Pulsatilla vulgaris (L.) Mill.

Pasque Flower, Pulsatilla vulgaris Miller

RANUNCULACEAE

SYN.: Anemone pulsatilla L.

Status: All British populations belong to subsp. vulgaris which is classified as ‘vulnerable’ (IUCN Criterion A2ac; Cheffings & Farrell, 2005), and listed as a UK BAP Priority Species in 2007. It is currently confined to 18 sites in 19 10km squares in England. In this account Pulsatilla vulgaris refers to subsp. vulgaris unless otherwise stated.

In partnership with:

1 Contents

1 Morphology, identification, taxonomy and genetics 1.1 Morphology and identification 1.2 Taxonomic considerations 1.3 Genetic implications 1.4 Medicinal properties

2 Distribution and current status 2.1 World 2.2 Europe 2.3 United Kingdom 2.3.1 England 2.3.1.1 Native populations 2.3.1.2 Introductions 2.3.2 Northern Ireland, Scotland & Wales

3 Ecology and life cycle 3.1 Life cycle and phenology 3.1.1 Flowering phenology 3.1.2 Flower biology 3.1.3 Pollination 3.1.4 Seed production 3.1.5 Seed viability and germination 3.1.6 Seed dispersal 3.1.7 Regeneration 3.1.8 Response to competition 3.1.9 Herbivory, parasites and disease

4 Habitat requirements 4.1 The landscape perspective 4.2 Communities & vegetation 4.3 Summary of habitat requirements

5 Management implications

6 Threats/factors leading to loss or decline or limiting recovery

7 Current conservation measures 7.1 In situ Measures 7.2 Ex situ Measures 7.3 Research Data 7.4 Monitoring and the Common Monitoring Standard

8 References 9 Contacts 10 Links 11 Annex 1 – site descriptions 13 Annex 2 – changes in population size, 1960-2006 14 Annex 3 – associates

2 1 Morphology, identification, taxonomy and genetics

1.1 Morphology and identification Hemicryptophyte; 2-15 cm, extending to ca. 45 cm in fruit. Rhizome obliquely erect or vertical, branching, black, 2-17 mm thick, eventually decaying to form new plants. New leaf rosettes arising from the branches of the rhizome by growth of lateral buds, producing groups of leaf rosettes connected below ground by an anastomosing rhizome system. The remains of old leaf bases protect the overwintering buds at the apex of the rhizome. Basal leaves up to 11 from each rhizome apex, bipinnatisect, silky-hairy and forming a rosette. Ascending, developing during anthesis and withering in the autumn (occasionally over-wintering). Petiole to 21 cm, blade to 11 × 7 cm, 2- to 4- pinnate. Cauline leaves 2(-4), sessile, 1.7-5.3 cm, smaller and more deeply divided into linear segments (only slightly lobed), white-hairy and reaching the perianth during most of the flowering period. All leaves silky-hairy at least initially, the basal with pubescent petioles. On emergence the silky-villose leaves are tightly curled around the apical growing points. Flowers solitary, terminal, erect at first but drooping after a few days, and becoming bell-shaped (campanulate) (Fig. 1a). Buds develop during late summer and become dormant over the winter months when they are protected by a dense covering of silky-villose hairs and the remains of the previous year’s leaves. Pedicel up to 8 cm and bent over less than 90º at anthesis, elongating to 25 cm in fruit. Perianth-segments 6, 16- 42 × 4-17 mm, deep violet-purple in British plants, more blue to violet-blue on the Continent, darker on the inside, paler and silky on the outside (rarely white or pink), subequal, only slightly curving outwards apically. Petals fading and becoming bleached after about a week. Stamens numerous, 50-120 per flower, crowded, the outermost shorter, sterile, club-shaped and secreting nectar. Staminodes and fertile stamens not more than half as long as perianth segments, 15-25 mm; filaments stout at the base, tapering to the adnately attached anthers, which are bright golden-yellow before fading. Styles purple, borne on a flattened, conical, receptacle, 30-90 per flower, each with a single functional ovule. Fruit is an achene, 2-3 mm long, with a single embryo, covered with simple, silky hairs and with a persistent feathery style 3.5-5 cm long. The internode between the stem leaves and flower elongates considerably after flowering, increasing the height at which the achenes are released (Fig. 1b). Flowers 1- 3(-12) per plant, actinomorphic, hermaphrodite and protogynous in England, pollinated by a variety of insects, especially bees (Apidae: Apis, Bombus).

1.2 Taxonomic considerations The common name Pasque Flower has several derivations; one is reputedly from the Latin pascha, meaning Easter, as Easter eggs were often stained by rubbing the eggs with the flowers and leaves for celebration. Originally the flower was known by the French as the ‘passe-fleur’, and then changed by Gerard (who considered it to be a worthy addition to the herbaceous border) to the ‘Pasque Flower’ on account of the flowers appearing around Easter time (Smith, 1996).

3 Figure 1 – Pulsatilla vulgaris: (a) flowers, Knocking Hoe, Bedfordshire, photo by K.J Walker; (b) elongated scape and achenes, Devil’s Dyke, Cambridgeshire, photo by K.J. Walker; (c) illustration by Stella Ross-Craig (1948).

Pulsatilla vulgaris was described by Carl Linnaeus (1753) as Anemone pulsatilla in the first volume of his Species plantarum (p. 539)1. The Scottish botanist Philip Miller (1768) changed the name to Pulsatilla vulgaris in the eight edition of The gardeners dictionary and this was subsequently retained in Aichele & Schwegler’s (1957) monograph of the genus which described a number of taxa within the Pulsatilla vulgaris group. As no holotype exists a lectotype has recently been designated from Linnaeus’ herbarium (Herb Linn. No. 710.5; Jarvis et al., 2005). This herbarium sheet contains a single flowering and two fruiting stems but has no collection details and thus its origin is unknown.2

Pulsatilla is a small genus within the large, primitive family Ranunculacae. The division of the Linnaean concept of ‘Anemone’ into three genera, Anemone sensu stricto, Hepatica and

1 see http://www.biodiversitylibrary.org/page/358106#551 2 see http://www.linnean‐online.org/5012/

4 Pulsatilla is now generally accepted based on both morphology and chloroplast DNA (e.g. Hantula et al., 1989). Morphologically Pulsatilla taxa are distinguished by the styles elongating greatly and becoming feathery in fruit and the presence of nectar-secreting staminodes (both absent in Anemone sensu stricto; Akeroyd, 1993). The current worldwide classification scheme of the Angiosperm Phylogeny Group (APG III) considers the Ranunculaceae to be among the most basal of the derived Eudicots clade (Hill & Preston, 2002): APG Clade: EUDICOTS APG Order: Ranunculales APG Family: Ranunculaceae Subfamily: Ranunculoideae Genus: Pulsatilla Species: Pulsatilla vulgaris Mill.

