Journal of Ecology 2012, 100, 1557–1608 doi: 10.1111/j.1365-2745.2012.02017.x BIOLOGICAL FLORA OF THE BRITISH ISLES* No. 269 List Vasc. PI. Br. Isles (1992) no. 39, 1, 1 Biological Flora of the British Isles: Fagus sylvatica John R. Packham1, Peter A. Thomas2†, Mark D. Atkinson3 and Thomas Degen4 1 School of Applied Sciences, University of Wolverhampton, Wolverhampton, WV1 1SB, UK; 2School of Life Sciences, Keele University, Staffs ST5 5BG, UK; 3Queens Square House, Queens Square, Llangandog, S. Wales, SA19 9BW, UK; and 4Forestry Unit, Catholic University of Louvain, Louvain-La Neuve, B-1348, Belgium Summary 1. This account presents information on all aspects of the biology of Fagus sylvatica L. 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. Fagus sylvatica (Beech) is a large usually single-stemmed deciduous tree native to south-east England but now growing over almost the whole of the British Isles, often planted as a forestry tree on all but the wettest soils. It forms extensive woodlands, where it is dominant over a large altitudinal range, competing primarily with Quercus robur. The outcome of this competition is determined by local soil and climatic conditions leading to a gradation into oak woodlands. It is monoecious, wind-pollinated and notable for its periodic large seed numbers (mast years); seed is dispersed by birds and mammals but mostly drops below the parent tree. 3. Fagus sylvatica is hardy, very shade tolerant, casts a deep shade and is fairly resistant to browsing but susceptible to spring frosts. 4. Due to its shallow rooting and intensive rather than extensive mode of soil water exploitation, it is also susceptible to drought, and this is likely to be the main factor controlling its expected response to climate change. 5. Fagus sylvatica is facing few conservation problems, and indeed, its range is currently expanding into central Europe. However, in the face of climate change, its range is likely to contract from its extremes in all but the north, and Phytophthora diseases may become more serious. Key-words: climatic limitation, communities, conservation, ecophysiology, geographical and altitudinal distribution, germination, herbivory, mycorrhiza, parasites and diseases, reproductive biology, soils Fagaceae. Fagus sylvatica L., European beech is a large tree of variable form, often 30–40 m tall, but occasionally reaching 50 m in near-natural conditions (Degen 2001). Bark silver-grey though often tinged green by epiphytic algae, smooth, occasionally slightly roughened. Buds 1–2 cm, fusiform, reddish-brown. Twigs dull purple-brown, becoming greyer in second year. Leaves alternate, ovate to elliptic, 4–10 cm long with five to nine pairs of veins which are prominent beneath, but trimmed individuals frequently have †Correspondence author. E-mail: p.a.thomas@keele.ac.uk *Nomenclature of vascular plants follows Stace (2010) and for nonBritish species, Flora Europaea. very large leaves with lamina reaching 16 cm long and 11.4 cm wide (measured from a young hedge in east Devon, May 1998); petiole 5–15 mm. Lamina margins at first markedly hairy with a wavy edge and more pronounced scalloping or slight toothing near the leaf tip. The hairiness later disappears but the scalloping or toothing, which is more pronounced in some cases than others, remains. Monoecious; male and female flowers borne on the same branches, opening as the leaves unfold; protogynous. Male flowers numerous, crowded into slender-stalked, pendent globose heads, each flower with 8–16 stamens surrounded by a 4–7 lobed perianth. Female inflorescence usually with two flowers, each with three styles and a 4–5 lobed perianth, each pair sur- © 2012 The Authors. Journal of Ecology © 2012 British Ecological Society 1558 J. R. Packham et al. rounded by a scaly 4-partite involucral cupule. Anemophilous. Fruit an ovoid sharply 3-angled nut 12–18 mm long, 1–2(5) nuts enclosed within a cupule 2–5(7.5) cm long, covered with prickly, awl-shaped appendages; peduncle stout and shortly hairy. A very unusual double capsule was collected from the Himley beech mast site on 8 October 2001. Fagus sylvatica has been regarded as having two subspecies (ssp. sylvatica and ssp. orientalis (Lipsky) Greuter & Burdet, oriental beech) and two intermediary types, ssp. moesiaca (K. Malý) Szafer and ssp. taurica (K. Malý) Szafer (Moore 1982; Denk et al. 2002). Ssp. sylvatica differs in a number of ways from ssp. orientalis, including leaf traits (Hatziskakis, Tsiripidis & Papageorgiou 2011); the latter is found in Asia Minor, Syria, Iran and the Caucasus Mountains. Although the two taxa have much in common, many authors (including Hora 1981) have treated oriental beech as a discrete, though closely related, species; we agree with Shen (1992), however, that subspecies status is more appropriate. The taxonomic status of the intermediate type, the Balkan beech (Fagus sylvatica ssp. moesiaca), has varied over the years. It has been treated as a separate species (Czeczott 1933), a phylogenetic link between F. sylvatica and F. orientalis (Mišić 1957), a hybrid between the two, though morphologically closer to F. sylvatica (Becker 1981), an ecotype (Staňescu 1979) or a subspecies (Gömöry et al. 1999, 2010). Isozyme markers indicate that the rank of subspecies is the most appropriate. Fagus sylvatica ssp. moesiaca differs morphologically from typical F. sylvatica in possessing larger leaves with more veins, larger nuts and a longer cupule peduncle (Czeczott 1933; Mišić 1957; Staňescu 1979). Paffetti et al. (2007) using chloroplast DNA concluded that spp. orientalis was the ancestral species of F. sylvatica, hence the close relationship of the two modern forms. The Crimean beech, ssp. taurica, is considered by some to be an intermediate form between ssp. sylvatica and ssp. orientalis and by others as an independent species (see Paule 1995 for references). More recently, Denk et al. (2002), after investigating nuclear rDNA internal transcribed spacer sequences, concluded that there is only a single species, Fagus sylvatica, in Europe and Asia Minor. Fagus sylvatica has a number of common cultivars, which have to be grafted (Hora 1981); details of their history are given by Mitchell (1996). Leaves of F. sylvatica ‘Asplenifolia’ (fernleaf beech) vary between narrowly strap-shaped to deeply pinnately lobed. F. sylvatica ‘Heterophylla’ (cutleaved beech) has two forms. In forma laciniata, the ovatelanceolate leaves taper at both ends, and the leaf margin has seven to nine deep serrations on each side, extending onethird of the way to the midrib. Forma latifolia has larger leaves than the type (up to 8 9 14 cm in young trees but somewhat smaller in older specimens). In purple or copper beeches (Fagus sylvatica ‘Purpurea’), which are of German origin, leaf chlorophylls are masked by varying proportions of anthocyanin pigments resulting in varying shades of purple, purplish-black or almost dark red. The golden-yellow young leaves of F. sylvatica ‘Zlatia’ later turn green. F. sylvatica ‘Dawyck’ (Dawyck’s beech), a fastigiate form which arose near Peebles, Scotland, as single tree around 1860, is widely planted. Weeping beeches (F. sylvatica ‘Pendula’) include forms in which the main branches are horizontal but draped with pendulous branchlets, as well as those in which the main branches are also pendulous. Weeping purple beeches are now not uncommon in English parks and gardens. Fagus sylvatica is native to south-east England on welldrained soils and to much of continental Europe, but very widely planted outside this range as a forestry tree (especially in France) and ornamentally on all but the wettest soils. It tends to dominate extensive woodlands within its native range, competing primarily with Quercus robur. I. Geographical and altitudinal distribution Fagus sylvatica is one of the most widespread and important deciduous broadleaved trees in Europe; its distribution is given by Preston & Hill (1997) as European Temperate. Undoubtedly native in Britain, though not in Scotland or Ireland, it has been much planted and is frequently naturalized. Beech has been used in landscaping from at least the eighteenth century, a notable example being its employment by the Earls of Chichester in Stanmer Park (including Rocky Clump), Brighton. Its status within the British Isles receives further consideration in X; the present distribution is shown in Fig. 1, while Fig. 2 shows the areas in which it is believed to be native, in a line from The Wash to south Wales and south to Dorset (Tansley 1939; Rackham 1980), including Sussex (Hall 1980) and north-west Essex (Jermyn 1974). Its status in Radnorshire is doubtful, but it is widely planted on freely drained sites in woodlands and as specimen trees in hedgerows (Woods 1993). In Britain, it occurs from sea level to 650 m south of Garrigill, Cumbria (Halliday 1997). Besides its outlying area of apparent survival as a native species in the Wyre Forest on the Shropshire/Worcestershire border (Rackham 1997), Fagus sylvatica is commonly found as individual trees or rows of trees in parks, old gardens, plantations, shelter belts and hedges in Shropshire where it is very widely planted for ornamental and economic use. Beech hedges are widespread, particularly in areas such as Exmoor, with the largest near Meikleour, Perthshire being 530 m long and 24–36 m high. It grows well even at quite high altitudes, which is to be expected in view of its performance as a montane tree in central Europe. Varieties such as the copper beech (F. sylvatica ‘Purpurea’) and cut-leaved beech (‘Heterophylla’) are frequently planted. The former hybridizes freely with the beech (Sinker et al. 1985). Green et al. (2000) describe its occurrence in 669 1-km squares of the approximately 1500 present in the Bristol region, where it is a widespread tree of woods and plantations on light soils, less often found in hedges. The local native population on well-drained limestone slopes is obscured by frequent plantings. In mainland Europe (Fig. 3), its distribution covers southern, central and western Europe, reaching southern Scandinavia. It avoids the areas of continental climate in Europe, reaching its eastern distribution limit in eastern Poland although it grows particularly well in the southern and © 2012 The Authors. Journal of Ecology © 2012 British Ecological Society, Journal of Ecology, 100, 1557–1608 Fagus sylvatica 1559 Fig. 1. Present distribution of Fagus sylvatica in the British Isles. Each dot represents at least one record in a 10-km square of the National Grid. Recorded: (●) 1970 onwards; (○) before 1970. Mapped by Colin Harrower, using Dr A. Morton’s DMAP software, Biological Records Centre, Centre for Ecology & Hydrology, Wallingford, mainly from data collected by members of the Botanical Society of the British Isles. hilly part of that country as well as the western and northwestern regions. It is absent from the Great Hungarian Plain and from the lower Danube and Po valleys where the climate is more continental (Pidek et al. 2010). Its wide distribution in southern Sweden is shown in Lid (1985), as is its presence in the coastal strip southeast of Oslo, its isolated occurrence in the region of Bergen and its absence from Finland. Beechwoods form a girdle, broken only by a gap in the eastern maritime Alps, in the prealpine massifs (and lower mountains adjoining) of the European Alps, stretching from Grenoble in the west to Vienna in the east. The distribution of F. sylvatica here is complementary to that of Larix decidua whose range extends along the high region of the Alps. Ozenda (1983) favours a climatic explanation for the total absence of beech from the intra-alpine area (see II.A), while pointing out that the difference in altitudinal range of the two species may to some extent have a historical origin. Larix decidua established in the intra-alpine area very early and maintained itself to some degree during the glaciations, whereas all beechwood disappeared in the glaciated area and subsequent recolonization has been slow. In Spain, Fagus sylvatica is found in the north in Pyrenees and Cantabrian range, and in some isolated locations further south (Belmonte et al. 2008). During favourable climatic periods, beech has often occupied the northern plains, while colonizing the high hills and mountains of southern Europe. It now occurs up to 1604 m in the mountains of France (Vitasse et al. 2009) and to between 1100 and 1900 m in Apennines of southern Italy (Piovesan et al. 2005), and in Spain, it forms dense forests between 500 and 2000 m (Tutin et al. 1993). Fagus sylvatica grows up to a tree line of 1950 m on Mount Etna, Sicily, its southernmost community in Europe (D.J.L. Harding, pers. comm.). Fagus sylvatica ssp. orientalis occurs in south-eastern Europe, notably in the Crimean Peninsula and on the western margin of the Caspian Sea, and also in Asia along the southern margins of the Black and Caspian Seas. Fagus sylvatica ssp. moesiaca occurs in former Yugoslavia, Albania, Bulgaria and Greece and sporadically in south-eastern Romania, Hungary and former Czechoslovakia (Fukarek 1954; Mišić 1957; Staňescu 1979). II. Habitat (A) CLIMATIC AND TOPOGRAPHICAL LIMITATIONS The natural limits of F. sylvatica in Britain are fairly certain but the underlying reasons are not easily explained (Rodwell 1991). It is most dominant in the warmer and drier south-east, © 2012 The Authors. Journal of Ecology © 2012 British Ecological Society, Journal of Ecology, 100, 1557–1608 1560 J. R. Packham et al. Fig. 2. Presumed distribution of native Fagus sylvatica in Britain. Horizontally hatched, areas of survival; ●, outlying localities; vertically hatched, extinct since Middle Ages; dotted areas, prehistoric records only. Redrawn from Rackham (1997). limited by summer drought in parts of East Anglia (Watt 1923, 1925), and late frosts, low summer temperatures and higher rainfall in the north and west (Watt 1923, 1925, 1931a,b). However, beech grows and regenerates very well further north, and it is possible that beech did not reach its northern limit before humans intervened (Rodwell 1991). Fagus sylvatica requires moist summers and mild winters and is thus absent from the more continental areas in eastern Europe. Ozenda (1983) points out that the innermost limit of Fagus sylvatica penetration from the prealpine to the intra-alpine areas of the European Alps tends to correspond with values of 45° of Gams’ angle of continentality, a measure designed specifically for application to mountains of medium altitude in the Alps. For a given point, continentality is expressed as P/A, where P is the main annual rainfall in mm and A is the altitude in metres of the place concerned. The angle is constructed by taking the value for altitude as the vertical axis. The Prealps, with an angle < 40° have an oceanic climate; angles greater than this imply an increasingly continental climate liable to periods of drought and temperature extremes, especially severe spring frosts. It seems that one of the main physiological requirements for the satisfactory development of beech is adequate relative humidity (Rol 1962). This ties in with an annual rainfall of 600–1000 mm, which Tessier du Cros et al. (1981), Rameau, Mansion & Dumé (1989) and Belmonte et al. (2008) suggested as the minimum for this species. However, Leuschner et al. (2006) record a case where mature beech was growing in a European location with an annual rainfall of only 520 mm. The importance of humidity is underlined by Lendzion & Leuschner (2008) who found that reducing relative humidity in growth chambers by 40% led to a 60% reduction in biomass growth of beech seedlings. Reducing relative humidity by 15% in open-topped chambers in the field led to a biomass growth reduction of 30%. This was attributable to reduced leaf growth (a reduction in area of 79% and 23%, respectively, in growth chambers and open-topped chambers). It is likely that this determines the natural limit to beech distribution in East Anglia (Rackham 1980). Temperature is also an important factor in its distribution. A mean annual temperature of 4.5–6.0 °C is necessary (Hoffmann 1991; Pezzi, Ferrari & Corazza 2008) with a warmest month mean of 13–20 °C (Pavari 1931; Pezzi, Ferrari & Corazza 2008) and a coldest month mean temperature of 2.3 °C (Pezzi, Ferrari & Corazza 2008). Lausi & Pignatti (1973) suggested that this corresponds to a growing season of 110–150 days with a daily maximum of 10 °C or more. © 2012 The Authors. Journal of Ecology © 2012 British Ecological Society, Journal of Ecology, 100, 1557–1608 Fagus sylvatica 1561 Fig. 3. The distribution of Fagus sylvatica in Europe. Main distribution, hatched; isolated occurrences (●); dark broken line in the area of the Black Sea, westernmost limit of Fagus sylvatica ssp. orientalis. Modified from Hultén & Fries (1986) with permission of Koeltz Scientific Books, Königstein, Germany. Tree-ring widths of F. sylvatica in France have been seen to be negatively correlated to minimum March and maximum August temperatures and positively correlated to May and July precipitation, which can lead to narrow rings in dry years (Bouriaud et al. 2004; Lebourgeois et al. 1995). Precipitation of the previous June–August and temperature of the previous July–November may also have an effect on ring width across Europe (Čufar et al. 2008; Grundmann, Bonn & Roloff 2008). (B) SUBSTRATUM Fagus sylvatica appears to favour well-drained soils (Stace 2010) and does not tolerate even relatively short-term flooding (Tessier du Cros et al. 1981). Mitchell (1996) emphasized its inability to grow on wet clay soils where common oak Quercus robur and hornbeam Carpinus betulus flourish. Otherwise beech grows on a wide variety of soils over Europe with a pH range from 3.5 to 8.5 (Rameau, Mansion & Dumé 1989; Grime, Hodgson & Hunt 2007) but not on the most acidic soils. It often forms pure woods, which are often the result of plantation planting, on chalk and soft limestone (as its presence on the South Downs indicates) and sometimes acid sandstone, gravels and some of the less heavy clays (Rackham 1980). It is likely that extensive planting of beech on thin chalk soils has led to a common misconception that this is its natural preference (O. Rackham, pers. comm.). It grows under a wide range of conditions in the Shropshire region, where the soils vary from damp to dry, and are often shallow, sandy or stony, sometimes on limestone. Here, Sinker et al. (1985) describe its habitats as phosphorus- and nitrogen-poor to rich, base-poor to rich, acid to calcareous soils in sun to shade. It is widely planted and regenerates from seed in a wide range of soil conditions from dry, shallow and infertile to damp and rich in Montgomeryshire, where it is found in most places, including the hills but absent from the mountains (Trueman, Morton & Wainwright 1995). In Poland, most soils in the Carpathian beechwoods are chiefly sandstones and shales but with at least small deposits of calcium carbonate. They tend to be shallow, loamy or sandy-loamy, fairly rich in mineral nutrients and very stony. Pawłowski, Medwecka-Kornaś & Kornaś (1966) show two profiles from the Cracow Jura with limestone in the substratum, the B layer of the second with a pH of 7.86. A third profile from the Gorce Mountains is of a mountain brown soil with traces of gleying in the C layer; pH here was A1 5.3, B 6.0, C 6.4. The lowland Pomeranian beechwoods, on the other hand, grow mainly on morainic deposits, most often on sandy loams which are sometimes marly (containing considerable amounts of calcium carbonate). Abundant gravel and water-rounded boulders occur locally. The large quantity of beech litter, mainly of leaves, supplied each year leads to the formation of a soil rich in humus; in Poland, this constantly keeps podzolization in check or never more than weak (Pawłowski, Medwecka-Kornaś & Kornaś 1966). Hagen-Thorn et al. (2004) state that the slow litter decomposition compared to other deciduous species may induce a slight decrease of pH due to the production of © 2012 The Authors. Journal of Ecology © 2012 British Ecological Society, Journal of Ecology, 100, 1557–1608 1562 J. R. Packham et al. organic acids and the delayed return of base cations to the soil. However, Schlich (1910), who reviews the influence of all the major timber trees, states that beech ‘improves’ the soil in the highest degree, because it has a dense crown and yields a heavy crop of leaves. These decay slowly due their unpalatability to earthworms, so beech woods, if undisturbed, show a thicker layer of humus than woods of any other species. In Normandy, Trap et al. (2011a,b) looked at soil changes beneath a chronosequence of beech stands from 15 to 130 years old. They found a shift from mull to moder humus forms along the chronosequence, which was associated with a decrease in decomposition rates, and litter turnover time changed from 20 months in the youngest stands to 31 months in the oldest. Soil pH changed from 3.56–4.47 in the youngest stands to 3.83–3.97 in the oldest. Microbial biomass did not change with age but the microbial biomass:N ratio decreased along the chronosequence in the litter layer. Beech forest maturation was accompanied by an increase in fungal biomass in the humified layers beneath the litter and an increase in heterotrophic bacteria functional diversity in the litter and humified layers. Beech forests are known to buffer soil water chemistry against acid precipitation compared to Picea abies stands (Oulehle & Hruška 2005). Kooijiman, van Mourik & Schilder (2009) studied microbial N and potential net N-mineralization in three sandy and three loamy beech forest soils from Luxembourg, investigating 22 micromorphological soil properties with principal component analysis. Microbial biomass N generally increased with higher soil pH and from sandy to loamy soil, while net N-mineralization showed the opposite trend, being highest in acid sandy soils. Godefroid & Koedam (2010) found soil compaction under Fagus sylvatica trees to be greatest at the edge of the tree canopy, corresponding to maximum movement of the root plate when the tree flexes in the wind and thus compresses the soil. III. Communities In the British communities recognized by Rodwell (1991), the three woodland types dominated by Fagus sylvatica are centred in the warmer and drier south-east of Britain. These are loosely based on the Fagetum calcicolum (W12), Fagetum rubosum (W14) and Fagetum ericetosum (W15) of Tansley (1939). On free-draining, base-rich soils characteristic of the scarp slopes of the North and South Downs, Chilterns and western end of the Cotswolds, F. sylvatica forms largely mono-dominant semi-natural and planted stands of Fagus sylvatica–Mercurialis perennis woodland (W12). The Mercurialis perennis subcommunity is also found beyond the native range of beech in north Humberside and west Yorkshire. The field layer of the Fagus–Mercurialis woodland is characteristic of base-rich soils and similar to Fraxinus– Acer–Mercurialis woodland (W8), particularly in the Mercurialis perennis subcommunity. Other trees may invade gaps, including Fraxinus excelsior, Quercus robur, Acer pseudoplatanus and, on drier sites, Sorbus aria and Taxus baccata. These last two may be relicts of an earlier successional stage but on the steepest, rockiest slopes, where beech is generally <12 m tall, both may survive in the canopy and T. baccata may form a dense under-canopy. With increasing aridity and exposure to wind and sun, there is a transition to Taxus baccata woodland (W13). As soils become deeper, moister and more base-poor, there is a transition to Fagus sylvatica–Rubus fruticosus woodland (W14). These stands contain the tallest and most majestic beech trees (commonly > 30 m tall), forming even-topped, closed stands that are characteristic of the dip slopes of the Chilterns and less commonly the North and South Downs and the New Forest. Pollarding has been common in this community type, leading to characteristic stands in the New Forest and Burnham Beeches, Buckinghamshire. Quercus robur, Betula spp. and Prunus avium are the more characteristic trees occasionally squeezing into the canopy, with a second tier of shade-tolerant trees below, particularly Ilex aquifolium and a dense ground cover of Rubus fruticosus. On the most acidic and infertile soils on which beech dominates (moving from mull to mor humus), the community changes to Fagus sylvatica–Deschampsia flexuosa woodland (W15) as typified by woodlands of the Weald, New Forest and parts of the Chiltern Plateau. Here, beech does not grow as well (< 20 m and frequently crooked), and a number of other trees grow, especially Quercus robur and Betula spp., which can become dominant enough for the community to merge to Quercus–Betula–Deschampsia woodland (W16). Decreased dominance of beech is especially found in the Deschampsia flexuosa and even more so in the wetter Vaccinium myrtillus subcommunities. As in the Fagus–Rubus woodland, Ilex aquifolium is frequent below the canopy along with Pteridium aquifolium, D. flexuosa and abundant bryophytes. It has been suggested that the three main types of beech forest are related in seral sequence, Fagus–Rubus leading to Fagus–Mercurialis to Fagus–Deschampsia although this is undoubtedly an oversimplification (Rodwell 1991) since Fagus–Deschampsia and Quercus–Betula–Deschampsia communities, and indeed Fagus–Deschampsia and Fagus–Rubus communities, may cyclically alternate. This intergrading is reflected in the woodland classification of Peterken (1981) where stand-type 8A consists of acid sessile oak–beechwoods, 8B is of acid pedunculate oak–beechwoods and 8C (which has three subtypes) covers calcareous pedunculate oak–ash– beechwoods. Stand-type 8D consists of acid pedunculate oak– ash–beechwoods, while 8E (sessile oak-ash-beechwoods) has three subtypes. Fagus sylvatica also occurs as an infrequent member of a number of other British woodlands, and indeed, the degree of its dominance helps to define the community. On the baserich soils of the lowland Fraxinus excelsior–Acer campestre– Mercurialis perennis woodlands (W8), it is very infrequent as scattered saplings but occurs even beyond its natural limit, as in the Teucrium scorodonia subcommunity of the Midlands. It is similarly present in the Fraxinus excelsior– Sorbus aucuparia–Mercurialis perennis woodland (W9), a © 2012 The Authors. Journal of Ecology © 2012 British Ecological Society, Journal of Ecology, 100, 1557–1608 Fagus sylvatica 1563 community of the wetter north-west, which also includes some of the planted beechwoods around Aberdeen (Watt 1931a). It is sometimes a more frequent component of Quercus robur–Pteridium aquilinum–Rubus fruticosus woodlands (W10) of the lowlands and may be a sparse member of the canopy, particularly in the Hedera helix subcommunity. As such, increasing proportions of beech and decreasing Q. robur lead to a gradation to Fagus–Rubus woodland (W14). Further north and west, W10 woodland is replaced by Quercus petraea–Betula pubescens–Oxalis acetosella (W11) and Quercus petraea–Betula pubescens–Dicranum majus (W17) woodlands in which climatic and edaphic factors result in beech being a very infrequent constituent. On the acidic soils of more marginal land, beech can be locally common (often due to planting) in woodlands of Quercus spp.