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Journal of Ecology 2007 95, 583–597

BIOLOGICAL FLORA OF THE BRITISH ISLES *

Blackwell Publishing Ltd

No. 246

List Br. Vasc. Pl. (1958) no. 434, 4

Biological Flora of the British Isles: Melampyrum sylvaticum L. SARAH E. DALRYMPLE School of Biological Sciences, University of Aberdeen, Cruickshank Building, St Machar Drive, Aberdeen AB24 3UU, UK

Summary 1 This account reviews information on all aspects of the biology of Melampyrum sylvaticum 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 Melampyrum sylvaticum is a hemiparasitic annual of upland, often birch-dominated woodlands. It is found across boreal and montane areas of Europe but within the UK it is predominantly found in the Scottish Highlands. These populations are consequently very isolated and vulnerable to a range of threats. Suitable habitat is characterized by open-canopied deciduous woodland close to water bodies, such as fast-flowing burns or lochs. Sites are typically north-facing, in cool and wet areas of Britain, on moderately acidic soils that are moist but freely draining. 3 Hemiparasitism allows M. sylvaticum to acquire nutrients from a range of hosts but very little is known about which species it is able to parasitize in the field. Melampyrum sylvaticum is associated with herb-rich patches of the understorey. 4 Melampyrum sylvaticum is insect-pollinated. Ants have been reported to be the main dispersal agents and the seed bears an elaiosome which offers them a lipid-rich reward. However, neither insect pollination nor ant dispersal has been observed directly in British populations. 5 Melampyrum sylvaticum has relatively large seeds and been described as an ‘annual K-strategist’; it has been suggested that this unusual combination makes it vulnerable to environmental change. Because of its endangered status, M. sylvaticum has been classed as a UK Biodiversity Action Plan species and a recovery project is underway to protect existing populations and to introduce it to suitable habitats in the Central Highlands of Scotland. Key-words: climatic limitation, communities, conservation, ecophysiology, geographical and altitudinal distribution, germination, hemiparasite, herbivory, parasites and diseases, reproductive biology, soils Journal of Ecology (2007) 95, 583–597 doi: 10.1111/j.1365-2745.2007.01234.x

Scrophulariaceae, Tribe Pedicularieae (Rhinantheae). Small cow-wheat. Melampyrum sylvaticum L. is a facul-

© 2007 The Author Journal compilation © 2007 British Ecological Society

Correspondence: Sarah Dalrymple (e-mail s.e.dalrymple @abdn.ac.uk) *Abbreviated references are used for many standard works: see Journal of Ecology (1975), 63, 335–344. Nomenclature of vascular plants follows Flora Europaea and, where different, Stace (1997).

tatively hemiparasitic summer annual (therophyte). Stems erect, simple or branched and up to 400 mm. Branches ascending, in opposite pairs. Base of both stem and branches softly hairy and tinged red-brown in larger plants. Hairs occur in two opposite rows on stem or branches in the plane perpendicular to branch or leaf emergence. Leaves 40–70 mm × 6–15 mm, cauline, opposite and decussate, sessile, linear–lanceolate and entire, broadest at about 1/4 of length of leaf from base.

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© 2007 The Author Journal compilation © 2007 British Ecological Society, Journal of Ecology, 95, 583–597

Very loose, racemose, terminal inflorescence, with (1–) 3–10 floral nodes bearing pairs of flowers facing the same way; bracts leaf-like but decreasing in size up the stem; upper bracts of larger individuals may rarely have ≤ 2 pairs of small teeth at bract base. Inflorescences on branches similar in structure to, but smaller than, those on main stem. Calyx 4-toothed, spreading, green although sometimes tinged purple at base, more or less equal to length of corolla tube. Corolla 8–12 mm, petals fused into conical tube with two lips, deep yellow turning orange prior to senescence. Lower lip deflexed, 3-lobed although central lobe is sometimes very reduced. Upper lip forms hood concealing stamen and style, with yellow hairs on underside. Stamens 4, didynamous. Capsule narrowly ovoid, acuminate, dehiscing dorsally (1–) 2– 4 seeds. Seeds ovoid, yellow brown, with pale elaiosome becoming black after dehiscence, 4.3 × 2.4 mm, c. 18 mg. The genus Melampyrum includes c. 30 species spread across much of the temperate and low Arctic areas of the Northern Hemisphere. The centre of its diversity, where two-thirds of the species in the genus can be found, is in south-east Europe and the Caucasus (Hong 1983). Species within the genus Melampyrum are often highly variable, showing a great deal of ecotypic variation, and M. sylvaticum is no exception, particularly in its southern European distribution (Stech & Drábková 2005). However, in Britain, its morphology was noted as being much more uniform, with height the most inconsistent characteristic (Rich et al. 1998). Height is typically highly variable in hemiparasitic summer annuals, depending on time of germination; plants of later cohorts are appreciably smaller than earlier emergents, and the presence of a suitable host species also affects biomass and height (Svensson et al. 2001; Svensson & Carlsson 2004). The identification of various forms of Melampyrum sylvaticum has resulted in regular reassessment of what constitutes a species, subspecies or variety. Melampyrum sylvaticum has been assigned up to seven subspecies across its European range (Soó 1927, cited in Rich et al. 1998), of which the British material was said to be represented by two: ssp. aestivale Ronn. (English and Irish plants; described as an ecotypic variant by Soó & Webb 1972), and ssp. subsilvaticum Schinz and Ronn (Scottish plants; Salmon 1929; Britton 1943). Individuals from the Aberfeldy, Perthshire, population of the latter subspecies have been assigned to var. toddae by Britton (1943) but, using the molecular technique of RAPD (randomly amplified polymorphic DNA) analysis, Sharp (2003) refuted this level of taxonomic separation by demonstrating that the population is not genetically distinct from others in Scotland. Sharp (2003) demonstrated that despite this lack of genetic distinctiveness at subspecies level, the Scottish populations are isolated and genetically divergent. Of the total genetic diversity identified by Sharp (2003) in seven Scottish populations, 76.7% was attributable to differences between the populations.

I. Geographical and altitudinal distribution The westernmost extent of the range of Melampyrum sylvaticum is in the British Isles, where it has been reported at 48 sites since 1950 (Fig. 1); of these, 40 are in Scotland, seven in Northern Ireland and one is in England. Despite the relatively large number of sites in Scotland, only 20 sites have been confirmed in the Scottish Highlands since 2000 and two of these may have been lost since then (Paul Gallagher, pers. comm.). The British altitudinal range extends from c. 20 m on the Isle of Lismore in Loch Linnhe, Argyllshire (Paul Gallagher, pers. comm.), to 760 m on Aonach air Crith, Wester Ross (Rumsey 1994), although Corner (1975) observed that M. sylvaticum is ‘rather rare’ above 615 m. The distribution of Melampyrum sylvaticum is described as European boreal-montane by Hill et al. (2004). It can be found in the mountains of the Alps (where it has been recorded at 1900 m, Stech & Drábková 2005), the Pyrenees, Central Italy and the Emilia-Romagna region (Alessandri & Branchetti 1987, cited in Rich et al. 1998), and southern Bulgaria. However, the majority of the range is in northern Europe encompassing Fennoscandia and extending into north-west Russia (Fig. 2). The altitudinal limit of M. sylvaticum in northern Europe is 1350 m, in the Jotunheimen mountains, Norway (Lid 1963).

