Biological Flora of the British Isles*: Stachys sylvatica L.
Nomenclature of vascular plants follows Stace (2010) and, for non-British species, Flora Europaea.
1. This account presents information on all aspects of the biology of Stachys sylvatica 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. A rhizomatous perennial herb, with strong far-creeping stolons, Stachys sylvatica is a polymorphic native herb of open woodlands, hedgerows, banks of rivers and streams, widespread throughout most of the British Isles.
3. Stachys sylvatica occurs in light to moderate shade. It is suggested that the red/far red ratio is more critical than reduced irradiance in the plant’s response to shading.
4. Stachys sylvatica occurs on moist or damp but not wet, weakly acid to weakly basic soils, and has been described as a nitrate indicator on base-rich soils.
5. Stachys sylvatica depends on seedlings established close to the parent plant for maintaining population density. Stolons are probably effective in extending the area of clones.
6. The hybrid between Stachys sylvatica and Stachys palustris, Stachys×ambigua, is most frequent in northern and western Britain, and occurs as an introduction outside the native range of Stachys sylvatica.
Hedge Woundwort. Lamiaceae, Lamioideae, Stachys sylvatica L. An almost hispid, foetid when bruised, polycarpic, rhizomatous perennial herb, with strong far-creeping stolons. Stems erect to 30–120 cm, often branched, square in section, with stalked glands in the upper parts. Leaves opposite, petiolate, with glandular and eglandular hairs; lamina 2–12 × 0.7–8.0 cm, soft medium green on upper surface, paler beneath, ovate, acuminate, cordate at base, coarsely crenate–serrate, sparsely to densely hairy on both surfaces. Inflorescence an interrupted terminal spike formed of 6-(8)-flowered whorls; flowers zygomorphic, hermaphrodite, hypogynous; calyx campanulate with 5 equal acute lobes; corolla 13–18 mm, dull reddish-purple, with white markings, pubescent outside, with hooded upper lip 4–5 mm and 3-lobed lower lip 6–7 mm; stamens 4, shorter than upper lip of corolla; ovary 4-celled, each cell with 1 ovule, with a single style and 2 stigmas. Fruit of four single seeded nutlets, 2.0–2.5 mm, obovoid, rounded at apex. There are various estimates of the mean air-dry mass of mature seeds: 1.9 mg (Salisbury 1942), 1.4 mg (Grime, Hodgson & Hunt 2007), 1.46 mg (Jankowska-Blaszczuk & Daws 2007), 1.67 mg (Fröborg 2001) and 1.4 ± 0.4 mg across central and north-western Europe (Graae et al. 2009).
Within this polymorphic and widespread species two varieties have been recognized (Sell & Murrell 2009):
var. sylvatica. Stem leaves and inflorescence with few to numerous simple, eglandular and glandular hairs. Cauline leaves 5–12 × 3–8 cm.
var. subsericea Grogn. Stems, leaves and inflorescence with dense simple eglandular and glandular hairs. Cauline leaves 2–7 × 0.7–5.0 cm.
Stachys sylvatica is a common native herb of generally moist habitats, in open woodlands, hedgerows, banks of rivers and streams, road verges and disturbed fertile ground, but absent from pastures. It is rare outside these core lowland habitats, but is recorded from bracken stands on coastal slopes (Pearman et al. 2008) and in boulder scree at the foot of cliffs (McCallum Webster 1978; Evans, Evans & Rothero 2002).
I. Geographical and altitudinal distribution
Stachys sylvatica is widespread throughout most of the British Isles, but is absent or rare on islands off the north and west coasts of Scotland (Fig. 1). According to Sell & Murrell (2009) the common plant throughout Great Britain and Ireland is var. sylvatica, and var. subcericea is recorded only from Cornwall, Devon, Glamorgan, Pembrokeshire, the Channel Islands, Norfolk and Cambridgeshire.
Stachys sylvatica is widely distributed in Europe (Fig. 2), but is rare in the Mediterranean region, and extends into Asia. Var. subcericea occurs in France.
Preston & Hill (1997) assign Stachys sylvatica to the Temperate Eurosiberian floristic element in the British and Irish flora.
Stachys sylvatica is common at low altitude but occurs up to 500 m above Malham, North Yorkshire and 845 m on Great Dun Fell, Cumbria (Halliday 1997; Pearman & Corner 2004). In continental Europe it has an altitudinal range of 8–1645 m in the northern half of the Iberian peninsula (Morales et al. 2010).
(A) Climatic and topographical limitations
Stachys sylvatica occurs in 2462 (maximum possible 2805) of the hectads (10 × 10-km) squares in Britain, 806 (985) in Ireland and 12 (14) in the Channel Islands; in these the mean annual rainfall is 1064 mm year−1, and the mean January and July temperatures are 3.6 °C and 14.7 °C, respectively (Hill, Preston & Roy 2004).
Stachys sylvatica prefers moist or damp but not wet soils (Ellenberg value for moisture = 6), in weakly acid or weakly basic conditions (Ellenberg value for pH = 7), and is often found in richly fertile places (Ellenberg value for soil fertility = 8) (Hill, Preston & Roy 2004).
In Scotland, Stachys sylvatica occurs in woodland in base-rich soils on steep to moderate slopes where there is some degree of flushing, or on terraces, often where the ground water is influenced by basic rocks. These brown forest soils are eutric cambisols, often a gleyic type (Birse 1982). The soils in which Stachys sylvatica is rooted are moderately base-saturated in the surface horizon, with pH values ranging from 4.9–5.4 (Table 1). Soil chemical analyses of samples taken from sites where Stachys sylvatica occurs in the lowland and southern upland regions of Scotland are shown in Table 1. The concentrations of total phosphorus fall in the lower half of the range (1–200 mg 100 g−1) for soils which are commonly found in the British Isles (Allen et al. 1989). There is little or no correlation between the phosphorus content and the carbon:nitrogen ratio.
|Site (N.G. ref.)||Organic matter (%)||pH||Base saturation (%)||Exchangeable ions (mg 100 g−1)||Total P (mg 100 g−1)||C/N ratio|
- All sites were in Aceri-Ulmetum glabrae communities on brown forest soil (Dystric) in the lowland and southern upland regions of Scotland.
Harris & Dart (1973) reported that in a number of sites there was an increased nitrogenase activity in the rhizosphere of Stachys sylvatica as measured by C2H2 reduction. Nitrogenase activity was concentrated in the rhizosphere and in particular in roots. Dilution plate counts from active samples of root and rhizosphere soil, on N-free mineral salts agar, yielded three types of nitrogen-fixing isolates.
Gebauer, Rehder & Wollenweber (1988) recorded the occurrence of Stachys sylvatica in four sample sites in Central Europe which had especially high soil nitrate contents (μmol NO3− g−1 dry mass) with a mean ( ± SE) of 0.104 ± 0.095 (n = 81) in an occasionally cut grassland, 0.649 ± 0.424 (n = 36) on the slopes of river banks, of 0.429 ± 0.389 (n = 21) at the edge of a ruderal hedge and 0.493 ± 0.348 (n = 9) at the edge of Spruce forest. The pH values in the same soils were 5.63 ± 0.42 (n = 81), 7.10 ± 1.47 (n = 36), of 6.95 ± 0.48 (n = 21) and 7.59 ± 0.35 (n = 9), respectively.
Stachys sylvatica is most frequent in the pH range 6.0–8.0 and absent below pH 4.0 in the Sheffield region (Grime, Hodgson & Hunt 2007).
