Abbreviated references are used for many standard works: see Journal of Ecology (1975), 63, 335–344. Nomenclature of vascular plants follows Flora Europaea and Stace (1997) for British species, and for bryophytes follows Blockeel & Long (1998).
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Scrophulariaceae Tribe Pedicularieae (Rhinantheae) Bartsia L. [subdivided into Section Bartsia by Molau (1990) and his description of the species is incorporated in the following account]. A tufted perennial hemiparasitic herb with a short woody subterranean rhizome bearing, often abundantly at the nodes, adventitious roots with sparse root hairs. Haustoria develop on those adventitious roots in contact with neighbouring roots of host plants. The aerial shoots annual, erect or ascending, 8–30(−40) cm tall, unbranched or with a few short lateral branches, the stems pilose to hirsute with retrorse, white eglandular hairs. Leaves 10–25 × 6–15 mm, remote, decussate, sessile, herbaceous or subcoriaceous, ovate, apex obtuse to subacute, rounded to truncate at base, glabrous and rugose above, pilose to hirsute beneath, margins crenate–serrate. Inflorescence relatively loose, terminal with (1–)4–8(−11) floral nodes; bracts like the leaves but decreasing in size upwards, dull purple, exceeding the calyx; flowers 17–22 mm long, shortly pedicellate. Calyx green, often suffused with purple, glandular-hirsute with violet hairs, 6–10 mm long, tubular-campanulate, 4-cleft; the lobes narrowly triangular, obtuse to acute, entire, about as long as the tube or shorter. Corolla 15–20 mm, with a cylindrical tube and 2-lipped limb, violet or deep purple; upper lip entire or emarginate, longer than the lower; lower lip 3-lobed. Stamens 4, didynamous; anthers hairy, equally mucronate at the base. Style 14–20 mm long, pale violet, straight, decurved at apex; the stigma capitate ± exserted. Capsule narrowly ovoid, about twice as long as the calyx, hirsute, held ± erect in fruit, dehiscing into two valves, many-seeded. Seeds winged, 0.7–1.6 mm long, with mass 0.08–0.19 mg.
Bartsia alpina shows rather little variation. Several forms with deviating corolla pigmentation appear occasionally throughout the distributional range but are of no taxonomical value: the yellow-flowered var. jensenii Lange described from Greenland, f. ochroleuca Blytt from Norway, and the rose-coloured var. pallida Wormskj. ex Lange from Greenland, also observed at Abisko, northern Sweden. None of these has been reported from the British Isles.
Most variation is in shoot size and leaf dimensions which may be partially correlated to degree of exposure, grazing and nutrient status; plants from Scottish cliff-ledge populations are often much larger than those of English mire and pasture populations which are subjected to sheep and cattle grazing. According to Molau (1990) the number and position of teeth on the leaf margins show geographically correlated variation. Following an assessment of tooth number in Swedish populations and examination of more than 6000 herbarium specimens of B. alpina from its entire range, he suggested that its distribution includes two different sets of populations: subarctic populations north of 59° N latitude (but including the British populations) with a mean of 7–10 teeth, and alpine populations including all other populations south of 59° N latitude with a mean of 10–14 teeth. However, examination of herbarium specimens in The Natural History Museum, London, does not support this simple geographical separation. To what extent Molau's forms may be correlated with cytological races [see section VI (D)] is unresolved.
Bartsia alpina is a native herb of moist basic soils in upland meadows and pastures, on unstable flushed slopes resulting from stream erosion, in hummocky calcareous marshes grazed by cattle and sheep in northern England (Pigott 1956), and on ungrazed periodically inundated ledges of calc-schist crags in herb-rich swards, mostly in the Scottish Breadalbane mountains (Lusby & Wright 1996; Wigginton & Rothero 1999).
I. Geographical and altitudinal distribution
Bartsia alpina is geographically restricted to two areas in the British Isles, northern England and the central Scottish Highlands (Fig. 1). It is extremely rare in northern England, where it is known from only two sites in Cumbria (a few plants in Orton pastures and a large population in marshy pastures in the Crosby Gill SSSI (Ratcliffe 1977; Halliday 1997; Wigginton & Rothero 1999)); just a few plants still survive in Great Close Mire, Malham, North Yorkshire (Ratcliffe 1977; Wigginton & Rothero 1999), and the Upper Teesdale NNR, in County Durham where it is locally frequent (Bradshaw & Clarke 1965; Ratcliffe 1977). In Scotland, it is very local but may be frequent where it occurs in the Breadalbane range of Perthshire and in Argyll (Lusby & Wright 1996); the two largest populations in the British Isles occur on Beinn Laoigh and Meall Ghaordie (G.P. Rothero, unpublished report to Scottish Natural Heritage).
It is frequent in the mountainous areas of northern Europe westwards from the Urals through northern Russia into Finland, Norway and Sweden, with small disjunct populations in the floristically rich mires of Östergotland and Gotland. It is abundant in Iceland and occurs in the Faroe Isles. The species is present in many mountain ranges in central Europe, including the Sudeten, Tatra, Jura, the Alps, the Massif Central of France, Carpathians, southern Alps, Velebit, Bosnia-Herzegovina, southwards to the Pyrenees and south-west Bulgaria (Fig. 2). Outside Europe B. alpina is present in Greenland, and in north-eastern Canada around Hudson Bay southwards to Labrador (Fig. 2).
Bartsia alpina has been included in the arctic-alpine element of the British Flora (Dist. Br. Fl.) and described as European Arctic-montane by Preston & Hill (1997). It is classified as an amphiatlantic, arctic-montane species by Hultén & Fries (1986).
The altitudinal range of B. alpina in the British Isles extends from 245 m near Orton, Cumbria (Halliday 1997) and from 510 m on Beinn an Dothaidh to an upper limit of 950 m on Creag Mhor, in the central Scottish Highlands, where most of the sites are between 600 and 800 m (Wigginton & Rothero 1999). In western and northern Norway it descends almost to sea level, and is very common throughout the mountains where it ascends to 1100 m in northern Norway and to 1960 m on Jotunheim, southern Norway (Atl. N. W. Eur.). In the Alps it reaches 3100 m, Schwarzwald 900–1450 m, Tatra 1000–2128 m, Velebit 1400–1798 m and Bosnia-Herzegovina 1500–1800 m (Vergl. Chor., Vol. 2, 1978).