II. Habitat (  )      

In Europe, Melampyrum sylvaticum is assigned to the boreal-montane element of the flora (Preston & Hill 1997). In Britain the distribution of M. sylvaticum reflects this, being found in Northern Britain only and generally in upland areas. The climatic limitations of M. sylvaticum are determined by a combination of elevation and latitude; the mean January temperature of 10-km squares where it occurs in Britain is 1.5 °C and the mean July temperature only 12.5 °C (Hill et al. 2004). Conolly & Dahl (1970) state that the mean annual maximum temperature limiting M. sylvaticum distribution is 23 °C although it is too restricted in the area to achieve a correlation with the 23 °C isotherm. Of eight Scottish M. sylvaticum populations surveyed by Dalrymple (2006) in order to describe M. sylvaticum habitats, the majority of the sites were classified in the ‘cool wet’ climatic zone (Table 1), which includes much of Highland Scotland and 19.8% of the British land area (Pyatt et al. 2001). Other sites were classified as ‘cool moist’ or ‘subalpine’ types. These climate types are derived from a combination of two measures. The first is accumulated day-degrees above a threshold temperature of 5 °C (abbreviated to AT5); M. sylvaticum populations were found to occupy the cooler regions within a range of 441–1110 AT5 (the UK maximum is 2000). The second measure indicates humidity by using the moisture deficit values (monthly rainfall subtracted

585 Melampyrum sylvaticum

Fig. 1 The distribution of Melampyrum sylvaticum in the British Isles. Each dot represents at least one record in a 10-km square of the National Grid. Native () pre-1950, () 1950 onwards. Mapped by H.R. Arnold, using Dr A. Morton’s DMAP software, Biological Records Centre, Centre for Ecology and Hydrology, Monks Wood, mainly from data collected by members of the Botanical Society of the British Isles.

from monthly evaporation); M. sylvaticum populations are found in sites with moisture deficit values of 0– 106 mm (the UK moisture deficit maximum is 240 mm). Melampyrum sylvaticum populations in Scotland were generally found on north-facing slopes indicating an ecological requirement for cooler sites that are not subjected to full sunlight (Dalrymple 2006). The degree of slope at eight sites in Scotland ranged from 10° to 41°. In Abisko National Park, Sweden, M. sylvaticum is not restricted to north-facing slopes and the range of slope was 0–28° (Dalrymple 2006). () © 2007 The Author Journal compilation © 2007 British Ecological Society, Journal of Ecology, 95, 583–597



The substrates supporting Melampyrum sylvaticum are acidic and therefore typical of upland Britain. The bedrock is commonly composed of metamorphic schists and gneisses, although metasedimentary sequences occasionally result in limestones forming the substrate upon which M. sylvaticum grows, for example on the

Isle of Lismore and Mar Lodge Estate, Aberdeenshire. Soils are fairly shallow, having developed from leaflitter and grit deposition on bedrock (Rich et al. 1998). The underlying rock is often visible as surface outcrops, between the pockets of soil that support trees and the understorey community (pers. observ.). Ellenberg indicator values reported in Hill et al. (2004) represent M. sylvaticum as occurring on acidic soils of average dampness and low fertility. The pH of the soils at eight sites supporting M. sylvaticum in Britain ranged from 3.9 to 4.7 and soil moisture recorded in situ in July 2004 was 11.2–24.1% (Dalrymple 2006; Table 1). Melampyrum sylvaticum is associated with National Vegetation Classification communities that are found on soils that do not undergo periodic drought (Rodwell 1991a,b; Rodwell 1992). Soil fertility at M. sylvaticum sites is low and classified as infertile according to Ellenberg values for nitrogen (Hill et al. 2004). Dalrymple (2006) sampled soil at eight Scottish populations to determine extractable nitrogen and phosphorus content

586 S. E. Dalrymple

Fig. 2 European distribution of Melampyrum sylvaticum (redrawn from Meusel & Jäger 1992). Table 1 Environmental variables measured and other attributes for Melampyrum sylvaticum sites. Variables were determined as a single value for the site (indicated by *) or as means of n quadrat values. Soil moisture values were not obtainable within an acceptable time at Tilt, and so were omitted. Data summarized from Dalrymple (2006) Site

Environmental variable Population size National Grid reference Altitude (m a.s.l.)* Aspect* Slope (°)* Distance from water (m) Climate type* AT5 (day deg. > 5 °C)* Moisture deficit (mm)* NVC community Soil moisture in July (%) Soil pH Soil phosphate (mg kg−1) Soil nitrate (mg kg−1) Soil ammonium (mg kg−1) Soil organic matter (%)

M n=5

E n=6

A n=6

O n = 10

Ab n=6

T n=5

K n=2

N n=3

90 NO 039988 640 320 41 10.56 Sub-A 441 0 H18 23.1 4.4 9.17 5.28 3.12 9.9

> 800 NH 060176 460 300 25 2.5 C-W 668 3 U16 27.3 4.3 8.29 11.6 9.84 25.9

200 NH 071177 440 330 38 6.87 C-W 692 9 U16 22.6 3.9 56.5 18.5 16.0 35.1

1000 NN 401682 400 320 15 9.6 C-W 815 28 U16 22.7 4.5 6.04 3.84 8.18 41.0

1700 NN 851472 280 340 26 17.17 C-W 927 70 W11 17.0 4.3 15.4 5.69 5.36 39.8

> 8000 NN 880690 200 286 22 18.9 C-W 1113 89 W11 – 4.6 20.6 0.99 38.7 70.1

37 NN 769497 180 225 12 15.1 C-M 1207 94 U20 15.0 4.7 4.68 4.26 7.80 17.7

87 NH 767447 110 340 10 8.03 C-M 1110 106 W11 11.2 4.2 1.24 2.54 6.26 14.0

Sites: M = Mar Lodge, Aberdeenshire; E = Eiridh, Ross & Cromarty; A = Athair, Ross & Cromarty; O = Loch Ossian, Westerness; Ab = Aberfeldy, Perthshire; T = Glen Tilt, Perthshire; K = Keltneyburn, Perthshire; N = River Nairn, Easterness. Climate types: Sub-A = Sub-alpine; C-W = Cool-wet; C-M = Cool-moist. Soil pH was determined using a pH meter (RS Components, Corby, UK) and soil moisture was recorded in situ with a Theta probe (Delta-T Devices, Cambridge, UK). Inorganic nitrogen and phosphorus were extracted using KCL and acetic acid, respectively, to determine extractable nitrate, ammonium and phosphate using a Flow Injection Analyser (Foss Tecator Ltd, Warrington, UK). Organic matter content was determined as loss-on-ignition (550 °C for 2 h).