The results of plant tissue analyses of mature, non-senescent leaves of Stachys sylvatica collected from various sites in the British Isles are presented in Table 2. The concentrations of N and P are relatively high, but the concentration of Ca is at the lower end of the ranges reported for herbs in many surveys (Thompson et al. 1997). The concentrations of plant N and high soil nitrate contents reported above are a good indication of the requirements of the plant (see VI E).
|Site (N.G. ref.)||N (%)||P (%)||Ca (%)||Mg (%)||K (%)|
|Birks Bridge (SD636664)||4.13||0.37||–||0.28||5.47|
|East Brownrigg (NY528377)||1.67||0.41||0.64||0.34||2.98|
|Haverthwaite Bridge (SD346)||2.11||0.40||1.02||0.26||3.38|
- Chemical analyses by Analytical Chemistry, Centre for Ecology and Hydrology, Lancaster, using the methods described by Allen et al. (1989).
Antosiewicz et al. (2008) sampled the indigenous plant species including Stachys sylvatica growing on a slag slope, and the soil in their rhizospheres, in the area around the old Zloty Stok arsenic and gold mine located in south-western Poland. Samples were analysed for concentrations of arsenic and various other elements. The soil contained very high concentrations of available phytotoxic mineral elements, primarily As up to 7451 mg kg−1 dry mass, Pb 1058 and Al 31 272. The ability of the species to increase or decrease the amount of bioavailable As in their rhizosphere was determined by a single extraction of soil samples with 0.1 M KH2PO4 buffer, pH 7.2. The lowest amount of available As (only 5% of the total) was found in the rhizosphere soil of Stachys sylvatica, and also the lowest shoot concentration (5–7 mg kg−1) compared with the other plant species. Stachys sylvatica was proposed as a good candidate for phytostabilization which aims at the reduction of the mobility of the contaminant As, including accompanying elements at lower concentrations such as Pb, Zn, Mn, Al and Cu, by means of root exudation. Phytostabilization using species such as Stachys sylvatica that tolerate high levels of As in the soil without accumulating it in large amounts in its shoots is advantageous since the spreading of the element arising from decaying plant tissues is restricted.
The Classification of British Plant Communities provides accounts of the habitats in which Stachys sylvatica occurs in the British Isles. In the following sections, the equivalent European phytosociological alliances are given in parenthesis and are taken from Rodwell et al. (2000). Communities described by other authors are inserted at an appropriate part of the text.
Stachys sylvatica together with Digitalis purpurea, Stellaria holostea and Teucrium scorodonia though preferential, are at most occasional in Alnus glutinosa–Fraxinus excelsior–Lysimachia nemorum woodland (W7; Alno-Ulmion), Deschampsia cespitosa sub-community. This sub-community is often found where flush waters drain down through colluvium and on to stream-side flats. It is widely, though locally, distributed throughout the upland fringes of the north and west, with outlying occurrences in the wetter parts of southern England, notably the Weald (Rodwell 1991). Also, Stachys sylvatica is scarce in the Urtica dioica sub-community. In Fraxinus excelsior–Sorbus aucuparia–Mercurialis perennis woodland (W9; Alno-Ulmion), Stachys sylvatica, Filipendula ulmaria and Geum rivale are preferential but only occasional in the Crepis paludosa sub-community, which occurs in the Pennines and north-west Scotland.
Stachys sylvatica is scarce in a number of woodland and scrub communities. It occurs in Alnus glutinosa–Urtica dioica woodland (W6; Salicion albae), a community which is widespread but local throughout the lowlands, occurring where active alluvial deposition is taking place on more mature rivers, and on the remnants of undrained flood plain mires where enriched waters flood fen peat. Stachys sylvatica is scarce in Fraxinus excelsior–Acer campestre–Mercurialis perennis woodland (W8; Carpinion betuli), in which Corylus avellana and Rubus fruticosus agg. are the other constant species, a community which is widespread over more base-rich soils in lowland Britain. However, in the Quercus robur–Carpinus betulus and Quercus petraea–Carpinus betulus woods of Hertfordshire, which are referable to this community, Stachys sylvatica occurs frequently in the woodland margins and rides and (in the former woods) it is one of the species which are frequent or common in the first or second year after coppicing (Salisbury 1916, 1918). In Scotland Stachys sylvatica is a character species in the Querco-Ulmetum Birse et Robertson 1976 association within the order Fagetalia sylvaticae in the class Querco-Fagetea, broad-leaved, semi-natural, mixed deciduous woodland on base-rich soils (Birse & Robertson 1976; Birse 1982). Stachys sylvatica is scarce in Quercus robur–Pteridium aquilinum–Rubus fruticosus woodland (W10; Carpinion betuli), which is widely distributed and common over the lowlands of England and Wales. It is also scarce in Fagus sylvatica–Mercurialis perennis woodland (W12; Fagion sylvaticae), Mercurialis perennis and Sanicula europaea sub-communities, which have a wide distribution, being especially characteristic of the scarps of the North and South Downs and the western end of the Cotswolds. Stachys sylvatica is one of the species common to the semi-natural beechwood in southern England, on chalk escarpments, on non-calcareous soils of the chalk plateau and also in Scottish beechwoods (Watt & Tansley 1932). It occurs in Crataegus monogyna–Hedera helix scrub (W2; Berberidion vulgaris) which includes many hedges especially in the Hedera helix–Urtica dioica sub-community in which Crataegus monogyna, Rubus fruticosus agg., Hedera helix, Urtica dioica and Galium aparine are constants, widely distributed through the British lowlands, and also in the floristically richer Mercurialis perennis sub-community, found on heavy-textured base-rich soils especially in areas with clays and shales. Stachys sylvatica is scarce in Prunus spinosa–Rubus fruticosus scrub (W22; Prunion fruticosae), widely distributed through the British lowlands. It also occurs in Rubus fruticosus–Holcus lanatus underscrub (W24; Rubion subatlanticum) sub-community Arrhenatherum elatius–Heracleum sphondylium that is consistently enriched by a very distinctive group of preferentials, Arrhenatherum elatius, Festuca rubra, Urtica dioica, Heracleum sphondylium, Taraxacum officinale agg. and Galium aparine which are constants, and frequently Anthriscus sylvestris and Chaerophyllum temulum, which is ubiquitous on suitable soils throughout the British lowlands.
Stachys sylvatica is also scarce in Arrhenatherum elatius–Filipendula ulmaria tall-herb grassland (MG2; Arrhenatherion elatioris) with the other constants Angelica sylvestris, Dactylis glomerata, Epilobium montanum, Festuca rubra, Geum rivale, Heracleum sphondylium, Mercurialis perennis, Poa trivialis, Silene dioica, Urtica dioica and Valeriana officinalis, a community which is confined to steep slopes, usually of northern aspect, on rendziniform soils overlying the Carboniferous limestone of Craven and Derbyshire in northern England (Rodwell 1992).
Both Stachys sylvatica and Stachys palustris are scarce in the Epilobium hirsutum community (OV26; Convolvulion), characteristic of moist but well-aerated mesotrophic to eutrophic mineral soils and fen peats in open-water transition mires, around ponds, in silting ditches, and along streamsides, widespread and common throughout the lowlands (Rodwell 2000). In the Epilobium (Chamerion) angustifolium community (OV27; Carici piluliferae-donnae), Stachys sylvatica is also scarce in damp fertile soils on disturbed, often burned, ground in woodlands, on heaths, road verges and wasteland throughout the British lowlands.
A number of fast-colonizing woodland species characteristic of undisturbed communities in ancient woodlands, including Stachys sylvatica are present in > 50% of secondary woodlands originating, after 1820, on former cultivated ground in central Lincolnshire (Peterken 1981).