(a) climatic and topographical limitations
The lower distribution limits of B. alpina in Highland Scotland can be correlated with the 20 °C mean annual maximum isotherm; however, in northern England the limiting temperature is c. 25 °C and in Scandinavia 28 °C (Conolly & Dahl 1970).
Bartsia alpina has been described by Ferreira (1959) as a distinctly basiphilous species which, in the central Highlands of Scotland, is confined to soils developed over soft, calcareous mica-schists of the Dalradian Series. Cliff ledge Dryas heath communities, containing B. alpina, on Creag Mhor, Perthshire, occur on a skeletal brown loam (Pl. Comm. Scot.). In similar communities on Ben Lui (= Beinn Laoigh), Perthshire, Elkington (1971) describes the occurrence of B. alpina in humic brown soils.
In England, the plant is confined to soils developed on deposits overlying Carboniferous limestone – in particular, to small marshes flushed with water from calcareous springs, and characterized by the formation of hummocks with intervening bare patches. Such habitat complexes occur on slopes and hollows in the undulating moraine deposits on Widdybank Pastures in Upper Teesdale. Pigott (1956) described the development of one particular turfy marsh in a small area of the old cattle pasture, where the marshy ground of a broad soakway, below a series of springs, consists of a patchwork of hummocks scattered over a more or less smooth sloping expanse of sparsely turf-covered calcareous, muddy gravel. The hummocks are residual pieces of the surrounding continuous turf and soil mantle of the pasture. The active erosive agents are cattle trampling and patchy disruption of the turf with subsequent washing away of the silty mud during wet periods (see also IV). The hummock top habitat of populations of B. alpina consists of highly calcareous, gravelly clay with a CaCO3 content of 36–41%. Similar examples are found in Great Close Mire at Malham, in Orton Pastures and in the Crosby Gill SSSI.
Soil analyses from some British habitats are given in Table 1. The data confirm that B. alpina is a calcicole in the British Isles; extractable Ca is > 300 mg 100 g−1 dry soil, with soil pH > 6.0 (Pl. Comm. Scot.). Additional measurements of soil pH have been made on samples collected from sites in Upper Teesdale, from Cetry Bank (6.9 and 7.2) and from cattle pasture on Widdybank Farm (6.4), also from the two main sites in the Crosby Gill SSSI (6.7 and 6.9).
Table 1. Chemical characteristics of soil samples collected from the rooting layer of some British habitats where Bartsia alpina is locally abundant. All results (except pH) given on dry weight basis
Quested et al. (2002) have investigated the role of Bartsia alpina and other root hemiparasitic Scrophulariaceae in nutrient cycling in a habitat low in available nitrogen and phosphorus on a solifluction creep soil in northern Sweden. The open site (400 × 600 m) on a gentle, north-facing slope, at c. 400 m a.s.l., is in the subalpine birchwoods close to Abisko (68°21′ N, 18°49′ E) and the local population of B. alpina consists of some 10 000 individuals (clones and genets) (Molau 1995). The species composition of the vegetation comprises dwarf shrubs, graminoids, herbaceous plants and Sphagnum species (Nilsson & Svensson 1997). The N content of mature green leaves and the N, P and C content of standing leaf litter were measured, including the most abundant hemiparasites in the community, B. alpina and Pedicularis lapponica, and also in co-occurring potential host species (Quested et al. 2002). In samples of fresh leaves and litter of dicot herbs (n = 4) the percentage N ± SE was 2.85 ± 0.05 and 2.00 ± 0.04 in B. alpina, 4.18 ± 0.06 and 1.81 ± 0.05 in P. lapponica, compared with 2.79 ± 0.02 and 0.77 ± 0.04 in the potential host Polygonum viviparum (Persicaria vivipara). In contrast, in the dwarf shrubs it was 2.53 ± 0.03 and 0.74 ± 0.02 in Betula nana, 1.00 ± 0.02 and 0.69 ± 0.02 in Empetrum nigrum ssp. hermaphroditum, in Vaccinium uliginosum 1.72 ± 0.10 and 0.48 ± 0.03, and in V. vitis-idaea 0.91 ± 0.01 and 0.83 ± 0.09, respectively. Thus fresh leaves of the hemiparasites had greater N concentrations than the leaves of the host species, and this difference was even more marked in leaf litter. Litter of B. alpina and of the above four potential dwarf shrub host species was decomposed alone and in two species mixtures, in a laboratory microcosm experiment. Bartsia alpina litter decomposed faster and lost between 5.4 and 10.8 times more N than that of the dwarf shrubs. Mixtures of dwarf shrub and hemiparasite litter showed significantly more mass loss and CO2 release than expected on the basis of the component species decomposing alone. Nutrient release from the rapidly decomposing litter of B. alpina may stimulate decomposition in the poor quality litter of the dwarf shrubs by enabling faster utilization of C substrates. Quested et al. (2003) have tested the hypothesis that plant growth is enhanced by the litter of B. alpina, in comparison with litter of co-occurring dwarf shrub species, using a pot-based bioassay approach. Growth of Betula nana and Poa alpina was up to 51% and 41% greater, respectively, in the presence of B. alpina litter, than when grown with dwarf shrub litter (Betula nana, Empetrum nigrum ssp. hermaphroditum and Vaccinium uliginosum). The nutrient concentrations of Betula nana grown with B. alpina litter were almost double those of plants grown with dwarf shrub litter, and a significantly greater proportion of biomass was allocated to shoots rather than roots, strongly suggesting that nutrient availability was higher where B. alpina litter was present. A further extended comparison of leaf and litter tissue quality, N resorption and decomposability in hemiparasites with those of a wide range of other plant groups (involving a total of 72 species and including other groups with access to alternative nutrient sources, such as N fixers and carnivorous plants) was carried out by Quested et al. (2004), and reinforced the results described above. A litter trapping experiment was also carried out by Quested et al. (2004) to assess the potential impact of hemiparasites on nutrient cycling. Bartsia alpina was estimated to increase the total annual N input from litter to the soil by c. 42%, within 5 cm of its stems. The results provide evidence of a novel mechanism by which hemiparasites (in parallel with N fixing species) may influence ecosystems in which they occur. Through the production of nutrient rich, rapidly decomposing litter, B. alpina potentially greatly enhances the availability of nutrients within patches where it is abundant, with possible consequent effects on small scale biodiversity.