(Table 1). Nitrate ranged from 0.99 to 18.5 mg kg−1 dry mass and ammonium from 3.12 to 16.0 mg/kg dry mass (with an outlying maximum of 38.7 mg kg−1 dry mass). Soil phosphate was very variable, generally ranging from 1.24 to 20.6 mg kg−1 dry mass, with a maximum of 56.5 mg kg−1 dry mass. Organic matter ranged from 9.9 to 70.1%.

III. Communities Melampyrum sylvaticum is associated with deciduous upland woodland, although this is sometimes limited to a few stunted trees alongside ravines, where grazing pressure is low. Rodwell (1991a,b, 1992) does not include


M. sylvaticum in any species lists of the National Vegetation Classification. In a survey of eight M. sylvaticum populations across an altitudinal range of 110–640 m, the majority of communities were W11 Quercus petraea– Betula pubescens–Oxalis acetosella woodland, with some U16 Luzula sylvatica–Vaccinium myrtillus tall-herb communities at sites around 400 m elevation and close matches with W17 Quercus petraea–Betula pubescens– Dicranum majus woodland communities throughout the range of elevations. W17 is very similar to W11 but occurs on more base-poor soils. Other communities identified by MATCH software (version 2.1, Unit of Vegetation Science, University of Lancaster 1997) include H18 Vaccinium myrtillus– Deschampsia flexuosa heath at a site on the Mar Lodge Estate, which represents the highest part of an altitudinal transition from W11 through W17 to H18 woodlands, and includes U16 where grazing pressures are minimal but the community has been unable to develop into scrub or pioneer woodland (Dalrymple 2006). All NVC communities occupied by Melampyrum sylvaticum occur in wet and cold upland habitats where soils are acidic, thin and free-draining but continually moist. A species list compiled from three Melampyrum sylvaticum populations at Keltneyburn, Aberfeldy and Loch Ossian extended to 56 species. Ecological characteristics of the 38 vascular species were determined using Grime et al. (1988), Stace (1997) and Preston et al. (2002). Species were then categorized according to their preference for key environmental conditions that have been identified by Rich et al. (1998) as being of particular relevance to M. sylvaticum: tolerance of slightly acid conditions, tolerance of shade, an upland or montane altitudinal range and occurrence in habitats that were characterized by low productivity, low disturbance, and communities primarily composed of perennial species. Their distributions were also classified as either widespread or being restricted to certain regions of the British Isles (Fig. 3). Eleven species were

grasses, 15 were herbaceous, 3 were dwarf shrubs and 9 were trees. In terms of predominant habitat, 40% were grassland species, 35% were woodland species, 20% were species of heath and moorland, while the remaining 7% were typical of other habitats, such as wetlands. The widespread distribution across Britain of 86% of the species (Fig. 3) suggests that M. sylvaticum should not be limited in site availability by the host community. The community was dominated by perennial species; two of only three annual species were hemiparasitic (M. pratense and Euphrasia sp.) and presumably utilize the same strategy and a similar niche to that of M. sylvaticum within the community. The analysis indicates that the community is broadly stress-tolerant, preferring low disturbance and acidic soils. The toleration of heavy shade was only expressed in 27% of the community; this corresponds with the preference of M. sylvaticum for lightly shaded habitats reported by Rumsey (2002) and Rich et al. (1998), as it appears that M. sylvaticum itself cannot tolerate deep shade. In Northern Europe M. sylvaticum is said to grow in herb-rich forest (Molau 1993), in the field layer of ‘many kinds of forest’ including deciduous and coniferous forests in Finland (Lehtilä & Syrjänen 1995), Pinus sylvestris stands across Fennoscandia including moist and sub-dry forest types (Kaitera & Hantula 1998) and the rich ground flora of spruce forests (primarily Picea abies) in the southern taiga (Polunin & Walters 1985). In Ellenberg’s (1988) work on the vegetation of central Europe, Melampyrum sylvaticum is included in the Vaccinio–Piceeta, Vaccinio Piceetalia woodlands. Rich et al. (1998) point out that although this may once have been the case in Scotland, M. sylvaticum is not found in Pinus sylvestris woodland. Gibson (1993b) studied M. sylvaticum in the Swiss Alps and found it growing along the border between Larix–Picea forest and acidic, nutrient-poor Nardus grassland. Rumsey (1994) likens the floristic composition of the British M. sylvaticum communities to the Geranium sylvaticum dominated communities found under birch canopies in Scandinavia. Rich et al. (1998) note that Passarge (1994) described the Holco–Melampyretum sylvatici community of European woodland fringes and that Holcus mollis is also a frequent associate of M. sylvaticum in Scotland.

IV. Response to biotic factors


Fig. 3 Characterization of habitat preferences of the vascular plant species in communities containing Melampyrum sylvaticum. Bars represent the percentage of total number of species for which information was available (n is shown above each bar).

Grazing by livestock is probably negligible at most Scottish populations of Melampyrum sylvaticum, given the inaccessibility of sites, and the only incidence of grazing has been recorded at Loch Ossian on the Corrour Estate, where deer are allowed access to the sparse birch woodlands but only rarely graze there. It has been suggested that because many of its close relatives (e.g. M. pratense and Rhinanthus minor) are sensitive to herbivory, M. sylvaticum might also be (Rich et al. 1998). However, Lehtilä & Syrjänen (1995) showed that if damage is inflicted on the plant prior to fruit formation, it has a much greater capacity for compensating for the