In Central Europe, (Ellenberg 1988) described the occurrence of the nitrate indicator Stachys sylvatica on moist base-rich soils in broadleaved woodland in the order Fagetalia. It is found in beechwoods in the alliance Fagion sylvaticae sub-alliance Galio odorati-Fagion (Eu-Fagion), especially in the Wild Garlic-rich beechwoods which occur in the lowlands of north-west and south-west Central Europe. It also occurs in the alliance Carpinion betuli in the Woundwort-Common Oak-Hornbeam woods on fairly wet soil, and less frequently in the Lime-Hornbeam woods. Especially at higher altitudes in Alder-Ash woods in the alliance Alno-ulmion, both Stachys sylvatica and Stachys palustris occur, the former in Oak-Ash wood (Pruno-Fraxinetum) in fertile flood plains and the latter in Alder swamp woods. In lowland flood plains, Stachys sylvatica is also present in willow communities of the alliance Salicion albae.
Stachys sylvatica is a diagnostic ground flora species in major broadleaved forest associations in continental Europe in the class Querco-Fagetea order Fagetalia Sylvaticae (Stortelder, Schaminée & Hermy 1999). In the alliance Alno-Padion the species occurs in all five associations, but is most abundant in the Pruno-Fraxinetum that mostly occurs in the more or less flat areas in stream or river valleys, which are regularly to occasionally inundated. Here, the soil mainly consists of base-rich, loamy sand with a high organic matter content. The tree layer is dominated by Fraxinus excelsior and Quercus robur with Alnus glutinosa and an understorey of Corylus avellana. In the herb layer Stachys sylvatica occurs with the species listed above together with Anemone nemorosa, Deschampsia cespitosa, Glechoma hederacea, Ficaria verna and Urtica dioica. Stachys sylvatica also occurs in the alliance Carpinion Betuli in the Stellario-Carpinetum on loamy soils where the groundwater is near the soil surface, but fluctuates considerably in depth throughout the year, being wet in winter and dry in summer. Dominant tree species are Fraxinus excelsior and Quercus robur, with Prunus avium, Acer pseudoplatanus and Carpinus betulus also present. Stachys sylvatica is a differential species in Urtica dioica (Circaeo-Alnenion), a community with just a few characteristic species (‘Romgemeenschappen’), dominated by Urtica dioica and Anthriscus sylvestris.
IV. Response to biotic factors
Corré (1984) grew seedlings of a number of sun and shade plants including Stachys sylvatica and Galinsoga parviflora (a weed of open wasteland), experimentally in aerated nutrient solution in a glasshouse at a radiant flux of 200 W m−2. Seedlings 2 weeks after germination were grown in monoculture and in a 1:1 mixture, 12 plants per pot with an area of 625 cm−2, in three light treatments 100%, 30% and 12% daylight. At the higher light fluxes the competitive ability of Galinsoga parviflora was greater. At 12% light flux the dry matter production of Stachys sylvatica was the greater, and seemed to depend on the larger mass of the plant at the start of the experiment. This latter feature appeared to pre-determine the result of the competition experiment, and whether the species was a sun or a shade plant was less important. However, at this low level of light flux productivity was really too low to ensure effective competition.
Selective grazing was studied in Åland, south-western Finland, by Hæggström (1990). He found that Stachys sylvatica was regularly defoliated by cattle and sheep, though only to a minor extent.
V. Response to environment
The stolons of Stachys sylvatica are most effective in extending its range locally by clonal spread (Wilcock 1974).
(B) Performance in various habitats
Stachys sylvatica occurs in light to moderate shade (Ellenberg value for light = 6; Hill, Preston & Roy 2004). In assessing the effect of shading on plant growth, Corré (1983a) has emphasized the need to consider the changes in the spectral distribution that occur in natural shade and the effects of irradiance of different spectral quality. Compared with sunlight, the spectral composition within and beneath a leaf canopy is relatively poor in blue and red light and relatively rich in green, and especially rich in far-red light. Two wavelengths 660 nm and 730 nm, which are the absorption maxima for the photoreceptor pigment phytochrome, are absorbed in different proportions and therefore shade light is characterized by the red/far-red ratio (R/FR). At latitude 53° N, the R/FR varies between c. 1.15 in the open to c. 0.10 in dense shade (Smith 1981).
Corré (1983a) grew seedlings of a number of species of different shade tolerance including Stachys sylvatica experimentally in aerated nutrient solution in a controlled environment room. In different experiments three different levels of irradiance (400–700 nm) were applied: a moderately reduced level of irradiance with a normal R/FR, and a very low level of irradiance with either a normal R/FR or a low R/FR (see also VI E). With decreased irradiance and a constant R/FR there was a decrease in the relative growth rate (RGR). In the low R/FR treatment there was an increase in stem elongation and a concomitant increase in stem dry mass and shoot weight ratio (SWR). A small decrease in leaf weight ratio (LWR) reduced the dry matter production. These morphogenetic adaptations of Stachys sylvatica to the low R/FR led to differences in the extent to which the RGR decreased, but changes in net assimilation rate (NAR) were of minor importance. It is suggested that the R/FR ratio is more critical than reduced irradiance in the plant’s response to shading.
In a further experiment Corré (1983b) assessed the growth and morphogenetic reaction of Stachys sylvatica to a combination of low irradiance and low nutrient supply, a combination typical of woodland habitats. There was an interaction between the effects of irradiance and NO3− supply: low supply of NO3− caused a much greater decrease in RGR under high irradiance, because of large changes in dry matter distribution; LWR decreased much more under high irradiance than under low irradiance, while the effect on NAR was small and not dependent on irradiance. It is unlikely that the shade tolerance of Stachys sylvatica is partly or wholly based on a lower sensitivity to low nitrate supply under a low level of irradiance.
However, an investigation carried out in a beech forest (Hordelymo-Fagetum association) with a species-rich herb layer on calcareous soil (pH 7.3) in lower Saxony, central Germany, showed that the level of shade was of secondary importance in the distribution of the woodland herbs (Leuschner & Lendzion 2009). It suggested that other abiotic factors are important in influencing the cover of the most abundant plant species. The abundance of Stachys sylvatica, which occurs on valley bottom and north-facing slopes with shallow soil, is primarily correlated with the lowest vapour pressure deficits and the highest soil moisture levels.
(C) Effect of frost, drought, and flooding
Ellenberg (1988) reported measurements of the soil water potential around the roots of a number of widely distributed herbaceous plants in a moist-soil Oak-Hornbeam wood. For Stachys sylvatica, on slightly moist soils, values were normally between −1 and −2 bar (−0.1 to −0.2 MPa). In an unusually dry late summer values reached −9 bar (−0.9 MPa) when the plant was completely wilted. These results confirmed those of Rehder (1960) who measured leaf water potentials of Stachys sylvatica. The potential of the leaves on fully turgid plants was always higher than −10 bar (−1.0 MPa) and generally amounted to −5 to −6 bar (−0.5 to −0.6 MPa). As the plants wilted, the potential was −11 to −12 bar (−1.1 to −1.2 MPa) and had reached −15 to lower than −20 bar (−1.5 to > −2.0 MPa) by the time they were completely flaccid. In a dry period many woodland herbs begin to wilt before the permanent wilting point of the soil is reached at c.−15 bar (−1.5 MPa).
In a pot culture experiment, three different genotypes of Stachys sylvatica produced significantly lower masses of rhizome (stolon) in wet soil than in dry soil; with mean dry masses g pot−1 of 0.46. 0.30 and 0.70 in the wet and 2.24, 0.90 and 1.44 in the dry treatments respectively (Wilcock 1974).
