Interaction of ash with elm, sycamore and beech stands in central Germany, ash took 70% of its water from In many ways, ash is similar in ecological needs to Ulmus gla- 0.2 to 0.3 m and 0.5 to 0.7 m below the soil surface while bra (wych elm), certainly in mainland Europe; both have a pref- beech used water from the intermediate depth of 0.3–0.5 m. erence for high pH, soil N and soil moisture although As ash trees increased in diameter (up to 39 cm), they took U. glabra is more demanding of the first two (Diekmann 1996) water progressively from the shallower depth. Growing 3- so competition is limited. The tree species most often seen as year-old saplings in rhizoboxes, Beyer et al. (2013) ecologically similar to ash, and thus serious competitors are observed that the longevity of fine roots of ash was not Acer pseudoplatanus (sycamore) and Fagus sylvatica (beech). much different from beech when grown separately (483 vs. Ash and sycamore occur on the same soils, although ash 565 days), but when grown together, ash roots lived much prefers moister sites (Claessens et al. 1999), and both are longer than beech (603 vs. 321 days). Beech and ash are opportunists producing large numbers of wind-dispersed commonly mixed on base-rich soils (Packham et al. 2012), seeds capable of invading woodland gaps (Petritan, Von but ash is more competitive on more extreme sites and so Lupke€ & Petritan 2009). Since sycamore is more shade tol- goes beyond the ecological limits of beech (Marigo et al. erant than ash, a number of authors have previously sug- 2000). On very base-rich sites and wetter sites, ash regener- gested that sycamore would supplant ash in many ates more readily than beech (Watt 1925) and so becomes woodlands (Watt 1925; Scurfield 1959; Helliwell 1973), dominant (producing W8 and W9 woodlands; see III), while especially as van Miegroet, Verhegghe & Lust (1981) found on more moderate sites, beech dominates forming Fagus– that the mortality of ash seedlings was higher than for syca- Mercurialis woodland (W12). In these beech woodlands, ash more in a mixed woodland. However, Merton (1970) is able to colonize gaps and so persist (Diekmann et al. pointed out that ash regeneration was abundant beneath 1999; Emborg, Christensen & Heilmann-Clausen 2000). Col- sycamore, perhaps because the ground flora was more open, onization is aided by the high seed density of ash and accu- favouring ash, or because pathogens and insects affecting mulated seedling bank and quick growth once gaps appear the sycamore in the canopy would reduce the viability of (Wagner 1990) reaching its maximum height 30–40 years sycamore seedlings beneath (Brotherton 1973). This led Tay- earlier than beech. Nevertheless, ash establishment may be lor (1982) to suggest a cycle of the two species, at least in limited on optimum sites for beech. Thus, a correlation the Chilterns, where ash regenerated below sycamore and between canopy openness and mean density of ash seedlings would come to dominate if the sycamore died quickly or was found by Modry, Hubeny & Rejsek (2004), and Strestil was wind-thrown, releasing the ash seedlings. In turn, syca- and Sammonil (2006) found that ash could not establish more would invade beneath ash and, being shade tolerant, itself under beech on south-facing slopes on limestone in would eventually overtop and replace the ash. This cycle the continental climate of the Czech Republic. could work at the stand level but in reality is much more Once in a gap, both sycamore and ash respond by growing likely to happen in the gaps created by the loss of individ- taller and thinner, investing in height growth at the expense of ual trees or small groups leading to a constant but spatially diameter growth. In a German mixed wood, Petritan, Von changing mix of sycamore and ash within a woodland. The Lupke€ & Petritan (2009) saw that in 50% full sunlight height balance may be altered depending upon site conditions with growth of sycamore and ash were 149 and 145%, respectively, ash favoured on less optimal sites and sycamore on very that of beech saplings. In deep shade, all species grew more disturbed sites (Merton 1970). History may also play a part; slowly but ash and sycamore still grew faster than beech. Radial for example, in the Derbyshire Dales, sycamore seed was growth at 5% full sunlight was lower in ash (0.27 mm) than in

© 2016 The Authors. Journal of Ecology © 2016 British Ecological Society, Journal of Ecology Fraxinus excelsior 11 beech and sycamore (0.3 and 0.33 mm) but at 50% sunlight, Baker 2006) despite later budburst in ash (see VII). In cold- ash (1.78 mm) outgrew sycamore (1.45 mm) and beech acclimated ash buds, extracellular and intracellular ice forma- (1.47 mm). As befits gap invaders, ash and sycamore had more tion occurs at c. À9 and À32 °C, respectively (Till 1956; open canopies for their height (29 and 21 cm2 total leaf area Pukacki & Przybył 2005). Death of damaged buds is cmÀ1 tree height, respectively, compared to 49 cm2 cmÀ1 in undoubtedly hastened by various fungal species (Pukacki & beech), a lower leaf area index (1.24 cm2 cmÀ2 in ash and Przybył 2005), including Gibberella baccata (Wallr.) Sacc. sycamore compared to 1.46 cm2 cmÀ2 in beech) and lower leaf (Ascomycota, Hypocreales) (=Fusarium lateritium Nees) and construction costs (1.29 g glucose gÀ1 in ash compared to Alternaria alternata (Fr.) Keissl. (Ascomycota, Pezizales). sycamore and beech (1.37 and 1.44 g glucose gÀ1, respec- Once cold hardening is lost in spring, shoots are damaged at tively) (Petritan, Von Lupke€ & Petritan 2010). À13 to À9 °C and bud tissue at À9toÀ4 °C (Pukacki & Hajek, Seidel & Leuschner (2015) working in central Ger- Przybył 2005). Young leaves can be damaged in spring at many reported that when beech and ash grew together, À3 °C (Till 1956). Trees that have introgressed with F. an- branches of ash lower in the canopy grew more slowly due to gustifolia, including planting stock introduced into Britain, reduced light levels but the ash trees responded by growing have reduced frost resistance compared to native stock taller, reducing the contact zone between the canopies. In (Gerard et al. 2013). Small seedlings growing in open habi- shade, ash and sycamore tended to carry 85% of the leaf area tats are liable to be killed by frost in April and May. Larger in the top 40% of the tree height (Petritan, Von Lupke€ & Pet- trees show strong powers of recovery but repeated frosting ritan 2010) reducing self-shading (Wagner 1990) and shading leads to badly forked trees, and indeed late spring frosts kill- from other trees. Given its extra height, ash swayed more, ing buds is considered to be a major cause of forking in causing damage to the beech canopy (Hajek, Seidel & young trees (Ningre, Cluzeau & Le Goff 1992); Kerr & Bos- Leuschner 2015). The thicker terminal branches of ash (7.9– well (2001) found 69% of 4147 trees surveyed in southern 26.8 mm, varying between different years) compared to beech Britain between 1991 and 1994 to have one or more forks. (3.3–13.1 mm) gave them a mechanical advantage and in the Late spring frosts that embolize the newly grown earlywood contact zone 14–25% of ash branches were broken at some vessels produced before bud burst can significantly reduce point in the 5-year study compared to 20–50% in beech. This hydraulic conductivity and lead to reduced growth (Cochard contact led to a mean gap between ash and beech canopies of et al. 1997). Long cold winters can greatly reduce growth in 0.6 m compared to 0.2 m between two beech trees. Ash trees subsequent years; Christianson (1889) recorded that after the in gaps had a higher total leaf area (1114 cm2 in ash com- three very cold winters of 1879–1881, the single ash they pared to 755 cm2 in beech) although total dry mass each of monitored in Scotland showed greatly reduced growth leaves, stem and root was no different (Einhorn, Rosenqvist (0.63 cm increase in girth compared to 1.78 cm in the year & Leverenz 2004). Ash also showed greater height growth before) and was ‘a wreck’. per unit of stem mass compared to beech in both open, light conditions (40.5 mm gÀ1 in ash, 38.8 mm gÀ1 in beech) and Drought in deep shade (163.6 mm gÀ1 in ash, 132.2 mm gÀ1 in beech) (Einhorn, Rosenqvist & Leverenz 2004). Adeficit of water in the shoots, due either to soil drought or The main danger for ash under deep shade is that saplings to desiccation by wind, results in their dying back, in yellow do not reach new light before death. Indeed, in shaded condi- coloration and early abscission of the leaves, and in failure of tions, ash had a higher mortality than beech (Petritan, Von the apical buds to open in the following spring (Wardle Lupke€ & Petritan 2007; Holzwarth et al. 2013). However, 1961). Kocher€ et al. (2009) ranked ash as the most drought- Watt (1925) considered that since ash can regenerate in gaps, sensitive species in comparison with Fagus sylvatica, Acer and beech can readily invade ash stands, that a regeneration pseudoplatanus, Tilia cordata and Carpinus betulus. This was cycle often develops in which both species persist with fluctu- attributed to ash having the least reaction to low water condi- ations in dominance, in much the same way as identified tions, with higher values of pre-dawn leaf water potential, leaf above for sycamore and ash. In this case, Rubus fruticosus is conductance and xylem flux density. However, desiccation of important since it forms a dense cover in beech gaps in which 1-year-old bare root seedlings for up to 36 hours had no ash but not beech can establish. Under an ash canopy, R. fru- effect on survival in ash and Quercus robur but killed almost ticosus is less prominent than in beech gaps and beech regen- all seedlings of F. sylvatica and Betula pendula (McKay, erates more effectively. Jinks & McEvoy 1999). Rackham (2014) pointed out that the very dry period over 1975–1976 led to severe ash dieback in the east Midlands. Nevertheless, ash has been seen to survive (C) EFFECT OF FROST, DROUGHT, ETC under extreme heat and drought, such as in France in 2003 (Saccone et al. 2009). Frost Newly opening leaf and flower buds are readily damaged by Flooding freezing temperatures (Wardle 1961). Ash is more sensitive to spring frosts than Fagus sylvatica, Acer pseudoplatanus or As befits a tree capable of growing in riparian areas, ash has A. platanoides (Baliuckas et al. 1999; Jinks, Willoughby & a high tolerance of spring flooding and an intermediate level

© 2016 The Authors. Journal of Ecology © 2016 British Ecological Society, Journal of Ecology 12 P. A. Thomas of tolerance to summer floods, similar to Quercus robur and at exposure of seedlings for 5 year (1 year old at the begin- Ulmus spp., less than in Alnus glutinosa but greater than Acer ning) to a UV-B level equivalent to 18% ozone reduction. pseudoplatanus, A. campestre, Fagus sylvatica and Betula They found a reduction in photosynthesis from À2 À1 pubescens (Iremonger & Kelly 1988; Siebel & Blom 1998; 10.8 Æ 0.46 lmol CO2 m s (SE, n = 10) in ambient À2 À1 Siebel, van Wijk & Blom 1998; Glenz et al. 2006; Vreugden- controls to 7.6 Æ 0.67 lmol CO2 m s at higher UV-B; hil, Kramer & Pelsma 2006). Ash can withstand 1-3 months stomatal density was also reduced (control 130 Æ 5.2; UV- of flooding during the growing season (Sp€ath 1988; Siebel & B47Æ 3.8 mmÀ2; SE, n = 25), as was leaf area (control Bouwma 1998) and 2- to 3-year-old seedlings can tolerate 17.7 Æ 1.39; UV-B 13.0 Æ 0.91 cm2, SE, n = 10). This flooding to ground level for two consecutive growing seasons 30% reduction in photosynthesis in ash was also found in (Iremonger & Kelly 1988), but ash is intolerant of anoxic the pioneer species Betula pendula (31%) but was far less stagnant water (Glenz et al. 2006). Part of the tolerance is than the other species tested Tilia cordata (45%), Quercus due to the ability to produce adventitious roots, hypertrophied robur (55%) and Acer pseudoplatanus (61%), suggesting lenticels and also aerenchyma (Frye & Grosse 1992; Siebel, some resilience to UV-B. Conversely, excluding UV-B radi- van Wijk & Blom 1998). Ash is most sensitive to late spring/ ation led to increased plant dry mass in ash and its competi- summer flooding, and in alpine floodplains, flooding in tors (Bogenrieder & Klein 1982). April–July can greatly reduce ash growth. River engineering to reduce flooding has thus greatly increased the potential of Fire ash growth over the past 20 years in these areas (Girel, Gar- guet-Duport & Pautou 1997). Tolerance of flooding does vary Ash is very fire sensitive, and its decline in Europe c. 6600 between ecotypes. Jaeger et al. (2009) looked at 3-year-old BP onwards has been attributed to the increase in human- seedlings grown from seed taken from a riparian and a moun- caused fires (Tinner et al. 1999, 2000, 2005). Delarze, Calde- tain population in southern Germany. The mountain popula- lari & Hainard (1992) found that ash along with Acer pseudo- tion after 2 9 2 week long flooding lost more leaves (>half; platanus, Tilia cordata, Fagus sylvatica and Corylus avellana none in the riparian seedlings) and new leaf formation almost were largely absent from plots burnt even 25 years prior in ceased (reduced by fifth in the riparian seedlings). When southern Switzerland. Ash biomass has a low calorific value flooded for 3–10 days, net assimilation in the mountain seed- (3600–6000 kJ kgÀ1 fresh mass) and low flammability, espe- lings was reduced to 20% of the control and in the riparian to cially after the spring flush of leaves (Nunez-Regueira,~ 66% which also had a greater accumulation of ethanol in the Rodrıguez An~on & Proupın Castineiras~ 1997) and so is more xylem sap (c. 3.5 nM compared to c. 2.4 nM in mountain likely to be damaged in mixed stands of more flammable seedlings – estimated from a figure), suggesting anaerobic species. metabolism. VI. Structure and physiology Ozone and ultraviolet light (A) MORPHOLOGY Sensitivity of ash to ozone pollution has been found to be variable but generally can be classified as moderately sensitive, Branching of the shoot is monopodial with a low number of usually more sensitive than Fagus sylvatica, Quercus robur, branch orders (3–5). Ash invests in vertical height growth Pinus sylvestris and Fraxinus ornus but less sensitive than Acer with rapid self-pruning of side branches while young. As it pseudoplatanus (Gunthardt-Goerg€ et al. 2000; Landolt et al. approaches maturity at 50–90 years (Claessens et al. 1999), 2000; Novak et al. 2003; Gravano et al. 2004; Bussotti et al. ash is typically 7–25 m tall and the canopy increases in width 2005; Contran & Paoletti 2007; Gerosa et al. 2009). Upon to eventually form a rounded rhombic crown up to 8 m diam- exposure to above-ambient concentrations, ash develops necro- eter. In the south of England, the crown of ash is consistently tic spots on the leaves and premature leaf abscission, and has a wider than those of any of its main competitor trees for all lower net assimilation rate. Reiner et al. (1996) gave 2-year-old trunk diameters (Hemery, Savill & Pryor 2005) as befits a seedlings 0–150 ppb of ozone (ambient c. 50 ppb) and found light-demanding adult tree. Hein & Spiecker (2008) give allo- that ozone stimulated stomatal closure and led to a decreased metric equations for growth of open-grown trees. On rich radial growth, although at lower levels (≤72 ppb) Hayes, Wil- alluvial soils, ash can reach 40–45 m in height and 1.6–1.8 m liamson & Mills (2015) found no effect on any growth aspect dbh, but in lowland forests, 20–25 m height is common of ash. Even ambient concentrations of ozone have proved (Hulden 1941; Collin & Badot 1997). Female trees generally detrimental to ash since its removal in charcoal-filtered air led are shorter and have thinner trunks than males (Tal 2006); to an increase in mean net photosynthesis by 18% and mean Rohmeder (1967) recorded that male trees in Germany were stomatal conductance by 8% (Novak et al. 2005), but growth 14% wider, 10% taller and 40% larger in volume than female rate (determined by increase in basal diameter) was not affected trees. Male trees may be bigger due to a lower investment in (Novak et al. 2007). reproduction although Tal (2006) argues that male costs may In addition to the direct impact of ozone, increased ultra- be as high as female since males have up to twice as many violet B light due to lower ozone levels in the stratosphere flowers and bear the burden of galls (see VIII(A)). When can have its own impact. Keiller & Holmes (2001) looked the crown becomes decadent, due to age or an unfavourable

© 2016 The Authors. Journal of Ecology © 2016 British Ecological Society, Journal of Ecology Fraxinus excelsior 13 habitat, epicormic shoots spring from the lower part of the trunk may appear to be part of the root system rather than the trunk (Wardle 1961). trunk. In such cases, which can be hard to distinguish in older The canopy leaves of trees and older saplings are morpho- trees, it may be necessary to add up to 25 years (possibly logically distinct from the juvenile leaves of seedlings, young more) to age estimates from ring counts at the apparent base saplings and epicormic and coppice shoots (see Wardle 1961 of the tree (Merton 1970). The bark of ash is thin. Kocher,€ for details). Only sun leaves are developed in adult foliage due Horna & Leuschner (2012) measured bark thickness in trees to the low canopy density; the leaf area index of ash is gener- 24–41 cm dbh as 7.56 Æ 2.26 mm (SD), similar to that of ally c. 3.5 compared to 4.6–5.2 in other competing species Fagus sylvatica and Acer pseudoplatanus. (Holscher€ 2004). Shaded saplings, however, have both sun and The wood is ring-porous. Earlywood vessels elements are shade leaves; the latter are thinner and possess only one distinct 80–170 lm in diameter and latewood 10–70 lm; both have palisade layer. Under heavy shade, the palisade mesophyll may a mean length of 0.25 mm (Burggraaf 1972). Juvenile wood be absent (Wardle 1961). Young stems and leaves of ash are in up to the first 30 annual growth rings has narrower but often tinged orange or purple (Rackham 2014). Specific leaf more frequent vessels and is of lower value as timber area (SLA) has been measured at 13.8 Æ 3.7 m2 kgÀ1 (as- (Helinska-Raczkowska~ & Fabisiak 1999). Ash wood is com- sumed to be SD) in ash, compared to 22.4 Æ 4.5 m2 kgÀ1 in paratively dense and comparable to Fagus sylvatica and Ulmus glabra (Alberti et al. 2005), fairly low in ash due to the Quercus spp. Density has been reported from 551 to presumed inclusion of the petiole and rachis. Holscher€ (2004) 790 kg dry mass mÀ3 (Loudon 1838; Le Goff et al. 2004; found the SLA of ash in central Germany to vary with height: Alberti et al. 2005; Rackham 2014). Much of this variation in the lower canopy (11 m above ground), leaves were thinner is attributable to the speed of growth since, in common with – 34.2 Æ 2.0 m2 kgÀ1 (SD) – compared to the upper canopy other ring-porous species, variation in the width of annual (28 m tall trees) at 11.9 Æ 0.8 m2 kgÀ1. Janse-ten Klooster, rings is primarily due to differences in the width of late Thomas & Sterck (2007) found that saplings in deep shade wood in response to growing conditions; fast growth with little direct sunlight had a leaf mass of 1.9 g compared to increases the relative proportion of late wood and hence those in light shade (>10–100% full sunlight) at 3.4 g, and this increases wood density. Fast grown ash, however, has less was reflected in the SLA: 36.0 in shade and 25.3 mÀ2 kgÀ1 in strength parallel to the grain due to thinner cell walls of the light. Leaves formed 66% of biomass of a current-year shoot in fibres in the earlywood (Clarke 1935). Fresh ash wood has a ash compared to 74% in Acer platanoides since there is more comparatively high moisture content (36%, compared to con- investment in stem and petioles (20 and 14%, respectively, of ifers and diffuse-porous trees at 14%) so the wood readily total shoot mass) in ash than in the maple (14 and 12%), so develops cracks on drying (Sorz & Hietz 2006). Ash wood total leaf construction costs were lower in ash than A. pla- density changes with height up the trunk. Alberti et al. tanoides; ash uses the leaves as cheap, disposable branches (2005) found density decreased to a minimum at 4–6m (Barthod & Epron 2005). Leaf construction cost per unit area height and then increased with height continuously to the was higher in A. platanoides than in ash (1.30 vs. 1.20 g glu- top of the 18 m trees investigated, a similar pattern to that cose gÀ1) but decreased less with shade in ash, so shade leaves found in F. sylvatica and Alnus glutinosa. Despite being were proportionately more expensive in ash and may help dense, ash wood rots quickly in contact with the ground explain their absence in mature trees. The petiole/rachis has a (Rackham 2014 notes that fence posts at Hayley Wood, low lignin, structural polysaccharide and protein content and it Cambridgeshire lasted just 4–5 years), suggesting a lack of has been calculated that the cost of its construction was 5% defensive compounds in the heartwood. lower per unit mass than that for leaflets (Niinemets & Kull Death or removal of buds can produce forking in ash. The 1999; Niinemets 1999). Niinemets (1999) also showed that the main causes are late spring or early autumn frosts, drought, petiole had c. 10% the chlorophyll concentration of the leaflets, damage by deer, birds or insects, wind and genetic predisposi- but the non-structural carbohydrate concentration was 20% tion (Ningre, Clueau & Le Goff 1992; Kerr & Boswell 2001). higher than leaflets, suggesting that the petioles are used to After wounding, the cambium grows wood with vessels up store food. Stomata are found only on the underside of leaves to 77% smaller in diameter but with a higher density of ves- (Morren 1866; Cornelissen et al. 2003). Stomatal density var- sels (by up to 475%) for the next year in an apparent shift to ied with height: sapling 95 Æ 32 mmÀ2 (SD), lower canopy improved hydraulic safety (Arbellay, Fonti & Stoffel 2012). 109 Æ 20 mmÀ2, upper canopy 185 Æ 36 mmÀ2 (Holscher€ Ash wood, in common with other ring-porous trees, contains 2004). tyloses to seal off embolized vessels (Schmitt, Richter & Terminal winter buds in the canopy are black, dry, packed Muche 1997). Detailed descriptions of wood composition and with brown hairs and possess three pairs of protective modified timber properties of ash are given by Bamford & Van Rest bud scales. The outer scales of the terminal buds of seedlings (1936) and Crivellaro et al. (2013), and hydraulic architecture tend to be less specialized (Wardle 1961). Seedlings raised in a by Burggraaf (1972), Cochard et al. (1997) and Bettiati, Petit glasshouse produced winter buds without protective modified & Anfodillo (2012). Height growth and form are under high scales (Wardle 1961 has drawings of the bud scales). genetic control (Savill et al. 1999); the additive genetic coef- On scree and unstable slopes, trees may become prostrate, ficient of variation ranged between 10.2 and 12.7% for height at least at the base. This portion of the trunk produces adven- and 1.5 and 2.1% for dbh (Mwase, Savill & Hemery 2008). titious roots on the underside so the lowest 1 m or so of the Allometric equations for predicting stem volume are given by

Alberti et al. (2005) for north-east Italy, Blujdea et al. (2012) ash roots. Despite the low species diversity, Lang & Polle for Romanian plantations, and Konopka,^ Pajtık&Sebe n (2011) in the same mixed stands found that the roots of ash (2015) for western Carpathian stands. had higher levels of most nutrients (except Ca) than roots of Ash seedlings have a superficial root system even on ectomycorrhizal trees (Fagus sylvatica and Tilia spp.), sug- deep riparian soils (Kostler,€ Brückner & Bibelrichther gesting better uptake. Moreover, Seven & Polle (2014), also 1968), reaching a depth of 0.15 m after 4 months (Fous- working in Germany, confirmed higher concentrations of Mg, sadier 1998; Rust & Savill 2000). Older trees develop an K and P, confirming that AM are better at taking up P than extensive and shallow lateral woody root system (Le Sueur ectomycorrhizal fungi. AM in ash only develop well on soils 1924; Kostler,€ Brückner & Bibelrichther 1968) that reaches with high levels of Ca and Mg (Weber & Claus 2000). a maximum depth of 0.30–0.50 m. The original tap root remains and is supplemented by vertical sinker roots (C) PERENNATION: REPRODUCTION between 0.75 and 2.5 m deep (Wardle 1961; Gordon 1964). In mixed stands, ash becomes more deeply rooted in Phanerophyte. It coppices strongly from cut stumps, and old response to competition from shallow-rooted species (Rust trees respond well to restarting pollarding (Slotte 1997). Young & Savill 2000) and competition for light above ground ash of poor form can be cut at ground level (stumping) to pro- (Wagner 1990). Conversely, on wet soils, the roots will not mote vigorous high-quality regrowth (van Miegroet 1956). Ash grow below the permanent water-table or any gleyed hori- may also perennate by layering in moist, shaded areas (Pola- zon. But ever the opportunist, ash roots will readily grow taycuk & Sparik 1993) or after branches are buried following down shrinkage cracks in clay soils formed during dry flooding. Ash is also known to occasionally sucker (unpub- weather (Wardle 1961). Root growth continues throughout lished information from C.D. Pigott, reported in Wardle 1961). life and results in mature ash having a root system with a Ash is fairly short-lived, c. 200 years although coppiced stools greater volume and biomass than that of Fagus sylvatica, and some individual maiden trees may survive more than Carpinus betulus or Acer pseudoplatanus (Kostler,€ Brückner 300 years (Scurfield 1959; Rackham 2003). In the Białowieza_ & Bibelrichther 1968; Collin & Badot 1997). The morphol- Forest, Poland, Falinski (1986) states that ash aged 250–400 years ogy of wood in roots changes when exposed to the air are not rare and some individuals may live even longer. (probably a mechanical response) with new wood usually New trees can be readily produced from cuttings taken having smaller vessels (Hitz et al. 2008). Leaf area to root from dormant trees using an enclosed mist unit (Silveira & biomass ratio increases with decreasing irradiance (36% Cottignies 1994; Jinks 1995) and by grafting. As with many down to 4% full sunlight), but more so in Acer pseudopla- trees, accelerated growth in ramets from younger trees com- tanus than ash (Barigah et al. 2006), associated with the pared with older ones is temporary and soon slows down greater shade tolerance of A. pseudoplatanus. (Mencuccini et al. 2007). Ash is also readily propagated Coarse roots (over 1 mm diameter) persist indefinitely and in vivo. Adventitious shoot regeneration has been reported appear able to withstand long periods of poor aeration. By from excised embryos for F. excelsior (Mockeliunaite & Kuu- contrast, the more numerous fine roots are mostly abscised siene 2004; Capuana et al. 2007) and epicotyl, leaf and root within 1 year and are readily killed by flooding or drought tissue (Hammatt 1994; Mitras et al. 2009; Lebedev & Sch- (Wardle 1961). Fine roots are at their greatest density in the estibratov 2013). Shoot tips can be cryopreserved (Schoen- top 5 cm of the soil (Wardle 1961). The highest densities weiss, Meier-Dinkel & Grotha 2005). were found in fen peat and in slightly acidic sand: 1000- 1500 cm of roots < 1 mm diameter in 85 cm3 of soil (Wardle (D) CHROMOSOMES 1961). On heavier loam soils, where root penetration was more difficult, values ranged from 230 to 400 cm. Fine roots 2n = 46. The amount of DNA per diploid cell has been mea- tend to grow in clearly defined, dense clumps with root-free sured at 2.0 pg (Grime, Hodgson & Hunt 2007). Genome size zones in between (Rust & Savill 2000). Ash has a gradual was estimated at 822 Mbp (1n value) by Siljak-Yakovlev decrease in fine root density within a radius of 10 m from the et al. (2013) and 875 Mbp by the British Ash Tree Genome trunk (Meinen, Hertel & Leuschner 2009). Project (2015) in a self-pollinated tree with low heterozygos- ity, containing c. 43 k genes.

(B) MYCORRHIZA (E) PHYSIOLOGICAL DATA In contrast to other Fraxinus species, F. excelsior forms arbuscular mycorrhizas (AM) but not ectomycorrhiza. As is Temperature, moisture and growth common with AM, a limited number of fungi are involved. For example, in mixed tree stands in Germany, Lang, Seven Ellenberg values (Ellenberg et al. 1991): temperature 5 (inter- & Polle (2011) found that the AM contributed 5% to total mediate); continentality 3 (between oceanic and suboceanic). stand mycorrhizal fungal species diversity. In ash and Acer Ash has a low-density canopy so leaves are readily exposed to spp., 19 Æ 9% (SD) of root tips were colonized by a rela- sunlight. In Switzerland, the upper side of leaves was c.3°C tively species-poor set of fungi; seven different sequences for warmer than ambient but lower surface was 3.5–5 °C cooler Glomeromycota were found, of which two occurred only on than ambient (Feller 2006). As with the majority of temperate

© 2016 The Authors. Journal of Ecology © 2016 British Ecological Society, Journal of Ecology Fraxinus excelsior 15 trees, growth of ash roots takes place whenever the soil temper- (Carlier, Peltier & Gielly 1992). Thus, ash tolerates wide leaf ature is above 4–6 °C and below 30 °C. Above-ground growth water potential variation without losing vigour. is at least partially dependent upon temperature, but moisture The ability to keep stomata open even at low water avail- probably plays a more important controlling role. Annual ring ability is aided by the accumulation of malate and mannitol in widths in ash have been seen to be positively correlated with the leaves; when pre-dawn water potential was À4 MPa, precipitation and air temperature of the previous winter malate and mannitol increased by 91.8 (reaching 600 mM) (December to February), precipitation in spring (May and June) and 92.2 (280 mM), respectively, possibly aided by and annual precipitation, and negatively correlated with sum- Ca-malate complexes and elastic adjustment of the cell walls mer and autumn air temperature (June to November) (Karpa- (Carlier, Peltier & Gielly 1992; Marigo & Peltier 1996). vicius & Vitas 2006; Mund et al. 2010). Lehto et al. (2004) measured 7.08 mg gÀ1 dry mass of man- Kocher,€ Horna & Leuschner (2012) working with mature nitol in stems and 22.10 mg gÀ1 in leaves of 1-year-old seed- trees in central Germany found the radial growth of the trunk lings compared to 0.06 mg gÀ1 in leaves of other trees such in a growing season to be highest in ash (c. 5.8 mm) com- as Alnus glutinosa and Prunus padus. This accumulation can pared to c. 2.8 mm in Fagus sylvatica and c. 1.5 mm in Acer lead to an osmotic adjustment of 0.6 MPa in adult ash during pseudoplatanus. Radial growth could exceed a maximum of a summer drought period (Peltier et al. 1994). Malate may be 70 lm dayÀ1 (mean 56.8 lm dayÀ1) in ash compared to involved in forcing closure of the stomata in ash in concentra- maximum rates of 20–40 lm dayÀ1 (mean 8.5– tions regularly found in the xylem sap (Patonnier, Peltier & 22.6 lm dayÀ1)inF. sylvatica, A. pseudoplatanus, Carpinus Marigo 1999). The opening of ash stomata appears to be pri- betulus and Tilia cordata. Growth in ash was highest in May. marily controlled by light (Besnard & Carlier 1990) and they Maximum growth of all five species occurred on days when are fairly insensitive to moisture content of leaves. Under relative humidity was 80–100% and was lowest on days when drought conditions, stomata will close around solar noon it was <75%. The authors suggest that at this scale, air tem- (Carlier, Peltier & Gielly 1992), but at a much lower water perature and soil moisture played a secondary role to humid- potential than its competitors (at À3.0 Mpa xylem water ity. High humidity reduced transpiration rates and hence very potential compared to À1.4 Mpa in Quercus robur). negative pressures in the xylem leading to increased turgor in High stomatal conductivity and open stomata lead to high cambial cells, promoting cell division and expansion. Con- transpiration rates, measured at between 3.5 and versely, Le Goff et al. (2004) found that high humidity (and 12 mmol mÀ2 sÀ1 (Besnard & Carlier 1990; Lemoine, Peltier hence low evapotranspiration) resulted in lower net assimila- & Marigo 2001; Stohr€ & Losch€ 2004) even on droughty soils, tion rates in ash. So, assimilation of carbon and its use in higher than the typical range for temperate deciduous trees of growth is not necessarily temporally linked in ash. 2.5–3.7 mmol mÀ2 sÀ1. In ash, therefore, sap flow is insensitive to water shortage (Kocher€ et al. 2009). When this is added to stomata being open for significant parts of the day, water loss Water relations in ash can be very high, up to 258 ml mÀ2 leaf area hourÀ1 Ellenberg et al. (1991) value: moisture X (indifferent). Ash has (Ladefoged 1963), reaching maximum daily totals of 1.7– a tolerant anisohydric strategy to water stress (Carlier, Peltier & 3.3 kg mÀ2 dayÀ1, higher than expected in tropical and tem- Gielly 1992). In ash, xylem flow does not decrease with perate lianas that are known for their high water use (Stohr€ & decreasing soil moisture or daily mean vapour pressure deficit Losch€ 2004). Maximum mean water use in saplings 5 m tall (Coners & Leuschner 2002; Holscher€ et al. 2005). The result is and 2.9 cm diameter tree reached 2.34 kg of water per day that soil drying is comparatively rapid and ash stops growing (Stohr€ & Losch€ 2004). sooner in drought conditions (Aussenac & Levy 1983). Thus, Although transpiration rates are high, the flux of water as described in V(C), ash is considered to be drought sensitive. through the xylem is low. Holscher€ et al. (2005) found that it Stomatal conductance is high but comparable to other decidu- was the lowest of the five species tested in central Germany ous species, in the order of 0.2–0.3 (0.44) mol mÀ2 sÀ1 when (Fagus sylvatica > Acer pseudoplatanus > Tilia cordata water is available, dropping as low as 1.8 mmol mÀ2 sÀ1 under > Carpinus betulus > ash) measured at 67 g cmÀ2 dayÀ1 in drought conditions (Besnard & Carlier 1990; Roberts & Rosier ash compared to 152 g cmÀ1 dayÀ1 in F. sylvatica. Xylem 1994; Cochard et al. 1997; Lemoine, Peltier & Marigo 2001; porosity in ash (0.59 mm3 mmÀ3) is very similar to that of Abdul-Hamid & Mencuccini 2009). However, there is compar- diffuse-porous trees (Gebauer, Horna & Leuschner 2008), but atively little stomatal control, so leaf water potential tends to ash has a smaller conducting area because, being ring-porous, decrease sharply in the morning reaching a minimum of À2.0 water conduction is primarily up the outermost annual rings, to À2.6 Mpa at solar noon (Aussenac & Levy 1992; Cochard usually accounting for < 1 cm width of sapwood so total sap- et al. 1997; Lemoine, Peltier & Marigo 2001) but not low wood area was c. 11 times smaller than in diffuse-porous spe- enough to induce stomatal closure and reduce further water cies (Holscher€ et al. 2005) and the ratio of area of conducting loss. Indeed, Guicherd et al. (1997) put 3-year-old seedlings xylem to basal area was 0.21, much lower than the 0.75 found under experimental drought and found that at a pre-dawn water in F. sylvatica (Gebauer, Horna & Leuschner 2008). The solu- potential of À6 MPa, the leaves showed loss of turgor pressure tion to this paradox does not lie in a superior ability of ash to but stomatal conductance was still measurable, and in adult withstand cavitation; Barigah et al. (2006) found ash to be trees stomata stay open until water potential nears À5 MPa intermediate (along with Acer pseudoplatanus) in risk of cavita-

© 2016 The Authors. Journal of Ecology © 2016 British Ecological Society, Journal of Ecology 16 P. A. Thomas tion and more vulnerable than Fagus sylvatica. Low conductiv- of fine roots to increase access to soil water; in central German ity may, however, be partially tied to mature ash having a lower stands, Holscher€ et al. (2005) found that ash accounted for total leaf area compared to other temperate tree species. Roberts 58% of total fine root biomass, but only 45% of the stem num- & Rosier (1994) in a Hampshire woodland found that while ber implying that ash had a greater density of fine roots com- ash made up 45% of the number of stem and 41% of the pared to other trees in the stand. This enables ash to maintain projected crown area, they had only 28% of the total leaf sufficient sap flow to keep the leaves functioning although at area. A small leaf area also fits the small amount of water the expense of large leaf water potential fluctuations (Kocher€ stored in the xylem. Bittner et al. (2012) noted that transpi- et al. 2009). ration in ash reaches a maximum around solar noon, yet roots reached maximum uptake two hours later. The shortfall Light and photosynthesis is met by water stored in the xylem. Kocher,€ Horna & Leuschner (2013) showed that while diffuse-porous trees Ash has an Ellenberg value for light of 4 (between a shadow held 10–22% of daily transpiration needs in the wood (5– and half shadow plant, >10% but much less than 100% full 12 kg dayÀ1 held), ash 25-28 m tall only held 0.5– sunlight). Morphologically, shade leaves are not found in 2.0 kg dayÀ1 or around 5.3% of their daily needs. Bittner adult trees but saturating irradiance has been shown to et al. (2012) suggest from modelling in the same site used decrease through the canopy (upper canopy 770 Æ 71 (SD); by Kocher€ that water storage can in fact reach a mean of lower canopy 535 Æ 25; saplings 338 Æ 109 lmol mÀ2 sÀ1), 24% of daily transpiration needs; the variation can be attrib- as did the light compensation point (upper 8 Æ 2, lower uted to different weather patterns, since at low transpiration 6 Æ 1, saplings 5 Æ 3 lmol mÀ2 sÀ1). Dark respiration was rates, stored water can provide a higher percentage of needs. similar at all levels, at between À0.4 and À0.5 lmol mÀ2 sÀ1 The small leaf area, and the ability of the leaves to tolerate (Holscher€ 2004). At irradiance below 23.5% full sunlight, the large water potential variations, suggests that a small amount leaves are liable to be abscised (Wardle 1961). Leaf total of stored water is adequate. chlorophyll levels were measured at 3.06 mg gÀ1 fresh mass The hydraulic architecture of ash includes a number of in April in Iran (Esfahani et al. 2013) and chlorophyll a/b adaptations to ensure all leaves get equal access to water. In ratio in the lower canopy (11 m above ground) at 2.8 Æ 0.1 lower (and therefore older) branches, 90% of the total resis- (SD) and in the upper canopy (28 m tall trees) at 3.2 Æ 0.3 tance to water flow comes from within the branch, while in (Holscher€ 2004). higher, younger branches 90% of the resistance is found Net assimilation rates at high irradiance have been mea- within the leaf since these branches have wider vessels (rachis sured at 12.5–16.3 lmol mÀ2 sÀ1 in ash (Holscher€ 2004; Le vessel diameter 22.6 Æ 5.4 lm (SD) in 2-year-old branches Goff et al. 2004) significantly higher than in Acer pseudopla- compared to 19.5 Æ 6.1 lm in 7-year-old ones) and younger tanus, Carpinus betulus or Tilia platyphyllos (Holscher€ 2004). branches have long shoot internodes. Both these adaptations Near the bottom of the canopy assimilation rates dropped to decrease xylem resistance to sap flow in younger branches so around 5 lmol mÀ2 sÀ1, comparatively higher than the trees this leads to the water potential required to attract water being listed above due to the open canopy of ash (see VI(A)), but similar throughout the canopy (Cochard et al. 1997). this compares to 10 lmol mÀ2 sÀ1 for Fagus sylvatica in Although xylem conductivity is low, modelling by Bittner similar climatic conditions (Lebaube et al. 2000). Assimila- et al. (2012) showed that ash has the ability to extract water tion rates decline with age. Mencuccini et al. (2005) found from very dry soils; F. sylvatica and Tilia cordata reduced their net assimilation rate of ash fell from >0.3 kg mÀ2 yearÀ1 in water uptake at soil matric potentials <À0.10 Mpa while ash trees <10 years old to c. 0.1 kg mÀ2 yearÀ1 in trees did not reduce water uptake until soil water matric potentials >100 years old. Similarly, relative above-ground growth rate were lower than À0.25 Mpa (Holscher€ et al. 2005). Wiersum dropped from >0.9 kg kgÀ1 yearÀ1 in young trees (<10 years & Harmanny (1983) showed that ash was relatively slow to old) to <0.2 kg kgÀ1 yearÀ1 in individuals >25 years old. reduce the permeability of its roots in response to drought. This Intercellular CO2 concentration has been measured at is despite ash roots having a small mean vessel diameter 2.112 Æ 0.064 to 2.375 Æ 0.008 lmol molÀ1, maximum car- (35.0 Æ 1.1 lm, SD) compared to beech (42.3 Æ 1.4 lm) in boxylation rate from 40 to 85 lmol mÀ2 sÀ1 at 25 °C, maxi- roots <3.5 mm diameter. These small vessels may reduce freez- mum electron transport rate at 120–225 lmol mÀ2 sÀ1, similar ing embolisms but reduce hydraulic conductivity. Although the to that of other common deciduous trees (Dreyer et al. 2001; xylem cross-sectional area in ash (42.2 Æ 1.3%) was in the Contran & Paoletti 2007; Abdul-Hamid & Mencuccini 2009). same order of magnitude as in Fagus sylvatica, Acer pseudo- Of 19 broadleaf and conifer species investigated, ash had the platanus, Tilia cordata and Carpinus betulus, the vessel density highest concentration of chlorophyll per unit area of bark was the lowest of all species (53 Æ 2mmÀ2) and the lumen (500 mg mÀ2); the concentration per unit mass was similar to area (5.8 Æ 0.4%) was less than that of F. sylvatica other species, showing that in ash the chlorophyll layer is dee- (6.9 Æ 0.8%). The net result was a much lower specific con- per into the twig than other species (Pfanz et al. 2002). Cur- ductance: 4.48 Æ 0.77 kg MPaÀ1 sÀ1 mÀ2 in ash compared to rent-year stems contain chlorophyll through to the pith with 13.03 Æ 1.40 in F. sylvatica (Kocher€ et al. 2012). The roots of total chlorophyll concentrations of 0.46 Æ 0.02 mg gÀ1 (SE, ash can supply enough water to the profligate stems not by n = 3) in summer, falling to 0.29 Æ 0.02 mg gÀ1 in winter speed of movement but instead appear to rely on a high density (Berveiller, Kierzkowski & Damesin 2007). Transmission of