The National Vegetation Classification (Rodwell 1991, 1992) records B. alpina as scarce in two communities (M10 and CG14). It occurs in Carex dioica–Pinguicula vulgaris mire (M10), an expanded version of the Pinguiculo-Caricetum dioicae (Jones 1973emend. Wheeler 1975, 1984), in the Molinia caerulea–Eriophorum latifolium variant of the Briza media–Primula farinosa subcommunity which is predominantly centred on the Pennines of northern England. This low productivity, base-rich, ground water-fed fen vegetation type has affinities with the ‘turfy marshes’ previously described by Pigott (1956) from Upper Teesdale, and included by Wheeler (1980) in the Caricion davallianae small-sedge mire, in particular the B. alpina variant of the Pinguiculo-Caricetum molinietosum, together with Juncus alpinoarticulatus, Kobresia simpliciuscula, Saxifraga aizoides and Tofieldia pusilla. Bartsia alpina is also found in the calcareous marshes of the Malham Tarn area (Sinker 1960), included by Wheeler (1980) in the Sesleria variant of the same sub-association, with Sesleria caerulea, Festuca ovina, Leontodon autumnalis and Campanula rotundifolia. At Orton pastures, Cumbria, B. alpina occurs in an example of sub-association filipenduletosum (Wheeler 1980), a species-rich community of spring mires with the distinguishing species Angelica sylvestris, Cirsium palustre, Filipendula ulmaria, Lotus pedunculatus and Mnium longirostrum (Plagiomnium rostratum). Carex capillaris also occurs at Orton near the Bartsia location.
In the central Scottish Highlands, B. alpina is found in the Dryas octopetala–Silene acaulis ledge community (CG14), in which Alchemilla alpina, Campanula rotundifolia, Carex capillaris, C. pulicaris, Dryas octopetala and Persicaria vivipara are constant species. This vegetation type is synonymous with the Dryas-Salix reticulata nodum of McVean & Ratcliffe (Pl. Comm. Scot.). It is a community which represents the nearest approach to the European montane dwarf-shrub heaths of the Elyno-Seslerietea (recast by Oberdorfer (1978) as the Seslerietea variae). Within this class, the Dryas-Silene community is closest to the kinds of Scandinavian vegetation included by Nordhagen (1928) in the species-rich Dryas association within the alliance Kobresieto-Dryadion (Elynion Bellardii) with which it shares a number of species: Astragalus alpinus, Bartsia alpina, Carex atrata, C. capillaris, C. rupestris, Dryas octopetala and Salix reticulata. In two localities in the Scottish highlands, B. alpina has also been recorded in stands of the Luzula sylvatica–Geum rivale tall-herb community (U17), and in a single locality the associated species seem closest to CG11, the Festuca ovina–Agrostis capillaris–Alchemilla alpina grass heath (G.P. Rothero, unpublished report for Scottish Natural Heritage).
On calcareous soils in the alpine-subalpine region of Norway and northern Scandinavia, B. alpina occurs in four associations in the alliance Kobresieto-Dryadion: in the Caricetum nardinae, Kobresia myosuroidis, Cassiopetum tetragonae dryadetosum and Dryadetum octopetalae (Nordhagen 1936, 1955). Examples of some of these communities have also been described for west Finnmark, in Norwegian Lappland (Coombe & White 1951), where B. alpina occurs in dry heaths on well drained dolomite, and in intermediate habitats between this type and the wettest calcicolous bogs. In the Pältsa region of northernmost Sweden B. alpina occurs in three associations of the Dryadion alliance (Hedberg et al. 1952).
In the mountains of the Torneträsk area of northern Sweden, B. alpina occurs in snow-bed communities on circum-neutral calcareous soils: in the species-rich Salicetum polaris association referred to the alliance Polarion and in the Trollius europaeus society in the alliance Ranunculo-Poion alpinae (Gjærevol 1950). In the subalpine belt, B. alpina occurs in open forest ecosystems in which Betula pubescens ssp. tortuosa (ssp. czerepanovii) is the most abundant tree. Where the ground vegetation is of the meadow type, B. alpina is present in the Geranium–Vaccinium myrtillus communities (Sonesson & Lundberg 1974).
In Finland, B. alpina occurs in rich, open, treeless Sphagnum warnstorfii fens in the forest zone, in areas of supplementary nutrient effect, together with Carex capillaris, C. vaginata, Festuca ovina, F. rubra, Angelica sylvestris, Cirsium heterophyllum, Crepis paludosa, Equisetum pratense, Filipendula ulmaria, Galium uliginosum, Geranium sylvaticum, Geum rivale, Parnassia palustris, Saussurea alpina and Solidago virgaurea (Eurola et al. 1984).
Bartsia alpina occurs in subalpine and alpine Calcareous Small Sedge Fens referred to the alliance Caricion davallianae, in the order Tofieldietalia, in Central Europe (Ellenberg 1988). In Poland, in the high-mountain calcareous grasslands of the Tatra mountains, B. alpina is a characteristic species of the order Seslerietalia coerulea (= variae) in the class Elyno-Seslerietea, and is also a constant in the Versicoloretum typicum association (Szafer 1966).
IV. Response to biotic factors
The abundance of several of the rare Teesdale plant species, including B. alpina, on the tops of hummocks in the turfy marshes, may be contrasted with their relative scarcity in the nearby closed hay meadows under the competition of the lusher vegetation. A detailed description of the vegetation in a small area of turfy marsh is given by Pigott (1956). The site he described was enclosed in 1956 by a wire and post fence to prevent grazing and trampling by cattle. After 20 years there was little change in the composition of the vegetation, although, in the years following enclosure, the number of flowering-shoots of B. alpina increased from fewer than 10 to > 200 (Pigott 1978).
The results of surveys carried out in 1976–81 and in 2000 show that during this period the frequency of B. alpina in various base-rich flushes in Widdybank Pasture has declined (unpublished report by R. Jerram for English Nature). It is clear that grazing regime is one of the most important factors. There is evidence that the vegetation has become coarser, with locally increased abundance of taller rushes and that once relatively open swards with patches of bare soil have become closed. The implications are that the pasture should be well grazed by the right type of stock and at the right time of year (see XI). Although grazing and trampling by cattle in this habitat are crucial for the maintenance of populations of B. alpina, leaf size is much reduced and the incidence of flowering and fruiting is greatly affected.