The genus Pulsatilla contains around 38 species worldwide all of which occur in the Northern Hemisphere, mainly in Europe and Asia with two species in North America. Nine species occur in Europe (Akeroyd, 1993). Five of these are restricted to the montane regions of southwest, central-south and southeast Europe (P. alba, P. alpina, P. halleri, P. montana, P. rubra); the remaining four taxa are more widespread in the lowlands of northern, central and eastern Europe extending from the Atlantic to Eurasia (P. patens, P. pratensis, P. vernalis, P. vulgaris).

Pulsatilla vulgaris is told from all other Pulsatilla species by its sessile cauline leaves, deeply pinnatisect basal leaves with 7-9 primary segments that wither in the autumn and erect flowers (nodding in anthesis). It is a very variable species for which a number of poorly defined infraspecific taxa have been described in the past. These, however, appear to represent the more distinct of the numerous isolated populations and probably represent a ‘dissected continuous’ type of variation caused by post-glacial climatic changes and the intolerance of the species to ploughing, shade and bad drainage (Akeroyd, 1993). Consequently infraspecific taxa do not often appear to fall into the geographical pattern characteristic of subspecies. The smaller and more isolated populations, particularly towards the edge of the range of the species, are fairly homogeneous (as in Britain), but in other areas there is considerable variation within populations. While it is likely that most populations are separable from one another, there is a large amount of overlap between them and intermediates occur frequently.

Today three subspecies are usually accepted. Subspecies vulgaris, to which all English populations belong, is the most widespread taxon extending from 61º N in Sweden to c. 45º N in the Bordeau region of France and from Gloucestershire in England to near to Poznan in western Poland where it is replaced by subsp. grandis (Lindell, 1998). Subsp. vulgaris is distinguished by the greater degree of lobing in the leaves (>100; <40 in subsp. grandis), narrower perianth segments and presence of leaves at flowering (occurring after the flowers in subsp. grandis; Akeroyd, 1993). A third taxon, subsp. gotlandica, confined to limestone pavement on the Swedish island of Gotland (Jonsell, 2001), is dubiously distinct and placed within subsp. grandis by some authorities (e.g. Akeroyd, 1993). On the whole British populations exhibit little variation although plants on the Oolitic limestone are generally larger and produce more flowers (Wells & Barling, 1971). Under heavy grazing plants also tend to be much smaller and more compact (Bailey, 1996).

5 1.3 Genetic implications The chromosome base-number of the genus is 8. Pulsatilla vulgaris is tetraploid (2n = 32) and may have arisen following hybridization between P. patens (2n = 16) and P. pratensis (2n = 16) (Böcher, 1934). Spontaneous hybrids between subsp. vulgaris and P. pratensis and P. patens are known from Northern Europe (Akeroyd, 1993) and work on Swedish populations has indicated that hybridization barriers are weak between subspecies of Pulsatilla vulgaris, and between P. vulgaris and P. halleri (Lindell, 1998).

Bailey (1996) found a low percentage of polymorphic loci in five sites across the geographic range of Pulsatilla vulgaris in England (Barton Hills, Knocking Hoe, Rodborough Common, Devils Dyke, Therfield Heath), suggesting that overall genetic variation is low, although there were significant differences for individual primers between some of the sites examined. Further work is needed to more fully assess these differences, and in relation to overall fitness, population size and degrees of geographical isolation.

Similar work has been undertaken in Germany on 11 populations ranging from 50 plants to 7300 plants (Hensen et al., 2005) and found a significant positive relationship between genetic diversity and both population size and seed mass (per population). Genetic diversity was significantly lower in smaller populations than in larger ones, suggesting that genetic drift (random change of allele frequency within a population) has been the main cause of the loss of diversity as populations have become smaller and fragmented following rapid land-use change (i.e. the chance of alleles being lost from one generation to another has been greater in smaller populations).

Hensen et al. (2005) also found a high level of within population variability which was attributed to life-history traits likely to preserve variability, namely allogamous pollination, a long life span and vegetative reproduction. Interestingly there was only weak, albeit significant differentiation between populations which was correlated to the geographical distance. This suggests that genetic drift has been the major force driving differentiation between German populations as the former larger population became fragmented. The weakness of this relationship suggests that the loss of genetic variability through drift has been, to some extent, balanced by gene flow between closer populations. Since seed dispersal in Pulsatilla vulgaris is limited it was concluded that the foraging radius of pollinators, currently thought to be in the order of several kilometres for honeybees (Steffan-Dewenter & Kuhn, 2003) and bumblebees (Osborne et al., 2008), is critical in offsetting genetic drift as populations become smaller and more isolated. However, even if pollinators forage over several kilometres it seems very unlikely that they would travel between English populations given their small size and degree of isolation.

1.4 Medicinal properties Pulsatilla vulgaris is unpalatable and poisonous to humans and animals due to the presence of the glycoside ranunculin in the leaves and roots which is converted to anemonine when the plant is dried (Plants for a Future, 2010). Small doses are taken internally in the treatment of pre-menstrual syndrome, inflammations of the reproductive organs, tension headaches, neuralgia, insomnia, hyperactivity, bacterial skin infections, septicaemia, spasmodic coughs in asthma, whooping cough and bronchitis. Externally, it is also used to treat eye conditions such as diseases of the retina, senile cataract and glaucoma. In homeopathy, extracts are used to treat measles as well as minor complaints such as nettle rash, toothache, earache and bilious indigestion (Plants for a Future, 2010).

6

2 Distribution and current status

2.1 World Pulsatilla vulgaris subsp. vulgaris is endemic to Western and Central Europe and is not known to have been introduced to other parts of the world.

2.2 Europe Pulsatilla vulgaris belongs to the European Temperate element (Preston & Hill, 1997) with the core of its distribution in the lowlands of western and central Europe (Fig. 2).