© 2016 The Authors. Journal of Ecology © 2016 British Ecological Society, Journal of Ecology Fraxinus excelsior 17 light through the phloem can reach 50% of full sunlight and is 55 (5.2), Zn 19 (4.4), B 26 (5.8) mg kgÀ1. Hejcman et al. still 0.4% at the pith in 1-year-old stems, 6 mm in diameter (R. (2014) similarly measured the elemental concentration in win- Langenfeld-Heyser, unpublished data in Pfanz et al. 2002). ter-collected annual twigs used as fodder (mg gÀ1): N 12.4, P Photosynthesis does seem to take place since the stem chlor- 1.5, K 8.5, Ca 9.9, Mg 1.2. Manganese concentration was very enchyma in 1- to 5-year-old twigs has been found to absorb low in both leaves and wood compared to ﬁve other competi-

CO2 before bud break and produce oxygen at a rate of 2.5– tor tree species tested (Hagen-Thorn & Stjernquist 2005), but À2 À1 3.0 lmol O2 m s (Langenfeld-Heyser et al. 1996). P, K and Ca had the highest concentration in leaves found in Photosynthates are transported partly as sucrose but carbo- nine deciduous species tested by Hejcmanova, Stejskalova& hydrates of the raffinose group are a more important transport Hejcman (2014). sugar in ash trees (Thoms et al. 2015). Fagus sylvatica used Other elements measured by Desideri, Meli and Roselli primarily sucrose, loaded apoplastically into the phloem cells, (2010) were as follows: Al < 100, As <1, Rb 6.0, Sr 26, Cd while ash used both apoplastic and symplastic loading, with 0.6, Sn 1.1, Hg < 0.1, Pb 0.7 mg kgÀ1dry mass. Aksoy & more emphasis on the latter at the end of the growing season. Demirezen (2006) found ash leaves to be a good biomonitor of soil heavy metal concentration in Turkey; in an urban roadside, they reached Pb 18.4, Cd 41, Cu 33, Zn 39, Ni 46, Mineral nutrients Cr 44 mg kgÀ1 dry mass. Lead was measured in bark in Ash is a nitrophilous species with a high demand for soil Frankfurt in 1997 at >400 mg kgÀ1 (Ballach, Wittig & Wulff nutrients, particularly N, P, Ca and Mg; the Ellenberg value 2002). In polluted sites in Iran, Sangi et al. (2008) found that is 7 (mostly on soils rich in mineral N; Ellenberg et al. ash had the highest bioaccumulation of heavy metals of any 1991). Height growth of ash is highly correlated with the tree tested except Ulmus carpinifolia. (=U. minor). Uptake of nitrogen content of the leaves (Gordon 1964; Weber-Blaschke heavy metals by ash does depend upon soil pH. For example, et al. 2008). As fits with a nitrophilous species, Schulz, leaves of ash seedlings growing in soil with As levels H€artling & Stange (2011) found that the N uptake of 2-year- >100 mg kgÀ1 dry mass contained 2.29 mg kgÀ1 dry mass old seedlings was greatest in ash (F. excelsior > Tilia when growing in soil with a pH of 6.36 but had a ‘much cordata > Pinus sylvestris > Picea abies > Fagus sylvat- lower’ concentration when on soils of pH 4.40 (Madejon & ica > Quercus petraea) although relative growth rate in ash Lepp 2007). In polluted street trees in Iran, the internal pH of was similar to the other species (0.375 g fresh mass dayÀ1 in leaves is decreased (pH 5.52 in polluted leaves; 7.02 in con- ash). Ash can react well to fertilizers on poor soils (Bulır trols) and, probably as a defence against excessive oxidation, 2007), but they have little effect on already rich soils (Cul- levels of ascorbic acid were increased from 0.22 mg gÀ1 leton, Murphy & McLoughlin 1996). fresh mass in unpolluted controls to 0.55 mg gÀ1 in polluted Desideri, Meli & Roselli (2010) found the concentration sites (Esfahani et al. 2013). of elements in ash leaves from Hungary to be (all in Particulate matter (PM) is fairly readily caught on leaf sur- mg kgÀ1 dry mass): (macroelements) K 10 684, Mg 1447, faces; the recorded levels of <10 lgcmÀ2 of PM 10-100 lm Ca 12 927, P 640, S 1900; (microelements) Cr < 2, Mn 20, and <1.5 lgcmÀ2 of PM 2.5-10 lm were similar to Acer Fe 131, Co < 1, Ni 4.7, Cu 7.7, Zn 11.0; (halogens) Cl 505, campestre but lower than in those with hairy leaves Br 1.8, I 4.9. None was particularly high or low compared (Dzierzanowski_ et al. 2011). Particulate matter <2 lmis to 34 medicinal plants also tested. Similar results are given by incorporated into bark tissue (Catinon et al. 2009) and Cati- Gałuszka et al. (2011), including Na 106, B 23 mg kgÀ1, non et al. (2008), suggesting that the chemical composition Nunez-Regueira,~ Rodrıguez An~on and ProupınCastineiras~ of bark largely reflects atmospheric deposition rather than (1997), Rosselli, Keller & Boschi (2003) and Hejcmanova, transport from the xylem; they give mineral concentration Stejskalova and Hejcman (2014). Using material from the data of young shoots from superficial deposits through Lake District, Gordon (1964) found higher levels of Ca successive tissue layers to the pith. (6784–27 437 mg kgÀ1) and P (750–1420 mg kgÀ1). Nitrogen Hagen-Thorn et al. (2006) looked at nutrient resorption content of leaves has been measured at 17–33 mg gÀ1 dry from leaves during autumn senescence in Lithuania and found mass (Gordon 1964; Broadmeadow & Jackson 2000; Barthod that resorption of many nutrients was low in ash compared to & Epron 2005; Abdul-Hamid & Mencuccini 2009; Hejc- Quercus robur, Tilia cordata and Betula pendula (N 36%, P manova, Stejskalova & Hejcman 2014) although it was lower 37%, K 38% and S 31% in ash) but was higher in Mg in current-year twigs in summer in Sweden at 7.90 Æ 0.62 (74%). This low resorption may be partly attributable to the mg gÀ1 (SE, n = 3); this was similar to Fagus sylvatica but high levels retained in the petiole and rachis; Tremolieres lower than other trees such as Betula pendula (13.00 Æ 1.68 et al. (1999) used just leaflets and found that up to 60% of N mg gÀ1)andAlnus glutinosa (14.68 Æ 0.97 mg gÀ1)(Berveil- was withdrawn, but some of this could have been lost by ler, Kierzkowski & Damesin 2007). Nitrogen is stored over external leaching rather than being resorbed. Certainly, winter primarily in the roots with smaller amounts remobilized Hagen-Thorn et al. (2006) observed that foliar leaching of from the stem in the spring (Marmann et al. 1997). Hagen- nutrients per unit of leaf area was highest in ash: K 29% of Thorn & Stjernquist (2005) using trees from across Europe green leaf content compared to 8–11% in the other three spe- found that leaves had higher concentrations than stemwood of cies; N 4.2% compared to 0.4–0.9%. The resulting litter was other elements: Cu 9.2 (3.7) leaves (wood), Fe 52 (28), Mn remarkably similar in nutrient levels compared to the other

© 2016 The Authors. Journal of Ecology © 2016 British Ecological Society, Journal of Ecology 18 P. A. Thomas three species although slightly lower in Mg, N and S. of ash have been found to variously contain coumarins (in- Although leaching loss per unit of leaf area is high, the lower cluding fraxin, fraxetin, scopoletin and to a lesser extent escu- leaf area held by trees resulted in the total loss of nutrients in lin), secoiridoids (mostly glucosides and esters of ash being comparatively low. Christiansen et al. (2010) in a hydroxyphenylethyl alcohols, including excelsioside), pheny- common garden experiment in west Denmark confirmed that lethanoid glucosides (including verbascoside and isoverbas- ash produced a low annual inorganic N throughfall coside), phenolic compounds (including oleuropein, (9.1 kg haÀ1). Soil N has been found to be similar to or ligstroside and olivil) and a number of flavonoids (Damtoft, higher than under other common deciduous species ranging Franzyk & Jensen 1992; Poukens-Renwart et al. 1992; Kos- from 30 to 108 kg haÀ1 (Dolle€ & Schmidt 2009; Christiansen tova & Iossifova 2007; Bai et al. 2010; Sanz et al. 2012). et al. 2010; Callesen et al. 2013). Soil C, however, at 2.0 t Carnat, Lamaison & Duband (1990) measured the following haÀ1 was comparable to Acer pseudoplatanus and Tilia cor- proportions of compounds in ash leaves (based on dry mass): data but low compared to Fagus sylvatica and Quercus robur mannitol 21.0%, phenolic acids 3.2%, tannin 2.5%, flavonoids (Christiansen et al. 2010). Litter from ash and Tilia spp. has 1.4%, rutoside 0.5%, and also mucilage 15.3% and an ash been shown to be easily decomposable and rich in nutrients, content of 9.6%. Young leaves contained more flavonoids particularly N, P, K, Mg and Ca (Norden 1994; Langenbruch, and less mucilage than older leaves. Concentrations of pheno- Helfrich & Flessa 2012; Vesterdal et al. 2012), promoting a lics in leaves, used as a UV protectant, have been seen to high return of base cations. increase with higher light intensity (Barthod, Cerovic & Ash has an improving effect on soil chemistry, including Epron 2007). Ash releases into the air comparatively low maintaining a higher soil pH and low concentration of Al ions levels of monoterpenes and isoprene that can be negative to compared to competitors such as A. pseudoplatanus and human health (Pokorska et al. 2012). Emissions were highest Q. robur (Hagen-Thorn et al. 2004; Mertens et al. 2007; Lan- in May (9.56 lg g dry massÀ1 hÀ1) and lowest in October genbruch, Helfrich & Flessa 2012; Cesarz et al. 2013). As an (1.17 lg g dry massÀ1 hÀ1). Ash emitted (Z)-b-ocimene, (E)- example, de Schrijver et al. 2012 working on abandoned agri- b-ocimene and a-farnesene during the entire measurement cultural soil in north Belgium found a decline in pH from 6.5 period and additionally isoprene only in May (Zemankova & to 4.5 under ash in 35 years, but this decline was less than Brechler 2010). Many of the compounds listed above have an below other tree species. Ash had the highest levels of soil Ca important medicinal role (see X). Fernandez de Simon et al. (reduced from 2500 to 1500 mg kgÀ1 under ash compared to (2014) list volatile compounds found in ash barrels important 400 mg kgÀ1 under Q. robur) and lowest levels of Al (in- in wine making. creased from c. 50 to 240 mg kgÀ1 under ash but was greater Mannitol is abundant in water-soluble bark extracts, and under other trees, reaching 530 mg kgÀ1 under Alnus gluti- planteose (13% dry mass) is the main soluble carbohydrate in nosa). The number and biomass of earthworms have also been seeds (Jukes & Lewis 1974). Phloem sap exuding from cuts in found to be highest under ash than under other tree species (de the bark contains a large number of sugars (collectively called Schrijver et al. 2012), reaching 11.6 Æ 4.7 g mÀ2 (SD) under manna in Mediterranean regions when this evaporates to a ash compared to 4.2 Æ 4.2 g mÀ2 under Q. robur (Neirynck solid, reflected in the abundant amount produced by the manna et al. 2000). Langenbruch, Helfrich & Flessa (2012) add that ash F. ornus). The manna has been measured as consisting of the presence of ash in F. sylvatica forests creates pockets of (all figures g 100 gÀ1): mannitol 39–48, fructose 9–16, glucose soil with a higher pH and higher cation, organic C and total N 2–3.7, sorbitol 0.5–06, galactose 0.02–0.74, oligosaccharides concentrations, increasing the horizontal and vertical diversity as mannotriose 13–22, stachyose 1–11 and traces of myoinosi- of the soil habitat. tol, mannose and sucrose (Caligiani et al. 2013). The pH tolerances of ash are given in II(B). Ash becomes chlorotic on very calcareous soils, and at the other end of the VII. Phenology pH scale, below pH <4, root development is suppressed by Al toxicity (at >100 lmol lÀ1) and Mn deficiency (Zollner & Inflorescence buds open in March to April before the leaves Kolling€ 1994; Weber-Blaschke, Claus & Rehfuess 2002; appear. Flowers on male trees open earliest and then her- Weber & Bahr 2000a; Kerr & Cahalan 2004). Root damage maphrodite trees followed by female trees last of all (Tal caused by Al can be reduced by adding extra Ca with Mg, 2011; Albert et al. 2013). Tal (2006) saw that flowers on but this does little to improve overall growth (Weber-Blas- male trees initially opened from large buds and then paused chke & Rehfuess 2002). so that the anthers were exposed but did not produce pollen for another 1–2 weeks. By contrast, inflorescences on hermaphrodites/female trees opened from smaller buds, gradually (F) BIOCHEMICAL DATA exposing the stigmas. In Germany, Tal (2006) noted that Fraxinus excelsior bark is composed of 32.5% cellulose, 20% flowering in forest trees started at the inner and bottom of the hemicellulose and 16.5% lignin (Buston & Hopf 1938) and canopy and progressed to the top and outer regions, while contains 25.8% hydrophilic extractives (as % dry mass) but Latorre & Bianchi (1998), investigating urban ash trees in negligible amounts of condensed tannins (Janceva et al. Argentina, found the opposite, that flowers at the top of the 2011). Gałuszka et al. (2011) give further details on the trees opened before those at the bottom opened after a lag of chemical composition of ash bark. The bark, leaves and seeds 2 weeks. This variation is undoubtedly due to the very differ-

© 2016 The Authors. Journal of Ecology © 2016 British Ecological Society, Journal of Ecology Fraxinus excelsior 19 ent growing conditions. Either way, the phased opening of and raffinose, possibly for increased drought tolerance (Jouve flowers helps to extend the overall flowering period to 3– et al. 2007) . 8 weeks, varying between years and location. Latorre & Bian- In the spring, seedlings expand the greater proportion of chi (1998) observed that in Argentina, pollen production their leaf surface before the canopy buds open and so com- occurred for 34 days with most being released over a 21-day plete most of their growth before the ‘dark phase’ of full period. Pollen production is related to spring temperatures. In summer sets in. In 1956, seedlings growing under a canopy Basel, Switzerland, it was found that a daily concentration of of ash started growth at the beginning of May, reached maxi- 30 ash pollen grains mÀ3 of air dayÀ1 was reached when the mum growth rate in the latter part of May and ceased grow- cumulative mean daily temperature (starting after the last day ing by the end of June (Wardle 1961). with minimum temperature ≤À2 °C) reached 214 °C (Peeters Being ring-porous, it is probable that the majority of large 2000) and when cumulated mean daily temperatures starting earlywood vessels at the start of the next spring are irre- on January 1 reach 220.7 °C (Peeters 1998). Ash stigmas are versibly embolized by winter freezing and ash thus relies on receptive as soon as they emerge from the bud scales and earlywood vessels grown in early spring to carry the bulk of remain so for about 2 weeks (Wallander 2001). the water (Haeke & Sauter 1996; Cochard et al. 1997). The Vegetative buds begin to swell in early March and open cambium becomes active in late March and xylem growth through May, although understorey trees usually begin earlier starts around 3 weeks before bud break, earlywood vessel and can have fully expanded leaves by the beginning of May maturation progressing basipetally down the branches and (Wardle 1961). Ash is determinate and all leaves are pre- stem before leaf emergence (Atkinson & Denne 1988; Sass- formed in the bud so expansion is rapid and is complete Klaassen, Sabajo & den Ouden 2011). The newly formed within c. 100 days, with formation of terminal buds in July outermost ring thus has the highest sap flux density, supply- and no further branch elongation for 9–11 months (Collin, ing the newly emerging leaves with the majority of their Badot & Millet 1995; Kerr 2002; Kerr & Cahalan 2004). water, although rings up to 27 years old were found to able However, in shoots that are physiologically young the buds to conduct some water by Gebauer, Horna & Leuschner can continue to form new leaves all through the summer, (2008). remaining green and succulent, and lacking protective scales Samaras are fully grown by the beginning of July, while and hairs (Wardle 1961). the enclosed seeds reach their full length by the beginning of Laube et al. (2014) looked at the triggers of spring bud August. The embryos grow until August or September. burst using material from southern Germany. They found that Viable seeds fall from September onwards, into the following ash did not have a long chilling requirement; chilling for March, the majority staying on the tree over winter (Kerr either 33 or 110 days (days with mean temperature <5 °C 1995). Most of the seeds lie on the ground for two winters after 1 November) resulted in bud burst c. 40 and 25 days, and finally germinate between mid-April and the end of May respectively, after bringing twigs into a growth chamber. By (Wardle 1961). Leaves are shed during October and the first comparison, the shorter chilling period did not trigger bud half of November, though a few persist into December (War- burst in either Fagus sylvatica or Acer pseudoplatanus. Pho- dle 1959; Grime, Hodgson & Hunt 2007). This is earlier than toperiod (from 8 to 16 hours of light per day) made no sig- many trees and gives a growing season of between 141 and nificant difference in timing of bud burst. Vitasse et al. 174 days, depending upon location and altitude (Le Goff & (2009c) looked at changes in the phenology of ash with alti- Ottorini 1996; Vitasse et al. 2009c); at low altitude, this is tude from 130 m to 1533 m in the French Pyrenees. Spring 44 days shorter than Quercus petraea (Vitasse et al. 2009c). leaf flushing started 2.9 Æ 0.4 (SD) days earlier at lower alti- Leaf fall can be somewhat earlier on polluted sites in or near tudes which was attributed to a sensitivity in ash to spring industrial centres. The leaves are still green when shed, temperature; leaf flushing began earlier by 6.6 Æ 0.4 days except under droughty conditions, when they turn yellow and °CÀ1. Vitasse et al. (2009c) concluded that in the French fall early. Vitasse et al. (2009c) found that autumn senes- Pyrenees, canopy duration of ash increased at lower altitude cence did not change with altitude and so must be more con- by 3.1 Æ 0.4 (SD) days 100 mÀ1 which converts to an trolled by day length than temperature. A similar result was increase in growing season by 6.9 Æ 1.0 days °CÀ1, primar- found for Acer pseudoplatanus, but both Fagus sylvatica and ily by altering spring bud burst. Vitasse et al. (2009a) also Quercus petraea started senescence earlier with altitude and found that when 1-year-old seedlings were grown in a com- so are more responsive to autumn temperatures. Seed mon garden at sea level, ash from the highest altitudes germination begins in January, peaking in early April flushed later at a rate of À1.9 days °CÀ1 while other species (Bourne 1945). such as F. sylvatica flushed earlier with altitude, suggesting that ash has greater protection from frost damage. Indeed, VIII. Floral and seed characters date of leafing of individual ash trees was found to be highly heritable, producing ecotype varieties with different degrees (A) FLORAL BIOLOGY of avoidance of spring frost (Kleinschmit et al. 2002). Later flushing varieties also showed reduced levels of putrescine A large amount has been written about the gender structure of (which is considered to confer stress tolerance) and increased ash trees that shows a continuum from pure male to pure levels of carbohydrates such as mannitol, sucrose, trehalose female trees with a variety of intermediate hermaphrodite

© 2016 The Authors. Journal of Ecology © 2016 British Ecological Society, Journal of Ecology 20 P. A. Thomas stages that can vary between years (Picard 1982; Binggeli & next year, 86% of trees showed the same sexual phenotype. Power 1991; Wallander 2001; Morand-Prieur et al. 2003; Males were least variable (171 of 174 trees remained male) Bacles et al. 2005; Albert et al. 2013). Binggeli & Power and female the least constant (21 of 27 staying the same). (1991) investigated a large number of flowers in Northern Ire- Gender appears to be under some degree of genetic control land (Table 1) and found more than half were male and only since Albert et al. (2013) found that clones grown in a seed 1.4% were female. However, many of the hermaphrodite orchard exhibited fairly stable gender phenotypes within each flowers were functionally female so overall 23.3% of flowers clone. Moreover, Tal (2006) found that male trees are consis- were functionally female, 8.8% hermaphrodite and 65.7% tently bigger, suggesting a constancy of gender. However, functionally male (the other 2.3% of flowers were non-func- there is some phenological variation since he also found a tional). In terms of whole trees, the proportions that were positive correlation between an increase in femaleness in a functionally one gender or another were slightly different: population and average minimum daily temperature in the 20.5% male, 68.1% hermaphrodite and 11.4% female, first half of April (the flowering period). although many trees contained flowers of more than one type. Ash is primarily wind-pollinated, and given 4–5 million The most remarkably detailed study of ash flowering was that flowers per tree (Tal 2006), it is not surprising that ash pollen of Tal (2006) who studied up to 91 trees in detail (averaging is an important seasonal allergen (Metz-Favre et al. 2010; 30 m tall and 59 cm dbh) over a 4-year period using the Feliu et al. 2013). The median pollen grain diameter from canopy crane in floodplain forest at Leipzig, Germany. Tal fresh dehisced anthers is 22.5 lm (Tal 2006) and so well found similar proportions to Binggeli & Power (1991). In the adapted to anemophily. Nevertheless, Tal (2006) in Germany male trees, the usually small pistils of hermaphrodite flowers found that the thrip Taeniothrips inconsequens Uzel (Thysa- were seen to wither in the cold weather accompanying anthe- noptera, Thripidae) and beetle Epuraea melanocephala (Mar- sis. In the polygamous hermaphrodite trees, apical flowers sham) (Coleoptera, Nitidulidae) were common in tended towards hermaphrodites and basal flowers towards inflorescences. Ash is known to have formed an important being female in female-biased trees. Males flowered every source of pollen for honeybees Apis mellifera L. (Hymenop- year at full intensity, whereas hermaphrodites/females skipped tera, Apidae) in February to mid-April in 1945 and 1946 at intensive flowering every 2–3 years (Tal 2006). He counted Rothamsted (Synge 1947) . Whether these insects visit both 9–82 fruits per infructescence, most on balanced hermaphro- male and female flowers frequently enough to act as pollinators dites (up to 750 000 fruits per tree) and female-based her- is open to question. Birds, in particular blue tits Cyanistes maphrodites, fewer on female trees, and male-based caeruleus (L.) (=Parus caeruleus L.), were observed in the hermaphrodites produced very few (<100 000 fruits per tree). inflorescences of all tree genders by Tal (2006). The median Tal (2006) suggests that hermaphrodite trees are functionally visit time per twig was between 2 and 6 seconds on different dioecious. Hermaphrodites are protogynous and self-pollina- dates; most visits were short but some lasted up to 25 seconds tion is physically possible (Morand-Prieur et al. 2003), but in for a single twig. One bird caught in 2005 on a female tree had natural populations, ash is preferentially outcrossed (FRAXI- 75 pollen grains of ash on c.1cm2 of its head, and thus birds GEN 2005), aided by the male fertility of hermaphrodite trees may act as effective, if low-key, pollinators. appearing to be much lower than that of male trees. Neverthe- Pollination is generally efficient since ash produces an less, the abundant pollen in hermaphrodite trees would seem excess of flowers, and unfertilized flowers are aborted before to account for their higher seed production over purely female fruits are produced (Tapper 1996b). Even so, Tal (2006) trees. found that 87% of ash stigmas had germinating pollen on The proportion of male and female flowers can vary from them (compared to 42% in Acer pseudoplatanus) with a med- year to year (Wardle 1961) but tends to stay fairly constant. ian of 10 germinating pollen grains per stigma (4 in A. pseu- Albert et al. (2013) found a similar sex ratio to Binggeli & doplatanus). Pollen tubes have been seen to start growing and Power (1991) in a French ash population in 2000, and the enter the style 24 h after pollination, reaching the style base within 2 days of pollination (Bochenek & Eriksen 2011). Fer- fi Table 1. Flowers of ash classi ed by their morphological type and tilization was delayed until after wilting of the stigma around fl their functionality, based on a total of 14 433 owers from Northern 3 weeks after pollination, but ovules were still fertilized by Ireland. Data from Binggeli & Power (1991) the first pollen grains to have landed on the stigma (Bochenek fl Flower morphology Flower functional type & Eriksen 2011). Pollen from male owers fertilized ten times more seeds compared to pollen from hermaphrodite Type % Type % flowers (Morand-Prieur et al. 2003). Tal (2006) found that <10% of fruits were empty except in Male 63.1 Male 62.3 > Non-functional 0.8 unusual years (in 2004 15% of fruits were empty in just two Hermaphrodite 35.5 Male 3.4 trees). Most fruits contain one seed, but Tal (2006) noted that Male + female 8.8 1-7% of the fruit per tree had two seeds and rarely some had Female 21.9 three seeds. The frequencies of empty fruit and of 2-seeded Non-functional 1.4 fruit are similar to that found by Gardner (1977) and interme- Female 1.4 Female 1.3 Non-functional 0.1 diate between Wardle (1959) who found more empty fruit and fewer double-seeded fruits and Hulden (1941) with more

2- and 3-seeded fruit. Gardner (1977) reports finding one seed flower until death at around 150–220 years old (Watt 1925; with all four ovules developing. The percentage of filled fruits Gatsuk et al. 1980; Kerr 1995; Bacles et al. 2005; Grime, is generally independent of the size of the total fruit crop Hodgson & Hunt 2007). Some seeds are usually produced (Tapper 1996b). each year although Chater (2010) studied 19 trees in Cardi- Tal (2006) also noted a massive gall infestation on male ganshire, mid-Wales (now Ceredigion) between 1975 and trees caused by the mite Eriophyes fraxinivorus (see IX(A)) 1993 and none fruited in 1976 and 1989. He also found no (called Aceria fraxinivorum by Tal, a misspelling of A. frax- ash fruits anywhere in Cardiganshire in 2005 and virtually inivorus Nalepa, now superseded by Eriophyes). Male trees none in the rest of Wales. However, ash produces mast years carried up to 15 kg of galls per tree, approaching the mass of of abundant seeds. Gardner (1977) suggested a biennial fruit production of female trees. Occasional galls were also masting pattern, but his evidence was limited and 2–5 years found on some hermaphrodite and female trees. Despite the is more usual (Harmer 1995; Kerr 1995) extending to 2– large gall mass, this seemed to have little effect on pollen 7 years in Sweden (Tapper 1992a,b). Low seed production production due to the large number of flowers held by each can be as low as 0.33 fruits mÀ2 in non-mast years in Der- male. byshire ashwoods (Gardner 1977) and up to 1100– Ash has been recorded as producing up to 140 000 seeds 1280 fruits mÀ2 in mast years (Gardner 1977; Tapper per tree annually (c. 10 kg) (Rohmeder 1949; Collin & Badot 1992a). Synchronicity between individuals may not be as 1997) or 1–1.5 million seed haÀ1 year À1 (Tal 2006). Samara close as in trees such as Quercus spp. or Fagus sylvatica fresh mass has been measured between 72 and 106 mg (Rackham 2003; Packham et al. 2012) although Blackstock (Grodzinski & Sawicka-Kaputa 1970; Tal 2006) and dry mass (2013) found masting to be synchronous between trees in 45.3–79.5 mg (Binggeli & Power 1991), size varying Wales and southern England. There is certainly some geo- between 33 and 46 mm long, 28 mm wide and 7–8 mm thick graphical variation in synchronicity. In Germany, Tal (2006) (Grime, Hodgson & Hunt 2007; Floran & Mihalte 2010; observed that most trees fluctuated in seed production S€aumel and Kowarik 2013;). Seed mass varied from 12 to between years, but this was not synchronous between trees, 46 mg in Britain (Gardner 1977; Binggeli & Power 1991; so overall the seed crop was fairly constant between years. Hulme & Borelli 1999) to 40–80 mg in Germany and Roma- However, Tapper (1992b) observed much more synchronicity nia (Floran & Mihalte 2010; S€aumel and Kowarik 2013). of flowering in Sweden that they attributed to a mechanism to satiate the seed eating moth larvae of Pseudargyrotoza conwagana (F.) (Lepidoptera, Tortricidae; see IX(A)) that (B) HYBRIDS did not occur at Tal’s study site. Tapper (1996b) looked at Fraxinus excelsior readily hybridizes and introgresses with 76 trees (55 female) over 14 years in Sweden and found that the closely related F. angustifolia in southern Europe (Raquin trees that leafed early in one year had a higher probability of et al. 2002a; Fernandez-Manjarres et al. 2006; Heuertz et al. fruiting the following year. But this seems unlikely to be 2006); the cross can happen both ways (Raquin et al. 2002a). due to resource storage/limitation since trees could fruit pro- Fraxinus angustifolia is expected to shift northwards with cli- lifically in successive years; for example, two trees fruited mate change, increasing contact with F. excelsior and increas- just once in 14 years and another produced abundant fruits ing hybridization (Hemery et al. 2010). Thomasset et al. in 13 of the years. Hulme & Hunt (1999) found seed preda- (2012) and Gerard et al. (2013) showed that in F. excelsior tion was density independent, so at all seed densities some planting stock introduced into Ireland, trees in different areas seeds would escape predation. However, Tapper (1992a) already showed genetic signs of potential hybrid origin with noted that the percentage of germinated seeds increased with F. angustifolia (28–58% were hybrids in Thomasset et al. increasing fruit crop during 1982–1986 in Sweden, further 2012). Most of these hybrids were cryptic and could help suggesting seed predator satiation as the mechanism behind explain the very variable performance of plantation ash in Ire- masting in ash. Within the masting pattern, the number of land. The introduced trees did not have a reproductive advan- seeds produced may be positively related to trunk diameter tage over native trees so hybrid genes will not be up to a certain limit after which seed production is largely preferentially spread (Thomasset et al. (2014). This hybrid is independent of size (Schmiedel 2010). This is complicated considered undesirable for forestry since F. angustifolia has since pure female trees may produce fewer or more seed poorer timber characteristics (Fernandez-Manjarres et al. than hermaphrodites (Binggeli & Power 1991; Tal 2006). In 2006). Artificially produced hybrids have been reported mast years, the width of annual growth rings is reduced between F. excelsior with F. americana and F. pennsylvanica (Bochenek & Eriksen 2010). (Santamour 1981). Artificial hybrids with Asian and Ameri- Immature fruits fall through the summer and some mature can ash species have the potential to provide F. excelsior with seeds drop in the autumn, but most of the viable seeds remain some resistance to ash dieback; see IX(C). on the tree through the winter (Wardle 1959), falling through the spring. The winged samara is primarily wind-dispersed. Fruits tend to travel a shorter distance compared to other (C) SEED PRODUCTION AND DISPERSAL winged fruits such as those of Betula spp. (McVean 1955) due Regular seed production starts at around 20–25 years in the to their larger size giving them a comparatively high vertical open and 30–40 years in closed forest, and trees will then velocity: 200 cm sÀ1 in ash compared to 107 cm sÀ1 in

‘maple’ (Levin & Kerster 1974). Dispersal distances follow a than recorded by Heuertz et al. (2003) was attributed to the log-normal distribution and Wagner (1997) recorded a mean more open nature of the fragmented wooded landscape facil- distance of 43.5 m, with 95% of fruits landing within 113 m of itating airborne pollen movement and alleviating the other- a single ash tree 130 years old and a dbh of 45.0 cm. However, wise detrimental genetic effects of population fragmentation. distance is obviously dependent upon wind speeds and topogra- In the open Irish landscape, Thomasset et al. (2014) found a phy, and distances of 125-180 m have been recorded (Wagner mean pollen spread of 260–382 m with a maximum (de- et al. 2004; Schmiedel & Tackenberg 2013), while Bacles, tected from tree parentage) of >4000 m. However, the rela- Lowe and Ennos (2006) recorded dispersal in deforested areas tive contribution of pollen and seeds to gene flow within of the Southern Uplands of Scotland in excess of 1.4 km with and between populations depends upon whether it is a mast occasional seeds travelling tens of kilometres. At the northern year (Bacles, Lowe & Ennos 2006; Bacles & Ennos 2008); end of its range, seeds are dispersed furthest by wind blowing in a mast year, seed dispersal is up to six times more effec- them across winter icy surfaces (Hulden 1941). tive in moving genes than pollen dispersal between frag- Praeger (1913) records that ash samaras floated in water for mented populations. 3 days. Schmiedel & Tackenberg (2013) investigated this in the laboratory using 50 samaras on a shaker to stop them (D) VIABILITY OF SEEDS: GERMINATION sticking to the side of the beaker and found that the first seeds sunk after 2 h, 50% were still floating after 12 h, only Germination is epigeal. When the fruit falls from the tree, a 10% after 24 h, but ‘some’ were still floating after 1 week. normal embryo is 7.5–8.5 mm long and occupies about half They drew the conclusion that 12 h would still allow seeds to the length of the seed. Before germination is possible, the move 44 km in a typical slow-moving European stream, and embryo must grow to the full length of the seed (Wagner 10% of the seeds would reach 76 km. S€aumel and Kowarik 1996). Blake, Taylor & Finch-Savage (2002) and Villiers (2013) released coloured seeds into two rivers around Berlin (1971) describe physical and hormonal changes inside strati- with flow rates of 0.1–0.2 m sÀ1 and 0.3–0.6 m sÀ1, respec- fied seeds associated with breaking embryo dormancy. In tively, and found that 25 Æ 6% (SD) and 30 Æ 3% of ash moist seeds at room temperatures (18–20 °C), embryos com- seeds reached 1.2 km downstream within 175 Æ 22 and plete their development within 14 weeks (Doody & O’Reilly 43 Æ 2 min, respectively, in the two rivers. 2011). The rate of growth is not affected by previous low Studies throughout Europe have shown that F. excelsior temperature treatment, but is significantly accelerated by populations show a low genetic differentiation among popula- removal of the indehiscent pericarp that has been suggested to tions (and thus high inbreeding; inbreeding coefficient, be impermeable to oxygen (Villiers & Wareing 1964) and

FIS = 0.064; Heuertz et al. 2004b) but with a high nuclear will delay embryo growth during the first winter. The endo- genetic diversity (Morand et al. 2002; Heuertz et al. 2004a,b; sperm and seed coat also physically constrain the radicle; the Nowakowska et al. 2004; Bacles et al. 2005; Ferrazzini, strength of these tissues declines during cold stratification Monteleone & Belletti 2007; Sutherland et al. 2010; Wester- independently of embryo growth (Finch-Savage & Clay gren et al. 2012; Beatty et al. 2015). In 42 British and 6 1997). Bourne (1945) attributed the high germination of ash French sites, Sutherland et al. (2010) found that allelic rich- in the spring of 1945 (despite low seed production for the ness increased from east to west attributed to pollen move- previous 6 years) to the very hard frosts in December 1944 ment. In Germany, Hebel, Haas & Dounavi (2006) found cracking the seed coat. Once the embryo is nearing maturity, high genetic diversity and also high gene flow/low levels of actual germination still does not occur until the seeds have inbreeding possibly due to human movement of trees between experienced prolonged low temperatures. Villiers & Wareing provenances. More isolated or fragmented populations, how- (1965a,b) found that this dormancy is due to production of a ever, maintain high levels of genetic differentiation between germination inhibitor by the endosperm, embryo and pericarp populations. Holtken,€ T€ahtinen & Pappinen (2003), for exam- and that it is broken by storage at 3–5 °C, due to production ple, investigated ash at the northern end of its range on an of a germination stimulator by the embryo. Without chilling, island archipelago in south Finland and found that increasing no germination takes place; Villiers (1972) reports keeping isolation (up to 15 km between populations) and decreasing unchilled, fully imbibed for over 6 years without any germi- population size resulted in almost no gene flow between pop- nation. The general prescription for breaking dormancy is ulations, leading to decreased genetic variability and increased moist warmth (15–20 °C) for 12–16 weeks followed by moist population differentiation. This was undoubtedly a result of cold (2–5 °C) for another 12–16 weeks (Tylkowski 1990) restricted pollen flow. Heuertz et al. (2003) modelled pollen although Doody & O’Reilly (2011) found that germination and seed movement based on genetic variation between popu- increased as the duration of warm conditions increased up to lations and found the mean distance of pollen movement was 18–30 weeks, further releasing the embryo chemically and <140 m and seed movement <14 m. Going further, spatial physically. Seeds from areas with cold winters need a longer paternity analysis in southern Scotland by Bacles & Ennos period of warm and cold stratification to break dormancy (2008) suggested that 85% of detected pollination occurred (Farcas 2000). With climate change, chilling requirements within 100 m and 15% between 300 and 1900 m although may not be met, even at the northern end of its range. Fur- comparison of remote population fragments indicates that pol- thermore, high spring temperatures can induce secondary ther- len dispersal up to 2900 m was possible. The greater distance mal dormancy (Piotto 1994). Seeds can be stored in liquid