V. Response to environment
Bartsia alpina forms local populations of dense clones with branching, perennial rhizomes.
(b) performance in various habitats
The density and vigour of British populations fluctuate mostly in response to grazing and trampling pressures by sheep and cattle and their management (see also IV, XI). In northern England, at Cetry Bank, Upper Teesdale NNR, on the steepest part of an eroded boulder-clay river bank with some evidence of grazing, there were some 300 flowering shoots in 1979, in 1985 there were > 1000 shoots, but only two in flower. In the Crosby Gill SSSI, in grazed neutral grassland, there were c. 263 shoots in total in the two main colonies on Hazel Moor in 1985, c. 440 in 1986, c. 890 in 1988, and c. 830 shoots in 1990; here plants though very short and highly branched with small leaves usually flower under the evidently favourable grazing regime (Crosby Gill: Bartsia alpina: Status Report 1993, by N.A. Robinson, English Nature NW Region, unpublished). In cattle-grazed Orton pastures, in three holdings there were some 234 shoots but only 11 inflorescences in 1993. The largest populations occur in Scotland where the plant is confined to ungrazed cliff ledges of calcareous schist which are subject to some irrigation (G.P. Rothero, unpublished report to Scottish Natural Heritage). Direct counts on crags are difficult so population estimates are based on more easily seen flowering shoots which were estimated to account for 20% of the total shoot populations; in Ben Laoigh, NNR, on one area of crags some 1750 shoots, on another c. 1125, and on a third area of crags c. 314 were recorded in 1995; on the large steep crags of Creag Laoghain, Meall Ghaordie, a total of > 1845 shoots were recorded in the same year.
(c) effect of frost, drought, etc.
In its montane and subarctic habitats, the aerial shoots die down in the autumn and the overwintering buds of Bartsia alpina are clearly extremely tolerant of freezing temperatures in winter. It is rarely subjected to drought, being confined to moist habitats and having high transpiration rates day and night which facilitate the movement of water from host species to the hemiparasite [see VI (E)].
VI. Structure and physiology
Bartsia alpina is a hemiparasite forming dense clones with perennial, branching, sympodial rhizomes composed of the persistent basal portions of previous generations of annual aerial shoots (Mathiesen 1921; Molau 1990). At the start of every growing season rhizomes develop from overwintering buds found in the axils of the uppermost scale leaves at the base of each dead aerial shoot. Each rhizome bears decussated scale-leaves and either grows in a direction horizontal to the ground surface, with elongated internodes, or may have quite short internodes and grow vertically, dependent upon the substrate nature. Plants sometimes have a lengthy and much thickened (to c. 5–8 mm diameter) root, which could be the original main root axis. Adventitious root formation at the nodes is very variable and perhaps reflects host environment and nutrient availability. In early summer, an innovation-bud develops in each of the axils of two opposite scale-leaves on each rhizome, either near the point where an elongated rhizome is beginning to turn upwards, or at the base of a vertical growing rhizome. The growing points of the rhizome show reduced internodes and die towards the end of the growing season, to be replaced in the following year by newly expanding rhizomes developing from overwintering buds formed at the bases of the dying aerial shoots. By the following mid-late summer new, unbranched aerial shoots arise from each of the two innovation-buds, some shoots remain vegetative whilst others are flower-bearing. After flowering and fruit-setting, the shoots die down leaving a persistent, subterranean basal portion immediately above the innovation-buds, and winter-buds are formed in the axils of the uppermost scale-leaves. Growth of the sympodial rhizome is continued by the development of these winter-buds. Seedlings, which develop from seed germinating in early summer, produce buds in the axils of the cotyledons. Whilst the uppermost part of the primary shoot dies, in the following growing season one of these buds develops into a foliage bearing shoot (Heinricher 1910). Further development of seedlings proceeds as described above for mature plants, but there is a time lag of at least 5 years, but more usually 10 years, from seed germination to first flowering (Mathiesen 1921; Molau 1995).
In material collected in Iceland, Musselman & Rich (1976) observed developing haustoria in the region of maturation behind the root tip on those adventitious roots of B. alpina in contact with neighbouring plant roots. They suggested that perhaps the production of adventitious roots ensures a continual supply of haustorial contacts. It was not clear in their study how long the haustoria survived; no haustoria examined appeared to be more than 1 year old. The presence of haustoria was confirmed on Carex sp., Bistorta (Persicaria) vivipara and Empetrum eamesii. The haustoria of B. alpina are small (0.1–1.0 mm in diameter), whitish in colour and their internal organization is similar to that of other parasitic Scrophulariaceae (Musselman & Dickison 1975). The vascular core of the haustorium resembles that of the related genera Melampyrum and Euphrasia in being only moderately developed. Like the vascular core elements of other parasites, the vessel elements are irregularly shaped with scalariform thickenings and lateral perforation plates. In the haustorium of B. alpina, the axial strands which extend from the vascular core to the xylem of the host are bowed similar to those of the Aureolaria type. In mature haustoria a continuous xylem conduit is present from the parasite to the host, but there is a striking lack of phloem sieve elements.
Visual examination of root connections and 14C labelling of suspected host species have been used by Nilsson & Svensson (1997) to identify the host range of two hemiparasites, B. alpina and Pedicularis lapponica; the latter method was more sensitive than root examination. This study was carried out in a subalpine open area close to Abisko, northern Sweden [see II (B)]. Both species made parasitic root connections to most other species in the surrounding vegetation. The 14C labelling revealed that the preferred hosts of B. alpina were 15 species in the families Betulaceae, Cyperaceae, Empetraceae, Equisetaceae, Ericaceae, Fabaceae, Lentibulariaceae, Liliaceae, Polygonaceae and Salicaceae, but the highest percentage of connections were to Pinguicula vulgaris > Carex norvegica, Salix glauca and Tofieldia pusilla. Visual examination of root connections also confirmed that the following were host species: Andromeda polifolia, Carex norvegica > Astragalus alpinus, Festuca ovina > Polygonum viviparum (Persicaria vivipara), Tofieldia pusilla and Vaccinium uliginosum.
