Milium Effusum

Journal of Ecology 2017, 105, 839–858 doi: 10.1111/1365-2745.12744

BIOLOGICAL FLORA OF THE BRITISH ISLES* No. 282

List Vasc. Pl. Br. Isles (1992) no. 153, 11, 1 Biological Flora of the British Isles: Milium effusum

Pieter De Frenne†,1,2,Jorg€ Brunet3, Mathias Cougnon2, Guillaume Decocq4, Bente J. Graae5, Jenny Hagenblad6, Martin Hermy7, Annette Kolb8, Isgard H. Lemke8, Shiyu Ma1, Anna Orczewska9, Jan Plue10, Guy Vranckx11, Monika Wulf12 and Kris Verheyen1 1Forest & Nature Lab, Ghent University, Geraardsbergsesteenweg 267, BE-9090 Gontrode-Melle, Belgium; 2Department of Plant Production, Ghent University, Proefhoevestraat 22, BE-9090 Melle, Belgium; 3Southern Swedish Forest Research Centre, Swedish University of Agricultural Sciences, Box 49, SE-230 53 Alnarp, Sweden; 4EDYSAN (FRE 3498 CNRS-UPJV), Universite de Picardie Jules Verne, 1 rue des Louvels, FR-80037 Amiens Cedex, France; 5Department of Biology, Norwegian University of Science and Technology, NO-7491 Trondheim, Norway; 6IFM – Biology, Linkoping€ University, SE-581 83 Linkoping,€ Sweden; 7Forest, Nature & Landscape, K.U. Leuven, Celestijnenlaan 200E, BE-3001, Leuven, Belgium; 8Vegetation Ecology & Conservation Biology, FB2, University of Bremen, Leobener Str., DE-28359 Bremen, Germany; 9Department of Ecology, Faculty of Biology & Environmental Protection, University of Silesia, ul. Bankowa 9, PL-40-007 Katowice, Poland; 10Department of Physical Geography, Stockholm University, SE-106 91 Stockholm, Sweden; 11Plant Conservation & Population Biology, K.U. Leuven, Kasteelpark Arenberg 31, Box 2435, BE-3001 Leuven, Belgium; and 12Institute of Land Use Systems, Leibniz-ZALF, Eberswalder Strasse 84, DE-15374 Muncheberg,€ Germany

Summary 1. This account presents information on all aspects of the biology of Milium effusum L. (Wood Mil- let) 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. The grass Milium effusum is a common species of mature woodland in central and southern Eng- land, but is less common in the wetter parts of northern England, Wales, Scotland and Ireland. World- wide, the species is native to many temperate, boreal, subarctic and subalpine parts of the northern hemisphere: from eastern North America across most of Europe (excluding Mediterranean climates) to the Ural Mountains and Black Sea, extending eastwards to the Himalaya, Korea and Japan. 3. Wood Millet is a shade-tolerant, relatively tall grass (up to 1Á8 m) producing up to 700 caryopses per individual. It is characteristic of temperate deciduous woodland, but can also occur in other woodland and forest types and even in scrub, alpine meadows, along railways and roads, and on rocks. In woods, it is one of the most conspicuous plants of the herb layer in the early summer after the disappearance of spring flowering species. While the species is generally considered an ancient woodland indicator in England and western Europe, it is also known to colonize secondary, post- agricultural forests relatively rapidly in other areas such as Denmark, southern Sweden and Poland. 4. The species has a wide amplitude in terms of soil acidity and nutrient availability, but predominantly grows on soils of intermediate soil fertility and soil pH and with high organic matter concentration. However, M. effusum can tolerate large quantities of tree-leaf litter on the forest floor and is able to grow on very acidic soils. 5. Changes in land use, climate, densities of large herbivores and atmospheric deposition of nitrogen are having effects on populations of Wood Millet. Significant responses of the life-history traits and population characteristics have been detected in response to environmental variation and to experimental treatments of temperature, nutrients, light and acidity. In many of its habitats across its range,

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

M. effusum is currently becoming more frequent. During the last century, its mean elevation of occurrence in upland areas of Europe has also increased by several hundreds of metres. Typically, management actions are directed towards the conservation of its main habitat type (e.g. ancient woodlands of the Milio-Fagetum association) rather than to the species speciﬁcally. Key-words: climatic limitation, communities, conservation, ecophysiology, geographical and altitudinal distribution, germination, latitudinal gradient, mycorrhiza, parasites and diseases, reproductive biology

Wood Millet. Poaceae. Milium effusum L. is a widespread Horticultural Society 2015) and also in the US it is recom- caespitose, rhizomatous, perennial grass of temperate to sub- mended for shady, moist habitats (Gunnel, Goodspeed & arctic regions of the Northern Hemisphere. Culms (45) 55– Anderson 2015). Allozyme studies have suggested the species 140 (180) cm, erect or geniculate, ascending from decumbent to be highly variable with less genetic diversity in northern bases; nodes generally 3–5. Sheaths smooth, ligules eciliate populations, but without clear geographic distribution of the membranous, (3) 4–9 (10) mm, obtuse, erose. Blades 5– diversity (Tyler 2002). 30 cm long, 5–17 mm wide, flat, smooth, hairless, evenly dis- The genus Milium belongs to the tribe Milieae of the Poa- tributed on the culms, blue-green to green. Panicles 10–30 ceae (Valdes & Scholz 2009). The only other native Milium (40) cm, branches 1–9 (13) cm, in pairs or fascicles, flexuous, species in Europe (and first detected in North America in spreading or drooping, scabrous, with spikelets mainly near 1987) is the annual Milium vernale M. Bieb. (early millet or the distal end. Spikelets 2Á4–3Á6(4Á0) mm, narrowly elliptic spring milletgrass) (Barkworth et al. 2007; Clayton et al. to ovate, pointed, single-flowered. Glumes 2Á5–5 mm, 2015). Early millet is not native in the British Isles except for smooth, 3-veined, acute to acuminate, narrowly elliptic to two localities on the north coast of Guernsey. ovate and greenish, membranous, with a narrow transparent In the British Isles and continental Europe, Milium effusum to white edge. Lemmas obscurely 5-veined, 2Á3–3 mm, lance- occurs predominantly in deciduous and mixed woodland, and olate to elliptic, pointed and smooth and shiny, becoming is locally abundant in oak and beech woods, especially on tough and hard. Palea 2-nerved, c. equal to lemma and partly moderately moist and heavy and calcareous soils rich with enfolded by it, narrowly ovate and somewhat rough on the humus. However, it also occurs in other woodland and forest keel. Anthers 3, 1Á5–3 mm. Caryopsis ovoid, smooth, 2Á5– types, thickets, in clear-cuts, on shaded banks, on rocks (e.g. 3 mm, light to dark brown at maturity, c. 40–700 per individ- in Scotland and Iceland), along railway tracks and roads, in ual, shorter than the lemmas and concealed at maturity; esti- scrub, in montane meadows or tall herbaceous vegetation and mated air-dry mass of 0Á5–1Á7 mg. The hilum is a short sometimes even in dunes. groove. The grass often bends towards the ground resulting in the characteristic shape of the panicle at caryopsis maturity. I. Geographical and altitudinal distribution This information was derived from Grime, Hodgson & Hunt (1988), Hubbard (1992), Conert et al. (1998), Barkworth Milium effusum is common throughout most of the British et al. (2007), Cope & Gray (2009), De Frenne et al. (2011b, Isles, occurring in 1391 of the 2805 10 km 9 10 km squares, c, 2014), Mossberg & Stenberg (2012), Clayton et al. (2015) but in only 91 of 985 squares in Ireland and none in the and Gr€aff, Moser & Heiselmayer (2015). Channel Islands (Fig. 1; Hill, Preston & Roy 2004). It is There are several subspecies of Milium effusum. European locally frequent, most common in southern and central Eng- M. effusum subsp. effusum has 4–5 panicle branches at most land, except in the Fens of eastern England. It is less abun- nodes and spikelets about 3 mm long (Fernald 1950; Bark- dant in the cooler and wetter north-western parts of England, worth et al. 2007; Valdes & Scholz 2009). North American Wales and the Scottish Lowlands, rare in the Highlands and plants belong to M. effusum subsp. cisatlanticum Fernald Inner Hebrides and absent from the Outer Hebrides, Orkney which grows in forests in eastern North America and has 2–3 and Shetland (Preston, Pearman & Dines 2002). In Ireland, it panicle branches at most nodes and spikelets of 2Á5–5mm is rare, and scattered throughout the country. Although it has length (Conert et al. 1998; Barkworth et al. 2007). Conert almost always been treated as a native, Forbes & Northridge et al. (1998), Tyler (2002) and Valdes & Scholz 2009 also (2012) suggest that it may have been accidentally introduced mention M. effusum subsp. alpicola Chrtek (M. alpicolum with imported trees or shrubs planted on large private estates. (Chrtek) Landolt) with much smaller panicles (only 12– In most parts of England, M. effusum is referred to as an indi- 16 cm) and occurring at higher elevations in thickets and cator of ancient woodland (see section V.B). alpine meadows in the Alps, Carpathian Mountains, Bohe- Milium effusum is classified as a member of the Circumpo- mian Forest, Balkans and Turkey. The M. effusum cultivar lar Boreo-temperate floristic element by Preston & Hill ‘Aureum’ has yellowish leaves in the spring that change to (1997) and occurs over much of the European continent from yellow-greenish later in the growing season and has been Iceland and the North Cape in northernmost Scandinavia east- developed for horticultural purposes. In the UK, for instance, ward to the Ural Mountains, south to the Mediterranean and this cultivar is sold by 55 suppliers across the country (Royal Black Sea and Crimea (Fig. 2), Middle East, and parts of

Fig. 1. The distribution of Milium effusum in the British Isles. Each dot represents at least one record in a 10-km square of the National Grid. (●) native 1970 onwards; (○) native pre 1970; (+) non-native 1970 onwards; (9) non-native pre-1970. Mapped by Colin Harrower, Biological Records Centre, Centre for Ecology and Hydrology, mainly from records collected by members of the Botanical Society of the British Isles, using Dr A. Morton’s DMAP software.