© 2016 The Authors. Journal of Ecology © 2016 British Ecological Society, Journal of Ecology Fraxinus excelsior 23 nitrogen for at least 2 years if dried to 4-6% moisture and very successful; in a survey of woodlands in southern Eng- while dormant (Chmielarz 2009). land, Harmer, Kerr & Boswell (1997) found mean seedling Van de Walle (1987) found that germination would start densities of >10 000 haÀ1. during cold stratification after approximately 14 weeks and reach completion by 33 weeks. This could be prevented by (E) SEEDLING MORPHOLOGY stratifying seeds at a lower moisture content (À1.5 MPa over sulphuric acid) and then, when allowed to germinate, germina- Germination begins by the radicle protruding into the soil. The tion would be much more uniform. Seeds will germinate when hypocotyl elongates rapidly to a length of 5–6 cm, forcing the submerged in water as completely as in soil although a little seed and enclosed cotyledons above the ground. As the cotyle- slower, as befits a plant capable of growing in river bottoms dons expand, they rupture the seed coat and then shed it; they (Dacasa Rudinger€ & Dounavi 2008). In vitro germination of are now yellowish and pressed together, 2.5–4 cm long. The isolated embryos allows a rapid method of germination with seedlings can reach this stage of development in the dark high germination results (Raquin et al. 2002b). A mineral-rich (Wardle 1961). Light is necessary for further development, in agar supplemented with sucrose and gibberellic acid gave the which the cotyledons open out and become green, the terminal highest germination although the more mature the embryo, the bud enlarges, and the first foliage leaves unfold. At the same less difference seen between media (Wagner & Kafka 1995). time, the first lateral roots appear on the upper part of the radi- Seed emergence stops in southern England once soil tempera- cle (Fig. 4). The first foliage leaves are unifoliate, but succes- ture is >25 °C (Jinks, Willoughby & Baker 2006); maximum sive pairs become compound with 3–7 leaflets from the second germination occurs at 10 °C under constant temperature. season in vigorous plants (Gatsuk et al. 1980). The leaves of Seeds subjected to normal outdoor temperatures germinate suppressed seedlings may not progress beyond the trifoliate in the spring, mostly after stratification for two winters, but a stage for many years (Wardle 1961). Seedling relative growth proportion (usually <5%) germinate after the first winter, both rate has been measured at <0.5 g dry mass weekÀ1 (Tapper in soil and in vitro (Wardle 1961). Under natural conditions, 1992a) and Oliver (1998) reported some seedlings growing seedlings can be expected to appear in especially large num- 0.5–1.0 m per year after the second year. bers in the second spring following a good seed year. Ash does not form a persistent soil seed bank beyond the time IX. Herbivory and disease taken to meet dormancy requirements (Poschlod & Jordan 1992; Jezdrzejczak 2013) although Puchner (1922) states that (A) ANIMAL FEEDERS OR PARASITES the seeds are capable of lying dormant in the ground for up to 6 years. This short-lived seed bank would aid rapid colo- Mammalia nization of woodland gaps, but the main strategy of ash is to form a seedling bank. The main reason for low germination Deer readily browse ash, particularly red (Cervus elaphus L.), in the field and short duration of the soil seed bank is that roe (Capreolus capreolus L.) and muntjac deer (Muntiacus seeds are readily consumed by small mammals (Gardner reevesi Ogilby) and moose (Alces alces L.) (Gezbcynska 1980; 1977), but to a lesser extent seed is lost to predation by the Cooke 1998; Chevallier-Redor et al. 2001; Cooke & Farrell moth Pseudargyrotoza conwagana (F.) (Lepidoptera, Tortrici- 2001). The smaller deer also frequently rub the bark from dae). Eggs are laid in the developing seed and the resulting saplings (Wardle 1961). Red deer readily browse ash in pref- larvae feed upon the endosperm and then emerge in autumn, erence to Salix caprea in mainland Europe (Gezbcynska 1980; leaving a characteristic hole in the testa and pericarp (Kloet & Chevallier-Redor et al. 2001) although Pepin et al. (2006) in À Hincks 1972). In 1954 and 1955, Wardle (1959) found that a Swiss enclosure with high deer density (15 hinds km 2) 9–66% of seeds had been killed by the moth, 9–39% were found Salix caprea was more browsed and mortality was underdeveloped, and 18–82% were viable. Gardner (1977) in higher than in ash. European bison (Bison bonasus L.) eat the Derbyshire ash woods found losses of 15–36% per year to shoots and leaves of ash in Poland, which along with Salix the moth (the smallest percentage in mast years) and another caprea and Populus tremula, are the most preferred trees 49–75% of seeds were lost to small mammals. (Borowski, Krasinski & Miłkowski 1967). Sheep more readily Seed viability can reach 95% (Villiers 1972), but emer- graze ash than Quercus spp. (McEvoy & McAdam 2008), gence (for the reasons above) is usually much lower. For and pollarding to produce foliage for cattle has been common example, Tapper (1992a) recorded that in Sweden the number in mainland Europe for centuries (Machatschek 2002). of seedlings represented 1.1–24.5% of fruit production Small mammals, particularly the woodmouse (Apodemus 2 years before. However, subsequent survival can be very sylvaticus L.) and bank voles (Myodes glareolus Schreber), high; Tapper (1992a) saw that 94.9% of the 735 germinated kill some seedlings by cutting the roots while tunnelling seedlings survived to produce true leaves. Seedlings are sus- (Wardle 1961; Kerr 1995) and by bark removal of saplings ceptible to late spring frosts, damping off in moist shade and <5 years old (Borowski 2007), and they eat significant num- desiccation in shallow soils (Wardle 1959). Wardle also bers of seeds that are on the ground (Flowerdew & Gardner records that on ‘stiff clay soil’, the hypocotyls can split or 1978). Wardle (1959) found that of 50 seeds exposed in even break due to resistance to raising the cotyledons and 325 cm2 plots, 49 were eaten when allowing in all small enclosing seed coat from the soil. But regeneration can be mammals, 43 when just small rodents could get in, and 5

Fig. 4. Seedlings of Fraxinus excelsior at various stages of growth. A seedling of Acer pseudoplatanus (a) is shown for comparison. Material was collected from Buff Wood and Harlton Cambridgeshire. Drawings by C.D. Pigott, taken from Wardle (1961). Scale: x½. when only birds and squirrels could get in. None were tive matter with whole fruits having a calorific content of removed when only earthworms and insects had access. Nev- 5259 calories gÀ1 dry mass, fairly average for deciduous ertheless, when given a choice of species, Hulme & Hunt trees. (1999) found that the woodmouse had a marked preference for Taxus baccata and Ulmus spp. over ash, Ulmus being Acari preferentially taken even when rare. The lower preference for ash may have been due to their high phenolic content (Hulme Five species of eriophyid mites (Acari, Eriophyidae) have & Borelli 1999). Hulme & Hunt (1999) observed that preda- been recorded on ash in the Database of Insects and their tion of seed by small mammals in north-east England wood- Food Plants (DBIF 2015). Eriophyes fraxini (Karpelles) and lands was density independent; the same proportion was eaten E. fraxinivorus Nalepa cause galls on the flower and fruit irrespective of seed density or frequency. Bank voles will pedicels, while E. fraxinicola (Nalepa) causes galling of damage the bark of ash, but ash is less susceptible than many leaves (Scannell 2008; Alford 2012). Wardle (1961) notes other common trees (Pigott 1985). Seedlings can be killed by that E. fraxini is not common, but infected trees usually have moles (Talpa europaea L.). Ash seems to be resistant to most all their inflorescences attacked. Phyllocoptes fraxini Nalepa commercial insecticides and rodent repellents (e.g. Gosling & causes galling by the rolling of leaf margins inwards. All Baker 2004). these mites are specifictoFraxinus excelsior except E. frax- Ash bark is readily eaten by hares and rabbits in winter, inivorus that has also been found on other Fraxinus species but after several years of such browsing, they recover better (DBIF 2015). The ash rust mite Aculus epiphyllus (Nalepa), than Fagus sylvatica (Watt 1925). However, compared with found primarily on F. excelsior but also Sambucus and Alnus many other broadleaves, ash is comparatively immune to grey species, causes bronzing of ash foliage and in severe cases squirrels, Sciurus carolinensis Gmelin (Kerr 1995; Oliver causing the shoot tips to blacken and die, leading to forking 2009; Rackham 2014). On the other hand, ash is a preferred (Alford 2012). Due to the forking, this can be a serious pest species for felling by beavers (Castor fiber L.) in eastern Eur- of commercial nurseries. ope. In the Czech Republic, out of 14 species used by beaver, ash with a diameter of 1–10 cm formed 41% of trees used Insecta (Urban, Suchomel & Dvorak 2008). Southwood (1961) recorded 41 species of insect associated with F. excelsior and concluded that ash, along with Corylus Aves avellana, Ilex aquifolium and Taxus baccata, have ‘remark- Ash seeds, and to a lesser extent buds, can form a major ably few associated insects’. Table 2 lists just over 100 insect part of the diet of bullfinches (Pyrrhula pyrrhula L.) in species associated with ash in Britain. Britain (Newton 1967). They take large numbers of seed, Ash supports a wide range of Homopteran bugs, particu- stripping some trees bare but ignoring those trees that have larly psyllids (Hemiptera, Homoptera, Psyllidae) that are seeds with low lipid and high phenolic concentrations found solely on ash or in some cases other Fraxinus species; (Greig-Smith 1988). Bullfinches drop small seeds, particu- Psyllopsis discrepans is common in the north of Britain, larly at the start of winter when they eat only half the fruits P. fraxini and P. fraxinicola in the Midlands, all inducing they pluck, and so may aid dispersal, especially as some galls on leaves and buds (Wardle 1961). Psyllopsis repens dropped seeds are split which helps release them from dor- Loginova has been recorded on ash for the first time from mancy (Greig-Smith 1988). Grodzinski & Sawicka-Kaputa Europe in Serbia (Malenovsky & Jerinic-Prodanovic 2011). (1970) found that 55% of the dry mass of fruits was nutri- The apple or maple mealybug Phenacoccus aceris (Signoret)

(Hemiptera, Homoptera, Pseudococcidae) can be a serious implicated in the formation of some cankers (Wardle 1961). pest of ash (Kaydan, Kilincer & Kondo 2015). Ash also sup- The European red click beetle Elater ferrugineus L. (Coleop- ports a number of capsid bugs (Hemiptera, Heteroptera, Miri- tera, Elateridae) is associated with wood mould in old hollow dae), but none is known to cause serious problems. The scale deciduous trees, primarily Quercus spp. but also a number of insect Chionaspis salicis L. (Hemiptera, Homoptera, Diaspidi- less important hosts including ash (Allen 1966). The saprox- dae) can affect a wide range of hosts including ash, forming ylic beetle Prionychus ater (Fabricius) (Coleoptera, Tenebri- heavy encrustations that can affect the growth of young trees onidae) has been found to be strongly associated with hollow (Alford 2012). Kaydan et al. (2006) list parasitoids and ash in south-east Sweden (Milberg et al. 2014). Johansson predators of mealybugs (Hemiptera, Homoptera, Coccidae) on (2011) lists other saproxylic beetles found in ash in south-east ash in Turkey. Sweden. The ash bud moth Prays fraxinella (=Prays curtisellus A small number of flies are dependent upon the ash. Most Don.; Lepidoptera, Yponomeutidae) is one of the main herbi- notable are three gall-forming species specific to ash: Dasy- vores of ash. Up to 26% of leaf and flower buds have been neura fraxinea (Diptera, Cecidomyiidae) that produces thick- seen to be damaged by this mining micromoth (Foggo & ening of leaflets, D. fraxini (=Perrisia fraxini Kieffer) that Speight 1993) which mines leaves during late summer, but causes galls on midribs and petioles, and D. acrophila overwinters at the base of the buds (Wardle 1961). It prefers (=P. acrophila Winn.) that raises pustules on leaves (Skrzypc- terminal buds (Foggo 1996) and so can cause reduced height zynska 2002). growth and, commercially more important, is one of the most important causes of forking (Kerr & Boswell 2001). Accord- Others ing to Gent (1955), seedlings below 0.6 m tall and shoots above 4.5 m are not attacked. Damage from this moth is The European hornet Vespa crabo L. (Hymenoptera, Vespi- likely to become more common with climate change due to dae) is known to cause occasional damage to the bark ash reduced winter mortality (Broadmeadow & Ray 2005). The stems while collecting material for nest building (Hempel & larvae of Pseudargyrotoza conwagana (F.) (=Argyotoza con- Wilhelm 1897, reported in Wardle 1961). Ash wood is very wayana Fabr.; Lepidoptera, Tortricidae) are found inside ash susceptible to various European termites including Reticuliter- seeds and so greatly reduce the number of viable seeds (War- mes banyulensis (Clement) (Isoptera, Rhinotermitidae) in dle 1959). In late autumn, they emerge to pupate and leave a Spain, even when the wood has been thermally treated which characteristic hole in the carpel (Wardle 1961). The main protects the timber of other trees (Oliver-Villanueva, Gascon- food plant of this moth is ash although it can be found also Garrido & de Sales Ibiza-Palacios 2013), and Indian termites on Ligustrum vulgare. Euphydryas maturna (L.) (Lepidoptera, such as Odontotermes horni (Wasmann) (Isoptera, Termiti- Nymphalidae) is a vulnerable species of high conservation dae) (Shanbhag & Sundararaj 2013). The nematode Meloidig- value, listed in the Habitats Directive of the European Union; yne sp. (Nematoda, Tylenchida) causes nodules on the roots it lays its eggs almost exclusively on ash in Italy and Ger- of plants of any age, particularly on sandy soils, but trees many (Freese et al. 2006; Dolek et al. 2013). show no obvious ill effects (Wardle 1961). Ash has relatively The emerald ash borer, Agrilus planipennis Fairmaire low palatability to the snail Cornu aspersum (Muller)€ (Gas- (Coleoptera, Buprestidae), a native to Asia, has killed millions tropoda, Helicidae, =Helix aspera) (Wratten, Goddard & of ash trees in North America since 2002. It was recorded in Edwards 1981) and Wardle (1961) records that slugs (Gas- Moscow in 2003 and is now moving west into Europe (Bar- tropoda) killed a negligible number of seedlings. anchikov et al. 2008; Orlova-Bienkowskaja 2014) and is sus- pected to be present in Sweden (Dobrowolska et al. 2011). (B) PLANT PARASITES AND EPIPHYTES Fraxinus excelsior is susceptible (Pureswaran & Poland 2009) and this beetle is set to become the biggest problem faced by In western Scotland, Bates (1992) found 30 species of ash in Europe, far more serious than ash dieback. The adults lichens, 21 bryophytes and 2 vascular plant epiphytes (Oxalis feed on ash leaves doing comparatively little damage; the acetosella and Hymenophyllum wilsonii), a total of 53 species trees are killed by the bark-boring larvae. compared to 67 on Quercus petraea. Bates & Brown (1981) On a lesser scale, the ash weevil Stereonychus fraxini (De did a similar comparison in south-west England and found 54 Geer) (Coleoptera, Curculionidae) affects leaves (Lemperiere species of bryophytes, lichens and non-lichenized fungi on & Malphettes 1983) in mainland Europe, and it has been ash bark, slightly more than Q. petraea in this case. Davies suggested that root damage to hedgerow ash trees, caused by et al. (2007) recorded 74 lichen, 14 moss, seven fungal and agricultural machinery, renders the trees more susceptible to three algal species on the bark of ash in London, while Moe the ash weevil via a reduction in leaf toughness (Foggo, & Botnen (1997) found 84 lichen, 72 bryophyte and 17 vas- Speight & Gregoire 1994). The large pine weevil Hylobius cular plant species in western Norway. Moe & Botnen (1997) abietis (L.) (Coleoptera, Curculionidae) although primarily a and Martin (1938) describe the zonation of epiphytes up ash conifer-feeding pest has been seen to feed on ash in Scandi- trunks. Rackham (2014) suggested that ash supports a larger navia but with a much lower preference than for Betula pen- bryophyte flora than Quercus spp. but less than Sambucus dula (Mansson & Schlyter 2004). Hylesinus fraxini (Panzer) nigra; in lowland England, he reported that ash had a similar (Coleoptera, Curculionidae) is a bark beetle that has been bryophyte flora to Acer spp. and in the north and west ash

Table 2. Insects recorded from Fraxinus excelsior in Britain. Data taken from the Database of Insects and their Food Plants (DBIF 2015)

Species/classiﬁcation Ecological notes

Hemiptera Asterolecaniidae Asterodiaspis minus (Lindinger) Larvae and adults; branches; mostly on Quercus Cicadellidae Empoasca vitis (Gothe) Larvae feeding; leaves; wide range of hosts Lamprotettix nitidulus (F.) Unspecified feeding Coccidae Parthenolecanium corni (Bouche) Scale on leaves and stems; very wide range of hosts Diaspididae Chionaspis salicis (L.) Larvae and adults; branches; wide range of hosts Lepidosaphes conchyformis (Gmelin in L.) Introduced; wide range of hosts L. ulmi (L.) Most tree parts; wide range of hosts Pseudaulacaspis pentagona (Targioni) Larvae and adults; leaves and stems Quadraspidiotus zonatus (Frauenfeld) Leaves and stems; wide range of hosts Eriococcidae Pseudochermes fraxini (Kaltenbach) Larvae and adults; bark; primarily on ash Miridae Orthops cervinus (Herrich-Schaffer) Larvae and adults; flowers, fruits and seeds Orthotylus nassatus (F.) Unspecified feeding O. tenellus (Fallen) Larvae and adults; flowers Phytocoris populi (L.) Larvae and adults; bark P. tiliae (F.) Partly predaceous Psallus flavellus Stichel Unspecified feeding on ash P. lepidus (Fieber) Unspecified feeding on ash Pseudoloxops coccineus (Meyer-Dur) Unspecified feeding on ash; rare Pemphigidae Prociphilus bumeliae (Schrank) Larvae and adults; small branches and buds; only on ash P. fraxini (F.) I Larvae and adults; bark and buds; only on ash Pseudococcidae Phenacoccus aceris (Signoret) Unspecified feeding; wide range of hosts Psyllidae (Psylloidea) Psyllopsis discrepans (Flor) Larvae; only on ash P. distinguenda Edwards Larvae; only on ash P. fraxini (L.) Larvae; only on ash P. fraxinicola (Forster) Larvae; only on ash Tenthredinidae Macrophya punctumalbum (L.) Larvae; leaves; mainly ash and Ligustrum Tenthredo livida L. Larvae; wide range of hosts Tomostethus nigritus (F.) Larvae; leaves; only on ash Lepidoptera (butterflies) Lycaenidae Quercusia quercus (L.) Larvae; flower and leaf buds Strymonidia w-album (Knoch) Larvae; flower and leaf buds, leaves; mainly on Ulmus Lepidoptera (macromoths) Cossidae Cossus cossus (L.) Wood boring larvae Zeuzera pyrina (L.) Wood boring larvae in branches Geometridae Apeira syringaria (L.) Larvae Campaea margaritata (L.) Larvae Cepphis advenaria (Hubner) Larvae Chloroclysta siterata (Hufnagel) Larvae Colotois pennaria (L.) Larvae; leaves Ennomos fuscantaria (Haworth) Larvae on ash and Ligustrum E. quercinaria (Hufnagel) Larvae; leaves Epirrita dilutata (Denis & Schiffermuller) Larvae; leaves Eupithecia exiguata (Hubner) Larvae E. fraxinata Crewe Larvae; flowers E. innotata (Hufn.) Larvae Lycia hirtaria (Clerck) Larvae; leaves Menophra abruptaria (Thunberg) Larvae; leaves

(continued)

Table 2. (Continued)

Species/classiﬁcation Ecological notes

Phigalia pilosaria (Denis & Schiffermuller) Larvae; leaves Plagodis pulveraria (L.) Larvae Selenia lunularia (Hubner) Larvae S. tetralunaria (Hufnagel) Larvae Trichopteryx polycommata (Denis & Schiffermuller) Larvae Lasiocampidae Poecilocampa populi (L.) Larvae, leaves Noctuidae Agrochola circellaris (Hufnagel) Larvae; flowers, fruits, seeds Amphipyra pyramidea (L.) Larvae; leaves Atethmia centrago (Haworth) Larvae; leaf and flower buds, leaves; only on ash Brachionycha nubeculosa (Esper) Larvae on leaves; wide range of hosts B. sphinx (Hufnagel) Larvae on leaves; wide range of hosts Craniophora ligustri (Denis & Schiffermuller) Larvae Dichonia aprilina (L.) Larvae and adults; leaf and flower buds, flowers and leaves Lithophane hepatica (Clerck) Larvae; wide range of hosts L. semibrunnea (Haworth) Larvae Orthosia munda (Denis & Schiffermuller) Larvae Trigonophora flammea (Esper) Larvae Sphingidae Acherontia atropos (L.) Larvae on leaves; migrant; wide range of woody and herb. Hosts Sphinx ligustri L. Larvae Lepidoptera (micromoths) Coleophoridae Coleophora trigeminella Fuchs Larvae mining leaves Gracillariidae Caloptilia syringella (F.) Larvae mining and rolling leaves Oecophoridae Oecophora bractella (L.) Dead wood, bark; rare Semioscopis steinkellneriana (Denis & Schiffermuller) Larvae webbing Pyralidae Euzophera pinguis (Haworth) Larvae; live bark Tortricidae Archips crataegana (Hubner) Larvae rolling leaves Pammene suspectana (Lienig & Zeller) Larvae; bark Pandemis corylana (F.) Larvae webbing Pseudargyrotoza conwagana (F.) Larvae; fruits and seeds, webbing Tortrix viridana (L.) Larvae; leaf buds and leaves; wide range of hosts Yponomeutidae Prays fraxinella (Bjerkander) Larvae mining in leaves and shoots; only on ash Zelleria hepariella Stainton Larvae; shoots and leaves, webbing; only on ash Coleoptera Anthribidae Platyrhinus resinosus (Scopoli) Dead wood boring larvae; on a variety of trees Cerambycidae Saperda populnea (L.) Galling on small stems; mostly Salicaceae Tetrops starkii Chevrolat Wood boring larvae; restricted to ash Chrysomelidae Psylliodes cuprea (Koch, J.D.W.) Feeding adults; mostly on herbs, particularly Brassicaceae Curculionidae Acrantus vittatus (F.) Larvae and adults; bark; mostly on Ulmus spp. Coeliodes rubicundus (Herbst) Larvae on flowers; also on Betula and Alnus Hylesinus crenatus (F.) Larvae and adults; bark; wide range of deciduous trees H. oleiperda (F.) Larvae and adults; bark and small branches; particularly in Oleaceae Leperisinus varius (F.) Larvae and adults; bark and wood Mesites tardii (Curtis) Wood boring larvae; wide range of trees Otiorhynchus niger (F.) Larvae; roots; including conifers Scolytus scolytus (F.) Larvae and adults; bark and wood; rarely on ash Xyloterus domesticum (L.) Larvae and adults; bark and wood; wide range of host trees

(continued)

Table 2. (Continued)

Species/classiﬁcation Ecological notes

Elateridae Ampedus cardinalis (Schioedte) Larvae; wood; commonest on Quercus Elater ferrugineus L. Old hollow trees Lucanidae Dorcus parallelipipedus (L.) Larvae; wood Lucanus cervus (L.) Larvae; wood of trunk and roots; wide range of tree hosts Melandryidae Abdera biﬂexuosa (Curtis) Associated with dead wood in ash and Quercus Meloidae Lytta vesicatoria (L.) Feeds on ash and Ligustrum Platypodidae Platypus cylindrus (F.) Larvae and adults; bark and wood; wide range of hosts Salpingidae Lissodema cursor (Gyllenhal) One record on ash L. quadripustulata (Marsham) Feeding on dead branches Tenebrionidae Corticeus bicolor (Olivier) Feeding on fungal bodies on ash? Diptera Agromyzidae Paraphytomyza heringi (Hendel) Leaf miner on ash Cecidomyiidae Contarinia marchali Kieffer Larvae; fruits and seeds of ash Dasineura acrophila (Winnertz) Galling on ash D. fraxinea Kieffer Galling on ash D. fraxini (Bremi) Galling on ash Thysanoptera Thripidae Oxythrips halidayi Bagnall Larvae and adults; leaves

resembles Acer pseudoplatanus, and ash is the main habitat In Sweden, lichen species diversity was found to be positively of Isothecium alopecuroides (Lam. ex Dubois) Isov., Homalia related to trunk diameter up to 65 years of age (Johansson, trichomanoides (Hedw.) Schimp. and Neckera complanata Rydin & Thor 2007). In Estonia, Jȕriado et al. (2009) identi- (Hedw.) Hub.€ Ash was considered favourable due to its fied 70 species of lichen on ash, more than other major forest higher bark pH (4.84–5.39) but oak bark, being rougher, held trees. water for longer (Bates 1992; Jȕriado et al. 2009; Steindor A full list of the 1856 fungal species so far known to be et al. 2011). associated with ash in Britain and Ireland can be found on Ellis, Coppins & Hollingsworth (2012) and Ellis et al. the Fungal Records Database (British Mycological Society (2013) identified 536 species of lichen epiphytic on ash in the 2016). Those fungal species directly associated with ash are UK (approaching a quarter of the British total – Rackham given in Table 3. Chen (2012) listed 90 fungal species found 2014). These included 84 threatened species, most notably on ash in New Zealand, and Griffith & Boddy (1991a,b, Fuscopannaria ignobilis (Anzi) P.M. Jorg.€ (Ascomycota, 1998) describe the succession of fungi on dead attached ash Peltigerales) and Wadeana dendrographa (Nyl.) Coppins & branches. P. James (Ascomycota, Incertae sedis) and also including 3 Scholtysik et al. (2013) listed 50 species of endophytic critically endangered, 9 endangered, 20 vulnerable and 52 fungi in leaves of ash in central Germany, the commonest near-threatened species (Woods & Coppins 2012). Only two being Alternaria alternata (Fr.) Keissl. and Lewia infectoria species are more common on ash than on other trees: (Fuckel) M.E. Barr & E.G. Simmons (=Alternaria infectoria Lithothelium phaeosporum (R.C. Harris) Aptroot (Ascomy- E.G. Simmons) (Ascomycota, Pleosporales). One of the cota, Pyrenulales) and Thelenella modesta (Nyl.) Nyl. commonest Ascomycetes causing decay of dead ash wood is (Ascomycota, Incertae sedis), the last being on just one tree Daldinia concentrica (Bolton) Ces. & De Not. (Xylariales) (Rackham 2014). A number of lichenized fungi are included though it also occurs occasionally on F. sylvatica in the south in Table 3. Ash is an important habitat for commoner species and commonly on Betula spp. in the north (Whalley & following the decline of large elms since both have a compar- Watling 1980). Johannesson, Ihrmark & Stenlid (2002) atively alkaline bark. In mainland Europe, Jonsson€ & Thor showed that this fungus is not any better at invading ash (2012) found 174 species of lichen epiphytic on ash on the wood than other substrates, and its commonness may be due island of Gotland in southern Sweden and modelled that ash to the fungus spreading readily through the ash wood xylem dieback would result in a likely loss of 38% of lichen species. (Boddy, Gibbon & Grundy 1985). Hysterographium fraxini

Table 3. Fungi (by Order) directly associated with Fraxinus excelsior Table 3. (Continued) not including those found on soil or litter below the trees, or those found solely on dead wood/bark. Details of these can be found in the Species/classification Ecological notes Fungal Records Database of Britain and Ireland (British Mycological Society 2016) Hypocreales Clonostachys compactiuscula (Sacc.) Twigs Species/classification Ecological notes D. Hawksw. & W. Gams Gibberella baccata (Wallr.) Sacc. Frost damaged buds Ascomycota G. pulicaris (Fr.) Sacc. Fallen samaras Arthoniales Gliocladium sp. Corda Fallen samaras Arthonia punctiformis Ach. Bark, lichenized Nectria fuckeliana C. Booth Dead shoots A. radiata (Pers.) Ach. Bark, lichenized N. galligena Bres. Living trunk and Enterographa crassa (DC.) Fee Bark, lichenized branches Opegrapha herbarum Mont. Bark, lichenized Trichothecium roseum (Pers.) Link Bark, lichenized O. prosodea Ach. Bark, lichenized Hysteriales Calosphaeriales Hysterium angustatum Alb. & Schwein. Bark Lecanactis abietina (Ehrh. ex Ach.) Bark, lichenized Volutella ciliata (Alb. & Schwein.) Petioles Korb.€ Fr. Botryosphaeriales Incertae sedis Dothiorella fraxinea Sacc. & Bark, attached twigs Aposphaeria sp. Berk Canker Roum. Arthrinium phaeospermum (Corda) Inner bark, twigs Candelariales M.B. Ellis Candelariella reflexa (Nyl.) Bark, lichenized Asteromella sp. Pass. & Thum.€ Fading leaves Lettau Bactrodesmium obovatum (Oudem.) Bark C. xanthostigma (Pers. ex Ach.) Bark, lichenized M.B. Ellis Lettau Chaenotheca ferruginea (Turner) Trunk, lichenized Capnodiales Mig. Mycosphaerella tassiana Fallen samaras Coleophoma cylindrospora (Desm.) Petioles (De Not.) Johanson Hohn.€ M. fraxini (Niessl) Lindau Live leaves Colletotrichum dematium (Pers.) Fr. Samaras Coronophorales Cryptocoryneum hysterioides Twigs Coronophora angustata Fuckel Living roots (Corda) Peyr. Diaporthales Psammina stipitata D. Hawksw. On green coccoid Diaporthe samaricola Samaras algae, live trunk, W. Phillips & Plowr. lichenized Dothideales Sclerophora peronella (Ach.) Tibell Bark, lichenized Aureobasidium pullulans Seeds Strigula taylorii (Carroll ex Nyl.) Bark, lichenized (de Bary & Lowenthal)€ Arnaud R.C. Harris Erysiphales Lecanorales Phyllactinia fraxini (DC.) Fuss Leaves Bacidia arceutina (Ach.) Rehm & Arnold Bark, lichenized P. guttata (Wallr.) Lev. Leaves B. arnoldiana Korb.€ Bark, lichenized Helotiales Cladonia coniocraea (Florke)€ Spreng. Bark, lichenized Anavirga laxa B. Sutton Leaves C. diversa Asperges Bark, lichenized Ciboria caucus (Rebent.) Fuckel Seeds C. macilenta Hoffm. Bark, lichenized Crocicreas coronatum (Bull.) Fallen petioles C. parasitica (Hoffm.) Hoffm. Living branches, S.E. Carp. lichenized C. dolosellum (P. Karst.) S.E. Carp. Petioles Cliostomum griffithii (Sm.) Coppins Bark, lichenized C. fraxinophilum (Svrcek) Fallen petioles Evernia prunastri (L.) Ach. Bark, lichenized Triebel & Baral Flavoparmelia caperata (L.) Hale Bark, lichenized Excipula chaetostroma Berk. & Fallen samaras Hypogymnia physodes (L.) Nyl. Bark, lichenized Broome H. tubulosa (Schaer.) Hav. Bark, lichenized Hymenoscyphus albidus (Gillet) Fallen petioles Lecania cyrtella (Ach.) Th. Fr. Bark, lichenized W. Phillips L. naegelii (Hepp) Diederich & Van den Bark, lichenized H. albopunctus (Peck) Kuntze Fallen petioles Boom H. calyculus (Sowerby) W. Phillips Trunk Lecanora chlarotera Nyl. Bark, lichenized H. caudatus (P. Karst.) Dennis Fallen petioles L. compallens Herk & Aptroot Bark, lichenized H. fructigenus (Bull.) Fr. Fallen petioles L. confusa Almb. Bark, lichenized H. imberbis (Bull.) Dennis Bark, fallen twigs L. conizaeoides f. conizaeoides Nyl. ex Bark, lichenized H. phyllophilus (Desm.) Kuntze Samaras Cromb. H. repandus (W. Phillips) Dennis Fallen petioles, dead L. dispersa (Pers.) Sommerf. Bark, lichenized twigs L. expallens Ach. Bark, lichenized Lachnum niveum (R. Hedw.) P. Karst. Fallen petioles Lecidella elaeochroma f. elaeochroma Bark, lichenized Vibrissea guernisacii P. Crouan & Roots (Ach.) M. Choisy H. Crouan Lepraria lobificans Nyl. Bark, lichenized

(continued) (continued)

Table 3. (Continued) Table 3. (Continued)

Species/classiﬁcation Ecological notes Species/classiﬁcation Ecological notes

Melanelia fuliginosa subsp. glabratula Bark Pleosporales (Lamy) Coppins Alternaria alternata (Fr.) Keissl. Samaras, buds M. subaurifera (Nyl.) Essl. Bark A. tenuissima (Kunze) Wiltshire Leaves Melanohalea exasperata (De Not.) O. Bark, lichenized Arthopyrenia analepta (Ach.) A. Massal. Bark, lichenized Blanco, A. Crespo, Divakar, Essl., D. A. punctiformis A. Massal. Bark, lichenized Hawksw. & Lumbsch Ascochyta metulispora Berk. & Broome Live leaves Parmelia saxatilis (L.) Ach. Bark, lichenized Lewia infectoria (Fuckel) M.E. Barr & Samaras, seeds, live P. sulcata Taylor Bark, lichenized E.G. Simmons leaves Parmelina carporrhizans (Taylor) Bark, lichenized Phoma pterophila Nitschke ex Fuckel Samaras Poelt & Vezda P. samararum Desm. Samaras P. quercina (Willd.) Hale Bark Pleospora herbarum (Pers.) Rabenh. ex Samaras, seeds P. tiliacea (Hoffm.) Hale Bark, lichenized Ces. & De Not. Parmotrema perlatum (Huds.) M. Choisy Bark, lichenized P. phaeocomoides (Berk. & Broome) G. Samaras P. reticulatum (Taylor) M. Choisy Bark, lichenized Winter Piccolia ochrophora (Nyl.) Hafellner Bark of ancient tree, Venturia fraxini Aderh. Live leaves lichenized Pyrenulales Platismatia glauca (L.) W.L. Culb. & Trunk, lichenized Acrocordia gemmata (Ach.) A. Massal. Bark, lichenized C.F. Culb. Anisomeridium biforme (Borrer) R.C. Bark, lichenized Pleurosticta acetabulum (Neck.) Elix & Bark, lichenized Harris Lumbsch A. ranunculosporum (Coppins & P. Bark, lichenized Pseudevernia furfuracea var. furfuracea Bark, lichenized James) Coppins (L.) Zopf Rhizocarpales Punctelia reddenda (Stirt.) Krog Bark, lichenized Catillaria chalybeia var. chalybeia Bark, lichenized P. subrudecta (Nyl.) Krog Live trunk, lichenized (Borrer) A. Massal. Pyrrhospora quernea (Dicks.) Korb.€ Bark, lichenized C. nigroclavata (Nyl.) Schuler Attached twig, Ramalina farinacea (L.) Ach. Bark, lichenized lichenized R. fastigiata (Pers.) Ach. Bark, lichenized Cucurbitaria obducens (Schumach.) Petr. Samaras R. fraxinea (L.) Ach. Bark, lichenized Epicoccum nigrum Link Dead spots on leaves Scoliciosporum chlorococcum (Graewe Bark, lichenized Pyrenula chlorospila (Nyl.) Arnold Bark, lichenized ex Stenh.) Vezda P. macrospora (Degel.) Coppins & Bark, lichenized Usnea florida (L.) Weber ex F.H. Wigg. Bark, lichenized P. James U. subfloridana Stirt. Bark, lichenized Rhytismatales Ostropales Ascodichaena rugosa Butin Bark Graphis elegans (Borrer ex Sm.) Ach. Bark, live trunk, Hypoderma rubi (Pers.) DC. Fallen petioles lichenized Teloschistales G. scripta (L.) Ach. Bark, live trunk, Amandinea punctata (Hoffm.) Coppins & Bark, wood, lichenized Scheid. lichenized Phlyctis agelaea (Ach.) Flot. Live trunk, lichenized Buellia disciformis (Fr.) Mudd Bark, lichenized Porina aenea (Wallr.) Zahlbr. Bark, lichenized Calicium viride Pers. Trunk, lichenized P. chlorotica f. chlorotica (Ach.) Live trunk, lichenized Caloplaca cerina var. cerina Bark, lichenized Mull.€ Arg. (Ehrh. ex Hedw.) Th. Fr. Thelotrema lepadinum (Ach.) Ach. Live bark, lichenized C. cerinelloides (Erichsen) Poelt Bark, lichenized Peltigerales C. flavorubescens (Huds.) J.R. Laundon Bark, lichenized Collema furfuraceum (Schaer.) Du Rietz Bark, lichenized C. holocarpa (Hoffm.) A.E. Wade Bark, lichenized Leptogium burgessii (L.) Mont. Bark, lichenized C. obscurella (J. Lahm) Th. Fr. Bark, lichenized Lobaria pulmonaria (L.) Hoffm. Bark, lichenized Diploicia canescens (Dicks.) A. Massal. Bark, lichenized L. scrobiculata (Scop.) DC. Bark, lichenized Phaeophyscia orbicularis (Neck.) Bark, lichenized L. virens (With.) J.R. Laundon Bark, lichenized Moberg Parmeliella triptophylla (Ach.) Bark, lichenized Physcia adscendens (Fr.) H. Olivier Bark, lichenized Mull.€ Arg. P. aipolia (Ehrh. ex Humb.) Furnr.€ Bark, lichenized Pertusariales P. tenella (Scop.) DC. Bark, lichenized Ochrolechia subviridis (Høeg) Erichsen Bark, lichenized Physconia grisea (Lam.) Poelt Bark, lichenized Pertusaria albescens var. albescens Bark, lichenized Rinodina roboris var. roboris (Dufour Bark, lichenized (Huds.) M. Choisy & Werner ex Nyl.) Arnold P. amara f. amara (Ach.) Nyl. Bark, lichenized Xanthoria parietina (L.) Th. Fr. Bark, lichenized P. hymenea (Ach.) Schaer. Bark, lichenized X. polycarpa (Hoffm.) Th. Fr. ex Rieber Bark, lichenized P. leioplaca DC. Bark, lichenized X. ucrainica S.Y. Kondr. Bark, lichenized P. multipuncta (Turner) Nyl. Bark, lichenized Umbilicariales P. pertusa (Weigel) Tuck. Bark, lichenized Fuscidea lightfootii (Sm.) Coppins & Bark, lichenized Pezizales P. James Tuber rufum Pico Roots (continued) (continued)