Leaves collected in August, 2002 from cattle pasture on Widdybank Farm, Upper Teesdale, had a mean stomatal frequency (n = 15) of 56 ± 6 mm−2 on the under surface but no obvious guard cells on the upper surface (W.J. Davies, personal communication).
Roots of Bartsia alpina collected in mid-July 2002 from Hazel Moor, Crosby Gill SSSI, and in August 2002 from Cetry Bank, Upper Teesdale were examined and found to be non-mycorrhizal (D. Johnson, Irene Johnson and G. Palfner, personal communication).
Harley & Harley (1987) record both the presence and absence of VA mycorrhiza in B. alpina from continental Europe. It is reported by Michelsen et al. (1998) to be non-mycorrhizal in a heath tundra site near Abisko, northern Sweden.
(c) perennation: reproduction
A nanophyllous to microphyllous proto-hemicryptophyte with long-lived rhizomes; in an isolated population in a small fen in the Abisko area of northern Sweden (125 clones observed during a 5-year period), recruitment was shown by Molau (1990) to be extremely slow; the mean individual life span (population turnover) was 194 years. Propagation seems generally to be by vegetative spread, especially fragmentation of the rhizome. In the British Isles seedlings have been noted occasionally and, although their survival has not been monitored, their presence indicates that recruitment sometimes takes place by this means (Wigginton & Rothero 1999). Seed reproductive effort has been assessed by Molau (1995) in terms of the fate of the originally initiated ovules in the average B. alpina capsule. Only 27% of ovules turned into dispersed seeds (73% were lost to abortion, predation and non-dispersal) and of these 24% were viable, but only 0.002% of the seeds produced new flowering genets.
Chromosome counts of B. alpina suggest that a range of cytotypes occurs. Whether these may be in part correlated to the morphological types recognized by Molau (1990) is, however, unclear. No counts of Scottish material have as yet been made. Material examined from Upper Teesdale, Durham and Great Close Mire, Malham, North Yorkshire (Elkington 1974, 1978), shows 2n = 24. This is the predominant number recorded throughout the European range of the species (F.J. Rumsey, unpublished; Molau 1990; Dobeš & Vitek 2000). A deviating count of c. 2n = 28 by Böcher & Larsen (1950) of material from West Greenland, led them to suggest that arctic material may differ in base number from that in Central Europe. Subsequent counts from the Scandinavian arctic have consistently given counts of 2n = 24. Confirmation of the apparently aberrant number from Greenland is therefore desirable, as would be counts from the North American portion of the amphi-atlantic range. Favarger (1953) suggested 2n = 24 represents the tetraploid level as Mattick (in Tischler 1950) reported 2n = 12 from Tyrolean specimens. Confirmation of this count is desirable because a base number of x = 6 seems unlikely given the range demonstrated elsewhere in the Pedicularieae, even assuming a near basal position for Bartsia. Other deviating counts have been reported from material from the Col de Lautaret in the French Alps (2n = 36, Doulat 1946), and Dobeš & Vitek (2000) list counts of 3n = 36, 2n = 48 and 3n = 72 from Austria.
(e) physiological data
Field measurements of the rates of carbon dioxide and water vapour exchange by four species of root hemiparasitic Scrophulariaceae, including the perennial B. alpina, were made by Press et al. (1988) in a subalpine, open site near Abisko, northern Sweden [see II (B)]. Foliar exchange rates of CO2 were measured using an ADC portable infra-red gas analyser and data logger. Measurements were made during 24-h periods in mid-July, 1986, on attached young, fully expanded leaves and exchange rates were expressed on a leaf area basis. The day- and night-time temperatures were 20 °C and 14 °C, respectively. Rates of light-saturated (photosynthetic photon flux > 650 µmol m−2 s−1) photosynthesis were low, and during periods of darkness rates of carbon loss were of the same order of magnitude as carbon gain during periods of light; mean (n ≥ 30) CO2 exchange rates in B. alpina were 3.77 ± 0.43 during the day and −2.76 ± 0.28 at night (± 95% confidence limits), compared with a range of values from 2.10 to 6.68 and −2.76 to −5.53 µmol m−2 s−1, respectively, in the four species measured. Thus, although the species are chlorophyllous parasites capable of autotrophic carbon fixation, the high rates of dark respiration will result in little daily net carbon gain. Therefore plants must have access to a heterotrophic host-derived carbon supply. Additional support for this conclusion is provided by Nilsson & Svensson (1997), who exposed host plants to 14CO2 and detected the transfer of 14C to the hemiparasites [see VI (A)]. Observations made by Musselman & Dickison (1975) and Musselman & Rich (1976) on the internal organization of the haustorium in the Scrophulariaceae show that there is xylem continuity but not that of phloem [see VI (A)], indicating that the CO2 economy of the parasites might be independent of the host. However, Press & Whittaker (1993) have suggested that solutes are transported apoplastically from host to parasite cells along both vascular and non-vascular pathways.
Day-time mean (n > 30) transpiration rates also measured by Press et al. (1988) were very high and comparable in the four species; in B. alpina 7.02 ± 0.01 mmol m−2 s−1 (± 95% confidence limits) they were 2 to 10 times those commonly found in mesophytes. Although no relationship was found between leaf conductance to water vapour and CO2 exchange rates during periods of light, there was a close relationship between night-time rates of transpiration and respiration. At night, normal closure of stomata was not observed, and mean potential transpiration rates were very high in two annual species, but were lower in the perennial B. alpina, 2.58 ± 0.21 mmol m−2 s−1, suggesting some conservation of water in the species. Potential transpiration rates, day and night, will facilitate movement of water, inorganic and organic solutes from host to parasite. Whereas in autotrophic plants stomata function to minimize water loss and maximize carbon gain, in the root hemiparasites the reverse is the case, whereby water loss is maximized in order to maximize carbon gain. These results support the earlier findings of Gauslaa (1984), who measured the transpiration decline of excised leaves of a wide range of species collected in Norway and calculated cuticular (rc) and stomatal (rs) diffusion resistances for water vapour. Three hemiparasites were measured including Bartsia alpina. Within 50 min their leaves lost 25–30% of fresh weight and wilted permanently. All had very low cuticular (rc) and stomatal (rs) diffusion resistances: mean values, total range and number of measurements of rc and rs (s cm−1) for B. alpina were 7.5 ± 1.6 (4) and 1.3 ± 0.6 (4), respectively, compared with a range of rc 3.2–62.5 s cm−1 and rs 0.6–17.4 s cm−1 in non-parasitic mesophytes. The hemiparasites can probably afford to use a lot of water because they are connected to the extensive root systems of their hosts.