Its current status in Europe is given in Table 1. France appears to be the stronghold for the plant in Europe and consequently it was not listed as a priority species for conservation in the most recent assessment of the French flora (unlike P. vernalis; Olivier et al., 1995). In comparison it appears to be threatened throughout the rest of its range. In Denmark, Germany and Southern Sweden it is still relatively widespread, but appears to have declined, especially in Sweden, where it is now classified as Vulnerable using IUCN threat criteria (A2ac; Gärdenfors, 2010), and Germany, where it’s populations are now small and highly fragmented (Hensen et al., 2005). Similar trends have been reported for Austria, where only around 2000 plants now survive in 23 sites (Franz, 2005), and Switzerland where it is very rare (Pfeifer et al., 2002) and classed as Endangered under IUCN threat criteria (Moser et al., 2002). In Belgium it is confined to two small areas in the southern province of Wallonia, where its habitat (limestone grassland) is under pressure from extensive tree planting (Quentin Groom, pers. comm.). In Luxembourg it is classified as Endangered under IUCN criteria having declined from 28 to 5 localities with population sizes now ranging from two to more than 7000 genets (Colling, 2005). It appears to be extinct in Finland, where it has not been seen since the 1930s (Rassi et al., 2001) and Holland. It’s status in Poland is unknown although recent maps (e.g. Fig. 2) show it to be very rare. Recent records for Norway all appear to be of casual escapes (Jonsell, 2001).

7

Figure 2 - Distribution map of Pulsatilla vulgaris subsp. vulgaris in Northwest and Central Europe, reproduced from Hensen et al. (2005). Small filled circles are individual site records from 1950 onwards. Small empty circles are individual site records older than 1950 or occurrences reported as extinct. Atlas Florae Europaeae data from Jalas & Suominen (1989) are also shown (large filled grey circles) to indicate 50 × 50 km squares from which no individual occurrence data were available. The doubtful two easternmost records from Poland are given by EUNIS (2004) but not by Wojtowicz (2001).

Table 1 – The status of Pulsatilla vulgaris in Europe. Country IUCN Status Reference Austria ? Declined to 2000 plants in 23 sites Franz, 2005 Belgium ? Very rare and declining Denmark ? Unknown Finland EW Formerly one site Rassi et al., 2001 France ? Not threatened? Olivier et al., 1995 Germany ? Widespread but declining Hensen et al., 2005 Holland EW Extinct Luxembourg EN Declined from 28 to 5 localities Colling, 2005 Norway - Casual escape Jonsell, 2001 Poland ? Unknown Sweden VU Ca.30% reduction in past 100 years Gärdenfors, 2010 Switzerland EN Marked decline Pfeifer et al., 2002; Moser et

8 al., 2002 UK VU Declined from ca.130 to 18 Cheffings & Farrell, 2005 localities

2.3 United Kingdom 2.3.1 England

2.3.1.1 Native populations Since its discovery near to Oxford in 1551 (Druce, 1886) Pulsatilla vulgaris has been recorded from around 130 sites in 19 English vice-counties (Table 2) but is now confined to 18 sites in just ten vice-counties (Table 3). Former strongholds include the Cretaceous chalk downland and ancient earthworks of Bedfordshire, Berkshire, Buckinghamshire, Cambridgeshire, Hertfordshire and Oxfordshire and the Jurassic limestone grasslands of Gloucestershire, Northamptonshire and Lincolnshire (Fig. 3). It was also formerly widespread in Magnesian limestone grasslands in northern England, extending as far north as Piercebridge in County Durham (Baker, 1906) but it is now restricted to a single site near to Wakefield (Abbott, 2005). Small clusters of populations also occurred in North Essex, Leicestershire, West Norfolk and West Suffolk but it has not been seen in any of these counties since 1888, 1992, 1914 and 1978 respectively (Table 4).

Table 2 – The number of Pulsatilla vulgaris populations recorded in English vice-counties. †Extinct. Population size (2000-10 period) Tota % Extinc 11- 201- l extinc VC Vice-county name 1-10 51-200 >1000 t 50 1000 no. t 19 North Essex† 2 2 100 20 Hertfordshire 7 1 8 88 22 Berkshire 12 1 13 92 23 Oxfordshire† 4 4 100 24 Buckinghamshire 2 1 3 67 26 West Suffolk† 3 3 100 28 West Norfolk† 1 1 100 29 Cambridgeshire 7 1 8 88 30 Bedfordshire 2 2 2 6 33 31 Huntingdonshire† 1 1 100 32 Northamptonshire 7 1 8 88 East 33 17 1 2 1 1 22 77 Gloucestershire West 34 4 1 5 80 Gloucestershire 53 South Lincolnshire 16 1 1 18 89 54 North Lincolnshire† 5 5 100 55 Leicestershire† 5 5 100 South-west 63 6 6 100 Yorkshire† 64 Mid-west Yorkshire 7 1 8 88 66 Durham† 1 1 100 Total 109 6 3 3 1 5 127 86

9

Of the 10 vice-counties with surviving populations, seven only have single colonies. Bedfordshire and East Gloucestershire have the most with 4 and 5 populations respectively. Half the English populations support less than 100 plants, including one site (Ledsham, Mid- west Yorkshire) with a single individual (known since 1984). Only five sites (28%) support in excess of 1000 plants (Fig 4a). Although total population sizes are difficult to estimate, recent counts on these sites suggest the following totals: 20,000 at Barnack Hill and Holes, 75,000 at Barnsley Wold, 5,000 at Barton Hills, 1,000 at Knocking Hoe and 60,000 at Therfield Heath (Tarpey, 1999; see Annex 2 for details). These five sites account for 99.3% of the total British population. Of the eighteen surviving populations 4 appear to be declining and are threatened with extinction, 9 are stable and 5 appear to be increasing due to improvements in grazing regimes (Table 3; see Annex 2 for details).

Figure 3 – The hectad distribution of Pulsatilla vulgaris in Britain and Ireland. Solid black circles are hectads where P. vulgaris has been recorded since 2000; solid grey circles, recorded 1987-1999; open circles, recorded before 1987; X, introduced.