588 S. E. Dalrymple


damage through re-growth and reduced seed abortion and, hence, is not so vulnerable to herbivory as M. pratense. Grazing pressures from red deer are highest in the early summer, prior to the main flush of growth on the open hill, where deer preferentially graze when food becomes available later in the summer (Chris Sydes, pers. comm.). This would be the least deleterious time for M. sylvaticum to undergo grazing as its compensatory mechanisms are able to respond most effectively before the end of flowering (Lehtilä & Syrjänen 1995). Plants in Scottish populations that have sustained damage to the main stem often produce longer and more numerous branches, presumably because of loss of apical dominance. In addition to directly affecting the growth of Melampyrum sylvaticum, herbivores can have indirect effects by grazing the surrounding vegetation. To test this, Dalrymple (2006) conducted an experiment simulating grazing at different stages of its life-cycle. An early grazing treatment, in which vegetation surrounding single M. sylvaticum plants was removed to a radius of 15 cm and down to the top of the moss layer, was applied in May 2004. The second grazing treatment consisted of the May cut supplemented with an additional cut in late June 2004. ‘Ungrazed’ control plants had the surrounding vegetation left intact. All plots, including the controls, were ‘trenched’ at a radius of 15 cm from the treated M. sylvaticum by cutting with a soil knife to a depth of 10 cm (or less where the soil was shallower) so that any potential host roots were severed. Thus, the M. sylvaticum individual could only take resources from those hosts which had undergone the grazing treatment. The effects were measured by recording the number of leaf pairs and flowers produced by each plant subjected to the grazing or ungrazed control treatments. Plant fitness in terms of relative plant size and number of reproductive structures was reduced when subjected to a combined early and late cut as compared with the early cut only or no cut at all. Grazing later in the growing season has also indirectly a more negative effect on Melampyrum sylvaticum performance, through the removal of the surrounding host vegetation. Melampyrum sylvaticum is affected by the presence of other animal groups as a result of pollination and seed dispersal (see VIII (A) and (C)). Ellenberg indicator values place M. sylvaticum in the category of plants found in light to medium shade where full-shade and full-light conditions are never encountered (Hill et al. 2004). Studies on previously unsurveyed sites have since shown that M. sylvaticum tolerates a much broader range of tree canopy cover than originally thought. At Mar Forest in the Cairngorms, for example, a small population exists at 640 m a.s.l. in the absence of a tree canopy. Tree canopy cover shows a negative correlation with altitude at M. sylvaticum sites, indicating that the light shade given by deciduous woodland is more important with decreasing elevation. The role of the tree cover is difficult to determine but is thought to be important through the maintenance of humidity levels at lower sites where increases in temperature at

lower altitudes mean that populations of M. sylvaticum are vulnerable to low humidity, compared with upland and montane sites. Dominance of ericoid shrubs (cover and height), in particular Vaccinium myrtillus, is negatively correlated with Melampyrum sylvaticum density and number of flowers per plant (Dalrymple 2006). This relationship could exist for two reasons; first, M. sylvaticum (and potential host plants) may be outcompeted for light by the dense understorey shrub layer at a height of 20– 50 cm; second, ericoid shrubs are allelopathic (Mallik & Pellisier 2000), and this has been shown to interfere with haustorial connections made by hemiparasitic species with host plants (Rice 1984). It is possible that both these mechanisms operate simultaneously. Regardless of the mechanism causing reduced densities of M. sylvaticum in ericoid-dominated stands, as ericoid shrubs generally prefer well-lit places and only tolerate partial shade (Hill et al. 2004), they tend to decrease in dominance with increasing shading allowing increased abundance of M. sylvaticum. Melampyrum sylvaticum performance may be further influenced by the community composition as this determines the presence of suitable host species (see V (B)).

V. Responses to the environment ()



Populations of Melampyrum sylvaticum in the British Isles tend to be limited in extent but can be very dense. The highest densities observed in Britain occur at a site in Glen Tilt, Perthshire, where the population has been estimated at > 8000 plants within an area of 6 × 18 m (based on densities of c. 800 plants m−2). The population at Loch Ossian, Westerness, is the least dense with approximately c. 1000 plants over an area of 500 × 20 m; within the population, M. sylvaticum individuals tend to form clumps with a maximum density equivalent to 100 plants m−2. High densities may be linked to organic matter content of the soil. This pattern of aggregation is repeated in consecutive generations. When the positions of individual plants in two consecutive generations of M. sylvaticum were mapped, the distribution changed very little and areas unoccupied by the first generation remained so in the second generation, despite the mapped area being homogenous in terms of abiotic conditions and community type. The mean distance travelled between closest neighbours from consecutive generations (although no parent–offspring link could be demonstrated and a seed bank cannot be discounted) was 15.5 cm at the Loch Ossian population, Scotland, and 16.6 cm in Abisko, Sweden (Dalrymple 2006). One of the primary causes for aggregation is dispersal, which is initially passive (seeds fall from the split capsule to the ground) and secondarily by animals, particularly ants. However, there is some evidence to suggest that the ant dispersal is not occurring at Scottish M. sylvaticum sites (see VIII (C)).


()

    

Environmental conditions at Scottish sites supporting Melampyrum sylvaticum are very variable, over an altitudinal range of 20–760 m a.s.l. (see II (A)). The constant features of M. sylvaticum habitats in Scotland are a close proximity to water, north-facing slopes and at least 30% shading, provided either by a tree canopy or the surrounding topography, all of which contribute to providing cool and, especially, humid conditions (Dalrymple 2006). The performance of Melampyrum sylvaticum in a range of habitats is affected directly by the presence of suitable hosts, as the identity of the host plant determines the growth rate through mineral accumulation and resource use-efficiency (Seel & Press 1993, 1994). Melampyrum sylvaticum is not host-specific, as evidenced by haustoria on the roots of species as diverse as Briza media, Calluna vulgaris, Carex sempervirens, Hieracium lachenalii, Melampyrum pratense, Picea abies, Salix aurita and Vaccinium myrtillus (Weber 1976). Surveys of community composition in quadrats with and without Melampyrum sylvaticum found no association with individual species or functional groups (Dalrymple 2006). As the study was conducted at three sites in Scotland and across a large area within Abisko National Park, Sweden, this also indicates that M. sylvaticum is not host-specific. Weber (1987) observed that the best hosts for parasitic Scrophulariaceae, including representatives of the genus Melampyrum, were annual legumes. Host– parasite compatibility was studied by the author in a pot trial using Lathyrus pratensis, Anthoxanthum odoratum and Plantago lanceolata as host plants. There was a marked difference in plant size and fitness depending on host identity; the plants that parasitized leguminous hosts were much larger and produced many more flowers and fruits than those grown on graminoids or herbs (Fig. 4). Surprisingly, even M. sylvaticum plants without hosts performed better then those grown with graminoids and non-leguminous herbs. Seel & Press (1993) supported the conclusion that leguminous hosts were better than other functional

Fig. 4 Performance of Melampyrum sylvaticum plants when grown with hosts of different functional types. Bars represent mean numbers of plant parts (leaf pairs, flowers or fruits) per plant, + SΕ; only one plant grown with a grass host survived.