Shoots of B. alpina growing in a natural habitat with and without nitrate fertilizer addition (106 g N m−2) were assayed for nitrate reductase activity (NRA) 72 h after the fertilizer addition (Lee & Stewart 1978). Mean NRA in control shoots was 1.43 µmol NO2 h−1 g−1 FW and after induction 4.06 µmol NO2 h−1 g−1 FW, values within the range of most species which are non-mire and non-nitrophile, indicating that the leaves of B. alpina do appear to possess the inducible isoform of the enzyme and have the capacity to assimilate NO3 if and when it becomes available. However, in common with non-mire and non-nitrophilous species, B. alpina is more likely to utilize mixed sources of N (NO3−, NH4+ or organic-N) by root from soils deficient in N rather than by shoot assimilation. The hemiparasite may also have access to reduced organic nitrogenous compounds synthesized by the hosts.
In addition to these sources of nutrients, Kerner (1895) has suggested that B. alpina may also obtain nutrients by preying on small animals. In the subterranean innovation buds produced towards the autumn, the arrangement and architecture of the scales are such that ducts are formed opening to the exterior. These ducts or recesses provide a mechanism for passively ensnaring Protozoa which occur in the infusions of decaying animal and plant matter in the soil. The presence of stalked glands on one wall of the ducts suggests that the prey are digested and absorbed. A similar mode of food-absorption was described for Lathraea squamaria.
Volatile compounds collected in northern Sweden from the inflorescences of individual B. alpina plants in subalpine (345 and 420 m) and alpine (880 and 1000 m) populations, have been analysed by gas chromatography and mass spectrometry (Bergström & Bergström 1989). The compounds detected were: α-pinene, Z-3-hexenol, Z-3-hexenyl acetate, phenyl acetaldehyde and phenyl acetonitrile. A significantly larger proportion of Z-3-hexanol and Z-3-hexenyl acetate was collected from the subalpine than from the alpine populations, but the differences between the amounts of the other compounds were slight. These differences in floral scent are related to the different altitudinal distribution range of pollinating bumble-bees; Bombus pascuorum occurs in the subalpine region with an upper altitudinal limit of c. 650 m whereas Bombus alpinus and B. hyperboreus are common in the mid-alpine belt [see also VIII (A)].
Three iridoid glucosides, two phenylpropanoid derivatives and one flavonoid have been isolated from the methanolic whole plant extract of B. alpina; some of these compounds have radical scavenging activity against DPPH or antioxidant activity against beta-carotene on TLC bioassay (Cuendet et al. 1999).
Each growing season, newly expanding rhizomes of B. alpina develop from overwintering buds at the bases of the previous year's dead aerial shoots. By early June, aerial shoots arise from subterranean innovation buds; some shoots remain vegetative whilst others are flower bearing. In July near the time of maximum extension of the new rhizomes, a pair of new innovation buds develops in each of the axils of two opposite scale leaves on each rhizome. These buds will give rise to aerial shoots in the following year. In Britain, flowers are in bud in early June, flowering takes place from mid-June to August and mature capsules are present in September. In subarctic Sweden flowering is in late June to late July, mature capsules are found in August, primary seed dispersal occurs during the first half of September and seed germination occurs in early June in the following year (Molau et al. 1989a,b).
VIII. Floral and seed characters
(a) floral biology
Reproduction is amphimictic and vivipary unknown. Faegri & van der Pijl (1979) have suggested that there are two kinds of clones with distinct flower types in B. alpina, one predominantly outcrossing type with the stigma exserted, and one autogamous type with the stigma included in the upper lip (galea). It has also been reported by Mathiesen (1921) that populations in the Alps have protruding styles with the stigma exposed whereas Scandinavian and Greenlandic material is either of this type or with the stigma enclosed within the corolla tube, immediately inside the throat of the flower or even far inside against the anthers. In this latter case, self-pollination seems inevitable. Recently, however, Molau et al. (1989a) have demonstrated experimentally that the two flower types described above are just unpollinated and pollinated flowers of a single type; the stigma is exserted beyond the galea until pollination, when the style ceases growing. Because the corolla continues to grow in length for several days, the stigma is soon hidden within the corolla tube. Thus each individual flower passes through both phases during its life-time (if pollinated), and autodeposition of pollen leading to seed set never occurs in the absence of visiting insects (Molau 1990). Bartsia alpina has a mixed mating system (Molau et al. 1989a). The dull, dark purple corollas have a tube over 15 mm long and the style matures early, well before the stamens are ripe (protogyny), although B. alpina is self compatible but not autogamous. Long-tongued bumble-bees visiting the flowers for the nectar secreted at the base of the tube come into contact with the style and deposit foreign pollen on it, effectively bringing about cross-pollination. Over 50% of the pollen grains deposited on a stigma originate from a flower on the same plant, i.e. geitonogamy.
During the flowering period from mid-June to mid-July, in a large population of B. alpina situated in an unshaded subalpine area close to Abisko, northern Sweden [see II (B)], the most important pollinators are Bombus pascuorum workers and B. balteatus queens, and each flower normally receives only a single visit (Molau et al. 1989a; Kwak & Bergman 1996). In the nearby mountains, in the middle-alpine belt where B. alpina occurs on a south-west-facing slope above Lake Latnjajaure at an altitude of 1000 m to 1150 m, only two species of bumble-bees, Bombus hyperboreus queens and B. alpinus workers were found to be common at the site, the former species being an obligate nest parasite of the latter. Both species collect the pollen and nectar of Saxifraga oppositifolia during the early part of the season, switching to Astragalus alpinus and Bartsia alpina as soon as they come into flower (Bergman et al. 1996; Stenstrom & Bergman 1998).
No hybrids of B. alpina are known. At no point in its wide range does it grow with any other Bartsia species.