–Betula spp.–Deschampsia flexuosa (W16), such as in the New Forest and parts of the Chilterns. As beech becomes more common, especially on the drier, more acidic soils, it leads to a gradation to Fagus–Deschampsia woodland (W15). A number of British scrub communities also contain F. sylvatica. Beech saplings are found in Crataegus monogyna–Hedera helix scrub (W21), particularly when good masting years ‘have coincided with agricultural neglect near to beech woodlands’ (Rodwell 1991) as was noted by Watt (1924, 1934a,b). On deeper, moister soils, it may also be aided by protection from herbivores by Juniperus communis, alongside Taxus baccata (Thomas & Polwart 2003; Thomas, El-Barghathi & Polwart 2007). On less calcareous soil, beech is also infrequent in Rubus fruticosus–Holcus lanatus underscrub (W24). In both communities, if beech establishes well enough to be frequent, the community succeeds towards Fagus–Rubus woodland (W14). Beech is also infrequent in Pteridium aquilinum–Rubus fruticosus underscrub (W25) and is never dominant enough to lead to beech woodland. In France, Renaux, Boeuf & Royer (2010) proposed classifying beech woodland into three associations. Deschampsio cespitosae–Fagetum sylvaticae, which also corresponds to Poa chaixii–Fagetum sylvaticae and Carpino betuli–Fagion sylvaticae, is common on the silt deposits of north-eastern France. Sorbo ariae–Quercetum petraeae is associated with the dry calcareous hills of Burgundy and adjacent areas. Carici brizoidis–Fraxinetum excelsioris, corresponding to Fraxino excelsioris–Quercion roboris, is characterized by pedunculate oak stands on hydromorphic silts. Fagus sylvatica intermixes with oak–hornbeam forests (Querceto–Carpinetum) at the eastern limits of its distribution in Poland (Pawłowski, Medwecka-Kornaś & Kornaś 1966). Here, two neutrophilous beech associations of the Order Fagetalia, Alliance (c) Fagion (communities on a fertile substratum that is fairly moist and whose herb layer is well developed for at least part of the year) differ in geographical character and the fact that mountain plants are present in the first, but not in the second (Pawłowski, Medwecka-Kornaś & Kornaś 1966). Carpathian beechwood (Fagetum carparticum) at one time occupied almost all the lower montane zones (600–1200 m) of the Carpathian Mountains, and extensive remnants are still present. Fagus sylvatica is dominant but Abies alba is quite abundant and frequently overtops the general canopy, occasionally exceeding 40 m. Picea abies becomes more common than Abies alba above 1000 m, at which altitude F. sylvatica loses its column-like shape and becomes squat and twisted. Acer pseudoplatanus and Ulmus glabra also occur but the shrub layer is almost entirely absent. Much of the ground is occupied by plant litter; mosses are scanty and bare soil almost absent; 30–60% of the forest floor is covered by the herb layer, which is best developed in the spring. A number of Carpathian subendemics are characteristic of the association. Cardamine glanduligera is the most widespread of these, while others include Symphytum cordatum (only in the eastern and central Carpathians) and Polystichum braunii. Cardamine bulbifera, Galium odoratum, Polystichum aculeatum and Veronica montana have a high constancy. The presence of Cardamine enneaphyllos and C. trifolia, both rare in Poland, is considered very significant; Allium ursinum is dominant in some particularly moist sites. The second of these associations is Pomeranian beechwood (Fagetum boreoatlanticum) which occurs in the western part of Polish Pomerania on young unleached morainic deposits and experiences a relatively Atlantic climate and is similar to the British Fagus–Mercurialis woodland (W12) described above, although poorer stands also contain Pinus sylvestris. Abies alba and Picea abies are generally absent. Lonicera xylosteum is the most frequent shrub. Melica uniflora, Festuca altissima and Hordelymus europaeus (all found much more rarely in the Carpathians) are regionally characteristic. Galium odoratum, Mercurialis perennis and Milium effusum, all characteristic of the Order and Alliance, occur here. Variations in exposure and soil moisture result in distinct facies within the association. On south-facing slopes, there is a poorer flora with Melica uniflora as a dominant, while north-facing slopes have a richer flora with Cardamine bulbifera; on the sea coast, there is a facies abounding in orchids. ‘Acidophilous beechwoods’, with a herb layer poor in species and similar to that of acidophilous Quercus–Pinus forests, should be placed in the Order Vaccinio-Piceetalia. Some occur on poorer, drier soils, but in Poland many such communities may have been created artificially by humans through the devastation of natural, rich Fagus communities (Pawłowski, Medwecka-Kornaś & Kornaś 1966). The Czech Republic was famous for its allegedly primeval or virgin forests (urwald) which offer evidence of the changing status of Fagus sylvatica in eastern Europe. That of Boubinsky Prales, southern Bohemia, covers 666 ha of which only the core of 47 ha, which was made into a reserve in 1858 in order to preserve a sample of untouched forest, is truly virgin. Peterken (1981) reported it as a magnificent stand of Abies alba (up to 58 m tall), Picea abies and F. sylvatica, with a good representation of younger age classes and much standing and lying dead wood. Since it became a reserve, the standing volume of timber has remained constant, but F. sylvatica has increased at the expense of Abies and Picea. A similar tendency is evident in the primeval forest of Badin, a steeply sloping reserve with an area of 30.7 ha near Zvolen, © 2012 The Authors. Journal of Ecology © 2012 British Ecological Society, Journal of Ecology, 100, 1557–1608 1564 J. R. Packham et al. Slovakia, which was subjected to catastrophic windthrow in 1947 (Packham & Helliwell 1993). This led to great changes in the proportions of the trees present. In 1957, Abies alba accounted for 65% and Fagus sylvatica 32% by volume of the trees present; by 1987, this had changed to 11% for Abies and 77% for F. sylvatica. This reserve has a diverse ground flora, including Cardamine enneaphyllos, Galium odoratum, Mercurialis perennis, Oxalis acetosella, Prenanthes purpurea and Senecio nemorensis. Two other so-called primeval forests near Zvolen are at Oblik (89.6 ha) and Kyjov (53.4 ha). The steeply sloping site at Oblik bears woodland strongly dominated by Fagus sylvatica, with some Acer pseudoplatanus, Acer platanoides, Fraxinus excelsior and Ulmus glabra at an altitude of 750–932 m. The Kyjov site entirely lacks conifers. In some communities, the presence or absence of conifers is due to historical events. For example, in the virgin Picea/Abies/Fagus forest relict ‘Hollbachspreng’ near Zweisel, Germany, Preuhsler (1997) points out that the loss of Abies alba over the last 100– 150 years was due to browsing by ‘game’; now, however, browsing is no longer a problem, and young firs are appearing in the understorey and are expected to proliferate into canopy gaps. Beechwood communities in the European Alps show great variation (Ozenda 1983). Many of the northern beechwoods have compositions corresponding to the standard Fagion medioeuropaeum. The southern communities include the submediterranean beechwoods of Upper Provence, beechwoods with Lavandula angustifolia ssp. angustifolia in southern Piedmont, Fagus–Abies woods with Trochiscanthes nodiflora, beechwoods with Ostyra carpinifolia and beechwoods with Illyrian (Greek) affinities. In Italy, the beech forests with Ilex aquifolium and Taxus baccata are distributed in the Apennines, mainly in the centre–south, with isolated fragments in Sicily, usually above 900 m of altitude (Scarnati et al. 2009). In the Slavonian Mountains of Croatia, the following associations of beech have been identified: acidophilic beech forests (Luzulo–Fagetum), submountainous beech forests (Festuco drymeiae–Fagetum luzuletosum and Caricetosum pilosae) and mountainous beech forests (Cardamino savensi–Fagetum) (Škvorc et al. 2011). IV. Response to biotic factors Fagus sylvatica is a competitive species, unless limited by drought or frost, and is one of the few deciduous trees of Britain that is effective in eliminating plants growing beneath it (Rodwell 1991). The established strategy of Fagus sylvatica is said by Grime, Hodgson & Hunt (2007) to be that of a stress-tolerant competitor, presumably because of its tolerance of poor soil conditions. In England, it normally competes with other broadleaved trees, but in many parts of continental Europe, its main competitors are conifers whose evergreen strategy contrasts markedly with that of the beech (see V.B and VI.E). Following extensive planting through Britain, oak (Quercus spp.) and beech have come to dominate similar communities (see above). The conditions under which either will dominate have long been discussed, and it is difficult to give a definitive account. Beech mast generally drops close to the parent (Watt 1923, 1925) while acorns spread further, making oak more likely to reach and successfully invade gaps, especially on suboptimal soils where the seed production of beech is more erratic. However, abundant beech saplings were found by Watt (1923) to have colonized gaps immediately after a good mast year followed by appropriate weather conditions. Newbold & Goldsmith (1981) conclude that oak and beech seedlings are adapted to different niches, but that both may succeed in the same woodlands because the ground surfaces are often very heterogeneous. Oak seedlings, with their long tap roots and extensive initial shoots, compete more efficiently with the ground vegetation both above- and belowground. The more shade-tolerant seedlings of beech, on the other hand, are better able to establish beneath the canopy of established trees; its seedlings need to do so before the development of tall-growing competitors. Beech is also favoured under high grazing and browsing pressure. Beech is usually less severely browsed, and more tolerant of browsing, than other broadleaved tree species, including sycamore and conifers (Ammer 1996; Van Hees, Kuiters & Slim 1996; Kuiters & Slim 2002). Certainly, beech is less browsed by deer (Capreolus capreolus and Cervus elaphus) than oak or silver birch (Van Hees, Kuiters & Slim 1996) and usually ranks low on the browsing preference scale for deer (Eiberle & Bucher 1989; Van Hees, Kuiters & Slim 1996). However, its biomass and height are reduced by the effect of browsing: 6-year-old saplings which had been browsed were commonly 30% shorter than unbrowsed ones (Van Hees, Kuiters & Slim 1996). Leaf biomass and area are more reduced than branch biomass. Under suboptimal edaphic conditions for beech, oak will dominate stands but oak grows poorly under beech, and so if beech invades first, even on suboptimal soils and outside its natural range, it can outcompete oak (Pigott 1983). Beech roots are most competitive on extremes of soil, on dry rendzinas and on impoverished acidic soils of Fagus–Deschampsia woodland. In a southern German beech and oak (Quercus petraea) woodland, it has been found that oak and beech stands have roughly the same amount of fine roots, but in mixed stands the fine roots of beech were four to five times more abundant than those of oak even though both trees had similar stem densities and leaf areas (Leuschner et al. 2001). This was taken as an indication that beech is outcompeting oak belowground. In this mixed woodland, F. sylvatica may again face competition as seedlings. Provendier & Balandier (2008) show that competition from grasses (primarily Agrostis capillaris, Holcus lanatus and H. mollis) on 2-year-old planted seedlings produced significantly less growth in height and diameter after 2 years. A similar conclusion was reached by Coll et al. (2003) who also found that increasing light availability improved beech growth primarily because competing vegetation changed from grasses to dicotyledonous plants which were less competitive. Simon et al. (2011) also noted © 2012 The Authors. Journal of Ecology © 2012 British Ecological Society, Journal of Ecology, 100, 1557–1608 Fagus sylvatica 1565 that sycamore (Acer pseudoplatanus) is a better competitor for inorganic and organic nitrogen than F. sylvatica. As noted above, Fagus sylvatica now competes very strongly with Abies alba and Picea abies on the lower hills of Slovakia. Indeed, in this area, the conifers now need special consideration when grown in selection forests with Fagus, in which the balance between the various species is maintained by felling, if the traditional balance between the three species is to be maintained. Recently germinated F. sylvatica seedlings growing under the canopy of Picea abies initially face more competition for below-ground resources than for light (Ammer, Stimm & Mosandl (2008). Growth in subsequent years, however, is increasingly determined by light levels. This competition for light by P. abies results in intraspecific competition within the beech. The ranking of seedlings by height showed that small differences in size at the end of the first growing season resulted in continuously increasing differences during the following years. Mortality data showed that the chance of a seedling surviving the intraspecific competition was determined strongly by its dominance ranking within the first 5 years after establishment. V. Response to environment (A) GREGARIOUSNESS Though in the northern and lowland parts of its range, F. sylvatica often occurs in pure stands, often due to planting in the UK, elsewhere it frequently grows mixed with other broadleaved species or coniferous species such as European silver fir (Abies alba) and Norway spruce (Picea abies). On the most base-rich soils in the UK, F. sylvatica is most commonly associated with Fraxinus excelsior, and on other soils Quercus robur (Rodwell 1991). As soils become acidic and wetter, F. sylvatica becomes a rare component of most communities. Other species that often appear with beech are Acer pseudoplatanus, Ulmus glabra, Sorbus aria, Ilex aquifolium. and, in the Shropshire region, Aesculus hippocastanum as a planted tree (Sinker et al. 1985). (B) PERFORMANCE IN VARIOUS HABITATS The performance of Fagus sylvatica is markedly influenced by habitat conditions. In eastern Europe, for example, it tends to grow more vigorously on the hills where summer temperatures and water stress are lower; on ascending further, the trees become progressively smaller towards the Kampfzone (struggle zone) of the tree line. This situation is well illustrated by Seifriz (1931) for the dense Fagus forest on the north side of the Yaila Plateau, Crimea. At 500 m, average tree height is 23 m and average trunk diameter 50 cm, increasing to 34 m and 47 cm at 720 m. Stature then decreases to 22 m and 28 cm at 1020 m, 18 m and 26 cm at 1200 m, and 12 m and 15 cm at 1300 m. At a slightly greater altitude, trees of this Crimean beech assume a typical Krummholz character and soon die out altogether. Seedlings of F. sylvatica below a Picea abies canopy in southern Germany were found to increase in height at an average of 12.6 and 10.9 cm year 1 over 7 years under 15% and 6.1% full PAR, respectively (Ammer, Stimm & Mosandl 2008). In similar German beechwoods, Pretzsch & Dieler (2011) found that between 1972 and 1980, beech trees with a mean diameter (d.b.h.) of 143 ± 44 mm (SD, n = 786) in 1972 grew in diameter 3.6 ± 1.8 mm year 1, and between 1999 and 2007 the same stand of trees, which were 223 ± 74 mm d.b.h. at the beginning of the period (n = 1374), grew by 2.1 ± 2.0 mm. This compares to similarsized Picea abies that grew by 4.8 ± 2.0 (n = 2466) and 3.5 ± 2.6 mm (n = 877), respectively, over the same periods. In beech forests in N.E. Spain, Barbeta et al. (2011) investigated stands in a 2380 ha continuous ‘forest’ and in ‘fragments’ up to 52 ha in size. They found that the forest and fragments had a similar stand structure, but in the fragments the trees had greater crown damage (11.6% in fragments, 2.9% in forest) and a higher proportion of dead trees (7.2% in fragments, 4.7% in forest), and lower seedling density (774 ha 1 in fragments, 25 917 ha 1 in forest). However, juvenile survival was higher in the fragments (per cent of new seedlings surviving from the smallest into the next size class (< 5 cm), 0.13% in fragments, in 0.01% forest). They suggest that the net effect is a similar recruitment of saplings in both fragments and continuous forest and that habitat fragmentation may not be as detrimental to beech as would appear from the low seedling numbers. Carbon storage in beech forest ecosystems in N.W. Spain (including trees, litter layer and mineral soil) was found by Merino et al. (2007) to range from 220 to 770 t ha 1 (mean 380). Tree biomass (above- and below-ground), which averaged 293 t C ha 1, constituted 50–97% of the ecosystem carbon pool. (C) EFFECT OF FROST, DROUGHT, ETC Cold in winter In Britain, winter cold seldom has an adverse influence on Fagus sylvatica whose buds have become dormant. The continental climate of eastern Europe is much more extreme, and in Poland, winter temperatures sometimes fall to below 40 °C. During the exceptionally severe winter of 1928/9, many trees were killed, including those of Abies alba and Carpinus betulus as well as Fagus sylvatica; Medwecka-Kornas (1966) illustrates the destruction by frost of Carpathian beechwood at this time. F. sylvatica is less tolerant of extreme winter cold than some other Fagus species, being listed by Peters (1997) as surviving a minimum temperature extreme of 30 °C, whereas F. grandifolia can survive 42 °C. Late and early frosts In Britain, the weather differs considerably from year to year, and the onset of spring may be much delayed, as in 1996. This seldom harms Fagus sylvatica, provided bud dormancy has not been broken; it is the very erratic late frosts, commonly into © 2012 The Authors. Journal of Ecology © 2012 British Ecological Society, Journal of Ecology, 100, 1557–1608 1566 J. R. Packham et al. late May, which cause damage that is most easily observed in beech hedges, seedlings and young saplings. Terminal buds develop very rapidly with the onset of warmer weather, producing long shoots whose leaves are at first limp and very vulnerable. If frosted, these soon blacken and die, to be replaced later by smaller shoots from previously dormant buds. More importantly, fruiting of Fagus sylvatica in Britain is not uncommonly greatly diminished, or even prevented, by late frosts which destroy the male flowers in particular (Matthews 1955). Such frosts appear to be at least one of the reasons why masting on the relatively exposed site at Fish Hill, Worcestershire, has frequently been inferior to that at Nettlebed, Oxfordshire, during the English Beech Masting Survey (1980 to date, see Packham & Hilton 2002 and Fig. 4). To protect the sprouting leaves, F. sylvatica has developed a high level of dormancy and needs either a long winter chilling period or a long period with temperatures > 5 °C to initiate budburst (Murray, Cannell & Smith 1989). In central Poland, frosts usually cease by mid-April, but in the mountains they frequently continue to the end of May and even into June, causing damage to both cultivated and forest trees. In May 1952, catastrophically low temperatures caused the complete destruction by frost of the young leaves of F. sylvatica in many parts of the Carpathians and highlands (Medwecka-Kornas 1966). Early autumnal frosts, perhaps via their effect in shortening the growing season, are likely to prevent the production of ripe seed in F. sylvatica flowering at high altitudes or high latitudes. Exposure to wind Fagus sylvatica, unlike oak, can grow successfully on the shallow soils of the South Downs but great numbers had their root plates pulled out of the ground when the great gale of 16 October 1987 struck southern England after a period of heavy rain. The root form and liability to wind blow of beech is often along the lines outlined by Helliwell (1989): see also Packham et al. (1992). Though many beeches on chalk soils blew down in 1987, the stability of this species was less on clay and worst of all on sand (Cutler 1991). Many fallen beeches survive with some roots intact and show extensive new growth from the horizontal trunk. Fig. 4. Positions of the main beech sampling sites used in the English Fagus sylvatica Masting Survey 1980–2007. Performance for each group of trees is expressed on a fivepoint scale, using the mean number of full nuts collected in a 7-min sample, for the years 1981–2007. 1, < 10 nuts collected; 2, 10–50; 3, 51–100; 4, 101–150; 5, > 150. Results for 1980 are based on the ease of collection table given by Hilton & Packham (1986). From Packham et al. (2008), courtesy of the Arboricultural Journal. © 2012 The Authors. Journal of Ecology © 2012 British Ecological Society, Journal of Ecology, 100, 1557–1608 Fagus sylvatica 1567 Fagus sylvatica, like Norway spruce Picea abies with which it is often associated in Sweden, is equally susceptible to uprooting by gales when in leaf, and the storm gap theory of forest dynamics developed by Sernander (1936) largely as a result of his investigations of Picea abies forests following the great storms of 1931 and 1932 applies also to beech. Trees of different ages and on different substrates vary in their ability to resist the wind, and it is those that are most susceptible that are uprooted, creating gaps which facilitate regeneration. Many young spruce and beech grow for many years as dwarf trees. It is the creation of storm gaps that eventually provides the light required for them to grow comparatively rapidly into adults. This theory is reviewed by Packham & Hytteborn (2012) in the light of subsequent investigations and the work of Watt (1925, 1947) who investigated forests of common beech in southern England, developing his theory of pattern and process in the plant community as a result. In northern Europe (Denmark, southern Norway, southern Sweden), Fagus sylvatica in leaf is very vulnerable to gales, and old unmanaged beech forests that have been left to grow naturally contain trees of many different ages. Very many of the trees involved developed from shade-tolerant dwarf trees that began to grow rapidly when the mature trees that formerly overshadowed them were destroyed by gales that created gaps in the forest. Trotsiuk, Hobi & Commarmot (2012) investigated the natural disturbance dynamics of the Uholka Fagus sylvatica forest of the Ukrainian Carpathian Mountains, which form the largest area of virgin beech forest in Europe. They took increment cores, of which the oldest was 451 years old, and measured the d.b.h. and height of all the 164 trees with a d.b.h. of 6 cm or more in four circular plots, each of which had an area of 0.1 ha. Age estimation by other methods suggested that beech could reach an age of up to 550 years in Uholka. All four plots covered an age span of at least 300 years and were uneven-aged with continuous tree establishment. Major storm damage occurs only rarely here. Indeed, during the period 1870–1999, the dynamics of the forest were driven by periodic small disturbances that cause damage to upper canopies of mature trees and so allow sufficient light to promote rapid growth of long-suppressed small beech on the forest floor. Investigations of storm damage and long-term mortality in the unmanaged semi-natural, temperate deciduous forest of Draved, southern Denmark, by Wolf et al. (2004) following the severe storm of 1999 are particularly interesting as they contrast the mortality patterns of Fagus sylvatica with other species characteristic of the boreal forests of Scandinavia. Storms killed many large trees, whilst a large number of the smaller individuals were killed by competition; standing dead individuals had narrower growth rings than the live survivors. Mortality patterns of Fagus and Betula differed. The former died less frequently than would be expected from its abundance, while the reverse was true of birch. Dead trees of Fagus, Betula pubescens and Tilia cordata, were mainly wind-thrown, whereas half of the dead of Alnus glutinosa and Fraxinus excelsior were hulks (standing dead trees). Drought Fagus sylvatica frequently has a shallow root system that makes it susceptible to drought (Peterken & Mountford 1996), but on dry soils its roots will penetrate to a depth of several metres to encounter water. Mitchell (1996) describes how, on the light acid sands soils of the New Forest, the roots fan out above, but do not enter, the clay lenses or beds. On the chalk of the South Downs, sinker roots of beech penetrate its fissures, giving access to more persistent supplies of water. It was the most drought sensitive of the five species investigated by Köcher et al. (2009) – Fraxinus excelsior, Carpinus betulus, Tilia cordata and Acer pseudoplatanus – and during drought, large trees may lose large branches. Beech is fairly responsive to drought in terms of reducing water loss through stomatal control but xylem water potential can still fall sharply (Köcher et al. 2009), primarily due to a poor ability to take up water under drought conditions (Scharnweber et al. 2011). The intensive root system of Fagus sylvatica, which exploits a relatively small volume of soil very