Historical losses appear to have been high in all vice-counties especially East Gloucestershire, South Lincolnshire and Berkshire where 77%, 89% and 92% of populations have gone extinct (Table 2). The rate of loss appears to have been increased consistently since 1750 from around 1.8 populations per decade to 6.0 since 1950 (Fig. 4b) although these figures presumably underestimate rates for earlier periods as fewer ‘extinction events’ are likely to have been detected by eighteenth century botanists (as fewer populations were then known). Consequently the total number of populations has displayed a consistent downward trend (Fig. 4c). However, since 1960, the first period when we have detailed information on the size of

10 English populations, the overall number of plants has increased considerably from an estimated 60,000 to over 160,000 individuals largely due to improvement in grazing regimes on four of the best sites (Barnack Hills and Holes, Barnsley Wold, Barton Hills, Therfield Heath; Fig. 4d). Despite these losses new populations continue to be found including a small population of around 15 plants in Swinstead Valley (South Lincolnshire) discovered in 2009 (Jefferson & Walker, 2010).

Table 3 – Details of extant populations of Pulsatilla vulgaris in England. Cons. Size/ Site VC 10-km Geology/management Design trend . Therfield Heath 20 TL33 Chalk, winter grazing E↑ SSSI Chalk, ungrazed exclosure, occ. SSSI Aston Upthorpe Down 22 SU58 B(r)↓ mown Steps Hill 24 SP91 Chalk, intermittent grazing B↓ SSSI TL56/ SSSI Devil's Dyke 29 Chalk, some areas grazed/mown C≈ 66 Barton Hills 30 TL03 Chalk, grazed excluding Jan-Mar D↑ NNR Ravensburgh Castle 30 TL02 Chalk, ungrazed B↓ SSSI Deacon Hill 30 TL12 Chalk, some areas grazed A≈ SSSI Knocking Hoe 30 TL13 Chalk, grazed D↑ NNR Limestone, grazed excluding Mar- NNR Barnack Hills and Holes 32 TF00 E↑ Sep Limestone, grazed excluding Mar- SSSI Barnsley Wold Warren 33 SP00 E↑ May Beaumonts Hay 33 SP12 Limestone, irregular grazing A≈ SSSI Limestone, grazed excluding Apr- SSSI Bourton Down 33 SP13 C≈ Aug Limestone, grazed excluding Mar- SSSI Hornsleasow Roughs 33 SP15 C≈ May Taylor’s Hill 33 SP01 Limestone, grazed C≈ - Rodborough Common 34 SO80 Limestone, light mowing/grazing B↓ SSSI Ancaster Valley 53 SK94 Limestone, winter grazed B(r)≈ SSSI Swinstead Valley 53 TF02 Limestone, summer grazed A≈ SSSI Ledsham 64 SE43 Limestone, winter grazed A(r) ≈ SSSI Code for population sizes and trends: A, 1-10; B, 11-100; C, 101-1000; D, 1001-10000; E, 10000-100000; (r), includes reintroduced plants. ↑, population increase; ↓, population decline; ≈ population stable.

Table 4 – Vice-counties in which Pulsatilla vulgaris is now extinct with reason for loss VC Vice-county Last recorded site Last Probable reason for loss name record 19 North Essex Bartlow Hill 1888 Scrubbed-over 23 Oxfordshire Upton Down 1883 Ploughed-up 26 West Suffolk Newmarket Heath 1978 Grassland altered by horse training 28 West Norfolk Sporle & Tulip Hills 1914 Scrubbed-over 31 Huntingdonshire Stibbington 1926 Possibly an error for sites in VC32?

11 54 North Broughton Far 1969 Scrubbed over; last plant ‘dug- Lincolnshire Wood up’ 55 Leicestershire Shacklewell Hollow 1992 Dumping of rubble 63 South-west Smeaton Crag 1870 Quarrying/mining Yorkshire Pastures 66 Durham Cliffe Wood 1906 Landscaping of parkland

Although there is no fossil evidence of the occurrence of Pulsatilla vulgaris in Europe it was probably much more widespread during the early post-glacial in dry, steppe grassland before retreating to open refugia, with shallow soils and low competition, following the spread of deciduous woodland (Hensen et al., 2005). Woodland clearance from the Neolithic onwards, however, is speculated to have created much new habitat enabling spread from refugia, although ‘barriers’ to migration would have been present in some regions. For example, woodland is thought to have restricted its colonisation of the southernmost chalk in England (Pigott & Walters, 1954; Rose, 1957) although its absence from Late Glacial refugia such as the Avon Gorge and centres of Neolithic farming activity, such as Salisbury Plain, suggests a much more complex phytogeographical history in Britain, or at least one that is impossible to reconstruct from modern records alone.

Figure 4 – The number and size of populations of Pulsatilla vulgaris in England: (a) size of extant populations; (b) number of populations lost per decade; (b) the number of populations

12 surviving in each year, and (c) the total number of populations and plants recorded since 1960. In (c) all populations were assumed to have been present in 1750 even if they were only discovered much later.

2.3.1.2 Introductions There are around a dozen deliberate or casual introductions known in England (Table 5), with most resulting from ‘tipping’ of garden waste by roadsides or in old quarries. There have also been six deliberate introductions to either re-establish populations on sites where it become extinct (Copper Hill Quarry, Southorpe Paddock), bolster extant populations (Aston Upthorpe, Ancaster, Ledsham) or create entirely new populations for the purposes of research (Hartslock) (see Table 11 for details). The most contentious site, however, is the small population that straddles the border of Dorset and South Wiltshire on Martin Down which interestingly appears to have increased since its discovery in 1983 (see http://www.hantsplants.org.uk). Both Bowen (2000) and Brewis et al. (1996) suggest it might be native given the typical nature of the habitat (ancient species-rich grassland on an earthwork). However, in view of its isolation from other native populations and late discovery, which is surprising given its close proximity to a path, it is probably best treated as an introduction unless convincing evidence is produced for it being of natural occurrence (Preston et al., 2002; Edwards & Pearman, 2004).

Table 5 – Known casual records of Pulsatilla vulgaris in England. Details of translocations are given in Table 11. VC VC name Details 7 North Wiltshire Planted on Morgan’s Hill in 1939 from where it possibly colonised Cherhill Down by 1941 (Grose, 1957) but this seems unlikely. 8/9 South Known from Martin Down since c.1983 where two small Wiltshire/Dorset populations grow on either side of the vice-county boundary on ancient species-rich chalk banks (SU0518, SU0418). Likely to have been planted given the distance to the nearest native populations (Edwards & Pearman, 2004). 13/1 West & East No details; presumed planted. 4 Sussex 20 Hertfordshire Discovered on road verges at two sites (TL1226; TL2426) where it was presumed to have been planted (T James, pers. comm.). 21 Middlesex No details; presumed planted. 24 Buckinghamshire Discovered in 1998 (SP8405) but assumed to have been planted. 29 Cambridgeshire In 1994 a few plants originating from a garden were planted on an area of downland reverting from arable (L Evans, pers. comm.). 30 Bedfordshire Recorded in a quarry where it had presumably been planted (C Boon, pers. comm.).