types in their work on Rhinanthus minor and Euphrasia frigida, but while their study also looked at M. sylvaticum, no specimens attached to leguminous hosts could be identified in the field. This pattern is repeated in Scotland; legumes are infrequent in communities associated with M. sylvaticum and therefore are rarely available for exploitation by the parasite (Dalrymple 2006). The apparent unsuitability of non-leguminous herbaceous species as hosts is not universal, as it has been shown that the qualitative and quantitative provision of compounds varies dramatically between hosts (Govier et al. 1967). Seel & Press (1993) found unattached Melampyrum sylvaticum plants performed significantly worse than plants that were allowed to parasitize Cornus suecica, a non-leguminous, creeping perennial herb (Table 2). It has been suggested (e.g. Marvier 1998) that hemiparasitic plants may perform better in habitats that are species-rich. Indeed, Rich et al. (1998) note that Melampyrum sylvaticum tends to occur in herb-rich patches of the woodland understorey. It is not clear whether the species-rich areas provide favourable conditions for the parasite thereby facilitating its presence, or alternatively M. sylvaticum maintains higher species diversity by

Table 2 Performance of Melampyrum sylvaticum either unattached (pot grown in forest soil) or attached to Cornus suecica (in situ measurements on the forest floor). Count data were square-root transformed before analysis using Student’s t-test but original means are shown here. All differences were statistically significant (P < 0.001). Reproduced from Seel & Press (1993)


Stem height (mm) Number of branches Total number of leaves Total leaf area (cm2) Number of open flowers Number of dead flowers Total stem + branch dry weight (mg) Total leaf dry weight (mg) Total dry weight of reproductive parts (mg) Total dry weight (mg)

Unattached (n = 20)

Attached (n = 15)

73.0 0.0 9.8 2.1 0.0 0.8 10.0 10.0 0.0 20.0

364.0 1.1 34.0 47.0 3.3 19.0 203.0 177.0 160.0 539.0

590 S. E. Dalrymple

constraining the growth of vigorous species as observed in Rhinanthus minor (Westbury 2004, and references within). ()

  , , .

Frost is unlikely to have deleterious effects on Melampyrum sylvaticum as it is a summer annual, and low temperatures may have positive effects by triggering stages of germination (see VIII (D)). Drought conditions adversely affect Melampyrum sylvaticum because, as a hemiparasite, it must maintain high transpiration rates to acquire water and nutrients through the host’s roots. To achieve this, annual hemiparasites often maintain open stomata even under water stress (Press et al. 1988). No data have been found on the specific effects of drought on M. sylvaticum. However desiccation of the seed may cause problems for germination (see VIII D).

VI. Structure and physiology ()

 

The morphology of Melampyrum sylvaticum is partly dependent on the suitability of the host plants it encounters and the time of emergence. In trials of different host species, leguminous hosts produced larger M. sylvaticum plants (see V (B)) that had morphological features that seem to be associated with larger plant size, such as toothed bracts (on the upper flowering nodes only), woody stems and branching patterns rarely seen in natural populations. Branches are typically borne at the vegetative nodes of the main stem in pairs. Large plants in natural populations often have two or three pairs of primary branches. Occasionally, secondary branching occurs, whereby the lower nodes of the primary branches are vegetative and support leaves and branches rather than bracts and flowers. In some of the legume-hosted experimental plants, two pairs of branches emerged from the same node of the main stem. Melampyrum sylvaticum produces flowers in pairs borne primarily on the main stem although branches on the larger plants can bear almost as many flowers as the main stem. ()



Melampyrum sylvaticum is reported as having no mycorrhizal associations although M. pratense does have vesicular-arbuscular mycorrhiza (Harley & Harley 1987). Melampyrum sylvaticum plants were ‘infected easily’ by VAM fungi in cultivation (Weber 1987). © 2007 The Author Journal compilation © 2007 British Ecological Society, Journal of Ecology, 95, 583–597

()



A chromosome number of 2n = 18 has been reported by Hess et al. (1972) for material from Austria, Finland and Norway. No chromosome counts using British material have been found in the literature. ()

  

The hemiparasitic strategy of Melampyrum sylvaticum enables it to take water, inorganic and organic solutes from a host plant via a haustorium, a structure that creates a continuum between the xylem of the host’s and parasite’s roots (Musselman & Dickison 1975). Hemiparasites are also capable of autotrophic nutrition through normal photosynthetic processes, primarily in the leaves (Musselman & Press 1995). Lehtilä & Syrjänen (1995) showed that M. sylvaticum relies heavily on the leaves for carbon acquisition but could not demonstrate whether this was due to the photosynthetic capabilities of the leaves or because hemiparasitic carbon acquisition is also dependent on the surface area of leaves. Maintaining a larger leaf surface area will contribute to maintaining high transpiration rates. Transpiration in hemiparasites determines the rate at which resources may be translocated from the host, and requires the water potential of the parasite to be lower than that of the host. Ehleringer & Marshall (1995) showed that the water potential within a hemiparasite may be 1–2 MPa lower than the host and this ensures a continuous flow of water and solutes from the host xylem into the parasite. Seel & Press (1993) found that foliar concentrations of potassium were significantly higher in the parasite than the host to which it was attached. Potassium is important in the regulation of stomatal conductance and therefore affects the efficiency of water use within the leaves. Seel & Press (1994) demonstrated that attachment to a host lowered leaf conductance and transpiration rates while increasing the wateruse efficiency, light saturation rates and photosynthesis compared to unattached parasites. Although not demonstrated for M. sylvaticum, leguminous hosts generally enhanced these effects providing a possible explanation for greater biomass seen in hemiparasites attached to legumes (Seel & Press 1994). The authors hypothesize that the greater availability of nitrogen resulting from legume attachment reduces the need to transpire and therefore resource-use efficiencies are improved and the parasites can achieve greater biomass. However, no direct evidence of reduced transpiration in response to increasing nitrogen supply was found within their study. ()

  

No information has been found. ()

: 

Melampyrum sylvaticum is a summer annual that overwinters as a seed; Raunkaier’s system classifies it as a therophyte. It reproduces only by seed.

VII. Phenology Melampyrum sylvaticum seedlings start to emerge in late March and continue to appear well into April. This