VI. Structure and physiology
Stachys sylvatica occasionally forms rhizomes (c. 3 mm in diameter) in the upper layer of the mineral soil horizon (at a mean depth of 4 cm), but produces far-creeping stolons both above ground and in the loose surface litter layer where resistance to spread is negligible. In leaf mould the stolons have been known to attain a length of 2 m (Salisbury 1925, 1961).
Farley & Fitter (1999) investigated the root proliferation responses of seven co-occurring perennial woodland herbs to soil nutrient-rich patches. Small plantlets with at least four leaves were transplanted into pots and grown in a glasshouse with supplementary lighting for 6 weeks. Each pot had a nutrient-enriched patch of garden soil on one side of the central plant, and an un-enriched area of coarse washed sand the same size on the other side to serve as a control. Stachys sylvatica produced a large root system (total root length 7–16 m plant−1) that extended throughout each replicate pot. It was the only species to respond solely by a change in root architecture. Exploitation of patches in Stachys sylvatica depends on producing a more effective spatial pattern of roots in the patch, rather than any increase in their number or length.
In transverse section, the largest vessel elements are clearly concentrated at the four corners of the square stem; there are about 30–50 vessels in each corner vascular bundle area, each vessel with a mean internal diameter of 25–35 μm (Xia et al. (1993).
Stachys sylvatica is hypostomatous, with a stomatal density of 136 mm−2 (range 128–144) (Salisbury 1927).
(C) Perennation: reproduction
Protohemicryptophyte. There may be selection for self-fertile individuals, associated with a dependence on seedling establishment for maintaining population density.
(E) Physiological data
Corré (1983a) grew seedlings of a number of species of different shade tolerance including Stachys sylvatica, in an aerated nutrient solution in a climatic room with day length 16 h, a day temperature of 20 °C and a night temperature of 15 °C. Two light treatments were used: one moderate energy fluence rate (400–700 nm) of 8 Wm−2 with either a normal (1.00) or low (0.11) R/FR ratio. Measurements of photosynthesis and respiration were made in an assimilation chamber by infrared gas analysis. Four plants of each species were measured from both light treatments every 5 days, then leaf areas and leaf and stem dry weights recorded. At the moderate light flux Stachys sylvatica showed a decrease in leaf area ratio, LWR and specific leaf area and an increase in SWR, by the reduction in the R/FR ratio. In contrast, another partial shade plant, Urtica dioica was unaffected by the reduction. The photosynthetic capacity of Stachys sylvatica was slightly lower, whereas photosynthetic efficiency did not seem to be influenced by the R/FR ratio. However, dark respiration on an area basis at the low R/FR ratio was increased. The increase in the dark respiration rate and higher SWR of Stachys sylvatica confirms that the rapidly elongating stem has a larger energy demand.
Al Gharbi & Hipkin (1984) assayed in vivo nitrate reductase activity (NRA), a good indicator of the availability of NO3−, in the leaves of 33 ground-layer species sampled from the edge of an Oak-Elm wood. The youngest, fully expanded leaves were taken back to the laboratory for enzyme assays. The mean activity for these species was 1.36 ± 0.29 μmol NO2− h−1 g−1 fresh wt. (range 0.1–3.21). Stachys sylvatica had a mean NRA of 1.90 (range 0.85–3.35), and therefore was in the upper end of the range for these woodland species.
In most studies involving discussion of ecologically significant aspects of the nitrogen nutrition of plants different approaches have been made in isolation from each other: available N in the soil and, the contents of nitrate, NRA and organic nitrogen in individual organs of plants (see also II B). Gebauer, Rehder & Wollenweber (1988) have compared all four methods in studying 48 Central European plant species in a range of habitats. Stachys sylvatica occurs on the slopes of river banks with soils containing 0.649 ± 0.424 (SE) μmolNO3− g−1 dry mass, and on the edge of Spruce forest 0.493 ± 0.348 μmol NO3− g−1 dry mass. On the slopes of river banks and on the edge of Spruce forest the plant had quite high concentrations of NO3− with the highest contents in the shoot axis plus petioles fraction, having mean (n = 3) values of 116.5 ± 29.4 and 113.8 ± 58.0 μmol NO3− g−1 dry mass respectively. With NRA values, highest in the laminae in the same two sites, of 2.85 ± 1.11 and 5.36 ± 1.30 μmol NO2− h−1 g−1 dry mass respectively, activities were moderately low. The organic nitrogen content was high in the river bank community and on the edge of Spruce forest, with the highest values of 33.0 ± 41.0 (SE) and 27.2 ± 0.6 in the laminae, and 33.0 ± 41.0 and 32.2 ± 4.9 in the reproductive fraction respectively, and represents the total amount of inorganic N assimilated. They concluded that these measures are suitable as indicators for the degree of nitrate supply of Stachys sylvatica in their natural sites and significantly correlate with the Ellenberg phytocoenological values.
Water flow in the xylem vessels has been imaged non-invasively using NMR microscopy, with an estimated mass flow of (5.1 ± 0.5) × 10−12 m3 s−1 (Xia et al. (1993).
Stachys sylvatica has been screened for polyphenols (Bankova et al. 1999). Above-ground parts contained three phenylethanol glycosides (acetoside, martinoside and forsythoside), and a flavonoid glycoside. Roots contained the same compounds but in lower concentrations.
The release of secretions by the glandular trichomes present on leaves and flowers of Stachys sylvatica has been investigated by Giuliani & Maleci Bini (2008). Histochemical tests show that small capitate hairs along the veins and large capitate hairs on intervein areas of adaxial and abaxial surfaces of leaves secrete a typical essential oil (terpene). Large capitate hairs, typical of inflorescences, produce a secretion consisting of polysaccharides, essential oil and polyphenols, particularly flavonoids.
Shoots begin to appear in late March and the plant is fully in leaf and has a peak of biomass by early June. It flowers from July to August, sets seed from July to October, and the shoots die down by the end of November.
In moist-soil Oak-Hornbeam woods in Central Europe, Stachys sylvatica has been described as an early flowering summer-green by Ellenberg (1988).
VIII. Floral and seed characters
(A) Floral biology
Flowers are hermaphrodite, markedly protandrous, and automatically self pollinated or cross fertilized by insect pollinators. Pollen grains are 43 μm in diameter (Knuth 1909) and are > 90% viable (Wilcock & Jones 1974). However, male-sterile plants and male-sterile populations occur, and these sometimes have unusually small flowers (Wilcock & Jones 1974). A wide range of floral abnormalities has been reported, including aberrant developments of the gynoecium (Bartlett 1909), peloria (the tendency to produce actinomorphic flowers), changes in the numbers of flower parts, and abortion of the stamens (Cutting 1921).
Flowers are frequently visited by various species of Hymenoptera; Andrena wilkella (Kirby), Anthidium manicatum L., Anthophora quadrimaculata (Panzer), Anthophora furcata (Panzer), Apis mellifera L., Bombus agrorum L., Bombus hortorum L., Bombus lapidarius L., Bombus pratorum, L., Bombus ruderarius (Müller) Bombus sichelii Radoszkowski Bombus veteranus (Fabricius) and Podalirius retusus L. Other visitors include species of Diptera; Eristalis tenax L., Platycheirus sp., Rhingia rostrata L. and Xylota sylvarum L. (Knuth 1909). Fussell & Corbet (1991) observed that the flowers are principally pollinated by the long-tongued bumblebees Bombus pascuorum (Scopoli) and Bombus hortorum. A hover fly Volucella bombylans also pollinates Stachys spp. (Proctor, Yeo & Lack 1996).