Table 3. (Continued) Ascomycota, Erysiphales); the last of these can, in turn, be parasitized by several Cladosporium spp. Link (Ascomycota, Species/classification Ecological notes Capnodiales) (von Tubeuf 1897; Talgø et al. 2011; Dolinska & Schollenberger 2012). Mycosphaerella fraxini (Niessl) Lin- Xylariales dau (=Septoria fraxini Desm.) (Ascomycota, Capnodiales) is Cryptosphaeria eunomia (Fr.) Fuckel Twigs and bark a sooty mould that can cause spotting on leaves and, accord- Basidiomycota Agaricales ing to Hempel & Wilhelm (1897, reported in Wardle 1961), Armillaria borealis Marxm. & Korhonen Tree base can kill seedlings. Excipula chaetostroma Berk. & Broome A. gallica Marxm. & Romagn. Live and dying roots (=Amerosporium chaetostroma Sacc.) (Ascomycota, Helo- A. mellea (Vahl) P. Kumm. Live roots and trunk tiales) is found on samaras on the ground, and once into the Calyptella capula (Holmsk.) Quel. Petioles, bark seed, the endosperm degenerates into a watery mass carrying Coprinellus micaceus (Bull.) Vilgalys, Living roots Hopple & Jacq. Johnson the pycnidia. As the fungus belongs to a saprophytic group, it Episphaeria fraxinicola Bark is possible that the seeds die before becoming infected, proba- (Berk. & Broome) Donk bly specific to ash (Wardle 1961). Fistulina hepatica (Schaeff.) With. Live trunk Laetiporus sulphureus (Bull.) Murrill (=Polyporus sul- Flammulina velutipes var. lactea Live trunk phureus (Bull.) Fr.) and in particular Polyporus squamosus (Quel.) Bas F. velutipes var. velutipes (Curtis) Singer Live trunk (Huds.) Fr. (Basidiomycota, Polyporales) are common on Gymnopilus junonius (Fr.) P.D. Orton Live trunk dead wood of large old trees and may occasionally act as a Lachnella alboviolascens Fallen petioles weak parasite (von Tubeuf 1897). A common Basidiomycete (Alb. & Schwein.) Fr. found particularly on ash trunks is the bracket Inonotus hispi- Macrotyphula juncea (Fr.) Berthier Rotting petioles dus (Bull.) P. Karst. (Basidiomycota, Hymenochaetales) caus- Marasmius epiphyllus (Pers.) Fr. Fallen petioles Pellidiscus pallidus (Berk. & Broome) Bark ing white rot, often associated with trunk breakage Donk (Cartwright, Campbell & Armstrong 1936; Rackham 2014;). Pholiota alnicola var. alnicola (Fr.) Live trunk Less common on dead ash wood is Auricularia auricula- Singer judae (Bull.) Wettst. (Basidiomycota, Atheliales) (Reid 1978). P. aurivella (Batsch) P. Kumm. Live trunk Pholiota spp., particularly P. squarrosa (Weigel) P. Kumm. P. limonella (Peck) Sacc. Live trunk P. squarrosa (Weigel) P. Kumm. Live trunk (Basidiomycota, Agaricales), are considered to be weakly par- Volvariella bombycina (Schaeff.) Singer Live trunk asitic on the trunk (Brooks 1953). Cantharellales Fraxinus excelsior is direct host to 95 taxa of slime moulds Cantharellus fissilis Fr. Petioles (Amoebozoa, Myxomycetes) listed in Table 4. This is similar Corticiales to the number found on Acer pseudoplatanus but 25 fewer spe- Dendrothele acerina (Pers.) P.A. Lemke Live trunk Hymenochaetales cies than found on Fagus sylvatica, which has more than twice Inonotus hispidus (Bull.) P. Karst. Live trunk the number of fungal records listed by the Fungal Records Mensularia radiata (Sowerby) Live trunk Database (British Mycological Society 2016) compared to ash Lazaro Ibiza and A. pseudoplatanus. Polyporales Fomes fomentarius (L.) J.J. Kickx Live trunk Ganoderma lucidum (Curtis) P. Karst. Live trunk (C) PLANT DISEASES Grifola frondosa (Dicks.) Gray Live trunk Laetiporus sulphureus (Bull.) Murrill Live trunk Various cankers on ash are caused by the bacteria Pseu- Podoscypha multizonata Roots domonas savastanoi (Janse) Gardan (=Phytomonas savastonoi (Berk. & Broome) Pat. Stev. var. fraxini Brown) and Pseudomonas syringae ssp. Polyporus squamosus (Huds.) Fr Live trunk = Russulales savastanoi ( Pseudomonas savastanoi) pv. fraxini, and pv. Heterobasidion annosum (Fr.) Bref. Trunk savastanoi (the latter also found on Olea europaea) (Janse Trechisporales 1982; Ramos et al. 2012). Bacterial infections can be Tubulicium vermiferum (Bourdot) Live trunk aggravated by the invasion of Nectria galligena Bres. € Oberw. ex Julich (Ascomycota, Hypocreales) and perhaps also by frost damage. Fungi that can be lichenized were identified from the British Isles List Phytoplasma rDNA has been found in ash in Poland of Lichens and Lichenicolous Fungi (Natural History Museum 2016). (Kaminska & Berniak 2009), associated with symptoms of stunting, shoot proliferation and dieback, and more widely is (Pers.) De Not. (Ascomycota, Hysteriales) is common on associated with the disease ash yellows (Sinclair & Griffiths dead twigs and sometimes branches (von Tubeuf 1897). A 1994; Griffiths et al. 1999). Ash yellows is transmitted by number of powdery mildews are common on live and/or dead insect vectors and known from N. America but is most severe leaves with varying degrees of specificity, forming spots in in urban areas of planted ash in Colombia (Woodward & Boa the lamina: Venturia fraxini Aderh. (=Actinonema fraxini 2013). All.) and Ascochyta metulispora Berk. & Broome (both Ash is very susceptible to infection of Phytophthora ramo- Ascomycota, Pleosporales), Phyllactinia guttata (Wallr.) Lev. rum Werres, De Cock & Man in’t Veld (Oomycota, Peronospo- (=P. corylea (Pers.) P. Karst.) and P. fraxini (DC.) Fuss (both rales) through the leaves and is host to P. multivora Scott &

Table 4. Slime moulds (Amoebozoa, Myxomycetes) associated with Table 4. (Continued) Fraxinus excelsior. Nomenclature follows the Fungal Records Data- L. microscopica D.W. Mitch. Live bark base of Britain and Ireland (British Mycological Society 2016) L. operculata (Wingate) G.W. Martin Live bark L. parasitica (Zukal) G.W. Martin Live bark Amaurochaete 1atra (Alb. & Schwein.) Live wood, bark L. perexigua T.E. Brooks & H.W. Keller Live bark Rostaf. L. sambucina D.W. Mitch. Live bark Arcyria cinerea (Bull.) Pers. Bark L. testudinacea Nann.-Bremek. Live bark A. denudata (L.) Wettst. Decaying wood Lycogala epidendrum (J.C. Buxb. ex L.) Fr. Dead wood A. incarnata (Pers. ex J.F. Gmel.) Pers. Dead wood L. terrestre Fr. Fallen branches A. major (G. Lister) Ing Fallen wood Macbrideola cornea (G. Lister & Cran) Live bark A. minuta Buchet Fallen wood Alexop. A. nutans (Bull.) Grev. Bark, dead wood M. macrospora (Nann.-Bremek.) Ing Live bark A. oerstedii Rostaf. Fallen wood Metatrichia floriformis (Schwein.) Nann.- Fallen trunks A. pomiformis (Leers) Rostaf. Live bark Bremek. Badhamia affinis Rostaf. Live bark M. vesparium (Batsch) Nann.-Bremek. Fallen trunks B. capsulifera Cooke Decaying wood Mucilago crustacea P. Micheli ex F.H. Fallen twigs, B. foliicola Lister Bark, dead leaves Wigg. branches and trunks B. utricularis (Bull.) Berk. Wood Paradiacheopsis cribrata Nann.-Bremek. Live bark Brefeldia maxima (Fr.) Rostaf. Very decayed wood P. fimbriata (G. Lister & Cran) Hertel Live bark Calomyxa metallica (Berk.) Nieuwl. Bark P. solitaria (Nann.-Bremek.) Nann.- Live bark Ceratiomyxa fruticulosa fruticulosa var. Fallen wood Bremek. € (O.F. Mull.) T. Macbr. Perichaena chrysosperma (Curr.) Lister Bark Clastoderma debaryanum A. Blytt Live bark P. corticalis (Batsch) Rostaf. Dead bark Colloderma oculatum (C. Lippert) G. Lister Bark P. depressa Lib. Bark Comatricha nigra € (Pers.) J. Schrot. Wood Physarum auriscalpium Cooke Bark Craterium leucocephalum var. Dead wood P. cinereum Link Bark, fallen wood leucocephalum (Pers. ex J.F. Gmel.) P. crateriforme Petch Bark Ditmar P. decipiens M.A. Curtis Bark C. minutum (Leers) Fr. Dead wood P. psittacinum Ditmar Bark, dead wood Cribraria argillacea (Pers. ex J.F. Gmel.) Fallen branch P. robustum (Lister) Nann.-Bremek. Dead wood Pers. P. vernum Sommerf. Bark C. tenella Schrad. Fallen branch Protostelium arachisporum L.S. Olive & Bark C. violacea Rex Wood Stoian. Diacheopsis insessa (G. Lister) Ing Bark Reticularia intermedia Nann.-Bremek. Dead wood Dianema depressum (Lister) Lister Dead bark, wood R. lycoperdon Bull. Dead wood D. harveyi Rex Dead wood R. olivacea var. olivacea (Ehrenb.) Fr. Wood Diderma chondrioderma (de Bary & Live bark Stemonitis flavogenita E. Jahn Twigs Rostaf.) Kuntze S. fusca var. fusca Roth Dead wood D. hemisphaericum (Bull.) Hornem. Dead branch Symphytocarpus flaccidus (Lister) Ing & Wood D. spumarioides (Fr.) Fr. Twigs Nann.-Bremek. Didymium clavus (Alb. & Schwein.) Dead trunk Trichia affinis de Bary Decaying wood Rabenh. T. botrytis var. botrytis (Pers. ex J.F. Live and decaying D. difforme (Pers.) Gray Bark Gmel.) Pers. wood D. squamulosum (Alb. & Schwein.) Fr. Bark, fallen twigs T. contorta var. contorta (Ditmar) Rostaf. Fallen branch and branches T. contorta var. inconspicua (Rostaf.) Lister Fallen branch Echinostelium brooksii K.D. Whitney Live bark T. contorta var. karstenii (Rostaf.) Ing Dead wood E. colliculosum K.D. Whitney & H.W. Live bark T. decipiens var. decipiens (Pers.) T. Dead wood, stumps Keller Macbr. E. corynophorum K.D. Whitney Live bark T. persimilis P. Karst. Fallen trunks E. minutum de Bary Live bark T. scabra Rostaf. Dead wood Enerthenema papillatum (Pers.) Rostaf. Live bark T. varia (Pers. ex J.F. Gmel.) Pers. Fallen trunks Fuligo candida Pers. Wood Tubulifera arachnoidea Jacq. Decaying wood F. septica flava var. (Pers.) Morgan Wood Willkommlangea reticulata (Alb. & Branch F. septica septica var. (L.) F.H. Wigg. Wood Schwein.) Kuntze Hemitrichia clavata (Pers.) Rostaf. Decayed wood H. minor G. Lister Bark Lamproderma scintillans (Berk. & Broome) Bark, leaves Morgan Jung and P. plurivora Jung & Burgess in the Czech Republic, Licea belmontiana Nann.-Bremek. Live bark and P. gonapodyides (H.E. Petersen) Buisman on twigs in the L. biforis var. biforis Morgan Live bark UK, but has low susceptibility/resistance to P. kernoviae Bra- L. bryophila Nann.-Bremek. Live bark sier, Beales & S.A. Kirk (Denman et al. 2006; Mrazkova et al. L. denudescens H.W. Keller & T.E. Brooks Live bark 2013; British Mycological Society 2016). Ash is a prolific pro- L. inconspicua T.E. Brooks & H.W. Keller Live bark L. kleistobolus G.W. Martin Live bark ducer of P. ramorum spores (Denman et al. 2006). L. marginata Nann.-Bremek. Live bark Ash is usually considered to be resistant to Armillaria mellea (Vahl) P. Kumm. (Basidiomycota, Agaricales), but it has (continued) been recorded on live ash along with A. borealis Marxm. &

Korhonen, A. gallica Marxm. & Romagn. Armillaria ostoyae thought to be caused by frost or drought (Pukacki & Przybył (Romagn.) Herink. has been found on dead ash. In Lithuania, 2005). However, Chalara fraxinea T. Kowalski (Ascomycota, A. cepistipes Velen. has caused root and butt rot of dying and Incertae sedis) was consistently isolated from moribund stems, dead ash (Lygis et al. 2005). Ash along with Ulmus glabra branches and sometimes roots (Kowalski 2006) and has been appears to be comparatively resistant to foliar fungal patho- shown through controlled inoculations to be the casual agent gens in comparison with Acer platanoides, Populus tremula of dieback (Bakys et al. 2009a,b; Kowalski & Holdenrieder and Tilia cordata (Hantsch et al. 2014). Przybył (2002a,b) 2009a). Chalara fraxinea was found to be the anamorphic lists fungi associated with necrosis of shoots and roots in stage of the teleomorph Hymenoscyphus fraxineus (T. Kowal- Poland. ski) Baral, Queloz, Hosoya (Kowalski & Holdenrieder 2009b; Black heart of ash, where wood at the centre of the tree Queloz et al. 2011; Baral & Bemmann 2014; Adamcıkova appears brown or black, has been considered to be of fungal et al. 2015), also called H. pseudoalbidus Queloz, Grunig,€ origin but in reality is a chemical staining, although the mech- Berndt, Kowalski, Lieber et Holdenrieder although Baral, anisms are largely unknown. Kerr (1998) reviews the litera- Queloz & Hosoya (2014) argue that the former name has ture and shows that 70- to 100-year-old trees are likely to all precedence. It is similar (but not a close relative) to the native be affected across up to 30% of the tree’s cross-sectional area. non-pathogenic H. albidus, a saprotroph of petioles in the lit- Black heart affected wood, sold as ‘olive wood’, is considered ter, and which is now much rarer, presumed to be due to to be of ornamental value (Rackham 2014). competition with H. fraxineus (Bengtsson et al. 2012; Gross et al. 2012b; McKinney et al. 2012a). Hymenoscyphus fraxineus is native to eastern Asia and was possibly introduced to Ash Dieback E. Poland or the Baltic States on infected Fraxinus mand- The recent and widespread ash dieback was first discovered shurica imported from the Russian Far East (Drenkhan, San- in north-east Poland and Lithuania in 1992 (Kowalski & der & Hanso 2014) and appears to have been introduced just Holdenrieder 2009a,b) before spreading rapidly across much once on at least two individuals (Gross, Hosoya & Queloz of eastern, western and Central Europe (Kowalski 2006; 2014). Gross et al. (2014) give a pathogen profile of H. frax- Bakys et al. 2009a; Skovsgaard et al. 2010; Rytkonen€ et al. ineus. Methods to detect the fungus include PCR (Ioos et al. 2011). This dieback was first identified in Britain in nursery 2009; Chandelier, Andre & Laurent 2010; Johansson et al. stock in Buckinghamshire in February 2012 (Forestry Com- 2010) and mass spectrometric techniques (Pham et al. 2013). mission 2015). Hymenoscyphus fraxineus is found on petioles and leaf Ash dieback has been found in Fraxinus excelsior and also blades and spreads primarily by spores (Gross et al. 2012b). Fraxinus angustifolia in some parts of Europe (Gross et al. Apothecia develop on petioles in the forest litter and spores 2014). Fraxinus ornus may also occasionally be infected but are released from the end of June to September–October (Kir- shows few symptoms (Kirisits et al. 2009) and the disease isits & Cech 2009; Timmermann et al. 2011; Chandelier has also been reported in Estonia on several ash species not et al. 2014). Hymenoscyphus fraxineus is heterothallic and native to Europe: F. nigra, F. pennsylvanica, F. americana infected petioles can contain both mating types and so readily and F. mandschurica (Drenkhan & Hanso 2010; Kr€autler & reproduce (Gross et al. 2012b, 2014). Ascospore production Kirisits 2012). is maximal in the mornings and reaches a peak in the autumn In newly infected shoots, death of the cambium and exter- just prior to leaf senescence (Hietala et al. 2013). Crown nal tissues turns the shoot red brown associated with wilting damage also tends to increase through a season; Bakys, of leaves and buds not opening in spring (Kowalski & Hold- Vasaitis & Skovsgaard (2013) noted it rising from 30% dam- enrieder 2009b). Infected trees develop lesions and necroses age to the canopy in June to 53% in September. Ash trees on shoots, branches and stems, followed by gradual dieback that flush early in spring and enter senescence earlier were of crowns (Kowalski & Łukomska 2005; Kowalski 2006) found to be less susceptible to dieback (McKinney et al. leading to progressively bare stems and bushy growth from 2011; Stener 2012; Bakys, Vasaitis & Skovsgaard 2013). new shoots (Skovsgaard et al. 2010). The bark lesions corre- McKinney et al. (2012b) observed that this was not because late well with a brownish discoloration of the wood (Schu- those with earlier phenology avoided infection through early macher, Kehr & Leonhard 2010) although the discoloration leaf drop, but that these individuals were physiologically tends to be more extensive than the bark lesion. The fungus more resistant to the disease, limiting the growth and spread can kill by girdling the trunk. of the fungus. Chandelier et al. (2014) found spores are dis- Dieback of ash in hedgerows, that has caused concern in persed most when air temperature >12 °C and spread down- Britain since the 1960s (Hull & Gibbs 1991), was most likely wind <50 m from an infected stand (measured over 3 years); caused by the ash bud moth Prays fraxinella in conjunction few spores were detected >3 m from the ground. Although with disturbance of roots and subsequent drought as a result spore dispersal is thus comparatively limited, infected petioles of ditching beside the hedges (Foggo & Speight 1993). Ongo- have been seen to produce spores for more than a year (Gross ing bouts of decline in Britain during the 1980s have been & Holdenrieder 2013), and for even up to 5 growing seasons attributed to fluctuations in the water-table as a result of cli- (Kirisits 2015), and so represent a risk of long-term infection. matic variations (Woodward & Boa 2013). So it is perhaps Moreover, the fungus in either its anamorph or teleomorph not surprising that dieback in eastern Europe was initially stage has been found in 8.3% of seeds originating from Lat-

© 2016 The Authors. Journal of Ecology © 2016 British Ecological Society, Journal of Ecology 34 P. A. Thomas via (Cleary et al. 2013) and 30% of seeds in southern Swe- (Tulik, Marciszewska & Adamczyk 2010). But Rosenvald den (Hayatgheibi 2013), from both resistant and susceptible et al. (2015) did not ﬁnd Armillaria spp. contributing to the ash clones. This may be an important way of the disease con- death of isolated retention trees. Conversely, a study from tinuing to spread to places currently free of ash dieback, such Poland and Denmark showed that Phytophthora spp. can as North America, through the importation of seed (Hayat- make ash trees more susceptible to ash dieback (Orlikowski gheibi 2013). It appears that the fungus was brought into Bri- et al. 2011). tain on horticultural imports, but there have also been Over the past two decades, ash dieback has already had a suggestions that this was supplemented by spores blown from serious effect on ash stands through mainland Europe, cover- mainland Europe. ing 2 million km2 from Scandinavia down to France and Italy The ascospores infect ash through the living leaf lamina (Gross et al. 2014), perhaps aided by the recent increase in and petioles. The mycelium develops intracellularly, passing ash abundance (XI). Within this area, the disease is wide- through pits between cells rather than through the cell walls, spread; for example, it has been estimated that 60–90% of and invades the phloem, xylem and pith via the ray parenchy- ash stands in Denmark are affected (Skovsgaard, Kehr & mal cells, readily spreading through the tree in all directions Leonhard 2010; van Opstal 2011) and ash is listed by Nord- (Schumacher, Kehr & Leonhard 2010; Dal Maso et al. 2012) Larsen et al. (2009) as the ﬁfth most abundant broadleaved and out to the cambium. The anamorph C. fraxinea produces species in Denmark. Infection rates within stands can also be conidia, but these are not directly involved in the infection high; for example, a survey of 337 ash trees in Sweden found process; instead, they are thought to act as spermatia in the 63% of trees infected in 2009 and 76% in 2011, of which 3% exchange of nuclei (Kirisits & Cech 2009; Kirisits et al. died over the 2 years (Bengtsson, Stenstrom€ & Finsberg 2009; Gross et al. 2012b). Chalara fraxinea has not been iso- 2013). lated from ash roots and so appears to have little, if any, All age classes are susceptible to ash dieback, but young endophytic abilities (Schumacher, Kehr & Leonhard 2010). trees in dense stands, especially on consistently damp soils Bakys et al. (2011) investigating ash in Lithuania found that (aiding spore production) or on very dry sites (stressing the 4 years after trees were felled, 58% of uninfected stumps had trees), have the highest infection rates (Kenigsvalde et al. produced new sprouts compared to 33% of dieback-infected 2010; Skovsgaard et al. 2010; McKinney et al. 2011; Schu- stumps. However, dieback symptoms were found on the macher 2011; Bakys, Vasaitis & Skovsgaard 2013; Bengts- leaves and bark of new shoots irrespective of whether the son, Stenstrom€ & Finsberg 2013). For example, on the island stump was infected or not. This, and the fact that the dieback of Gotland in southern Sweden, 84% of trees were infected fungus did not enter sprouts from stumps, suggests infection on dense unmanaged sites compared to 66% on more open of new shoots from aerial spores. Hymenoscyphus fraxineus grazed sites (Jonsson€ & Thor 2012). Death could be rapid can, however, invade new hosts vegetatively by direct contact (Bengtsson, Stenstrom€ & Finsberg (2013) noted 5 trees of infected wood with the epidermis of current-year branches healthy in 2009 were dead by 2011) but generally older trees (Schumacher 2011; Kr€autler, Treitler & Kirisits 2015). Differ- are slower to die. Thus, Enderle et al. (2013), looking at four ent genotypes of the fungus have been found on the same sites in south-west Germany, found that while 94% of trees trees and within the same lesion (Bengtsson et al. 2014). showed symptoms of dieback, between 2005 and 2012 only The virulence of H. fraxinea has been attributed at least in 9% of trees died. This might be because older trees build up part to the phytotoxin viridiol (Andersson et al. 2010) greater populations of protective endophytes or simply because it has been seen to experimentally provoke brown because more damage is needed in a larger tree to kill it necrotic spots on ash leaves (Grad, Kowalski & Kraj 2009; (Bakys, Vasaitis & Skovsgaard 2013). Infected trees can pro- Andersson et al. 2010) and seedlings of clones more suscepti- duce many new shoots and so the canopy can appear to ble to H. fraxinea have been seen to be more affected by become healthier and seem to be recovering (Bengtsson, Sten- viridiol in a laboratory study (Cleary et al. 2014). However, strom€ & Finsberg 2013), but given time mortality can eventu- other non-virulent species of Hymenoscyphus also produce ally be high. For example, in Lithuania, one of the longest viridiol, and viridiol concentration does not always correlate infected countries (Juodvalkis & Vasiliauskas 2002), trees with degree of plant damage in tests (Junker et al. 2014). The were felled in an attempt at stopping spread and the area of volatile lactone 3,4-dimethylpentan-4-olide may also be part ash stands decreased by 30% between 1995 and 2012. Cur- of the virulence since it can completely inhibit germination of rently, the epidemic is chronic with all remaining ash stands ash seeds by causing necroses (Citron et al. 2014). showing some damage and their health condition continues to Seedlings die within a few years of infection, but older decline (Riepsas 2009; Gustiene_ 2010; Pliura et al. 2011). In trees may take a number of years to die. There is evidence 2009, a quarter of all ash trees in southern Sweden were dead that trees over 20 years old are weakened by ash dieback but or severely damaged and ash was considered vulnerable to actually die from secondary effects such as Armillaria spp. further loss (Pihlgren et al. 2010; Stenlid et al. 2011). In (Bakys et al. 2011) or environmental stresses (Bakys et al. assessments of the likely impact of ash dieback in Britain, the 2009a,b; Schumacher, Kehr & Leonhard 2010) exacerbated worst-case scenario is taken as 95% mortality of ash (Mitchell by ash dieback-infected ash having narrower vessels in the et al. 2014a). As yet, we have no real idea whether such high xylem (reducing from 0.15 mm in healthy to 0.12 mm in mortality rates will be reached, but they are by no means infected trees) with consequent reduced hydraulic conductivity improbable.

It is not just the loss of current trees that is of concern, as was expected to produce ‘almost healthy’ seedlings, and only there is also evidence that the effects of dieback are not four trees would produce ‘fairly healthy’ seedlings. This is in restricted to the current generation of trees and specifically that agreement with findings from the clonal trials of McKinney ash will not regenerate very effectively on affected sites. For et al. (2011) also in Denmark, where only one of 39 tested example, Lygis et al. (2014) looked at what happened when clones would produce ‘almost healthy’ seedlings and three infected stands were felled in Lithuania. Before ash dieback, ‘fairly healthy’ seedlings, based on assessments in 2009. This ash made up 40–100% of stands, but 10 years after felling ash low proportion of resistant trees is likely to be similar through- made up only 0–21% of stands. Of all the new ash trees out the range of ash but has still to be tested (Kebler et al. (n = 775), 53.9% were diseased, 16.8% were dead, and only 2012). Although the proportion of resistant ash in a population 29.3% were visually healthy and so the disease cycle looked looks to be too low to avoid population collapse in the near set to repeat itself. Moreover, ash was among the slowest future, it does provide hope that ash can gradually recover in growing species so other faster growing trees including Alnus the future and will not be entirely lost to future generations. incana, Populus tremula and Betula pendula/B. pubescens Since this resistance is inheritable (Lobo et al. 2015), it is also would put further competitive pressure on the ash. possible that breeding programmes can be undertaken to Can action be taken to reduce the spread and impact of enhance the resistance, much as is being done for Castanea the disease? Improved phytosanitation can help though it is dentata following its devastation in N. America by chestnut largely too late for this to be effective within Europe. It blight (Thompson 2012). Several Asian and American ash spe- could also be argued that the porous nature of national cies have appeared to be resistant after wound inoculation, boundaries within the EU and the perceived lack of politi- including F. chinensis Roxb., F. bungeana DC., F. latifolia cal will to prioritize this problem led to biosecurity mea- Benth. and F. velutina Torr. (Aas & Holdenrieder, unpub- sures being ineffective. Woodward & Boa (2013) take a lished, reported by Pautasso et al. 2013). It should therefore conciliatory view that long-term dieback from other causes be possible to breed ash trees that look similar to native ash such as insects and climate (see above) hid the true fungal but with the resistance of their cousins. However, the virulence cause and that H. fraxineus was initially thought to be a of H. fraxineus may change since it is variable and reproduces strain of the native H. albidus and ‘it would [have been] sexually (Gross et al. 2012a), plus new genes are likely to be futile to set up any regulations or protected areas to prevent spread by further introductions throughout Europe, so if resis- the spread of a pest or pathogen which already exists in tance is based on a narrow genetic range, it might be rapidly that area’. While it is true that the identity of H. fraxineus overcome (Pautasso et al. 2013). was confirmed only in 2011 by Queloz et al., the fungal Other direct action is possible. Fungicides are likely to be nature of Chalara fraxinea was known in 2006, and yet of limited use since the fungus permeates woody tissues so few adequate biosecurity measures were taken. Current pol- completely. More promising is the use mycoviruses; one in icy responses by the UK Government for controlling the particular (HfMV1) has been found in 90% of field isolates of disease are given by Gilligan et al. (2013). H. fraxineus in two Swiss populations (Schoebel, Zoller & Some proposed phytosanitation measures may be of use Rigling 2014), suggesting that it can be effectively spread and because of their comparative simplicity. For example, Schu- may help resistance as similar microviruses have in Dutch macher (2011) points out that removing litter in the autumn elm disease (Hintz et al. 2013). can slow dispersal of the fungus in urban areas. International Less direct but with potential for slowing the spread and trade in ash seed and seedlings is likely to continue in the degree of infection is silvicultural thinning and retention for- future and can potentially be safeguarded with hot water. estry where specimen trees are retained, particularly in young Hauptman et al. (2013) found that immersing bare-rooted 3- stands which are most likely to be infected (Skovsgaard et al. year-old seedlings in hot water at 36 °C for 5 h effectively 2010). As noted above, more open stands are less damaged killed Chalara fraxinea, while the seedlings survived as well by ash dieback and the reduced competition for water, light as in controls. Indeed, seedlings could withstand immersion and nutrients should make the trees more resistant to the dis- in water at 44 °C for 5 h (37.5% survival) and even for 10 h ease. Rosenvald et al. (2015) followed the fate of 577 ash (5% survival) and so this may form an effective control in trees left after felling (retention trees); after 13 years, 65% nursery stock. Samaras can also survive 5 h at 44 °C and still remained alive and 15% were healthy despite all trees being be have 60% viability (c. 25% less than the control) and so infected. The most isolated individuals fared best, particularly can be heat-treated (McCartan, Webber & Jinks 2015). those that had been exposed to semi-open conditions for A promising lead lies in the fact that some ash clones are longer such as those along forest edges, which holds out hope resistant to ash dieback although none are probably immune for mature retention trees surviving as seed parents. They (Pliura et al. 2011; McKinney et al. 2012b; Stener 2012; stress that disease progression, not infection probability, is the Enderle et al. 2015). However, Kjær et al. (2012) estimated most important variable, not whether trees get the disease but that in Danish ash populations, only 1% of trees were how slowly it progresses. hyposensitive and had the potential of producing offspring Strategies and research needs to restrict the impact of ash with <10% of crown damage under current infection condi- dieback and mitigate the impacts of a large-scale decline of tions. They suggested that of the 101 seed trees tested, none ash are discussed by Pautasso et al. (2013), Charlton & Mem- would produce completely healthy seedlings, only one tree mott (2013), Worrell (2013), Mitchell et al. (2014a,b,c) and

Hinsley & Pocock (2014). Mitchell et al. (2014b,c) discuss et al. 1999; Joannin et al. 2013). Thereafter, spread was mainly the merits of 11 and 22 native species, respectively, that determined by increases in humidity and climate cooling, ash could most likely take over different aspects of the ecological moving into the East Balkans by 11 840 BP but becoming niche of ash; overall, Alnus glutinosa, Tilia cordata and Sor- much commoner (>2.5% of pollen) after 7635 BP (Filipova- bus aucuparia were most similar, except Quercus robur/ Marinova et al. 2013a), and Bulgaria and north-east Poland Q. petraea and Fagus sylvatica would prove better replace- around 7800 BP (Filipova-Marinova et al. 2013b; Karpinska- ments for maintaining the most associated species (see XI) Kołaczek, Kołaczek & Stachowicz-Rybka 2013) along with but which are otherwise very dissimilar ecologically to ash. It Alnus, Ulmus and Fagus spp. Ash had slowly reached the Wes- is obvious that no one species can ecologically replace ash in tern Carpathians by c. 6000 BP in forests dominated by Cory- the British landscape. In terms of management, in the short lus avellana and Picea abies, although ash, along with Ulmus term (<10 years), thinning and/or felling and allowing natural and Tilia spp., declined from about 4800 BP as Fagus sylvat- regeneration are suggested to be the best management ica, Picea abies, Carpinus betulus became more dominant options; in the long term (<100 years), it is likely that man- (Feurdean et al. 2010). Tinner et al. (2000) give evidence that agement choices made now will make little difference to the the decline of ash in the Italian Southern Alps was synchronous final outcome on local biodiversity and community function- to charcoal fluctuations and was human driven. So the more ing. Following on from this, Hinsley & Pocock (2014) dis- recent expansion of ash in mainland Europe is very likely due cuss the long-term monitoring required to follow potential to a decrease in the rural human population, allowing invasion changes associated with significant ash loss. The problems of of abandoned land (Pigott & Pigott 1959; Marigo et al. 2000), public perception of the risks of the disease (‘social amplifica- and to a reduction in the use of fire (Tinner et al. 1999) rather tion of risk’) are examined by Pidgeon & Barnett (2013). than a direct response to increasing nitrogen deposition (Hofmeister, Mihaljevic&Hosek 2014). Figure 5 shows a general decline in ash from 5000 years BP. X. History Sutherland et al. (2010) raised the possibility of the pres- Ash, along with other deciduous trees, is thought to have ence of ash 12 000 BP in several parts of Britain, suggesting occupied northern Europe including Svalbard and Greenland that relict populations may have survived in secondary refugia during the Cretaceous period, spreading into Central Europe in the Forth and Tay watersheds in eastern Scotland and the following periods of cooling (Marigo et al. 2000). Thereafter, Lleyn Peninsula in north-west Wales close to the ice sheets, there is molecular evidence (Hinsinger et al. 2014) that Euro- allowing rapid colonization of these areas prior to the mass pean ash species diverged from Fraxinus mandshurica c.15 colonization from Europe. This is possible since Brewer mya in southern Europe as the Mediterranean formed and the (2002) found ash pollen (>1%) in southern Sweden from the climate went through cycles of drying and that F. excelsior same period. However, nuclear DNA make-up of current and F. angustifolia split 7.2–5.3 mya during the most extreme Swedish populations has similarities to that of south-eastern drying cycles, with F. excelsior restricted to the more temper- Europe (the biggest suggested glacial refuge) that British pop- ate areas. ulations do not show (Heuertz et al. 2004b); instead, Britain Fraxinus excelsior is recognized as a low pollen producer, and Central Europe form largely a single deme. Nor do shedding around a fifth of the pollen of prolific trees such as chloroplast haplotype markers support such relicts (Heuertz Alnus, Betula and Quercus species (Brostrom€ et al. 2008). et al. 2004a). However, ash has been found to be present in Fraxinus excelsior pollen has been found to rapidly drop off the Shetland mainland around 7400–5400 BP (although within 20 m of a dryland/fen carr edge (Binney et al. 2005; extinct by 3100 BP) and the Western Isles of Scotland from Bunting et al. 2005), even more rapidly than other wind- 6000 BP at the latest (Bennett et al. 1992; Fossitt 1996). The pollinated trees such as Betula and Quercus spp., and so majority of British ash populations are of the same chloro- tends to be underrepresented in post-glacial pollen records, plast haplotype (H04) as found in the Iberian Peninsula (Petit rarely forming >5% of total tree pollen, and so representing et al. 2003; Heuertz et al. 2004a); since this is not currently local rather than regional presence. Nevertheless, pollen data found in France, it is suggested that ash migrated along the (Fig. 5) suggest that ash expanded in the Early Holocene edge of the Atlantic coast and onto the land bridge and into from refugia in the Balkan Peninsula, the Alps and Apennines Britain (Heuertz et al. 2004a). In the south-east of England, (Huntley & Birks 1983; Gliemeroth 1997; Brewer 2002). there is a small presence of haplotype H03 that is mainly Based on chloroplast and nuclear DNA data, Heuertz et al. found in the Apennines of Italy, suggesting a small post-gla- (2004a,b) also suggested further refuge areas east of the Bal- cial influx from this region. kans and Carpathian Mountains, and on the Iberian Peninsula. By 5000 BP, ash was common in Britain, especially in As it started spreading from these refugia, ash was part of the northern England (Rackham 2003). Following the elm decline cool-temperate summergreen tree/shrub mix across Eurasia of 5000 BP (Parker et al. 2002), ash pollen reached 10% of including species of Acer, Euonymus, Prunus and Quercus total tree pollen since it was likely the most effective colo- robur (Allen, Watts & Huntley 2000). Initial spread from nizer (Conway 1954). Thereafter in the Bronze and Iron these refugia has been attributed to a warming climate and Ages, browsing for fodder and harvesting for ash wood, along increasing forest clearance (Godwin 1975) and ash is recorded with other high-quality trees such as Acer, Tilia and Ulmus widely in the Alps between 14 700 and 11 500 BP (Tinner spp., led to their decline accompanied by an expansion of

15 cal. BP 14 cal. BP 13 cal. BP 12 cal. BP

11 cal. BP 10 cal. BP 9 cal. BP 8 cal. BP

Fraxinus 0 % − 0.5 % 0.5 − 1 % 7 cal. BP 6 cal. BP 5 cal. BP 4 cal. BP 1 − 2 % 2 − 4 % 4 − 8 % > 8 %

3 cal. BP 2 cal. BP 1 cal. BP 0 cal. BP

Fig. 5. Presence of ash during the Quaternary period through Europe as a proportion of total tree pollen. Data from the European Pollen Data- base (www.europeanpollendatabase.net), maps kindly supplied by Prof. Richard Bradshaw.