emergence of the cotyledons precedes the main flush of growth of grasses in the surrounding understorey vegetation and also occurs before the tree canopy has reached maximum cover (Dalrymple 2006). When the growth of understorey and canopy is apparent, the M. sylvaticum seedlings have already managed to produce several, if small, pairs of leaves in addition to the cotyledons. It is not known whether this is a mechanism for avoiding light competition or whether the early growth is enabled by the hemiparasitism, as roots may be parasitized prior to host shoot growth. Leaves always emerge as opposite pairs. Leaf numbers increase steadily with the number of branches; not all plants produce branches but any branching usually occurs by mid-June; thereafter, new leaves and flowers are borne on existing branches. June also marks the beginning of flowering. The vast majority of plants flower first in June, although some individuals only start flowering in July. Melampyrum sylvaticum plants that do not flower at all tend to be smaller. A survey in 2003 showed that non-flowering individuals had an average of 3.5 leaf pairs, compared to 9.2 in flowering plants. This suggests that by June, individuals must have attained a critical size in order to produce flowers. Early emergence conveys benefits in terms of increased vegetative size and reproductive fitness, as shown by a study that compared the performance of two cohorts of M. sylvaticum (Dalrymple 2006). Flowering time is staggered so that as one pair of flowers matures the pair above is developing, and as one pair senesces the next pair becomes ready for pollination. The flowering period lasts throughout June and July, with early August the most important period for seed pod dehiscence. As a result of sequential flowering and seed development, some seed is likely to be produced before the latest flowers mature in early August; senescence is evident before all the seeds have been shed and starts in mid-August, with only a handful of plants surviving into September. Signs of senescence include a loss of turgidity and a change in the lustre and bright green colour of leaves to a dull green. The phenology of flowering times of M. sylvaticum observed by Molau (1993) in Sweden were not stable over two consecutive years, suggesting that phenological changes are sensitive to short-term temperature variations. First flowering times were on 3 July 1989 and 26 June 1990 corresponding with entire snowmelt occurring on 20 May 1989 and 3 May 1990, respectively (Molau 1993). Peak flowering times were also earlier in the second year, occurring on 14 July 1989 and 9 July 1990, respectively (Molau 1993).

VIII. Floral and seed characters © 2007 The Author Journal compilation © 2007 British Ecological Society, Journal of Ecology, 95, 583–597

()

  

Melampyrum sylvaticum displays a number of features that show an adaptation to entomophilous pollination. The zygomorphic flowers are gamopetalous with the

fused corolla forming two lips, the lower of which forms a platform for pollinating insects to land on. The paired stamens are pressed together to prevent pollen loss unless an insect comes into contact with the stamen, and are nototribic so that pollen is transferred to the upper side of the insect when it pushes into the corolla to collect nectar. Flower colour sends a visual signal to pollinating insects and yellow is particularly obvious to bees; as the flowers mature they turn orange and this may discourage further insect visitation as bees are attracted to flowers displaying spectral purity (Proctor et al. 1996). Although it is not clear whether M. sylvaticum is a pollen or nectar provider, two other species from the genus, M. pratense and M. arvense have been shown to provide both (Kwak 1988; Jennersten & Kwak 1991). Plants which are a good source of pollen and nectar are likely to receive insect visitors throughout the growing season, especially later in the year when larvae are developing. Given the flower morphology, colour and comparisons of pollinator activity with other species of the genus, it is likely that M. sylvaticum is primarily pollinated by bees (Rumsey 1994). However timed observations of 2 × 2 m quadrats at three Scottish sites did not record any insect visitation, despite ideal weather conditions. Seed production in M. sylvaticum is possible in the absence of insect visitation. In a study undertaken in Sweden, autodeposition of pollen in plants where a mesh cage prevented insect pollination resulted in seed production of 92% of that observed in open-pollinated plants (Molau 1993). ()



No hybrids have been confirmed (Rich et al. 1998). Artificial crossings between M. sylvaticum and the very similar M. pratense resulted in no seed set, suggesting that the species have internal mechanisms for maintaining reproductive isolation (Molau 1993). ()

   

Each flower produces a capsule fruit (pod) that bears 1–4 seeds. In the field, 1 or 2 seeds per pod is normal but larger plants are more likely than smaller individuals to produce 4. The number of seeds produced per plant is positively correlated with the number of leaves, showing that seed production is dependent on the biomass accumulated by the plant (Dalrymple 2006). Biomass is in turn dependent on host identity and availability, length of the growing season and time of emergence (see V (B) and VII). Seed production is greatest when the parent plant is attached to a leguminous host. Molau (1993) calculated the relative reproductive success by multiplying seed : ovule ratio and fruit : flower ratio of six subalpine hemiparasitic Scrophulariaceae. When expressed as a proportion, the reproductive success of M. sylvaticum was 0.45 and relatively low when

592 S. E. Dalrymple


compared to the other annuals included in the study: Euphrasia frigida (0.78), Rhinanthus minor (0.61) and M. pratense (0.55). The comparatively low reproductive success was a result of high seed abortion. Hiei & Ohara (2002) found that the earliest and, consequently, lowest flowers on the inflorescence of M. roseum var. japonicum had a higher rate of fruit set and hypothesized that this was due to the proximal and earlier-opening flowers receiving a higher proportion of available resources than the later flowers and the subsequent fruits. Melampyrum sylvaticum seeds are relatively large and heavy. The average length of seeds collected from Scottish populations was 4.34 mm ± 0.005 mm (SE), with a mean diameter of 2.43 mm ± 0.002 mm. The Scottish seeds weighed 18 ± 1.4 mg but those from Abisko National Park, Sweden (Molau 1993), averaged 24 ± 3.2 mg. Gibson (1993b) determined the mean fresh weight of seeds collected in Davos, Switzerland, by weighing 100 seeds in lots of 10 and reported the mean to be 10.4 mg. Salisbury (1974) compared the seed mass of 56 congeneric species pairs of open and woodland habitats including M. sylvaticum and quoted the mean mass of 1.64 mg, a value which is probably erroneous. As a facultative hemiparasite, M. sylvaticum can complete its life cycle without a host, but this has only been seen in cultivated individuals and seed production has never been observed in unattached wild plants. All but two of nine plants cultivated without hosts produced 1–2 capsules, each of which yielded at least one seed. The seeds of Melampyrum sylvaticum bear an elaiosome which offers a lipid-rich reward for ants that are capable of dispersing the seeds (Weiss 1908). Given the size of the seeds it is likely that only ants of the genus Formica are able to carry the seeds in order to remove the elaiosome (Mark Young, pers. comm.). In M. lineare, a species with very similar seeds, Gibson (1993a) found that ants moved seeds to sites associated with their nests that provided favourable conditions for germination (relatively high light fluxes for woodland understorey). By excluding different groups of animals from removing Melampyrum seeds, Gibson (1993b) found that the number of M. sylvaticum seeds removed by ants was much higher than the number of seeds removed by rodents. Seed removal by either ants or rodents differed markedly depending on the time of survey: ants removed 93% of the seeds during the night and 85% of the seeds during the day, rodents took 70% of the seeds during the night but none during the day. It was proposed by Gibson (1993b) that because of the timing of foraging, early morning capsule dehiscence conferred a selective advantage through seed-predator avoidance, as rodents are assumed to destroy the seed, even though some of the seed may be cached. No ants of the genus Formica have been observed at any of the Scottish sites included in Table 1. This indicates that in parts of its range the main mode of dispersal (by ants) is failing and M. sylvaticum is only able to disperse passively (see V (A)).