There are barriers to hybridization between Stachys palustris and Stachys sylvatica. These species usually occur in different habitats and, in some regions of Britain, are geographically separated. However, the two parents can be found growing together in tall-herb vegetation (OV26) dominated by Epilobium hirsutum and Urtica dioica (see III). More often the hybrid Stachys sylvatica×Stachys palustris = Stachys×ambigua occurs in communities in the absence of one or both parents, but especially Stachys sylvatica, particularly in the north and west. In these circumstances the hybrid appears to be a relic of cultivation and is presumably distributed by human fragmentation of the brittle rhizome.
Stachys×ambigua is frequent in parts of northern and western Britain where it often grows as a weed of cultivation, becoming rare towards south and east England (Fig. 3). It is native by streams and rivers, and often found in disturbed ground by roadsides. It is common at low altitude but occurs up to 300 m at Pentre Llyncwmmer, Cardiganshire (Pearman & Corner 2004). The hybrid and hybrid swarms have been recorded from many parts of Europe (Ball 1972).
Stachys×ambigua is a sterile rhizomatous perennial herb which reproduces by rhizome fragments. It is intermediate between both parents in most characters and usually has a bright red coloured corolla. There is, however, an overlap in leaf morphology between Stachys×ambigua and Stachys palustris, while Stachys sylvatica appears to be distinct (Wilcock 1972; Stace 2004).
Wilcock & Jones (1974) found that interspecific hybrids and back-crosses were difficult to produce artificially, indicating strong internal barriers to hybridization. Experimental hybridization proved to be more successful with Stachys sylvatica as the maternal parent. Different chromosome numbers in the polyploid parents may be one of the important internal barriers leading to irregular pairing at meiosis and low levels of pollen germination (generally >50% inviability) in the hybrid. Using Stachys sylvatica as the seed parent (Wilcock 1973), the hybrid showed an extremely low level of nutlet-set (0–50%); only 7% of the seeds germinated and all of them died in the seedling stage. Using Stachys palustris as the seed parent no seed was obtained. Stachys×ambigua has a chromosome number determined variously as 2n = 83 (Morton 1973) and 78–86, mostly 83 and 84 (Wilcock & Jones 1974) for British material. As the F1 hybrid is largely, if not completely, sterile it is almost entirely, if not totally, dependent on clonal production to maintain populations (Wilcock 1973). It may have been introduced for consumption as a vegetable or use as medicinal plant (Allen & Hatfield 2004).
Three species of Coleoptera (Circulionidae, Ceutorhynchinae) (Hoffmann 1954) feed on the hybrid: Ceutorhynchus angulosus Boheman, Ceutorhynchus urticae Boheman and Ceutorhynchus viduatus (Gyllenhal).
A list of the fungi associated with Stachys×ambigua is presented in Table 3.
|Craterium minutum (Leers) Fr.||On dead stems|
|Neoerysiphe galeopsidis (DC.) U. Braun||A powdery mildew occurring on the living leaves|
|Crocicreas cyathoideum var. cyathoidium (Bull.) S.E. Carp||On dead stems|
|Ophiobolus erythrosporus Riess||On dead stems|
|Hygrocybe pratensis var. pratensis (Fr.)||On dead stems|
- Source: British Mycological Society (2010).
(C) Seed production and dispersal
Most commonly, seed falls close to the parent plant and seedlings of Stachys sylvatica will become established locally and increase the population density (Wilcock 1973). However, seed may be dispersed by adhesion to the bodies of animals, by means of the pointed teeth on each calyx (Hermy et al. 1999; Grime, Hodgson & Hunt 2007).
(D) Viability of seeds: germination
Seeds of Stachys sylvatica dispersed in the autumn lie dormant during the winter and germination takes place in the following spring–summer. Thompson & Grime (1979) recorded a ‘seed bank’ of < 10 seeds in surface soil samples in cylinders of 7 cm diameter to a depth of 3 cm collected throughout the year from a hedgerow in the Sheffield region. A similar result was obtained by Warr, Kent & Thompson (1994) for the number of seeds germinating from soil samples taken from two woodland sites on base-rich soils in south-west England.
Roberts & Boddrell (1984) sowed seeds of Stachys sylvatica, freshly collected in autumn, onto sterilized soil confined in cylinders sunk in the ground outdoors and periodically cultivated. Seedling emergence was recorded for 5 years and the seasonal pattern of emergence was also determined. Peak emergence occurred in March–April and in greatest numbers in the first year (75% of seeds sown), a few seeds germinated in the following years, and an average of only 2.5% of the viable seed initially sown still remained after 5 years.
Slade & Causton (1979) assessed the effects of five potentially dormancy-breaking treatments; potassium nitrate, scarification, ethylene, light and stratification, on the germination of 13 deciduous woodland herbs under laboratory conditions. The seeds were air-dried and stored in the dark at room temperature and humidity for 6 months prior to the application of the five treatments in a complete factorial experiment. Seeds were then germinated at 18 °C. The best germination (70%) of the seed of Stachys sylvatica was achieved following stratification in the dark in an imbibed state for 6 weeks at 5 °C.
The seeds of Stachys sylvatica stored dry at 5 °C then placed on a thermogradient bar under warm white fluorescent tubes, providing a light flux of 18.46 W m−2 and a day length of 18 h, were subjected to a range of fluctuating temperatures by Thompson & Grime (1979). They recorded that the species required a large diurnal temperature fluctuation (9 °C) to achieve 50% of the maximum germination under the experimental conditions.
Graae et al. (2009) found that fresh seed of Stachys sylvatica, collected from a range of sites across central and north-western Europe, had a very low percentage germination (0–19%). After 18 weeks of cold stratification followed by 6 weeks of warm incubation (14 h light/20 °C and 10 h dark/10 °C) germination ranged from 13% to 54%. When seed was exposed first of all to 6 weeks of warm incubation followed by 18 weeks of cold incubation and finally 6 weeks of warm incubation, germination was increased to 50–91%.
Fröborg (2001) sowed seeds of a number of species including Stachys sylvatica in a deciduous forest in south-west Sweden. She then investigated the relationship between seed mass and seedling emergence in the presence and absence of litter. Removal of litter did not affect seedling emergence which was lower in Stachys sylvatica than in the species with larger seeds.
Jankowska-Blaszczuk & Daws (2007) investigated the relationship between seed mass, seed germination and light, in particular the R/FR. Unfiltered daylight has an R/FR of c. 1.2, but leaf canopies and the presence of leaf litter on the soil surface lower this to 0.1–0.2. They demonstrated experimentally that after cold stratification the germination of seeds of Stachys sylvatica and larger-seeded herbaceous species was independent of R/FR over the range 0–1.2, in contrast to small-seeded species in which there was a negative relationship between R/FR and germination.
(E) Seedling morphology
Germination is epigeal. Muller (1978) illustrates a seedling of Stachys sylvatica with the cotyledons, the first pair of leaves expanded and the second pair beginning to unfold. Two cotyledons, 4–6 mm, ovate, are somewhat wider than long with truncate base and petioles 2–8 mm. The first pair of opposite true leaves is ovate with base rounded-emarginate 6–15 mm, crenate and petioles 2–7 mm. Both the hypocotyl (3–9 mm) and the epicotyl (1–7 mm) are herbaceous. The seedlings are covered in multicellular ± glandular hairs of varying lengths.