intensively, appears not to be able to extend its laterals sufficiently quickly towards damper soil when stressed even though beech roots are not restricted in soil exploration by nearby conspecifics (Lang et al. 2010). Indeed, fine root growth is maximal during optimum soil conditions (Mainiero, Kazda & Schmid 2010). Beech also has a high turnover of fine roots, with a mean longevity of 77 days compared to 273 days in Picea abies (Mainiero, Kazda & Schmid 2010), and root mass may decline significantly during a drought (Meier & Leuschner 2008a). Indeed, Meier & Leuschner (2008b) found that fine root biomass decreased by almost a third from stands with 4950 mm year 1 of precipitation to those with < 550 mm year 1. At the same time, leaf biomass remained constant, resulting in a significantly lower fine root/leaf biomass ratio in drier sites, making the problem of drought worse. However, water reserves inside the tree (stored in branches, phloem, etc.) although low, could provide 1–50% of daily water needs under drought conditions, giving it some resistance to drought (Betsch et al. 2011). Due to shallow rooting, hydraulic lifting of water from deeper roots to shallow, found in over 50 species, appears rare in beech, but it may benefit from hydraulic lifting by nearby oak (Zapater et al. 2011). Drought tolerance may to some degree be under genetic control since trees from drought-prone areas have proved more drought tolerance in common garden experiments (e.g. Rose et al. 2009). Certainly, Fotelli et al. (2009), working with beech in Greece, found that leaf water potential, effective quantum yield and d18O showed no significant variation between wet and dry years, and the trees did not appear to have suffered from drought stress. Foliar carbon isotopic composition (d13C), however, did appear to be more sensitive to climatic differences between years and was higher during the dry year of 2003. Regression analysis showed that it was linked to current soil water content and vapour pressure deficit of the preceding month. Nevertheless, beech trees from Greece were more tolerant of drought than those further north. © 2012 The Authors. Journal of Ecology © 2012 British Ecological Society, Journal of Ecology, 100, 1557–1608 1568 J. R. Packham et al. F. sylvatica consequently suffers much higher losses than most other species in years with very marked summer drought such as 1959 and 1976. Indeed, on the Ebworth Estate, near Stroud, UK, the cutting of dying trees continued for more than two years after the very damaging drought of 1976 when some trees died within 10 days, having been subject to mid-day temperatures of c. 33–37 °C with a drying northerly wind, while other trees with embolized xylem succumbed in the following spring (J. Workman, pers. comm.). Some trees survived because it rained in early September, whereas in the drought of 1959, adequate rain was delayed until November. Stress imposed by the 1976 drought undoubtedly led to poorer long-term performance by many of the survivors. Evidence of past periods of drought is provided by dendrochronological studies (e.g. van der Werf, Sass-Klaassen & Mohren 2007), while Power (1994) used twig growth studies of beech to provide historical information about tree growth at a number of sites in southern England from 1960 onwards. The substantial reduction in growth found for all trees during 1976 and 1977 was caused by the severe drought in southern England in 1976. Healthy trees quickly regained their pre1976 growth rates after 1977, but a number of unhealthy trees continued to show greatly reduced rates of growth many years later. Stribley (1996a,b) also monitored the health of beech and employed quantitative twig analysis. Waterlogging F. sylvatica is badly affected by waterlogging. The presence of a high water-table confines the root system to even shallower depths than usual, with the result that in dry summers such trees may be very strongly droughted. Fire The thin bark of F. sylvatica provides little protection from fires which have always been an important influence on its survival. Ohlson et al. (2011) examined a set of 75 macroscopic charcoal records that showed that invasion of northern Europe by Picea abies in the late Holocene diversified the fire regime, previously considered to be predominantly controlled by the macroclimate. As Norway spruce invaded boreal European forests, it significantly reduced wildfire activity. This had an important influence on Fagus sylvatica, which invaded Sweden at the same time as Norway spruce with which it was often associated on a subcontinental scale. While adult beeches are fire-intolerant and become more dominant without fire, beech can, however, regenerate quickly after fire. Following a beech forest fire in the central Apennines, Italy, beech seedlings and sprouts from burnt stumps were overwhelmingly dominant and are expected to become a monospecific beech forest (van Gils, Odoi & Andrisano 2010). Working in the Siggaboda Reserve in southern Småland, Sweden, Niklasson, Lindbladh & Bjorkman (2002) established a long-term record of Quercus decline, logging and fires in this southern Swedish Fagus–Picea forest. Using tree- ring data, pollen and charcoal analysis, they reconstructed forest development and disturbance by fire and logging over the last thousand years. The fire of 1652 was particularly severe, affecting most of the reserve, including the core area. Quercus was common in the whole area until the late 18th century. Quercus disappeared completely at the end of the 18th century, when almost all the Pinus went also. No oaks have regenerated in the core area since the last fire in 1748, although a few single Pinus sylvestris established in the neighbouring managed forest around 1920. Norway spruce on the other hand has greatly increased since 1748 while Fagus became particularly abundant in the late 19th century and is still prominent today. Response to atmospheric pollution Acid rain and general forest decline (Waldsterben) in Europe were considerable problems faced by F. sylvatica in the 1980s, drastically affecting its physiology and morphology (e.g. Lonsdale 1986). Fortunately, changes in pollution production have largely resolved these problems. Response of beech health to atmospheric pollution (NOx, NH3 and SO2) is somewhat complex and also dependent on more local factors, such as the soil, or climatic events particularly drought. In practice, atmospheric pollution levels seem to affect the health of Fagus sylvatica mainly on acidic soils that are not adequately buffered against additional acid deposition (Ling, Power & Ashmore 1993). The importance of soil acidification was underlined by Jonard et al. (2010) who found that applications of dolomitic limestone (3 t ha 1) to the acidic brown soils of the Belgian Ardennes produced increased girth growth of beech over the next 13 years and increased foliar Ca and Mg (which was linked to reduced defoliation). In comparison, application of N, P and K (with or without lime) had no effect on tree growth and health. Compared to control plots, limed stands showed better crown condition during the intense drought of 2003. Oulehle & Hruška (2005) discuss the effects on soil water acidification and aluminium chemistry at Picea abies and Fagus sylvatica sites in the Ore Mountains, Czech Republic, subjected to long-term acidification due to intensive burning of locally mined lignite. There were major differences between these two types of forest; the effect on the Norway spruce being so profound that more than 50% of its area consisted of dead and dying trees, which had to be clear-cut. Spruce canopies captured far more acidic aerosols, particulates and cloud water than those of beech. As a result, the soil waters in the spruce stand were more acidic and had concentrations of aluminium, sulphate and nitrate that were significantly higher than those beneath the beech stand, which were richer in both calcium and potassium. Stribley & Ashmore (2002) reported changes in twig growth pattern of young woodland beech (F. sylvatica) in relation to climate and ozone over a 10-year period. Power (1994) considered it possible that continued poor twig growth in trees at two of his sites might have been due to ozone pollution. © 2012 The Authors. Journal of Ecology © 2012 British Ecological Society, Journal of Ecology, 100, 1557–1608 Fagus sylvatica 1569 Dittmar, Zech & Elling (2003), whose dendroecological studies of the changing growth potential of beech involved 36 stands in continental Europe, found that at high altitude sites (in marked contrast to those at lower levels), growth rates as evidenced by tree-ring widths became slightly smaller after 1950. This forest decline was ascribed to increased tropospheric ozone concentrations. Warren et al. (2007) found that when they compared trees grown in normal atmospheres with those fumigated in the open with twice the ambient ozone levels, rates of net photosynthesis in the latter were reduced by about 25%. In southern Switzerland, Cascio et al. (2010) found a similar (19–28%) reduction in net photosynthesis in normal air compared to air from which 50% of the ozone was filtered. Studies using whole trees have found that ozone pollution reduces growth. Matyssek et al. (2010), in an 8year-long experiment doubling ozone levels in stands 60 years old and up to 28 m high, found lowered photosynthesis and a 44% reduction in whole-stem growth (compared to no growth reduction in Picea abies), but increased soil respiration. However, rhizosphere and mycorrhizal associations appear largely unaffected by high ozone levels (Pritsch et al. 2009). Tyler & Olsson (2006) studied the importance of atmospheric deposition, charge and atomic mass of minor and rare elements in developing, ageing and wilted leaves of F. sylvatica in a beech stand at 130 m a.s.l. at Hassleholm, northcentral Scania, south Sweden, which was isolated from even minor roads or arable ground. The podzolic soil here had a well-defined layer of mor humus with no traces of mineral particles down to a depth of 7–10 cm. Contents per leaf of K, Rb, Cs, Cu and P were highest in young leaves, decreasing throughout the growing season and usually in the subsequent winter. In contrast, there was a continuous, mostly even increase in the amounts of Be, Ba, Hg, Al, Tl, Pb, Bi, V, W, As, Sb and Se. Amounts of rare earth elements and some transition metals such as Co, Ti and the actinides Th and U were more stable in the growing season after an initial increase in early summer: winter increase of these elements in dead attached leaves must be due to deposition of material transported from far away. Amounts of several mainly nonessential elements including Ni, Sc, Zr, Cr, Ag and Cd were not much lower in young or maturing leaves than in winter dead leaves. Some of these appeared to originate from internal translocation in the tree. VI. Structure and physiology (A) MORPHOLOGY Individuals of Fagus sylvatica are large trees. These include one in a wood near Hallyburton House, Coupar Angus, Scotland (46 m tall/4.9 m girth), another at Beaufort Castle, Hexham (44/5.5 m), and a tree at Ebworth near Stroud in the Cotswolds measuring 42/3.5 m, which grew beside another of 28/4.9 m whose low branches spread 30 m (Mitchell 1996). F. sylvatica almost invariably has a single stem, but Peters (1997) provides an illustration of a natural multi-stemmed tree with a large number of branching stems growing in Krkonose, Czech Republic. Some large trees with several stems, such as one on the Hafod estate, Cardiganshire, 21 m high but with an 8.27 m girth at 75 cm and a spread of 37 m, almost certainly result from the practice of ‘bunch-planting’ of several saplings together (Chater 2010). The beech bole is quite characteristic, often being virtually cylindrical and covered by a relatively thin smooth silver-grey bark. The trunks of beech trees grown in open situations bear massive branches quite low on the trunk, and these may become so long and heavy that some actually touch the ground, sometimes layering (forming roots) and sending up vertical stems. At Tregrehan, Cornwall, the main trunk of a layered tree measures 18/ 4.3 m. Such trees often have a splendid appearance, but they are not good at providing sound structural timber. In dense forest stands, the trunks are often without side branches until a height of 20 m or more and their green crowns high above the ground, while translucent in spring, cast a shade so dense that no other tree can develop beneath it. Mitchell (1996) describes beech’s unusual annual pattern of growth, one in which the large terminal bud erupts into a shoot 45–60 cm long in early May and hangs, drooping and grey with silky hairs until July, when the terminal bud adds an additional 30–45 cm to its length. The shoot straightens by September, if not before, in a pattern of growth that depends on summer rain to be successful. The palisade cells of shade leaves of Fagus sylvatica are shorter, and the number of palisade layers is fewer than in sun leaves. The mean thickness of the palisade tissue decreases from 77.2 lm at the top of crowns to 41.1 lm at the base and even lower (a mean of 39.2 lm) for leaves of understorey trees (Aussenac & Ducrey 1977). There is also a relative increase of the spongy mesophyll in shade leaves, whose intercellular spaces are much more conspicuous. Differences in the intensity and seasonal duration of the photosynthetic activity of sun and shade leaves borne on the same tree in the Solling Mountains, Germany, are reported by Schulze (1970) – see Fig. 5. Rates of CO2 uptake in these two types of leaf were about the same in relation to leaf dry weight, whereas on a leaf-area basis assimilation, shade leaves was approximately half that of sun leaves. A study of the anatomy of beech leaves through the canopy has shown that the mean leaf thickness decreases from 197.5 lm at the top of the crown to 99.7 lm at the base (Aussenac & Ducrey 1977). The stomatal density decreases from 238 mm ² to 149 mm ², and specific leaf mass also decreases from 102.3 to 34.9 g m ². Stomatal density has been measured as 165.8 ± 3.4 mm 2 (SE, n = 60) (Čaňová, Ďurkovič & Hladká 2008) and 238 mm 2 (Aussenac & Ducrey 1977) but can be as high as 242 mm ² in some cultivars (‘Aurea Pendula’) with an average length of 23.84 ± 0.18 lm (Čaňová, Ďurkovič & Hladká 2008). In general, petioles tend to be longer in sun leaves or leaves of fruiting twigs than in shade leaves (Denk 2003). The evidence for a reduction in stomatal density with increases in CO2 concentration is ambiguous for F. sylvatica (Beerling et al. 1996; Beerling & Kelly 1997) but suggests that there has been little change so far post-industrial revolution. © 2012 The Authors. Journal of Ecology © 2012 British Ecological Society, Journal of Ecology, 100, 1557–1608 1570 J. R. Packham et al. Fig. 5. A comparison of photosynthetic activities of sun and shade leaves of common beech (Fagus sylvatica) and Norway spruce (Picea abies) growing on the Solling Plateau, Germany. (a) Maximum rate of photosynthesis; (b) total CO2 uptake in the vegetative period; (c) leaf biomass (proportion formed in the current year, stippled) and (d) annual net photosynthetic gain. Columns for sun leaves white; shade leaves hatched. 0, 1 and 2 correspond, respectively, to spruce leaves developed in the current year and one and 2 years previously. Drawn from the data of Schulze, Fuchs & Fuchs (1977b); from Packham et al. (1992) Functional Ecology of Woodlands and Forests, Chapman and Hall, fig. 2.15; reproduced with kind permission from Springer Science + Business Media B.V. Individual beech tree architecture varies greatly between open and closed canopies. In shaded environments under closed canopies, a decrease in leaf number per shoot, an increase in leaf size and regular leaf dispersion all tend to diminish the within-shoot shading. In accordance with Horn’s theory (Horn 1971), beech branches in shaded environments adopt a monolayer strategy (large horizontal regularly distributed leaves spread in a single layer to maximize light capture). In contrast, beech adopts a multilayer strategy in sunny conditions; this enables an optimization of the light levels over the whole canopy thanks to an increase of light penetration, and the leaves held more erectly. Leaf arrangement in understorey conditions reflects the shade-tolerant behaviour of beech (Planchais & Sinoquet 1998). Tree form When grown in close canopy, Fagus sylvatica has a virtually cylindrical bole, the vascular cambium nearer the apex having produced, in a shorter time, almost as much wood as the cambium at the base of the trunk. Gruber (1997), working with F. sylvatica seedlings of known age, found that the number of tree rings present in the middle of the hypocotyl was identical to that in shoots formed in the leaf axils of the original primary shoot. False wood rings, which were not due to the production of lammas shoots, could be distinguished by the blurred nature of their boundaries. Gruber provides a field method to determine the age of young seedlings accurately and illustrates the five different branching patterns found in 1year-old seedlings. He also shows a 1-year-old plant of type 3 (which has developed the first true leaves) with opposite primary axillary buds, a 1-year-old plant of type 4 or 5 (which has produced branches from buds grown the same year) and regular opposite primary axillary shoots of type 3. Tree form can be extensively modified by environment. Late spring frosts can change a tree’s shape by injuring or destroying terminal buds and consequently increasing the incidence of forking (Ningre & Colin 2007). The creation of openings in a dense canopy can lead to rapid and extensive branch reorientation upwards within 4 years of canopy opening (Collet et al. 2011). Compared to oak, branches in beech are slow to die but once dead are shed very rapidly; this matches the greater shade tolerance of beech compared to oak (Kint et al. 2010). Multi-stemmed individuals on the Wrekin, Shropshire, appear to have developed as result of coppicing. Holeksa et al. (2009) measured some notably large trees in the West Carpathians. The mean of the 10 biggest trees gave a height of 43.3 m, d.b.h. 72.8 cm, height of the crown base 27.1 m, crown width 12.4 m and a crown volume of 1038 m3. Stands had 104 stems ha 1 with a growing stock of 201.2 m3 ha 1, though Trotsiuk, Hobi & Commarmot (2012) working in virgin stands in the same area found stand size to reach 270–590 stems ha 1 and 525–1237 m3 ha 1. Peter, Otto & Hubert (2010) and a number of previous studies gave regressions based on modelling that predict leaf area with the size of the tree: a tree with a cross-sectional area at breast © 2012 The Authors. Journal of Ecology © 2012 British Ecological Society, Journal of Ecology, 100, 1557–1608 Fagus sylvatica 1571 height of 6000 cm2 had an estimated 800 m2 of leaf area. Allometric equations allowing prediction of productivity/biomass of beech stands from stand parameters can be found in Genet et al. (2011). The cork cambium normally remains active throughout the life of the tree, growing laterally to accommodate the increasing girth of the trunk, hence the long-term scarring caused by graffiti. Little corky tissue is produced, and the thin grey bark remains smooth or sometimes slightly roughened, being shed in dust-like fragments. The bark of a beech 30 cm in diameter is usually only 6 mm thick (Thomas 2000). The amount of phloem produced each year by the mature tree is small, and its production precedes that of the fresh xylem. Older phloem contributes to the inner bark, but this becomes dominated by expansion tissue resulting from dilation of the external regions of the medullary rays. Structure of wood The white or pale brown timber is diffuse porous with essentially uniform xylem vessels fairly evenly distributed, although vessels formed early in the year are slightly larger and more numerous. Growth rings are conspicuous; in microscopic T.S., they can be seen, at intervals, to dip slightly towards the centre of the stem (Jane 1970). Moderately conspicuous rays are of two groups of size: the larger rays may be several mm high and as many as 25 cells wide. It is these which are responsible for the brown flecking which is the characteristic figure seen on the radial surfaces of quarter-sawn logs. Beech xylem has predominantly simple perforations, although some of the smaller vessels may have scalariform perforations. The average wood density of beech ranges around 720 kg m 3 at a moisture content of 12%. Gryc et al. (2008a), Gryc, Vavrčík & Gomola (2008b) give details of wood anatomy and properties of F. sylvatica. The wood dries easily though tending to distort, is hard, tough, of high compressive strength but somewhat brittle and shortgrained, works easily, takes a good finish and turns especially well. Beech sometimes develops strongly red heartwood which, although it does not weaken the wood, decreases its value (see Sorz & Hietz 2008 for references). Hristovski & Melovski (2010) provide data on dendrochemistry across annual rings. Zipse et al. (1998) showed that wood from wind-exposed trees growing in the borders of Scotland was stronger and allowed larger strains before failure than wood from beech growing in a sheltered part of Germany. Measurements of longitudinal and radial strength showed that timber on the leeward sides of the trees was stiffer and stronger than that on the windward sides, the effect being greater in trees that were leaning than those that were erect. Root form The root system is both shallow and intensive; its short laterals with numerous short and extremely fine terminals enable the tree to utilize a relatively small volume of soil very effectively. Inability swiftly to extend the roots to fresh soil makes F. sylvatica vulnerable to drought. Bakker et al. 2008 looking at a chronosequence in northern France using soil pits and trench wall observations found a lesser proportion of fine roots (< 2 mm diameter) in the top 30 cm of soil in older stands (146 years old; 65% of fine roots) than younger stands (9 years old; 74% of fine roots). Biomass of fine and small roots (2– 20 mm diameter) in beech stands along this chronosequence was higher in young stands (9 and 26 years old; 9.8 and 13.3 t ha 1, respectively) than older stands (82 and 146 years old; 7.4 and 3.6 t ha 1, respectively). Claus & George (2005), using soil auger samples, found a similar although smaller fine root biomass in Europe: 5.3–6.4 t ha 1 in young stands 15 and 30 years old and 3.3 t ha 1 in older stands (62 and 111 years old). (B) MYCORRHIZA Fagus sylvatica forms mainly ectomycorrhizal roots (Harley & Harley 1987). Russula spp. (Basidiomycota, Russulales) are common in beechwoods but Laccaria amethystina (Huds.) Cooke (Basidiomycota, Agaricales) has also been recorded (Roy et al. 2008). Kjøller (2006) and Goicoechea, Closa & de Miguel (2009) list ectomycorrhizal mycelial species in a Danish and Spanish beech forest, respectively; of these, Tomentella Pat. spp. (Basidiomycota, Thelephorales) and Cenococcum geophilum Fr. (Ascomycota, Dothideomycetes) were the commonest, respectively. There have been many investigations of the physiology of mycorrhizal associations. Harley’s group at Oxford used excised Fagus roots (most likely colonized by Lactarius subdulcis (Pers.) Gray) as a model system Harley (1936). Harley & McCready (1950, 1952) reported uptake of phosphate and the distribution of this material between the host root and the fungus, while Harley & Loughman (1963) demonstrated its immediate incorporation into nucleotides and sugars. As Bartlett & Lewis (1971) point out, the rate at which sheathing (ectotrophic) and vesicular–arbuscular (endotrophic) mycorrhizas absorb orthophosphate from dilute solution or soils is much greater than that of uninfected roots. This, however, is only one fraction of soil phosphorus as a whole. Complex inorganic and organic phosphates are also important sources, and these authors found that the mycorrhizal roots of beech growing in the humus layer possessed active surface phosphatases that catalysed the hydrolysis of an important range of soil phosphates. The roles of ectotrophic mycorrhizas in the soil phosphate cycle and their ability to compete and survive in marginal habitats are discussed in detail. Clowes (1981) investigated the organization of the meristem and rates of cell proliferation in its regions, comparing those bearing intact fungal sheaths with those in which the apices had grown through the sheaths and with uncolonized roots. Intact fungal sheaths have to deal with a very high production of cells by the host meristem. This may involve the use of some of the host cell constituents; Harley (1978) estimated that the carbohydrate passing to the fungus amounted to 10% of that going to timber production; this is if anything an understatement. Warren Wilson & Harley (1983) studied the development of mycorrhiza on Fagus sylvatica seedlings in their first © 2012 The Authors. Journal of Ecology © 2012 British Ecological Society, Journal of Ecology, 100, 1557–1608 1572 J. R. Packham et al. growing season in pot experiments and under natural woodland conditions. All root tips, colonized or uncolonized, passed through a sequence in which the elongation rate progressively declined, root diameter decreased and the root cap became smaller. Mycorrhizal colonization did not occur until the root tip had passed through this sequence and elongation had nearly or completely ceased. Formation of mycorrhiza caused a resumption of slow elongation with a swelling in width in the new region. Certain features of the host root varied quantitatively with the species of mycorrhizal fungus concerned. Structurally intact mitochondria isolated from beech mycorrhiza by Coleman & Harley (1976) actively respired with Krebs cycle intermediates; in each case, the oxidation was tightly coupled to phosphorylation. The cyanide-sensitive respiratory pathway was the favoured route of oxidation under phosphorylating conditions, but respiration in some of the mitochondrial population was cyanide-insensitive and did not result in phosphorylation. Strips of fungal sheath were dissected from Fagus sylvatica mycorrhizas and incubated in phosphate solutions under a range of conditions by