()

  : 

Germination in natural populations was observed within cages to exclude predators by Dalrymple (2006). Mean germination of seeds of M. sylvaticum from two populations in Scotland was 40%. Germination is not dependent on host presence (Weber 1981) but may be dependent on specific temperature cues corresponding with seasonal variation. Other species within the genus Melampyrum have a complicated germination process involving stages of development separated by periods of temperatureinduced dormancy (Curtis & Cantlon 1963; Masselink 1980). If the same is true for M. sylvaticum, sustained cold periods will be important for triggering and maintaining epicotyl dormancy between the initial radicle germination and cotyledon emergence. In M. pratense, optimal radicle emergence occurred at 7.5 °C and storage at 5 °C for 4 weeks was necessary to break epicotyl dormancy (Masselink 1980). Simulated seasonal changes in temperature were required to progress the M. pratense seed through several stages of germination. The optimum temperature for radicle germination in the autumn was 7.5 °C, lower temperatures (< 5 °C) were necessary to break epicotyl dormancy while the seed overwintered, and the final stage of germination occurred when seeds were stored at 5–7.5 °C (Masselink 1980). The presence of a seed bank in natural populations has not been investigated but pot trials by the author have shown that M. sylvaticum seeds are capable of lying dormant in the soil for one year before germinating. Kaitera & Nuorteva (2003) noted that seeds of Melampyrum spp. (including M. sylvaticum) took up to 2 years after sowing to germinate and develop into ‘test’ plants for their rust fungus inoculation trials. Dormancy has been induced in M. sylvaticum by storing the seeds in semi-darkness for 7 days at a temperature range of 11–17 °C prior to sowing in pots that were kept outside. In three replicates of 25 seeds, none emerged in the following growing season, and only 2 or 3 seedlings per replicate emerged 12 months later. It is possible that the elevated temperatures induced dormancy for 1 year in keeping with similar conclusions drawn by Masselink (1980) on the germination of M. pratense. Desiccation may adversely affect germination at two separate stages of the overwintering process (pers. observ.). Firstly, if desiccation over a period of more than 24 h occurs immediately after seed dehiscence it has the potential to reduce germination from 50% (undesiccated control seeds) to only 8.6%. However, it is not known to what extent the reduced germination rate is due to desiccation-induced dormancy rather than seed death. Secondly, if desiccation of the seed occurs as the cotyledons are emerging, the dry seed coat becomes tough and prevents expansion of the cotyledons causing damage and seedling death. Favourable germination microsites for M. lineare were provided by lichen cover over moss and litter layers, as the lichens

and the cotyledons opening to a horizontal position. The cotyledons develop from being very flat and waxy-looking to appearing plumper and a matt, mid-green. The cotyledons are not hairy but the stems sometimes appear to be subtly hairy. At this point the seedlings may be 2–5 cm in height and the first pair of true leaves can be seen as two protrusions at the base of the cotyledons. As these leaf pairs develop, they extend upwards initially, before opening out to a horizontal position perpendicular to the previous pair of leaves or cotyledons. The internode extends as the leaves enlarge.


IX. Herbivory and disease ()

Fig. 5 Development of Melampyrum sylvaticum seedlings in March 2003 from seeds sown in August 2002. The smaller seedling has an intact seed coat that has prevented expansion of the cotyledons.

maintained soil moisture while occupying sites which benefited from high light fluxes (Gibson 1993a). Further investigation is needed to determine what temperature regimes promote germination and dormancy and whether scarification can improve germination. ()


  

Seedlings emerge from the ground-layer vegetation with the cotyledons pressed together and pointing downwards. At this stage the seedling already has well-developed roots (Fig. 5). Occasionally the seed coat has not been shed and continues to surround the cotyledons. This probably indicates overly dry conditions that prevent the seed coat from softening sufficiently for the cotyledons to emerge fully. In these conditions the cotyledons will continue to enlarge within the seed coat and, if dry conditions persist, the seedling will probably die as a result of damage to the cotyledons. Normal emergence continues with straightening of the stem

   

Herbivory by large ruminants is covered in IV. Invertebrate feeders include the caterpillars of moths which can be found within the uppermost, youngest leaves, whose edges are ‘sewn’ together to form a protective case for the feeding caterpillar within. This has been observed by the author although the moth species were not identified. The lead-coloured pug, Eupithecia plumbeolata Haworth (Lepidoptera: Geometridae), has been reported to feed on M. sylvaticum in Finland (Savela 2006); in Britain caterpillars of this moth feed on M. pratense, M. arvense and Rhinanthus minor (Riley & Prior 2003) and are likely to also feed on M. sylvaticum as their distributions overlap, although this has not been confirmed in the field. Melampyrum pratense is an important host food plant for larvae of the heath fritillary butterfly, Mellicta athalia Rottemburg (Lepidoptera: Nymphalidae), which has also been reported as feeding on M. sylvaticum in Finland (Warren 1987a). However, as Mellicta athalia is only found in a few sites in southern England (Warren 1987b), it is unlikely that the species feeds on M. sylvaticum in Britain. Macrosiphum melampyri Mordvilko (Hemiptera: Aphididae) feeds only on M. sylvaticum and M. pratense (Peat & Fitter 1994). The seeds of M. sylvaticum are eaten by a variety of animal groups and Gibson (1993a) found that rodents are the main seed consumers. Melampyrum spp. seeds are normally dispersed by ants because the elaiosome is a rich food source (Weiss 1908; Gibson 1993a) but the removal of the elaiosome leaves the viable seed intact. As discussed in section VIII (C), ants can pre-empt mammal seed predation by removing seeds in the morning before mammals become very active. However, the absence of Formica ant species from key sites supporting British populations of M. sylvaticum may promote rodent predation and given the cyclic nature of rodent populations, seed predation may be periodically high enough to reduce M. sylvaticum populations significantly. ()

 

Cronartium flaccidum (Alb. & Schwein.) G. Winter (Basidiomycota: Uredinales), the two-needle pine rust,

594 S. E. Dalrymple

is hosted by Melampyrum spp. in northern Europe but is particularly important where the hemiparasites grow amongst stands of commercially valuable conifers such as Scots pine (Pinus sylvestris) (Kaitera et al. 1999). Melampyrum sylvaticum was first observed as a host to C. flaccidum in Finland by Kaitera & Hantula (1998). Experimental inoculations suggest that M. sylvaticum is relatively susceptible to the rust compared with M. pratense (Kaitera 1999). At different life-stages, M. arvense and M. nemorosum were more susceptible than M. sylvaticum to inoculation (Kaitera & Nuorteva 2003) but of the four Melampyrum species the latter was found to be the most important as a host of C. flaccidum in northern Finland due to its association with Scots pine stands (Kaitera et al. 2005). ()

 

See (B).