Carpinus betulus and Fagus sylvatica (Hejcmanova, Ste- (James 1968). It was commonly used as firewood by late Neo- jskalova & Hejcman 2014). There are records in eastern lithic people in Jura, France (Dufraisse 2008), and by the late France of ash being planted as hedging along ditches and Mesolithic–early Neolithic in north-west Belgium (Deforce drainage canals from the beginning of the 19th century (Girel, et al. 2013), and Mesolithic and Neolithic in the Netherlands Garguet-Duport & Pautou 1997). But according to Rackham (Out 2010), and in Dorset from the Neolithic (Salisbury & Jane (2014), ‘The twentieth century was kind to ash’, since this is 1940). It is still highly prized as firewood primarily due to the when it underwent a large expansion in Britain and across high levels of oleic acid, a flammable fatty acid enabling it to mainland Europe east into Russia (Hofmeister, Mihaljevic& burn even when green (Thomas 2014). Hosek 2014), and many of our beloved ash woodlands in the Ash was also used for building, originally through the use Mendips, Derbyshire and Shropshire first came into existence of coppiced wood. Of the 1286 timbers excavated at a (Pigott & Pigott 1959) for the reasons listed above, with the Neolithic lake site in south-west Germany, 52% were ash addition in Britain that introduced grey squirrels have compared to the next most common species, ‘maple’ at 10% prevented hazel from being a competitor (Rackham 2014). (Million & Billamboz 2011). In the Sweet Track in Somerset Certainly, Mullerov€ a, Hedl & Szabo (2015) showed that after (c. 5800 BP), ash forms around 10% of the coppiced wood coppice was abandoned in the Czech Republic early in the used (Hillam et al. 1990; Rackham 2014). In the historic per- 20th century, ash increased in abundance. iod, although John Evelyn (1664) claimed ‘The use of ash (next to that of the oak itself) [is] one of the most universal’, Rackham (2014) was of the opinion that ash was a low-status USES material since it was not used in church carpentry or similar, Ash has a long cultural history (Scheer 2001; Bell et al. 2008) but was used for such things as wattle; in East Anglia, ash and forms the world ash tree of Yggdrasil of Norse mythology wattle rods were less common than those of Salix spp. and

Corylus avellana but still made up 18% of the number used. severe diseases, such as the bacteria-caused ash yellows (IX Ash has, however, been used for shipbuilding (boat frames (C)), that could be major future problems in Europe. and tenon pegs) (Sadori et al. 2015) and for musical instru- Without these threats, ash would, ironically, otherwise ments, particularly guitars (Puszynski, Molinski & Preis appear to be doing well since it is becoming increasingly 2015) and, along with other ring-porous woods, as shock- common in many parts of Europe. In 2003–2004, Amar et al. resistant handles for tools. (2010) resurveyed 249 sites scattered through England, Scot- Though most ash trees in the British Isles are from natural land and Wales originally surveyed in 1980. They found that regeneration, it is often planted for ornament, shelter and tim- ash had increased in frequency in both the canopy and shrub ber (Wardle 1961). Ash was ‘among the earliest non-fruit layers in many woodlands in a band from South Wales to trees known to be planted’ (Rackham 2014) and has been Suffolk and also in Argyll. In other sites, ash showed no used extensively for forestry particularly on fertile soils in the change, but in none had it decreased. Other such increases west where it can produce valuable timber in relatively short have been reported in the UK countryside survey between rotations of 70 years or less (Kerr & Cahalan 2004; Savill 1998 and 2007 (Carey et al. 2009) and in permanent plots in 2015) or in continuous cover forestry (Djomo 2014) by either Wytham Woods, Oxfordshire, from the 1950s onwards planting or direct seeding (Willoughby et al. 2004). The qual- (Mihok et al. 2009; Kirby et al. 2014) including faster diame- ity of ash timber declines to the east of its range and in Iran ter growth in ash compared to competitor species. Similar it is a very poor forestry tree (Yousefi et al. 2013). Reviews changes have been reported in mainland north-west Europe, of growing ash as a forestry tree can be found in Kerr (2004), possibly due to the ability of ash to utilize the growing nitro- Kerr & Cahalan (2004) and Maltoni et al. (2010), and prun- gen inputs from pollution (Hofmeister, Mihaljevic&Hosek ing for maximum useful production in Danescu et al. (2015). 2014) allied to its invasion of less intensively used agricul- As noted above, ash foliage was used as a year-round fod- tural land in more marginal areas (Marigo et al. 2000; Strestil der for sheep and goats (Loudon 1838; Rasmussen 1989; Del- & Sammonil 2006). As outlined in VIII(C), genetic vitality, hon et al. 2008). Ash keys have also been pickled in vinegar even between fragmented ash woodlands, does not appear to for human use (Rackham 2014). Humans have also eaten a be a problem for its long-term future. Moreover short-term sweet exudate – manna – from damaged bark (Dumont climate change would appear to be beneficial to ash. 1992). It acts as a sweetener and mild laxative. The composi- In mainland Europe, several forest types are protected tion of manna is given in VI(F). under the Habitat Directive of the European Union, Directive Extracts of leaves and bark of F. excelsior have been 92/43 (Commission of the European Communities 2007), part of traditional herbal medicine since Hippocrates’ time designated primarily because they were considered to be of for a number of conditions including rheumatism, inflamma- high conservation value. These include alluvial forests with tion, diarrhoea, dysentery, gout, gallstones and intestinal F. excelsior and Alnus glutinosa (Alno-Padion, Annex I: worms (El-Ghazaly et al. 1992; Middleton et al. 2005; 44.3, Natura 2000 code: 91E0) and mixed ravine forests Corp & Pendry 2013; Flanagan et al. 2013). Soluble gly- dominated by Acer pseudoplatanus with F. excelsior, Ulmus coside extracts from ash seeds and fruits have also been glabra and Tilia cordata (Tilio-Acerion, Annex I: 44.4, Nat- shown to be highly effective in reducing blood glucose ura 2000 code: 9180). The severe risk to ash from ash die- levels without significantly affecting insulin levels and so back is such that in 2010, the Swedish Species Information can be used for the treatment of hypertension, obesity and Centre placed ash on the list of threatened species (G€arden- diabetes (Bai et al. 2010; Zulet et al. 2014; Gomez-Garcia fors 2010). et al. 2015). Extracts are known to be inhibitory to bacte- If the loss of ash due to ash dieback and the emerald ash rial and fungal growth (Middleton et al. 2005; Kostova & borer becomes severe, which appears highly probable, this Iossifova 2007). Linnaeus suggested that the bark of ash will cause large-scale change to many communities (see III) had some effects on malaria, and Aydin-Schmidt, Thorsell and many associated organisms will also decline (Pautasso & Wahlgren (2010) confirmed that lipo- and hydrophilic et al. 2013) including lichens (Jonsson€ & Thor 2012; Ellis extracts of the bark were effective against in vitro cultures et al. 2013; Lohmus~ & Runnel 2014), insects (Littlewood of the malaria parasite Plasmodium falciparum. Parveen et al. 2015) and fungi specifictoF. excelsior (see IV (B) and et al. (2015) generated silver nanoparticles from aqueous IX(C)). More generally, Mitchell et al. (2014a) suggests that leaf extracts of ash that may prove useful in delivering the 1058 species are associated with ash or ash woodland includ- above therapeutic benefits. Wood dust can cause occasional ing 12 birds, 55 mammals, 78 vascular plants, 58 bryophytes, occupational asthma and rhinitis (Fernandez-Rivas, Perez- 68 fungi, 239 invertebrates and 548 lichens species, many of Carral & Senent 1997). which are threatened or endangered. Of these species, 44 are considered obligate on living or dead ash (4 lichens, 11 fungi and 19 invertebrate species) and another 62 are ‘highly asso- XI. Conservation ciated’ with ash (13 lichens, 19 fungi, 6 bryophytes and 24 Ash faces a number of serious problems; most immediate is invertebrates) and these are most likely to decline in number ash dieback (IX(C)) but the emerald ash borer (IX(A)) will be and potentially become locally extinct. Measures to mitigate potentially as devastating, if not more so, as it progresses these losses are given under IX(C). In response to Pautasso westwards across Europe. Added to this are a number of other et al. (2013), Heilmann-Clausen & Bruun (2013) suggest that

© 2016 The Authors. Journal of Ecology © 2016 British Ecological Society, Journal of Ecology Fraxinus excelsior 39 all may not be completely lost as woodlands become tem- requirement and phenotypic plasticity not to be affected by porarily more open with a wider range of niches. warmer winter temperatures in medium-term climate change scenarios. Ash will in fact benefit from climate change because the growing season is likely to become longer espe- CLIMATE CHANGE cially among anemophilous species like ash (Gordo & Sanz The drought tolerance and sensitivity to frost will help ash 2009). Hamunyela et al. (2013) observed that between 2000 respond well to climate change (Percival, Keary & Al-Habsi and 2010, there was earlier leafing out of ash across western 2006; Scherrer, Bader & Korner€ 2011). Modelling of climate Europe in response to increasing spring temperatures. More- change within Britain suggests that ash will initially do well. over, Vitasse et al. (2009b) compared flushing dates between Broadmeadow & Jackson (2000) grew 1-year-old seedlings of 1976 and 1984 along elevational gradients in the French Pinus sylvestris, Quercus petraea and ash in outdoor open Pyrenees and found that leaf flushing moved earlier by À1 À1 top chambers in a factorial experiment of 92 ambient CO2 6.6 days °C for ash compared to 1.9 days °C for F. syl- (700 ppm), 92 ambient ozone (20 ppb overnight, rising to a vatica and 5.0 days °CÀ1 for A. pseudoplatanus. From this, it peak of 100 ppb during the day) and irrigation. In ash, irriga- is concluded that ash has high phenotypic plasticity in tion and elevated CO2 increased growth by c. 60% and 20%, response to temperature and therefore should respond favour- respectively, while the increased ozone levels had no signifi- ably to temperature changes. Vitasse et al. (2013) also cant effect. Increases in growth from CO2 fertilization were showed that ash readily produced seedlings and saplings similar to that seen in the other two species. But by the third above the current altitudinal limit for adults, and so ash year, increased CO2 had a negative effect on ash, was neutral should readily increase its range altitudinally and latitudinally in P. sylvestris and was still positive in Q. petraea; the poor in response to climate change. long-term performance of ash was attributable to a nitrogen Ash may replace Fagus sylvatica in forestry in southern deficiency in this nitrophilous species, which may be less of a England, and there will be more sites for growing high-qual- bottleneck in the future as nitrogen pollution increases. ity ash in northern Britain (Broadmeadow & Ray 2005; Indeed, Bloor, Barthes & Leadley (2008) noted that under Broadmeadow, Ray & Samuel 2005). Indeed, ash may show elevated CO2, ash seedlings showed a marginally significant increased productivity in south-east and north-east England biomass increase irrespective of any N supplementation. and much of Scotland though with some loss of productivity Crookshanks, Taylor & Broadmeadow (1998) observed that in west England and a major loss (predicted to fall below 3 À1 À1 doubling CO2 from pre-industrial levels led to a rapid growth 4m ha year ) in the fenlands of east England due to response of roots in fast-growing species like ash. Root length increased moisture deficits. With further climate change, ash under elevated CO2 (as a ratio with ambient CO2) increased may in turn be replaced by Quercus robur (Broadmeadow, 3.40 over 6 months in ash compared to 1.95 in Quercus pet- Ray & Samuel 2005). raea. However, total dry mass of roots of the whole tree over Ash may also be beneficial in reducing climate change. 8 months was smallest in ash, indicating less investment in sus- There is some evidence that ash root interactions with the soil tained root growth. Saxe & Kerstiens (2005) found that ele- reduce N2O soil emissions (a potent glasshouse gas) by 94– vated temperature (+2.8 °C) and CO2 (c. +373 ppm) had a 98%, much more than does F. sylvatica (Fender et al. 2013). positive synergistic effect on ash seedlings compared to F. syl- Afforestation of grassland with ash in Ireland led to an vatica due to increased root mass and height growth, particu- increase in the total ecosystem C from 90.2 Mg C haÀ1 in larly in shade equivalent to being below a canopy of trees. the grassland to 162.6 Mg C haÀ1 in 47-year-old forest; the Under current conditions, ash gains a competitive advantage soil lost C but the above-ground biomass gain outweighed over F. sylvatica by arching the new leaves upwards to gain this (Wellock et al. 2014). extra light, but they found that under elevated conditions, ash relied more on building a denser area of leaves, shading the lower parts of the beech. They concluded that ash is likely to Acknowledgements become more competitive and increase at the expense of F. syl- Harvard University is gratefully acknowledged for providing time and space to vatica. Moreover, the ability of ash to maintain a slow but read, think and write as part of a Bullard Fellowship at Harvard Forest. My steady transpiration stream during water shortage (VI(E)) and thanks to the many people at Harvard and elsewhere who spent time sharing having an open canopy aiding air movement will help keep the their knowledge. Tony Davy is especially thanked for providing the opportunity fl À ° for updating an older Biological Flora of the British Isles accounts. The in u- canopy 0.5 1.5 C cooler than trees such as Acer pseudopla- ence of the late Professor John Packham is deeply embedded throughout this tanus and F. sylvatica (Scherrer, Bader & Korner€ 2011), fur- manuscript. ther increasing the competitive advantage of ash. et al. As noted in VII above, Laube (2014) showed that References ash had a short requirement for winter chilling. Clark (2013) conducted a reciprocal transplant experiment over a 2000 km Abdul-Hamid, H. & Mencuccini, M. (2009) Age- and size-related changes in physiological characteristics and chemical composition of Acer pseudopla- transect from the south of France to Scotland and found that tanus and Fraxinus excelsior trees. Tree Physiology, 29,27–38. while chilling requirement increased northerly, it was fully Adamcıkova, K., Kadasi-Horakova, M., Jankovsky, L. & Havrdova, L. (2015) met in all provenances. Thus, she concluded that all prove- Identification of Hymenoscyphus fraxineus, the causal agent of ash dieback in Slovakia. Biologia, 70, 559–564. nances had sufficient genetic variation in winter chilling

Aksoy, A. & Demirezen, D. (2006) Fraxinus excelsior as a biomonitor of Baliuckas, V., Ekberg, I., Eriksson, G. & Norell, L. (1999) Genetic variation heavy metal pollution. Polish Journal of Environmental Studies, 15,27–33. among and within populations of four Swedish hardwood species assessed in Albert, B., Morand-Prieur, M.-E., Brachet, S., Gouyon, P.-H., Frascaria-Lacoste, a nursery trial. Silvae Genetica, 48,17–25. N. & Raquin, C. (2013) Sex expression and reproductive biology in a tree spe- Ballach, H.-J., Wittig, R. & Wulff, S. (2002) Twenty-five years of biomonitor- cies, Fraxinus excelsior L. Comptes Rendus Biologies, 336, 479–485. ing lead in the Frankfurt/Main area. Environmental Science & Pollution Alberti, G., Candido, P., Peressotti, A., Turco, S., Piussi, P. & Zerbi, G. (2005) Research, 9, 136–142. Aboveground biomass relationships for mixed ash (Fraxinus excelsior L. and Bamford, K.F. & Van Rest, E.D. (1936) The relationship between chemical Ulmus glabra Hudson) stands in Eastern Prealps of Friuli Venezia Giulia composition and mechanical strength in the wood of English ash (Fraxinus (Italy). Annals of Forest Science, 62, 831–836. excelsior Linn.). Biochemical Journal, 30, 1849–1854. Alford, D.V. (2012) Pests of Ornamental Trees, Shrubs and Flowers: A Color Baral, H.-O. & Bemmann, M. (2014) Hymenoscyphus fraxineus vs. Handbook. Academic Press, New York, NY, USA. Hymenoscyphus albidus – A comparative light microscopic study on the cau- Allen, A.A. (1966) The rarer Sternoxia (Col.) of Windsor Forest. Entomolo- sal agent of European ash dieback and related foliicolous, stroma-forming gist’s Records, 78,14–23. species. Mycology, 5, 228–290. Allen, J.R.M., Watts, W.A. & Huntley, B. (2000) Weichselian palynostratigra- Baral, H.-O., Queloz, V. & Hosoya, T. (2014) Hymenoscyphus fraxineus, the phy, palaeovegetation and palaeoenvironment; the record from Lago Grande correct scientific name for the fungus causing ash dieback in Europe. IMA di Monticchio, southern Italy. Quaternary International, 73,91–110. Fungus, 5,79–80. Amar, A., Smith, K.W., Butler, S., Lindsell, J.A., Hewson, C.W., Fuller, R.J. Baranchikov, Y., Mozolevskaya, E., Yurchenko, G. & Kenis, M. (2008) Occur- & Charman, E.C. (2010) Recent patterns of change in vegetation structure rence of the emerald ash borer, Agrilus planipennis in Russia and its poten- and tree composition of British broadleaved woodland: evidence from large- tial impact on European forestry. EPPO Bulletin, 38, 233–238. scale surveys. Forestry, 83, 345–356. Barigah, T.S., Ibrahim, T., Bogard, A., Faivre-Vuillin, B., Lagneau, L.A., Andersson, P.F., Johansson, S.B.K., Stenlid, J. & Broberg, A. (2010) Isolation, Montpied, P. & Dreyer, E. (2006) Irradiance-induced plasticity in the hydrau- identification and necrotic activity of viridiol from Chalara fraxinea, the fun- lic properties of saplings of different temperate broad-leaved forest tree spe- gus responsible for dieback of ash. Forest Pathology, 40,43–46. cies. Tree Physiology, 26, 1505–1516. Angiolini, C., Foggi, B. & Viciani, D. (2012) Acer-Fraxinus dominated woods Barrington, R.M. & Vowell, R.P. (1884–1888) Report on the Flora of Ben Bul- of the Italian peninsula: a floristic and phytogeographical analysis. Acta Soci- ben and the adjoining mountain range in Sligo and Leitrim. Proceedings of etatis Botanicorum Poloniae, 81, 123–130. the Royal Irish Academy, Science, 4, 493–517. Arbellay, E., Fonti, P. & Stoffel, M. (2012) Duration and extension of anatomi- Barthod, S., Cerovic, Z. & Epron, D. (2007) Can dual chlorophyll fluorescence cal changes in wood structure after cambial injury. Journal of Experimental excitation be used to assess the variation in the content of UV-absorbing phe- Botany, 63, 3271–3277. nolic compounds in leaves of temperate tree species along a light gradient? Arca, M., Hinsinger, D.D., Cruaud, C., Tillier, A., Bousquet, J. & Frascaria- Journal of Experimental Botany, 58, 1753–1760. Lacoste, N. (2012) Deciduous trees and the application of universal DNA Barthod, S. & Epron, D. (2005) Variations of construction cost associated to barcodes: a case study on the circumpolar Fraxinus. PLoS One, 7, e34089. leaf area renewal in saplings of two co-occurring temperate tree species (Acer Atkinson, C.J. & Denne, M.P. (1988) Reactivation of vessel production in ash platanoides L. and Fraxinus excelsior L.) along a light gradient. Annals of (Fraxinus excelsior L) trees. Annals of Botany, 61, 679–688. Forest Science, 62, 545–551. Aussenac, G. & Levy, G. (1983) Influence du dessechement du sol sur le com- Bates, J.W. (1992) Influence of chemical and physical factors on Quercus and portement hydrique et la croissance du chêne pedoncule(Quercus peduncu- Fraxinus epiphytes at Loch Sunart, western Scotland: a multivariate analysis. lata Ehrl.) et du frêne (Fraxinus excelsior L.) cultives en cases de vegetation. Journal of Ecology, 80, 163–179. Annales des Sciences Forestieres, 40, 251–264. Bates, J.W. & Brown, D.H. (1981) Epiphyte differentiation between Quercus Aussenac, G. & Levy, G. (1992) Les exigences en eau du frêne (Fraxinus petraea and Fraxinus excelsior trees in a maritime area of South West Eng- excelsior L.). Revue Forestiere Francaise, 44,32–38. land. Vegetatio, 48,61–70. Aydin-Schmidt, B., Thorsell, W. & Wahlgren, M. (2010) Carolus Linnaeus, the Beatty, G.E., Brown, J.A., Cassidy, E.M., Finlay, C.M.V., McKendrick, L., ash, worm-wood and other anti-malarial plants. Scandinavian Journal of Montgomery, W.I., Reid, N., Tosh, D.G. & Provan, J. (2015) Lack of Infectious Diseases, 42, 941–942. genetic structure and evidence for long-distance dispersal in ash (Fraxinus Bacles, C.F.E., Burczyk, J., Lowe, A.J. & Ennos, R.A. (2005) Historical and excelsior) populations under threat from an emergent fungal pathogen: contemporary mating patterns in remnant populations of the forest tree Fraxi- implications for restorative planting. Tree Genetics & Genomes, 11, arti- nus excelsior L. Evolution, 59, 979–990. cle 53. Bacles, C.F.E. & Ennos, R.A. (2008) Paternity analysis of pollen-mediated Bedford, the Duke of & Pickering, S.U. (1919) Science and Fruit Growing. gene flow for Fraxinus excelsior L. in a chronically fragmented landscape. Macmillan, London, UK. Heredity, 101, 368–380. Bell, S., McLoughlin, J., Reeg, T., Gavaland, A., Muehlthaler, U., Makinen, K. Bacles, C.F.E., Lowe, A.J. & Ennos, R.A. (2006) Effective seed dispersal et al. (2008) Cultural Aspects of the Trees in Selected European Countries. across a fragmented landscape. Science, 311, 628. VALBRO, COST E42, Valuable Broadleaved Tree Species in Europe. Bai, N., He, K., Ibarra, A., Bily, A., Roller, M., Chen, X. & Ruhl,€ R. (2010) COST, Brussels, Belgium. http://bibliotecadigital.ipb.pt/handle/10198/3913 Iridoids from Fraxinus excelsior with adipocyte differentiation-inhibitory and (accessed 8 October 2015). PPARr activation activity. Journal of Natural Products, 73,2–6. Bengtsson, S.B.K., Barklund, P., von Bromssen,€ C. & Stenlid, J. (2014) Sea- Bakys, R., Vasaitis, R., Barklund, P., Thomsen, I.M. & Stenlid, J. (2009a) sonal pattern of lesion development in diseased Fraxinus excelsior infected Occurrence and pathogenicity of fungi in necrotic and non-symptomatic by Hymenoscyphus pseudoalbidus. PLoS One, 9, e76429. shoots of declining common ash (Fraxinus excelsior) in Sweden. European Bengtsson, S.B.K., Vasaitis, R., Kirisits, T., Solheim, H. & Stenlid, J. (2012) Journal of Forest Science, 128,51–60. Population structure of Hymenoscyphus pseudoalbidus and its genetic rela- Bakys, R., Vasaitis, R., Barklund, P., Ihrmark, K. & Stenlid, J. (2009b) Investi- tionship to Hymenoscyphus albidus. Fungal Ecology, 5, 147–153. gations concerning the role of Chalara fraxinea in declining Fraxinus excel- Bengtsson, V., Stenstrom,€ A. & Finsberg, C. (2013) The impact of ash dieback sior. Plant Pathology, 58, 284–292. on veteran and pollarded trees in Sweden. Quarterly Journal of Forestry, Bakys, R., Vasaitis, R. & Skovsgaard, J.P. (2013) Patterns and severity of 107,27–33. crown dieback in young even-aged stands of European ash (Fraxinus excel- Bennett, K.D., Boreham, S., Sharp, M.J. & Switsur, V.R. (1992) Holocene his- sior L.) in relation to stand density, bud flushing phenotype, and season. tory of environment, vegetation and human settlement on Catta Ness, Lun- Plant Protection Science, 49, 120–126. nasting, Shetland. Journal of Ecology, 80, 241–273. Bakys, R., Vasiliauskas, A., Ihrmark, K., Stenlid, J., Menkis, A. & Vasaitis, R. Bergqvist, G., Bergstrom,€ R. & Wallgren, M. (2012) Browsing by large herbi- (2011) Root rot, associated fungi and their impact on health condition of vores on Scots pine (Pinus sylvestris) seedlings in mixture with ash (Fraxi- declining Fraxinus excelsior stands in Lithuania. Scandinavian Journal of nus excelsior) or silver birch (Betula pendula). Scandinavian Journal of Forest Research, 26, 128–135. Forest Research, 27, 372–378. Balandier, P. & Dupraz, C. (1999) Growth of widely spaced trees. A case study Berveiller, D., Kierzkowski, D. & Damesin, C. (2007) Interspecific variabil- from young agroforestry plantations in France. Agroforestry Systems, 43, ity of stem photosynthesis among tree species. Tree Physiology, 27,53– 151–167. 61. Balandier, P. & Marquier, A. (1998) Vers une remise en question des Besnard, G. & Carlier, G. (1990) Potentiel hydrique et conductance stomatique avantages d’une plantation frêne – aulne. Revue Forestiere Francaise, 50, des feuilles de frêne (Fraxinus excelsior L.) dans une forêt alluviale du Haut- 231–243. Rhone^ francais. Annals of Forest Science, 47, 353–365.

Bettiati, D., Petit, G. & Anfodillo, T. (2012) Testing the equi-resistance princi- Broadmeadow, M.S.J., Ray, D. & Samuel, C.J.A. (2005) Climate change and ple of the xylem transport system in a small ash tree: empirical support from the future for broadleaved tree species in Britain. Forestry, 78, 145–161. anatomical analyses. Tree Physiology, 32, 171–177. Brooks, F.T. (1953) Plant Diseases, 2nd edn. Oxford University Press, Oxford, Beyer, F., Hertel, D., Jung, K., Fender, A.-C. & Leuschner, C. (2013) Competi- UK. tion effects on fine root survival of Fagus sylvatica and Fraxinus excelsior. Brostrom,€ A., Nielsen, A.B., Gaillard, M.J., Hjelle, K., Mazier, F., Binney, H. Forest Ecology and Management, 302,14–22. et al. (2008) Pollen productivity estimates of key European plant taxa for Binggeli, P. & Power, A.J. (1991) Gender variation in ash (Fraxinus excelsior quantitative reconstruction of past vegetation: a review. Vegetation History L.). Miscellaneous Notes and Reports in Natural History, Ecology, Conserva- and Archaeobotany, 17, 461–478. tion and Resources Management. http://www.mikepalmer.co.uk/woodyplante- Brotherton, D.I. (1973) The Management of a Woodland Nature Reserve With cology/docs/MNR-ashgender.pdf (Accessed 08 October 2015). Particular Reference to the Cohabitation of Tree Species. Discussion Paper Binney, H.A., Wallera, M.P., Bunting, M.J. & Armitage, R.A. (2005) The in Conservation No. 6, University College London, London, UK. interpretation of fen carr pollen diagrams: The representation of the dry land Brullo, S. & Spampinato, G. (1999) Syntaxonomy of hygrophilous woods of vegetation. Review of Palaeobotany and Palynology, 134, 197–218. the Alno-Quercion roboris. Annali di Botanica, 57, 133–146. Bittner, S., Janott, M., Ritter, D., Kocher,€ P., Beese, F. & Priesack, E. (2012) Bulır, P. (2007) Effects of varying doses of Frisol on European ash (Fraxinus Functional–structural water flow model reveals differences between diffuse- excelsior L.) planted on spoil banks. Journal of Forest Science, 53,35–40. and ring-porous tree species. Agricultural and Forest Meteorology, 158–159, Bunting, M.J., Armitage, R.A., Binney, H.A. & Waller, M.P. (2005) Estimates 80–89. of relevant source area of pollen assemblages from moss polsters in two Nor- Bjørnlund, L. & Christensen, S. (2005) How does litter quality and site hetero- folk (UK) woodlands. The Holocene, 15, 459–465. geneity interact on decomposer food webs of a semi-natural forest? Soil Biol- Burggraaf, P.D. (1972) Some observations on the course of the vessels in the ogy and Biochemistry, 37, 203–213. wood of Fraxinus excelsior L. Acta Botanica Neerlandica, 21,32–47. Blackstock, T.H. (2013) Synchronised variation in fruit production in Fraxinus Bussotti, F., Agati, G., Desotgiu, R., Matteini, P. & Tani, C. (2005) Ozone excelsior (Ash). Botanical Society of the British Isles News, 123,15–16. foliar symptoms in woody plants assessed with ultrastructural and fluores- Blake, P.S., Taylor, J.M. & Finch-Savage, W.E. (2002) Identification of absci- cence analysis. New Phytologist, 166, 941–955. sic acid, indole-3-acetic acid, jasmonic acid, indole-3-acetonitrile, methyl jas- Buston, H.W. & Hopf, H.S. (1938) Note on certain carbohydrate constituents monate and gibberellins in developing, dormant and stratified seeds of ash of the bark of ash (Fraxinus excelsior). Biochemical Journal, 32,44–46. (Fraxinus excelsior). Plant Growth Regulation, 37, 119–125. Caligiani, A., Tonelli, L., Palla, G., Marseglia, A., Rossi, D. & Bruni, R. (2013)

Bloor, J.M.G., Barthes, L. & Leadley, P.W. (2008) Effects of elevated CO2 and Looking beyond sugars: Phytochemical profiling and standardization of manna N on tree–grass interactions: an experimental test using Fraxinus excelsior exudates from Sicilian Fraxinus excelsior L. Fitoterapia, 90,65–72. and Dactylis glomerata. Functional Ecology, 22, 537–546. Callesen, I., Nilsson, L.O., Schmidt, I.K., Vesterdal, L., Ambus, P., Chris- Bloor, J.M.G., Leadley, P.W. & Barthes, L. (2008) Responses of Fraxinus tiansen, J.R., Hogberg,€ P. & Gundersen, P. (2013) The natural abundance of excelsior seedlings to grass-induced above- and below-ground competition. 15N in litter and soil profiles under six temperate tree species: N cycling Plant Ecology, 194, 293–304. depends on tree species traits and site fertility. Plant and Soil, 368, 375–392. Blujdea, V.N.B., Pilli, R., Dutca, I., Ciuvat, L. & Abrudan, I.V. (2012) Allo- Capuana, M., Petrini, G., Di Marco, A. & Giannini, R. (2007) Plant regenera- metric biomass equations for young broadleaved trees in plantations in tion of common ash (Fraxinus excelsior L.) by somatic embryogenesis. In Romania. Forest Ecology and Management, 264, 172–184. Vitro Cellular & Developmental Biology-Plant, 43, 101–110. Bochenek, G.M. & Eriksen, B. (2010) Annual growth of male and female indi- Carcaillet, C. & Brun, J.J. (2000) Changes in landscape structure in the north- viduals of the common ash (Fraxinus excelsior L.). Plant Ecology and western Alps over the last 7000 years: lessons from soil charcoal. Journal of Diversity, 3,47–57. Vegetation Science, 11, 705–714. Bochenek, G.M. & Eriksen, B. (2011) First come, first served: delayed fertiliza- Carey, P.D., Wallis, S., Chamberlain, P.M., Cooper, A., Emmett, B.A., Mas- tion does not enhance pollen competition in a wind-pollinated tree, Fraxinus kell, L.C. et al. (2009) Countryside Survey: UK Results From 2007. NERC/ excelsior L. (Oleaceae). International Journal of Plant Sciences, 172,60–69. Centre for Ecology & Hydrology, Wallingford, UK. Boddy, L., Gibbon, O.M. & Grundy, M.A. (1985) Ecology of Daldinia concen- Carlier, G., Peltier, J.P. & Gielly, L. (1992) Comportement hydrique du frêne trica: effect of abiotic variables on mycelial extension and interspecific inter- (Fraxinus excelsior L.) dans une formation montagnarde mesoxerophile. actions. Transactions of the British Mycological Society, 85, 201–211. Annales des Sciences Forestieres, 49, 207–223. Bogenrieder, A. & Klein, R. (1982) Does solar UV influence the competitive Carnat, A., Lamaison, J.L. & Duband, F. (1990) Contents of the main con- relationship in higher plants? The Role of Solar Ultraviolet Radiation in stituents of ash leaves Fraxinus excelsior L. Plantes Medicinales et Phy- Marine Ecosystems (ed. J. Calkins), pp. 54–71. Plenum Press, New York, totherapie, 24, 145–151. NY, USA. Cartwright, K.G., Campbell, W.G. & Armstrong, F.H. (1936) The influence of Boodle, L.A. (1915) Abnormal phyllotaxy in the ash. Annals of Botany, 24, fungal decay on the properties of timber. I – The effect of progressive decay 307–308. by Polyporus hispidus, Fr., on the strength of English ash (Fraxinus excelsior Borowski, S., Krasinski, Z. & Miłkowski, L. (1967) Food and role of the Euro- L.). Proceedings of the Royal Society of London. Series B, 120,76–95. pean bison in Forest Ecosystems. Acta Theriologica, 12, 367–376. Catinon, M., Ayrault, S., Boudouma, O., Asta, J., Tissut, M. & Ravanel, P. Borowski, Z. (2007) Damage caused by rodents in Polish forests. International (2009) The inclusion of atmospheric particles into the bark suber of ash trees. Journal of Pest Management, 53, 303–310. Chemosphere, 77, 1313–1320. Boshier, D. & Stewart, J. (2005) How local is local? Identifying the scale of Catinon, M., Ayrault, S., Daudin, L., Sevin, L., Asta, J., Tissut, M. & Ravanel, P. adaptive variation in ash (Fraxinus excelsior L.): results from the nursery. (2008) Atmospheric inorganic contaminants and their distribution inside stem Forestry, 78, 135–143. tissues of Fraxinus excelsior L. Atmospheric Environment, 42, 1223–1238. Bourne, R. (1945) Neglect of natural regeneration. Forestry, 19,33–40. Cerm ak, P. & Mrkva, R. (2006) Effects of game on the condition and develop- Braun-Blanquet, J. & Tuxen, R. (1952) Irische Pflanzengesellschaften. Die ment of natural regeneration in the Vrapac National Nature Reserve Pflanzenwelt Irlands (ed. W. Ludi),€ Hans Huber, Bern. Veroffentlichungen€ (Litovelske Pomoravı). Journal of Forest Science, 52, 329–336. des geobotanischen Institutes Rubel€ in Zurich€ , 25, 224–415. Cesarz, S., Fender, A.-C., Beyer, F., Valtanen, K., Pfeiffer, B., Gansert, D., Breuste, J.H. (2013) Investigations of the urban street tree forest of Mendoza, Hertel, D., Polle, A., Daniel, R., Leuschner, C. & Scheu, S. (2013) Roots Argentina. Urban Ecosystems, 16, 801–818. from beech (Fagus sylvatica L.) and ash (Fraxinus excelsior L.) differentially Brewer, S. (2002) Recolonisation postglaciaire de quelques taxons temperes en affect soil microorganisms and carbon dynamics. Soil Biology & Biochem- Europe: une approche spatiale et temporelle. PhD thesis, Institut Mediter- istry, 61,23–32. raneen d’Ecologie et de Paleoecologie, Marseille, France. Chandelier, A., Andre, F. & Laurent, F. (2010) Detection of Chalara fraxinea British Ash Tree Genome Project (2015) http://www.ashgenome.org/ (Accessed in common ash (Fraxinus excelsior) using real time PCR. Forest Pathology, 8 October 2015). 40,87–95. British Mycological Society (2016) Fungal Records Database http://www.field- Chandelier, A., Helson, M., Dvorak, M. & Gischer, F. (2014) Detection and mycology.net/frdbi/frdbi.asp (Accessed 12 January 2016). quantification of airborne inoculum of Hymenoscyphus pseudoalbidus using Broadmeadow, M. & Ray, D. (2005) Climate Change and British Woodland. For- real-time PCR assays. Plant Pathology, 63, 1296–1305. estry Commission Information Note 69, Forestry Commission, Edinburgh, UK. Charlton, N.L. & Memmott, J. (2013) Impact of Chalara Dieback of Ash on Broadmeadow, M.S.J. & Jackson, S.B. (2000) Growth responses of Quercus Community Function and Stability. Forestry Commission, Bristol, UK. petraea, Fraxinus excelsior and Pinus sylvestris to elevated carbon dioxide, Chater, A.O. (2010) Flora of Cardiganshire. Cambrian Printers, Aberystwyth, ozone and water supply. New Phytologist, 146, 437–451. UK.