Chilvers & Harley (1980). Accumulation of phosphate was closely paralleled by increases in the number and size of polyphosphate-containing metachromatic granules which formed a major pool of storage phosphate. Quantitative experiments along the same lines described by Harley & McCready (1981) showed that a large fraction of the phosphate in the fungus accumulated as polyphosphate. Strullu et al. (1982) showed that granules present in the vacuoles of hyphae of the sheath of Fagus sylvatica mycorrhiza in electron microscope preparations contained phosphorus and calcium. Considerable amounts of calcium were present in the hyphal walls of the fungal sheath. Little calcium or phosphorus was present in the clear regions of the hyphal vacuoles. When Strullu et al. (1983) measured the relative phosphorus and calcium contents of the phosphatic granules of Fagus before and after phosphate absorption from KH2PO4 solution, the phosphorus content greatly increased but their calcium content did not, so the P/Ca ratio fell. These results are discussed in the context of the cation content of the granules and estimates of the amount of phosphate present in granule form. When Collignon, Calvaruso & Turpault (2011) studied the temporal dynamics of exchangeable K, Ca and Mg in acidic bulk soil, outer rhizosphere and inner rhizosphere under Picea abies and Fagus sylvatica, they found that both rhizosphere compartments were richer in these three exchangeable nutrients than the bulk soil. This suggests that tree roots, associated bacteria and mycorrhizal fungi increased nutrient availability through weathering or mineralization processes. In contrast to beech, there was a drastic decrease in the exchangeable cations in the bulk soil beneath spruce between November and February, an effect that could be due to increased aluminium solubility. Martin et al. (1986) studied the assimilation of 15NH4 by Fagus sylvatica ectomycorrhizas. Absorption of ammonium ions was associated with rapid synthesis of free amino acids, particularly glutamine, in the mycorrhizal tissues. Studies involving nuclear resonance spectroscopy suggested that in ammonia-fed beech mycorrhizas, ammonia assimilation occurs mainly via the glutamine synthetase/glutamate synthase pathway, with glutamate dehydrogenase playing little, if any, part in the process. Read & Perez-Moreno (2003) review the complex ways in which mycorrhizal fungi are involved in the mobilization of nitrogen and phosphorus from natural substrates. The biomes of grassland, temperate forest (to which Fagus belongs), boreal forest and heathland, each with their characteristic soil, nitrogen source, mycorrhizas and fungal symbiont activity, are shown arranged along an axis corresponding to increasing latitude or altitude. This axis also corresponds to decreasing soil pH and increasing phosphorus availability and P/N ratio. Temperate forests have brown earth (moder-mull) soils, NH4NO3 mineralization and ectomycorrhizas, with arbuscular mycorrhizas in the understorey. Their ecto-fungi are of reduced saprotrophic capability and their arbuscular mycorrhizas largely non-saprotrophic. (C) PERENNATION, REPRODUCTION, LONGEVITY The three methods by which reiterative sprouts of trees develop their own root systems (Koop 1987) are all employed by Fagus sylvatica: 1 Additional root systems produced by suckers arising from the root of a tree. Root suckers occasionally occur in F. sylvatica: photograph 107 in Tansley (1939) shows a beechwood in winter, including young trees which arose from surface beech roots. These individuals were some metres from the trunks of the parent trees, unlike the large tree of F. sylvatica under the north wall of Ludlow Castle, Shropshire, where root suckers are present within a metre of the trunk base. Root suckers are much more common and important in the North American Fagus grandifolia (Peters 1997), while root collar sprouts are especially common in F. japonica. Papalexandris & Milios (2010) observed that regeneration in N.E. Greece on ‘medium productivity’ sites from sprout origin (from a stump or roots) amounted to 2037 plants ha 1, 18% of the regeneration from seed. 2 Reiterative sprouts can develop from the trunk of a broken, partly uprooted or otherwise damaged or senescent tree and eventually replace the parent tree. This may happen when a stem of F. sylvatica leans on a mound produced by the uprooting of another tree as occurs in the Hasbruch forest reserve, Germany, and in Stuzica, Slovakia (Koop 1987). Adventitious roots may also develop when a trunk of F. sylvatica lies flat on the forest floor, as observed in the Fontainebleau Forest Reserve, France. Koop (1987) also reports the successful reproduction of Fagus sylvatica when the flexible lower branches of uprooted trunks were pressed against the ground in the forest reserves of Fontainebleau, Neuenberg and Hasbruch. Beech can even regenerate from the scorched bases of trees whose main trunks have been destroyed by lava flows as in the case of Fagus sylvatica on Mount Etna, Sicily (D.J.L. Harding, pers. comm.). Vigorous new shoots arose from the base of each old tree which had been engulfed by a © 2012 The Authors. Journal of Ecology © 2012 British Ecological Society, Journal of Ecology, 100, 1557–1608 Fagus sylvatica 1573 lava flow early in the 20th century (see Packham, Hobson & Norris 2012). 3 Several branches may become layered so that many reiterative sprouts with adventitious roots develop simultaneously. Layering downslope occurs when stems are forced to the ground by snow pressure where F. sylvatica grows near the alpine limits of tree growth in the mountains of central Europe (Koop 1987). Fagus sylvatica does not show self-coppicing in which an old tree rots at the base, falls down and is replaced by a ring of shoots growing from its base, as occurs in one of the Japanese beeches (Rackham 2002). See also X. The vast majority of beech trees develop from seed, and there are many sites in Britain where regeneration is satisfactory. Harding (1986) made a detailed study of the regeneration of oak and beech in a 75 9 40 m plot in Saltwells Wood Local Nature Reserve, Dudley, producing size-class distributions of young plants with a diameter < 15 cm at 5 cm above-ground level. Of these, 56% of the young oaks and 61% of the young beech had diameters < 2 cm. The lifespan of Fagus sylvatica is frequently between 150 and 300 years (Rameau, Mansion & Dumé 1989), rarely exceeds 300 (Grime, Hodgson & Hunt 2007) but may reach 550 years (Trotsiuk, Hobi & Commarmot 2012). Certainly, pollarded beech may reach 500 years. (D) CHROMOSOMES The chromosome number of Fagus sylvatica is 2n = 24 (Lid 1985). The 2C DNA value was recorded on Sheffield material as 0.8 pg (Grime, Hodgson & Hunt 2007) by staining with Schiff’s reagent and measurement by microdensitometry. Further determinations of F. sylvatica material from the vicinity of Reims, France, were made by Gallois, Burrus & Brown (1999) using flow cytometry and propidium iodide staining: 2C values of 1.11 pg were obtained for the common beech and for the variety ‘Tortuosa’. Slightly higher values were obtained for the variety ‘Pendula’ (1.13 pg) (which was significantly higher than the value for ‘Tortuosa’) and the variety ‘Purpurea’ (1.12 pg). A karyotype analysis of F. sylvatica (Ohri & Ahuja 1991) showed that all the chromosome pairs can be identified by length, arm ratio and c-banding pattern. The longest chromosome was 3.43 lm long, and the ratio between the longest and shortest was 1.77. Three pairs were described as median point (ratio between long and short arms 1.0), three pairs as median region (ratio 1.2–1.3), three pairs as submedian (ratio 1.8–2.5) and three as subterminal (ratio 3.5–8). One B chromosome was also observed. Thiebaut, Lumaret & Vernet (1982) used starch gel electrophoresis to study bud enzymes of several French populations of F. sylvatica. Polymorphism was examined in 11 southern and two northern populations for two peroxidase loci (Px1 and Px2). Both were monomeric enzymes, the first locus being composed of two alleles Px11.00 and Px11.05 (with silent alleles in certain cases; this allele is particularly com- mon in trees from the driest sites). The second had three alleles Px21.13, Px20.26 (whose alleles are particularly frequent in individuals experiencing cold climates) and Px20.40. All the alleles were found in each of the 13 populations; variations in their frequencies appeared to be related to the climate experienced by the beech stand involved, with the first locus being related to moisture regime and the second to temperature regime. Allelic diversity tends to increase where F. sylvatica experiences less favourable ecological conditions under dry climates at the southern limit, or under a cold climate on mountains; conversely allelic diversity diminishes towards the geographical and ecological centre of the populations investigated. Thiebaut, Lumaret & Vernet (1982) also found that Asiatic species of Fagus could be distinguished from the European and American ones on the basis of peroxidase analysis. (E) PHYSIOLOGICAL DATA Response to shade and ultraviolet light Seedlings of F. sylvatica have a compensation point of only 2% of full sunlight in an open field as Helliwell (2012) mentions in his description of the roles of direct sunlight and diffuse light in woodlands. More diffuse light is produced on the cloudy days so common in the UK, and it is the most important energy source for tree seedling growth in woodland situations. Though very shade tolerant, beech does respond favourably to light levels higher than that commonly found on the woodland floor (Collet, Lanter & Pardos 2001). Seedlings of 10 European tall-shrub species and F. sylvatica were grown by Grubb et al. (1996) at 0.3, 1.6, 11 and 63% daylight for 110 days on chalk grassland soil and on a more nutrient-rich soil developed under Crataegus monogyna in an experiment designed to investigate the interaction of irradiance and soil nutrient supply amongst species commonly found along forest margins and in gaps. There were 10 seedlings per treatment for each species. All 10 Fagus seedlings died on both soil types at 0.3% irradiance. At 1.6% one died on the grassland soil and three on the scrubland soil. At 11 and 63% irradiance, none and one died on the grassland soil and one and none on the scrubland soil. Total dry mass per seedling at 110 days was greatest on the soil with the higher nutrient supply at 63% irradiance (1074 ± 113 mg). At 1.6 and 11% irradiance, the highest values were on the grassland soil (162 ± 18 and 751 ± 76 mg, respectively). The conclusion appears to be that beech seedlings need a relatively high level of irradiance if they are to utilize a greater supply of nutrients. The conclusions regarding the differing behaviour of the 10 tall-shrub species in this experiment give an insight into the nature of the competitive struggle between them during early forest succession. Details of allocation to roots and shoot mass, relative growth rate (RGR), leaf area ratio (LAR) and specific leaf area (SLA) are provided for them and for beech. In relation to chlorophyll content, the apparent assimilation of shade leaves of Fagus sylvatica was only one-third of that © 2012 The Authors. Journal of Ecology © 2012 British Ecological Society, Journal of Ecology, 100, 1557–1608 1574 J. R. Packham et al. of the sun leaves (Aussenac & Ducrey 1977). By the time the shade leaves reached maximal assimilation in August, the photosynthetic activity of the sun leaves had already declined. Senescence of sun leaves began much earlier than in shade leaves (Schulze 1970), probably because of the higher temperatures they experienced and the accelerated photooxidation of photosynthetic pigments at higher light fluxes. Working with 60-year-old trees in the Kranzberg forest near Freising, Germany, Warren et al. (2007) examined internal conductance to CO2 transfer (gi) and photosynthetic production in sun and shade leaves. They found that gi was approximately twice as great in the thick sun leaves as in the thin shade leaves and tentatively concluded that in F. sylvatica liquid-phase conductance, rather than gas-phase conductance, is the dominant component of gi. Rates of net photosynthesis and stomatal conductance were approximately twice as high in sun leaves compared with shade leaves. Compared with trees grown in normal atmospheres, those fumigated in the open with twice the ambient ozone levels had rates of net photosynthesis equal to 75% of the former treatment. Though gi was not affected in this experiment, the authors conclude that it might well be at higher ozone levels. The IBP investigations into the growth of a single tree of F. sylvatica (27 m tall and 100 years old, Schulze 1970) during 1968 and of Picea abies (25.6 m high and 89 years old, Schulze, Fuchs & Fuchs 1977a,b) in 1972 growing within a kilometre of each other on the Solling Plateau, Germany, illustrated their contrasting strategies of production. Both the sun and shade leaves of Fagus had a much higher photosynthetic capacity per unit dry weight than even 1-year-old needles of Picea. Fagus showed positive CO2 uptake on only 176 days in the year, against 260 for Picea. Fagus had a higher annual production of leaves than the evergreen Picea, but the latter had a much greater photosynthesizing biomass because of the long life of its needles, some of which survived for as long as 12 years. Figure 5 contrasts the photosynthetic activities of these two species. Petriţan, von Lüpke & Petriţan (2009) in a field study in Germany, compared saplings of beech, ash Fraxinus excelsior and sycamore Acer pseudoplatanus growing under a shelterwood canopy giving 3–60% of the above canopy sunlight. Under the lower light levels, annual height increment was slightly higher in sycamore and ash than in beech. With increased light, beech was progressively outgrown by the other two species. As fits with its shade tolerance, beech did not show increased height growth above 35% full sunlight. Beech has a range of adaptations to shade compared to other trees. It keeps leaves over a greater depth of canopy (particularly in the middle crown). Biomass is preferentially allocated to radial growth rather than height, especially in low light fluxes where it shows distinct plagiotropic growth in shade as a horizontal light-foraging strategy. Compared to ash and sycamore, beech also has the highest specific leaf area, a greater total leaf area per unit tree height, a slightly greater leaf area index and a greater plasticity to light in total leaf area. Thus, while ash and sycamore regenerate best in canopy gaps, beech is adapted to tolerate and cope with deep shade. However, F. sylvatica is capable of responding to increased light in ways other than height growth. Gardiner et al. (2009) studied 7-year-old European beech regeneration in open patches and thinned (receiving a third of the PAR) Picea abies plantation in southwestern Sweden. The leaf blades of beech in open patches had an average mass per unit area (LMA) 54% greater than that of those in thinned stands but beech in patches had a 78% lower leaf area ratio (LAR). Photosynthetic capacity (A1600, net photosynthesis at a photosynthetic photon flux density of 1600 lmol m 2 s 1) of beech with respect to the canopy gradient was best related to leaf mass and declined substantially with increasing canopy openness. Experimental manipulation to alter UV-B from 17.8 to 226 (ambient 181) lW cm 2 on beech saplings was conducted by Láposi et al. (2009). They found that increased UV-B led to significantly lower chlorophyll and leaf water content and higher specific leaf mass and levels of xanthophyll cycle pigments (violaxanthin, antheraxanthin and zeaxanthin) and flavonoids, which act as protectants in the leaf. Lenk & Buschmann (2006) investigated the accumulation of substances that protected against damaging UV radiation in the epidermis of sun and shade leaves of a free standing beech tree growing at Karlsruhe, Germany. Higher concentrations of substances that absorbed UV light were present in sun than in shade leaves. UV-shielding was more effective on the upper (adaxial) surfaces than on the lower (abaxial) surfaces of both sun and shade leaves. Leaf area index and stand leaf mass Leaf area index (LAI) was investigated in F. sylvatica, together with stand leaf mass (M1) on a landscape scale and across strong environmental gradients by Leuschner et al. (2006). LAI was measured by litter trapping in 23 closed mature stands across gradients of rainfall, soil acidity or fertility. Mean LAI was 7.4 (range, 5.6–9.5), relatively high compared to other broad-leaved species. Bequet et al. (2011) found somewhat lower figures of 3.2–4.2 in a Belgian stand, compared to 2.4– 3.3 in oak (Quercus robur). Leuschner et al. (2006) observed that neither increasing soil acidity (from pH 7 to pH 3) nor decreasing water availability (rainfall gradient from 1030 to 520 mm year 1) had any significant effect on LAI, although Bequet et al. (2011) found in a Belgian stand that precipitation over the previous winter (an indicator of soil water recharge) and solar radiation levels the previous summer had a positive effect on LAI. Stand leaf mass, however, increased slightly with higher soil fertility. LAI and stand leaf mass are mainly under the control of age-related physiological factors, and both measures declined as forest stands became older. The influence of soil chemistry and rainfall is relatively low. However, more detailed studies by Meier & Leuschner (2008c) found precipitation did have an impact on LAI. Along a precipitation gradient in Germany, they found that average leaf size in dry stands (520–550 mm year 1) was about 40% larger, and specific leaf area was higher than in moist stands (910–970 mm year 1). As a consequence, LAI in dry stands was 19–45% higher than moister stands, ranging from c. 8 to < 5 in moist areas. © 2012 The Authors. Journal of Ecology © 2012 British Ecological Society, Journal of Ecology, 100, 1557–1608 Fagus sylvatica 1575 Temperature Height growth is affected by spring temperatures. In France, it was found that mean May temperatures ranging from 12 to 14 °C were optimal with a maximum of 17 to 20 °C. Height growth was also slowed by high July temperatures and drought (Seynave et al. 2008). The prominent climatic signals linked to annual ring width are summer temperature (July– August) and precipitation (June–August) of the previous year (Grundmann, Bonn & Roloff 2008), but see II(A). Water relations Fagus sylvatica is fairly conservative in its use of water and has been measured as having sun-leaf conductance 30% lower than in Quercus petraea (Backes & Leuschner 2000) and 40% lower than in Fraxinus excelsior (Köcher et al. 2009). These last authors measured daily maxima of leaf conductance in F. sylvatica as 150–170 mmol m 2 s 1. Transpiration rates of a beech stand (measured using the heat pulse velocity method) have been measured as oscillating between 0.6 and 1.4 l m ² leaf area day 1, equal to 0.6–1.5 mm day 1 (Ladefoged 1963) with a maximum sap flow of 10 9 10 5 m3 m 2 h 1 (Betsch et al. 2011) in trees of 95–175 cm diameter in N.E. France. Stomatal response to water loss is rapid (completely closed once leaf water potential falls to 2.5 MPa) and sufficiently fast to protect xylem from dysfunction under non-drought conditions (Lemoine, Cochard & Granier 2002). However, under drought conditions, when roots cannot supply sufficient water, the water potential in sun leaves has reached a minimum of 2.6 MPa, in central Germany (as compared to no discernible change in Carpinus betulus and Tilia cordata in similar drought conditions; Köcher et al. 2009) and 4.5 MPa in eastern France (Lemoine, Cochard & Granier 2002). In the short term, Beerling et al. (1996) suggested minimal stomatal closure in response to increased CO2 concentration. However, in the past century, water-use efficiency in F. sylvatica has increased by 44% in high forests of N.E. France, associated with increased atmospheric CO2 levels, via stomatal control and possibly N deposition (Duquesnay et al. 1998). Vulnerability to xylem cavitation is fairly low (equal to that of Pinus sylvestris) and, surprisingly, is higher in populations in northern France compared to the south. Xylem water pressure causing 50% loss of hydraulic conductivity in the trunk develops at 3.77 MPa in the north and 2.4 MPa in the south (Herbette et al. 2010). This was attributed to northern trees being adapted to resist low winter temperatures (and thus air bubble formation in the xylem) and the frequent severe summer droughts, while southern trees survived by resisting internal water deficits. Mineral nutrition Beech is capable of using nitrogen in various forms, including both inorganic and amino acids (Stoelken et al. 2010). It also employs ammonium, but nitrate and organic forms, predomi- nately glutamine, are much more important (Simon et al. 2011). Ammonium uptake by beech roots is usually insignificant (presumably due to intense competition with soil microbes). In N-limited beech forests, there is intense competition between beech and plant microbes for N since beech uptake of N is negatively correlated to soil microbial biomass (Simon et al. 2011). However, intraspecific competition between adults and seedlings of beech appears to be reduced by temporal differences; seedlings have their highest demand for N in spring while adult trees take up most N in the autumn (Simon et al. 2011). Nitrogen uptake rates were investigated by Schulz, Härtling & Stange (2011) and found to be lowest in oak (Quercus petraea) and then in the order: oak < beech < spruce (Picea abies) < pine (Pinus sylvestris) < lime (Tilia cordata) < ash (Fraxinus excelsior). Phosphorus nutrition is discussed extensively under Mycorrhiza (VI.B). The mineral nutrition of beech is more highly affected by flooding than is that of Quercus robur. Ferner, Rennenberg & Kreuzwieser (2012) found that soluble carbohydrate concentrations fell in roots of flooded beech but not in flooded oak. This was associated with higher C levels in leaves due to impeded phloem transport. Hertel (2011) found that the biomass of living fine roots in ‘crown humus pockets’ (collections of organic matter held within the tree canopy) was about seven times higher than in terrestrial soil beneath the tree (39.5 mg g 1 in the pockets compared to 5.8 mg g 1 below – all based on dry masses). The canopy roots had a lower percentage of root tips colonized by ectomycorrhizal fungi than terrestrial roots (87% v. 93%). It is, however, not clear how much these canopy roots add to tree nutrition; their contribution is likely to be fairly minor. (F) BIOCHEMICAL DATA European beech produces large quantities of volatile organic compounds (VOC), including monoterpenes, particularly sabinene, a homoterpene (C14H18), three sesquiterpenes, isoprene and methyl salicylate (Demarcke et al. 2010; Joó et al. 2010). Emissions increase with increased light and temperature. Emissions have been measured in the range of 2–32 lg g 1 h 1 (normalized to 1000 lmol m 2 s 1, 30°C; Dindorf et al. 2006; Demarcke et al. 2010). Emissions during the night were negligible. These monoterpene emissions represent between 0.01 and 0.3% of assimilated carbon (Šimpraga et al. 2011). Interestingly, the VOCs have been seen to change in composition when attacked by aphids from mostly monoterpenes to linalool, a-farnesene, (E)-b-ocimene and honoterpene (Joó et al. 2010). Phenolic compounds have been detected in leaves and bark of F. sylvatica in Greece, particularly isoconiferin and syringin (Petrakis et al. 2011). Concentrations in leaves varied from 69.2 ± 1.0 to 82.1 ± 0.8 mg g 1 dry mass (SD, n = 5) in insect-free and full-sunlit leaves, respectively. They also found that the concentration of phenolics in leaves between trees was weakly inversely related to the abundance of insects found on the trees but not with concentration in the bark. © 2012 The Authors. Journal of Ecology © 2012 British Ecological Society, Journal of Ecology, 100, 1557–1608 1576 J. R. Packham et al. The impact of ozone is via the decrease in quantum yield of electrons reaching the acceptor side, which indicated the inactivation of the end acceptors of electrons, so producing an excess of oxidative pressure (Cascio et al. 2010). VII. Phenology The roots are the first part of the tree to resume growth after winter, though in a mild winter they may never have stopped. Shoot activity follows several weeks later, commencing with breaking of the buds in response to increasing day length. Beech was amongst the fifteen woody perennials whose date of bud burst was studied by Murray, Cannell & Smith (1989). F. sylvatica has a late date of budburst, and its already large thermal time to budburst (days with temperature > 5 °C since 1 January) increases greatly with a decrease in winter chilling (number of days with temperature  5 °C since 1 November) to less than about 150 chill days. In fact, its large chilling requirement seemed to be only just met in the current British climate. In places where its chilling requirement is poorly satisfied at present, climatic warming will not bring about earlier budburst because there will be a large increase in the thermal time to budburst. This turned out to be the case with F. sylvatica at Braemar. Vitasse et al. (2011a) showed via modelling that beech phenology did indeed appear to be comparatively unresponsive to climate change. They showed that oak (Quercus petraea) will increase its canopy season by 3.7 days per decade compared to 2.8 days for beech. In mainland Europe, bud burst has been recorded as occurring between mid-April and mid-May in France (Menzel, Estrella & Fabian 2001; Lebourgeois et al. 2002) and midApril in Slovenia, affected primarily by March and April temperatures (Čufar et al. 2008). In the Slovenian study, leaf unfolding was immediately followed by growth in the cambium at breast height. One week later, the cambium reached its maximum width (around 11 cell layers), and the rate of cell division increased until the end of May/beginning of June. By the end of June, 75% of the tree-ring was formed. Cambial cell divisions stopped from the end of July to midAugust. The average time of cambial activity was 100 days (Čufar et al. 2008). The spring