Siberia, Kamchatka, north-western Iran, Kazakhstan, Afghani- stan, Pakistan, India (the Himalaya), China, Taiwan, Japan and Korea. In northern Europe, it does not occur on the Faroe Islands and Svalbard (Conert et al. 1998; Mossberg & Sten- berg 2012). Close to the edge of its northern range, the species occurs typically in small deciduous forest patches within a largely subalpine/subarctic tundra matrix where it is associated with moist, relatively nutrient-rich sites (e.g. in Abisko in northern Sweden). Towards southern Europe, M. effusum is more sparsely distributed and it is absent from most of the Mediterranean region, except in uplands and mountains (e.g. in the Pyrenees, Alps, Apennines and on Corsica). It is absent from the Azores and Crete. The southern range limit in Eur- ope is around 38–40°N in the Iberian Peninsula and Italy. The North American M. effusum has only a limited range from latitude 51Á5° at the western entrance to the Straits of Belle Isle westward to the north shore of Lake Superior (lati- Fig. 2. The distribution of Milium effusum in Europe and neighbour- ° ing areas using a Lambert Azimuthal Equal Area projection and reso- tude 47 ) and Minnesota, south to Nova Scotia, northern and lution of 10 km 9 10 km (redrawn after Hulten & Fries 1986). western New England, Pennsylvania, upland Maryland, West [Colour ﬁgure can be viewed at wileyonlinelibrary.com] Virginia, south-central Ohio, northern Indiana and north-central Illinois. The species is unknown in western North Amer- 5 m a.s.l. in western Belgium and 30 m a.s.l. in several sites ica (Fernald 1950; Kartesz 2015), but has been recorded in in Germany and Sweden; Van Landuyt et al. 2006; De New Zealand (Conert et al. 1998). Frenne et al. 2014) up to 2400 m a.s.l. in the eastern Swiss Milium effusum occurs almost from sea level, being Alps (Unterengadin; Conert et al. 1998). The maximal reported as present in dunes and lowlands (e.g. at a few recorded elevation of M. effusum in Britain is 380 m a.s.l. in metres above sea level (a.s.l.) in Jægerspris, Denmark, at a site west of Dockray, Cumbria (Pearman & Corner 2015).

In a large-scale floristic inventory of forest plant communi- (B) SUBSTRATUM ties from the lowland to the upper subalpine vegetation belt Milium effusum has a wide amplitude in terms of soil acidity (0–2600 m a.s.l.) over five mountain ranges in France (the and nitrogen (N) availability (Hoennekes 1934; Pearsall western Alps, northern Pyrenees, Massif Central, western 1938). Ellenberg species indicator values are intermediate Jura, Vosges), the mean elevation of occurrence of between the potential extremes, i.e. 5 for moisture (F), for pH M. effusum was 834 (931–1032; 95% confidence interval) m (R) and for nitrogen (N) (Ellenberg & Leuschner 2010). Hill, a.s.l. in the years 1905–1985 and 1209 (1343–1624) m a.s.l. Preston & Roy (2004) mention the same values for the F and between 1986 and 2005 (after correcting for sampling N indicator values but recommend using R = 6 for the British biases). Thus, the mean elevation of occurrence within these situation. The species is most common on moderately moist mountain habitats exhibited a striking upward shift of and heavy, loamy or calcareous soils, rich in humus and of 412 m, probably related to climate change (Lenoir et al. intermediate fertility and intermediate pH with a deep, humic 2008). The maximal elevation where M. effusum was soil of sand, stones or pure clay (Conert 2000). recorded in these mountain plots was 1315, 1400, 1510, Table 1 summarizes forest floor and topsoil characteristics 1700 and 2210 m a.s.l. in the Vosges, Jura, Massif Central, measured in Wood Millet populations occurring in beech and northern Pyrenees and western Alps, respectively (J. Lenoir, oak woodlands across its European distribution range. The personal communication). In Norway, the elevational limit is species is able to tolerate widely differing amounts of tree- 1380 m a.s.l. in the Hardanger Vidda National Park and leaf litter and bare soil, and is able to penetrate through a rel- 700 m a.s.l. in northern Norway (Hulten & Fries 1986). In atively thick layer of leaf litter (up to 10 cm deep, Table 1) southern Kazakhstan, it grows at elevations as high as (Sydes & Grime 1981; Dzwonko & Gawronski 2002). How- 1800 m a.s.l. (Dimeyeva et al. 2015). ever, few plants occur in sites in deciduous woodlands where litter mass exceeds 200 g mÀ2 (more than c. 10 cm) in the British Isles; there is, however, no correlation between dry II. Habitat mass of tree litter and biomass of M. effusum shoots (Sydes & Grime 1981; Baskin & Baskin 2014). (A) CLIMATIC AND TOPOGRAPHICAL LIMITATIONS Wood Millet often grows on mull soils typically colonized In Great Britain, Wood Millet is mostly confined to areas by an active invertebrate fauna and continuously disturbed by where the annual rainfall is less than 1000 mm (Chandler & burrowing animals, like voles and earthworms (Pearsall 1938; Gregory 1976) and where there are fewer than 160 wet days Staaf, Jonsson & Olsen 1987; Rodwell 1991), leading to a per year (Ratcliffe 1968). The hectads (10-km squares) in quick and deep incorporation of organic material in the soil which M. effusum occurs in Britain are characterized by a profile of Cambisols (Andrianarisoa et al. 2009). In the USA, mean January temperature of 3Á6 °C and a mean July temper- Milium effusum has been found to be an indicator species of ature of 15Á3 °C. The mean annual precipitation in these hec- a moderate invasion by European earthworms of the Lumbri- tads amounts to 928 mm (Hill, Preston & Roy 2004). The cidae family (Bennett 2013). High subsoil water conditions mean annual and July temperatures across its entire European may promote growth of the species, but it only tolerates rare range are 4Á69 °C and 16Á9 °C, respectively (De Frenne et al. flooding events and is absent from wetlands or regularly inun- 2013). dated woods (Grime, Hodgson & Hunt 1988; Van Looy et al. In general, M. effusum is a shade-tolerant species (the 2003; Glaeser & Wulf 2009). Ellenberg species indicator value, as well as the adapted Bri- In Great Britain, M. effusum occurs on various soil types tish value, for light is 4; Ellenberg & Leuschner 2010; Hill, derived from a wide variety of parent material. In the rela- Preston & Roy 2004) mostly confined to sites below a wood- tively warm and dry southern lowlands, it is most common land canopy (see section III). However, in woodlands it is over sedimentary limestones, shales and clays and superficial favoured by thinning that increases direct solar irradiance and deposits like glacial drift. Since leaching at these sites is lim- rainfall (Staaf, Jonsson & Olsen 1987; Falkengren-Grerup & ited to superficial depletion of calcium (Ca) carbonate, soils Tyler 1991). De Frenne et al. (2014) showed that in M. ef- are often characterized by a low surface pH (4Á5 or less), but fusum, biomass production and root:shoot ratios were base-rich conditions with much exchangeable Ca in the lower enhanced under a simulated canopy opening in a common horizons (Rodwell 1991). In areas where the influence of the garden experiment using caryopses (henceforth referred to as parent material is more dominant, however, the profiles can ‘seeds’) sampled across a large part of its European range. be base-rich and calcareous throughout (surface pH between 6 Particularly under high subsoil water conditions, for instance and 7 or more) (Rodwell 1991; Table 1). In the south-eastern at the base of slopes, M. effusum occurs in high-light habitats part of Britain, the species is also associated with the more where it may form extensive communities (Pearsall 1938). base-rich conditions over rendzinas, which are shallow, free- Also in the northern part of its range, M. effusum is most fre- draining, rich in free Ca carbonate and with a high surface quent on flat ground or only gentle slopes with no distinct pH between 7 and 8 (e.g. Adamson 1921; Watt 1934; Avery response to aspect. In the Sheffield region, it was not 1958). Additionally, M. effusum avoids habitats with a high recorded from steep slopes over 60% from horizontal (Grime, proportion of bare soil, at least in the Sheffield region (Grime, Hodgson & Hunt 1988). Hodgson & Hunt 1988), and skeletal habitats, although its

Table 1. Forest ﬂoor (litter) and topsoil (chemical analyses) characteristics of Milium effusum populations spread across the distribution range in Europe (ranked from south to north). Data from De Frenne et al. (2014)

P K Mg Ca Extr. N Elevation Litter thickness Lat. (°N) Long. (°E) Country (m a.s.l.) (cm) pH-KCl C (%) N (%) C:N (mg kgÀ1 dry soil)