2.3.2 Northern Ireland, Scotland & Wales Pulsatilla vulgaris does not occur in Northern Ireland, Scotland or Wales.

3 Ecology & life cycle

3.2 Life cycle and phenology Pulsatilla vulgaris is a monoecious, long-lived, polycarpic hemicryptophyte which appears to reproduce mainly vegetatively by growth of adventitious buds on the branched rhizome. These

13 produce several daughter rosettes close to the parent plant each year. Although new flower buds are produced during late summer the whole plant is dormant during the winter months (August to March). The tightly furled leaves appear in March and unfurl at or after flowering and wither in the autumn or after the first frosts.

Plants of Pulsatilla vulgaris are very difficult to age due to the production of new ramets from the branched rhizome (‘type C perennials’ sensu Grubb, 1990). However, observations in England suggest that large plants with rhizomes 15-20 mm long may be at least 20 years old (Wells & Barling, 1971) although individual genets are potentially much longer-lived with half- life of more than 50 years (Grubb, 1990). Plants grown from seed will flower in pots in 1.5-2.5 years but in the wild this is likely to be 4-5 years.

3.1.1 Flowering phenology Temperature appears to be a very important cue that regulates the timing and rate of flower and fruit development (Widén & Lindell, 1996). Flowering commences when temperatures rise above 12-15°C (Kratochwil, 1988; Widén & Lindell, 1996), usually in the first week of April, reaching a peak between 4-5 weeks later, and continues to the end of June (Fig. 4; Wells (1994) gives the main flowering period as the 6 April to 20 May). However, the onset of flowering and flower production does vary from year to year depending on climatic conditions. For example, flowering and fruit maturation is known to be higher in warmer years (e.g. 1988; Widén & Lindell, 1996) and for cultivated plants exposed to full sun light either in the greenhouse (Widén & Lindell, 1996) or under experimental shading conditions (Fig. 5; Walker et al., in press). In large populations, however, the behaviour of individuals is variable, some plants flowering in successive years whilst others remain vegetative (Wells & Barling, 1971). In addition, drought in one summer may affect flowering the following year as primordia are initiated in late summer (Rich, 1997).

60

50

40

30

20

10 Number of site records site of Number 0 1 2 3 4 5 6 7 8 9 101112131415161718192021 Weeks from 1st March

Figure 4 – Phenology of Pulsatilla vulgaris in England based on the number of historical records for sites held in the Vascular Plants Database, regardless of location, year & recorder.

3.1.2 Flower biology Each plant produces 1-3(-12) bell-shaped flowers with numerous carpels with long purple styles (30-150) and bright yellow stamens, the outer smaller, sterile and secreting nectar (Fig. 1a). These are produced on very short stalks and face the sky for about 48 hours after first opening, only closing at night or during rain (Wells & Barling, 1971). Flowers are hermaphrodite and markedly protogynous with the female reproduction organs reaching

14 maturation before the male (andro- and gyno-monoecious and dioecous forms have been reported from the continent but are likely to be rare). Both stamens and styles continue to grow during anthesis increasing the distance between the anthers and stigmatic papillae (Jonsson et al., 1991). On cultivated plants the obligate female phase (the time from the beginning of anthesis to the opening of the first pollen sac) lasts just over a day whereas pollen is produced for about 4 days and remains viable for 7-8 days (Jonsson et al., 1991). The obligate female phase appears to be much shorter late in the flowering season and is directly correlated with an increase in temperature (Kratochwil, 1988; Jonsson et al., 1991). In most populations the length of the obligate female phase is likely to be sufficient for some cross- pollination to take place since the great proportion of flowers receive pollen before the onset of the male phase (Jonsson et al., 1991). However, geitonogamous pollination is probably also common as most populations include plants with 2 or more flowers, including flowers on identical (daughter) genets growing close-by (Warden, 2001).

Figure 5 – Effects of experimental shading on (a) the % survival and (b) flowering performance of Pulsatilla vulgaris grown at Monks Wood Experimental Station, Cambridgeshire, 1970-80 (Walker et al., in press). Plants were planted in a chalk subsoil to a depth of 1 m and exposed to three levels of shading (dense, medium, light) simulated using black gauze screens erected over each plot. Each plot consisted of 12 regularly spaced plants 25 cm apart. Three replicates of each treatment and a control (no shade) were arranged in a randomised latin square and the survival of transplants and flowering performance recorded in April and May of each year. The plots were fenced to exclude rabbits and weeded to remove competition.

3.1.3 Pollination The flowers of Pulsatilla vulgaris are insect-pollinated mainly by aculeate Hymenoptera and bees (Apidae: Apis, Bombus). Many other insects have been recorded visiting flowers in England and on the continent but appear not to contribute significantly to pollination (e.g. flies, beetles, Lepidoptera, non-Apoidea Hymenoptera; Wells & Barling, 1971; Kratochwil, 1988; Warden, 2001). Experiments with exclusion of pollinators showed that Pulsatilla vulgaris is mainly an outbreeding plant due to the absence of spontaneous selfing (index of self- incompatability (ISI) <0.1, n = 18; ISI cited in Henssen et al., 2005). However, work on Swedish

15 populations has shown that dichogamy is incomplete, since artificial selfing produces a small amount of fertile seed although selfed flowers produced fewer seeds than those that cross (Jonsson et al., 1991; Lindell, 1998). Seed set from self-pollination is variable with reported values of 18% in England (Warden, 2001) and 31-50% in Sweden (Lindell, 1998). Insects seem to be necessary even for self-fertilisation as enclosed flowers do not set seed automatically (Wells & Barling, 1971; Kratochwil, 1988; Widén & Lindell, 1996) and early flowering plants and those in small populations have lower seed-set due to pollinator-limitation (Widén & Lindell, 1996).