increase in leaf area index in a Belgian stand (from 22 April to 15 May) was found to be followed by a halt in growth of 3 weeks before resuming and reaching a maximum by the end of June to mid-July (Bequet et al. 2011). Leaf yellowing in the same study began at the end of October, positively affected by minimum July temperatures and negatively by September precipitation (Čufar et al. 2008). First leafing date in the French Pyrenees was delayed by an average of 11 days for every 1000-m increase in elevation (data from 2005 and 2006), compared to 34 days in oak (Vitasse et al. 2009), while Dittmar & Elling (2006) found a delay of 2 days for every 100-m increase in southern Germany. Vitasse et al. (2009) found that differences in leafing date between 1979 (a cool year) and 1994/1997 (warm years) was 16 days in beech but 42 and 36 days in Quercus petraea and Fraxinus excelsior, respectively. Though temper- ature is an important factor triggering leaf flushing, it is not the only one (Vitasse et al. 2011b). Menzel, Estrella & Fabian (2001) also concluded that beech is less responsive to changes in winter and spring than most other tree species. Chmura & Rożkowski (2002) observed that bud break can vary across the range of beech by up to 20 days. They also found that this has a genetic base such that a mix of different phenologies exists within a population, but there are also geographical differences with later-breaking forms more common in areas with greater frequency of late spring frosts (such as the north-western part of beech’s range and at higher altitudes). This gives beech population great flexibility (Kraj & Sztorc 2009). Beech shoots have determinate (fixed) growth, the whole of the next year’s shoot being preformed in summer and then expanded within a week or so in spring. The terminal bud of the new shoot then quite quickly takes on its winter appearance. A few additional shoots often develop in summer, this lammas growth being particularly obvious in hedges. The very complete leaf mosaic of Fagus sylvatica develops quite swiftly in spring, rapidly reducing the proportion of light reaching the forest floor and greatly influencing the shrub layer, usually but scantily developed, and the phenology of the herbaceous vegetation. When used for hedging its leaves are retained for much longer than is the case with major trees, indeed on hedge plants the leaves of the previous season are often present as the new leaves expand. The initiation of flower buds begins in May, and by August, male flowers may have the rudiments of anthers (Büsgen, Münch & Thomson 1929). Flowers open simultaneously with the leaves (Belmonte et al. 2008), females before the males. Pawłowski, Medwecka-Kornaś & Kornaś (1966) describe the Polish beechwoods as having a vernal aspect more marked than in any other forest association. A herb layer including Corydalis cava, Cardamine enneaphyllos, C. glanduligera and Galanthus nivalis is luxuriously developed just before the tree canopy opens but rapidly blooms, bears fruit and dies down again before the summer. VIII. Floral and seed characters (A) FLORAL BIOLOGY F. sylvatica is wind-pollinated and appears to be generally self-incompatible; self-pollination produced 92% empty nuts in the Danish trees investigated by Nielsen & de Muckadeli (1954). Isolated trees consequently often produce a high proportion of empty nuts, a striking example being the single tree at Withdean Park, Brighton, sampled for many years by Packham & Hilton (2002) in which many of the nuts are usually empty. In 1990, however, some 79% of the nuts sampled from a very large crop were full, and nearly all were undamaged. In 1990, and also 1995 and 2000, it seems likely that pollen from distant trees blew to the site. Nilsson & Wästljung (1987) also observed a high percentage (84%) of empty nuts for isolated trees (more than 100 m from other beeches). © 2012 The Authors. Journal of Ecology © 2012 British Ecological Society, Journal of Ecology, 100, 1557–1608 Fagus sylvatica 1577 Pollen grains are 36–42 lm in diameter, (sub)spheroidal with vermiculate (rugulate) exine ornamentation (Denk 2003). Pollen transport is generally fairly limited and generally < 500 m. Oddou-Muratorio et al. (2010) examined variance in allelic frequencies and estimates of contemporary gene flow in French stands and found the average distance of pollen dispersal was limited to 38 m. In S.E. Poland, Poska & Pidek (2010) found that the majority of pollen fell within 300 m of a stand with a maximum distance of 1800 m. However, Belmonte et al. (2008) concluded from using atmospheric modelling data from 1983 to 2007, that beech in the Catalonian Mountains of north Spain were primarily pollinated by trees in N.E. France and S.W. Germany, pollen thus covering distances of thousands of kilometres. This conclusion does not seem to be compatible with the pollen trap data quoted here but supporting it is evidence from Poska & Pidek (2010) who found an average of 1100 grains cm 2 year 1 falling into traps (a fifth of that seen in Pinus sylvestris), including c. 500 grains cm 2 year 1 from regional sources outside the stand being sampled. It appears that occasional long-distance transport of pollen is responsible for gene transfer supplementing more common, local dispersal. The average masses of the ‘seeds’ of the 20 woodland trees listed by Salisbury (1942) range from 0.17 mg to 4.05 g, that given for Fagus sylvatica being 225 mg. Packham & Hilton (2002) list air-dry mass of filled beech nuts from 12 sites scattered throughout England for the years 1995, 1997, 1998, 1999 and 2001 and show that these vary very considerably from site to site, tree to tree and year to year. During these years, the lowest mean nut mass per tree at Killerton, Devon, was 136 mg in 1998, while the highest was 509 mg in 1999. The lowest mean nut mass per tree from any site over the same period was Fish Hill, Worcestershire (94 mg in 1999). The lowest value for any tree over the entire 22-year period 1980–2001, also from Fish Hill, was 90 mg. (B) HYBRIDS Fagus as described by Seifriz (1931) in his description of the vegetation of the Crimea (see also V.B) showed intermediates between typical Fagus sylvatica and F. sylvatica ssp. orientalis. One of these, the Crimean beech had leaves intermediate in size between the two taxa, but its fruits were those of typical Fagus sylvatica. On the other hand, the flowers and the production of root shoots were features resembling Fagus sylvatica ssp. orientalis (typical Fagus sylvatica seems not to produce root shoots here). The specific name proposed for these trees by Poplawska (1928), F. taurica, has since been abandoned. Papageorgiou et al. (2008) suggests that there may be some hybridization between the two subspecies in Greece but the evidence is not conclusive. (C) SEED PRODUCTION AND DISPERAL Beech, as is typical of shade-tolerant trees, begins flowering fairly late in life, at approximately 40 years of age in the open to 60–80 years in dense stands (Firbas 1949). Reproduction is primarily sexual. Masting is the periodic synchronous production of very large seed crops. Sufficient seed remains for the initiation of a new crop of seedlings after seed predators have become completely satiated. Beech is notable for the strength of its masting pattern, which appears to be based on an intrinsic biennial production of seed, although in mainland Europe this may tend to cycles of 4–8 years (reviewed by Pidek et al. 2010), sometimes with intervals between mast years of up to 15 years (Fisher 1896; Schlich 1910; Bourne 1942; Matthews 1955). This cycling is modified by external factors, of which frosting, rainfall, nitrogen levels and strong sunlight at appropriate times of the year are the most important (Hilton & Packham 1986, 1997; Packham & Hilton 2002; Schmidt 2006; see also V.C). In mainland Europe, good masting years are also synchronous with years of high pollen production (Pidek et al. 2010), which in turn is linked to higher-thanaverage June and July air temperature and to a positive impact of July drought on seed production in the following year. Packham & Hilton (2002) characterized masting success by the total numbers of full nuts collected in a 7-min period. Regeneration success, which is influenced by insect damage, mould attack and the conditions under which the seeds germinate, is another matter but many trees, particularly in continental Europe commenced their lives in consequence of a very heavy mast. An extensive series of masting records for lower Franconia (southern Germany) has been collated by Maurer (1964). He singles out 1888 as ‘Jahrhundertmast’, the mast of the century, resulting in many German beechwoods of that age; an excellent mast in 1946 did not produce the same afforestation effect as 80% of the nuts were collected for edible oil production. In his classic paper on the ecology of Swedish beechwoods, Lindquist (1931) gives records for four sites spanning 33 years. They show a clear pattern of every two or three years, broken only once. In examining the failure of a regular biennial pattern, he studied weather records and noted the importance of high temperatures in June and July of the year preceding masting when the flower buds are initiated, together with the absence of severe frost in late April and May of the year of masting, when male and female flowers would be killed. Matthews (1955) established a significant regression of masting scale on daily mean difference from average July temperature: the higher the temperature is in July, the better the mast of the following year provided it does not follow a good masting year. Using these and other records, Hilton & Packham (2003) attempted to collate records of masting by F. sylvatica in northern Europe for the last two centuries. Records for the first 28 years of the English Beech Mast Survey, which began with the doctoral studies of Hilton (1988), are given by Packham et al. (2008). The regenerative ability of trees so heavily diseased as to be near death can be remarkably high, as in the case of the beech at Patcham Place, Brighton, described by Packham (2003). The tree concerned had a trunk so diseased that it had been felled for safety reasons, yet virtually every branch from © 2012 The Authors. Journal of Ecology © 2012 British Ecological Society, Journal of Ecology, 100, 1557–1608 1578 J. R. Packham et al. the bottom of the canopy to the crown bore a very heavy mast that contained excellent seeds. Seed production in a mast year can range up to 1500– 4000 seeds m 2 (Harmer 1994). Olesen & Madsen (2008) in Denmark found 307–1168 seeds m 2 of which 10–18% were infected by fungi and another 10–12% were empty. Watt (1923) suggests that whereas the average annual production of seed by ash is 33% of a full crop, beech and oak produce only 16–17% and so show greater variation between poor and mast years. Not surprisingly, such is the drain on resources during a masting year, that annual ring growth is lower than expected in such years (Drobyshev et al. 2010), and the number of leaves per shoot, the length of terminal shoots and the dry mass of terminal shoots are approximately 2-fold lower in masting years (Han, Kabeya & Hoch 2011). Seed dispersal is possible by water and gravity but is primarily by animals such as squirrels and jays, while in Spain the nuthatch (Sitta europaea L.) appears to be the main seed disperser (Perea, San Miguel & Gil 2011). Caches of seeds are sometimes neglected and consequently give rise to seedlings. Richards (1958) studied concealment of beech nuts by coal tits (Parus atar) and stated ‘where beech trees grow at the edge of a pine wood most of the nuts were hidden about the conifers or on the ground under pine needles or bracken’. Oddou-Muratorio et al. (2010) looked at variance in allelic frequencies and estimates of contemporary gene flow in French stands and found that the average distance of seed dispersal of F. sylvatica was normally 10.5 m, although this was backed up by long-distance seed dispersal from outside the study site. Other studies have suggested values of 11–15 m (Hasenkamp et al. 2011). Oddou-Muratorio et al. (2010) also found that the seedlings in a 7.2-ha stand resulted from 12 years of recruitment, with one predominant year of seedling recruitment in 2002 and several years without significant recruitment. Fagus sylvatica has no persistent seedbank, and the seeds germinate in the spring following their dispersal: seedbank type II (Grime, Hodgson & Hunt 2007; Thompson, Bakker & Bekker 1997). Linnard (1987) found that in the autumn of 1984, a mast year, 40% of seed in Wytham Woods disappeared within 1 month of falling, and by March, < 3% of full seed remained. The precise agent of predation was not known but was thought to be small mammals and birds as suggested by Watt (1923). (D) VIABILITY OF SEEDS: GERMINATION Seed germination occurs in spring. Adequate moisture availability is necessary for germination, and young seedlings are readily killed by drought or late frost (Watt 1923). There has been some debate over the desiccation tolerance of beech seeds: some have described them as desiccation-tolerant (orthodox) (Poulsen & Knudsen 1999) while others have described them as less so (intermediate) because of their greater sensitivity to drying and storage conditions than typical orthodox seeds (Gosling 1991; León-Lobos & Ellis 2002; Pukacka & Ratajczak 2007). However, it appears that seeds of beech develop desiccation tolerance some 16 weeks after flowering time by the build up of dehydrin-like proteins (Kalemba, Janowiak & Pukacka 2009). Seed dormancy seems to have two components: embryo dormancy and dormancy imposed by the seed coat (Nicolás, Nicolás & Rodriguez 1996). Dormancy may be broken by chilling (Newbold & Goldsmith 1981). A cold stratification on a wet medium (giving a seed moisture content of approximately 55%) at 1–3 °C for 90 days can break this dormancy (Suszka 1966). The problem of this technique is that seeds start to germinate in such conditions. Therefore, Suszka (1975) recommended the maintenance of seed water content at 28–30% during the stratification period, which broke dormancy while not allowing germination, but, as a consequence, a longer stratification period was often needed. Abscissic acid (ABA) prevents germination and reverses the effect of cold treatments. During cold-induced breaking of dormancy, a gradual increase in RNA and protein synthesis occurs (this protein synthesis can be reduced by application of ABA). Exogenous application of gibberellic acid (GA3) is able to substitute cold treatment and hence to break dormancy. The process of seed dormancy/germination is controlled by the levels of the two hormones (ABA and GA3). The levels of GA3 are very low in dormant seeds and increase during dormancy release (Nicolás, Nicolás & Rodriguez 1996). Watt (1923) found that direct access to liquid water was essential to the germination of F. sylvatica. High relative humidity alone was insufficient, as a film of water over the seed was necessary to keep the level of water uptake above that of water loss until germination had occurred. Watt & Tansley (1932) considered a covering of leaf litter to be essential for beech regeneration in Britain since this helps maintain adequate moisture but also partly protects the seeds from frost and predation by mice, gastropods and wireworms. They added, however, that a depth of litter beneath the seed sufficient to prevent the radicle reaching the mineral soil may inhibit regeneration in the north where litter decomposes slowly. Brown (1953) considered that the tendency of litter to dry out and its higher acidity made it a less favourable rooting medium and that the formation of mor humus might restrict regeneration. He concluded that the best conditions for regeneration of beech are provided by calcareous soils sheltered from the wind, with a rapid breakdown of litter and a good crumb structure under a general but thin litter cover. This is probably the case, but it is clear that beech will regenerate under a considerable range of conditions provided it is not subjected to high initial competition and has adequate water. In an old-growth beech forest, Peltier et al. (1997) found that germination and establishment of both F. sylvatica and Fraxinus excelsior was best in semi-shade. Low recruitment in canopy gaps was also attributed to poor soil conditions, although Watt (1923) observed that the increased density of ungrazed shrub and herbaceous vegetation following gap formation excluded F. sylvatica seedlings unless it was partially suppressed. Commercial seed storage at 7 or 22 °C can be successful for 3–4 years but subsequent germination falls dramatically if stored at 5–6% moisture (< 25% germination) rather © 2012 The Authors. Journal of Ecology © 2012 British Ecological Society, Journal of Ecology, 100, 1557–1608 Fagus sylvatica 1579 (a) (b) (c) (d) (e) 5 cm Fig. 6. Stages in the germination and early development of Fagus sylvatica: (a) Radicle breaking through the nut wall; (b) radicle wellestablished and hypocotyl emerging; (c) hyocotyl fully elongated, developing cotyledons well above the ground; (d) cotyledons, whose undersides at this stage have a white sculpted appearance, almost fully expanded; (e) vigorous young seedling whose first two leaves have been damaged by insects. Drawings were made from seedlings at various times and places rather than progressively from a single batch. All five stages drawn by John R. Packham; (e) was originally published in Packham & Harding (1982) and Thomas & Packham (2007); reproduced courtesy of Cambridge University Press. than 8–9% (< 66% germination) (Procházková & Bezděčková 2008). IX. Herbivory and disease (A) ANIMAL FEEDERS OR PARASITES (E) SEEDLING MORPHOLOGY The germination of F. sylvatica is epigeal (Fig. 6). The two cotyledons found in each seed are used initially as storage organs, and subsequently for photosynthesis. Oliver (1996) reported that in May of that year, five distinct types of Fagus sylvatica seedling were commonly present within the beech woods on Windmill Hill, near Ludgershall, Wiltshire. Those in which the coloration of the upper surface of the cotyledons was bright green, glaucous blue-green or copper beech grew on to produce adult-type leaves of similar colour although the difference between the first two types diminished somewhat. Differences between these three types appear to be of genetic origin. Albino seedlings with cream coloured cotyledons failed to produce shoots, while those in which there were radial striations from the cotyledon stalks outwards, with alternating cream and green lines along veins, produced sickly shoots which soon died. It was conjectured that the last two types developed as a result of exposure to prolonged cold associated with periods of harsh north-easterly winds (similar damage develops in other species from frost damage during periods of rapid growth). The predation of tree seeds and seedlings may be significantly related to density or to distance from the parent tree, although Akashi (1997) found that in a cool-temperate forest in western Japan, herbivory of Fagus crenata seedlings was, in fact, not significantly related to distance from the parent tree. Mammalia The North American grey squirrel (Sciurus carolinensis Gmelin), which has now displaced the native red squirrel (Sciurus vulgaris L.) from most English woodlands, feeds voraciously on beech nuts and is also a cache former. It is a major cause of beech regeneration failure also due to bark removal especially at the pole stage and can seriously damage surviving trees. Studies of the edible dormouse (Glis glis L.) by Morris (1997) and Morris, Temple & Jackson (1997) show that this exotic species will also take a considerable toll of beech nuts as it spreads further. Although beech is less susceptible to browsing than many woody species, in a montane mixed forest with spruce, fir and sycamore in the Bavarian Alps, beech was affected by © 2012 The Authors. Journal of Ecology © 2012 British Ecological Society, Journal of Ecology, 100, 1557–1608 1580 J. R. Packham et al. ungulate browsing, as were all other tree species present. Moreover, beech bark is heavily stripped by red deer Cervus elaphus L. in the Vosges Mountains of France (SaintAndrieux et al. 2009). In N.E. France, dogwood (Cornus sp.) and field rose (Rosa arvensis) appeared to be the most selected species by red and roe deer whereas beech, common mezereon (Daphne mezereum) and wild-service tree (Sorbus torminalis) were always avoided (Boulanger et al. 2009). When beech is browsed, this tends to reduce growth rather than survival of saplings (Harmer 2001; Olesen & Madsen 2008). Saplings taller than 30 cm can survive several years of severe browsing under heavy shade of > 50% reduction in sunlight (Harmer 2001, 1999) leading to some delay in growth (e.g. 3–4 years) before they grow above the browse limit of deer (Roth 1996). Thus, it is normally expected that beech, together with Norway spruce (Picea abies), will increase at the expense of other trees in areas of high deer browsing (Gill 1992). However, very young seedlings can be vulnerable to browsing (Harmer 2001; Madsen 1995). An important factor influencing the effect of deer on beech regeneration is the number of young seedlings that are available to be eaten. Olesen & Madsen (2008) observed that in Danish woods, roe deer (Capreolus capreolus L.) at a density of 24 deer km 2 did not affect regeneration on natural, undisturbed seedbeds (5 seedlings m 2 after 2 months, 1 sapling m 2 after 8 years). However, on cultivated seedbeds (rotavated or stripped to mineral soil), a mean of 191 seedlings m 2 was found on fenced plots, dropping to 22 on unfenced plots, producing 22 and 2 saplings m 2, respectively. In this case, roe deer only seemed to be a problem when there were patches with high densities of seedlings in a larger area devoid of seedlings. Harmer (1994) suggested that for natural regeneration to be successful, there needed to be 2–5 seedlings m 2, which, assuming a 1% success rate would require 200–600 seed m 2, which was considered satisfactory in Belgium by Weissen (1978). Beech nuts are rich in oil (46%) and are an important food for pigs in many regions, a phenomenon notably seen in the New Forest in 2002; the term pannage is applied to the fruits of Fagus as well as Quercus. Beech nuts, acorns and chestnuts account for 75% of the diet of wild boar during autumn in the French Pyrenees and Catalonia (Valet et al. 1994). Rooting by wild boar, which consumes the fine roots, causes damage to beech seedlings and young saplings, in late winter and spring (Groot Bruinderink & Hazebroek 1996). Apodemus sylvaticus L. and Myodes glareolus Schreber (=Clethrionomys glareolus L.) consume many beech nuts (Jensen 1985; Abt & Bock 1998). Le Louarn & Schmitt (1972) found a strong relationship between Apodemus densities and the abundance of beech nuts, the density being much higher during masting years due to a longer autumnal breeding season. Moreover, they have shown that seed predation occurs mainly during seed fall and is low during winter until seed germination. Olesen & Madsen (2008), working in Danish beech stands, found that in early spring 1996, the density of the yellow-necked field mouse Apodemus flavicollis (Melchior) was 12.2 individuals ha 1 and bank vole Myodes glareolus 17.6 individuals ha 1. They estimated that a mean of 15 beechnuts m 2 was consumed by the rodents over winters, which followed a mast year. This represented just 1.2–4.8% of the total seedfall in different stands. However, sowing seeds in small patches can result in very high predation; Birkedal et al. (2009) found that in plots in south Sweden of 54 m2, every one of the 120 seeds sown could be removed by rodents. Aves Woodpigeons (Columba palumbus L.) frequently consume beech nuts, as do corvids and bramblings (Fringilla montifringilla L.), and such predation is responsible for quite important damage to beech regeneration (Huss, Kratsch & Röhring 1972; Jenni 1987). Chamberlain, Gosler & Glue (2007) recorded that in Britain, seven bird species were significantly lower in abundance in gardens in years of highest beech mast, suggesting that beech seeds are a significant part of their diet. In addition to the woodpigeon, these included great spotted woodpecker (Dendrocopos major L.), great tit (Parus major L.), coal tit (Periparus ater L.), nuthatch (Sitta europaea L.), jay (Garrulus glandarius L.) and chaffinch (Fringilla coelebs L.). They also suggested that beech seed forms a significant part of the diet of the blackbird (Turdus merula L.) and siskin (Carduelis spinus L.). Indeed, Perdeck, Visser & Van Balen (2000) and Perrins (1966) showed that the annual survival and movement of juvenile and adult great tits was closely correlated to the size of the beech crop since beech seeds form a large part of their winter food supply. In Sweden, the jay is a most important agent in spreading beech. Working in a study area a few kilometres N.W. of Stockholm, Kardell (2005) showed that this bird, which buries the seeds of both Fagus and Quercus, was responsible for the steady expansion of fresh beech trees from the original ‘mother trees’ at an average rate of 6.6 m per year. Acari The species recorded (Acari, Eriophyidae) are all gall formers and are all restricted to F. sylvatica. Aceria nervisequa (Canestrini) is common as a hairy patch on veins on the upper side of leaves (Redfern, Shirley & Bloxham 2002; Stubbs 1986; Phillipson & Thompson 1983; Darlington 1968). Aceria fagineus (Nalepa) is common as a hairy patch on the underside of leaves (Redfern, Shirley & Bloxham 2002). Acalitus stenaspis (Nalepa) is locally common on F. sylvatica, causing death of opening buds, malformation and stunting of young leaves (Alford 1991) and upward rolling of the leaf margin (Redfern, Shirley & Bloxham 2002). Acalitus blastophthirus (Nalepa) causes young leaves to be coated with silver hairs (Redfern, Shirley & Bloxham 2002). Acalitus plicans (Nalepa) causes the leaf to be covered with folds and hairs and to be a reddish colour (Redfern, Shirley & Bloxham 2002). Monochetus sulcatus (Nalepa) forms a gall as a tuft of hairs on the underside of the leaf © 2012 The Authors. Journal of Ecology © 2012 British Ecological Society, Journal