43Á711Á7 Italy 1120 5 3Á93Á80Á35 10Á88Á8 110 122 1150 8Á8 47Á48Á5 Switzerland 480 1 3Á93Á80Á33 11Á711Á4 62 104 992 14Á3 47Á325Á5 Romania 637 3Á54Á46Á60Á55 12Á010Á0 166 128 3678 3Á2 48Á02Á8 France 100 1 3Á62Á40Á18 13Á05Á241149410Á7 48Á917Á6 Czech Republic 620 10 3Á63Á90Á37 10Á76Á6 132 86 1386 17Á0 49Á41Á0 France 126 7 3Á23Á50Á24 14Á874Á1 70 16 150 7Á6 49Á82Á2 France 107 6Á53Á84Á40Á37 11Á86Á9 141 148 2631 7Á7 50Á013Á9 Czech Republic 470 0Á53Á53Á90Á32 12Á183Á1 70 30 418 4Á0 50Á05Á1 Belgium 200 7Á75 3Á98Á30Á61 13Á724Á1 108 101 1559 45Á8 50Á18Á3 Germany 230 2Á53Á28Á90Á61 14Á726Á5 167 86 439 8Á2 50Á418Á8 Poland 261 6Á75 3Á63Á20Á21 15Á412Á4 30 16 236 10Á9 50Á83Á7 Belgium 100 3 4Á65Á20Á37 14Á137Á2 199 94 2451 12Á5 50Á88Á7 Germany 240 4 3Á53Á50Á25 13Á88Á4 85 25 178 9Á7 51Á7 À2Á7 UK 190 2Á75 3Á57Á40Á58 12Á830Á9 142 120 564 36Á5 52Á05Á7 Netherlands 49 0Á53Á73Á40Á27 12Á677Á5 35 13 284 19Á2 52Á1 À0Á1UK 752 6Á06Á10Á54 11Á49Á0 258 315 399 8Á7 53Á013Á9 Germany 110 2Á53Á32Á40Á20 12Á459Á9 35 12 146 12Á6 53Á28Á7 Germany 30 3 3Á53Á40Á26 12Á88Á6 57 20 131 18Á6 55Á713Á3 Sweden 65 5 3Á26Á60Á52 12Á720Á3 65 85 185 17Á1 56Á012Á3 Denmark 35 2 3Á52Á90Á25 11Á223Á5 66 34 239 13Á0 58Á917Á2 Sweden 44 0Á25 3Á83Á40Á30 11Á410Á8 152 149 439 2Á0 59Á710Á7 Norway 124 2 3Á96Á00Á48 12Á523Á5 201 137 907 12Á4

Lat.: latitude, Long.: longitude, Extr. N: extractable N measured as ammonium and nitrate (see De Frenne et al. 2014 for a detailed account of the methods). occurrence on rocks is mentioned by Cope & Gray (2009). It water of 3Á1 vs. 4Á7, respectively) (Henrichfreise 1981). On is less frequent on sandstone than on other substrates and the contrary, addition of carbonates (SrCO3 or CaCO3 + occurs on limestone only with sufﬁcient humus (Conert MgCO3; leading to a pH of 3Á7–5Á2) decreased root:shoot 2000). Milium effusum is especially abundant on mull soils ratios under experimental conditions (Falkengren-Grerup & (Staaf, Jonsson & Olsen 1987; Schonhar€ 2001); it occurs on Tyler 1993). Like many other woodland herbs, M. effusum moder (Conert 2000; Schneider et al. 2004), but rarely on has shown a displacement of frequency towards lower topsoil surface mor (Rodwell 1991). In Scandinavia, where the spe- pH during the 20th century, probably mainly as a result of cies is mostly common and widespread, M. effusum is known atmospheric deposition (Falkengren-Grerup 1986). The spe- to be rare in areas with predominantly siliceous bedrock and cies, however, is absent from highly acid and base-deﬁcient acid moraines (Tyler 2002). soils like podzols (Tyler 2002), and does not survive more Wood Millet also occurs on eutric cambisols, luvisols and than a few years when transplanted to strongly acid mor pod- gleysols (Andrianarisoa et al. 2009; Schneider et al. 2004; zols, unless the soil is limed (Staaf 1992). Low soil pH values van Oijen et al. 2005; Orczewska 2009b). It grows well at are usually associated with increasing concentrations of phe- high pH (up to 7–8) and with nitrate as source of inorganic nolic acids and aluminium (Al). Kuiters & Sarink (1986) N, but it is also tolerant of a soil solution pH as low as 3Á7 showed that high concentrations of phenolic acids (10À3 M (measured directly in centrifuged soil solution which is inter- compared to 0, 10À5 and 10À4 M), an important intermediate mediate to pH values measured in water and KCl) and with product in the decomposition of litter material, halved the + ammonium (NH4 ) as the main N source in dystric cambisols growth of M. effusum under experimental conditions. Under (Falkengren-Grerup & Tyler 1993; Falkengren-Grerup & natural conditions M. effusum may occur on dystric cambisols Lakkenborg-Kristensen 1994; Falkengren-Grerup 1995; characterized by concentrations of 15–25 lMAl(0Á015– Falkengren-Grerup et al. 2004). Generally, a typical tolerance 0Á025 mmol LÀ1; Schottelndreier€ et al. 2001). High Al range between pH 3 and 6 is described (Pearsall 1938; Tow- concentrations constrain growth in M. effusum under experi- pasz & Szymska 1983; Fitter & Peat 1994; De Frenne et al. mental conditions (concentrations of 0Á2–8Á0 mmol LÀ1 were 2014). In soils collected in range-wide M. effusum popula- tested by Henrichfreise 1981). In comparison, Falkengren- tions in beech and oak woodlands, the lowest recorded soil Grerup, Quist & Tyler (1995) found maximal total and pH was 3Á2 measured in KCl (Table 1; De Frenne et al. reactive Al concentrations of 0Á1 and 0Á03 mmol LÀ1, respec- 2014). There is experimental evidence that biomass produc- tively, in the soil solution in a southern Swedish beech tion and root length of M. effusum seedlings are reduced wood. They found no negative effects of the Al concentration when growing in acid soils compared to less acid soils (pH in in the soil solution on the percentage cover of M. effusum.

Nevertheless, in solution experiments, 0Á02 mmol LÀ1 reac- Athyrium filix-femina, Luzula pilosa, Maianthemum bifolium tive Al was toxic to Allium ursinum and Bromus benekenii. and Rubus fruticosus (Milio-Fagetum association). However, In southwestern Poland, M. effusum and co-occurring species in recent decades, the frequency of occurrence in resurveyed (e.g. Mercurialis perennis, Stellaria nemorum, Moehringia semi-permanent vegetation plots has increased considerably trinervia and Adoxa moschatellina) preferred sites with high (on average with c. 2Á1% within ancient woodlands across cation exchange capacity, available P and moist mull (Orc- Europe; De Frenne et al. 2013) and M. effusum is now more zewska 2009b). Towards southern Europe, M. effusum occurs widespread than before. It has increased especially in promi- on moist to wet, base-rich to moderately acidic soils with nence in more eutrophic oak-ash and even ash-alder woods mesotrophic humus, mostly on loamy substrates. (Van der Werf 1991; Hermy et al. 2009; Cornelis et al. 2009). This expansion may be related to enhanced disturbance, light intensity and nutrient inputs, and shifts in spe- III. Communities cies composition as a consequence of N deposition In lowlands, Milium effusum is primarily a shade-tolerant spe- (section VI), pushing the species towards more rich and cies typical of the herb layer of deciduous and mixed wood- more humid soils. land (both under closed canopies as well as in gaps and In central and eastern Europe, M. effusum occupies a wide clearings) but it also occurs in scrub and hedgerows (Roweck range of deciduous and mixed forests and shaded banks of 1981; Grime, Hodgson & Hunt 1988; Rodwell 1991; Sell & different moisture levels, in lowlands, uplands and mountains. Murell 1996; Jurij & Rozenbergar 2001; Schmidt et al. 2003; Although predominantly recorded in oak-hornbeam and beech Van Landuyt et al. 2006; Cope & Gray 2009; Wehling & communities, it is also present in a variety of riverside com- Diekmann 2009; Online Atlas of the British & Irish Flora munities, in wet alder forests, mountain sycamore forests on 2015). At higher altitudes, M. effusum can be a component of rocky, steep slopes, and even in fir and spruce communities, tall herbaceous plant communities, scrub in forest clearings and the dwarf pine belt in mountains (Chytry & Rafajova and floodplain forests with sparse trees (Hardtke & Ihl 2000; 2003; Kazcki & Sliwi nski 2012). Glaeser & Wulf 2009; Mossberg & Stenberg 2012; Dimeyeva Towards southern Europe, the species occurs primarily in et al. 2015). Figure 3 gives an impression of the typical habi- communities of the Fagetalia sylvaticae phytosociological tats and communities of the species. order, but it can also be found in clear-cuts and clearings In the British Isles, M. effusum is part of a number of wood- (communities of the Epilobietea angustifolii class), as well as land communities especially dominated by Fraxinus excelsior, in tall herbaceous mountain vegetation (communities of the Fagus sylvatica and Quercus robur. The species is a com- Adenostylion alliariae alliance). mon component of the Fraxinus excelsior–Acer campestre– Mercurialis perennis (W8), the Fraxinus excelsior–Sorbus IV. Response to biotic factors aucuparia–Mercurialis perennis (W9), the Quercus robur– Pteridium aquilinum–Rubus fruticosus (W10), the Fagus In several of its closed-canopy habitats (e.g. in some Milio- sylvatica–Mercurialis perennis (W12), and the Fagus sylvat- Fagetum woodlands; Fig. 3c–e), widely spaced plants may ica–Rubus fruticosus (W14) woodland types according to the suffer relatively low levels of intraspecific above-ground com- national vegetation classification system of Rodwell (1991). petition for light and below-ground competition for nutrients Wood Millet usually covers a small proportion of the ground in and water within the herbaceous layer. Nonetheless, in other, all these communities, and flowers only where canopy shade is more open habitats (e.g. post-agricultural forests or mountain- not too dense. Lothian records show predominance in mixed, as ous, open forests) where M. effusum occurs, the herbaceous opposed to deciduous woodlands (Edinburgh Biodiversity layer can be dense (Fig. 3a, b and f). Action Plan 2010). Clones of M. effusum differ considerably in their rhizome In Fennoscandia, M. effusum occurs in a wide range of morphology, depending on the level of competition with other meso- and eutrophic broadleaved and mixed woodlands, in herb-layer species. Strongly branched rhizomes pointing in all eutrophic spruce forests, but also on riverbanks and in lake- directions were observed in conditions with high levels of shore thickets as well as in wooded hay meadows, subalpine competition (in a Polish wood with dense herb-layer cover, and subarctic mountain birch forests and alpine tall-herb with a high density of tussocks of Carex brizoides), whereas meadows (Diekmann 1994; Rydin, Snoeijs & Diekmann rhizomes with linear, unbranched architecture developed in 1999; Tyler 2002). Canopy opening usually increases growth conditions with lower competition levels (in a site in Poland and flowering and the species is sensitive to grazing and with lower plant densities within the herb layer and lower mowing and has become more widespread during the 20th interspecific competition) (Towpasz & Szymska 1983). century after abandonment of traditionally managed wooded The competitive ability of M. effusum has also been shown meadows and pastures (Tyler et al. 2007; Jonsell 2010). to change from north to south. De Frenne et al. (2011c) sam- In western Europe, M. effusum used to occur in a rather pled 44 M. effusum populations along a 2300-km latitudinal limited range of mesotrophic broadleaved deciduous wood- gradient from northern France to northern Sweden and deter- lands (oak-beech woods) on moderate acid and relatively dry mined the position of these in the leaf-height-seed ecology loamy soils where it is often accompanied by species such strategy scheme [a combination of three ecologically impor- as Oxalis acetosella, Anemone nemorosa, Stellaria holostea, tant traits: specific leaf area (SLA), seed mass and plant