3.1.4 Seed production Between 30-90 carpels are borne on a flattened, conical receptacle, each containing a single embryo which when fertilised develops into an achene 2-3 mm long with a persistent feathery style (3-5 cm) borne on stems that elongate after anthesis (Fig. 1b). Achenes ripen 4-5 weeks after the flowers open and fruits may be ripe from mid May to mid June. There is considerable variation in the number of achenes produced per flower and total achene production per plant. For example, Wells & Barling (1971) found 23-74 achenes per flower in five English sites, with an average of 46, though not all may have been fertile (Rich, 1997) whereas Warden (2001) found an average of 62 at Aston Upthorpe in Berkshire of which ca.30-35 were viable (‘filled’). In Sweden Widén & Lindell (1996) found a similar average of 18 and 28 viable (undamaged) seeds per flower at two sites excluding achenes damaged by seed-boring insects.

In Germany Kratochwil (1988) found fruit set to exceed 70% over four years, even though only a few hours of favourable conditions occurred in most years. However, intermediate flowering plants appear to be more fecund than earlier or late flowers, because early flowers encounter a paucity of pollen vectors and suffer from early frosts whereas late flowers suffer from greater predation and may have to compete with developing leaves for resources (Widén & Lindell, 1996; Warden, 2001). Later-flowering plants also appear to develop seeds more rapidly due to higher temperatures (Widén & Lindell, 1996). Flowers in most populations produce infertile achenes containing no embryo, usually towards the centre of the flower; these weigh about 0.6 mg whereas fertile achenes weigh 3 mg (Wells & Barling, 1971) although seeds containing no embryo can sometimes weigh more than those that are viable (Bailey, 1996). The cause of this infertility is unknown but is presumably caused by cold, inclement weather at the time the flower is produced and the abundance of flying insects. (e.g. 1996 in England; Bailey, 1996).

3.1.5 Seed viability and germination The viability of fresh seeds is generally high with reported germination values at room temperature of 47% for Swedish material (Widén & Lindell, 1996) and 59% (Bailey, 1996), 75% (Warden, 2001) and 90% (Wells & Barling, 1971) for English material. Under more controlled laboratory conditions 80% germination was been achieved on 1% Agar solution at 20°C, 8/16 hours light and dark and 95% at 21°C, 12/12 hours light and dark (RBG Kew, Wakehurst Place). In comparison, only 16% of seeds germinated in a field germination trial increasing to 29% when seeds were covered with 3 mm of soil (Wells & Barling, 1971).

Tests on the viability of seed stored at room temperature have shown variable declines with age. Wells & Barling (1971) found between 15-65% germination after 8-9 months with no germination occurring after 2.5 years. However, only a small decreases in viability has been reported for seed stored at 4°C for one year (Warden, 2001) and dried to low moisture contents and stored for 13 years (RBG Kew, Wakehurst Place). Germination appears to be unaffected by light levels or storage at temperatures as low as -7°C (Wells & Barling, 1971).

16

3.1.6 Seed dispersal Achenes of Pulsatilla vulgaris are adapted for wind-dispersal by modification of the style into a feathery pappus and the elongation of the fruiting stems (by a process of cell elongation), increasing the height at which the ripe seeds are released to above the general level of the surrounding vegetation (Fig. 1b). For example Wells & Barling (1971) give a mean scape height at fruiting of 18.4 cm for 50 plants at Barnsley Wold in 1966 as opposed to 4 cm for the surrounding grassland. Despite these adaptations, long-distance dispersal is most probably absent or very rare (Tackenberg et al., 2003). Observations in England suggest that seeds disperse less than 20 cm from parent plants often because the entire head remains intact or the feathery tail becomes entangled in the surrounding vegetation (Wells & Barling, 1971; Warden, 2001). In addition simulations of aemochorous dispersal showed that 90% of the seeds land within the mother population with only 0.05% of seeds being dispersed over a distance of more than 100m (Tackenberg, 2001). According to Röder & Kiehl (2006) Pulsatilla seeds also have a high potential for epizoochory, including dispersal on machinery, which might be a more important strategy for long distance dispersal in modern landscapes. Establishment of new populations in this way is likely to be rare, but may have occurred at one site in Cambridgeshire where a new population was discovered 300 m from the nearest population (Leslie, 2004; see Devil’s Dyke, Annex 1). Dispersal by machinery is the most likely vector at this site as the new colony occurs on a mown road verge inaccessible to livestock.

3.1.7 Regeneration Despite the production of viable, highly germinable seeds, establishment of new individuals from seed appears to be rare (seedlings observed at only one site by the author) and most regeneration, is probably achieved by the disintegration of the branched rootstock (Wells & Barling, 1971). Plants reproduce vegetatively by growth of adventitious buds on the rhizome 2 cm or more below ground level, producing a small rosette of leaves close to the parent plant. Two or three new rosettes may be produced each year and excavation of groups of plants has revealed as many as seven distinct rosettes from a single rootstock, the younger plants being clustered around the parent plant. Consequently, the density of flowering stems can reach up to 67 plants m-2, although an average of ca.4 plants is probably more typical in short, well managed grassland (Wells & Barling, 1971).

Pulsatilla vulgaris appears to have a short-lived, transient seed bank (Thompson et al., 1997) and so most recruitment is likely to occur shortly after the seed is dispersed. Once the seed reaches the soil surface hygroscopic movement of the style may help bury the seed, but this has not been observed. Germination is epigeal, the green cotyledons expanding 3-6 mm above the soil surface. The slender primary root of the seedling grows vertically downwards reaching a depth of 15 cm within 6 months of germination by which time it has formed an extensive root system. At this stage the underground stem is ca.2 mm long with 2 or 3 leaves arising from axillary buds at the apex of the rootstock.

The establishment of new plants appears to be a rare event as seedlings have only been observed a few times in recent decades. For example seedlings were found on only one site during a recent survey of all extant British populations (Fig. 6). At this site (Bourton Down) seedlings were confined to bare soil in very open grassland with abundant limestone rubble at or on near the soil surface (see Fig. 9k).

Soil moisture appears to be critical for establishment as seedlings only appear to survive in wet summers (Wells, 1994; Rich, 1997). For example, Wells & Barling (1971) showed that

17 higher germination occurred where seeds were covered with a thin layer of soil but that all seedlings suffered high mortality due to physical disturbance and herbivory. In addition, seedling development was extremely slow and even after two years plants were still very small.

These factors, combined with low seed production and frequent dessication in drought-prone soils, probably explain the apparent inability of this species to spread to new sites and the rarity of seedlings in the wild.