of Ecology, 100, 1557–1608 Fagus sylvatica 1581 (Redfern, Shirley & Bloxham 2002). Eriophyes nervisequus (Canestrini) and Monochetus sulcatus (Nalepa) form galls on beech, and Rhyncaphytoptus gracilipes (Nalepa) (Acari, Rhyncaphytoptidae) also occurs on beech. Fallen cupules in the forest floor provide a microhabitat for feeding, moulting and oviposition by a variety of predatory and saprophagous invertebrates, including pseudoscorpions, springtails and mites. Certain phthiracaroids (‘Armadillo mites’, Oribatida) such as Steganacarus magnus (Nic.) and Phthiracarus anonymum Grdjn. embed their prelarvae (‘eggs’) in the microbially conditioned surface of the valves and pedicel. Soft-bodied immatures (larvae and three nymphal stages) burrow within the woody tissues, emerging as adults from frass-filled tunnels about a year later; adults of the smaller P. anonymum (length c. 0.5 mm, S. magnus c. 1.0–1.7 mm) may continue to live endophagously, laying prelarvae in their burrow walls (Harding & Easton 1984). Insecta Beech is relatively poor in insect diversity compared with oak but is still host to many insects compared to most woody plants. The estimate for beech by Kennedy & Southwood (1984) is 94, and for oak 421. Similarly, Petrakis et al. (2011) found 298 insects associated with beech and dead beech wood in Greece, compared to almost five times that on oak, attributed to the high phenolic content of beech trees. Table 1 lists nearly 200 species that have been found associated with beech. Salamon, Scheu & Schaefer (2008) discussed the collembolan communities of German beech forests. A number of mesophyll-sucking leafhoppers (Hemiptera, Homoptera, Cicadellidae) are found on F. sylvatica (see Table 1) but seldom cause serious damage to the host plant. Fagocyba cruenta (Herrich-Schaeffer), which mainly feeds on beech but also on other trees, accounted for 80% of the samples of typhlocybine leafhoppers sampled in three sites in south Wales (Claridge & Wilson 1981). Phyllaphis fagi (L.) (Hemiptera, Homoptera, Callaphididae) is common and widespread on F. sylvatica, causing leaves to curl and small swellings to develop on the upper surface (Darlington 1968; Redfern, Shirley & Bloxham 2002) and eventually to wither and die (Stroyan 1977; Alford 1991); it can be a serious nursery pest (e.g. Iversen & Harding 2007). Growth of sooty moulds can follow infestation, and the insect can cause significant damage (Bevan 1987). Cryptococcus fagisuga Lindinger (beech scale; Hemiptera, Homoptera, Eriococcidae) is generally abundant on the trunk and branches of F. sylvatica (Alford 1991) and is found throughout Europe and the eastern USA (Williams 1985). It causes punctures in the bark, leaving the tree open to infection, particularly by the ascomycete Nectria coccinea (Pers. Ex Fr.), which causes beech bark disease (Wainhouse & Howell 1983). There was considerable variation in susceptibility of trees to infestation by beech scale, and trees 20–25 years old were much more susceptible to attack (Wainhouse & Howell 1983). Krabel & Petercord (2000) note that infestation by the beech scale is closely linked to tree genotype and in particular the gene locus A of isocitrate dehydrogenase (IDH-A), which appears to act by controlling nutrient availability to the insect. A large number of Lepidopteran larvae eat, mine, roll or spin webs in leaves (see Table 1). Cydia fagiglandana (Zeller) (Lepidoptera, Tortricidae) is commonly met (Bradley, Tremewan & Smith 1973) since it frequently hollows out the nut of F. sylvatica (Emmet 1979). It is found in Wales, southern and central England, southern Scotland and south-western Ireland (Emmet 1991). The larvae can cause considerable destruction of beech nuts (Fig. 7). Percentage destruction of nuts by Cydia is much greater in non-masting years than in masting years but at Buckholt, Gloucestershire, where nuts were very regularly attacked, 14.9% were destroyed in the mast year 2000 (Packham & Hilton 2002). Even when mouldy nuts were taken into consideration, however, this still left 113.7 viable full nuts per tree in each 7-min sample. Nilsson & Wästljung (1987) studied seed predation and crosspollination at Stenbrohult, south Sweden. Pre-dispersal destruction of beech seeds by C. fagiglandana was 3.1% in a mast year and 38% in a non-mast year. Variation in seed destruction by vertebrates was much less in mast (5.7%) than non-mast (12%) years (Nilsson & Wästljung 1987). Their results led them to disagree with Silvertown (1980), who considered that a reduction in population size of seed-eating animals in non-mast years is necessary to a predator-satiation explanation of mast seeding. Results of Danish investigations and the English Beech Masting Survey (1980 to date) support their view. Habitat quality can be important in determining insect abundance. For example, Heiermann & Schütz (2008) found that the pale tussock moth (Calliteara pudibunda L.), a marked pest of beech in Europe, declined rapidly in beech forests as the proportion of Picea abies stems rose to 25% while Lymantria monacha L., a more polyphagous species, was largely unaffected by such changes. Müller, Hothorn & Pretzsch (2007b) and Müller, Bußler & Kneib (2008) found that the species richness of saproxylic beetles in German beech woods decreased markedly with increase in management intensity. Moreover, in German beech woods, the species richness of oribatid mites and collembolan species was found to be positively and negatively correlated with annual leaf litter fall, respectively (Irmler 2006). Interestingly, although it is normally thought that a large bole is better for conserving saproxylic insects, Schiegg (2001) in a study in Switzerland found that limbs of beech held 529 species of saproxylic Diptera and Coleoptera while trunks held 237 species. There was an overlap in species of 55.3% for Diptera and 82.6% for Coleoptera, suggesting that many species would benefit from limbs being left in woodlands even if the trunks were removed. Many Coleoptera but comparatively few Hymenoptera or Diptera are directly associated with F. sylvatica (Table 1). The Diptera restricted to F. sylvatica are primarily gall midges (Diptera, Cecidomyiidae) (Niblett 1941). While galls may be extremely numerous on beech leaves, Fernandes, Duarte & Lüttge (2003) found that for five common galling Diptera species in Germany, more than 77% of the attempts of the © 2012 The Authors. Journal of Ecology © 2012 British Ecological Society, Journal of Ecology, 100, 1557–1608 1582 J. R. Packham et al. Table 1. Insects recorded from Fagus sylvatica in Britain Species/classification Hemiptera Aradidae Alnetoidia alneti (Dahlborn) Aradus corticalis (L.) Cicadellidae Arboridia ribauti (Ossiannilsson) Edwardsiana flavescens (F.) Edwardsiana frustrator (Edwards, J.) Eurhadina concinna (Germar) Fagocyba cruenta (Herrich-Schaeffer) Lamprotettix nitidulus (F.) Lindbergina aurovittata (Douglas) Ribautiana debilis (Douglas) Typhlocyba quercus (F.) Ossiannilssonola callosa (Then) Cicadidae Cicadetta montana (Scopoli) Callaphididae Phyllaphis fagi (L.) Diaspididae Quadraspidiotus ostreaeformis (Curtis) Q. zonatus (Frauenfeldt) Coccidae Eulecanium tiliae (L.) Eriococcidae Cryptococcus fagisuga Lindinger Lachnidae Lachnus exsiccator Altum Pseudococcidae Phenacoccus aceris (Signoret) Trionymus newsteadi (Green) Miridae Psallus perrisi (Mulsant & Rey) Lepidoptera Arctidae Atolmis rubicollis (L.) Eilema deplana (Esper) Blastobasidae Blastobasis decolorella (Wollaston) Nepticulidae Stigmella hemargyrella (Kollar) S. tityrella (Stainton) Incurvariidae Nematopogon swammerdamella (L.) Ecological notes Source Recorded on beech and other trees in south Wales Found under bark of beech and other trees, mainly in southern England 1, 12 1, 43 Feeds mainly on hornbeam and beech; scattered throughout England, Wales and Ireland and most of Europe Occasional on beech Feeds mainly on beech; throughout the British Isles and most of Europe; causes silver flecking of the foliage Feeds on beech and other trees in England, Wales, Ireland, S. and C. Europe Feeds on beech; rather local but widespread in the British Isles and scattered in Europe Feeds on beech in south Wales Feeds principally on sycamore but also on beech and other trees; locally distributed in the British Isles and in C. and S. Europe 1 1, 2, 30, 12 1 1, 12, 30 1, 2, 30 1 1, 12, 30 1, 30 1, 12 1, 30 Adults; rare, local 1 Causes leaves to curl and develop small swellings on the upper surface before death; pest 1, 16, 35 Larvae, adults; pest Larvae, adults 1 1 Larvae and adults; ant-attended 1 Beech scale; generally abundant on trunk and branches; pest 1, 2 Rare and local aphid Widespread in Britain Known only from beech; mainly from south-east England 1, 46 1, 46 Adult 1 1 1 Leaf roller, webber 1 Leaf miner on either side of the leaf; locally common throughout the British Isles Leaf miner near the margin on the leaf underside of the leaf; common in England and Wales and widespread in the west of Ireland 1, 18, 19 Leaf miner in their early stages; widely distributed and often common in woodland over most of mainland Britain and in Ireland 1, 18, 19 25 © 2012 The Authors. Journal of Ecology © 2012 British Ecological Society, Journal of Ecology, 100, 1557–1608 Fagus sylvatica 1583 Table 1. (continued) Species/classification Cossidae Zeuzera pyrina (L.) Limacodidae Apoda limacodes (Hufnagel) Heterogenea asella (Denis & Schiffermuller) Gracillariidae Parornix fagivora (Frey.) Phyllonorycter maestingella (Müller) P. messaniella (Zell.) Sesiidae Synanthedon vespiformis (L.) Yponomeutidae Argyresthia semitestacella (Curtis) Ypsolopha vittella (L.) Oecophoridae Carcina quercana (F.) Diurnea fagella (Denis & Schiffermuller) Gelechiidae Teleiodes paripunctella (Thunb) Tortricidae Aphelia paleana (Hübner) Clepsis rurinana (L.) Cydia fagiglandana Zell. Ditula angustiorana (Haworth) Tortrix viridana (L.) Acleris sparsana (D. & S.) Ancylis mitterbacheriana (D. & S.) Strophedra weirana (Douglas) Pammene herrichiana (Heinemann) Geometridae Abraxas sylvata (Scopoli) Alcis jubata (Thunberg) Angerona prunaria (L.) Ecological notes Source Leopard moth; larvae feed in branches; local in southern Britain 40 The festoon; feeds on beech and oak; local in southern England The triangle; larvae feed on beech and oak; very local in southern England 1, 20, 41, 44 1, 41, 44 Mines leaves of Fagus and Carpinus and later folds them; widespread mainly in southeast England, but at low density Generally common on beech in C. and N. Europe and the British Isles; mines the underside of leaves, causing them to fold downwards Feeds mainly on Quercus ilex, occasionally on Fagus; mines the underside of leaves; widespread throughout the British Isles 1, 19, 21 Yellow-legged clearwing; mining larvae on oak, beech and other trees; widely distributed over central southern England 1, 5 Miner of shoots; throughout the British Isles Web spinner on leaves and flowers of Ulmus or Fagus 1, 19, 20 1, 19 Spins webs under leaves; widespread throughout the British Isles Spins webs or rolls leaves; abundant on F. sylvatica; widespread in Great Britain, S. and E. Ireland, throughout Europe 1, 2, 19, 20 Webber; principal hosts are oak and Myrica gale but recorded as also feeding on F. sylvatica 1, 20, 38 Webber of herbaceous plants and occasionally F. sylvatica; local in England, Ireland and southern Scotland; pest Rolls leaves; local and scarce in England and Ireland Hollows out the nut of F. sylvatica; generally common in Wales, S. and C. England, S. Scotland and S.W. Ireland; serious pest of seeds Spins webs on buds and twigs; widespread throughout the British Isles Larvae feed principally on Quercus but will feed on F. sylvatica; pest; widely distributed in oakwoods throughout Britain and Ireland Webber; widespread and generally common in woodland throughout the British Isles; widespread in Europe where it also attacks other trees Webber; locally common on beech and oak throughout Europe Larvae feed between two spun leaves of beech; throughout England and Wales Larvae feed in a cocoon in the mast of F. sylvatica; Wales, S.E. and Midlands of England 1, 10, 19 Clouded magpie; larvae feed mainly on foliage of Ulmus spp. but also F. sylvatica; widespread Larvae Orange moth; feeds on beech and other trees and shrubs; S. England and W. Ireland © 2012 The Authors. Journal of Ecology © 2012 British Ecological Society, Journal of Ecology, 100, 1557–1608 1, 2, 19, 21 1, 19, 21 1, 2, 19, 20 1, 10, 19 1, 10, 19, 20 2, 20 1, 10 1, 2, 10, 19 1, 2, 19 1, 19 1, 19, 20 1, 3, 20, 44 1 1, 20, 44 1584 J. R. Packham et al. Table 1. (continued) Species/classification Archiearis parthenias (L.) Alsophila aescularia (D. & S.) Biston betularia (L.) Campaea margaritata (L.) Cleorodes lichenaria (Hufnagel) Crocallis elinguaria (L.) Cyclophora linearia (Hübner) Deileptenia ribeata (Clerck) Ectropis bistortata (Goeze) E. consonaria (Hubner) Ennomos erosaria (D. & S.) E. quercinaria (Hufnagel) Epirrita christyi (Allen) Eupithecia irriguata (Hübner) Geometra papilionaria (L.) Odontopera bidentata (Clerck.) Operophtera brumata (L.) O. fagata (Scharf.) Paradarisa consonaria (Hübner) Plagodis dolabraria (L.) Selenia tetralunaria (Hufnagel) Notodontidae Drymonia dodonaea (D. & S.) Furcula furcula (Cl.) Phalera bucephala (L.) Ptilodon capucina (L.) Stauropus fagi (L.) Lymantriidae Arctornis l-nigrum (Müller, O.F.) Euproctis similis (Fuessly) Lymantria dispar (L.) L. monacha (L.) Orgyia recens (Hübner) Sphrageidus similis (Fuessly) Ecological notes Source Orange underwing; larvae feed on leaves; widepread March moth; larvae feed on leaves; throughout most of Europe Peppered moth; feeds on many trees and shrubs; widespread Light emerald; feeds on many deciduous trees and shrubs; throughout the British Isles Larvae Scalloped oak; feeds on many trees and shrubs; widespread in the British Isles Clay triple-lines; larvae feed on leaves of Fagus and is widespread throughout the British Isles Satin beauty; feeds mostly on conifers; England, Wales, S. Scotland and E. Ireland The engrailed; feeds on leaves of beech and other trees; mainland Britain and S.W. Ireland 20, 44 2 September thorn; found on oak, birch, lime and beech; throughout mainland Britain and E. Ireland August thorn; also feeds on many other trees and shrubs; widespread in the British Isles Widespread on deciduous trees including beech Marbled pug; feeds on oak and beech foliage; Wales and S. England Large emerald; larvae occasionally feed on leaves, widespread throughout the British Isles Scalloped hazel; feeds on many trees; widespread in the British Isles Webber; pest Northern winter moth; feeds on leaves throughout mainland Britain Square spot; feeds on beech and a few other trees; England, Wales and S.W. Ireland Scorched wing; feeds on leaves; widespread Larvae Marbled brown; larvae feed under the leaves of oak, birch and beech; locally common in England, Scotland, S.W. Ireland and S. Europe Sallow kitten; feeds on willows and F. sylvatica; restricted to Wales and S. and C. England Buff-tip; feeds on many trees and shrubs; can cause defoliation; throughout the British Isles Coxcomb prominent; feeds on the leaves of beech and other trees; widespread in the British Isles Lobster moth; feeds also on other trees; widely distributed in S. England, S.W. Ireland and Europe Black V moth; feeds on beech and other tree species; rare and scattered in Britain Yellow-tail; feeds mostly on hawthorn; widespread through the British Isles Gypsy moth; feeds on leaves and buds mainly of oak; can cause severe defoliation Larvae; pest Scarce vapourer; feeds on many other trees and shrubs; restricted to S.E. and C. England Larvae; webber 1, 20, 42, 44 1, 3, 20, 44 1 1, 20, 44 1, 20 1, 3, 20 2, 20 1 1, 3, 20 1, 3, 20 1, 3, 20, 24, 48 1, 3, 20 1, 3, 20, 42 2, 20 1 1, 2, 3, 20 1, 3, 20, 42, 44 1, 2, 3, 20 1 23 20, 44 1, 2, 3, 20 1, 3, 20, 42, 44 1, 23 1, 3, 20 3, 20, 23, 44 2 1 1, 3, 20, 44 1 © 2012 The Authors. Journal of Ecology © 2012 British Ecological Society, Journal of Ecology, 100, 1557–1608 Fagus sylvatica 1585 Table 1. (continued) Species/classification Nolidae Nola confusalis (Herrich-Schaeffer) Noctuidae Acronicta alni (L.) Agrochola macilenta (Hübner) Brachionycha sphinx (Hufnagel) Colocasia coryli (L.) Cosmia trapezina (L.) Eupsilia transversa (Hufnagel) Moma alpium (Osb.) Noctua fimbriata (Schreber) Orthosia cerasi (F.) O. incerta (Hufn) O. miniosa (D & S) Pseudoips fagana (F.) Trisateles emortualis (D. & S.) Xanthia aurago (D. & S.) Drepanidae Drepana cultraria (F.) Tineidae Triaxomasia caprimulgella (Stainton) Coleoptera Lycidae Platycis cosnardi (Chevrolat) Platycis minutus (F.) Cleridae Tillus elongatus (L.) Lymexylidae Hylecoetus dermestoides (L.) Elateridae Ampedus cinnabarinus (Eschsch) A. elongantulus (F.) A. nigerrimus (Lacordaire) A. nigrinus (Herbst) A. pomonae (Stephens) Ecological notes Source Least black arches; feeds on beech and other trees; local throughout the British Isles 1, 3, 20, 36, 44 Alder moth; also feeds on other trees and shrubs; widespread but local throughout the British Isles Yellow-line quaker; limited range of hosts including beech, oak and black poplar catkins; larvae initially feed in spun terminal shoots; local throughout mainland Britain Sprawler; feeds on many trees and shrubs; widespread in the British Isles Nut-tree tussock; webber on leaves of many deciduous trees; generally distributed throughout the British Isles Dun-bar; feeds on beech and other trees and shrubs and carnivorous on other larvae; generally common and widespread Satellite; webber; feeds on many trees, shrubs and herbaceous plants; can be carnivorous; widespread throughout the British Isles Scarce merveille du jour; feeds mainly on oak leaves oak but also beech; restricted to S. England Broad-bordered yellow underwing; autumn feeder on docks and other herbaceous plants and in the spring on many trees and shrubs including beech; widespread Common quaker; webber; feeds especially on oak but also on beech and other trees; widespread Clouded drab; feeds on many trees; widespread throughout the British Isles and Europe Blossom underwing; eggs laid on oak, but later disperse to other trees and shrubs, including beech; England, Wales and S. Ireland Green silver-lines; larvae feed on the underside of leaves of oak, beech and other trees; widespread in the British mainland to S. Scotland and scattered in Ireland Olive crescent; larvae feed in the withering leaves of oak and more rarely beech; very rare and local in S.E. England Barred sallow; webber of F. sylvatica and Acer campestre; particularly common in S.E. England 1, 2 1, 3, 11, 42 1, 3, 20, 42, 44 1, 11 1, 2, 20 1, 3, 20, 42 20, 44 1, 3, 20 1, 2, 3, 20, 44 2, 20 2, 20 1, 11, 44 1, 11 1, 3, 11, 42 Barred hook-tip; webber; widespread in Wales and the southern half of England 1, 20, 22 Larvae 1 Larvae, adults 1, 45 1, 4 1, 4 Pest; rare and scattered 1, 14 Polyphagous Polyphagous Polyphagous Polyphagous; alpine Polyphagous 1, 1, 1, 1, 1, © 2012 The Authors. Journal of Ecology © 2012 British Ecological Society, Journal of Ecology, 100, 1557–1608 14, 31, 34 31 37 37 4 1586 J. R. Packham et al. Table 1. (continued) Species/classification A. pomorum (Herbst) A. praeustus (F.) Ampedus rufipennis (Stephens) Cardiophorus gramineus (Scopoli) Ischnodes sanguinicollis (Pan) Limoniscus violaceus (Muller) Megapenthes lugens (Redtenbacher) Melanotus erythropus (Gmelin) Stenagostus villosus (Fourcro) Eucnemidae Eucnemis capucina Ahrens Hylis olexai (Palm) Melasis buprestoides (L.) Buprestidae Agrilus angustulus (Illiger) A. pannonicus (Piller & Mitterpacher) A. viridis (L.) Melanophila acuminata (Degeer) Buprestidae Agrilus angustulus (Illiger) Hellrigl Cucujidae Cryptolests spartii (Curtis) Uleiota planata (L.) Colydiidae Cicones variegata (Hellwig) Cerylonidae Cerylon fagi Brisout Cisidae Cis alni Gyllenhal Anobiidae Grynobius planus (F.) Ptilinus pectinicornis (L.) Salpingidae Rabocerus foveolatus (Ljungh) Rabocerus gabrieli Gerhardt Mordellidae Tomoxia bucephala Costa Melandryidae Melandrya caraboides (L.) Tenebrionidae Helops caeruleus (L.) Pseudocistela ceramboides (L.) Scarabaeidae Melolontha melolontha (L.) Saprosites mendax Blackburn Cerambycidae Anaglyptus mysticus (L.) Clytus arietis (L.) Leiopus nebulosus (L.) Leptura scutellata F. Prionus coriarius (L.) Curculionidae Acalles ptinoides (Marsham) Acalles turbatus Boheman Otiorhynchus singularis (L.) Phyllobius argentatus (L.) P. viridicollis (F.) P. pyri (L.) Ecological notes Source Polyphagous 1, 1, 1, 1, 1, 1, 1, 1, 1, Polyphagous Extinct Larvae Larvae Larvae Larvae Adults 31 31, 37 4, 31, 34, 37 31 31 31, 37 37 31 4 1, 45 1, 4, 32 1, 45, 47 Larvae Larvae; rare, local to scattered Larvae; rare, local Larvae; rare and local 1, 1, 1, 1, 9, 26 9, 26 26, 47 26 1 1, 45 1, 45 1, 4 1, 15, 45 1, 4 Larvae; pest 1, 45 1 1, 4 4, 45 1, 4 1, 4 1, 4 1, 4 Larvae, adults; pest Larvae Pest Adult; pest Larvae, adults; pest Can cause great damage to foliage 1 1, 4 1, 1, 1, 1, 1, 4 4 17 4 4 1, 4 1, 4 1, 27 1 47 2 © 2012 The Authors. Journal of Ecology © 2012 British Ecological Society, Journal of Ecology, 100, 1557–1608 Fagus sylvatica 1587 Table 1. (continued) Species/classification P. argentatus (L.) Polydrusus cervinus (L.) P. mollis (Strom) P. prasinus (Olivier) P. pterygomalis Boheman P. undatus (F.) Rhynchaenus fagi (L.) Rhyncolus gracilis Rosenhauer R. lignarius (Marsham) R. truncorum (Germar) Strophosomus capitatus (Degee) S. melanogrammus (Förster) Trachodes hispidus (L.) Attelabidae Apoderus coryli (L.) Attelabus nitens (Scopoli) Byctiscus betulae (L.) Deporaus betulae (L.) Apionidae Apion vorax Herbst Scolytidae Dryocoetinus alni (Georg) Ernoporus fagi (F.) Hylesinus oleiperda (F.) Balachows Scolytus intricatus (Ratzebur) S. rugulosus (Muller, P) Taphrorychus bicolor (Herbst) Xyleborus dispar (F.) X. dryographus (Ratzeb) X. saxeseni (Ratzeburg) X. domesticum (L.) Platypodidae Platypus cylindrus (F.) Pyrochroidae Pyrochroa coccinea (L.) Hymenoptera Tenthredinidae Caliroa annulipes (Klug) Nematus fagi Zaddach Diptera Cecidomyidae Contarinia fagi Rübsaamen Hartigiola annulipes (Hartig) Mikiola fagi (Hartig) Oligotrophus fagineus Kieffer Phegomyia fagicola (Kieffer) Drosophilidae Stegana nigrithorax Strobl Ecological notes Source Eats leaves of various trees including F. sylvatica Adult Adult Adult Adult Adult Larvae, adults; miner 2 Larvae; miner Larvae; miner Adult; pest Common pest of trees and shrubs; widely distributed in Europe 1, 1, 1, 1, 1, 1, 1, 1, 1, 1, 1, 4, 33 4 27 27 27 28, 45,47 45 39 4 27 2 1, 45 Common leaf roller on many trees Leaf roller Polyphagous Leaf roller, mainly on birch but also beech and other trees 1, 1, 1, 1, Pest 1, 13 Rare and scattered Larvae and adults Larvae, adults; pest; rare and local Larvae and adults; pest, rare and scattered Larvae and adults; rare and local to scattered Larvae and adults; pest, rare and local Rare and local 1, 1, 6 1, 6 1, 1, 1, 1, 1, Larvae, adults; pests 1, 6, 45 Larvae, adults 2 28 28, 39 2 45 6, 28, 45, 47 6 4, 6 6 6, 45 45 45 1, 4 Feeds on oak, lime, birch, willow beech and Vaccinium myrtillus; locally common in Britain, Ireland and N. and C. Europe Larvae are solitary, feeding on the edge of F. sylvatica leaves; widespread in southern England as far north as Perthshire 2 Galling of terminal buds; pupates in the soil; gregarious Produces small cylindrical galls on the upper surface of leaves; common Produces ovoid galls on the upper surface of leaves; larvae pupate in autumnal fallen galls Produces a rounded pustule gall by a thickening of the leaf parenchyma Reddish larvae live in folds along the lateral veins which have a slit-like opening on the upper side 1, 7, 35 Larvae, adults © 2012 The Authors. Journal of Ecology © 2012 British Ecological Society, Journal of Ecology, 100, 1557–1608 1, 8, 47 1, 7, 35 1, 7, 35 1, 7 1, 7, 35 1 1588 J. R. Packham et al. Table 1. (continued) Species/classification Lonchaeidae Lonchaea contigua Collin Ecological notes Source Larvae 1 Data taken from: (1) Phytophagous Insects Data base, (2) Alford (1991), (3) Allan (1949), (4) Allen (1984), (5) Baker (1985), (6) Balachowsky (1949), (7) Barnes (1948), (8) Benson (1958), (9) Bily (1982), (10) Bradley, Tremewan & Smith (1973), (11) Bretherton, Goater & Lorimer (1983), (12) Claridge & Wilson (1981), (13) Cockbain, Bowen & Bartlett (1982), (14) Cooter (1983), (15) Crowson (1982), (16) Darlington 1968; (17) Duffy (1953), (18) Emmet (1976), (19) Emmet (1979), (20) Emmet (1991), (21) Emmet, Watkinson & Wilson (1985), (22) Goater (1991), (23) Gould 2008; (24) Harper (1980), (25) Heath & Pelham-Clinton (1976), (26) Hellrigl (1978), (27) Hoffmann (1950), (28) Hoffmann (1958), (29) Lekander et al. (1977), (30) Le Quesne & Payne (1981), (31) Leseigneur (1972), (32) Lucht (1981), (33) Morris (1978), (34) Palm (1972), (35) Redfern, Shirley & Bloxham (2002), (36) Revell (1979), (37) Rudolph (1974), (38) Sattler (1980), (39) Scherf (1964), (40) Skinner (1985a), (41) Skinner (1985b), (42) South (1961), (43) Southwood & Leston (1959), (44) Stokoe & Stovin (1948), (45) Walsh & Dibb (1954), (46) Williams (1962), (47) Winter (1983), (48) de Worms (1979). Fig. 7. Four beech nuts damaged by larvae of the moth Cydia fagiglandana Zell. A perfect exit hole is shown by the nut at bottom right. The other three show exit holes that have been enlarged by birds endeavouring to reach a larva, one of which is shown bottom left. Fungal mycelium is present on the two nuts on the right-hand side. Shown at c. 3 × life size. Photograph by Dr M. Inman, first published in Packham & Hilton (2002); reproduced courtesy of the Arboricultural Journal. insects to induce galls on beech failed and led to death of the galling larvae; this was attributed to defences of the beech. There are reviews of Diptera from the soil of a Danish beech wood (Nielsen & Nielsen 2007) and from dead wood in a German stand (Hövemeyer & Schauermann 2003). (B) AND (C) PLANT PARASITES AND DISEASES Plants Parasites are few, but beech woodlands are renowned for their distinctive mycoheterotrophs, particularly Hypopitys monotropa (Ericaceae) and two orchids, Neottia nidus-avis (typical of the deep litter of Fagus-Mercurialis woodland), and the occasional records of Epipogium aphyllum (Taylor & Roberts 2011). In the UK, Neottia nidus-avis requires the presence of the fungus Sebacina dimitica for germination and