(a) (b)

(e) (f)

Fig. 3. Some of the typical habitats and communities of Milium effusum: (a) storm gap in The Mens, an ancient woodland in West Sussex, southern England, (b) in a subarctic birch forest at latitude 68°N near Abisko, northern Sweden, (c) in a beech wood, Brakelbos, near Brakel, Belgium, (d) in a beech-hornbeam wood, Forêt de Fremontiers, near Amiens, northern France, (e) in a beech wood at c. 700 m above sea level in the Vercors mountains in the Drome,^ near Die, southern France, and (f) in an overgrown ride in Great Wood in Wiltshire, southern England (photos: Simon Smart, Pieter De Frenne & Guillaume Decocq). height]. The species displayed a significant 4Á3% increase in nutrient-rich soils. In an artificial canopy gap experiment plant height (corresponding to c. 3 cm) with every degree where gaps were deliberately created [by removing clumps of northward shift. This translates to an almost doubling of plant low quality hardwood species from hemlock (Tsuga canaden- height between the southernmost (average 82Á9 Æ 2Á4 cm) sis) stands in Michigan, USA], and combined with exclosures and northernmost populations (average 148Á7 Æ 1Á8 cm; to assess deer browsing effects, M. effusum did not respond Fig. 4a). Neither seed mass nor SLA showed a significant lat- significantly in terms of cover frequency to the treatments itudinal cline. This increase in plant height in northern com- after 5 years (Holmes & Webster 2011). pared to southern populations was also found in a common garden experiment suggesting that this pattern is genotypic in V. Response to environment origin (De Frenne et al. 2011b). Populations of M. effusum are usually favoured by thinning (A) GREGARIOUSNESS and/or clear-cutting with extensive flowering and seed production under such situations (see sections II and III). Neverthe- Milium effusum tends to occur as solitary individuals. less, in a resurvey of woodlands in southern Belgium However, small patches of hundreds of individuals several converted from traditional coppice-with-standards to high for- square metres in size also occur, especially in high-light envi- est management where dominant canopy cover shifted from ronments such as woodland gaps. Regeneration from seed is the shrub to the tree layer in all conversion types, Van Calster the most important means of population persistence and et al. (2008) found the cover of M. effusum not to show any spread but the species also exhibits clonal growth (Tyler significant changes over time on both nutrient-poor and 2002; section VI.C).

Latitude (°) 49·8 50·9 52·6 53·3 55·6 59·0 63·8 68·4 Leaf C:N ratio Plant height (cm) 10 15 20 25 30 35 40 45 60 80 100 120 140 160 45 50 55 60 65 70 45 50 55 60 65 70 Latitude (°N) Latitude (°N) ) –1 ) –1 Leaf Ca−concentration (mg kg Leaf P−concentration (mg kg 2000 4000 6000 8000 10 000 12 000 1000 1500 2000 2500 3000 3500 0 2000 4000 6000 8000 10 000 1·0 1·5 2·0 2·5 3·0 3·5 4·0 Soil Ca−concentration (mg kg–1) Leaf N−concentration (%)

Fig. 4. Plant height and foliar nutrient concentrations of Milium effusum populations sampled in eight regions along a latitudinal gradient from northern France (temperate) to northern Sweden (subarctic) (n = 6 populations per latitude, except in Stockholm, latitude 59Á0°N, where n = 2). The colour of the dots denotes the latitude of origin, from south (red) to north (blue). Data from De Frenne et al. (2011c) and unpublished results.

(B) PERFORMANCE IN VARIOUS HABITATS traits (including plant height, seed mass, seed bank persis- The status of M. effusum as ancient woodland indicator is tence and the dispersal syndrome). They did not classify ambiguous. Like many other temperate forest understorey M. effusum as an ancient woodland indicator species across plants, it is affected by legacies of the former land use, and is the UK based on these traits. mostly limited to ancient woodland in the British Isles and In the last few decades, its establishment in more recent several western European countries such as Belgium (Peter- and/or disturbed forests seems to have increased in some ken 1981; Peterken & Game 1984; Hermy et al. 1999; Ver- regions, probably because of its epi- and endozoochorous dis- heyen et al. 2003; De Frenne et al. 2011a; but see Kimberley persal by large mammals (Graae 2002; Heinken & Raud- et al. 2013). Peterken (1981) and Kirby (2006) stressed a nitschka 2002; Oheimb et al. 2005; Delatte & Chabrerie high afﬁnity with ancient woodland for this species, and Rose 2008) and the parallel increase in the population densities of (1999) mentioned it as indicator of ancient woodland for these mammals. The species is, for instance, known to colo- southern Britain. However, Kimberley et al. (2013) applied a nize secondary, post-agricultural forests relatively rapidly in classiﬁcation tree analysis to a plant trait database to assess southern Sweden (Brunet et al. 2012) and Denmark (Graae the extent to which ancient woodland species can be sepa- 2000). Although in Poland it is listed as an ancient woodland rated from other woodland plants based on their life-history indicator species (Dzwonko & Loster 2001), it also occurs in

© 2017 The Authors. Journal of Ecology © 2017 British Ecological Society, Journal of Ecology, 105, 839–858 Milium effusum 847 sites disturbed by felling, and colonizes nitrophilous, recently Kucherov (2003) discussed a latitudinal cline in the ecolog- post-agricultural forests. It appears to be a species without a ical niche and ability of M. effusum to persist under tree- clear preference for ancient woodlands in this region canopy shade. He described a shift in the species’ occurrences (Orczewska 2009a,b; Kazcki & Sliwi nski 2012). from productive valley forest to semi-open, less productive, In a meta-analysis of recovery rates of post-agricultural mountain forest, from southern to northern Russia. forests across Europe, a mean recovery rate of À0Á71 was calculated as the log-response ratio of frequency in post- (C) EFFECT OF FROST, DROUGHT, ETC agricultural forests over ancient woodlands across Europe. Negative values indicate a higher afﬁnity to ancient than to Drought stress is unlikely to occur frequently in its typical post-agricultural forest. In other words, the frequency of habitats, at least in woodlands on relatively moist soils, which occurrence in ancient woods was c. 2Á0 times the frequency could explain the relatively few large metaxylem vessels in of occurrence in post-agricultural forests. Wood Millet was roots of Wood Millet (Wahl & Ryser 2000; Fig. 5). Al-Mufti ranked intermediate, i.e. as the 36th slowest to recover species et al. (1977) report frost damage to overwintering shoots of out of 90 forest understorey plants (De Frenne et al. 2011a). M. effusum. Nevertheless, this does not seem to affect its dis- Mean colonization rates from ancient woodlands into adja- tribution negatively in, for instance, the northern of its distri- cent post-agricultural forests are region-dependent but range bution range or at high elevations (>2000 m a.s.l.) in from 0Á4–2Á78 m yearÀ1 in southern Sweden (Brunet & von mountains, possibly due to the insulating properties of the Oheimb 1998; Brunet et al. 2012) to 0Á91–1Á05 m yearÀ1 in typical thick litter layer and/or snow where it occurs. south-western Poland (Orczewska 2009a) making this species an intermediate to relatively fast colonizer compared to other VI. Structure and physiology forest understorey species (Bossuyt, Hermy & Deckers 1999; Brunet et al. 2012). Addition of M. effusum seeds to subplots (A) MORPHOLOGY in ancient and post-agricultural forests in Denmark resulted in a spectacular increase of 77% occupancy (which was the The area of the green leaves per plant averages c. 500 mm2 highest of the eight tested species). The increase was highest but ranges between 250 and 2000 mm2 (Gr€aff, Moser & in the post-agricultural forests and is a strong experimental Heiselmayer 2015). Leaves have an average life span of demonstration of seed-limited recruitment (Graae, Hansen & 52 days (Ryser & Urbas 2000). Based on 19 mg dry mass Sunde 2004). for each of 27 harvested individuals, Ryser & Wahl (2001) À In a high-light environment, M. effusum has a mean relative found that M. effusum has a SLA of 38Á8mm2 mg 1, a leaf À1 À1 growth rate of 0Á058 g g day , which is relatively low area ratio (the area of CO2 assimilating surface per plant dry À compared to other grasses (Ryser & Wahl 2001; see sec- biomass) of 17Á2m2 kg 1 and contains 0Á226 g leaf dry mat- tion VI.E). De Frenne et al. (2011c) found that M. effusum ter per g fresh leaf. De Frenne et al. (2011c) reported a mean increased in plant height towards the north (cf. section IV) and plants were also taller under a more open canopy. There was no relationship between the latitude of origin and the number of growing degree-hours and the seed mass of M. effusum. Enhanced plant size (height and biomass) similarly occurred when Wood Millet was transplanted into soils coming from colder sites than the seed origin. In a common garden experiment in a glasshouse, De Frenne et al. (2014) assessed growth responses to non-local soils by planting seeds in soil sampled in 22 ancient woodland sites across a 1600- km latitudinal gradient and transferred to the glasshouse. The performance of M. effusum increased when transplanted into soils from currently cooler areas and decreased in transloca- tions to soils from warmer sites. These growth responses were most likely related to differences in experienced N deposition rates, soil pH, and soil K and Ca concentrations, and occurrences of mycorrhiza and fungal pathogens. In the same common garden glasshouse experiment, direct experimental warming also increased the performance and seedling emergence rates of M. effusum. The predicted climatic changes thus have the potential to signiﬁcantly improve growth and accelerate seedling emergence of this species, not only by Fig. 5. Root tissue structure of Milium effusum. Image showing seg- ments of a root cross-section stained with Toluidine Blue. Co, cortex; directly affecting plant performance, but also indirectly En, endodermis; MX, large metaxylem vessel; St, stele. Bar, 50 lm. through positive plant–soil feedbacks during migration (De Photo by Peter Ryser. Reproduced with permission. See also Wahl & Frenne et al. 2012; Maes et al. 2014). Ryser (2000).