Figure 6 – Seedlings of Pulsatilla vulgaris recorded at Bourton Down in Gloucesterhire on 30th April, 2005.

3.1.8 Response to competition Pulsatilla vulgaris occurs at highest density where soils are shallowest and above ground competition (biomass) is low (Fig. 7a). Flower production also decreases as competition from tall grasses increases, with a sharp fall occurring when the surrounding vegetation reaches 10- 15 cm (Fig. 7b). This was first observed in grazing exclosures (Wells, 1968) and has been attributed to the smothering effect of leaf litter of Bromopsis erectus and increased competition from tall grasses. For example, Mitchley (1988) showed a positive correlation between interference ability and mean height of the rosette leaves in Bromopsis erectus grassland. This was attributed to the ability of dominant species such as B. erectus to project their leaves into the upper canopy thereby reducing the amount of photosynthetically active radiation able to reach lower levels (Mitchley & Willems, 1995). Bromopsis erectus is also known to generate high ‘shoot thrust’, enabling it to attain early dominance in the vegetation by physically restricting the growth of surrounding species, especially low-growing hemicryptophytes such as Pulsatilla vulgaris (Campbell et al., 1992). Attempts to simulate these effects through shading have shown significant decline in longevity, survivorship and flowering performance at increasing levels (Fig. 5). Likewise transplants of Pulsatilla vulgaris have significantly greater survivorship and performance (number of leaves) when competition from surrounding vegetation is removed (Warden, 2001). These findings highlight the critical role of above-ground competition plays in restricting the amount of light reaching the base of

18 the sward and thereby determining the relative abundance of hemicryptophytes such as Pulsatilla vulgaris.

(a) (b)

Figure 7 – The effects of competition on Pulsatilla vulgaris. (a) The relationship between depth of soil and above-ground biomass on the density of Pulsatilla vulgaris at Barnsley Wold, Gloucestershire. Means based on 50 samples at each soil depth. (b) The relationship between sward height and the % of Pulsatilla vulgaris plants in flower in a grazing exclosure at Barton Hills, Bedfordshire. Each dot represents a year with overall numbers increasing from 138 following the withdrawal of grazing 1964 to 654 in 1969. Both figures adapted from Wells & Barling (1971).

3.1.9 Herbivory, parasites and disease Pulsatilla vulgaris is a plant of sheep and rabbit grazed downland and is well adapted to grazing by herbivores. The plant is dormant during the winter, and at other times the vegetative and floral buds and leaves are generally at ground level and therefore not readily available to grazing animals. Occasionally whole flowers are grazed by rabbits, or the flower or part of it are eaten by caterpillars, pheasants (Bowen, 1997) or small mammals (wood mouse Apodemus sylvaticus, field vole Microtus agrestis) (Carter, 1967). Although the leaves contain anemonin they are eaten by sheep, rabbits, slugs and snails. Caterpillars of two leaf- mining moths of the genus Cnephasia have also been recorded on leaves in the UK (Database of Insects and their Food Plants, accessed August 2010). At least two other leaf-mining insects have been reported on the continent and nematode worms of the genus Meloidogyne have been reported to cause root galls in the Netherlands caused by (Wells & Barling, 1971).

In Sweden achenes are attacked by the larvae and pupuria of a range seed-boring flies belonging to two Diptera families, the Agromyzidae and Cecidomyiidae, and are a potentially serious factor reducing seed production by up to 36% (Widén & Lindell, 1996). Many small flies have been reported visiting flowers of Pulsatilla vulgaris but no evidence of attack of seed has so far been observed (Warden, 2001). Parasites on Pulsatilla vulgaris include Cuscuta epithymum, which has been recorded on plants at Barnsley Wold. The fungal rust Coleosporium pulsatilla has also been recorded on Pulsatilla species on the Continent (Aichele & Schwegler, 1957), but it is not known if hosts include Pulsatilla vulgaris.

4 Habitat requirements

4.1 The landscape perspective

19 In England Pulsatilla vulgaris is confined to moderately steep south to southwest facing slopes where insolation is high, soils are shallow and competition from other species is restricted (Fig. 8). Most populations are confined to escarpment grasslands of Chalk and Jurassic limestone (Fig. 9c, 9e-g, 9i-l) but it also occurs in similar grasslands in old quarries (e.g. Hornsleasow Roughs, Fig. 9b) and on ancient earthworks such as hill-forts (e.g. Ravensburgh Castle, Fig. 9d) and Anglo-Saxon dykes (e.g. Devil’s Dyke, Fig. 9a). In old quarries and on earthworks plants tend to occur on relatively shallow slopes on a greater range of aspects, although even on these plants are generally found on more southerly aspects than those facing northwards (Wells & Barling, 1971). Plants usually occur at greatest density on the steepest (mid) part of the slope where soils are shallowest, rather than on deeper soils at the top or bottom. For example, Wells & Barling (1971) recorded densities of 7.5 plants m-1 where the soil was 5 cm deep but only 1.2 plants m-1 at soil depths greater than 100 cm (Fig. 7a).

(a) (b)

Figure 8 – The aspect (a) and slope (b) of Pulsatilla vulgaris populations in England. The figures include values for the 29 populations included in Wells & Barling (1971) and five populations discovered since then.

With the exception of Hildersham Furze Hills (see below), Pulsatilla vulgaris occurs on shallow (5-15(25) cm) drought-prone calcareous rendzinas over chalk and limestone with relatively high surface soil pH (average 7.5; range 7.1-7.8; Table 6). These soils are very friable and porous with high contents of calcium carbonate (mean 67%; range 34-91%), organic matter (mean 15%; range 8-22%) and total nitrogen (mean 0.5%; range 0.3-0.7%) (Wells & Barling, 1971). All are base-saturated with calcium being the most abundant cation present (320-830 mg 100g-1 dry soil) with other mineral nutrients, especially phosphorous, occurring at low levels (Table 6). The clay/silt/sand fractions of these soils is also low (<17%).