growth, which appears to persist in mycorrhizal association with F. sylvatica (McKendrick et al. 2002). Fungi A large number of fungi has been recorded on litter or soil underneath beech trees. Table 2 lists those fungi that are found directly on beech other than those recorded on dead wood; a total listing of all fungi recorded on beech in the Britain Isles (some 3195 records) can be found in the Fungal Records Database of Britain and Ireland (British Mycological Society 2011). Sieber & Hugentobler (1987) produced a similarly long list of endophytic fungi found in beech in the Jura Mountains, and Ódora et al. (2006) described the dead wood fungi associated with semi-natural beech stands in mainland Europe including those that are threatened (and listed all the species in an electronic appendix). Heilmann-Clausen & Christensen (2005) reported a similar study of macrofungi in Denmark. Parasitic fungi causing serious diseases of Fagus sylvatica include Phytophthora cactorum (Lebert & Cohn) J. Schröt., P. citricola Sawada and P. cambivora (Petri) Buisman, which can cause bleeding cankers and extensive die-back of mature beech trees (Belisario, Maccaroni & Vettorazzo 2006; Nelson, Weiland & Hudler 2008; Fleischmann, Raidl & Oßwald 2010), understorey saplings (Nechwatal et al. 2011) and other species in mainland Europe (e.g. Munda, Zerjav & Schroers 2007). Fagus sylvatica is also now proving very susceptible to sudden oak death (Phytophthora ramorum Werres, De Cock & Man in ‘t Veld) and to Phytophthora kernoviae Brasier, Beales and S.A. Kirk (DEFRA 2008) although potassium phosphate might give some © 2012 The Authors. Journal of Ecology © 2012 British Ecological Society, Journal of Ecology, 100, 1557–1608 Fagus sylvatica 1589 Table 2. Fungi (and Order) directly associated with Fagus sylvatica, not including those found on soil or litter below the trees, or those found solely on dead wood. Details of these can be found in the Fungal Records Database of Britain and Ireland (British Mycological Society 2011). Nomenclature follows this data base Species/classification Fungi Oomycota Phytophthora cactorum (Lebert & Cohn) J. Schröt. (Peronosporales) P. cambivora (Petri) Buisman P. citricola Sawada P. cryptogea Pethybr. & Laff. Pythium intermedium de Bary (Pythiales) P. ultimum Trow Zygomycota Mortierella elongata Linnem. (Mortierellales) M. gamsii Milko M. parvispora Linnem. Mucor hiemalis f. hiemalis Wehmer (Mucorales) M. hiemalis f. luteus (Linnem.) Schipper M. racemosus f. racemosus Fresen. M. racemosus f. sphaerosporus (Hagem) Schipper Ascomycota Alternaria alternata (Fr.) Keissl. (Pleosporales) Anungitea rhabdospora P.M. Kirk (Pleosporales) Apiognomonia errabunda (Roberge ex Desm.) Höhn. (Diaporthales) Arachnophora fagicola Hennebert (Incertae sedis) Ascodichaena rugosa Butin (Diaporthales) Bactrodesmium arnaudii S. Hughes (Incertae sedis) B. spilomeum (Berk. & Broome) E.W. Mason & S. Hughes Botryosphaeria quercuum (Schwein.) Sacc. (Botryosphaeriales) Botrytis cinerea Pers. (Helotiales) Bulgaria inquinans (Pers.) Fr. (Leotiales) Camposporium cambrense S. Hughes (Incertae sedis) C. pellucidum (Grove) S. Hughes Cephalotrichum stemonitis (Pers.) Nees (Microascales) Chaetomium bostrychodes Zopf (Sordariales) C. funicola Cooke Chloridium botryoideum var. botryoideum (Corda) S. Hughes (Chaetosphaeriales) Coniochaeta subcorticalis (Fuckel) Munk (Coniochaetales) Fumagospora capnodioides G. Arnaud (Capnodiales) Fuscidea lightfootii (Sm.) Coppins & P. James (Umbilicariales) Gliomastix murorum var. felina (Marchal) S. Hughes (Hypocreales) Humicola fuscoatra Traaen (Sordariales) Hypocrea schweinitzii (Fr.) Sacc. (Hypocreales) Leptodothiorella sp. Höhn. (Botryosphaeriales) Melanopsammella vermicularioides (Sacc. & Roum.) Réblová, M.E. Barr & Samuels (Chaetosphaeriales) Oidiodendron rhodogenum Robak (Incertae sedis) O. tenuissimum (Peck) S. Hughes Phyllactinia guttata (Wallr.) Lév. (Erysiphales) Rhytisma acerinum (Pers.) Fr. (Rhytismatales) Rutstroemia petiolorum (Roberge ex Desm.) W.L. White (Helotiales) R. sydowiana (Rehm) W.L. White Truncatella hartigii (Tubeuf) Steyaert (Xylariales) Basidiomycota Abortiporus biennis (Bull.) Singer (Polyporales) Agrocybe erebia (Fr.) Singer (Agaricales) Antrodiella romellii (Donk) Niemelä (Polyporales) Armillaria mellea (Vahl) P. Kumm. (Agaricales) A. ostoyae (Romagn.) Herink Athelia acrospora Jülich (Atheliales) A. arachnoidea (Berk.) Jülich A. epiphylla Pers. A. teutoburgensis (Brinkmann) Jülich Ecological notes Seedlings Roots Bark Trunk Leaves Leaves Leaves Seeds, decaying cupules Living and dead trunks, bark, branches Cupules Bark Living and dead bark Leaves Living and dead trunks Cupules Cupules Leaves and cupules Cupules Bark Bark Bark Living leaves Bark Mycorrhizal root Mycorrhizal root Leaves, bark, wood Dark spots on fading leaves Bark Non-mycorrhizal root Non-mycorrhizal root Living and dead leaves Live leaves Petioles Petioles Diseased root Wood of live trees Roots, fallen wood Bark Live and dead trees Roots, decaying wood and branches Leaves Bark Wood Twigs © 2012 The Authors. Journal of Ecology © 2012 British Ecological Society, Journal of Ecology, 100, 1557–1608 1590 J. R. Packham et al. Table 2. (continued) Species/classification Ecological notes Aureobasidium pullulans var. pullulans (de Bary & Löwenthal) Arnaud (Boletales) Auricularia auricula-judae (Bull.) Wettst. (Auriculariales) Chamaemyces fracidus (Fr.) Donk (Agaricales) Daldinia concentrica (Bolton) Ces. & De Not. (Xylariales) Exidia repanda Fr. (Auriculariales) Ganoderma australe (Fr.) Pat. (Polyporales) G. pfeifferi Bres. G. resinaceum Boud. Lichenomphalia umbellifera (L.) Redhead, Lutzoni, Moncalvo & Vilgalys (Agaricales) Oudemansiella mucida (Schrad.) Höhn. (Agaricales) Phellinus ferreus (Pers.) Bourdot & Galzin (Hymenochaetales) Pholiota alnicola var. alnicola (Fr.) Singer (Agaricales) P. aurivella (Batsch) P. Kumm. P. squarrosa (Weigel) P. Kumm. Sparassis spathulata (Schwein.) Fr. (Polyporales) protection from Phytophthora species (Dalio, Fleischmann & Osswald 2011). Phytophthora syringae (Klebahn) Klebahn and P. undulata Petersen and Dick damage roots, and P. gonapodyides Petersen and P. plurivora Jung and Burgess have been recovered from stem tissue, but none of these appear to cause much damage or loss of growth (Fleischmann et al. 2002; Nelson, Weiland & Hudler 2010) although the last may damage understorey beech (Nechwatal et al. 2011). Bracket fungi (Basidiomycota) found on old or unhealthy trees include Fomes fomentarius (L.) J.J. Kickx, Phellinus ignarius (L.) Quél.(=F. ignarius (L.) Cooke) and Ganoderma applanatum (Pers.) Pat. In southern Germany, Fomes fomentarius is the most common fungus in virgin forests and strict forest reserves but is almost absent from highly managed forests (Müller, Engel & Blaschke 2007a). Auricularia auricula-judae (Bull.) Wettst. sometimes occurs on Fagus sylvatica but is much commoner on Sambucus nigra. Oudemansiella mucida (Schrad.) Höhn. was present on F. sylvatica at the Woodbury Down, Devon, sampling site used by Hilton & Packham (1997). The edible oyster fungus (Pleurotus ostreatus (Jacq.) P. Kumm.), which can cause considerable damage to F. sylvatica, is commercially cultivated in some countries (Hora 1981). The white rot fungus Trametes versicolor (L.) Pilát (Basidiomycota, Polyporales) and the soft rot fungus Kretzschmaria deusta (Hoffm.) P.M.D. Martin [=Ustulina deusta] (Ascomycota, Xylariales) are strongly invasive of beech wood (Deflorio et al. 2008). Bernicchia et al. (2007) list 166 species of aphyllophoraceous fungi growing on F. sylvatica in Italy. Libertella faginea Desm. (Pezizomycotina) has been found on beech branches in Slovakia (Adamčíková, Juhásová & Kobza 2011), and Sieber & Hugentobler (1987) list a number of endophytic fungi found in beech in the eastern Jura Mountains. Nectria coccinea (Pers.) Fr. (Ascomycota, Hypocreales) causes the serious beech bark disease which now damages English pole-stage stands, where entry is via puncture wounds made by the minute sap-sucking felted beech coccus Crypto- Leaves Fallen wood Roots Upright and fallen dead wood; notable for being most common on ash Bark Living trunk Living trunk Living trunk Bark Dead and living trunks and branches Branches Trunk, live roots Living trunks Living trunks Living trunks and roots coccus fagisuga Lindinger. ‘Tarry spots’ are caused by the exudation of fluid from patches of bark killed by the fungus (Lonsdale 1986; Lonsdale & Wainhouse 1987). Older trees stressed by drought, nutritional imbalance or root disorders may become susceptible to attack by the fungus even in the absence of the insects which facilitate initiation of the disease in younger trees. Serious disease of beech can be caused by the ubiquitous Heterobasidion annosum (Fr.) Bref. (Łakomy & Cieślak 2008) and by Armillaria species. Of these, the following have been recorded on beech: Armillaria mellea (Vahl) P. Kumm. (on live and dead trees), A. gallica Marxm. and Romagn. (on stumps), A. ostoyae (Romagn.) Herink (roots, decaying wood and branches) and A. tabescens (Scop.) Emel (on buried wood). As with many angiosperm trees, a number of species of wood-rotting fungi have been found present in apparent healthy sapwood of beech, leading to rapid decay upon death (Parfitt et al. 2010). The diversity of saprotrophic fungi in beech forests has been shown to be related to the age and continuity of woodlands, in the same way as that of lichens, by Ainsworth (2004, 2005), who surveyed saprotrophs growing on large-diameter beech logs in Windsor Forest for a decade. Peterken (1996) emphasized the importance of fungal indicator species for British beech forests of high conservation value. The 30 indicators now used on bulky beech substrata such as logs and branches in Britain are listed in Table 3. They belong to several fungal groups, and almost all are also found on other species of tree. Thick tarcrust Camarops polysperma (Mont.) J.H. Mill., spiraltarcrust Eutypa spinosa (Pers.) Tul. and C. Tul. (another ascomycete whose fruit bodies spiral down beech trunks), toothed powdercap Flammulaster muricatus (Fr.) Watling, fragrant toothcrust Mycoacia nothofagi (G. Cunn.) Ryvarden and a number of gilled and poroid bracket fungi are particularly notable. In Denmark, a list of 42 species of potential fungal indicators was proposed by Heilmann-Clausen & Christensen © 2012 The Authors. Journal of Ecology © 2012 British Ecological Society, Journal of Ecology, 100, 1557–1608 Fagus sylvatica 1591 (2005) and subsequently used, with variations, in much of continental Europe. The use of a single European list for such indicators is not straightforward because of the differing geographical (and dynamic) ranges of the fungi involved. Nevertheless, results obtained when a list of 21 European indicators was applied to 126 European beech forests were extremely interesting. Two Slovakian communities came top, both with a score of 16 out of the 21 possible, followed by others from the Czech Republic (15), France (15) and Denmark (14). The Wood Crates (13) and Denny Wood (12) areas of the New Forest were, respectively, sixth and eighth. All of the 11 largest British beech forests were in the top 30, so the use of this relatively new method of assessment has emphasized their conservation value. Epiphytes Tables 4 and 5 list the epiphytic lichens and slime moulds (Amoebozoa, Myxomycetes), respectively, found associated with beech in the British Isles. Fritz & Heilmann-Clausen (2010), Fritz, Gustafsson & Larsson (2008) and Nascimbene, Marini & Nimis (2007) list epiphytic lichens and mosses associated with beech in Sweden and Italy. In the UK, relatively few bryophytes are associated specifically with beech, with the notable exception of Zygodon forsteri. This has a wide European range but is notably rare and in the north of its range is largely restricted to knot-holes or seepage tracks on old beeches in Epping Forest, Burnham Beeches and the New Forest (Proctor 1961; Little 1967; Adams 1984). Other bryophytes found on beech in southern England (Table 6) are characteristic of acidic or nutrient-poor bark with the exception of Rhynchostegium confertum and Brachythecium rutabulum, which are very common mosses often also on less acidic substrates. Though Zygodon forsteri was not present in the 34 tetrads on which Table 6 is based, two other Zygodon species were. Not surprisingly, older trees tend to hold more epiphyte species (Fritz, Niklasson & Churski 2009), and the history of the ecosystem is also important (Thomas & Packham 2007). For example, the richness of epiphytic lichen communities is frequently related to the length of time the dominant trees have been established in the forest. Fagus sylvatica has a south-western distribution in Sweden where aged beech trees in old forest stands often have an extremely rich lichen flora including the rare Lobaria pulmonaria (L.) Hoffm., a leafy green lichen found throughout the Northern Hemisphere. As well as the age of the individual trees, the age and ‘continuity’ of the forest stand are very important. In the province of Halland, Sweden, certain lichen species, such as Pyrenula nitida (Weigel) Ach., Catinaria laureri (Hepp ex Th. Fr.) Degel. and Bacidia rosella (Pers.) Not. (=B. phacodes Körb.) occur only in areas that have been covered by beech for many hundreds of years. In contrast, planted Fagus sylvatica forests on ground that lacks ‘beech continuity’ are never inhabited by these species (Hultengren 1999). Such lichens are thought formerly to have been widespread and relatively common in virgin forests throughout Europe (Rose 1988), forming part of the Lobarion assemblage of foliose Table 3. Deadwood fungi indicative of ancient beech woodland in Britain, organized by fungal order. Nomenclature follows the Fungal Records Database of Britain and Ireland (British Mycological Society 2011). From Ainsworth (2005) Ascomycota Boliniales Camarops polysperma (Mont.) J.H. Mill. Xylariales Eutypa spinosa (Pers.) Tul. & C. Tul. Basidiomycota Agaricales Flammulaster limulatus (Fr.) Watling (=F. limulatus var. limulatus (Fr.) Watling F. muricatus (Fr.) Watling Hohenbuehelia auriscalpium (Maire) Singer H. mastrucata (Fr.) Singer Phyllotopsis nidulans (Pers.) Singer Volvariella bombycina (Schaeff.) Singer Ossicaulis lignatilis (Pers.) Redhead & Ginns Atractiellales Phleogena faginea (Fr.) Link Hymenochaetales Inonotus cuticularis (Bull.) P. Karst. I. nodulosus (Fr.) P. Karst. Phellinus cavicola Kotl. & Pouzar Oxyporus latemarginatus (Durieu & Mont.) Donk Polyporales Gloeohypochnicium analogum (Bourdot & Galzin) Hjortstam Mycoacia nothofagi (G. Cunn.) Ryvarden Aurantiporus alborubescens (Bourdot & Galzin) H. Jahn A. fissilis (Berk. & M.A. Curtis) H. Jahn Ceriporiopsis gilvescens (Bres.) Domanski C. pannocincta (Romell) Gilb. & Ryvarden Coriolopsis gallica (Fr.) Ryvarden Ganoderma pfeifferi Bres. Spongipellis pachyodon (Pers.) Kotl. & Pouzar S. delectans (Peck) Murrill Russulales Lentinellus ursinus (Fr.) Kühner L. vulpinus (Sowerby) Kühner & Maire Hericium cirrhatum (Pers.) Nikol. H. coralloides (Scop.) Pers. H. erinaceus (Bull.) Pers. Scytinostroma portentosum (Berk. & M.A. Curtis) Donk and crustose lichens which develop as a late-successional grouping on the bark of large trees. They include species of the genera Lobaria, Sticta, Pseudocyphellaria, Parmeliella, Pannaria, Nephroma, Peltigera and Parmelia. Lobarion occurred through most of Europe well into the nineteenth century, but changes in forest practice and pollution have greatly reduced its area; it is now largely confined to montane forests and the lowland oceanic zone from south-west Norway to the Iberian Peninsula. X. History PALAEOBOTANY AND RECENT HISTORY The fossil record suggests Fagus originated in the Early Tertiary in the northern Pacific Basin (Denk 2003). Of the 13 species of Fagus recognized by Shen (1992), eleven are East Asian; F. sylvatica is European and F. grandifolia is © 2012 The Authors. Journal of Ecology © 2012 British Ecological Society, Journal of Ecology, 100, 1557–1608 1592 J. R. Packham et al. Table 4. Lichens (and Order) directly associated with Fagus sylvatica. Nomenclature follows the Fungal Records Database of Britain and Ireland (British Mycological Society 2011) Species/classification Ecological notes Agyriales Trapeliopsis pseudogranulosa Coppins & P. James Arthoniales Chrysothrix candelaris (L.) J.R. Laundon Lecanactis abietina (Ehrh. ex Ach.) Körb. Opegrapha vulgata (Ach.) Ach. Schismatomma decolorans (Turner & Borrer ex Sm.) Clauzade & Vezda Lecanorales Catinaria atropurpurea (Schaer.) Vezda & Poelt Cladonia cornuta (L.) Hoffm. C. macilenta Hoffm. C. parasitica (Hoffm.) Hoffm. C. polydactyla var. polydactyla (Flörke) Spreng. Evernia prunastri (L.) Ach. Hypogymnia physodes (L.) Nyl. H. tubulosa (Schaer.) Hav. Lecanora chlarotera Nyl. L. conizaeoides f. conizaeoides Nyl. ex Cromb. L. expallens Ach. L. jamesii J.R. Laundon Lecidella elaeochroma f. elaeochroma (Ach.) M. Choisy Lepraria incana (L.) Ach. Loxospora elatina (Ach.) A. Massal. Melanelia subargentifera (Nyl.) Essl. Melanohalea exasperatula (Nyl.) O. Blanco, A. Crespo, Divakar, Essl., D. Hawksw. & Lumbsch (=Parmelia exasperatula Nyl.) Mycoblastus fucatus (Stirt.) Zahlbr. Parmelia sulcata Taylor Parmeliopsis ambigua (Wulfen) Nyl. P. hyperopta (Ach.) Arnold Platismatia glauca (L.) W.L. Culb. & C.F. Culb. Pseudevernia furfuracea var. ceratea (Ach.) D. Hawksw. Ramalina farinacea (L.) Ach. R. fraxinea (L.) Ach. Scoliciosporum chlorococcum (Graewe ex Stenh.) Vezda Usnea ceratina Ach. U. florida (L.) Weber ex F.H. Wigg. U. rubicunda Stirt. U. subfloridana Stirt. Ostropales Graphina anguina (Mont.) Müll. Arg. Graphis elegans (Borrer ex Sm.) Ach. Phaeographis dendritica (Ach.) Müll. Arg. P. lyellii (Sm.) Zahlbr. Phlyctis agelaea (Ach.) Flot. Porina chlorotica f. chlorotica (Ach.) Müll. Arg. P. leptalea (Durieu & Mont.) A.L. Sm. Stictis radiata (L.) Pers. Thelopsis rubella Nyl. Thelotrema lepadinum (Ach.) Ach. Peltigerales Lobaria virens (With.) J.R. Laundon Peltigera collina (Ach.) Schrad. P. horizontalis (Huds.) Baumg. P. praetextata (Flörke ex Sommerf.) Zopf P. albescens var. corallina (Zahlbr.) J.R. Laundon P. amara f. amara (Ach.) Nyl. P. flavida (DC.) J.R. Laundon P. hemisphaerica (Flörke) Erichsen 1932 P. hymenea (Ach.) Schaer. P. multipuncta (Turner) Nyl. Base of trunk Bark Living bark Living trunk Wood Bark Bark Decayed bark Decayed bark Bark Fallen branches Fallen twigs and branches, wood Bark Bark Bark Twig Twig Bark Bark Bark Fallen twigs Fallen trunk Bark Bark Bark Bark Bark Bark Branches Bark Bark Bark Bark Bark Bark Bark © 2012 The Authors. Journal of Ecology © 2012 British Ecological Society, Journal of Ecology, 100, 1557–1608 Fagus sylvatica 1593 Table 4. (continued) Species/classification Ecological notes P. pertusa (Weigel) Tuck. P. velata (Turner) Nyl. Pertusariales Pertusaria albescens var. albescens (Huds.) M. Choisy & Werner Pyrenulales Asteromassaria macrospora (Desm.) Höhn. Kirschsteiniothelia aethiops (Berk. & M.A. Curtis) D. Hawksw. Pyrenula occidentalis (R.C. Harris) R.C. Harris Teloschistales Amandinea punctata (Hoffm.) Coppins & Scheid. Buellia disciformis (Fr.) Mudd Caloplaca obscurella (J. Lahm ex Körb.) Th. Fr. Heterodermia leucomela (L.) Poelt Physcia aipolia (Ehrh. ex Humb.) Fürnr. P. pulverulenta (Schreb.) Hampe Rinodina exigua (Ach.) Gray Xanthoria parietina (L.) Th. Fr. Incertae sedis Chaenotheca ferruginea (Turner ex Sm.) Mig. Graphis scripta (L.) Ach. Bark North American. Some extinct Fagus species had macromorphological characteristics that are regarded as primitive (Peters 1997). These often migrated and gave rise to forms that are present today. A very short, very stout, very hairy cupule is regarded as primitive: this feature is still found in Fagus lucida (China) and some Fagus hayatae ssp. hayatae (Taiwan). The past and present richness of Fagus species in China supports the view that this was the area in which Fagus originated. The complex relationships between fossil and present species are summarized in Peters (1997). None of the species now extant grew in the Miocene, when the species known to have existed were F. evenensis, F. palaeojaponica, F. antipofi, F. protolongipetiolata, F. stuxbergii, F. palaeocrenata and F. menzelii. Common beech Fagus sylvatica is considered to have evolved from F. saxonica (Oligocene) via F. menzelii (Miocene) and F. kraeuselii (Upper Pliocene). Besides dealing with the evolutionary history of the various species of Fagus, Peters (1997) describes the changing forms of the forests that they dominated or in which they played a significant part. Beech forests in Eurasia, and particularly in Japan, were more intensively manipulated by humans than those in North America. The role of humans in creating pure European forests of Fagus sylvatica, often on less fertile sites, was important, as was the actions of the first farmers in aiding the spread of beech in forests dominated by Tilia. Fagus sylvatica has been widespread at different times through Europe. In northern Italy, Fagus pollen was around in low values 32 000–16 500 cal., BP (before present) with local and regional high counts of beech pollen in association with Abies, Vitis and Quercus (up to 5%) perhaps favoured by humid microclimates. From 22 900–18 500 cal., BP pollen of temperate trees including Fagus declined, and by 17 000– c.16 500 cal., BP were reduced to isolated stands in steppe conditions (Kaltenrieder et al. 2009). Wood Dead wood and twigs Rotting wood Bark Wood, fallen sticks Bark Twigs Twigs Base of trunk Fallen wood Living tree bark Bark F. sylvatica appears to have survived the last glaciation as small populations scattered across Europe and may have survived as far north as the Carpathians (Magri et al. 2006; Magri 2008), Balkans (Magri et al. 2006), north-eastern Italy (Kaltenrieder et al. 2009), S.E. Alps (Brus 2010) and the Iberian Mountains (López-Merino et al. 2008). The central European refugia were separated from those of the Mediterranean, which did not contribute to the colonization of central and northern Europe (Comps et al. 1987, 1990). Far from being geographical barriers preventing the expansion of beech, mountain chains actually facilitated its diffusion and contributed to the modern genetic diversity of Fagus sylvatica in Europe. In the late Holocene, the expansion of beech followed climate amelioration to a cool-temperate climate with warmer winter conditions (Huntley 1988; Tonkov et al. 2008; Valsecchi et al. 2008) and did not become a dominant species in Bulgaria and many other regions until late in the Holocene (Tonkov 2003). Modelling by Bialozyt, Bradley & Bradshaw (2012) suggests that F. sylvatica would have spread by seed dispersal at a rate of 100 m year 1 in late Holocene Scandinavia (compared to 250 m year 1 in Picea abies). Tinner & Lotter (2006) described five hypotheses to explain the Holocene expansion of beech and common silver fir (Abies alba) in central Europe. These were climatic change, migrational lag, delay in population increase, human disturbance and fire disturbance. Their investigations suggested that neither human nor fire disturbance substantially promoted the expansion of these two species though they did affect them at particular places at particular times. In practice, Fagus and Abies expanded relatively rapidly in response to climatic change involving cooling and heavy precipitation around 8200 years ago and similar events around 3800–3400 and 2750–2350 years ago. There are many examples in the literature where an expansion of © 2012 The Authors. Journal of Ecology © 2012 British Ecological Society, Journal of Ecology, 100, 1557–1608 1594 J. R. Packham et al. Table 5. Slime moulds (Amoebozoa, Myxomycetes) directly associated with Fagus sylvatica. Nomenclature follows the Fungal Records Database of Britain and Ireland (British Mycological Society 2011) Species/classification Ecological notes Arcyria affinis Rostaf. (Trichiida) A. cinerea (Bull.) Pers. Fallen tree, especially beech in S. England Dead leaves, bark, wood, especially oak but also other hardwoods; very common Rotten hardwoods; very common Mossy, rotting wood; frequent in S. and E. Fallen wood, especially oak, very common Dead wood especially beech; very common Fallen branches of hardwoods; common Fallen branches; uncommon Fallen wood especially beech and elm; common in S. England Dead wood especially beech; common Dead wood; widespread Dead wood (usually conifers); abundant Leaf litter especially beech; common in S. Soil and leaf litter; common in S. Fallen leaf Dead leaves and twigs especially holly and oak; common Normally on very decayed wood of conifers Normally on very decayed wood of conifers Fallen wood of conifers but also beech Normally on decayed wood of conifers; rare Stumps, wood of oak, beech and conifers; uncommon Fallen leaves; common in S. England Bark; Atlantic woodlands Dead wood especially beech; common Fallen leaves of hard-leaved trees; rare Litter; rare, England only Fallen leaves of especially beech; widespread Fallen leaves and cupules; frequent in S. England Fallen leaves and cupules; frequent in S. Dry dead leaves, litter; frequent Fallen branches; frequent Fallen leaves, litter; common Dead leaves and twigs; very common Dead leaves, especially holly; common Dead leaves, especially oak; frequent in S. Dead leaves; abundant Dead wood particularly oak and pine; very common Fallen leaves; scattered Litter and mosses; Atlantic Dead wood; very common Dead wood and leaves; scattered Dead wood especially beech; common in S. Dead wood; uncommon Dead leaves; very rare Dead leaves and twigs, litter especiaaly conifers; very common Living bark on epiphytes; common Very rotten wood; increasingly common Dead wood particularly elm and beech; frequent in S. England Dead wood and leaves; live trunk; very common on limestone Bark of ash normally; common in S. Dead ash wood normally; southern Branches, dead wood Bark, litter; common in S. Litter, cupules; common Leaves and litter; scattered Rotten wood; very common Rotten wood; frequent Wood, fallen branches Dead wood; common Fallen branches especially of conifer or oak; common A. denudata (L.) Wettst. A. ferruginea Saut. A. incarnata (Pers. ex J.F. Gmel.) Pers. A. nutans (Bull.) Grev. (=A. obvelata (Oeder) Onsberg) A. pomiformis (Leers) Rostaf. Badhamia macrocarpa (Ces.) Rostaf. (Physarida) B. panicea (Fr.) Rostaf. B. utricularis (Bull.) Berk. Brefeldia maxima (Fr.) Rostaf. (Stemonitida) Ceratiomyxa fruticulosa var. fruticulosa (O.F. Müll.) T. Macbr. (Protostelida) Craterium aureum (Schumach.) Rostaf. (Physarida) C. leucocephalum var. leucocephalum (Pers. ex J.F. Gmel.) Ditmar C. leucocephalum var. scyphoides (Cooke & Balf. f.) G. Lister C. minutum (Leers) Fr. Cribraria argillacea (Pers. ex J.F. Gmel.) Pers. (Liceida) C. aurantiaca Schrad. C. cancellata var. cancellata (Batsch) Nann.