SLA of 33Á1 Æ 1Á05 mm2 mgÀ1 (SE) across its range. Unlike M. effusum saw great receptor profit peaking at 5–10% of the other grasses of shaded woodland environments, M. effusum incident photon flux density. Clonal growth in M. effusum is has stomata on both the upper and lower surfaces of the leaf thus an effective foraging mechanism improving the use of (Bary 1884; Conert et al. 1998), with a density of 103 stom- the limited availability of light on the forest floor (Gr€aff, ata mmÀ2 recorded on the upper (adaxial) leaf surface (Fitter Moser & Heiselmayer 2015). & Peat 1994). We found no data on abaxial stomatal densities. Wood Millet’s canopy height (maximal height of the (B) MYCORRHIZA panicle) averages 109 Æ 3Á6 cm (SE) throughout its European distribution range, with substantial latitudinal variation. Popu- Although the roots of M. effusum have been found to be fre- lations in northern France reached an average height of c. quently colonized with vesicles of arbuscular mycorrhizal 80 cm whereas individuals in northern Sweden attained a (AM) fungi (Dominik & Boullard 1961; Krjuger 1961; mean height of 148 cm (maximum of 187 cm) (De Frenne Grime, Hodgson & Hunt 1988; Mayr & Godoy 1990; Tur- et al. 2011c; see section VI). nau, Mitka & Kedzierska 1992; Maes et al. 2014), several The adventitious root system arises from the stem base. published records have demonstrated the absence of mycor- The species also possesses rhizomes covered in densely, rhizas (Dominik & Wojciechowska 1961; Michelsen et al. short-haired scales ending in a single sprouting bud (Conert 1998). Such differences in mycorrhizal status between studies et al. 1998) from which new above-ground shoots and roots can be ascribed to environmental settings. First, harsh cli- may be formed (Jonasson & Widerberg 1988). This allows matic conditions in arctic areas have been suggested to limit the species to form large stands of loosely tufted individuals. AM colonization in M. effusum even when potential host In a comparative root anatomical study of 19 grasses, Wahl plants are present (Michelsen et al. 1998; Olsson, Eriksen & & Ryser (2000) found, based on samples from seven individ- Dahlberg 2004). Second, fertilization (e.g. from atmospheric uals, that M. effusum has very high root tissue mass densities N deposition or from past agricultural P fertilization) may (0Á245 Æ 0Á017 mg mmÀ3) while having relatively small pro- decrease the occurrence and colonization of M. effusum roots portions of root stele (0Á023 Æ 0Á004 mm2), due to a dense with AM fungi. Despite the complete loss of AM fungi in root cortex (Fig. 5). Similarly, M. effusum roots contained control plots in response to fertilization with each of exceptionally few xylem vessels (1Á14 Æ 0Á14 for a given 200 kg haÀ1 N, P and K, the performance and ground cover root diameter), compared to 3Á86 Æ 0Á55 in another shade-tol- of M. effusum was enhanced in fertilized plots (Turnau, erant grass, Poa nemoralis. P. nemoralis differs in this regard Mitka & Kedzierska 1992). However, contrary to the study from other, non-shade adapted Poa spp. such as P. trivialis of Turnau, Mitka & Kedzierska (1992), no effects of N addi- and P. pratensis (having 1Á38 Æ 0Á26 and 1Á88 Æ 0Á23 xylem tion on mycorrhizal colonization of M. effusum were found vessels, respectively, for a given root diameter). Additional by Maes et al. (2014). Finally, in a common garden trans- anatomical root traits such as root cross-sectional area plant experiment, a higher incidence of arbuscular mycor- (0Á157 Æ 0Á03 mm2), stele cell size (70Á2 Æ 8Á79 lm2), stele rhizas was observed in populations that were replanted at cell number (184 Æ 34) or proportion of xylem (total xylem their home site (local accessions) than in foreign prove- in root cross-sectional area: 0Á72 Æ 0Á06%) were similar to nances, suggesting adaptation to the local AM fungi (Maes the other grass species although they had lower root tissue et al. 2014). mass densities. This exceptional trait combination in the roots of M. effusum, combined with its slow growth, may be (C) PERENNATION: REPRODUCTION explained by the environment of its preferred forest habitat where drought is unlikely to occur, but shade may limit Milium effusum is a hemicryptophyte, overwintering by com- growth (Wahl & Ryser 2000; cf. also section V). bining an evergreen canopy with rhizomes, immature tillers Gr€aff, Moser & Heiselmayer (2015) assessed whether plant and subterranean buds (Al-Mufti et al. 1977; Jonasson & architecture affected the amount of radiation reflected by Widerberg 1988). Vegetative reproduction occurs by means neighbouring plants. Light transmittance through M. effusum of the short rhizomes, with a maximum annual clonal spread À leaves was 2Á49 Æ 3Á22& (SD) of incoming PAR. This was of c. 20 cm year 1 (Brunet & von Oheimb 1998). Growth comparatively high compared to the other woodland plants and vegetative expansion in M. effusum occur in four distinct studied (e.g. Stellaria holostea, Lamium galeobdolon and phases, closely related to the light availability through the tree Galium odoratum). Leaf reflectance was significantly higher canopy (Jonasson & Widerberg 1988): (i) rapid growth of at 9Á77 Æ 1Á23%. Milium effusum performed poorly as a radi- overwintered tillers and tiller primordia until canopy leaf ation donor with a mean photon flux density of 0Á12 Æ 1Á00 flushing, (ii) an early-summer phase characterized by flower- (SD) mmol mÀ2 dayÀ1. This low donor radiation capacity is ing, no leaf growth but formation of new tiller primordia, (iii) likely due to M. effusum’s plant architecture which leads to a a late-summer/early autumn phase after canopy tree leaf shed- significant degree of self-shading because of its relatively ding with M. effusum tillers developing from previously large leaf surface area (Gr€aff, Moser & Heiselmayer 2015). formed primordia, with expanding stem bases and rhizomes, Nonetheless, M. effusum’s architecture and donor radiation and ultimately the formation of new tiller primordia and (iv) facilitated light absorption in neighbouring plants of Brachy- in late autumn, senescence of some of the above-ground podium sylvaticum. Similarly, connected clonal ramets of shoots and winter dormancy.