Chen, J. (2012) Fungal Community Survey of Fraxinus excelsior in New Zealand. and timber properties. International Scientiﬁc Conference on Hardwood Pro- MSc thesis, Swedish University of Agricultural Sciences, Uppsala, Sweden. cessing (ISCHP 2013) (eds. S. Berti, A. Achim, M. Fioravanti, T. Lihra, Chevallier-Redor, N., Verheyen-Tixier, E., Verdier, M. & Dumont, B. (2001) V.L. Munoz,~ R. Marchal, J. Wiedenbeck & R. Zanuttini), pp. 70–76. Cnr- Foraging behaviour of red deer Cervus elaphus as a function of the relative Ivalsa Trees and Timber Institute, Florence, Italy.

availability of two tree species. Animal Research, 50,57–65. Crookshanks, M., Taylor, G. & Broadmeadow, M. (1998) Elevated CO2 and Chmielarz, P. (2009) Cryopreservation of dormant European ash (Fraxinus tree root growth: contrasting responses in Fraxinus excelsior, Quercus pet- excelsior) orthodox seeds. Tree Physiology, 29, 1279–1285. raea and Pinus sylvestris. New Phytologist, 138, 241–250. Christiansen, J.R., Vesterdal, L., Callesen, I., Elberling, B., Schmidt, I.K. & Culleton, N., Murphy, W.E. & McLoughlin, A. (1996) The use of fertilizers in Gundersen, A. (2010) Role of six European tree species and land-use legacy the establishment phase of common ash (Fraxinus excelsior L.). Irish For- for nitrogen and water budgets in forests. Global Change Biology, 6, 2224– estry, 53,28–35. 2240. Cundall, E.P., Cahalan, C.M. & Connolly, T. (2003) Early results of ash (Frax- Christianson, D. (1889) Observations on the annual increase in girth of trees in inus excelsior L.) provenance trials at sites in England and Wales. Forestry, the Royal Botanic Garden, and at Craigiehall, near Edinburgh. Transactions 76, 385–400. of the Botanical Society of Edinburgh, 17, 390–410. Dacasa Rudinger,€ M.C. & Dounavi, A. (2008) Underwater germination poten- Citron, C.A., Junker, C., Schulz, B. & Dickschat, D.S. (2014) A volatile lac- tial of common ash seed (Fraxinus excelsior L.) originating from flooded tone of Hymenoscyphus pseudoalbidus, pathogen of European ash dieback, and non-flooded sites. Plant Biology, 10, 382–387. inhibits host germination. Angewandte Chemie, 53, 4346–4349. Dal Maso, E., Fanchin, G., Mutto Accordi, S., Scattolin, L. & Montecchio, L. Claessens, H., Pauwels, D., Thibaut, A. & Rondeux, J. (1999) Site index curves (2012) Ultrastructural modifications in common ash tissues colonised by and autecology of ash, sycamore and cherry in Wallonia (Southern Belgium). Chalara fraxinea. Phytopathologia Mediterranea, 51, 599–606. Forestry, 72, 171–182. Damtoft, S., Franzyk, H. & Jensen, S.R. (1992) Excelsioside, a secoiridoid glu- Clark, J.R. (2013) The adaptation of ash (Fraxinus excelsior L.) to climate coside from Fraxinus excelsior. Phytochemistry, 31, 4197–4201. change. PhD thesis, Bangor University, UK. Danescu, A., Ehring, A., Bauhus, J., Albrecht, A. & Hein, S. (2015) Modelling Clarke, S.H. (1935) Recent work on the relation between anatomical structure discoloration and duration of branch occlusion following green pruning in and mechanical strength in English ash. Forestry, 9, 132–138. Acer pseudoplatanus and Fraxinus excelsior. Forest Ecology and Manage- Cleary, M.R., Andersson, P.F., Broberg, A., Elfstrand, M., Daniel, G. & Sten- ment, 335,87–98. lid, J. (2014) Genotypes of Fraxinus excelsior with different susceptibility to Davies, L., Bates, J.W., Bell, J.N.B., James, P.W. & Purvis, O.W. (2007) the ash dieback pathogen Hymenoscyphus pseudoalbidus and their response Diversity and sensitivity of epiphytes to oxides of nitrogen in London. Envi- to the phytotoxin viridiol – A metabolomic and microscopic study. Phyto- ronmental Pollution, 146, 299–310. chemistry, 102, 115–125. DBIF (2015) Database of Insects and their Food Plants. http://www.brc.ac.uk/ Cleary, M.R., Arhipova, N., Gaitnieks, T., Stenlid, J. & Vasaitis, R. (2013) dbif/homepage.aspx (Accessed 8 October 2015). Natural infection of Fraxinus excelsior seeds by Chalara fraxinea. Forest Deforce, K., Bastiaens, J., Van Neer, W., Ervynck, A., Lentacker, A., Sergant, Pathology, 43,83–85. J. & Crombe, P. (2013) Wood charcoal and seeds as indicators for animal Cochard, H., Peiffer, M., Le Gall, K. & Granier, A. (1997) Developmental con- husbandry in a wetland site during the late mesolithic–early neolithic transi- trol of xylem hydraulic resistances and vulnerability to embolism in Fraxinus tion period (Swifterbant culture, ca. 4600–4000 B.C.) in NW Belgium. Vege- excelsior L: impacts on water relations. Journal of Experimental Botany, 48, tation History and Archaeobotany, 22,51–60. 655–663. Delarze, R., Caldelari, D. & Hainard, P. (1992) Effects of fire on forest dynam- Collin, P., Badot, P.M. & Millet, B. (1994) Complete defoliation induces ics in southern Switzerland. Journal of Vegetation Science, 3,55–60. renewal of shoot elongation and temporary inhibition of radial growth in ash Delhon, C., Martin, L., Argant, J. & Thiebault, S. (2008) Shepherds and plants in the tree (Fraxinus excelsior L). Comptes Rendus de L’Academie des Sciences, Alps: multi-proxy archaeobotanical analysis of neolithic dung from “La Grande Riv- 317, 1005–1011. oire” (Isere, France). Journal of Archaeological Science, 35, 2937–2952. Collin, P., Badot, P.M. & Millet, B. (1995) Etude de la croissance et du Denman, S., Kirk, S., Whybrow, A., Orton, E. & Webber, J.F. (2006) Phytoph- developpement du frêne commun, Fraxinus excelsior, cultive en conditions thora kernoviae and P. ramorum: host susceptibility and sporulation potential control^ ees. Canadian Journal of Botany, 73, 1464–1470. on foliage of susceptible trees. EPPO Bulletin, 36, 373–376. Collin, P. & Badot, P.-M. (1997) Le point des connaissances relatives ala Desideri, D., Meli, M.A. & Roselli, C. (2010) Determination of essential and croissance et au developpement du Frêne commun (Fraxinus excelsior L.). non-essential elements in some medicinal plants by polarised X ray fluores- Acta Botanica Gallica, 144, 253–267. cence spectrometer (EDPXRF). Microchemical Journal, 95, 174–180. Collin, P., Epron, D., Alaoui-Sosse, B. & Badot, P.M. (2000) Growth responses Diekmann, M. (1994) Deciduous forest vegetation in Boreo-nemoral Scandi- of common ash seedlings (Fraxinus excelsior L.) to total and partial defolia- navia. Acta Phytogeographica Suecica, 80,1–116. tion. Annals of Botany, 85, 317–323. Diekmann, M. (1996) Ecological behaviour of deciduous hardwood trees in Commission of the European Communities (2007) Interpretation Manual of Boreo-nemoral Sweden in relation to light and soil conditions. Forest Ecol- European Union Habitats – EUR27. European Commission, DG Environ- ogy and Management, 6,l–14. ment, Brussels, Belgium. Diekmann, M., Eilertsen, O., Fremstad, E., Lawesson, J.E. & Aude, E. (1999) Coners, H. & Leuschner, C. (2002) In situ water absorption by tree fine roots Beech forest communities in the Nordic countries: a multivariate analysis. measured in real time using miniature sap-flow gauges. Functional Ecology, Plant Ecology, 140, 203–220. 16, 696–703. Djomo, A.N. (2014) Continuous cover forestry and harvest event analysis. Contran, N. & Paoletti, E. (2007) Visible foliar injury and physiological International Journal of Forestry and Wood Science, 1,10–26. responses to ozone in Italian provenances of Fraxinus excelsior and F. ornus. Dobrowolska, D., Hein, S., Oosterbaan, A., Wagner, S., Clark, J. & Skovs- The Scientific World, 7(S1), 90–97. gaard, J.P. (2011) A review of European ash (Fraxinus excelsior L.): impli- Conway, V.M. (1954) Stratigraphy and pollen analysis of southern Pennine cations for silviculture. Forestry, 84, 133–148. blanket peats. Journal of Ecology, 42, 117–147. Dolek, M., Freese-Hager, A., Geyer, A., Balletto, E. & Bonelli, S. (2013) Mul- Cooke, A.S. (1998) Survival and regrowth performance of coppiced ash (Fraxi- tiple oviposition and larval feeding strategies in Euphydryas maturna (Linne, nus excelsior) in relation to browsing damage by muntjac deer (Muntiacus 1758) (Nymphalidae) at two disjoint European sites. Journal of Insect Con- reevesi). Quarterly Journal of Forestry, 92, 286–290. servation, 17, 357–366. Cooke, A.S. & Farrell, L. (2001) Impact of muntjac deer (Muntiacus reevesi)at Dolinska, T.M. & Schollenberger, M. (2012) Cladosporium species as hyper- Monks Wood National Nature Reserve, Cambridgeshire, eastern England. parasites of powdery mildew fungi. Journal of Agricultural Sciences, 50 Forestry, 74, 241–250. (Suppl.), 24–28. Cornelissen, J.H.C., Cerabolini, B., Castro-Dıez, P., Villar-Salvador, P., Dolle,€ M. & Schmidt, W. (2009) Impact of tree species on nutrient and light Montserrat-Martı, G., Puyravaud, J.P., Maestro, M., Werger, M.J.A. & Aerts, availability: evidence from a permanent plot study of old-field succession. R. (2003) Functional traits of woody plants: correspondence of species rank- Plant Ecology, 203, 273–287. ings between field adults and laboratory-grown seedlings? Journal of Vegeta- Doody, C.N. & O’Reilly, C. (2011) Effect of long-phase stratification treat- tion Science, 14, 311–322. ments on seed germination in ash. Annals of Forest Science, 68, 139–147. Corp, N. & Pendry, B. (2013) The role of Western herbal medicine in the treat- Drenkhan, R. & Hanso, M. (2010) New host species for Chalara fraxinea. ment of gout. Journal of Herbal Medicine, 3, 157–170. Plant Pathology, 22, 16. Crivellaro, A., Giulietti, V., Brunetti, M. & Pelleri, F. (2013) European ash Drenkhan, R., Sander, H. & Hanso, M. (2014) Introduction of Mandshurian (Fraxinus excelsior L.) secondary woodlands in Italy: management systems ash (Fraxinus mandshurica Rupr.) to Estonia: Is it related to the current epi-

demic on European ash (F. excelsior L.)? European Journal of Forest emission by saplings of ash, but not of beech, in temperate forest soil. Euro- Research, 133, 769–781. pean Journal of Soil Biology, 54,7–15. Dreyer, E., Le Roux, X., Montpied, P., Daudet, F.A. & Masson, F. (2001) Fernandez de Simon, B., Martınez, J., Sanz, M., Cadahıa, E., Esteruelas, E. & Temperature response of leaf photosynthetic capacity in seedlings from seven Munoz,~ A.M. (2014) Volatile compounds and sensorial characterisation of temperate tree species. Tree Physiology, 21, 223–232. red wine aged in cherry, chestnut, false acacia, ash and oak wood barrels. Dufour, S. & Piegay, H. (2008) Geomorphological controls of Fraxinus excel- Food Chemistry, 147, 346–356. sior growth and regeneration in floodplain forests. Ecology, 89, 205–215. Fernandez-Manjarres, J.F., Gerard, P.R., Dufour, J., Raquin, C. & Frascaria- Dufraisse, A. (2008) Firewood management and woodland exploitation during Lacoste, N. (2006) Differential patterns of morphological and molecular the late Neolithic at Lac de Chalain (Jura, France). Vegetation History and hybridization between Fraxinus excelsior L. and Fraxinus angustifolia Vahl Archaeobotany, 17, 199–210. (Oleaceae) in eastern and western France. Molecular Ecology, 15, 3245– Dumont, D.J. (1992) The ash tree in Indo-European culture. The Mankind 3257. Quarterly, 1992, 323–336. Fernandez-Rivas, M., Perez-Carral, C. & Senent, C.J. (1997) Occupational Dzierzanowski,_ K., Popek, R., Gawronska, H., Sæbø, A. & Gawronski, S.W. asthma and rhinitis caused by ash (Fraxinus excelsior) wood dust. Allergy, (2011) Deposition of particulate matter of different size fractions on leaf sur- 52, 196–199. faces and in waxes of urban forest species. International Journal of Phytore- Ferrazzini, D., Monteleone, I. & Belletti, P. (2007) Genetic variability and mediation, 13, 1037–1046. divergence among Italian populations of common ash (Fraxinus excelsior Edmondson, J.L., O’Sullivan, O.S., Inger, R., Potter, J., McHugh, N., Gaston, L.). Annals of Forest Science, 64, 159–168. K.J. & Leake, J.R. (2014) Urban tree effects on soil organic carbon. PLoS Feurdean, A., Willis, K.J., Parr, C.L., Tantau, J. & Farcas, S. (2010) Post-gla- One, 9, e101872. cial patterns in vegetation dynamics in Romania: homogenization or differen- Eiberle, K. (1975) Ergebnisse einer Simulation des Wildverbisses durch den tiation? Journal of Biogeography, 37, 2197–2208. Triebschnitt. Schweizerische Zeitschrift fur€ Forstwesen, 126, 821–839. Filipova-Marinova, M., Pavlov, D., Coolen, M. & Giosan, L. (2013a) First Eiberle, K. (1979) Folgewirkungen eines simulierten Wildverbisses auf die high-resolution marinopalynological stratigraphy of Late Quaternary sedi- Entwicklung junger Waldb€aume. Schweizerische Zeitschrift fur€ Forstwesen, ments from the central part of the Bulgarian Black Sea area. Quaternary 129, 757–768. International, 293, 170–183. Eiberle, K. & Bucher, H. (1989) Interdependenzen zwischen dem Verbib ver- Filipova-Marinova, M., Pavlov, D., Vergiev, S., Slavchev, V. & Giosan, L. schiedener Baumarten in einem Plenterwaldgebiet. Zeitschrift f€ur Jagdwis- (2013b) Palaeoecology and Geoarchaeology of Varna Lake, Northeast- senschaft, 35, 235–244. ern Bulgaria. Proceeding of the Bulgarian Academy of Sciences, 66, 377– Einhorn, K.S., Rosenqvist, E. & Leverenz, J.W. (2004) Photoinhibition in seed- 392. lings of Fraxinus and Fagus under natural light conditions: implications for Finch-Savage, W.E. & Clay, H.A. (1997) The influence of embryo restraint forest regeneration? Oecologia, 140, 241–251. during dormancy loss and germination of Fraxinus excelsior seeds. Basic El-Ghazaly, M., Khayyal, M.T., Okpanyi, S.N. & Arens-Corell, M. (1992) and Applied Aspects of Seed Biology (eds R.H. Ellis, M. Black, A.J. Mur- Study of the anti-inflammatory activity of Populus tremula, Solidago virgau- doch & T.D. Hong), pp. 245–253. Kluwer Academic Publishers, Boston, rea and Fraxinus excelsior. Drug Research, 42, 333–336. MA, USA. Ellenberg, H., Weber, H.E., Dull,€ R., Wirth, V. & Werner, W. (1991) Zeigerw- Fischer, A., Fischer, H.S. & Lehnert, U. (2012) Avalanches creating high struc- erte von Pflanzen in Mitteleuropa. Scripta Geobotanica, 18,1–248. tural and floristic diversity in mountain mixed forests in the Alps. Biodiver- Ellis, C.J., Coppins, B.J., Eaton, S. & Simkin, J. (2013) Implications of ash sity and Conservation, 21, 643–654. dieback for associated epiphytes. Conservation Biology, 27, 899–900. Flanagan, J., Meyer, M., Pasamar, M.A., Ibarra, A., Roller, M., Alvarez i Ellis, C.J., Coppins, B.J. & Hollingsworth, P.M. (2012) Lichens under threat Genoher, N., Leiva, S., Gomez-Garcıa, F., Alcaraz, M., Martınez-Carrasco, from ash dieback. Nature, 491, 672. A. & Vicente, V. (2013) Safety evaluation and nutritional composition of a Emborg, J., Christensen, M. & Heilmann-Clausen, J. (2000) The structural Fraxinus excelsior seed extract, FraxiPureTM. Food and Chemical Toxicology, dynamics of Suserup Skov, a near-natural temperate deciduous forest in Den- 53,10–17. mark. Forest Ecology and Management, 126, 173–189. Floran, V. & Mihalte, L. (2010) The variability of peculiarities of samaras and Enderle, R., Nakou, A., Thomas, K. & Metzler, B. (2015) Susceptibility of seeds belonging to different genotypes of Fraxinus excelsior (L.). Agricultura autochthonous German Fraxinus excelsior clones to Hymenoscyphus – Stiintas i Practica, 1–2,52–60. pseudoalbidus is genetically determined. Annals of Forest Science, 72, Flowerdew, J.R. & Gardner, G. (1978) Small rodent populations and food sup- 183–193. ply in a Derbyshire ashwood. Journal of Animal Ecology, 47, 725–740. Enderle, R., Peters, F., Nakou, A. & Metzler, B. (2013) Temporal development Foggo, A. (1996) Patterns of herbivory by the ash bud moth Prays fraxinella: of ash dieback symptoms and spatial distribution of collar rots in a prove- implications for the silviculture of ash in Europe. Forest Ecology and Man- nance trial of Fraxinus excelsior. European Journal of Forest Research, 132, agement, 4, 231–240. 865–876. Foggo, A. & Speight, M.R. (1993) Root damage and water stress: treatments Esfahani, A.A., Amini, H., Samadi, N., Kar, S., Hoodaji, M., Shirvani, M. & affecting the exploitation of the buds of common ash Fraxinus excelsior L., Porsakhi, K. (2013) Assessment of air pollution tolerance index of higher by larvae of the ash bud moth Prays fraxinella Bjerk. (Lep., Yponomeuti- plants suitable for green belt development in east of Esfahan City, Iran. Jour- dae). Oecologia, 96, 134–138. nal of Ornamental and Horticultural Plants, 3,87–94. Foggo, A., Speight, M.R. & Gregoire, J.-C. (1994) Root disturbance of com- Espahbodi, K., Kiasari, S.M., Barimani, H. & Ghobadian, H. (2003) Investiga- mon ash, Fraxinus excelsior (Oleraceae), leads to reduced foliar toughness tion on the suitable spacing and combination of ash (Fraxinus excelsior L.) and increased feeding by a folivorous weevil, Stereonychus fraxini (Coleop- and maple (Acer velutinum Boiss) in plantations. Iranian Journal of Forest tera, Curculionidae). Ecological Entomology, 19, 344–348. and Poplar Research, 11,19–34. Foot, F.J. (1871) On the distribution of plants in Burren, County of Clare. Evelyn, J. (1664) Sylva. Jo. Martin & Ja. Allestry, London. Transactions of the Royal Irish Academy, 24, 143–160. Falinski, J.B. (1986) Vegetation Dynamics in Temperate Lowland Primeval Forestry Commission (2003) National Inventory of Woodland and Trees: Great Forest. Kluwer, Dordrecht, The Netherlands. Britain. Inventory Report. Forestry Commission, Edinburgh, UK. Farcas, C. (2000) Cercetari privind ^ınteruperea starii dorminde a semintelor de Forestry Commission (2015) http://www.forestry.gov.uk/ashdieback (Accessed frasin comun (Fraxinus excelsior L.), cires pasaresc (Prunus avium L.) si pal- 5 October 2015). tin de munte (Acer pseudoplatanus L.), prin abordarea unor metode noi de Fossitt, J.A. (1996) Late Quaternary vegetation history of the Western Isles of tratament, care sa conduca la cresterea randamentului culturilor ^ın pepiniera. Scotland. New Phytologist, 132, 171–196. PhD thesis, Transilvania University of Brasov, Brasov, Romania. Foussadier, R. (1998) Initiation des successions vegetales dans les lits endigues Feliu, A., Gonzalez-de-Olano, D., Gonzalez, E., Rodrıguez, B., Ruiz-Hornillos, des cours d’eau alpins. PhD thesis, Universite Joseph Fourier, Grenoble, J., Jimeno, L. & de la Torre, F. (2013) A multicenter study of sensitization France. profiles in an allergic pediatric population in an area with high allergen expo- FRAXIGEN (2005) Ash Species in Europe: Biological Characteristics and sure. Journal of Investigational Allergology and Clinical Immunology, 23, Practical Guidelines for Sustainable Use. Oxford Forestry Institute, Univer- 337–344. sity of Oxford, Oxford, UK. Feller, U. (2006) Stomatal opening at elevated temperature: an underestimated Freese, A., Benes, J., Bolz, R., Cizek, O., Dolek, M., Geyer, A., Gros, P., Kon- regulatory mechanism. General and Applied Plant Physiology, 32,19–31. vicka, M., Liegl, A. & Stettmer, C. (2006) Habitat use of the endangered Fender, A.-C., Leuschner, C., Schutzenmeister,€ K., Gansert, D. & Jungkunst, butterfly Euphydryas maturna and forestry in Central Europe. Animal Con-

H.F. (2013) Rhizosphere effects of tree species – Large reduction of N2O servation, 9, 388–397.

Frye, J. & Grosse, W. (1992) Growth response to flooding and recovery of Griffith, G.S. & Boddy, L. (1991a) Fungal decomposition of attached angios- deciduous trees. Zeitschrift fur€ Naturforschung, 47, 683–689. perm twigs. I. Decay community development in ash, beech and oak. New Gałuszka, A., Migaszewski, Z.M., Podlaski, R., Dołezgowska, S. & Michalik, Phytologist, 116, 407–415. A. (2011) The influence of chloride deicers on mineral nutrition and the Griffith, G.S. & Boddy, L. (1991b) Fungal decomposition of attached angios- health status of roadside trees in the city of Kielce, Poland. Environmental perm twigs. II. Moisture relations of twigs of ash (Fraxinus excelsior L.). Monitoring and Assessment, 176, 451–464. New Phytologist, 117, 251–257. G€ardenfors, U. (2010) The 2010 Red List of Swedish Species. ArtDatabankan, Griffith, G.S. & Boddy, L. (1998) Fungal communities in attached ash (Fraxi- Uppsala, Sweden. nus excelsior) twigs. Transactions of the British Mycological Society, 91, Gardner, G. (1976) Light and the growth of ash. Light as an Ecological Factor 599–606. II (eds G.C. Evans, R. Bainbridge & O. Rackham), pp. 557–563. Blackwell Griffiths, H.M., Sinclair, W.A., Smart, C.D. & Davis, R.E. (1999) The phyto- Scientific Publications, Oxford, UK. plasma associated with ash yellows and lilac witches’-broom: ‘Candidatus Gardner, G. (1977) The reproductive capacity of Fraxinus excelsior on the Der- Phytoplasma fraxini’. International Journal of Systematic Bacteriology, 49, byshire limestone. Journal of Ecology, 65, 107–118. 1605–1614. Gatsuk, L.E., Smimova, O.V., Vorontzova, L.I., Zaugolnova, L.B. & Zhukova, Grime, J.P., Hodgson, J.G. & Hunt, R. (2007) Comparative Plant Ecology: A L.A. (1980) Age states of plants of various growth forms: a review. Journal Functional Approach to Common British Species, 2nd edn. Castlepoint Press, of Ecology, 68, 675–696. Dalbeattie, UK. Gebauer, T., Horna, V. & Leuschner, C. (2008) Variability in radial sap flux Grodzinski, W. & Sawicka-Kaputa, K. (1970) Energy values of tree-seeds eaten density patterns and sapwood area among seven co-occurring temperate by small mammals. Oikos, 21,52–58. broad-leaved tree species. Tree Physiology, 28, 1821–1830. Gross, A., Grunig,€ C.R., Queloz, V. & Holdenrieder, O. (2012a) A molecular Gezbcynska, Z. (1980) Food of the roe deer and red deer in the Białowieza_ Pri- toolkit for population genetic investigations of the ash dieback pathogen meval Forest. Acta Theriologia, 25, 487–500. Hymenoscyphus pseudoalbidus. Forest Pathology, 42, 252–264. Gent, J. (1955) The cultivation of ash in relation to Prays curtisellus, the ash Gross, A. & Holdenrieder, O. (2013) On the longevity of Hymenoscyphus pseu- bud moth. Oxford University Forestry Society, 3,9–13. doalbidus in petioles of Fraxinus excelsior. Forest Pathology, 43, 168–170. Gerard, P.R., Temunovic, M., Sannier, J., Bertolino, P., Dufour, J., Frascaria- Gross, A., Holdenrieder, O., Pautasso, M., Queloz, V. & Sieber, T.N. (2014) Lacoste, N. & Fernandez-Manjarres, J.F. (2013) Chilled but not frosty: Hymenoscyphus pseudoalbidus, the causal agent of European ash dieback. understanding the role of climate in the hybridization between the Mediter- Molecular Plant Pathology, 15,5–21. ranean Fraxinus angustifolia Vahl and the temperate Fraxinus excelsior L. Gross, A., Hosoya, T. & Queloz, V. (2014) Population structure of the invasive (Oleaceae) ash trees. Journal of Biogeography, 40, 835–846. forest pathogen Hymenoscyphus pseudoalbidus. Molecular Ecology, 23, Gerosa, G., Marzuoli, R., Desotgiu, R., Bussotti, F. & Ballarin-Denti, A. (2009) 2943–2960. Validation of the stomatal flux approach for the assessment of ozone visible Gross, A., Zaffarano, P.L., Duo, A. & Grunig,€ C.R. (2012b) Reproductive injury in young forest trees. Results from the TOP (transboundary ozone pollu- mode and life cycle of the ash dieback pathogen Hymenoscyphus pseudoal- tion) experiment at Curno, Italy. Environmental Pollution, 157, 1497–1505. bidus. Fungal Genetics and Biology, 49, 977–986. Gill, R.M.A. & Beardall, V. (2001) The impact of deer on woodlands: the Guicherd, P., Peltier, J.P., Gout, E., Bligny, R. & Marigo, G. (1997) Osmotic effects of browsing and seed dispersal on vegetation structure and composi- adjustment in Fraxinus excelsior L.: malate and mannitol accumulation in tion. Forestry, 74, 209–218. leaves under drought conditions. Trees, 11, 155–161. Gilligan, C.A., Fraser, R., Godfray, C., Hanley, N., Leather, S., Meagher, T. Gunthardt-Goerg,€ M.S., McQuattie, C.J., Maurer, S. & Frey, B. (2000) Visible et al. (2013) Final Report. Tree Health and Plant Biosecurity Expert Task- and microscopic injury in leaves of five deciduous tree species related to cur- force. Department for the Environment, Food and Rural Affairs, London, UK. rent critical ozone levels. Environmental Pollution, 109, 489–500. Girel, J., Garguet-Duport, B. & Pautou, G. (1997) Landscape structure and his- Gustiene,_ A. (2010) Grybo Chalara fraxinea reiksme_ uosiu˛dziuties procese. torical processes along diked European valleys. A case study of the Arc/Isere [Importance of fungus Chalara fraxinea in the process of ash dieback]. Musu z confluence (Savoie, France). Environmental Management, 21, 891–907. Girios, 11,18–19. Glenz, C., Schlaepfer, R., Iorgulescu, I. & Kienast, F. (2006) Flooding toler- Haeke, U. & Sauter, J.J. (1996) Xylem dysfunction during winter and recovery ance of Central European tree and shrub species. Forest Ecology and Man- of hydraulic conductivity in diffuse-porous and ring-porous trees. Oecologia, agement, 235,1–13. 105, 435–439. Gliemeroth, A.K. (1997) Pal€aookologische€ Aspekte der Einwanderungs- Hagen-Thorn, A., Callesen, I., Armolaitis, K. & Nihlgard, B. (2004) The geschichte einiger Baumgattungen w€ahrend des Holoz€ans nach Europa. impact of six European tree species on the chemistry of mineral topsoil in Angewandte. Botanik, 71,54–61. forest plantations on former agricultural land. Forest Ecology and Manage- Godwin, H. (1975) History of the British Flora, 2nd edn. Cambridge University ment, 195, 373–384. Press, Cambridge, UK. Hagen-Thorn, A. & Stjernquist, I. (2005) Micronutrient levels in some temper- Gomez-Garcia, F., Flanagan, J., Garcıa-Molina, O., Vilaplana-Vivo, V., Garcıa- ate European tree species: a comparative field study. Trees, 19, 572–579. Carrillo, N., Berthon, P.F., Bily, A., Roller, M., Ortega, V.V. & Issaly, N. Hagen-Thorn, A., Varnagiryte, I., Nihlgard, B. & Armolaitis, K. (2006) (2015) Preventive effect of a Fraxinus excelsior L seeds/fruits extract on hep- Autumn nutrient resorption and losses in four deciduous forest tree species. atic steatosis in obese type 2 diabetic mice. Journal of Diabetes & Metabo- Forest Ecology and Management, 228,33–39. lism, 6, article 527. Hajek, P., Seidel, D. & Leuschner, C. (2015) Mechanical abrasion, and not Gordo, O. & Sanz, J.J. (2009) Long-term temporal changes of plant phenology competition for light, is the dominant canopy interaction in a temperate in the Western Mediterranean. Global Change Biology, 15, 1930–1948. mixed forest. Forest Ecology and Management, 348, 108–116. Gordon, A.G. (1964) The nutrition and growth of ash, Fraxinus excelsior,in Halden, B. (1928) Asken (Fraxinus excelsior L.) vid sin svenska nordgr€ans. natural stands in the English Lake District as related to edaphic site factors. Svenska Skogsvardsforeningens€ Tidskrift, 26, 846–934. Journal of Ecology, 52, 169–187. Hammatt, N. (1994) Shoot initiation in the leaflet axils of compound leaves Gosling, P.G. & Baker, C. (2004) Six chemicals with animal repellent or insecti- from micropropagated shoots of juvenile and mature common ash (Fraxinus cide properties are screened for phytotoxic effects on the germination and via- excelsior L.). Journal of Experimental Botany, 45, 871–875. bility of ash, birch, Corsican pine and sycamore seeds. Forestry, 77, 397–403. Hamunyela, E., Verbesselt, J., Roerink, G. & Herold, M. (2013) Trends in Gotmark,€ F., Fridman, J., Kempe, G. & Norden, B. (2005) Broadleaved tree spring phenology of western European deciduous forests. Remote Sensing, 5, species in conifer-dominated forestry: Regeneration and limitation of saplings 6159–6179. in southern Sweden. Forest Ecology and Management, 214, 142–157. Hantsch, L., Braun, U., Haase, J., Purschke, O., Scherer-Lorenzen, M. & Bruel- Grad, B., Kowalski, T. & Kraj, W. (2009) Studies on secondary metabolite pro- heide, H. (2014) No plant functional diversity effects on foliar fungal patho- duced by Chalara fraxinea and its phytotoxic influence on Fraxinus excel- gens in experimental tree communities. Fungal Diversity, 66, 139–151. sior. Phytopathologia, 54,61–69. Harmer, R. (1995) Natural regeneration of broadleaved trees in Britain: III. Gravano, E., Bussotti, F., Strasser, R.J., Schaub, M., Novak, K., Skelly, J. & Germination and establishment. Forestry, 68,1–9. Tani, C. (2004) Ozone symptoms in leaves of woody plants in open top Harmer, R. (2001) The effect of plant competition and simulated summer chambers: ultrastructural and physiological characteristics. Physiologia Plan- browsing by deer on tree regeneration. Journal of Applied Ecology, 38, tarum, 121, 620–633. 1094–1103. Greig-Smith, P.W. (1988) Bullfinches and ash trees. Assessing the role of plant Harmer, R., Boswell, R. & Robertson, M. (2005) Survival and growth of tree chemicals in controlling damage by herbivores. Journal of Chemical Ecol- seedlings in relation to changes in the ground flora during natural regenera- ogy, 14, 1889–1903. tion of an oak shelterwood. Forestry, 78,21–32.

Harmer, R., Kerr, G. & Boswell, R. (1997) Characteristics of lowland broadleaved Hietala, A.M., Timmermann, V., Børja, I. & Solheim, H. (2013) The invasive woodland being restocked by natural regeneration. Forestry, 70,199–210. ash dieback pathogen Hymenoscyphus pseudoalbidus exerts maximal infec- Harmer, R., Kiewitt, A. & Morgan, G. (2012) Effects of overstorey retention tion pressure prior to the onset of host leaf senescence. Fungal Ecology, 6, on ash regeneration and bramble growth during conversion of a pine planta- 302–308. tion to native broadleaved woodland. European Journal of Forest Research, Hillam, J., Groves, C.M., Brown, D.M., Baillie, M.G.L., Coles, J.M. & Coles, 131, 1833–1843. B.J. (1990) Dendrochronology of the English Neolithic. Antiquity, 64, 210– Hatch, L.C. (2007) Cultivars of Woody Plants. Vol 1, A-G. New Ornamentals 220. Society, Raleigh, NC, USA. Hinsinger, D.D., Gaudeul, M., Couloux, A., Bousquet, J. & Frascaria-Lacoste, Hauptman, T., Piskur, B., de Groot, M., Ogris, N., Ferlan, M. & Jurc, D. N. (2014) The phylogeography of Eurasian Fraxinus species reveals ancient (2013) Temperature effect on Chalara fraxinea: heat treatment of saplings as transcontinental reticulation. Molecular Phylogenetics and Evolution, 77, a possible disease control method. Forest Pathology, 43, 360–370. 223–237. Hayatgheibi, H. (2013) Studies on the microflora associated with the seeds of Hinsley, S.A. & Pocock, M.J.O. (2014) Ash Dieback: Long-Term Monitoring European ash (Fraxinus excelsior) and the infection biology of the pathogen of Impacts on Biodiversity. JNCC Report No. 484, Joint Nature Conservation Hymenoscyphus pseudoalbidus causing ash dieback. MSc thesis, Swedish Committee, Peterborough, UK. University of Agriculture Science, Uppsala, Sweden. Hintz, W.E., Carneiro, J.S., Kassatenko, I., Varga, A. & James, D. (2013) Two Hayes, F., Williamson, J. & Mills, G. (2015) Species-specific responses to novel mitoviruses from a Canadian isolate of the Dutch elm pathogen ozone and drought in six deciduous trees. Water, Air, and Soil Pollution, Ophiostoma novo-ulmi (93–1224). Virology, 10, e252. 226, article 156. Hitz, O.M., G€artner, H., Heinrich, I. & Monbaron, M. (2008) Wood anatomical Hebel, I., Haas, R. & Dounavi, A. (2006) Genetic variation of common ash changes in roots of European ash (Fraxinus excelsior L.) after exposure. (Fraxinus excelsior L.) populations from provenance regions in southern Ger- Dendrochronologia, 25, 145–152. many by using nuclear and chloroplast microsatellites. Silvae Genetica, 55, Hofmeister, J., Mihaljevic, M. & Hosek, J. (2014) The spread of ash (Fraxinus 38–44. excelsior) in some European oak forests: an effect of nitrogen deposition or Heilmann-Clausen, J. & Bruun, H.H. (2013) Dieback of European ash (Fraxi- successional change? Forest Ecology and Management, 203,35–47. nus excelsior) – Sheer misery or an opportunity for biodiversity? – Reply to Holscher,€ D. (2004) Leaf traits and photosynthetic parameters of saplings and Pautasso. Biological Conservation, 167, 450–451. adult trees of co-existing species in a temperate broad-leaved forest. Basic Hein, S. & Spiecker, H. (2008) Crown and tree allometry of open-grown ash and Applied Ecology, 5, 163–172. (Fraxinus excelsior L.) and sycamore (Acer pseudoplatanus L.). Agroforestry H€olscher, D., Koch, O., Korn, S. & Leuschner, C. (2005) Sap flux of five co- Systems, 73, 205–218. occurring tree species in a temperate broad-leaved forest during seasonal soil Hejcman, M., Hejcmanova, P., Stejskalova, M. & Pavlu, V. (2014) Nutritive drought. Trees, 19, 628–637. value of winter-collected annual twigs of main European woody species, Holtken,€ A.M., T€ahtinen, J. & Pappinen, A. (2003) Effects of discontinuous mistletoe and ivy and its possible consequences for winter foddering of live- marginal habitats on the genetic structure of common ash (Fraxinus excelsior stock in prehistory. The Holocene, 24, 659–667. L.). Silvae Genetica, 52, 206–212. Hejcmanova, P., Stejskalova, M. & Hejcman, M. (2014) Forage quality of leaf- Holzwarth, F., Kahl, A., Bauhus, J. & Wirth, C. (2013) Many ways to die – fodder from the main broad-leaved woody species and its possible conse- partitioning tree mortality dynamics in a near-natural mixed deciduous forest. quences for the Holocene development of forest vegetation in Central Eur- Journal of Ecology, 101, 220–230. ope. Vegetation History and Archaeobotany, 23, 607–613. Holzwarth, F.M., Daenner, M. & Flessa, H. (2011) Effects of beech and ash on Helinska-Raczkowska,~ L. & Fabisiak, E. (1999) Radial variation of earlywood small-scale variation of soil acidity and nutrient stocks in a mixed deciduous vessel lumen diameter as an indicator of the juvenile growth period in ash forest. Journal of Plant Nutrition and Soil Science, 174, 799–808. (Fraxinus excelsior L.). European Journal of Wood and Wood Products, 57, Hulden, E. (1941) Studien uber€ Fraxinus excelsior L. Acta Botanica Fennica, 283–286. 28,1–250. Helliwell, D.R. (1973) The Growth of Sycamore (Acer Pseudoplatanus L.) Hull, S.K. & Gibbs, J.N. (1991) Ash Dieback - A Survey of Non-Woodland Seedlings in Different Woodland Soils. Merlewood Research and Develop- Trees. Forestry Commission Bulletin 93, HMSO, London, UK. ment Paper No. 28, Institute of Terrestrial Ecology, Merlewood Research Hulme, P.E. (1996) Natural regeneration of yew (Taxus baccata L): microsite, Station, Cumbria, UK. seed or herbivore limitation? Journal of Ecology, 84, 853–861. Helliwell, D.R. & Harrison, A.F. (1979) Effects of light and weed competition Hulme, P.E. & Borelli, T. (1999) Variability in post-dispersal seed predation in on the growth of seedlings of four tree species on a range of soils. Quarterly deciduous woodland: relative importance of location, seed species, burial and Journal of Forestry, 73, 160–177. density. Plant Ecology, 145, 149–156. Hemery, G.E., Clark, J.R., Aldinger, E., Claessens, H., Malvolti, M.E., O’Con- Hulme, P.E. & Hunt, M.K. (1999) Rodent post-dispersal seed predation in nor, E., Raftoyannis, Y., Savill, P.S. & Brus, R. (2010) Growing scattered deciduous woodland: predator response to absolute and relative abundance of broadleaved tree species in Europe in a changing climate: a review of risks prey. Journal of Animal Ecology, 68, 417–428. and opportunities. Forestry, 83,65–81. Huntley, B. & Birks, H.J.B. (1983) An Atlas of Past and Present Pollen Maps of Hemery, G.E., Savill, P.S. & Pryor, S.N. (2005) Applications of the crown Europe: 0–13,000 Years Ago. Cambridge University Press, Cambridge, UK. diameter–stem diameter relationship for different species of broadleaved Ioos, R., Kowalski, T., Husson, C. & Holdenrieder, O. (2009) Rapid in planta trees. Forest Ecology and Management, 215, 285–294. detection of Chalara fraxinea by a real-time PCR assay using a dual-labelled Hempel, G. & Wilhelm, C. (1897) Die Bäume und Sträucher des Waldes. Ver- probe. European Journal of Plant Pathology, 125, 329–335. lag Von Ed. Hölzel, Vienna, Austria. Iremonger, S.F. & Kelly, D.L. (1988) The responses of four Irish wetland tree Hester, A.J., Mitchell, F.J.G. & Kirby, K.J. (1996) Effects of season and inten- species to raised soil water levels. New Phytologist, 109, 491–497. sity of sheep grazing on tree regeneration in a British upland woodland. For- Ivimey-Cook, R.B. & Proctor, M.C.F. (1966) The plant communities of the est Ecology and Management, 88,99–106. Burren, Co., Clare. Proceedings of the Royal Irish Academy, 64B, 211–301. Heuertz, M., Carnevale, S., Fineschi, S., Sebastiani, F., Hausman, J.F., Paule, Jackson, G. & Sheldon, J. (1949) The vegetation of Magnesian limestone cliffs L. & Vendramin, G.G. (2006) Chloroplast DNA phylogeography of Euro- at Markland Grips near Sheffield. Journal of Ecology, 37,38–50. pean ashes, Fraxinus sp. (Oleaceae): roles of hybridization and life history Jacob, M., Viedenz, K., Polle, A. & Thomas, F.M. (2010) Leaf litter decompo- traits. Molecular Ecology, 15, 2131–2140. sition in temperate deciduous forest stands with a decreasing fraction of Heuertz, M., Fineschi, S., Anzidei, M., Pastorelli, R., Salvini, D., Paule, L., beech (Fagus sylvatica). Oecologia, 164, 1083–1094. Frascaria-Lacoste, N., Hardy, O.J., Vekemans, X. & Vendramin, G.G. Jaeger, C., Gessler, A., Biller, S., Rennenberg, H. & Kreuzwieser, J. (2009) (2004a) Chloroplast DNA variation and postglacial recolonization of com- Differences in C metabolism of ash species and provenances as a conse- mon ash (Fraxinus excelsior L.) in Europe. Molecular Ecology, 13, 3437– quence of root oxygen deprivation by waterlogging. Journal of Experimental 3452. Botany, 60, 4335–4345. Heuertz, M., Hausman, J.-F., Hardy, O.J., Vendramin, G.G., Frascaria-Lacoste, Jahn, G. (1991) Temperate deciduous forests of Europe. Ecosystems of the N. & Vekemans, X. (2004b) Nuclear microsatellites reveal contrasting pat- World, 7, 377–502. terns of genetic structure between western and southeastern European popula- James, E.O. (1968) The tree of life. Folklore, 79, 241–249. tions of the common ash (Fraxinus excelsior L). Evolution, 58, 976–988. Janceva, S., Dizhbite, T., Telisheva, G., Spulle, U., Klavinsh, L. & Dzenis, M. Heuertz, M., Vekemans, X., Hausman, J.-F., Palada, M. & Hardy, O.J. (2003) (2011) Tannins of deciduous trees bark as a potential source for obtaining Estimating seed vs. pollen dispersal from spatial genetic structure in the com- ecologically safe wood adhesives. Proceedings of the 8th International Scien- mon ash. Molecular Ecology, 12, 2483–2495. tific and Practical Conference, 1, 265–270.