IX. Herbivory and disease
(A) Animal feeders
A list of the insects feeding on Stachys sylvatica is presented in Table 4. The larvae of numerous phytophagous insects, especially the caterpillars of Lepidoptera, feed on the plant. The Woundwort Shieldbug (Eysarcoris venustissimus) is particularly associated with Stachys sylvatica in southern Britain. Gange, Stagg & Ward (2002) found that the aphis Cryptomyzus ribis showed increased growth on mycorrhizal plants relative to their growth on non-mycorrhizal plants.
|Eriophyes solidus Nalepa||Both larvae and adults feed||2|
|Cassida viridis L.||Both larvae and adults feed on leaves||17|
|Ceutorhynchus urticae Boheman||Adults feed from March–October||12|
|Datonychus urticae (F.)||Larvae feed||15|
|Meligithes brunnicornis Sturm||Larvae feed on flower buds||13|
|Amauromyza labiatarum (Hendel)||Larvae mining leaves||19|
|Ophiomyia labiatarum Hering||Larvae mining stems||21|
|Cyrtodiplosis crassinerva (Kieffer)||Larvae galling on flower buds||8|
|Ametrodiplosis crassinerva (Kieffer)||Larvae galling on flower buds||8|
|Macrolabis heraclei (Kaltenbach)||Larvae feed on leaves June–September||4|
|Wachtliella stachydis (Bremi)||Larvae feed on flower buds and leaves, galling||7|
|Eupteryx stachydearum (Hardy)||Larvae feed on leaves||14|
|Hauptidia maroccana (Melichar)||Larvae feed||18|
|Dicyphus constrictus (Boheman)||Partly predacious||20|
|Dicyphus errans (Wolff, J.F.)||Partly predacious larvae and adults (June–October)||20|
|Dicyphus stachydis Reuter||Larvae and adults feed||20|
|Macrolophus nubilis (Herrich-Schaffer)||Larvae and adults feed||20|
|Macrotylus solitarius (Meyer-Dur)||Larvae and adults feed||20|
|Eysarcoris venustissimus (Schrank)||Larvae and adults feed on flowers, fruits and seeds||20|
|Crptomyzus korschelti Börner, C.II||Larvae and adults feed on shoots and leaves||6|
|Crptomyzus ribis (L.)II||Larvae and adults feed on shoots and leaves||6|
|Lysandra bellargus (Rottemberg)||Larvae feed||5|
|Pseudopanthera macularia (L.)||Larvae feed||1, 22|
|Perizoma alchemillata (L.)||Larvae feed on fruits, seeds and flowers||1, 22|
|Phlogophora meticulosa (L.)||Larvae feed on leaves||16|
|Autographa jota (L.)||Larvae feed on leaves||1, 16|
|Autographa pulchrina (Haworth)||Larvae feed||22|
|Coleophora lineola (Haworth)||Larvae feed on leaves, mining||9, 10|
|Ambylyptilia acanthadactyla (Hubner)||Larvae feeds on fruits, seeds and flowers||9, 11|
|Ambylyptilia punctidactyla (Haworth)||Larvae feed on fruits and seeds||9, 11|
|Phlyctaenia stachydalis (Germar)||Larvae feed on leaves, webbing||9|
|Endothenia ericetana (Humphreys & Westwood)||Larvae feed on roots and stems, mining||9, 11|
|Endothenia nigricostana (Haworth)||Larvae feed on roots and stems, mining||9, 11|
|Endothenia quadrimaculana (Haworth)||Larvae feed on roots and stems||11|
|Cnephesia asseclana (Denis & Schiffermuller)||Larvae feed on leaves, mining||3|
|Cnephesia stephensiana (Doubleday)||Larvae feed on leaves, mining, webbing||3|
- Sources: 1, Allan (1949); 2, Bagnall & Harrison (1928); 3, Balmer (1982); 4, Barnes (1946); 5, Blab & Kudrna (1982); 6, Börner (1952); 7, Buhr (1964); 8, Buhr (1965); 9, Emmet (1988); 10, Emmet (1996); 11, Emmet & Heath (1991); 12, Hoffmann (1954); 13, Kirk-Spriggs (1996); 14, Le Quesne & Payne (1981); 15, Morris (1982);16, K. Noble, unpublished data; 17, Read (1984);18, Ribaut (1936); 19, J. Robbins, unpublished data; 20, Southwood & Leston (1959); 21, Spencer (1972); 22, Waring & Townsend (2003).
(B) Associated fungi
|Peronospora lamii (Lib.) Corda||A downy mildew which forms greyish-brown or greyish-lilac patches on the yellowed leaves, September and May.|
|Ramularia lamii Sacc.||Leaf spots|
|Ramularia stachydis Sacc.||Leaf spots|
|Septoria stachydis Fr.||Leaf spots|
|Anguillospora crassa Ingold|
|Melanomma pulvis-pyrius Nitschke ex Fuckel||On dead stems|
|Ophiobolus erythrosporus Riess||On dead stems|
|Phoma exigua Sacc.||On dead leaves|
|Neoerysiphe galeopsidis (DC.) U. Braun||A powdery mildew occurring on the living leaves|
|Botrytis cinerea P.Michelli ex Pers.||Grey mould on dead plants, often parasitic on stems, leaves, flowers and fruit|
|Calycina herbarum Nees ex Gray||On dead stems|
|Crociceras cyathoideum var. cyathoideum Fr.||On dead stems|
|Mollisia sp. (Fr.) P. Karst||On dead stems|
|Unguiculella hamulata Höhn.||On dead stems|
|Nectria cinnabarina (Fr.) Fr.||Coral spot on leaves|
|Phomatospora berkeleyi Sacc.||On dead stems|
|Pleurophragmium parvisporum Constantin||On dead stems|
|Entoloma papillatum (Fr.) P. Kumm||On soil in contact with roots|
|Lachnella villosa Fr.||On dead stems|
|Lacrymaria lacrymabunda Pat.||On dead stems|
|Mycena arcangeliana (Pers.) Roussel||On dead leaves|
|Simocybe sumptuosa P. Karst||On dying leaves|
|Tricholoma argyraceum (Fr.) Staude|
|Phlebiella sulphuria P. Karst|
|Puccinia hieracii var hieracii Pers.||Leaf and stem rust|
|Russula vesca Pers.||On dying leaves|
- Source: British Mycological Society (2010).
Ascomycota: Erisyphales, Neoerysiphe galeopsidis, a powdery mildew on living leaves of Galeopsis spp. and on Stachys sylvatica. Details of the infection of Stachys sylvatica are described by Pastirčáková, Ivanová & Bernadovičová (2008).
Ascomycota: Capnodiales, Septoria stachydis. On living leaves of Stachys sylvatica and Stachys palustris, causing dark brown spots, June–November.
In the Pleistocene stage, nutlets of Stachys sylvatica have been recovered from the Cromer Forest Bed series and the Cromerian interglacial itself. It occurred in the late Anglian and also in sub-stage II of the ensuing Hoxnian interglacial. Flandrian zone VIIb and VIII records all have an archaeological context: Neolithic, Bronze Age, Roman and Mediaeval (Godwin 1975).
The first historical record is for 1629 from Kent (Atkins & Atkins 2004). The name ‘Woundwort’ derives from its traditional use in staunching the flow of blood and healing wounds. “The leaves hereof stampt with Axungia or hogs grease, and applied unto greene wounds in manner of a pultesse, heale them in short time, and in such absolute manner, that it is hard for any that have not had the experience thereof to beleeve...” (Gerard 1636).
There is no evidence for a change in the overall distribution of Stachys sylvatica which is widespread in the British Isles (Preston, Pearman & Dines 2002). No specific measures appear to be necessary to conserve the species. It is the food plant of the larvae of a number of butterflies and other phytophagous insects listed in Table 3.
The potential impact of herbicide drift on Stachys sylvatica and other species in nature reserves and field margin habitats has been studied experimentally by Marrs, Frost & Plant (1991). The herbicide drift downwind (0–8 m) of a standard agricultural sprayer applying mecoprop at recommended rates enhanced the growth of Stachys sylvatica, although six other species showed evidence of reduction in performance.