The short rhizomes, combined with the observation that À30Á4 13C& (Smith & Brown 1973). Milium effusum does ramets sampled a few metres apart in M. effusum stands not have Kranz anatomy (Smith & Brown 1973). In a high- belonged to different genets, led Tyler (2002) to conclude that light environment, M. effusum has a mean net assimilation the main mode of reproduction, spread and persistence is rate of 3Á4gmÀ2 dayÀ1, which is relatively low compared to through regeneration from seed rather than through vegetative other grasses (Ryser & Wahl 2001). perennation or clonal reproduction, except in closed stands. Enhanced atmospheric inputs of N together with climate However, studies on the structure and dynamics of popula- warming have probably been responsible for an increase in tions in natural oak-hornbeam and mixed pine-oak forests in the frequency of M. effusum across the European continent southern Poland revealed that vegetative growth via rhizomes (see section III). Pollution by atmospheric N inputs has also and fragmentation of parent-plant individuals was predomi- resulted in a displacement towards lower topsoil pH during nant. Regeneration from seeds became the predominant type the 20th century (Falkengren-Grerup 1986). Yet, in a com- of reproduction when M. effusum colonized open spaces in mon garden experiment with a range-wide of provenances forest gaps and clearings (Towpasz & Szymska 1983). performed in Belgium, the species did not respond to N addi- À1 While Wilson & Thompson (1989) estimated reproductive tion of 62Á5kgNha alone (applied as NH4NO3). Only allocation (proportion of above-ground biomass allocated to seed mass was significantly increased as a result of N addi- reproductive structures) in M. effusum to be only 0Á2% of the tion in sown plants, but this was not the case in plants that above-ground biomass for an English provenance (sampled in were transplanted by means of rhizomes. Nevertheless, inter- Devon/southeast Cornwall), range-wide data from a common active effects between warming temperatures (simulated by garden experiment suggest a mean biomass allocation of southward transplantation along a latitudinal gradient) and N 8Á4% to the seeds and 9Á8% to the inflorescences (i.e. sum of addition were found; N addition led to increased biomass 18Á2% reproductive allocation) (De Frenne et al. 2011b). growth only under the coldest temperatures (Maes et al. 2014). The total N concentration in M. effusum leaves in forest (D) CHROMOSOMES tundra in northern Sweden was 1Á97 Æ 0Á07% (SE) (Michel- Milium effusum has almost exclusively been found to have sen et al. 1998), whereas the N concentration varied between the chromosome number 2n = 28 in populations across North 0Á94 and 4Á36% (mean of 3Á07 Æ 0Á15%) along a latitudinal America, Europe, Russia and Japan (Bennett & Thomas gradient from temperate France to subarctic Sweden (Fig. 4b–d). 1991; Bennett & Bennett 1992), although a single uncon- Jonasson & Widerberg (1988) noticed a strong seasonal pat- firmed chromosome count of 2n = 14 has also been reported tern in leaf N concentrations from 3Á64 Æ 0Á74% (SE) in the (Sokolovskaya & Strelkova 1960). The base chromosome spring (April) to 0Á85 Æ 0Á17% in the summer (August). The number is 7. Based on chromosomal banding patterns, the seeds contain 2Á80% N expressed per dry weight (Jensen species has been suggested to be an ancient allotetraploid, but 1982). it shows diploid meiotic behaviour (bivalent-forming) (Ben- Falkengren-Grerup & Lakkenborg-Kristensen (1994) per- nett & Thomas 1991) and allozyme diversity is consistent formed two glasshouse experiments to establish the relation- + À with a diploid mode of inheritance (Tyler 2002). The tetra- ship between growth and N uptake as either NH4 or NO3 ploid origin is found throughout its natural distribution range, in Wood Millet. Neither total biomass nor the root:shoot ratio from Britain to the rest of Europe (Gadella & Kliphuis 1963; responded to any of the seven treatments in the first experi- Skalinska, Pognan & Czapik 1978; Vachova 1978; Bennett & ment in which nutrient solutions with various combinations + À Thomas 1991), North America (Bowden 1960) and Asia and concentrations of NH4 and NO3 were applied to adult (Tateoka 1957). The variation in chromosome number in the M. effusum plants grown from seed. In a follow-up experi- + + À entire genus Milium can be attributed to allopolyploidy and ment, NH4 uptake from a mixed solution of NH4 and NO3 À multiple hybridization events during speciation (Bennett & was significantly higher than the NO3 uptake. The uptake of + Thomas 1991). The DNA amount within natural M. effusum NH4 and NO3 was also significantly higher when applied in populations is reasonably consistent among different conti- isolation compared to uptake of each N form when available nents, with a mean nuclear 2C DNA amount of 7Á88 pg (Ben- in a mixture. Despite being able to grow on very acidic soils, nett & Bennett 1992), although Grime, Hodgson & Hunt growth of M. effusum did not display any preference towards (1988) report a nuclear DNA amount of 9Á4 pg. Bennett & a specific N form, perhaps due to its wide soil pH range (sec- Bennett (1992) noted a higher 2C value (mean of 9Á92 pg) in tion II.B). Nevertheless, the hypothesis that species which can À ex situ cultivated individuals growing in botanic gardens occur on relatively acidic soils are not dependent on NO3 + which they suggest is the result of the environmental differ- and can grow well with NH4 as sole N source was supported ences between in situ (wild) and ex situ (cultivated) popula- in the patterns observed in M. effusum. tions and the effects on nuclear DNA quantity. The physiological response to fertilization and shading of M. effusum collected from birch forest in northern Sweden was investigated in detail by Eckstein & Karlsson (2001). (E) PHYSIOLOGICAL DATA Individuals transplanted in pots were subjected to two facto- 12 13 Milium effusum uses the C3 pathway to fixCO2; the C /C rial manipulations of light (ambient vs. 64% light reduction) ratio was lower than À22 13C& (Waller & Lewis 1979), i.e. and N (1 vs. 10 g N mÀ1 yearÀ2) for two growing seasons.

All above-ground biomass was harvested on three occasions the species can occur on very acid soils (although these plants during the growing season, weighed and chemically analysed. might be distinct, acid-tolerant genotypes; see also sec- Across treatments, M. effusum had an average N pool of tion II.B), and concentrations used in the experiment were 6 mmol N per plant [based on chemical analyses of leaves, similar to concentrations in woodland soils. stems (including leaf sheaths), inflorescences, roots and rhizomes] and net primary productivity averaged at 7Á3 g dry (F) BIOCHEMICAL DATA matter per plant per year. The large N pool in M. effusum led to a strong increase in net primary production of M. effusum The glucosylceramides of M. effusum leaves that are involved (from 2Á1–3Á1to11Á9–12Á0 g dry matter per plant per year) in the cryostability of plasma membranes and thus in cold under both light treatments in response to N fertilization. Sim- acclimation, contain relatively high amounts of unsaturated ilar responses to N fertilization were noted for losses in N hydroxy fatty acids (4-hydroxy-8-sphingenines: t18:1(8Z) and (from 0Á5–1Á3to3Á9–6Á1 mmol N per plant per year) and lit- t18:1(8E)) but lower amounts of 2-hydroxy arachidic acid ter production (0Á52–0Á57 to 4Á18–4Á62 g dry matter per plant (20h:0) compared to other Poaceae species (Watanabe & Imai per year). In a glasshouse experiment at two temperatures (av- 2011). Wood Millet foliage also contains coumarin (a ben- erage temperatures of 11Á6 °C and 15Á3 °C), De Frenne et al. zopyrone) (Mossberg & Stenberg 2012) and flavonoids of the (2014) found a ten-fold decline in above-ground biomass flavonol family (quercetin 3-O-rutinoside, quercetin 3-O- from ambient light to a reduction in light by 95% with shade glucoside, kaempferol 3-O-rutinoside and kaempferol 3-O- cloth (from 26Á3mgto2Á8 mg per individual). Below-ground glucoside), considered to be a primitive feature, instead of the biomass declined even further, by a factor of 16 (from 38Á0 flavone family, which is commonly found in other Poaceae to 2Á4 mg). (Moulton & Whittle 1989). In a study on nutrient allocation, Jonasson & Widerberg (1988) demonstrated significant seasonal fluctuations in VII. Phenology nutrient content (N, Ca, P, K and Mg) in relation to light as a determinant of growth dynamics and nutrient use in The species is evergreen, with the foliage remaining visible M. effusum. Rapid spring growth translated into high mobi- above-ground during winter. Shoot biomass increases in lization of K, Ca and Mg in the leaves as well as into spring prior to tree-leaf flushing and there is clear seasonal- high leaf concentrations of N and P and a strong above- ity in the amount of above-ground biomass. The species ground biomass increase. The large fluxes of light available reaches its peak biomass during late spring and early sum- prior to tree-leaf flushing coincided with this pattern and mer (Al-Mufti et al. 1977; Towpasz & Szymska 1983; allowed large quantities of nutrients to be used to produce Tyler 2002). For instance, winter biomass in December was À leaves with high N content and high photosynthetic rates, <1 g dry matter m 2 in a southern Yorkshire wood, while achieving high carbon return on invested N. When light peak summer biomass (in June) amounted to c. 8 g dry was scarce in the mid-season, N and P were withdrawn matter mÀ2 (Al-Mufti et al. 1977). The growth of overwin- from the leaves to reduce the respiratory cost of high N tering shoots begins in early spring (in Sweden in April, concentrations. When these nutrients were allocated to root earlier further south) (Jonasson & Widerberg 1988) and the growth, autumn tillers can benefit from the resulting growth of the panicle starts in April–May. In 2008, more increased root growth and potential uptake of nutrients late than 10% of the shoots in large populations in woods in the season such that the species can maintain high pho- across Europe were flowering (defined as the moment when tosynthesis rates in autumn tillers. The nutrient concentra- the anthers were visible) on 1 May (Belgium), 9 May tions in autumn tillers therefore differ clearly from spring (northern France), 10 May (north-western Germany) and 22 tillers. Finally, Jonasson & Widerberg (1988) concluded May (southern Sweden). Seed maturation usually occurs that nutrient leaching in M. effusum was negligible in living from June (UK, France, Belgium and The Netherlands) and dead leaves, except for K, which quickly leached from until August (northern Scandinavia). The seeds are dis- dead leaves. Carbohydrates may be leached in significant persed nearly instantaneously after maturity (predominantly amounts, but only from the youngest living leaves. barochorous and epizoochorous dispersal) and can germinate Although M. effusum occurs along a wide soil acidity gra- immediately when shed (see section VIII). Virtually all new dient, it does not seem to use root exudates to detoxify Al in seedlings from European populations start to flower only acid soils. Schottelndreier€ et al. (2001) reached this conclu- two growing seasons after sowing, although, very infre- sion based on a hydroponic experiment in which adult plants quently (c. 1% of individuals tested), some individuals grown from seeds were exposed to three different Al concen- flower and set seed in the first year (De Frenne et al. trations (0, 25 and 75 lM) at a pH of 4. M. effusum did not 2011b). Jonasson & Widerberg (1988) noticed a second exude significant amounts of oxalic acid or citric acid above-ground biomass peak in September in a wood north (<0Á01 lmol hÀ1 gÀ1 root dry mass) in relation to elevated of Goteborg€ on the Swedish west coast, but this peak was Al concentrations, but it did exude small concentrations of absent in the UK population (Al-Mufti et al. 1977). Jonas- malic acid, though only at the highest Al treatment (mean of son & Widerberg (1988) relate this second peak to the 0Á025 Æ 0Á053 lmol hÀ1 gÀ1 root dry mass). These findings growth of immature tillers that coincides with the shedding for M. effusum and other woodland grasses were surprising as of the tree-canopy leaves.