(c) seed production and dispersal
The clones (individuals) within the main study population of B. alpina at Abisko, northern Sweden [see II (B)], have a life span of at least 25 years and usually produce 1–30 flowering ramets annually after a juvenile period of normally > 10 years. The inflorescence is a raceme producing on average 4.5 floral nodes (range 1–13) with paired flowers. The fruit is a dry, dehiscent, two-locular capsule containing on average 47.9 ± 1.1 winged seeds (n = 529 capsules collected from 118 plants) (Molau et al. 1989a). An earlier estimate of the mean seed number was 39.7 ± 2.44 (n = 25 capsules collected from 35 plants) for British material (Rep. Capac.), and a single ramet collected in July 1990 from Cetry Bank, Upper Teesdale yielded a mean of 45.4 ± 8.96 seeds per capsule (n = 7). Most ramets produce from 4 to 8 capsules, thus seed production is c. 200–400 per ramet.
The northern Swedish subalpine population of B. alpina has been found by Molau et al. (1989b) to suffer high levels of pre-dispersal seed predation by larvae of two insect species [see IX (A)]; normally 40–50% of the fruits are attacked. Large inflorescences suffered significantly higher predation pressures than small ones, and predation was most intense in the middle of the inflorescences. Attacked capsules did not open to the same extent as unattacked owing to damage of the capsule wall, and furthermore, frass from the predators plugged the exit. Seeds from attacked capsules entered the seed pool only when ramets fell to the ground. During the first winter after flowering no ramets fell and accordingly no seeds in predated capsules were dispersed. In the second winter 20% of the ramets fell and during the third winter the remainder (80%) fell. However, inspection of herbarium specimens by Molau et al. (1989b) has shown that predator-attacked capsules are rare or absent in the British Isles.
Even though the seeds are light, dry, and possess narrow wings, wind dispersal in B. alpina seems to be of little importance and takes place over very short distances; seed traps placed around clones in stongly wind-exposed sites in northern Sweden revealed a mean wind dispersal distance of only c. 30 cm (Molau 1990, 1995); a similar mean distance (32.7 ± 2.3 cm; n = 42) has also been calculated from seedling recruitment mapping (F.J. Rumsey, unpublished). Therefore, Molau has proposed a two step seed dispersal mechanism. The first step is the passive dispersal of the dry seeds when the capsules ripen, dehisce and shake in the wind. Once on the ground, the seeds will absorb water, especially in early autumn when moisture increases, and the moistened wings stick efficiently to smooth moistened surfaces such as the snouts and feet of grazing animals. Thus, the second step involving occasional secondary seed dispersal mediated by adhesion to grazing birds and mammals is important for moderate long-distance dispersal. Downstream water dispersal in autumn is common in B. alpina. The seeds have high buoyancy provided by the wings and can remain floating for months, but if the water freezes, they will sink immediately after thawing. Below its normal alpine and subalpine habitats in Fennoscandia, B. alpina occurs along the shores of large lakes and major rivers, often in dense populations (see Atl. N.W. Eur.).
Seeds collected from plants in Upper Teesdale had a mean mass of 0.11 mg (Rep. Capac.). Seed sampled from the northern Swedish subalpine population in June, 1988, following overwintering, was separated by length into three size classes (0.7–1.0, 1.0–1.3 and 1.3–1.6 mm) by Molau et al. (1989a). Batches of 200 seeds from each class had a mean mass of 0.084, 0.148 and 0.187 mg, respectively. According to Molau (1991) seed weight is usually strongly positively correlated with offspring fitness. The maternal plant has a profound influence on seed weight in B. alpina, and regulation is brought about by a combination of two important determinants: maternal genotype and environmental factors, especially the supply of nitrogen, a nutrient which is normally deficient in moist arctic soils.
(d) viability of seeds: germination
Laboratory experiments have been carried out to elucidate some effects of temperature and exogenous gibberellic acid (GA3) on the germination of seeds of B. alpina collected near Abisko, northern Sweden, in August and stored before being tested. Seeds were pre-treated for 48 h in either distilled water or a GA3 solution at room temperature before being transferred in lots of 50 to filter paper kept moistened with distilled water in glass Petri dishes. Three replicates of each treatment were set up, then transferred to the different temperature regimes in Fisons Fitotron 600 growth cabinets programmed for 12 h light/12 h dark, with the lower temperature regime in split temperature regime experiments coinciding with the dark period. The experimental results shown in Fig. 3 indicate that seeds exposed to the split temperature regime (25/15 °C) showed a greater germinability than those at a constant 13 °C, which might be an effect of the alternating temperatures but also the higher average temperature (20 °C). Pre-treatment with gibberellic acid (GA3) produced the highest germination rates (62–64%). In a further experiment seeds pre-treated with 750 p.p.m. GA3, transferred to a growth cabinet at 8 °C for a week when the temperature was adjusted to 15/8 °C for a further 2 weeks, germination reached 83%. The levels of endogenous gibberellins are low in many dormant seeds but they increase in response to chilling temperatures (Wareing 1976). Thus the application of exogenous gibberellic acid to seed of B. alpina has probably replaced the chilling requirement and has stimulated seed germination.
Molau et al. (1989b) collected seeds at Abisko, northern Sweden from capsules on the overwintering still standing ramets of B. alpina at the beginning of the growing season (1 June) the first, second and third year after flowering. The seeds were sown on filter paper in Petri dishes (n = 5 × 100 seeds in each year) and germinated under uniform conditions in a glasshouse. Viability of the seeds were 86.8% (SE = 1.9), 8.2% (SE = 3.1), and < 1%, respectively. In late August, 100 apparently undamaged seeds were collected from unattacked and attacked capsules, respectively, from randomly selected last-year infructescences of B. alpina. The germination capacity of these 1-year-old seeds in unattacked capsules was 37% compared with 18% in attacked ones. This indicates a marked decrease of viability even though the seeds were not physically damaged. Approximately 25% of the seeds remain apparently undamaged when the capsule is attacked by a predator. These seeds are dispersed by the third winter after flowering when the viability of seeds in general has decreased to < 1%, and as they have only half the normal germination capacity make a negligible contribution to the seed pool.