We thank Colin Harrower, Biological Records Centre, for providing the maps for 1, 3, and Sven Koeltz for granting permission to reproduce the European distribution map (Fig. 2). We gratefully acknowledge the useful comments of Tony Davy on the text and for his detailed editing of the final manuscript.
- 1984) Studies on nitrate reductase in British angiosperms I. A comparison of nitrate reductase activity in ruderal, woodland-edge and woody species. New Phytologist, 97, 629– 639. & (
- 1949) Larval Foodplants. Watkins & Doncaster, London, UK. (
- 2004) Medicinal Plants in Folk Tradition: An Ethnobotany of Britain & Ireland. Timber Press, Portland, USA. & (
- 1989) The Chemical Analysis of Ecological Materials, 2nd edn. Blackwell Scientific Publications, Oxford, UK. , , & (
- 2008) Indigenous plant species for the phytomediation of arsenic and metals contaminated soils. Water Air and Soil Pollution, 193, 197– 210. , , & (
- 2004) First Records of British Flowering Plants. Anthony Rowe, Eastbourne, UK. W. A. Clarke (1900, 1909) reprinted with corrections. & (
- 1928) A catalogue of the British Eriophyidae. Annals and Magazine of Natural History, 1, 427– 445. & (
- 1972) Stachys L. Flora Europaea, Vol. 3 (eds T.G. Tutin, V.H. Heywood, N.A. Burges, D.M. Moore, D.H. Valentine, S.M. Walters & D.A. Webb), pp. 151– 157. Cambridge University Press, Cambridge, UK. (
- 1982) Vergleichende Untersuchungen zur Biologie schweizerischer Cnephasini (Lep Tortricidae). Mitteilungen der Sweizerischen Entomologischen Gesellschaft, 55, 349– 382. (
- 1999) Polyphenols in Stachys and Betonica species (Lamiaceae). Zeischrift für Naturforschung Section C, 54, 876– 880. , , , , & (
- 1946) Gall Midges of Economic Importance. Vol 1 Root and Vegetable Crops. Crosby Lockwood, London, UK. (
- 1909) On an abnormal gynoecium in Stachys sylvatica, Linn. New Phytologist, 8, 138– 142. (
- Biological Records Centre (2010) Database of Insects and their Food Plants. Available at: http://www.brc.ac.uk/dbif/ (accessed February 2010).
- 1982) The main types of woodland in North Scotland. Phytocoenologia, 10, 9– 55. (
- 1976) Plant Communities and Soils of the Lowland and Southern Upland Regions of Scotland. The Macaulay Institute for Soil Research, Craigiebuckler, Aberdeen, UK. & (
- 1982) Hilfsprogramm für Schmetterlinge, pp. 1– 135. Kilda-Verlag, Graven, Germany. & (
- 1952) Europae centralis Aphides. Mitteilungen des Thüringischen botanischen Gesellschaft, 4, 1– 484. (
- British Mycological Society (2010) Fungal Records Database of Britain and Ireland. Available at: http://www.fieldmycology.net/FRDBI/assoc.asp (accessed February 2010).
- 1964) Bestimmungstabellen der Gallen (Zoo- und Phytocecidien) an Pflanzen Mittel- und Nordeuropas, Vol. 1, pp. 1– 761. Fischer, Jena, Germany. (
- 1965) Bestimmungstabellen der Gallen (Zoo- und Phytocecidien) an Pflanzen Mittel- und Nordeuropas, Vol. 2, pp. 762– 1572. Fischer, Jena, Germany. (
- 1983a) Growth and morphogenesis of sun and shade plants II. The influence of light quality. Acta Botanica Neerlandica, 32, 185– 202. (
- 1983b) Growth and morphogenesis of sun and shade plants III. The combined effects of light intensity and nutrient supply. Acta Botanica Neerlandica, 32, 277– 294. (
- 1984) Growth and morphogenesis of sun and shade plants IV. Competition between sun and shade plants in different light environments. Acta Botanica Neerlandica, 33, 25– 38. (
- 1921) Observations on variations in the flowers of Stachys sylvatica, Linn. Annals of Botany, 35, 409– 425. (
- 1988) Vegetation Ecology of Central Europe, 4th edn. Cambridge University Press, Cambridge, UK. (
- 1997) Microfungi on Land Plants: An Identification Handbook, 2nd edn. Croom-Helm, London, UK. & (
- 1988) A Field Guide to the Smaller British Lepidoptera, 2nd edn. The British Entomological and Natural History Society, London, UK. , ed. (
- 1996) The Moths and Butterflies of Great Britain and Ireland, Vol. 3, Yponomeutidae to Elachistidae. Harley Books, Colchester, UK. , ed. (
- 1991) The Moths and Butterflies of Great Britain and Ireland, Vol. 7 Part 2, Lasiocampidae to Thyatiridae. Harley Books, Colchester, UK. & (
- 2002) Flora of Assynt. Privately published. , & (
- 1999) The responses of seven co-occurring woodland herbaceous perennials to localized nutrient rich patches. Journal of Ecology, 87, 849– 859. & (
- 2001) Seed size and seedling emergence in 16 temperate forest herbs and one dwarf shrub. Nordic Journal of Botany, 21, 373– 384. (
- 1991) Forage for bumble bees and honey-bees in farmland. Journal of Apicultural Research, 30, 87– 97. & (
- 2002) Arbuscular mycorrhizal fungi affect phytophagous insect specialism. Ecology Letters, 5, 11– 15. , & (
- 1988) Nitrate, nitrate reduction and organic nitrogen in plants from different ecological and taxonomic groups of Central Europe. Oecologia, 75, 371– 385. , & (
- 1636) The Herball or Generall Historie of Plantes. (edn of Thomas Johnson), London, UK. (
- 2008) Insight into the structure and chemistry of glandular trichomes of Labiatae, with emphasis on subfamily Lamiodeae. Plant Systematics and Evolution, 276, 199– 208. & (
- 1975) The History of the British Flora, 2nd edn. Cambridge University Press, Cambridge, UK. (
- 2009) Germination requirements and seed mass of slow-and fast-colonizing temperate forest herbs along a latitudinal gradient. Ecoscience, 16, 248– 257. , , , , , et al. (
- 2007) Comparative Plant Ecology: A Functional Approach to Common British Species, 2nd edn. Castlepoint Press, Colvend, UK. , & (
- 1990) The influence of sheep and cattle grazing on wooded meadows in Åland, SW Finland. Acta Botanica Fennica, 141, 1– 28. (
- 1997) A Flora of Cumbria. Centre for North West Regional Studies, University of Lancaster, Lancaster, UK. (
- 1987) A check-list of mycorrhiza in the British flora. New Phytologist, 105(Suppl.), 1– 102. & (
- 1973) Nitrogenase activity in the rhizosphere of Stachys sylvatica and some other dicotyledonous plants. Soil Biology and Biochemistry, 5, 277– 279. & (
- 1957) Studies on vesicular-arbuscular endophytes I. A strain of Pythium ultimum Trow in roots of Allium ursinum L. and other plants. Transactions of the British Mycological Society, 40, 375– 390. , , & (
- 1999) An ecological comparison between ancient and other forest plant species of Europe, and the implications for forest conservation. Biological Conservation, 91, 9– 22. , , , & (
- 2004) PLANTATT. Attributes of British and Irish Plants: Status, Size, Life History, Geography and Habitats. Centre for Ecology and Hydrology, Huntingdon, UK. , & (
- 1954) Coléoptères Curculionides. Faune de France, 59, 487– 1208. (
- 1986) Atlas of North European Vascular Plants North of the Tropic of Cancer, Vols II & III. Koeltz Scientific Books, Königstein, Germany. & (