-Bremek. C. microcarpa (Schrad.) Pers. C. tenella Schrad. Diachea leucopoda (Bull.) Rostaf. (Stemonitida) Diacheopsis insessa (G. Lister) Ing (Stemonitida) Dictydiaethalium plumbeum (Schumach.) Rostaf. ex Lister (Liceida) Diderma asteroides (Lister & G. Lister) G. Lister (Physarida) D. donkii Nann.-Bremek. D. effusum (Schwein.) Morgan D. globosum Pers. D. hemisphaericum (Bull.) Hornem. D. spumarioides (Fr.) Fr. D. umbilicatum var. umbilicatum Pers. Didymium clavus (Alb. & Schwein.) Rabenh. (Physarida) D. difforme (Pers.) Gray D. nigripes (Link) Fr. D. serpula Fr. D. squamulosum (Alb. & Schwein.) Fr. Enerthenema papillatum (Pers.) Rostaf. (Stemonitida) Fuligo candida Pers. (Physarida) F. muscorum Alb. & Schwein. F. septica var. flava (Pers.) Morgan F. septica var. septica (L.) F.H. Wigg. Hemitrichia calyculata (Speg.) M.L. Farr (Trichiida) H. clavata (Pers.) Rostaf. H. leiotricha (Lister) G. Lister Leocarpus fragilis (Dicks.) Rostaf. (Physarida) Licea parasitica (Zukal) G.W. Martin (Liceida) Metatrichia floriformis (Schwein.) Nann.-Bremek. (Trichiida) M. vesparium (Batsch) Nann.-Bremek. Mucilago crustacea var. crustacea P. Micheli ex F.H. Wigg. (Physarida) Perichaena corticalis (Batsch) Rostaf. (Trichiida) P. depressa Lib. Physarum album (Bull.) Chevall. (Physarida) P. cinereum Link P. compressum Alb. & Schwein. P. contextum (Pers.) Pers. P. leucophaeum Fr. P. psittacinum Ditmar P. robustum (Lister) Nann.-Bremek. P. vernum Sommerf. P. viride var. viride (Bull.) Pers. © 2012 The Authors. Journal of Ecology © 2012 British Ecological Society, Journal of Ecology, 100, 1557–1608 Fagus sylvatica 1595 Table 5. (continued) Species/classification Ecological notes Reticularia lobata Lister (=Enteridium lobatum (Lister) M.L. Farr (Liceida) R. lycoperdon Bull. (=Enteridium lycoperdon (Bull.) M.L. Farr) R. splendens var. jurana (Meyl.) Kowalski (=Enteridium splendens var. juranum (Meyl.) Härk.) Symphytocarpus amaurochaetoides Nann.-Bremek. (Stemonitida) Trichia affinis de Bary (Trichiida) T. botrytis var. botrytis (Pers. ex J.F. Gmel.) Pers. T. contorta var. contorta (Ditmar) Rostaf. T. contorta var. iowensis (T. Macbr.) Torrend T. decipiens var. decipiens (Pers.) T. Macbr. T. decipiens var. hemitrichioides Brândza T. flavicoma (Lister) Ing T. lutescens (Lister) Lister T. persimilis P. Karst. T. scabra Rostaf. T. varia (Pers. ex J.F. Gmel.) Pers. T. verrucosa Berk. Stump; scattered and uncommon Dead wood and trunks; common Fallen branches especially of oak; common Dead stumps; uncommon Leaf litter, very rotten wood; very common Bark, fallen branches; very common Fallen trees; frequent Fallen trees; rare Dead wood, fallen branches; very common Fallen branches; very rare so far Dead wood;; rare Bark; decaying logs; rare Very decayed wood; very common Fallen dead wood especially elm and beech; common in S. Very rotten wood; very common Fallen branches especially conifers; scattered Data taken from the Fungal Records Database of Britain and Ireland (British Mycological Society 2011) and Ing (1999). Fagus pollen appears to be associated with indicators of human disturbance, such as an increase in cereal pollen and disturbance by fire, from Spain to Bulgaria and Sweden (Odgaard 1994; Küster 1997; Bolte, Czajkowski & Kompa 2007; Lindbladh et al. 2008; Tonkov et al. 2008; Muñoz Sobrino et al. 2009; Pèlachs et al. 2009). Most palaeoecological studies lack sufficient resolution to determine whether the increase in Fagus and human activity are exactly contemporaneous. However, in southern Scandinavia, Bradshaw & Lindbladh (2005) compared stand-scale pollen records with charcoal concentrations and pollen indicators of anthropogenic presence and found that charcoal levels and pollen from cultivated cereals were usually higher immediately prior to the appearance of F. sylvatica pollen. Though once established, beech declined after local fires. This helps explain the contradictory picture where increases in beech have been linked to a decrease in forest fire occurrence (Valsecchi et al. 2008; Tonkov et al. 2008) but also to an increase in local clearance using more fire (Küster 1997). Bradshaw & Lindbladh (2005) argue that this link with human activity would have contributed to a patchy colonization of F. sylvatica and slowed its Holocene spread in comparison with other dominant trees such as Picea abies. However, a number of studies has shown that the link does not always hold (e.g. Gardner & Willis 1999). In the northern Alps, the spread of beech preceded significant human activity (Tinner & Lotter 2006; Heiss & Oeggl 2008), and further west in Bulgaria and northern Hungary, F. sylvatica appeared some 5000 years ago, despite human activity dating back almost 9000 years (Gardner 2002; Tonkov 2003; Galaty 2005). Moreover, Kardell (2005), describing the northern movement of F. sylvatica from its arrival in southern Sweden around 800 BC, suggests that although its initial spread was probably assisted by bronze- and iron-age humans, active cultivation of the land later impeded its northern advance so that the ‘beech boundary’ was imposed by humans rather than the climate. Today, the northern spread of beech is promoted by increased fertility, resulting from the deposition of available nitrogen and an increasingly warm climate. Following a marked decline, Fagus expanded between 5300–4700 cal. year BP, again coinciding with increased human presence (Valsecchi et al. 2008; Bradshaw, Kito & Giesecke 2010). Beech populations continued to expand until about 3500 BP. In the past three millennia, beech populations have increased at a slower rate, tending towards a static distribution or even declining slightly (Magri 2008). In Britain, the post-glacial advance of F. sylvatica, as elsewhere in north-west Europe, was comparatively late and was local until the Sub-Atlantic (Godwin 1975a). At the beginning of the Bronze Age, it expanded rapidly in S.E. England and Wales, attributed to either a wetter climate or its invasion into felled woodland or abandoned cultivated ground (Rackham 2003) and beech pollen (which is poorly dispersed) has been found in small quantities in south Wales (Godwin & Mitchell 1938; Hyde 1940) and East Anglia (Godwin & Clifford 1938). Small amounts of pollen have also been found outside of the ‘natural’ distribution, such as near York (Atherton 1976), which suggests that beech had begun to colonize further north before it was extensively planted. Subsequent spread northwards in the late Bronze Age was undoubtedly helped by human intervention, particularly ground disturbance (Björkman 1999) and activities such as pannage may have particularly favoured beech (Grant, Waller & Groves 2011). The abundance of F. sylvatica was in some cases associated with an anthropological decline in Tilia such as at Epping Forest, north London c. 1800 BP (Grant & Dark 2006), and the New Forest c. 600 BP (Grant & Edwards 2008), and a concomitant decline in Quercus spp. (Godwin 1975b). Humans therefore appear to have artificially hastened the © 2012 The Authors. Journal of Ecology © 2012 British Ecological Society, Journal of Ecology, 100, 1557–1608 1596 J. R. Packham et al. Table 6. Bryophytes found associated with Fagus sylvatica in southern England by Bates et al. (1997), Bates, Roy & Preston (2004); data kindly extracted by C.D. Preston. The number of tetrads is from a total of 34 of the original 107 in which beech was found. The Ellenberg reaction values, where available, indicate association with very acidic (1) to very alkaline (9) substrates (Hill et al. 2007). Nomenclature follows Smith (2004) and Paton (1999) Species Bryophyta Hypnum cupressiforme Hedwe. Brachythecium rutabulum (Hedwe.) Schimp. Dicranoweisia cirrata (Hedwe.) Lindb. Dicranella heteromalla (Hedwe.) Schimp. Eurhynchium praelongum (Hedwe.) Schimp. Isothecium myosuroides Brid. Mnium hornum Hedwe. Hypnum resupinatum Taylor H. andoi A.J.E. Sm. Pseudotaxiphyllum elegans (Brid.) Z. Iwats. Dicranum scoparium Hedwe. Rhynchostegium confertum (Dicks.) Schimp. Amblystegium serpens (Hedwe.) Schimp. Plagiothecium nemorale (Mitt.) A. Jaeger Bryum capillare Hedwe. Dicranum montanum Hedwe. Hypnum cupressiforme s.l. Hedwe. Neckera complanata (Hedwe.) Huebener Orthotrichum affine Schrad. ex Brid. O. striatum Hedwe. Plagiothecium succulentum (Wilson) Lindb. Ulota bruchii Hornsch. ex Brid. Aulacomnium androgynum (Hedwe.) Schwägr. Ceratodon purpureus (Hedwe.) Brid. Ctenidium molluscum (Hedwe.) Mitt. Dicranum tauricum Sapjegin Didymodon sinuosus (Mill.) Delogne Eurhynchium crassinervium (Taylor) Schimp. Hypnum jutlandicum Holmen & Warncke Isothecium alopecuroides (Dubois) Isoviita Neckera pumila Hedwe. Orthotrichum diaphanum Brid. Plagiothecium curvifolium Schlieph. ex Limpr. P. undulatum (Hedwe.) Schimp. No. of tetrads Ellenberg reaction value 16 12 4 6 12 4 11 3 11 5 11 11 10 8 7 4 4 4 4 3 6 6 3 7 4 3 2 2 2 Table 6. (continued) Species Pleurozium schreberi (Willd. ex Brid.) Mitt. Pohlia nutans (Hedwe.) Lindb. Polytrichum formosum Hedwe. Schistidium apocarpum s.l. (Hedwe.) Bruch & Schimp. Syntrichia laevipila Brid. Thuidium tamariscinum (Hedwe.) Schimp. Tortula muralis Hedwe. Ulota crispa (Hedwe.) Brid. Ulota crispa s.l. (Hedwe.) Brid. Zygodon conoideus (Dicks.) Hook. & Taylor Zygodon viridissimus s.l. (Dicks.) Brid. Hepatophyta Lophocolea heterophylla (Schrad.) Dumort. L. bidentata (L.) Dumort. Metzgeria furcata (L.) Dumort. M. temperate Kuwah. Frullania dilatata (L.) Dumort. Lepidozia reptans (L.) Dumort. Microlejeunea ulicina (Taylor) A. Evans Diplophyllum albicans (L.) Dumort. Lejeunea cavifolia (Ehrh.) Lindb. Plagiochila porelloides (Torr. ex Nees) Lindenb. Porella platyphylla (L.) Pfeiff. No. of tetrads Ellenberg reaction value 1 1 1 1 1 1 1 1 1 1 1 15 4 5 5 4 3 2 2 1 1 1 1 2 2 2 2 2 1 1 1 1 1 1 1 1 1 1 1 1 spread of beech through the British Isles before natural colonization could occur. The status of F. sylvatica in Radnorshire is regarded by Woods (1993) as uncertain, though its pollen is found in peat deposits dating to at least pre-Roman times (Moore 1978). SOCIOECOLOGY Wood from F. sylvatica has a long and varied history of human use, and beech is an important European forestry tree, but perhaps less so in the UK since it is less well matched to the climate and is very susceptible to grey squirrel damage. Beech timber lasts well under water but, unless suitably impregnated, deteriorates when exposed to the weather. Winchester Cathedral was constructed above vast numbers of piles, said to be of beech, which supported it excellently until some misguided individual ordered the area surrounding the cathedral to be drained (M.C.F. Proctor, pers. comm.). Beech timber can be steam-bent and yields an excellent veneer when rotary-peeled. It is much used for machine-made furniture and is used for kitchen utensils, tool handles, sabots (shoes made entirely from wood) and for the soles of clogs. Beech block floors wear well. Beech makes excellent fire- © 2012 The Authors. Journal of Ecology © 2012 British Ecological Society, Journal of Ecology, 100, 1557–1608 Fagus sylvatica 1597 wood and charcoal. Beech has been used in ship-building, especially for the keel as it forms very long logs and is more rigid than oak. In previous centuries, it appears that foresters working in parks and estates occasionally planted a number of seedlings in a single hole (bundle planting) with the intention of producing impressive trees relatively quickly (Green 1996). An outstanding copper beech, with semi-vertical fusion marks on the trunk, at Forde Abbey, Dorset, appears to have arisen from several individuals planted in this way. The relative dominance of beech and oak in Britain has been extensively modified by planting and selective felling. Beech dominance in the New Forest was undoubtedly helped by the extraction of oak in the 18th and 19th centuries for ship-building (Peterken & Tubbs 1965) and, more widely, a reduction in pony and cattle herbivory during the Second World War. Peters (1997) demonstrates that the sustained use of European forests has existed for many centuries, receiving considerable impetus in the Late Middle Ages, a period when there was a shortage of wood. By the beginning of the twentieth century, well-informed foresters had abandoned clear-cutting in favour of selection systems. Gayer (1898) gave particular emphasis to the importance of mixed species stands and a return to natural stand forms. Beech is indeed often harvested commercially from mixed forests. Working on the development of the structure of a Bavarian beech–spruce forest, von Gadow (1997) describes changes in the density and structure caused in both species by thinning. Beech has been extensively used and valued by humans, and there is evidence from the Chilterns of domestic use since medieval times (Roden 1968). Certainly, Schlich (1910) recognized the value of beech as a timber crop. Forestry has involved shelterwood systems and more recently clear-felling especially during the World Wars (Matthews 1989), and particularly from what would naturally be the Fagus-Rubus woodlands (Rodwell 1991). More recently, F. sylvatica has been planted under a nurse crop of pine. Though not as popular as oak, beech timber has also been used in building construction as well as a fuel. Site productivity involving Fagus sylvatica has been shown to vary over time in a number of instances, of which those reported from Denmark by Skovsgaard & Henriksen (1996) are particularly interesting. In two large-scale silvicultural experiments on natural regeneration, there was a considerable increase in site productivity as measured by height growth. Between the 1920s and 1990, the trees underwent an increase of c. 3.6 m (at the reference age of 100 years). Height growth of beech planted after beech increased similarly in this area. Remnants of Fagus sylvatica forest near the tree line at 1600–1850 m in the central Apennines, Italy, left growing after logging following World War II, are of especial interest. The identification here by Piovesan et al. (2005) of a persistent Fagus community, in which gap-phase regeneration has led to a mono-specific multi-aged stand at spatial scales of a few hectares, is of particular importance as far as the longterm conservation of such forests is concerned. In continental Europe, there has in the last half century been a tendency to shift from Picea abies to Fagus sylvatica as the most important tree to plant in large-scale forestry, particularly in France. In view of the large chilling requirement for this species to break dormancy, this may not be a suitable policy in the future. There is evidence, however, that mixed stands of P. abies and F. sylvatica produce more biomass than a combination of pure stands of both species, particularly on poor soils (Pretzsch et al. 2010). Picea abies benefits from the greater nutrient turnover from the more rapid decomposition of the beech litter, which also improves soil water storage and pH while beech is unaffected by competition from P. abies. In comparison with P. abies, beech litter has a higher Ca, Mg and K content, as well as a lower C/N ratio (Augusto et al. 2002). On very fertile sites, however, beech growth of the canopy and roots tends to outcompete P. abies, and the yield of mixed stands is reduced. Comparing oak and beech as forestry trees and the effects these have on nutrient capitals, André, Jonard & Ponette (2010) found that for equivalent harvesting scenarios, beech led to higher Mg exports than oak (Quercus petraea), but lower exports of Ca. They also gave details of nutrient contents of different parts of a beech tree and concluded that harvesting large branches (  7 cm diameter) in addition to the trunks of beech would yield 32% extra biomass but lead to an average increase in nutrient exports of 34% (Ca), 40% (K), 61% (Mg) and 55% (P). This would increase further to a 60% increase in biomass and nutrient exports of 65% (Ca), 81% (K), 123% (Mg) and 162% (P) for complete tree harvesting. Important aspects of the commercial production of beech are the combined effects of drought and disease in critical years such as 1959 and 1976 in S.E. England and the Chilterns. These need prompt attention to minimize financial loss. After the 1976 outbreak, the Forestry Consultant John Workman (pers. comm.) advised that in the following winter all dead trees and those with black spots indicating serious and probably irreversible damage to the cell structure, which might or might not be infected with Beech Bark disease Nectria coccineaa, should be felled and marketed while their timber still had value. In the last part of the twentieth century the Continuous Cover Forestry Group was very successful in promoting this method of regenerating forests instead of clear-cutting and re-planting. Fagus sylvatica was one of the species of which particular note was taken, as Packham (1993) indicates. Under commercial production, beech produces weak coppice shoots and rarely dominates a coppice underwood (Rackham 1980; Peterken 1981). However, coppice stands in the Fagus-Rubus stands of the Chiltern plateau were extensively used in the 18th and 19th centuries by the ‘chairbodgers’. In the past, beech was frequently pollarded in Europe to provide both wood and leaf fodder for farm animals. The F. sylvatica pollards of Epping Forest and Burnham Beeches are particularly notable. Read (2008) reports the results of a recent survey and provides excellent illustrations of modern pollarding, which is very extensive in Romania, where pollards are cut for winter fodder and some trees are © 2012 The Authors. Journal of Ecology © 2012 British Ecological Society, Journal of Ecology, 100, 1557–1608 1598 J. R. Packham et al. shredded, that is, they are allowed to grow to their full height but have their side branches removed. XI. Conservation Fagus sylvatica is a widespread tree across Europe with few immediate threats to its long-term survival. Indeed, its range is currently expanding in central Europe, particularly where forests with a high percentage of conifers are being converted into more natural mixed forests (e.g. Bončina, Diaci & Gašperšič 2003). Climate change may have significant effects on beech, particularly at the extremes of its range (Peñuelas et al. 2008). Certainly, beech is known to be responsive to climatic changes, and at current levels, these are primarily beneficial to beech. Bontemps, Hervé & Dhôte (2009, 2010) analysed height and radial growth of dominant beech trees in stands across N.E. France and found a gradual increase in growth (50% increase in annual ring width over the last century). However, Charru et al. (2010) modelled the growth of beech stands in the same area and found that stand basal area increased by 27.8% between 1977 and 1987, but then decreased by approximately 5% between 1987 and 2004, which they ascribe to lower water availability. Fagus sylvatica productivity under simulated climate change conditions is affected by interactions between temperature, water vapour saturation deficit, nitrogen availability and soil moisture; these effects have been linked to leaf number rather than leaf area or photosynthetic activity (Fender, MantillaContreras & Leuschner 2011). However, the most important limiting factor for beech under climate change scenarios is likely to be drought, particularly at the south of its current range where it is likely to become less competitive (Geßler et al. 2007), and its range is highly likely to contract (Jump & Peñuelas 2006; Jump, Hunt & Peñuelas 2006) or move to higher altitudes (Peñuelas & Boada 2003), disappearing from the south of France, Italy, the former Yugoslavia and Greece by 2050 (Kramer et al. 2010). Surviving populations in areas such as the central Appenines, Italy, may show restricted growth (Piovesan et al. 2008). However, southern populations are highly genetically diverse (Demesure, Comps & Petit 1996; Scarascia-Mugnozza et al. 2000) and are better able to withstand drought (Tognetti, Johnson & Michelozzi 1995; García-Plazaola et al. 2008; Fotelli et al. 2009) compared to those in the north. The range of F. sylvatica has also been predicted to contract in the east due to drought. Czúcz, Gálhidy & Mátyás (2011) suggested from a modelling study that 56–99% of present-day beech forests in Hungary might be outside their present bioclimatic niche by 2050 (compared to 82–100% of Quercus petraea forests). Reproduction appears to be the key to surviving in the south since modelling shows that as climate warms and becomes drier, beech will produce more seeds, increasing the chances of establishment (Silva et al. 2012). Contraction of range is also likely in the west due to inadequate chilling as winter warms more than summer by 2100 (Sykes, Prentice & Cramer 1996). Over much of its current range and at its northern current extreme, modelling results indicate that beech has a high adaptive potential to environmental change if recruitment is frequent and many trees contribute seeds encouraging genetic diversity (Kramer et al. 2008), and it should maintain or expand its populations into Scandinavia and the Baltic States by 2100 (Kramer et al. 2010). It is also predicted that beech will expand at the expense of Abies alba at low altitudes (Maxime & Hendrik 2011). There may be some negative influences, for example, Fleischmann, Raidl & Oßwald (2010) found that beech seedlings were more susceptible to the root pathogen Phytophthora citricola Sawada under doubled CO2 levels but only on low N soils. Carbon storage may be affected by climate change. Soil organic carbon in Germany is known to decrease by about 25% from stands with 4900 to those with 600 mm precipitation year 1 (Meier & Leuschner 2010), and although C storage in stems increased slightly, it has been concluded that a reduction in precipitation will lead to beech forests moving from being a sink (Pilegaard et al. 2011) to becoming a net source of carbon. The potential effects of climatic changes in the UK are complex and difficult to predict, but more extreme scenarios envisage parts of Kent and Sussex becoming unsuitable for beech (Broadmeadow & Ray 2005). Although beech is unlikely to disappear from southern England, its yield potential will become lower, thus reducing its competitive ability compared to oak and ash. Wesche, Kirby & Ghazoul (2006) were particularly concerned with the quality and nature of the communities likely to occur in future native beech woodlands to the north and west of the existing native range of Fagus sylvatica. Their investigations involved a considerable number of quadrat studies beneath beech woodland both within and outside what is considered to be its present native range, that is, in Cumbria, the Peak District National Park, Oxfordshire, the Chilterns Area of Outstanding Natural Beauty and Kent. They also used data from county floras and took account of mature beech woodlands outside the presumed present native range of F. sylvatica. Many such woodlands are on acid soils but there is a stand on base-rich soil near Port Appin, West Scotland, whose rich flora includes Neottia nidus-avis, Daphne laureola and Cephalanthera longifolia. They conclude that the communities that form in future beech woodlands in the north and west will not be identical to those of the southeast. Wesche, Kirby & Ghazoul (2006) also pointed to the need to revise present conservation policy, especially where much conservation effort is focused on resisting change by removing beech from northern and western oakwoods. In some cases, these efforts can be justified, as in stands where the particular vascular plant composition encourages the retention of rich bryophyte communities. In at least some other cases where beech is already abundant and regenerating abundantly, and where mature trees exist outside the existing native range, beech woodland should be allowed to develop naturally. This should be done on both acid and base-rich soils as their floras will differ. © 2012 The Authors. Journal of Ecology © 2012 British Ecological Society, Journal of Ecology, 100, 1557–1608 Fagus sylvatica 1599 Plant communities of beech woodlands are often distinctive and contain a number of Ancient Woodland Vascular Plants (AWVP) indicators which are of conservation value (Rose 1999; Thomas & Packham 2007). Though topography and geographical location influence the presence of some of them, many are useful indicators over considerable areas. Peterken (1993, 1996) studied AWVPs in Britain, continental Europe and North America, demonstrating that the best indicators had a strong affinity for ancient woods, showed little or no ability to colonize secondary woodland and were rarely found in recent woodland or other habitats. The AWVP list for Shropshire gives both strong indicators and others which are either less strong or relatively weak (Whild 2003). Rackham (2003) provides a useful discussion of flowering plants and ferns in ancient woods and points out that many important species have been lost from ancient woodland sites because of excessive shade; this is particularly the case where coppicing of ancient beechwoods has been abandoned. This is unfortunately true of formerly orchid-rich coppices on calcareous soils. There do not appear to be any lists of AWVPs specific to beechwoods, which because of its extreme shade tolerance are particularly associated with Oxalis acetosella, a species also found in habitats other than woodland (Packham 1979). As in woodlands dominated by other types of tree, the species present in the ground vegetation of beechwoods varies on soils of differing types and pH. Acknowledgements We thank the University of Wolverhampton for the use of its facilities over many years and are most grateful to Dr N.J. Musgrove for assistance with IT and the literature survey. JRP thanks Dr G.M. 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