Janse, J.D. (1982) Pseudomonas syringae subsp. savastanoi (ex Smith) subsp. Kaydan, M.B., Kilincer, N., Uygun, N., Japoshvilli, G. & Gaimari, S. (2006) nov., nom. rev., the bacterium causing excrescences on Oleaceae and Neriurn Parasitoids and predators of Pseudococcidae (Hemiptera: Coccoidea) in oleander L. International Journal of Systematic Bacteriology, 32, 146–169. Ankara, Turkey. Phytoparasitica, 34, 331–337. Janse-ten Klooster, S.H., Thomas, E.J.P. & Sterck, F.J. (2007) Explaining inter- Keiller, D.R. & Holmes, M.G. (2001) Effects of long-term exposure to elevated specific differences in sapling growth and shade tolerance in temperate for- UV-B radiation on the photosynthetic performance of five broad-leaved tree ests. Journal of Ecology, 95, 1250–1260. species. Photosynthesis Research, 67, 229–240. Jezdrzejczak, E. (2013) Soil seed bank in selected patches of vegetation in the Kenigsvalde, K., Arhipova, N., Laivins, M. & Gaitnieks, T. (2010) Fungus beech forest of Beskid Sla zski (Southern Poland). Casopis Slezskeho Zems- Chalara fraxinea as a causal agent for ash decline in Latvia. Mezzinatne , 21, keho Muzea (A), 62, 137–150. 110–120. Jensen, T.S. (1985) Seed-seed predator interactions of European beech, Fagus Kerr, G. (1995) Silviculture of ash in southern England. Forestry, 68,63–70. sylvatica and forest rodents, Clethrionomys glareolus and Apodemus flavicol- Kerr, G. (1998) A review of black heart of ash (Fraxinus excelsior L.). For- lis. Oikos, 44, 149–156. estry, 71,49–56. Jinks, R.L. (1995) The effects of propagation environment on the rooting of leafy Kerr, G. (2002) Factors affecting the early growth and form of Fraxinus excel- cuttings of ash (Fraxinus excelsior L.), sycamore (Acer pseudoplatanus L.), sior L. in Britain. Ph.D. thesis, University of Wales, Bangor, UK. and sweet chestnut (Castanea sativa Mill.). New Forests, 10, 183–195. Kerr, G. (2003) Effects of spacing on the early growth of planted Fraxinus Jinks, R.L., Parratt, M. & Morgan, G. (2012) Preference of granivorous rodents excelsior L. Canadian Journal of Forest Research, 33, 1196–1207. for seeds of 12 temperate tree and shrub species used in direct sowing. For- Kerr, G. (2004) The growth and form of ash (Fraxinus excelsior) in mixture with est Ecology and Management, 278,71–79. cherry (Prunus avium), oak (Quercus petraea and Quercus robur), and beech Jinks, R.L., Willoughby, I. & Baker, C. (2006) Direct seeding of ash (Fraxinus (Fagus sylvatica). Canadian Journal of Forest Research, 34, 2340–2350. excelsior L.) and sycamore (Acer pseudoplatanus L.): The effects of sowing Kerr, G. & Boswell, R.C. (2001) The influence of spring frosts, ash bud moth date, pre-emergent herbicides, cultivation, and protection on seedling emer- (Prays fraxinella) and site factors on forking of young ash in southern Bri- gence and survival. Forest Ecology and Management, 237, 373–386. tain. Forestry, 74,29–40. Joannin, S., Vanniere, B., Galop, D., Peyron, O., Haas, J.N., Gilli, A., Chapron, Kerr, G. & Cahalan, C. (2004) A review of site factors affecting the early E., Wirth, S.B., Anselmetti, F., Desmet, M. & Magny, M. (2013) Climate growth of ash (Fraxinus excelsior L.). Forest Ecology and Management, and vegetation changes during the Lateglacial and early–middle Holocene at 188, 225–234. Lake Ledro (southern Alps, Italy). Climate of the Past, 9, 913–933. Kebler, M., Cech, T.L., Brandstetter, M. & Kirisits, T. (2012) Dieback of ash Johannesson, H., Ihrmark, K. & Stenlid, J. (2002) Differential decay extension (Fraxinus excelsior and Fraxinus angustifolia) in Eastern Austria: disease capability of Daldinia spp. in wood of Betula pendula, Alnus glutinosa and development on monitoring plots from 2007 to 2010. Journal of Agricultural Fraxinus excelsior. Forest Ecology and Management, 167, 295–302. Extension and Rural Development, 4, 223–226. Johansson, H. (2011) Comparison of saproxylic beetle assemblages on four dif- Kirby, K.J., Bazely, D.R., Goldberg, E.A., Hall, J.E., Isted, R., Perry, S.C. & ferent broad-leaved tree species in south-eastern Sweden. MSc thesis, Thomas, R.C. (2014) Changes in the tree and shrub layer of Wytham Woods Linkopings€ Universitet, Linkoping,€ Sweden. (Southern England) 1974–2012: local and national trends compared. For- Johansson, P., Rydin, H. & Thor, G. (2007) Tree age relationships with epi- estry, 87, 663–673. phytic lichen diversity and lichen life history traits on ash in southern Swe- Kirisits, T. (2015) Ascocarp formation of Hymenoscyphus fraxineus on several- den. Ecoscience, 14,81–91. year-old pseudosclerotial leaf rachises of Fraxinus excelsior. Forest Pathol- Johansson, S.B.K., Vasaitis, R., Ihrmark, K., Barklund, P. & Stenlid, J. (2010) ogy, 45, 254–257. Detection of Chalara fraxinea from tissue of Fraxinus excelsior using spe- Kirisits, T. & Cech, T.L. (2009) Beobachtungen zum sexuellen Stadium des cies-specific ITS primers. Forest Pathology, 40, 111–115. Eschentriebsterben-Erregers Chalara fraxinea in Osterreich.€ Forstschutz Jonsson,€ M.T. & Thor, G. (2012) Estimating coextinction risks from epidemic Aktuell, 48,21–25. tree death: affiliate lichen communities among diseased host tree populations Kirisits, T., Matlakova, M., Mottinger-Kroupa, S., Cech, T.L. & Halmschlager, of Fraxinus excelsior. PLoS One, 7, e45701. E. (2009) The current situation of ash dieback caused by Chalara fraxinea in Jouve, L., Jacques, D., Douglas, G.C., Hoffmann, L. & Hausman, J.-F. (2007) Austria. SüLeyman Demirel University Faculty of Forestry Journal, Serial A Biochemical characterization of early and late bud flushing in common ash (Special Issue), 97–119. (Fraxinus excelsior L.). Plant Science, 172, 962–969. Kjær, E.D., McKinney, L.V., Nielsen, L.R., Hansen, L.N. & Hansen, J.K. Jukes, C. & Lewis, D.H. (1974) Planteose, the major soluble carbohydrate of (2012) Adaptive potential of ash (Fraxinus excelsior) populations against the seeds of Fraxinus excelsior. Phytochemistry, 13, 1519–1521. novel emerging pathogen Hymenoscyphus pseudoalbidus. Evolutionary Junker, C., Mandey, F., Pais, A., Ebel, R. & Schulz, B. (2014) Hymenoscyphus Applications, 5, 219–228. pseudoalbidus and Hymenoscyphus albidus: viridiol concentration and viru- Kleinschmit, J., Luck, F.W., Rau, H.M. & Ruetz, W.F. (2002) Ergebnisse eines lence do not correlate. Forest Pathology, 44,39–44. Eschen-Herkunftsversuches [Results of an ash provenance experiment.]. Juodvalkis, A. & Vasiliauskas, A. (2002) Lietuvos uosynuz dziuvimo apimtys ir Forst und Holz, 57, 166–172. jas lemiantys veiksniai. [The extent and possible causes of dieback of ash Kleinschmit, J., Svolba, J., Enescu, V., Franke, A., Rau, H.-M. & Ruetz, W. stands in Lithuania.] LZUU Mokslo Darbai. Biomedicinos Mokslai, 56, (1996) Erste Ergebnisse des Eschen- Herkunftsversuches von 1982. For- 17–22. starchiv, 67, 114–122. Juodvalkis, A., Kairiukstis, L. & Vasiliauskas, R. (2005) Effects of thinning on Kloet, G.S. & Hincks, W.D. (1972) A Checklist of British Insects. Part 2. Lepi- growth of six tree species in north-temperate forests of Lithuania. European doptera. Royal Entomological Society of London, London, UK. Journal of Forest Research, 124, 187–192. Kocher,€ P., Gebauer, T., Horna, V. & Leuschner, C. (2009) Leaf water status Jȕriado, I., Liira, J., Paal, J. & Suija, A. (2009) Tree and stand level variables and stem xylem flux in relation to soil drought in five temperate broad-leaved influencing diversity of lichens on temperate broad-leaved trees in boreo- tree species with contrasting water use strategies. Annals of Forest Science, nemoral floodplain forests. Biodiversity and Conservation, 18, 105–125. 66, article 101. Kaminska, M. & Berniak, H. (2009) ‘Candidatus Phytoplasma asteris’ in Frax- Kocher,€ P., Horna, V., Beckmeyer, I. & Leuschner, C. (2012) Hydraulic prop- inus excelsior and its association with ash yellows newly reported in Poland. erties and embolism in small-diameter roots of five temperate broad-leaved Plant Pathology, 58, 788. tree species with contrasting drought tolerance. Annals of Forest Science, 69, Karpavicius, J. & Vitas, A. (2006) Influence of environmental and climatic fac- 693–703. tors on the radial growth of European ash (Fraxinus excelsior L.). Ekologija, Kocher,€ P., Horna, V. & Leuschner, C. (2012) Environmental control of daily 1,1–9. stem growth patterns in five temperate broad-leaved tree species. Tree Physi- Karpinska-Ko łaczek, M., Kołaczek, P. & Stachowicz-Rybka, R. (2013) Pathways ology, 32, 1021–1032. of woodland succession under low human impact during the last 13,000 years Kocher,€ P., Horna, V. & Leuschner, C. (2013) Stem water storage in five coex- in northeastern Poland. Quaternary International, 328–329, 196–212. isting temperate broad-leaved tree species: significance, temporal dynamics Kassas, M. (1951) Studies in the ecology of Chippenham Fen. II. Recent his- and dependence on tree functional traits. Tree Physiology, 33, 817–832. tory of the Fen, from evidence of historical records, vegetational analysis and Kollas, C., Korner,€ C. & Randin, C.F. (2013) Spring frost and growing season tree-ring analysis. Journal of Ecology, 39,19–32. length co-control the cold range limits of broad-leaved trees. Journal of Bio- Kaydan, M.B., Kilincer, N. & Kondo, T. (2015) Descriptions of all female geography, 41, 773–783. stages of the maple mealybug, Phenacoccus aceris (Hemiptera: Coccoidea: Konopka,^ B., Pajtık, J. & Sebe n, V. (2015) Biomass functions and expansion Pseudococcidae), with notes on its biology. Acta Zoologica Academiae Sci- factors for young trees of European ash and Sycamore maple in the Inner entiarum Hungaricae, 61, 255–277. Western Carpathians. Austrian Journal of Forest Science, 132,1–26.

Kostler,€ J.N., Brückner, E. & Bibelrichther, H. (1968) Die Wurzeln der Lemperiere, G. & Malphettes, C.-B. (1983) Observations sur l’ecologie de deux Waldbaume;€ Untersuchungen zur Morphologie der Waldbaume in Mitteleu- coleopteres ravageurs du Frêne. Revue Forestiere Francaise, 35, 283–288. ropa. Paul Parey, Hamburg, Germany. Lenz, A., Hoch, G., Vitasse, Y. & Korner,€ C. (2013) European deciduous trees Kostova, I. & Iossifova, T. (2007) Chemical components of Fraxinus species. exhibit similar safety margins against damage by spring freeze events along Fitoterapia, 78,85–106. elevational gradients. New Phytologist, 200, 1166–1175. Kowalski, T. (2006) Chalara fraxinea sp. nov. associated with dieback of ash Le Sueur, A.D.C. (1924) The common ash. Quarterly Journal of Forestry, 18, (Fraxinus excelsior) in Poland. Forest Pathology, 36, 264–270. 217–227. Kowalski, T. & Holdenrieder, O. (2009a) Pathogenicity of Chalara fraxinea. Levin, D.A. & Kerster, H.W. (1974) Gene flow in seed plants. Evolutionary Forest Pathology, 39,1–7. Biology, 7, 139–185. Kowalski, T. & Holdenrieder, O. (2009b) The teleomorph of Chalara fraxinea, Linhart, Y.B. & Whelan, R.J. (1980) Woodland regeneration in relation to graz- the causal agent of ash dieback. Forest Pathology, 39, 304–308. ing and fencing in Coed Gorswen, North Wales. Journal of Applied Ecology, Kowalski, T. & Łukomska, A. (2005) Badania nad zamieraniem jesionu (Fraxi- 17, 827–840. nus excelsior L. w drzewostanach Nadlesnictwa Włoszczowa [The studies on Littlewood, N.A., Nau, B.S., Pozsgai, G., Stockan, J.A., Stubbs, A. & Young, ash dying (Fraxinus excelsior L.) in the Włoszczowa Forest Unit stands.]. M.R. (2015) Invertebrate species at risk from ash dieback in the UK. Journal Acta Agrobotanica, 58, 429–439. of Insect Conservation, 19,75–85. Kr€autler, K. & Kirisits, T. (2012) The ash dieback pathogen Hymenoscyphus Lobo, A., McKinney, L.V., Hansen, J.K., Kjær, E.D. & Nielsen, L.R. (2015) pseudoalbidus is associated with leaf symptoms on ash species (Fraxinus Genetic variation in dieback resistance in Fraxinus excelsior confirmed by spp.). Journal of Agricultural Extension and Rural Development, 4, 261– progeny inoculation assay. Forest Pathology, 45, 379–387. 265. Locket, G.H. (1946) Observations on the colonization of bare chalk. Journal of Kr€autler, K., Treitler, R. & Kirisits, T. (2015) Hymenoscyphus fraxineus can Ecology, 33, 205–209. directly infect intact current-year shoots of Fraxinus excelsior and artificially Lof,€ M., Bolte, A., Jacobs, D.F. & Jensen, A.M. (2014) Nurse trees as a forest exposed leaf scars. Forest Pathology, 45, 274–280. restoration tool for mixed plantations: effects on competing vegetation and Kuehne, C., Kublin, E., Pyttel, P. & Bauhus, J. (2013) Growth and form of performance in target tree species. Restoration Ecology, 22, 758–765. Quercus robur and Fraxinus excelsior respond distinctly different to initial Lohmus,~ A. & Runnel, K. (2014) Ash dieback can rapidly eradicate isolated growing space: results from 24-year-old Nelder experiments. Journal of For- epiphyte populations in production forests: A case study. Biological Conser- estry Research, 24,1–14. vation, 169, 185–188. Kullberg, Y. & Bergstrom,€ R. (2001) Winter browsing by large herbivores on Loudon, J.C. (1838) Arboretum et Fruticetum Britannicum. Privately published, planted deciduous seedlings in southern Sweden. Scandinavian Journal of London, UK. Forest Research, 16, 371–378. Lygis, V., Bakys, R., Gustiene, A., Burokiene, D., Matelis, A. & Vasaitis, R. Ladefoged, K. (1963) Transpiration of forest trees in closed stands. Physiologia (2014) Forest self-regeneration following clear-felling of dieback-affected Plantarum, 16, 378–414. Fraxinus excelsior: focus on ash. European Journal of Forest Research, 133, Landolt, W., Buhlmann,€ U., Bleuler, P. & Bucher, J.B. (2000) Ozone expo- 501–510. sure-response relationships for biomass and root/shoot ratio of beech (Fagus Lygis, V., Vasiliauskas, R., Larsson, K. & Stenlid, J. (2005) Wood-inhabiting sylvatica), ash (Fraxinus excelsior), Norway spruce (Picea abies) and Scots fungi in stems of Fraxinus excelsior in declining ash stands of northern pine (Pinus sylvestris). Environmental Pollution, 109, 473–478. Lithuania, with particular reference to Armillaria cepistipes. Scandinavian Lang, C. & Polle, A. (2011) Ectomycorrhizal fungal diversity, tree diversity Journal of Forest Research, 20, 337–346. and root nutrient relations in a mixed Central European forest. Tree Physiol- Machatschek, M. (2002) Laubgeschichten - Gebrauchsgeschichte Einer Alten ogy, 31, 531–538. Baumwirtschaft, Speise-und Futterlaubkultur [Stories on Leaves - the Lang, C., Seven, J. & Polle, A. (2011) Host preferences and differential contri- History of an Old Tree Management System.]. Bohlau-Verlag,€ Vienna, butions of deciduous tree species shape mycorrhizal species richness in a Austria. mixed Central European forest. Mycorrhiza, 21, 297–308. Madejon, P. & Lepp, N.W. (2007) Arsenic in soils and plants of woodland Langenbruch, C., Helfrich, M. & Flessa, H. (2012) Effects of beech (Fagus syl- regenerated on an arsenic-contaminated substrate: A sustainable natural reme- vatica), ash (Fraxinus excelsior) and lime (Tilia spec.) on soil chemical prop- diation? Science of the Total Environment, 379, 256–262. erties in a mixed deciduous forest. Plant and Soil, 352, 389–403. Malenovsky, I. & Jerinic-Prodanovic, D. (2011) A revised description of Psyl- Langenfeld-Heyser, R., Schella, B., Buschmann, K. & Speck, F. (1996) lopsis repens Loginova, 1963 (Hemiptera: Psylloidea: Psyllidae), with first

Microautoradiographic detection of CO2 fixation in lenticel chlorenchyma of records from Europe. Archives of Biological Sciences, 63, 275–286. young Fraxinus excelsior L. stems in early spring. Trees, 10, 255–260. Maltoni, A., Mariotti, B., Tani, A. & Jacobs, D.F. (2010) Relation of Fraxinus Latorre, F. & Bianchi, M.M. (1998) Relationships between flowering develop- excelsior seedling morphology to growth and root proliferation during field ment of Ulmus pumila and Fraxinus excelsior and their airborne pollen. establishment. Scandinavian Journal of Forest Research, 25(Suppl. 8), 60–67. Grana, 37, 233–238. Mansson, P.E. & Schlyter, F. (2004) Hylobius pine weevils adult host selection Laube, J., Sparks, T.H., Estrella, N., Ho€fler, J., Ankerst, D.P. & Menzel, A. and antifeedants: feeding behaviour on host and non-host woody scandina- (2014) Chilling outweighs photoperiod in preventing precocious spring vian plants. Agricultural and Forest Entomology, 6, 165–171. development. Global Change Biology, 20, 170–182. Marie-Pierre, J., Didier, A. & Gerard, B. (2006) Patterns of ash (Fraxinus Lebaube, S., Le Goff, N., Ottorini, J.-M. & Granier, A. (2000) Carbon balance excelsior L.) colonization in mountain grasslands: the importance of manage- and tree growth in a Fagus sylvatica stand. Annals of Forest Science, 57, ment practices. Plant Ecology, 183, 177–189. 49–61. Marigo, G. & Peltier, J.-P. (1996) Analysis of the diurnal change in osmotic Lebedev, V. & Schestibratov, K. (2013) Effect of natural and synthetic growth potential in leaves of Fraxinus excelsior L. Journal of Experimental Botany, stimulators on in vitro rooting and acclimatization of common ash (Fraxinus 47, 763–769. excelsior L.) microplants. Natural Science, 5, 1095–1101. Marigo, G., Peltier, J.-P., Girel, J. & Pautou, G. (2000) Success in the demo- Le Goff, N., Colin-Belgrand, M. & Muller, G. (1993) Croissance et produc- graphic expansion of Fraxinus excelsior L. Trees, 15,1–13. tiviteduchêne rouge dans le Nord-Est de la France. Le Chêne Rouge Marmann, P., Wendler, R., Millard, P. & Heilmeier, H. (1997) Nitrogen storage D’Amerique (ed. Anon.). pp. 172–176. INRA editions, Paris, France, and remobilization in ash (Fraxinus excelsior) under field and laboratory con- Le Goff, N., Granier, A., Ottorini, J.-M. & Peiffer, M. (2004) Biomass incre- ditions. Trees, 11, 298–305. ment and carbon balance of ash (Fraxinus excelsior) trees in an experimental Martin, N.M. (1938) Some observations on the epiphytic moss flora of trees in stand in northeastern France. Annals of Forest Science, 61,1–12. Argyll. Journal of Ecology, 26,82–95. Le Goff, N. & Ottorini, J.-M. (1996) Leaf development and stem growth of ash Maskell, L., Henrys, P., Norton, L., Smart, S. & Wood, C. (2013) Distribution (Fraxinus excelsior) as affected by tree competitive status. Journal of Applied of ash Trees (Fraxinus excelsior) in Countryside Survey Data. Centre for Ecology, 33, 793–802. Ecology and Hydrology, Wallingford, UK. Lehto, T., R€ais€anen, M., Lavola, A., Julkunen-Tiitto, R. & Aphalo, P.J. (2004) McCartan, S.A., Webber, J.F. & Jinks, R.J. (2015) Hot-water treatment as a Boron mobility in deciduous forest trees in relation to their polyols. New possible method for eradicating Chalara fraxinea (Hymenoscyphus pseudoal- Phytologist, 163, 333–339. bidus) infection from ash fruits (Fraxinus excelsior L.). Quarterly Journal of Lemoine, D., Peltier, J.-P. & Marigo, G. (2001) Comparative studies of the Forestry, 109,18–23. water relations and the hydraulic characteristics in Fraxinus excelsior, Acer McEvoy, P.M. & McAdam, J.H. (2008) Sheep grazing in young oak Quercus pseudoplatanus, and A. opalus trees under soil water contrasted conditions. spp. and ash Fraxinus excelsior plantations: vegetation control, seasonality Annals of Forest Science, 58, 723–731. and tree damage. Agroforestry Systems, 74, 199–211.

McKay, H.M., Jinks, R.L. & McEvoy, C. (1999) The effect of desiccation and Modry, M., Hubeny, D. & Rejsek, K. (2004) Differential response of naturally rough-handling on the survival and early growth of ash, beech, birch and regenerated European shade tolerant tree species to soil type and light avail- oak seedlings. Annals of Forest Science, 56, 391–402. ability. Forest Ecology and Management, 188, 185–195. McKinney, L.V., Nielsen, L.R., Hansen, J.K. & Kjær, E.D. (2011) Presence of Moe, B. & Botnen, A. (1997) A quantitative study of the epiphytic vegetation natural genetic resistance in Fraxinus excelsior (Oleraceae) to Chalara frax- on pollarded trunks of Fraxinus excelsior at Havra, Osterøy, western Nor- inea (Ascomycota): an emerging infectious disease. Heredity, 106, 788–797. way. Plant Ecology, 129, 157–177. McKinney, L.V., Thomsen, I.M., Kjær, E.D., Bengtsson, S.B.K. & Nielsen, L.R. Moraal, L.G. & Goedhart, P.W. (1997) Differences in palatability of Fraxinus (2012a) Rapid invasion by an aggressive pathogenic fungus (Hymenoscyphus excelsior L., for the vole, Microtus arvalis, and the scale, Pseudochermes pseudoalbidus) replaces a native decomposer (Hymenoscyphus albidus): a case fraxini L. Physiology and Genetics of Tree-Phytophage Interactions - Inter- of local cryptic extinction? Fungal Ecology, 5, 663–669. national Symposium (eds F. Lieutier, W.J. Mattson & M.R. Wagner), pp. McKinney, L.V., Thomsen, I.M., Kjær, E.D. & Nielsen, L.R. (2012b) Genetic 111–120. Gujan, France. resistance to Hymenoscyphus pseudoalbidus limits fungal growth and symp- Morand, M.-E., Brachet, S., Rossignol, P., Dufour, J. & Frascaria-Lacoste, N. tom occurrence in Fraxinus excelsior. Forest Pathology, 42,69–74. (2002) A generalized heterozygote deficiency assessed with microsatellites in McVean, D.N. (1955) Ecology of Alnus glutinosa (L.) Gaertn. II. Seed distribu- French common ash populations. Molecular Ecology, 11, 377–385. tion and germination. Journal of Ecology, 43,61–71. Morand-Prieur, M.-E., Raquin, C., Shykoff, J.A. & Frascaria-Lacoste, N. Meinen, C., Hertel, D. & Leuschner, C. (2009) Biomass and morphology of fine (2003) Males outcompete hermaphrodites for seed siring success in con- roots in temperate broad-leaved forests differing in tree species diversity: is trolled crosses in the polygamous Fraxinus excelsior (Oleaceae). American there evidence of below-ground overyielding? Oecologia, 161,99–111. Journal of Botany, 90, 949–953. Meißner, M., Kohler,€ M., Schwendenmann, L. & Holscher,€ D. (2012) Partition- Morren, M.E. (1866) III. Notes on the number of stomata of some indigenous ing of soil water among canopy trees during a soil desiccation period in a and cultivated plants in Belgium. Transactions of the Botanical Society of temperate mixed forest. Biogeosciences, 9, 3465–3474. Edinburgh, 8, 171–180. Mencuccini, M., Martınez-Vilalta, J., Hamid, H.A., Korakaki, E. & Van- Mottet, A., Julien, M.P., Balent, G. & Gibon, A. (2007) Agricultural land-use derklein, D. (2007) Evidence for age- and size-mediated controls of tree change and ash (Fraxinus excelsior L.) colonization in Pyrenean landscapes: growth from grafting studies. Tree Physiology, 27, 463–473. an interdisciplinary case study. Environmental Modeling and Assessment, 12, Mencuccini, M., Martınez-Vilalta, J., Vanderklein, D., Hamid, H.A., Korakaki, 293–302. E., Lee, S. & Michiels, B. (2005) Size-mediated ageing reduces vigour in Mrazkova, M., Cern y, K., Tomsovsky, M., Strnadova, V., Gregorova, B., trees. Ecology Letters, 8, 1183–1190. Holub, V., Panek, M. & Havrdova, L. (2013) Occurrence of Phytophthora Mertens, J., Van Nevel, L., De Schrijver, A., Piesschaert, F., Oosterbaan, A., multivora and Phytophthora plurivora in the Czech Republic. Plant Protec- Tack, F.M.G. & Verheyen, K. (2007) Tree species effect on the redistribution tion Science, 49, 155–164. of soil metals. Environmental Pollution, 149, 173–181. Mullerov€ a, J., Hedl, R. & Szabo, P. (2015) Coppice abandonment and its impli- Merton, L.F.H. (1970) The history and status of the woodlands of the Der- cations for species diversity in forest vegetation. Forest Ecology and Man- byshire limestone. Journal of Ecology, 58, 723–744. agement, 343,88–100. Metz-Favre, C., Papanikolaou, I., Purohit, A., Pauli, G. & de Blay, F. (2010) Munch,€ E. & Dieterich, V. (1925) Kalkeschen und Wassereschen. Silva, 13, Actualite dans l’allergie au pollen de frêne [The reality of ash pollinosis.]. 129–135. Revue Francaise D’Allergologie, 50, 568–573. Mund, M., Kutsch, W.L., Wirth, C., Kahl, T., Knohl, A., Skomarkova, M.V. & Middleton, P., Stewart, F., Al-Qahtani, S., Egan, P., O’Rourke, C., Abdulrah- Schulze, E.-D. (2010) The influence of climate and fructification on the man, A. et al. (2005) Antioxidant, antibacterial activities and general toxicity inter-annual variability of stem growth and net primary productivity in an of Alnus glutinosa, Fraxinus excelsior and Papaver rhoeas. Iranian Journal old-growth, mixed beech forest. Tree Physiology, 30, 689–704. of Pharmaceutical Research, 2,81–86. Mwase, W.F., Savill, P.S. & Hemery, G. (2008) Genetic parameter estimates van Miegroet, M. (1956) Untersuchungen uber€ den Einfluß der waldbaulichen for growth and form traits in common ash (Fraxinus excelsior, L.) in a Behandlung und der Umweltsfaktoren auf den Aufbau und die morphologis- breeding seedling orchard at Little Wittenham in England. New Forests, 36, chen Eigenschaften von Eschendickungen im schweizerischen Mittelland. 225–238. PhD thesis, Eidgenossischen€ Technischen Hochschule, Zurich, Switzerland. Mysterud, A., Lian, L.-B. & Hjermann, D.Ø. (1999) Scale-dependent trade-offs van Miegroet, M., Verhegghe, J.F. & Lust, N. (1981) Trends of development in foraging by European roe deer (Capreolus capreolus) during winter. in the early stages of mixed natural regenerations of ash and sycamore. Silva Canadian Journal of Zoology, 77, 1486–1493. Gandavensis, 48,1–22. Natural History Museum (2016) British Isles List of Lichens and Lichenicolous Mihok, B., Kenderes, K., Kirby, K.J., Paviour-Smith, K. & Elbourn, C.A. Fungi http://www.nhm.ac.uk/research-curation/scientific-resources/biodiver- (2009) Forty-year changes in the canopy and understorey in Wytham Woods. sity/uk-biodiversity/uk-species/checklists/NHMSYS0000357024/index.html Forestry, 82, 515–527. (Assessed 12 January 2016). Milberg, P., Bergman, K.O., Johansson, H. & Jansson, N. (2014) Low host-tree Neirynck, J., Mirtcheva, S., Sioen, G. & Lust, N. (2000) Impact of Tilia preferences among saproxylic beetles: a comparison of four deciduous spe- platyphyllos Scop., Fraxinus excelsior L., Acer pseudoplatanus L., Quercus cies. Insect Conservation and Diversity, 7, 508–522. robur L. and Fagus sylvatica L. on earthworm biomass and physico-che- Million, S. & Billamboz, A. (2011) Pile-dwellings at lake Degersee (SW-Ger- mical properties of a loamy topsoil. Forest Ecology and Management, many) – a challenge for dendrochronology. Tree Rings in Archaeology, Cli- 133, 275–286. matology and Ecology, Vol. 9. (eds M. Maaten-Theunissen, H. Spiecker, H. Newton, I. (1967) The feeding ecology of the Bullfinch (Pyrrhula pyrrhula L.) G€artner, G. Helle & I. Heinrich), pp. 114–121. GFZ Potsdam, Scientific in southern England. Journal of Animal Ecology, 36, 721–744. Technical Report STR 11/07, Potsdam, Germany. Niinemets, U.€ (1999) Differences in chemical composition relative to functional Mitchell, R.J., Bailey, S., Beaton, J.K., Bellamy, P.E., Brooker, R.W., Broome, differentiation between petioles and laminas of Fraxinus excelsior. Tree A. et al. (2014a) The Potential Ecological Impact of Ash Dieback in the UK. Physiology, 19,39–45. JNCC Report No. 483 Joint Nature Conservation Committee, Peterborough, Niinemets, U.€ & Kull, O. (1999) Biomass investment in leaf lamina versus UK. lamina support in relation to growth irradiance and leaf size in temperate Mitchell, R.J., Beaton, J.K., Bellamy, P.E., Broome, A., Chetcuti, J., Eaton, S. deciduous trees. Tree Physiology, 19, 349–358. et al. (2014c) Ash dieback in the UK: A review of the ecological and conser- Niinemets, U.,€ Kull, O. & Tenhunen, J.D. (1998) An analysis of light effects on vation implications and potential management options. Biological Conserva- foliar morphology, physiology, and light interception in temperate deciduous tion, 175,95–109. woody species of contrasting shade tolerance. Tree Physiology, 18, 681–696. Mitchell, R.J., Broome, A., Harmer, R., Beaton, J.K., Bellamy, P.E., Brooker, Ningre, F., Cluzeau, C. & Le Goff, N. (1992) La fourchaison du frêne en plan- R.W. et al. (2014b) Assessing and Addressing the Impacts of Ash Dieback on tation: causes, consequences et controle.^ Revue Forestiere Francaise, 44, UK Woodlands and Trees of Conservation Importance (Phase 2). Natural Eng- 104–114. land Commissioned Reports, Number 151. Natural England, Peterborough, UK. Norden, U. (1994) Leaf litterfall concentrations and fluxes of elements by Mitras, D., Kitin, P., Iliev, I., Dancheva, D., Scaltsoyiannes, A., Tsaktsira, M., deciduous tree species. Scandinavian Journal of Forest Research, 9,9–16. Nellas, C. & Rohr, R. (2009) In vitro propagation of Fraxinus excelsior L. Nord-Larsen, T., Johannsen, V.K., Vesterdal, L., Jørgensen, B.B. & Bastrup- by epicotyls. Journal of Biological Research – Thessaloniki, 11,37–48. Birk, A. (2009) Skove og Plantager 2008 [Forests and Plantations 2008.]. Mockeliunaite, R. & Kuusiene, S. (2004) Organogenesis of Fraxinus excelsior University of Copenhagen, Copenhagen, Denmark. L. by isolated mature embryo culture. Acta Universitatis Latviensis, Biology, Novak, K., Cherubini, P., Saurer, M., Fuhrer, J., Skelly, J.M., Kr€auchi, N. & 676, 197–200. Schaub, M. (2007) Ozone air pollution effects on tree-ring growth, d13C,