(e) seedling morphology
The seeds are 0.7–1.6 mm long with 6–13 broad longitudinal wings which are 0.4–0.6 mm wide and are transversely striate (Fig. 4a–c). Germination is epigeal. Early stages in the development of seedlings of B. alpina are illustrated in Fig. 4(d–g); the onset of germination is indicated by the emergence of the radicle, which elongates, followed by the release of the cotyledons from the seed coat. Once the cotyledons have developed, seedling growth usually slows 2–3 days after germination in Petri dishes. Heinricher (1910) sowed seed of B. alpina and followed seedling development in cultivation. The plants in culture were grown with Agrostis alba var. alpestris and Avena (Trisetum) flavescens as host species. At the expanded cotyledon stage, a resting bud was produced in the axil of each cotyledon and the primary shoot developed. The primary axis died back as far as the resting buds during the winter. One of the cotyledonary buds developed into a foliage-bearing shoot in the following year, provided that the seedling had formed a connection with a host root by means of a haustorium. The early stages of seedling development up to the end of the second vegetative period are illustrated by Heinricher (1910).
IX. Herbivory and disease
(a) animal feeders
In alpine and sub-arctic areas of northern Europe, seeds of B. alpina are destroyed by the larvae of two relatively host-specific pre-dispersal seed predators (Molau et al. 1989b): the microlepidopteran Aethes deutschiana Zett. (Lepidoptera-Tortricidae) is the most frequent of the two predators, and the dipteran Gimnomera dorsata Zett. (Diptera-Scatophagidae) occurs in much smaller numbers. Oviposition normally starts when most of the plant population is about to begin flowering in late June, is most intense in the first few days and lasts for about two weeks. The violet lower bracts enclosing the young racemes act as predator-attracting cues. The eggs are mostly placed in small clusters on the lower surface of the bracts. After a few days the eggs hatch and the larvae drill into the nearest developing ovary, leaving a minute entrance hole. Normally there is a single larva in each capsule. The young larvae drill into developing seeds and eat them from the inside out. The contents of a single capsule locule is sufficient for the development of one G. dorsata larva, which is not capable of moving around in the raceme. The larvae of A. deutschiana each require the contents of both loculi of the fruit. If seed set in a capsule is insufficient, a larva will leave the capsule, crawl upwards in the raceme, and enter the nearest unattacked capsule above. In mid-August, the larvae leave the B. alpina capsules to pupate in the soil immediately beneath the host. Both seed predators are attacked by a small polyphagous parasitic wasp Scambus brevicornis Grav. (Hymenoptera-Parasitica-Ichneumonidae), which oviposits in predator-affected fruits of B. alpina. After consuming the contents of a predator larva, the parasite pupates in the capsule and hatches in June the following year. In this way, seed predator populations are normally reduced by 30–40%.
(b) and (c) plant parasites and plant diseases
No information found.
A seed of B. alpina has been tentatively identified from the Middle Weichselian deposits at Barnwell Station, Cambridge (Godw. Hist.).
In historical times, first found by John Ray in 1668 at or very close to its present locality in Orton pastures, Westmorland, and in 1789 George Don claimed the first Scottish record from rocks on the east side of Meall Ghaordie, in the Breadalbane mountains (Raven & Walters 1956). Bartsia alpina had been found in Upper Teesdale by 1805 (Winch et al. 1805).
The status of Bartsia alpina in Britain is Lower Risk–Near Threatened, but not threatened in Europe (Wigginton & Rothero 1999). The present overall distribution of the species (Preston et al. 2002) is unchanged from that shown in the 1962 Atlas (Atl. Br. Fl.). More recently there has been an apparent decline or progressive loss of sites in the east, perhaps owing to habitat management, in particular grazing regimes and possibly wider climatic changes. The increase in Scottish records to the west undoubtedly reflects better recording activity in what is an underworked and remote area. In England, B. alpina sites have been lost from pastures through overgrazing, trampling by cattle and drainage. In Scotland, searches in the 1980s and in 1992 failed to detect any plants in previously known or likely sites in the lower flush-pasture of Ben Lawers in a community comparable with the type found in northern England, and also subjected to heavy grazing and drainage. The Scottish ledge communities are largely unaffected being out of reach of grazing animals, but there is little doubt that grazing restricts the occurrence of B. alpina on sites in Scotland (Wigginton & Rothero 1999).
Light grazing and trampling by cattle or sheep are crucial for the maintenance of populations in hummocky flush-pasture, by keeping the lusher vegetation down and the habitat open (Pigott 1956), although stock should be removed during the flowering and fruiting period. Possible causes of a reduction in the area of distribution and the density of rare plant species including B. alpina in Widdybank pastures, Upper Teesdale, between 1976 and 2000 have been assessed in relation to farm management in the last 50 years by M.E. Bradshaw (appendix to the unpublished report by R. Jerram for English Nature (see IV)). The most important factor contributing to the increased density of competing tall rushes is the high water-table, which is in part owing to the choked state of drainage ditches (the grips). Stocking rates of sheep, cattle and ponies are catalogued in detail: in particular the breeds of cattle, their behaviour and their grazing preferences which are major factors causing the reduction of the rare plants in all habitats. The pastures should be grazed by suitably hard-mouthed cattle which will eat rushes, and not concentrate on the drier ground. These cattle should be light, so that poaching is not excessive, alhough some poaching is required to maintain open swards and fresh germination niches. Stocking arrangements have varied greatly in the last 50 years. In recent years, however, the introduction of heavier, softer-mouthed cattle breeds from continental Europe and crosses has led to an increase in erosion and also a change in grazing preferences. Probably the greatest threats to the English sites are an unsympathetic grazing regime and excessive trampling of colonies along well-used paths [see also IV, V (B)].
We thank Mr and Mrs J. Wood for permission to visit Crosby Gill/Hazel Moor and English Nature, Cumbria Team, especially Simon Webb, for permitting the sampling of plant material of Bartsia alpina from this SSSI. Also thanks to Chris McCarty, Site Manager Moor House-Upper Teesdale NNR, English Nature Northumbria Team, for useful on-site discussion. We are indebted to Miss Irene Johnson, Dr D. Johnson and Dr Götz Palfner for examining root samples for VA mycorrhizal infection, Professor W.J. Davies for determining stomatal number and Professor M.C. Press and Dr B.D. Wheeler for helpful comments. Gordon Rothero kindly supplied details of individual Scottish localities for B. alpina. We thank Henry Arnold, Biological Records Centre, Monks Wood, for providing the map for Fig. 1. Permission to reproduce an edited version of the amphiatlantic distribution map of Bartsia alpina (Fig. 2) has been granted by Sven Koeltz.