(endozoochorous) seeds (von Oheimb et al. 2005). Deposition VIII. Floral and seed characters of dung by European bison (Bison bonasus L.) in the Polish Bialowieza_ forests has been demonstrated to increase the seed (A) FLORAL BIOLOGY bank of M. effusum (Jaroszewicz & Piroznikow_ 2008; Jaros- Milium effusum has green hermaphroditic, feebly protogy- zewicz 2013). The relatively abundant seed production in nous, wind-pollinated flowers (Grime, Hodgson & Hunt combination with regular epizoochorous and endozoochorous 1988). seed dispersal and highly germinable seeds (section VIII.D) may partly explain the rapid colonization of recently estab- lished forest patches by M. effusum in some regions such as (B) HYBRIDS Denmark and southern Sweden (Graae 2000; Graae, Sunde & No hybrids have been recognized. Fritzboger 2003; Brunet et al. 2012; see section V.B). Com- pared to 42 other woodland herbs, M. effusum had the fourth highest dispersal potential based on a principal components (C) SEED PRODUCTION AND DISPERSAL analysis of four life-history traits (dispersal distance, diaspore Vegetative shoots start to form inflorescences in their second mass, clonal spread and plant height) that were strongly year or later (Towpasz & Szymska 1983; Jonasson & Wider- related to colonization rates (Brunet et al. 2012). berg 1988; Wilson & Thompson 1989). Seed production then The seeds stored in the seed bank offer an additional mode generally recurs annually (Tyler 2002). On average, of delayed reproduction (Plue et al. 2013). Seed bank density 68Á0 Æ 28Á7% (SD) of all M. effusum shoots present in a of M. effusum was found to range from 37 to 3212 ger- population flower annually and produce seeds (De Frenne minable seeds mÀ2 in deciduous woodlands across western et al. 2011c). Each reproductive shoot produces 40–700 seeds Europe (Plue et al. 2013), and from 570 to 4958 seeds mÀ2 with an air-dry mass of 0Á5–1Á7 mg each (De Frenne et al. in deciduous and mixed pine-oak forests in Poland (Towpasz 2011b,c). In common garden experiments, transplants from & Szymska 1983). Most of the seeds are situated in the upper across the distribution range produced on average 10 cm topsoil layer (Kjellsson 1992; Bossuyt, Heyn & Hermy 82Á6 Æ 46Á8 (SD) seeds per panicle (De Frenne et al. 2011b). 2002). The seed accumulation index (an index of seed long- In a study by Plue et al. (2013), seed production per shoot evity), calculated as the ratio of all plots in deciduous wood- was significantly related to the population size (combined lands across western Europe where the species was solely effect of species density, species percentage cover, the num- present in the seed bank over those where the species was ber of inflorescences and the total number of shoots in the present in the seed bank, vegetation or both, amounts to 0Á03 population, which were all correlated) but not to the soil in M. effusum (Plue et al. 2013). Thus, M. effusum occurs in moisture, soil pH, temperature variables or to the latitude of the seed bank only when parent individuals are present. This the sampled site. Seed production was, however, positively implies that the species possesses relatively limited seed long- correlated with distance to the forest edge suggesting an effect evity (mean of c. 5 years), rendering it heavily reliant upon of microclimate (light, temperature). Seed mass has been regular seed inputs to maintain a seed bank (Plue et al. found to show little variation with latitude (De Frenne et al. 2013). 2011c). However, when plants were transplanted to more southern sites, seed mass decreased, which was interpreted as (D) VIABILITY OF SEEDS: GERMINATION light limitation under denser canopies in the south (De Frenne et al. 2011c). Positive effects of light on seed production Freshly shed seeds of M. effusum from temperate regions usu- were also reported by Towpasz & Szymska (1983) who men- ally have high germination of between 70% and 100% when tion 261 Æ 12Á0 (SD) seeds per panicle in populations which sown onto agar pads, in petri dishes on filter paper, or in for- developed in mixed pine-oak forest, where the illumination est or potting soil (Towpasz & Szymska 1983; Thompson level reached 23% of full light, and 190 Æ 8Á2 (SD) seeds 1989; Staaf 1992; Falkengren-Grerup & Tyler 1993; De per panicle in oak-hornbeam woodlands with 6% of light pen- Frenne et al. 2011b, 2012, 2014). However, germination was etrating to the forest floor. much lower (c. 20%) for freshly shed seeds sampled in sub- Most of the smooth seeds of M. effusum fall to the ground arctic, northern populations (De Frenne et al. 2012). Accord- close to the mother plant (barochory). There are no specific ing to a study conducted in southern Poland, germination of adaptations for wind dispersal. However, because of its tall seeds and establishment of seedlings under natural conditions stature and easy seed release (at maturity, although the spike- are much lower than in laboratory experiments (c. 3% of all lets remain firmly attached to the panicle, the seeds are easily seeds produced; Towpasz & Szymska 1983). Based on a dislodged), mature seeds may be dispersed in the coats of modelling exercise, it has been suggested that seeds germinate mammals. Extensive epizoochorous dispersal of Wood Millet in the same year as they are shed for Wood Millet popula- seeds has been demonstrated experimentally in the coat of a tions originating from lower latitudes (Central Europe), while dog over distances as far as 600 m (Graae 2002). Seeds of seeds from populations at higher latitudes in Scandinavia ger- the species collected from dung samples of red deer (Cervus minate in the following spring, as a result of seed dormancy elaphus L.) have been successfully germinated, indicating a (Thompson 1980). However, in an empirical study, De Frenne potential of long-distance dispersal of ingested et al. (2012) did not detect a latitudinal pattern in mean

© 2017 The Authors. Journal of Ecology © 2017 British Ecological Society, Journal of Ecology, 105, 839–858 852 P. De Frenne et al. germination time between France and northern Sweden, with in Poland showed that M. effusum is eaten by red deer an average of 20 weeks between sowing in potting soil and (Cervus elaphus) and roe deer (Capreolus capreolus L.) seedling emergence. In this experiment, seeds were exposed (Gezbczynska 1980) as well as by bank voles (Myodes glareo- in incubators to a seasonal cycle simulating autumn at 10 °C lus Schreber) (Gezbczynska 1976). In laboratory experiments for 8 weeks (continuous light of 112 lmol mÀ2 sÀ1), winter on food preferences of the bank vole, M. effusum seeds were at 2 °C for 11 weeks (8 h light, 16 h darkness) and early preferred over the seeds of six other tested species, but beech spring at 10 °C for 2 weeks (8 h light, 16 h darkness). (Fagus sylvatica) seeds were more preferred than M. effusum Thompson (1980) also found that post-harvest after-ripening seeds (Jensen 1982). Tast (1966) noted that in some sites in in dry storage is important for successful, fast germination of Finland root voles (Microtus oeconomus Pallas) also feed on M. effusum seeds sampled in Sussex. Wet chilling (at 2 °C) M. effusum. Analyses of faeces collected in woods in north- and alternating, fluctuating temperatures (12 h day/night tem- eastern Germany showed that seeds are consumed by wild peratures of 21/11 °C and 26/16 °C) also promote germina- boar (Sus scrofa L.), although not in large quantities (Hein- tion, and can result in near 100% success (Thompson 1980). ken, Hanspach & Schaumann 2001). According to Falkowski Accordingly, the species is categorized as having physiologi- (1976), seeds of M. effusum are also consumed by birds. cal dormancy (Thompson 1980; Jankowska-Blaszczuk & More than 30 phytophagous invertebrates have been Daws 2007; Baskin & Baskin 2014). reported to feed on M. effusum, the majority being the larvae Germination percentages on agar pads are reported to be of leaf miner flies and moths (Table 2). A number of these temperature-dependent, with the fastest and highest subse- (Elachistidae, grass-miner moths) are restricted to graminoids quent germination (near 100%) between 16 and 21 °C. for food plants, and at least two species, Elachista cingillella Thompson (1980) suggests that the germination patterns and E. diederichsiella, appear to feed exclusively on observed across Europe are the result of the temperature M. effusum. Elachista cingillella is very rare in the UK, but it regime experienced by the mother plant. Light is often key to has been suggested that the species would be found more the germination of small-seeded species, but seems to have frequently if looked for in suitable habitats (Emmet 1996). relatively limited effects on germination of M. effusum seeds (Thompson 1980) supporting the shade tolerance of the species. However, germination of Wood Millet seeds sampled in Białowieza,_ Poland, increased with increasing red: far red light ratios allowing the plant to detect the absence of shading vegetation (Jankowska-Blaszczuk & Daws 2007). Soil pH, P concentration and organic matter concentration do not seem to affect the emergence of seedlings significantly (Staaf 1992; Falkengren-Grerup & Tyler 1993; Graae, Hansen & Sunde 2004). Litter removal increased germination of seeds of M. effusum (Dzwonko & Gawronski 2002). The mortality of the juveniles during the first year after emergence is usually low (<20%) (Graae, Hansen & Sunde 2004). However, in forests in southern Poland with high competition at the forest floor, only 11% of seedlings survived the first growing season (Towpasz & Szymska 1983).

(E) SEEDLING MORPHOLOGY

The epigeal cotyledon appears enrolled just like the new leaves of older seedlings. The leaves, however, unfold to the typically flat-leaved structure of the adult plant. The leaves of the seedlings are bright green with soft, very short hairs. Dur- ing the first year, only a relatively small, vegetative plant develops with c. 4–15 leaves (Fig. 6) and most new seedlings start to flower after two growing seasons (De Frenne et al. 2011b).

IX. Herbivory and disease

(A) ANIMAL FEEDERS OR PARASITES

Wood Millet leaves are consumed by mammals such as deer, Fig. 6. The development of Milium effusum from germination to an voles and wild boar. Stomach analyses of animals in forests adult, ﬂowering individual, drawn by Frederik Lerouge.