- 2007) Impact of red: far red ratios on germination of temperate forest herbs in relation to shade tolerance, seed mass and persistence in the soil. Functional Ecology, 21, 1055– 1062. & (
- 1996) Pollen Beetles. Coleoptera: Kateretidae and Nitidulidae: Meligethinae. Handbooks for the Identification of British Insects, Vol. 5 (6a), Royal Entomological Society of London, London, UK. (
- 1909) Handbook of Flower Pollination, Vol. 3 (translated by J.R. Ainsworth Davis). University Press, Oxford, UK. (
- 1981) Handbooks for the Identification of British Insects, Vol. 2 (2c), pp. 9– 36. Royal Entomological Society of London, London, UK. & (
- 2009) Air humidity, soil moisture and soil chemistry as determinates of the herb layer composition in European beech forests. Journal of Vegetation Science, 20, 288– 298. & (
- 1991) Effect of mecoprop drift on some plant species of conservation interest when grown in standardized mixtures in microcosms. Environmental Pollution, 73, 25– 42. , & (
- 1978) Flora of Moray, Nairn & East Inverness. Aberdeen Úniversity Press, Aberdeen, UK. (
- 2010) Flora Iberica: Volume 12. Verbenaceae-Labiatae-Callitrichaceae. Real Jardín Botánico, CSIC, Madrid, Spain. , , , & , eds (
- 1982) Dorset weevils (Coleoptera, Circulionoidea): additional critical and notable species 1968–1982. Proceedings of the Dorset Natural History and Archaeological Society, 104, 159– 164. (
- 1973) A cytological study of the British Labiatae (excluding Mentha). Watsonia, 9, 239– 246. (
- 1978) Seedlings of the North-Western European Lowland. Centre for Agricultural Publishing and Documentation, Wageningen, and Dr W. Junk, The Hague, The Netherlands. (
- 2008) Neoerysiphe galeopsidis on Stachys species in Slovakia and the Czech Republic based on a re-examination of herbarium collections. Czech Mycology, 60, 251– 264. , & (
- 2004) Altitudinal Limits of British and Irish Vascular Plants, 2nd edn. Botanical Society of the British Isles, London, UK. & (
- 2008) The Flora of Rum: An Atlantic Island Reserve. Privately published, Truro, UK. , , & (
- 1981) Woodland Conservation and Management. Chapman & Hall, London, UK. (
- 1997) The geographical relationships of British and Irish vascular plants. Botanical Journal of the Linnean Society, 124, 1– 120. & (
- 2002) New Atlas of the British and Irish Flora. Oxford University Press, Oxford, UK. , & (
- 1996) The Natural History of Pollination. Harper Collins, London, UK. , & (
- 1984) Cassida viridis (Coleoptera: Chrysomelidae). Entomologists’ Record and Journal of Variation, 96, 30– 31. (
- 1960) Saugkraftmessungen an Stachys sylvatica im frischen und welken Zustand. Bericht der Deutschen Botanischen Gesellschaft, 73, 82. (
- 1936) Homoptères Auchenorhynques(Typhlocybidae). Faune de France, 31, 1– 228. (
- 1984) Seed survival and seasonal emergence of seedlings of some ruderal plants. Journal of Applied Ecology, 21, 617– 628. & (
- 1991) British Plant Communities. I. Woodlands and Scrub. Cambridge University Press, Cambridge, UK , ed. (
- 1992) British Plant Communities. III. Grassland and Montane Communities. Cambridge University Press, Cambridge, UK. , ed. (
- 2000) British Plant Communities. V. Maritime Communities and Vegetation of Open Habitats. Cambridge University Press, Cambridge, UK. , ed. (
- 2000) Review of Coverage of the National Vegetation Classification. Joint Nature Conservation Committee Report, No. 302. J.N.C.C. in house, Peterborough, UK. , , , , , & (
- 1916) The oak-hornbeam woods of Hertfordshire, parts I and II. Journal of Ecology, 4, 83– 117. (
- 1918) The oak-hornbeam woods of Hertfordshire, parts III and IV. Journal of Ecology, 6, 14– 52. (
- 1925) The structure of woodlands. Veröffentlichungen des Geobotanischen Institutes Rübel in Zürich, 3, Festschrift Carl Schröter, (ed. H. Brockman-Jerosch), pp. 334– 354. Hans Huber, Bern, Switzerland. (
- 1927) On the causes and ecological significance of stomatal frequency, with special reference to the woodland flora. Philosophical Transactions of the Royal Society, 216B, 1– 65. (
- 1942) The Reproductive Capacity of Plants. G. Bell, London, UK. (
- 1961) Weeds and Aliens. Collins, London, UK. (
- 2009) Flora of Great Britain and Ireland, Vol. 3, Mimosaceae – Lentibulariaceae. Cambridge University Press, Cambridge, UK. & (
- 1979) The germination of some woodland herbaceous species under laboratory conditions: a multifactorial study. New Phytologist, 83, 549– 557. & (
- 1981) Light quality as an ecological factor. Plants and their Atmospheric Environment (eds J. Grace, E.D. Ford & P.G. Jarvis), pp. 93– 110. Blackwell Scientific Publications, Oxford, UK. (
- 1959) Land and Water Bugs of the British Isles. Warne, London, UK. & (
- 1972) Diptera: Agromyzidae. Handbook for the Identification of British Insects, Vol.10 (5G). Royal Entomological Society of London, London, UK. (
- 2004) Interactive Flora of the British Isles (DVD-ROM) (eds R. Van Der Meijden & I. De Kort). ETI Information Services Ltd, University of Amsterdam, Amsterdam, The Netherlands. (
- 2010) New Flora of the British Isles, 3rd edn. Cambridge University Press, Cambridge, UK. (
- 1999) Querco-Fagetea. De Vegetatie van Nederland, Deel 5. Pflanzengemeenschappen van ruigten, struwelen en bossen (eds A.F.H. Stortelder, J.H.J. Schaminée & P.W.F.M. Hommel), pp. 287– 331. Opulus Press, Leiden, The Netherlands. , & (
- 1979) Seasonal variation in the seed banks of herbaceous species in ten contrasting habitats. Journal of Ecology, 67, 893– 921. & (
- 1997) A comparative study of leaf nutrient concentrations in a regional herbaceous flora. New Phytologist, 136, 679– 689. , , & (
- 2003) Field Guide to the Moths of Great Britain and Ireland. British Wildlife Publishing, Hook, Hampshire, UK. & (
- 1994) Seed bank composition and variability in five woodlands in south-west England. Journal of Biogeography, 21, 151– 168. , & (
- 1932) British beechwoods. Die Buchenwälder Europas (ed. E. Rübel). Veröffentlichungen des Geobotanischen Institutes Rübel in Zürich, 8, pp. 1– 69. Hans Huber, Bern, Switzerland. & (
- 1972) Is Stachys×ambigua Sm. always distinguishable? Watsonia, 9, 62. (
- 1973) The experimental taxonomy of Stachys × ambigua Sm., S. palustris L. and S. sylvatica L. in Britain. PhD Thesis, University of London, UK. (
- 1974) Population variation, differentiation and reproductive biology of Stachys palustris L. S. sylvatica L. and S. × ambigua Sm. New Phytologist, 73, 1233– 1241. (
- 1974) The identification and origin of Stachys x ambigua Sm. Watsonia, 10, 139– 147. & (
- 1993) Non invasive imaging of water flow in plants by NMR microscopy. Protoplasma, 173, 170– 176. , , & (