X. History The phylogeny of Melampyrum sylvaticum and its relationship with other Scrophulariaceae was studied by Young et al. (1999) in order to determine whether hemiparasitism was an evolutionary transition period between autotrophism and holoparasitism. Contrary to the traditional classification (Stace 1997) it was classified within the Orobanchaceae, based on the fact that the parasitic species are monophyletic. Pollen grains of Melampyrum spp. have been identified from south-west and Highland Scotland from around 7000  (Birks 1975) and the North York Moors from 5670 ± 90  (Simmons & Innes 1988) but these could be either pratense or sylvaticum as the pollen grains of the two species have overlapping size ranges: 18–24 µm for pratense and 21–27 µm for sylvaticum (Smith 1963). The habitat and community types identified in these deposits (Turner & Hodgson 1983) offer no indication of one species over the other. Melampyrum sylvaticum was first recorded in July 1775 by J. Lightfoot in Perthshire (Druce 1932). Britton (1943) reported that its distribution in Britain was centred on Scotland, extending to ‘but few districts’ in England and Wales. However, many historic records have been rejected as inaccurate as a result of subsequent inspections of field sites or herbarium specimens which proved to be misidentified M. pratense (Rich et al. 1998).

XI. Conservation


In 1972, the Botanical Society of the British Isles included M. sylvaticum on a list of rare species that members were to avoid collecting (Richards 1972). However, M. sylvaticum was only included in the list for England and Wales presumably because it was not deemed rare enough for inclusion on the Scottish list. The New Atlas of the British and Irish Flora reports it

as being found in 75 10-km squares in Britain (Preston et al. 2002) and therefore is classed as rare in Hill et al. (2004). It was initially estimated that M. sylvaticum had been lost from 30% of its former range (UK Biodiversity Group 1999) and as a result it was classified as nationally scarce by Rumsey (1994). However, recent reassessment of the M. sylvaticum distribution in the UK indicates a loss of 84% (Paul Gallagher, pers. comm.) and it now falls under the category of ‘endangered’ in the new Red Data Lists (Cheffings & Farrell 2005). This status has been conferred because the species has undergone ‘an observed, estimated, inferred or suspected population size reduction of ≥ 50% over the last 10 years’ and where this degree of loss is thought to have occurred, the causes of its decline ‘may not have ceased or may not be understood or may not be reversible’. However, this designation is probably an inaccurate reflection of the status of M. sylvaticum because the decline is not thought to have occurred within the last 10 years. Melampyrum sylvaticum should instead be classified as vulnerable (Tim Rich, pers. comm.) as the extent of the reduction cannot be determined because of inaccurate recording in the past (Rich & Sydes 2000). Rich et al. (1998) speculate that one of the major threats to M. sylvaticum is the development of dense canopies either through commercial forestry or invasion of introduced exotic species such as Rhododendron ponticum. They base this on the observation that populations tend to be found under light shade and, indeed, some sites from which M. sylvaticum has become extinct are unlikely to sustain M. sylvaticum in the future because of heavy shading caused by conifer plantation or vigorous understorey vegetation (Rich & Fitzgerald 1995). The Species Action Plan (SAP) for M. sylvaticum aimed to address the reduction in distribution in the British Isles. The SAP includes three targets: (i) maintain existing populations of this species as components of viable and functioning ecosystems; (ii) establish, by 2010, M. sylvaticum at five suitable sites in order to commence the process of extending its distribution in Britain; and (iii) ensure there are five new populations of this species of enhanced genetic diversity by 2010 (UK Biodiversity Group 1999). The SAP acknowledged that the information on M. sylvaticum was insufficient and could not pinpoint the causes of its rarity. Subsequent studies have identified that current status is due to a combination of habitat loss and an inability to recolonize suitable habitat, resulting in small and isolated populations. These populations are genetically divergent and may be undergoing the effects of sustained isolation and the associated loss of genetic diversity, with local adaptation in response to localized selection pressures (Sharp 2003). This has left M. sylvaticum vulnerable to a host of threats including further habitat loss, genetic drift and inbreeding and, potentially, climate change. In 2005, the M. sylvaticum Species Recovery Project was initiated to meet targets (ii) and (iii) of the



SAP (funded by the Scottish Executive’s Biodiversity Action Grants Scheme). Seeds were taken from three donor populations at the Birks of Aberfeldy, Loch Ossian and Coire na Eiridh in West Affric and transplanted to five new sites within the Highland Perthshire Forest Habitat Network. Although restoration efforts often recommend using local seed, the donor populations were selected despite their geographical separation as Sharp (2003) found that interpopulation genetic variation was not correlated with distance between populations. In addition, these three populations were the largest in the UK (a larger population at Glen Tilt was discovered after this study was initiated), and were identified by Sharp (2003) as having the greatest genetic diversity compared to other UK populations. The seeds from each donor population were mixed and sown in equal parts at each site in order to promote genetic mixing between previously isolated population genotypes. Existing populations will continue to be protected and managed sympathetically in order to prevent any further decline in the size or fitness of these populations. As a putative annual K-strategist, M. sylvaticum may be susceptible to environmental change (Molau 1993). This idea is supported by the fact that it shows adaptations to existing in a perennial community, including short dispersal distances of large seeds, with reliance on ant dispersal. As such, M. sylvaticum does not have the ability to exploit opportunistic habitats as ruderal annuals do and neither can it adapt to, or track changes in, climate (Dalrymple 2006). As a hemiparasite, M. sylvaticum is likely to show particular responses to the effects associated with climate change, including warming, drought and elevated atmospheric carbon dioxide levels (Phoenix & Press 2005). Given that the response of M. sylvaticum will probably be negative to warming (Dalrymple 2006) but positive to increased carbon dioxide, both directly and indirectly through host performance (Hättenschwiler & Körner 1997; Hättenschwiler & Zumbrunn 2006), the actual effect of climate change on M. sylvaticum in its core range in Northern Europe will be hard to predict (Phoenix & Press 2005). The effects of climate change on M. sylvaticum in the UK are easier to predict because the overriding factor in determining its distribution is humidity (Dalrymple 2006). Hulme et al. (2002) predict wetter winters and drier summers in Scotland. This is likely to affect M. sylvaticum adversely because of its reliance on humid conditions during the warmer summer months. The relative benefits of increased atmospheric carbon dioxide are likely to be minimal compared to the magnitude of deleterious effects of climatic shifts and further range contractions may push even the larger UK populations irreversibly towards extinction.

Acknowledgements I thank Sarah Woodin and Tim Rich for useful comments on the manuscript. Paul Gallagher deserves

many thanks for making available his site records and knowledge, as do David Pearman and Henry Arnold for the collation and production of British distribution records and map, respectively. The work by the author was supported through a PhD studentship funded by NERC (NER/S/A/2002/10307) and Scottish Natural Heritage at the University of Aberdeen.

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