Table 2. Phytophagous invertebrates recorded as feeding on Milium effusum. Nomenclature and presence of the species in the UK follow Fauna Europaea (de Jong 2014), unless otherwise noted

Species Ecological notes Present in the UK Sources

Acari Eriophyidae Aceria tenuis (Nalepa) Leaf margin rolling No 3 Diptera Agromyzidae Agromyza mobilis Meigen Larvae mine leaves. Reported for Milium ssp. Yes 12 Cerodontha (Poemyza) muscina (Meigen) Larvae mine leaves. Reported for Milium ssp. Yes 12, 18 Chromatomyia fuscula (Zetterstedt) Larvae mine leaves No 10 Chromatomyia milii (Kaltenbach) Larvae mine leaves. Particularly on Yes 10, 12, 17, 18 M. effusum, but species feeds also on other genera Chromatomyia nigra (Meigen) Larvae mine leaves Yes 10, 12, 17, 18 Liriomyza ﬂaveola (Fallen) Larvae mine leaves. Reported for Milium ssp. Yes 12 Hemiptera Aphididae Forda formicaria von Heyden Yes 24 Metopolophium (Metopolophium) Yes 13 dirhodum (Walker) Rhopalosiphum padi (Linnaeus) Yes 13 Sitobion (Sitobion) avenae (Fabricius) Yes 13 Sitobion (Sitobion) fragariae (Walker) Yes 13 Hymenoptera Cephidae Cephus nigrinus C.G. Thomson Larvae Yes 15, 20 Lepidoptera Cosmopterigidae Cosmopterix orichalcea Stainton Larvae mine leaves. Reported for Milium ssp. Yes 8 Elachistidae Elachista (Aphelosetia) adscitella Stainton Larvae mine leaves Yes 7, 19, 21 Elachista (Elachista) albifrontella (Hubner)€ Larvae mine leaves Yes 7, 12, 21 Elachista (Elachista) apicipunctella Stainton Larvae mine leaves Yes 7, 12, 19, 21 Elachista (Elachista) atricomella Stainton Larvae mine leaves. Reported for Milium ssp. Yes 7, 21 Elachista (Elachista) bifasciella Treitschke Larvae mine leaves No 19, 21, 23 Elachista (Aphelosetia) cingillella Larvae mine leaves. Only M. effusum Yes 12, 19, 21 (Herrich-Sch€affer) has been reported as food plant Elachista (Elachista) diederichsiella Larvae mine leaves. Only M. effusum No 12, 21 E. Hering has been reported as food plant Elachista (Elachista) elegans Frey Larvae mine leaves No 12, 21 Elachista (Elachista) luticomella Zeller Larvae mine leaves; mining may cause Yes 7, 12, 21 the plant to wilt and become discoloured Elachista (Aphelosetia) obliquella Stainton Larvae mine leaves. Reported for Milium ssp. Yes 21 Elachista (Elachista) stabilella Stainton Larvae mine leaves Yes 7, 12, 21 Hesperiidae Carterocephalus silvicola (Meigen) Larvae No 16 Noctuidae Apamea illyria Freyer Larvae. Not clear whether observation is No 4 from the wild Apamea scolopacina (Esper) Larvae feeding on leaves Yes 4, 6, 9, 11 Diarsia mendica (Fabricius) Adults were observed sucking on ﬂowering Yes 5, 6 individuals Oligia versicolor (Borkhausen) Larvae Yes 22 Nymphalidae Aphantopus hyperantus (Linnaeus) Larvae Yes 1, 2, 14 Coenonympha hero (Linnaeus) Larvae No 2 Erebia euryale (Esper) Larvae No 2 Erebia ligea (Linnaeus) Larvae No 2 Erebia medusa (Denis & Schiffermuller)€ Larvae No 2 Pyronia (Pyronia) tithonus (Linnaeus) Larvae Yes 2, 14 Tortricidae Cnephasia (Cnephasia) asseclana Larvae mine leaves. Reported for Milium ssp. Yes 12 (Denis & Schiffermuller)€

(continued)

Table 2. (continued)

Species Ecological notes Present in the UK Sources

Cnephasia (Cnephasia) chrysantheana Larvae mine leaves. Reported for Milium ssp. No 12 (Duponchel) Cnephasia (Cnephasia) incertana Larvae mine leaves. Reported for Milium ssp. Yes 12 (Treitschke)

Sources: 1, Allan (1979); 2, Blab & Kudrna (1982); 3, Davis et al. (1982); 4, Ebert (1997); 5, Ebert (1998); 6, Ebert (2005); 7, Emmet (1996); 8, Emmet & Langmaid (2002); 9, Goater (1974); 10, Grifﬁths (1980); 11, Heath & Emmet (1983); 12, Hering (1957); 13, Holman (2009); 14, Khan (1989); 15, Liston et al. (2014); 16, Settele, Feldmann & Reinhardt (1999); 17, Spencer (1972); 18, Spencer (1976); 19, Steuer (1976); 20, Taeger et al. (1998); 21, Traugott-Olsen & Schmidt Nielsen (1977); 22, Wirooks & Theissen (1999); 23, Worz€ (1957); 24, Zwolfer€ (1958).

Elachista diederichsiella occurs in large parts of Europe, but Phaeosphaeria nigrans, which is saprobic and has been is absent from the British Isles (de Jong 2014). The snail Col- observed on dead plant material. Also, a slime mould umella edentula (Draparnaud) has been on observed on M. ef- (Arcyria denudata Fries) has been reported for M. effusum fusum in an oak-hornbeam wood in Poland (Piskorz & (British Mycological Society 2015). White & Baldwin (1992) Urbanska 2007). did not ﬁnd any stromata or endophytic fungus mycelium in the leaves of M. effusum collected in Telford, Shropshire, UK. (B) AND (C) PLANT PARASITES AND DISEASES

Milium effusum is often infected by the smut Ustilago stri- X. History iformis, which forms dark stripes on the leaf sheaths and blades (Conert et al. 1998; Table 3). Infected plants show Milium effusum was known to herbalists such as Gerarde restricted growth and develop no or only small inflorescences. (1597), who is credited with the first British record (Clarke Infections by the powdery mildew Blumeria graminis are also 1900), as Gramen Miliaceum. The current binomial was coined common (Conert et al. 1998; British Mycological Society in Linnaeus’ Species Plantarum in 1753. The taxonomic iden- 2015). Furthermore, M. effusum may be infected by a number tification of Poaceae species from pollen remains is almost of other ascomycete and basidiomycete fungi (Table 3), all of impossible. Nevertheless, M. effusum has been mentioned in which are classified as diseases or parasites, except pollen diagrams of the Atlantic period (7200–4900 BP) in the Netherlands, along with other species of the Fagetalia sylvati- Table 3. Fungi associated with Milium effusum. Nomenclature fol- cae community type (Groen 2007). In a study mostly con- lows MycoBank (International Mycological Association 2017) ducted in Sweden, the spatial genetic structure of M. effusum revealed no clear pattern, rendering any inference on refugia Species Sources and post-glacial migration routes difficult (Tyler 2002). Macro- Ascomycota remains of M. effusum have been reported from various Erysiphales archaeological sites of the Neolithic and Bronze Age in Central Blumeria graminis (DeCandolle) Speer 3, 4 Europe. Wood Millet leaves have been (and are still) used to Capnodiales aromatize tobacco (Conert et al. 1998) or alcohol (because of Passalora graminis (Fuckel) Hohnel€ 7 Helotiales the presence of coumarin; Mossberg & Stenberg 2012). Rhynchosporium orthosporum Caldwell 2 (reports species Although the seeds are small, they were also used for feeding for Milium ssp.) (exotic) birds, and even sown in woodlands and landscape Rhynchosporium secalis (Oudemans) Davis 6 parks for ornamental purposes, and as food source for game Hypocreales (e.g. in England, Belgium and Germany) due to their relatively Claviceps purpurea (Fries) Tulasne 1 Epichlo€e typhina (Persoon) Tulasne & 5 high starch content (Vietz & Kerndl 1818; Hubbard 1984; Van C. Tulasne Landuyt et al. 2006). The energy content of seeds sampled in Pleosporales a Danish wood was 4Á71 kcal gÀ1 dry weight. That is, how- Phaeosphaeria nigrans (Roberge ex 3 ever, relatively low compared to seeds of Anemone nemorosa, Desmazieres) L. Holm Fagus sylvatica and Melica uniflora (Jensen 1982). Basidiomycota Pucciniales Puccinia coronata Corda 4 XI. Conservation Ustilaginales Ustilago striiformis (Westendorp) Niessl 4, 8 The species is not listed as threatened, endangered or vulnera- ble on any Red List consulted. A recent survey in Britain found Sources: 1, Bove (1970); 2, Braun (1995); 3, British Mycological Society (2015); 4, Conert et al. (1998); 5, Kohlmeyer & Kohlmeyer no evidence for change in its distribution between 1987 and (1974); 6, Lebedeva & Tvaruzek (2006); 7, Swiderska-Burek (2007); 2004 (Braithwaite, Ellis & Preston 2006). The frequency of 8, Vanky (2012). occurrence of the species in resurveyed semi-permanent

© 2017 The Authors. Journal of Ecology © 2017 British Ecological Society, Journal of Ecology, 105, 839–858 Milium effusum 855 vegetation plots has even increased by c. 2Á1% in ancient wood- Brunet, J. & von Oheimb, G. (1998) Migration of vascular plants to secondary – lands across Europe (De Frenne et al. 2013) (section III). As a woodlands in southern Sweden. Journal of Ecology, 86, 429 438. Brunet, J., De Frenne, P., Holmstrom,€ E. & Mayr, M.L. (2012) Life-history widespread species, specific management actions are therefore traits explain rapid colonization of young post-agricultural forests by under- currently directed towards the conservation of some of its main story herbs. Forest Ecology and Management, 278,55–62. habitat types rather than to the species directly. For instance, Chandler, T.J. & Gregory, S. (1976) The Climate of the British Isles. Longmans Group, London, UK. M. effusum is an indicator species in woodlands of high conser- Chytry, M. & Rafajova, M. 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