visible foliar injury and leaf gas exchange in three ozone-sensitive woody Petritan, A.M., Von Lupke,€ B. & Petritan, I.C. (2007) Effects of shade on plant species. Tree Physiology, 27, 941–949. growth and mortality of maple (Acer pseudoplatanus), ash (Fraxinus excel- Novak, K., Schaub, M., Fuhrer, J., Skelly, J.M., Hug, C., Landolt, W., Bleuler, sior) and beech (Fagus sylvatica) saplings. Forestry, 80, 397–412. P. & Kr€auchi, N. (2005) Seasonal trends in reduced leaf gas exchange and Petritan, A.M., Von Lupke,€ B. & Petritan, I.C. (2009) Influence of light ozone-induced foliar injury in three ozone sensitive woody plant species. availability on growth, leaf morphology and plant architecture of Environmental Pollution, 136,33–45. beech (Fagus sylvatica L.), maple (Acer pseudoplatanus L.) and ash Novak, K., Skelly, J.M., Schaub, M., Kr€auchi, N., Hug, C., Landolt, W. & (Fraxinus excelsior L.) saplings. European Journal of Forest Research, Bleuler, P. (2003) Ozone air pollution and foliar injury development on 128,61–74. native plants of Switzerland. Environmental Pollution, 125,41–52. Petritan, A.M., Von Lupke,€ B. & Petritan, I.C. (2010) A comparative analysis Nowakowska, J., Jabłonowski, S., Mockeliunait e,_ R. & Bieniek, J. (2004) of foliar chemical composition and leaf construction costs of beech (Fagus Genetic Variability within and among Polish and Lithuanian Populations of sylvatica L.), sycamore maple (Acer pseudoplatanus L.) and ash (Fraxinus Common Ash (Fraxinus excelsior L.) based on RAPD Analysis. Baltic For- excelsior L.) saplings along a light gradient. Annals of Forest Science, 67, ar- estry, 10,57–64. ticle 610. Nunez-Regueira,~ L., Rodrıguez An~on, J.A. & Proupın Castineiras,~ J. (1997) Pfanz, H., Aschan, G., Langenfeld-Heyser, R., Wittmann, C. & Loose, M. Calorific values and flammability of forest species in Galicia. Continental (2002) Ecology and ecophysiology of tree stems: corticular and wood photo- high mountainous and humid Atlantic zones. Bioresource Technology, 61, synthesis. Naturwissenschaften, 89, 147–162. 111–119. Pham, T.L.H., Zaspel, I., Schuemann, M., Stephanowitz, H. & Krause, E. Nykvist, N. (1959) Leaching and decomposition of litter I. Experiments on leaf (2013) Rapid in-vitro and in-vivo detection of Chalara fraxinea by means of litter of Fraxinus excelsior. Oikos, 10, 190–211. mass spectrometric techniques. American Journal of Plant Sciences, 4, 444– Oliver, J. (1998) Variability in the common ash (Fraxinus excelsior). Botanical 453. Society of the British Isles News, 78,28–29. Picard, J.-F. (1982) Contribution al’etude de la biologie florale et de la fructifi- Oliver, J. (2009) Squirrel-stripping of native, naturalised, plantation and exotic cation du frêne commun (Fraxinus excelsior L). Revue Forestiere Francaise, trees. Botanical Society of the British Isles News, 112,14–17. 34,97–107. Oliver-Villanueva, J.-V., Gascon-Garrido, P. & de Sales Ibiza-Palacios, M. Pidgeon, N. & Barnett, J. (2013) Chalara and the Social Amplification of Risk. (2013) Evaluation of thermally-treated wood of beech (Fagus sylvatica L.) Department for Environment, Food and Rural Affairs, London, UK. and ash (Fraxinus excelsior L.) against Mediterranean termites (Reticuliter- Pigott, C.D. (1969) The status of Tilia cordata and T. platyphyllos on the Der- mes spp.). European Journal of Wood Products, 71, 391–393. byshire limestone. Journal of Ecology, 57, 491–504. Oostra, S., Majdi, H. & Olsson, M. (2006) Impact of tree species on soil car- Pigott, C.D. (1985) Selective damage to tree-seedlings by bank voles (Clethri- bon stocks and soil acidity in southern Sweden. Scandinavian Journal of onomys glareolus). Oecologia, 67, 367–371. Forest Research, 21, 364–371. Pigott, M.E. & Pigott, C.D. (1959) Stratigraphy and pollen analysis of Malham van Opstal, N.A. (2011) Introduction to the EPPO Workshop on Chalara frax- Tarn and Tarn Moss. Field Studies, 1,84–101. inea, a major threat for ash trees in Europe. EPPO Bulletin, 41,1–2. Pihlgren, A., Hallingb€ack, T., Aronsson, M., Dahlberg, A., Edqvist, M., Johans- Orlikowski, L.B., Ptaszek, M., Rodziewicz, A., Nechwatal, J., Thinggaard, K. & son, G., Krikorev, M. & Thor, G. (2010) The new Swedish red list 2010. Jung, T. (2011) Phytophthora root and collar rot of mature Fraxinus excelsior Svensk Botanisk Tidskrift, 104, 210–226. in forest stands in Poland and Denmark. Forest Pathology, 41, 510–519. Pinto, P.E. & Gegout, J.-C. (2005) Assessing the nutritional and climatic Orlova-Bienkowskaja, M.J. (2014) Ashes in Europe are in danger: the invasive response of temperate tree species in the Vosges Mountains. Annals of Forest range of Agrilus planipennis in European Russia is expanding. Biological Science, 62, 761–770. Invasions, 16, 1345–1349. Piotto, B. (1994) Effects of temperature on germination of stratified seeds of Out, W.A. (2010) Firewood collection strategies at Dutch wetland sites in the three ash species. Seed Science and Technology, 22, 519–529. process of Neolithisation. The Holocene, 20, 191–204. Pliura, A., Lygis, V., Suchockas, V. & Bartkevicius, E. (2011) Performance of Packham, J.R., Thomas, P.A., Atkinson, M.D. & Degen, T. (2012) Biological twenty-four European Fraxinus excelsior populations in three Lithuanian pro- Flora of the British Isles: Fagus sylvatica L. Journal of Ecology, 100, 1557– geny trials with a special emphasis on resistance to Chalara fraxinea. Baltic 1608. Forestry, 17,17–34. Parker, A.G., Goudie, A.S., Anderson, D.E., Robinson, M.A. & Bonsalle, C. Pokorska, O., Dewulf, J., Amelynck, C., Schoon, N., Joa, E., Simpraga, M., (2002) A review of the mid-Holocene elm decline in the British Isles. Pro- Bloemen, J., Steppe, K. & Van Langenhove, H. (2012) Emissions of bio- gress in Physical Geography, 26,1–45. genic volatile organic compounds from Fraxinus excelsior and Quercus Parveen, M., Ahmad, F., Malla, A.M. & Azaz, S. (2015) Microwave-assisted robur under ambient conditions in Flanders (Belgium). International Journal green synthesis of silver nanoparticles from Fraxinus excelsior leaf extract of Environmental Analytical Chemistry, 92, 1729–1741. and its antioxidant assay. Applied Nanoscience, 6, 267–276. Polataycuk, V.K. & Sparik, J.S. (1993) Jasen obyknovennyj v Ukrainskich Patonnier, M.P., Peltier, J.P. & Marigo, G. (1999) Drought-induced increase in Karpatach. Lesovedenie, 1,25–34. xylem malate and mannitol concentrations and closure of Fraxinus excelsior Pollard, E. (1973) Hedges. VII. Woodland Relic Hedges in Huntingdon and L. stomata. Journal of Experimental Botany, 50, 1223–1229. Peterborough. Journal of Ecology, 61, 343–352. Pautasso, M., Aas, G., Queloz, V. & Holdenrieder, O. (2013) European ash Popert, A.H. (1950a) Sylviculture of ash in Great Britain. Journal of Ecology, (Fraxinus excelsior) dieback – A conservation biology challenge. Biological 38, 410. Conservation, 158,37–49. Popert, A.H. (1950b) Contributor to symposium on ash as a forest tree. For- Pearsall, W.H. (1938) The soil complex in relation to plant communities. II. estry, 23, 117–122. Characteristic woodland soils. Journal of Ecology, 26, 194–209. Poschlod, P. & Jordan, S. (1992) Wiederbesiedlung eines aufgeforsteten Kalk- Peeters, A.G. (1998) Cumulative temperatures for prediction of the beginning magerrasenstandorts nach Rodung. Zeitschrift fur€ Okologie€ und Naturschutz, of ash (Fraxinus excelsior L.) pollen season. Aerobiologia, 14, 375–381. 22, 119–139. Peeters, A.G. (2000) Frost periods and beginning of the ash (Fraxinus excelsior Poukens-Renwart, P., Tits, M., Wauters, J.-N. & Angenot, L. (1992) L.) pollen season in Basel (Switzerland). Aerobiologia, 16, 353–359. Reversed-phase HPTLC densitometric evaluation of fraxin in Fraxinus excel- Peltier, J.-P., Agasse, F., De Bock, F. & Marigo, G. (1994) Ajustement osmo- sior leaves. Journal of Pharmaceutical and Biomedical Analysis, 10, 1089– tique chez le frêne commun et stress hydrique. Comptes Rendus de 1091. L’Academie des Sciences. Serie 3. Sciences de la Vie, 317, 679–684. Praeger, R.L. (1913) On the buoyancy of the seeds of some Britannic plants. Pepin, D., Renaud, P.-C., Boscardin, B.Y., Goulard, M., Mallet, C., Anglard, F. Scientific Proceedings of the Royal Dublin Society, 14,13–62. & Ballon, P. (2006) Relative impact of browsing by red deer on mixed Prentice, I.C. & Helmisaari, H. (1991) Silvics of north European trees: Compi- coniferous and broad-leaved seedlings – an enclosure-based experiment. For- lation, comparisons and implications for forest succession modelling. Forest est Ecology and Management, 222, 302–313. Ecology and Management, 42,79–93. Percival, G.C., Keary, I.P. & Al-Habsi, S. (2006) An assessment of the drought Price, P.W. (1991) The plant vigour hypothesis and herbivore attack. Oikos, tolerance of Fraxinus genotypes for urban landscape plantings. Urban For- 62, 244–251. estry & Urban Greening, 5,17–27. Prieditis, N. (1999) Picea abies- and Fraxinus excelsior-dominated wetland for- Petit, R.J., Aguinagalde, I., de Beaulieu, J.-L., Bittkau, C., Brewer, S., Ched- est communities in Latvia. Plant Ecology, 144,49–70. dadi, R. et al. (2003) Glacial refugia: hotspots but not melting pots of Przybył, K. (2002a) Fungi associated with necrotic apical parts of Fraxinus genetic diversity. Science, 300, 1563–1565. excelsior shoots. Forest Pathology, 32, 387–394.

Przybył, K. (2002b) Mycobiota of thin roots showing decay of Fraxinus excel- Rysavy, T. (1991) Ursachen der Vereschung: ein Beitrag zu einem vieldisku- sior L. young trees. Dendrobiology, 48,65–69. tierten Ph€anomen. Forstarchiv, 62, 184–188. Puchner, H. (1922) Die verzogerte€ Keimung von Baums€amereien. Forstwis- Rytkonen,€ A., Lilja, A., Drenkhan, R., Gaitnieks, T. & Hantula, J. (2011) First senschaftliches Centralblatt, 44, 445–455. record of Chalara fraxinea in Finland and genetic variation among isolates Pukacki, P.M. & Przybył, K. (2005) Frost injury as a possible inciting factor in sampled from Aland, mainland Finland, Estonia and Latvia. Forest Pathol- bud and shoot necroses of Fraxinus excelsior L. Journal of Phytopathology, ogy, 41, 169–174. 153, 512–516. Saccone, P., Delzon, S., Pages, J.-P., Brun, J.-J. & Michalet, R. (2009) The role Pureswaran, D.S. & Poland, T.M. (2009) Host selection and feeding preference of biotic interactions in altering tree seedling responses to an extreme cli- of Agrilus planipennis (Coleoptera: Buprestidae) on ash (Fraxinus spp.). matic event. Journal of Vegetation Science, 20, 403–414. Environmental Entomology, 38, 757–765. Sadori, L., Allevato, E., Bellini, C., Bertacchi, A., Boetto, G., Di Pasquale, G., Puri, G.S. (1948) The ash-oak woods of the English Lake District. Journal of Giachi, G., Giardini, M., Masi, A., Pepe, C., Ermolli, E.R. & Lippi, M.M. the Indian Botanical Society, 27, 211–227. (2015) Archaeobotany in Italian ancient Roman harbours. Review of Puri, G.S. (1950a) Surface geology, vegetation and plant succession. Indian Palaeobotany and Palynology, 218, 217–230. Forester, 76,1–21. Salisbury, E.J. & Jane, F.W. (1940) Charcoals from Maiden Castle and their Puri, G.S. (1950b) The ecology of the humus layer in some English forests. significance in relation to the vegetation and climatic conditions in prehistoric Indian Forester, 76, 453–466. times. Journal of Ecology, 28, 310–325. Puszynski, J., Molinski, W. & Preis, A. (2015) The effect of wood on the Sangi, M.R., Shahmoradi, A., Zolgharnein, J., Azimi, G.H. & Ghorbandoost, sound quality of electric string instruments. Acta Physica Polonica A, 127, M. (2008) Removal and recovery of heavy metals from aqueous solution 114–116. using Ulmus carpinifolia and Fraxinus excelsior tree leaves. Journal of Queloz, V., Grunig, C.R., Berndt, R., Kowalski, T., Sieber, T.N. & Holden- Hazardous Materials, 155, 513–522. rieder, O. (2011) Cryptic speciation in Hymenoscyphus albidus. Forest Santamour, F.S. (1981) Flavonoids and coumarins in Fraxinus and their poten- Pathology, 41, 133–142. tial utility in hybrid verification. Proceedings of the 27th Northeast Forest Rackham, O. (1995) The History of the Countryside. Weidenfeld & Nicolson, Tree Improvement Conference (ed. D.H. Dehayes), pp. 42–46. University of London, UK. Vermont, Burlington, VT, USA. Rackham, O. (2003) Ancient Woodland, its History, Vegetation and Uses in Sanz, M., Fernandez de Simon, B., Cadahıa, E., Esteruelas, E., Munoz,~ England. Castlepoint Press, Dalbeattie, UK. A.M., Hernandez, M.T. & Estrella, I. (2012) Polyphenolic profile as a use- Rackham, O. (2014) The Ash Tree. Little Toller, Fratrum, UK. ful tool to identify the wood used in wine aging. Analytica Chimica Acta, Rajapaksha, N.S.S., Butt, K.R., Vanguelova, E.I. & Moffat, A.J. (2013) Effects 732,33–45. of short rotation forestry on earthworm community development in the UK. Sarlov€ Herlin, I.L. & Fry, G.L.A. (2000) Dispersal of woody plants in forest Forest Ecology and Management, 309,96–104. edges and hedgerows in a Southern Swedish agricultural area: the role of site Ramos, C., Matas, I.M., Bardaji, L., Aragon, I.M. & Murillo, J. (2012) Pseu- and landscape structure. Landscape Ecology, 15, 229–242. domonas savastanoi pv. savastanoi: some like it knot. Molecular Plant Biol- Sass-Klaassen, U., Sabajo, C.R. & den Ouden, J. (2011) Vessel formation in ogy, 13, 998–1009. relation to leaf phenology in pedunculate oak and European ash. Den- Raquin, C., Brachet, S., Jeandroz, S., Vedel, F. & Frascaria-Lacoste, N. drochronologia, 29, 171–175. (2002a) Combined analyses of microsatellite and RAPD markers demonstrate S€aumel, I. & Kowarik, I. (2013) Propagule morphology and river characteristics possible hybridisation between Fraxinus excelsior L. and Fraxinus angustifo- shape secondary water dispersal in tree species. Plant Ecology, 214, 1257– lia Vahl. Forest Genetics, 9, 103–111. 1272. Raquin, C., Jung-Muller, B., Dufour, J. & Frascaria-Lacoste, N. (2002b) Rapid Savill, P. (2015) High forest management and the rise of even-aged stands. seedling obtaining from European ash species Fraxinus excelsior (L.) and Europe’s Changing Woods and Forests (eds K.J. Kirby & C. Watkins), pp. Fraxinus angustifolia (Vahl.). Annals of Forest Science, 59, 219–224. 93–106. CABI, Wallingford, UK. Rasmussen, P. (1989) Leaf-foddering of livestock in the Neolithic: archaeob- Savill, P.S., Spencer, R., Roberts, J.E. & Hubert, J.D. (1999) Sixth Year results otanical evidence from Weier, Switzerland. Journal of Danish Archeology, 8, from four ash (Fraxinus excelsior) breeding seedling orchards. Silvae Genet- 51–71. ica, 48,92–100. Reid, D.A. (1978) Unusual hosts for some common British fungi. Bulletin of Saxe, H. & Kerstiens, G. (2005) Climate change reverses the competitive bal- the British Mycological Society, 12,87–89. ance of ash and beech seedlings under simulated forest conditions. Plant Reiner, S., Wiltshire, J.J.J., Wright, C.J. & Colls, J.J. (1996) The impact of Biology, 7, 375–386. ozone and drought on the water relations of ash trees (Fraxinus excelsior L.). Scannell, M.J.P. (2008) The cauliflower ash gall on Fraxinus excelsior L. Journal of Plant Physiology, 148, 166–171. (Ash) in Ireland. Irish Naturalists’ Journal, 29, 135–136. Riepsas, E. (2009) Pazeistuz uosynuz atsikurimo/atk urimo bukl e_ ir taikytinos Scheer, R. (2001) In Yggdrasils Schatten. Fraxinus excelsior - Baum des Jahres priemones_ [Regeneration of damaged common ash stands and recommended 2001. Stadt und Gruen, 10, 695–702. measures.]. Musu z Girios, 10,18–19. Scherrer, D., Bader, M.K.-F. & Korner,€ C. (2011) Drought-sensitivity ranking Rishbeth, J. (1948) The flora of Cambridge walls. Journal of Ecology, 36, of deciduous tree species based on thermal imaging of forest canopies. Agri- 136–148. cultural and Forest Meteorology, 151, 1632–1640. Roberts, J. & Rosier, P.T.W. (1994) Comparative estimates of transpiration of Schmiedel, D. (2010) Invasionsbiologie und okologisches€ Verhalten der gebi- ash and beech forest at a chalk site in southern Britain. Journal of Hydrol- etsfremden Baumart Fraxinus pennsylvanica Marsh. in den Auenw€aldern der ogy, 162, 229–245. Mittelelbe im naturschutzfachlichen Kontext. PhD thesis, Technische Univer- Rodwell, J.S. (1991) British Plant Communities, vol. 1. Woodlands and Scrub. sit€at Dresden, Dresden, Germany. Cambridge University Press, Cambridge, UK. Schmiedel, D. & Tackenberg, O. (2013) Hydrochory and water induced germi- Rohmeder, E. (1949) Der geschlechtliche Dimorphismus als pflanzenzuchter-€ nation enhance invasion of Fraxinus pennsylvanica. Forest Ecology and isches Problem, argestellt an den Wuchsleistungen m€annlicher und weiblicher Management, 304, 437–443. Eschen. Forstwissenschaftliches Centralblatt, 68, 680–691. Schmitt, U., Richter, H.G. & Muche, C. (1997) TEM study of wound-induced Rohmeder, E. (1967) Berziehungen zwischen Frucht-bzw. Samenerzeugung und vessel occlusions in European ash (Fraxinus excelsior L.). IAWA Journal, Holzerzeugung der Waldbaume. Allgemeine Forst Zeitschrift, 22,33–39. 18, 401–404. Rosenvald, P., Drenkhan, R., Riit, T. & Lohmus,~ A. (2015) Towards silvicul- Schoebel, C.N., Zoller, S. & Rigling, D. (2014) Detection and genetic charac- tural mitigation of the European ash (Fraxinus excelsior) dieback: the impor- terisation of a novel mycovirus in Hymenoscyphus fraxineus, the causal agent tance of acclimated trees in retention forestry. Canadian Journal of Forest of ash dieback. Infection, Genetics and Evolution, 28,78–86. Research, 45, 1206–1214. Schoenweiss, K., Meier-Dinkel, A. & Grotha, R. (2005) Comparison of cryop- Rosselli, W., Keller, C. & Boschi, K. (2003) Phytoextraction capacity of trees reservation techniques for long-term storage of ash (Fraxinus excelsior L.). growing on a metal contaminated soil. Plant and Soil, 256, 265–272. CryoLetters, 26, 201–212. Ruhnke, H., Sch€adler, M., Klotz, S., Matthies, D. & Brandl, R. (2009) Variabil- Scholtysik, A., Unterseher, M., Otto, P. & Wirth, C. (2013) Spatio-temporal ity in leaf traits, insect herbivory and herbivore performance within and dynamics of endophyte diversity in the canopy of European ash (Fraxinus among individuals of four broad-leaved tree species. Basic and Applied Ecol- excelsior). Mycological Progress, 12, 291–304. ogy, 10, 726–736. de Schrijver, A., de Frenne, P., Staelens, J., Verstraeten, G., Muys, B., Ves- Rust, S. & Savill, P.S. (2000) The root systems of Fraxinus excelsior and terdal, L., Wuyts, K., van Nevel, L., Schelfhout, S., de Neve, S. & Verheyen, Fagus sylvatica and their competitive relationships. Forestry, 73, 499–508. K. (2012) Tree species traits cause divergence in soil acidification during

four decades of postagricultural forest development. Global Change Biology, Sydes, C. & Grime, J.P. (1981a) Effects of tree leaf litter on herbaceous vegeta- 18, 1127–1140. tion in deciduous woodland: I. Field investigations. Journal of Ecology, 69, Schulz, H., H€artling, S. & Stange, C.F. (2011) Species-specific differences in 237–248. nitrogen uptake and utilization by six European tree species. Journal of Plant Sydes, C. & Grime, J.P. (1981b) Effects of tree leaf litter on herbaceous vege- Nutrition and Soil Science, 174,28–37. tation in deciduous woodland: II. experimental investigation. Journal of Ecol- Schumacher, J. (2011) The general situation regarding ash dieback in Germany ogy, 69, 249–262. and investigations concerning the invasion and distribution strategies of Cha- Sykes, M.T., Prentice, I.C. & Cramer, W. (1996) A bioclimatic model for the lara fraxinea in woody tissue. EPPO Bulletin, 41,7–10. potential distributions of north European tree species under present and future Schumacher, J., Kehr, R. & Leonhard, S. (2010) Mycological and histological climates. Journal of Biogeography, 23, 203–233. investigations of Fraxinus excelsior nursery saplings naturally infected by Synge, A.D. (1947) Pollen collection by honeybees (Apis mellifera). Journal of Chalara fraxinea. Forest Pathology, 40, 419–429. Animal Ecology, 16, 122–138. Scurfield, G. (1959) The ashwoods of the Derbyshire Carboniferous limestone: Tabari, M., Lust, M. & Neirynk, J. (1998) Effect of light and humus on sur- Monk’s Dale. Journal of Ecology, 47, 357–369. vival and height growth of ash (Fraxinus excelsior L.) seedlings. Silva Gan- Seven, J. & Polle, A. (2014) Subcellular nutrient element localization and davensis, 63,36–49. enrichment in ecto- and arbuscular mycorrhizas of field-grown beech and ash Tal, O. (2006) Comparative flowering ecology of Fraxinus excelsior, Acer pla- trees indicate functional differences. PLoS One, 9, e114672. tanoides, Acer pseudoplatanus and Tilia cordata in the canopy of Leipzig’s Shanbhag, R.R. & Sundararaj, R. (2013) Physical and chemical properties of floodplain forest. PhD thesis, University of Leipzig, Leipzig, Germany. some imported woods and their degradation by termites. Journal of Insect Tal, O. (2011) Flowering phenological pattern in crowns of four temperate Science, 13, article 63. deciduous tree species and its reproductive implications. Plant Biology, 13 Shimwell, D.W. (1999) Colonisation of the ramparts and walls of Berwick- (Suppl. 1), 62–70. upon-Tweed by native and alien trees and shrubs. Botanical Society of the Talgø, V., Sundheim, L., Gjærum, H.B., Herrero, M.L., Suthaparan, A., British Isles News, 112,20–22. Toppe, B. & Stensvand, A. (2011) Powdery mildews on ornamental trees Siebel, H.N. & Blom, C.W.P.M. (1998) Effects of irregular flooding on the and shrubs in Norway. European Journal of Plant Science and Biotechnol- establishment of tree species. Acta Botanica Neerlandica, 47, 231–240. ogy, 5,86–92. Siebel, H.N. & Bouwma, I.M. (1998) The occurrence of herbs and woody juve- Tapper, P.-G. (1992a) Demography of persistent juveniles in Fraxinus excel- niles in a hardwood floodplain forest in relation to flooding and light. Jour- sior. Ecography, 15, 385–392. nal of Vegetation Science, 9, 623–630. Tapper, P.-G. (1992b) Irregular fruiting in Fraxinus excelsior. Journal of Vege- Siebel, H.N., van Wijk, M. & Blom, C.W.P.M. (1998) Can tree seedlings sur- tation Science, 3,41–46. vive increased flood levels of rivers? Acta Botanica Neerlandica, 47, 219– Tapper, P.-G. (1996a) Tree dynamics in a successional Alnus-Fraxinus wood- 230. land. Ecography, 19, 237–244. Siljak-Yakovlev, S., Temunovic, M., Robin, O., Raquin, C. & Frascaria- Tapper, P.-G. (1996b) Long-term patterns of mast fruiting in Fraxinus excel- Lacoste, N. (2013) Molecular–cytogenetic studies of ribosomal RNA genes sior. Ecology, 77, 2567–2572. and heterochromatin in three European Fraxinus species. Tree Genetics & Taylor, N.W. (1982) The ecology and status of sycamore, and its value to wild- Genomes, 10, 231–239. life. MSc dissertation, University College London, London, UK. Silveira, C.E. & Cottignies, A. (1994) Period of harvest, sprouting ability of Thomas, P.A. (2014) Trees: Their Natural History, 2nd edn. Cambridge cuttings, and in vitro plant regeneration in Fraxinus excelsior. Canadian University Press, Cambridge, UK. Journal of Botany, 72, 261–267. Thomasset, M., Fernandez-Manjarres, J.F., Douglas, G.C., Bertolino, P., Fras- Sinclair, W.A. & Griffiths, H.M. (1994) Ash yellows and its relationship caria-Lacoste, N. & Hodkinson, T.R. (2012) Assignment testing reveals mul- to dieback and decline of ash. Annual Review of Phytopathology, 32, tiple introduced source populations including potential ash hybrids (Fraxinus 49–60. excelsior x F. angustifolia) in Ireland. European Journal of Forest Research, Sjoman,€ H., Ostberg,€ J. & Buhler,€ O. (2012) Diversity and distribution of the 132, 195–209. urban tree population in ten major Nordic cities. Urban Forestry & Urban Thomasset, M., Hodkinson, T.R., Restoux, G., Frascaria-Lacoste, N., Douglas, Greening, 11,31–39. G.C. & Fernandez-Manjarres, J.F. (2014) Thank you for not flowering: con- Skovsgaard, J.P., Thomsen, I.M., Skovgaard, I.M. & Martinussen, T. (2010) servation genetics and gene flow analysis of native and non-native popula- Associations among symptoms of dieback in even-aged stands of ash (Fraxi- tions of Fraxinus (Oleaceae) in Ireland. Heredity, 112, 596–606. nus excelsior L.). Forest Pathology, 40,7–18. Thompson, H. (2012) The chestnut resurrection. Nature, 490,22–23. Skrzypczynska, M. (2002) Studies on insects and mites causing galls on the Thoms, R., Kohler,€ M., Gessler, A. & Gleixner, G. (2015) Transport of soluble leaves of common ash Fraxinus excelsior L. in the Ojcow National Park in carbohydrates in temperate deciduous trees: beech (Fagus sylvatica) and ash Poland. Journal of Pest Science, 75,11–12. (Fraxinus excelsior) in comparison. Geophysical Research Abstracts, 17, Slotte, H. (1997) Pollarding: A look back on its history, and advice to nature EGU2015–EGU9291. conservationists. Svensk Botanisk Tidskrift, 91,1–21. Till, O. (1956) Uber€ die Frosth€arte von Pflanzen sommergruner€ Laubw€alder. Sorz, J. & Hietz, P. (2006) Gas diffusion through wood: implications for oxy- Flora – Allgemeine Botanische Zeitung, 143, 499–542. gen supply. Trees, 20,34–41. Timmermann, V., Børja, I., Hietala, A.M., Kirisits, T. & Solheim, H. (2011) Southwood, T.R.E. (1961) The number of species of insect associated with var- Ash dieback: pathogen spread and diurnal patterns of ascospore dispersal, ious trees. Journal of Animal Ecology, 30,1–8. with special emphasis on Norway. EPPO Bulletin, 41,14–20. Sp€ath, V. (1988) Zur Hochwassertoleranz von Auenwaldb€aumen. Natur und Tinner, W., Conedera, M., Ammann, A. & Lotter, A.F. (2005) Fire ecology Landschaft, 7, 312–315. north and south of the Alps since the last ice age. The Holocene, 15, article Steindor, K., Palowski, B., Goras, P. & Nadgorska-Socha, A. (2011) Assess- 1214. ment of bark reaction of select tree species as an indicator of acid gaseous Tinner, W., Conedera, M., Gobet, E., Hubschmid, P., Wehrli, M. & Ammann, pollution. Polish Journal of Environmental Studies, 20, 619–622. B. (2000) A palaeoecological attempt to classify fire sensitivity of trees in Stener, L.-G. (2012) Clonal differences in susceptibility to the dieback of Frax- the southern Alps. The Holocene, 10, 565–574. inus excelsior in southern Sweden. Scandinavian Journal of Forest Research, Tinner, W., Hubschmid, P., Wehrli, M., Ammann, B. & Conedera, M. (1999) 28, 205–216. Long-term forest fire ecology and dynamics in southern Switzerland. Journal Stenlid, J., Oliva, J., Boberg, J.B. & Hopkins, A.J. (2011) Emerging diseases of Ecology, 87, 273–289. in European forest ecosystems and responses in society. Forests, 2, 486– Tremolieres, M., Schnitzler, A., Sanchez-Perez, J.-M. & Schmitt, D. (1999) 504. Changes in foliar nutrient content and resorption in Fraxinus excelsior L., Stohr,€ A. & Losch,€ R. (2004) Xylem sap flow and drought stress of Fraxinus Ulmus minor Mill. and Clematis vitalba L. after prevention of floods. Annals excelsior saplings. Tree Physiology, 24, 169–180. of Forest Science, 56, 641–650. Strestil, S. & Sammonil, P. (2006) Ecological valence of expanding European von Tubeuf, K.F. (1897) Diseases of Plants Induced by Cryptogamic Parasites ash (Fraxinus excelsior L.) in the Bohemian Karst (Czech Republic). Journal (English Translation by W.G. Smith). Longmans, London, UK. of Forest Science, 52, 293–305. Tulik, M., Marciszewska, K. & Adamczyk, J. (2010) Diminished vessel diame- Sutherland, B.G., Belaj, A., Nier, S., Cottrell, J.E., Vaughan, S.P., Hubert, J. & ter as a possible factor in the decline of European ash (Fraxinus excelsior Russell, K. (2010) Molecular biodiversity and population structure in com- L.). Annals of Forest Science, 67, article 103. mon ash (Fraxinus excelsior L.) in Britain: implications for conservation. Tylkowski, T. (1990) Mediumless stratification and dry storage of after-ripened Molecular Ecology, 19, 2196–2211. seeds of Fraxinus excelsior L. Arboretum Kornickie , 35, 143–152.

Urban, J., Suchomel, J. & Dvorak, J. (2008) Contribution to the knowledge of Watt, A.S. (1925) On the ecology of British beechwoods with special reference to woods preferences of European beaver (Castor fiber L. 1758) in bank vege- their regeneration: part II, sections II and III. The development and structure of tation on non-forest land in the forest district Soutok (Czech Republic). Acta beech communities on the Sussex Downs. Journal of Ecology, 13,27–73. Universitatis Agriculturae et Silviculturae Mendelianae Brunensis, 56, 289– Weber, G. & Bahr, B. (2000a) Wachstum und Ern€ahrungszustand junger 294. Eschen (Fraxinus excelsior L.) und Bergahorne (Acer pseudoplatanus L.) auf Van de Walle, C. (1987) Germination uniformity of Fraxinus excelsior con- Sturmwurffl€achen in Bayern in Abh€angigkeit vom Standort. Forstwis- trolled by seed water content during cold treatment. Physiologia Plantarum, senschaftliches Centralblatt, 119, 177–192. 69, 645–650. Weber, G. & Bahr, B. (2000b) Eignung bayerischer Standorte fur€ den Anbau Van Uytvanck, J., Milotic, T. & Hoffmann, M. (2010) Interaction between von Esche (Fraxinus excelsior L.) und Bergahorn (Acer pseudoplatanus L.). large herbivore activities, vegetation structure, and flooding affects tree seed- Forstwissenschaftliches Centralblatt, 119, 263–275. ling emergence. Plant Ecology, 206, 173–184. Weber, G. & Claus, M. (2000) The influence of chemical soil factors on the Vesterdal, L., Elberling, B., Christiansen, J.R., Callesen, I. & Schmidt, I.K. development of VA mycorrhizas of ash (Fraxinus excelsior L.) and sycamore (2012) Soil respiration and rates of soil carbon turnover differ among six (Acer pseudoplatanus L.) in pot experiments. Journal of Plant Nutrition and common European tree species. Forest Ecology and Management, 264, 185– Soil Science, 163, 609–616. 196. Weber-Blaschke, G., Claus, M. & Rehfuess, K.E. (2002) Growth and nutrition Vesterdal, L., Schmidt, I.K., Callesen, I., Nilsson, L.O. & Gundersen, P. (2008) of ash (Fraxinus excelsior L.) and sycamore (Acer pseudoplatanus L.) on Carbon and nitrogen in forest floor and mineral soil under six common Euro- soils of different base saturation in pot experiments. Forest Ecology and pean tree species. Forest Ecology and Management, 255,35–48. Management, 167,43–56. Villiers, T.A. (1971) Cytological studies in dormancy. I. Embryo maturation Weber-Blaschke, G., Heitz, R., Blaschke, M. & Ammer, C. (2008) Growth and during dormancy in Fraxinus excelsior. New Phytologist, 70, 751–760. nutrition of young European ash (Fraxinus excelsior L.) and sycamore maple Villiers, T.A. (1972) Cytological studies in dormancy. II. Pathological ageing (Acer pseudoplatanus L.) on sites with different nutrient and water statuses. changes during prolonged dormancy and recovery upon dormancy release. European Journal of Forest Research, 127, 465–479. New Phytologist, 71, 145–152. Weber-Blaschke, G. & Rehfuess, K.E. (2002) Correction of Al toxicity with Villiers, T.A. & Wareing, P.F. (1964) Dormancy in fruits of Fraxinus excelsior European ash (Fraxinus excelsior L.) growing on acid soils by fertilization L. Journal of Experimental Botany, 15, 359–367. with Ca and Mg carbonate and sulfate in pot experiments. Forest Ecology Villiers, T.A. & Wareing, P.F. (1965a) The possible role of low temperature in and Management, 167, 173–183. breaking the dormancy of seeds of Fraxinus excelsior L. Journal of Experi- Weissen, F., Baix, P., Boseret, J.P., Bronchart, L., Lejeune, M., Maquet, P. mental Botany, 16, 519–531. et al. (1991) Le Fichier Ecologique des Essences. Ministere de la Region Villiers, T.A. & Wareing, P.F. (1965b) The growth-substance content of dor- Wallonne, Namur, Belgium. mant fruits of Fraxinus excelsior L. Journal of Experimental Botany, 16, Weiser, F. (1964) Beitrag zum Problem der sog. Bodenrassen bei unseren 533–544. Waldbaumarten, unter besonderer Berucksichtigung€ der Esche. Fraxinus Vitasse, Y., Delzon, S., Bresson, C.C., Michalet, R. & Kremer, A. (2009a) Alti- Excelsior L. Forstwissenschaftliches Centralblatt, 83,23–33. tudinal differentiation in growth and phenology among populations of tem- Wellock, M.L., Rafique, R., LaPerle, C.M., Peichl, M. & Kiely, G. (2014) perate-zone tree species growing in a common garden. Canadian Journal of Changes in ecosystem carbon stocks in a grassland ash (Fraxinus excelsior L.) Forest Research, 39, 1259–1269. afforestation chronosequence in Ireland. Journal of Plant Ecology, 7, 429–438. Vitasse, Y., Delzon, S., Dufrêne, E., Pontailler, J.-Y., Louvet, J.-M., Kremer, Westergren, M., Jarni, K., Brus, R. & Kraigher, H. (2012) Implications for the A. & Michalet, R. (2009b) Leaf phenology sensitivity to temperature in use of forest reproductive material of common ash (Fraxinus excelsior L.) in European trees: Do within-species populations exhibit similar responses? Slovenia based on the analysis of nuclear microsatellites. Sumarski List, 86, Agricultural and Forest Meteorology, 149, 735–744. 263–271. Vitasse, Y., Hoch, G., Randin, C.F., Lenz, A., Kollas, C., Scheepens, J.F. & Whalley, A.J.S. & Watling, R. (1980) Daldinia concentrica versus Daldinia Korner,€ C. (2013) Elevational adaptation and plasticity in seedling phenology vernicosa. Transactions of the British Mycological Society, 74, 399–406. of temperate deciduous tree species. Oecologia, 171, 663–678. Wiersum, L.K. & Harmanny, K. (1983) Changes in the water-permeability of Vitasse, Y., Porte, A.J., Kremer, A., Michalet, R. & Delzon, S. (2009c) roots of some trees during drought stress and recovery, as related to prob- Responses of canopy duration to temperature changes in four temperate tree lems of growth in the urban environment. Plant and Soil, 75, 443–448. species: relative contributions of spring and autumn leaf phenology. Oecolo- Willoughby, I., Jinks, R.L., Kerr, G. & Gosling, P.G. (2004) Factors affecting gia, 161, 187–198. the success of direct seeding for lowland afforestation in the UK. Forestry, Vreugdenhil, S.J., Kramer, K. & Pelsma, T. (2006) Effects of flooding duration, 77, 467–482. -frequency and -depth on the presence of saplings of six woody species in Woods, R.G. & Coppins, B.J. (2012) A Conservation Evaluation of British north-west Europe. Forest Ecology and Management, 236,47–55. Lichens and Lichenicolous Fungi. Joint Nature Conservation Committee, Wagner, J. (1996) Changes in dormancy levels of Fraxinus excelsior L. Peterborough, UK. embryos at different stages of morphological and physiological maturity. Woodward, S. & Boa, E. (2013) Ash dieback in the UK: a wake-up call. Trees, 10, 177–182. Molecular Plant Pathology, 14, 856–860. Wagner, J. & Kafka, I. (1995) Effects of medium composition on in vitro ger- Worrell, R. (2013) An Assessment of the Potential Impacts of Ash Dieback in mination of embryos of Fraxinus excelsior at different stages of develop- Scotland. Forestry Commission Scotland, Edinburgh, UK. ment. Journal of Plant Physiology, 146, 566–568. Wratten, S.D., Goddard, P. & Edwards, P.J. (1981) British trees and insects: Wagner, S. (1990) Zu: Vereschung - Problem oder Chance? Allgemeine Forst- the role of palatability. American Naturalist, 118, 916–919. Zeitschrift, 32, 806–807. Yaltirik, F. (1978) Oleaceae. Flora of Turkey and the East Aegean Islands, vol. Wagner, S. (1997) Ein Modell zur Fruchtausbreitung der Esche (Fraxinus 6 (ed. P.H. Davis), pp. 145–158. Edinburgh University Press, Edinburgh, excelsior L.) unter Berucksichtigung€ von Richtungseffekten. Allgemeine UK. Forst-und Jagdzeitung, 168, 149–155. Yousefi, M., Pourmajidian, M.R., Karimi, M. & Darvishi, L. (2013) Quantita- Wagner, S., W€alder, K., Ribbens, E. & Zeibig, A. (2004) Directionality in fruit tive and qualitative evaluation of forest plantations by four species and sug- dispersal models for anemochorous forest trees. Ecological Modelling, 179, gestion the appropriate species in the Hyrcanian forest. European Journal of 487–498. Experimental Biology, 3, 352–360. Wallander, E. (2001) Evolution of wind-pollination in Fraxinus (Oleaceae) - an Zemankova, K. & Brechler, J. (2010) Emissions of biogenic VOC from forest ecophylogenetic approach. PhD thesis, Goteborg€ University, Goteborg,€ Swe- ecosystems in central Europe: estimation and comparison with anthropogenic den. emission inventory. Environmental Pollution, 158, 462–469. Wallander, E. (2008) Systematics of Fraxinus (Oleaceae) and evolution of Zollner, A. & Kolling,€ C. (1994) Eschenkulturen auf ungeeigneten Standorten. dioecy. Plant Systematics and Evolution, 273,25–49. Allgemeine Forstz, 2,61–64. Walthert, L., Pannatier, E.G. & Meier, E.S. (2013) Shortage of nutrients and Zulet, M.A., Navas-Carretero, S., Lara y Sanchez, D., Abete, I., Flanagan, excess of toxic elements in soils limit the distribution of soil-sensitive tree J., Issaly, N., Fanca-Berthon, P., Bily, A., Rollerc, M. & Martineza, J.A. species in temperate forests. Forest Ecology and Management, 297,94–107. (2014) A Fraxinus excelsior L. seeds/fruits extract benefits glucose Wardle, P. (1959) The regeneration of Fraxinus excelsior in woods with a field homeostasis and adiposity related markers in elderly overweight/obese layer of Mercurialis perennis. Journal of Ecology, 47, 483–497. subjects: A longitudinal, randomized, crossover, double-blind, Wardle, P. (1961) Biological Flora of the British Isles: Fraxinus excelsior L. placebo-controlled nutritional intervention study. Phytomedicine, 21, 1162– Journal of Ecology, 49, 739–751. 1169.