Pulsatilla vulgaris is confined to similar calcareous strata over most of its European range and in Sweden, Jutland and Zealand it also occurs on sandy, acid soils. At Hildersham Furze Hills, Cambridgeshire, where it was last seen in 1990, a small population also grew on soil derived from glacial sands and gravels mixed with chalk flints and chalky boulder clay. The soil is calcareous sandy loam with no free calcium carbonate, a pH of 5.2 and high sand content (Wells & Barling, 1971; Trist, 1988; Table 6). This site therefore differs considerably from all others in Britain (see Fig. 10b) and provides an important link with continental populations in Sweden and Denmark where Pulsatilla vulgaris grows in acidophilous communities on soils with pH values of 4.8-5.7 with low calcium content and virtually no free calcium carbonate.

20 Table 6 – Chemical and mechanical analysis of soil from Pulsatilla vulgaris sites in England and five sites on sandy soils in Sweden for comparison. These summarise data presented for 10 sites in Table 1 of Wells & Barling (1971). Limestone Calc. Chalka Mean Range Sweden b sandc pH 7.6 7.4 7.5 7.1-7.8 5.2 5.0 Organic matter 13 8-22 8 (%) 15 11 8.5 Nitrogen (%) 0.5 0.4 0.5 0.3-0.7 0.2 0.3 K (mg 100g-1) 18 21 19 11-31 0.9 18 Ca (mg 100g-1) 654 492 582 320-830 170 44 Mg (mg 100g-1) 13 11 12 7-17 12 6 P (mg 100g-1) 1.5 1.0 1.3 0.6-2.3 0.8 1.1 CaCO3 (%) 71 62 67 34-91 0.8 <0.5 Clay (%) 14 13 13 3-21 17 Low Silt (%) 4 13 8 1-42 3 Low Sand (%) 10 17 12 5-34 79 High The ten sites included by Wells & Barling (1971) are as follows (with indication whether Pulsatilla vulgaris is extinct): a chalk, Aldbury Nowers (extinct), Aston Upthorpe, Devil’s Dyke, Knocking Hoe, Pitstone Hill (extinct); b limestone, Barnack Hills & Holes, Barnsley Wold, Holywell Mound (extinct), Shacklewell Hollow (extinct); c calcareous sand, Hildersham Furze Hills (extinct).

All English populations are lowland with an altitudinal range from ca.15 m in Cambridgeshire (also formerly in North Lincolnshire and Northamptonshire) to 245 m at Hornsleasow Roughs in Gloucestershire, with ca.70% of recently recorded populations occurring between 41-160 m. Like many other central and southern European species present in Britain the 16º C mean monthly isotherm for July marks it northwestern limit (mean of 16.5º C for all extant populations). It grows in regions where the annual total precipitation ranges from 520 mm to at least 1088 mm; the mean for extant populations in England is 700 mm. High summer temperatures combined with low summer rainfall therefore restrict its distribution southwards whereas its eastern and northeastern limits are probably determined by its sensitivity to low winter temperature. Perring (1956) speculated that higher humidity might be responsible for its absence from the southern most chalk in England based on an analysis of precipitation/saturation deficit ratios but this has been rejected by Wells & Barling (1971) who cite the past history of chalklands as a much more plausible explanation (but see section 2.3.1.1).

21

Figure 9 – Habitats of extant populations of Pulsatilla vulgaris in England (arrows mark the position of small populations): (a) Anglo-Saxon earthwork, Devil’s Dyke, Cambridgeshire; (b) shallow limestone quarry workings, Hornsleasow Roughs, Gloucestershire; (c) Knocking Hoe and ‘Spiranthes Bank’, Bedfordshire; (d) Ravensburgh Castle Iron Age hill fort, Bedfordshire; (e) Ledsham Banks, Mid-west Yorkshire; (f) Steps Hill (Incombe Hole), Buckinghamshire.

22

Figure 9 continued. Habitats of Pulsatilla vulgaris in England: (g) Beaumonts Hay, Gloucesterhire; (h) Barnack Hill and Holes, Northamptonshire; (i) Barnsley Wold, Gloucestershire; (j) Barton Hills, Bedfordshire; (k) Bourton Down, Gloucestershire; (l) Church Hill, Therfield Heath, Hertfordshire.

4.2 Communities & vegetation In England Pulsatilla vulgaris is almost entirely confined to short, herb-rich Bromion grasslands on calcareous soils derived from the Chalk or Oolitic Limestone (Rodwell, 1992). The main

23 National Vegetation Classification (NVC) grassland type on both chalk and limestone is Bromus erectus grassland (CG3), including grazed species-rich and ungrazed species-poor sub- communities (CGa-b and CG3d respectively) (Fig. 10a). It occurs less frequently in Bromus erectus-Brachypodium pinnatum (CG5) and Brachypodium pinnatum (CG4) grasslands, mainly on limestone (Rodwell, 1992). These three communities form the core alliance of the Brometalia in western Europe and are broadly characterised by the grasses Brachypodium pinnatum, Bromopsis erectus, Helictotrichon pratense, Koeleria macrantha and a wide range of herbs (Rodwell et al., 2007). It occasionally occurs in other calcareous grasslands, especially Festuca ovina (CG2) grasslands on chalk, usually where heavy grazing by sheep and rabbits has reduced the cover of Bromopsis erectus to very low levels. In all these communities the vegetation is typically very diverse (23 species m-2) with a high cover of broad-leaved herbs (44 % m-2) and constant associates include Bromopsis erectus, Carex flacca, Cirsium acaule, Festuca ovina, Helianthemum nummularium and Sanguisorba minor and associated (see Annex 3).

Figure 10 – Grassland communities in which Pulsatilla vulgaris occurs in England: (a) National Vegetation Classification (NVC) grassland types; and (b) ordination plot (Detrended Correspondence Analysis) showing overall variation in species composition. Both plots include quadrat data for 30 sites including all 29 visited by Wells & Barling (1971) plus Swinstead Valley discovered in 2009. Twenty-nine of these quadrats were recorded in 1964-1968 and 27 recorded since 2000. * includes sub-communities 2a & 2d; ** includes sub-communities 3a, 3b and 3d.

Overall there is remarkably little variation between the composition of these grasslands on chalk or limestone (Fig. 10b), the main difference being the almost complete replacement of Brachypodium pinnatum by Bromopsis erectus on nearly all the sites on the chalk (Wells & Barling, 1971). Two notable exceptions, positioned to the extreme left of the first axis of the ordination plot, are Hildersham Furze and Unhill Bottom. Both were rank, species-poor swards dominated by Festuca rubra by the time of the 1964-68 survey. At one of these sites, Hildersham Furze Hills, Pulsatilla vulgaris formerly grew on an acidic soil derived from glacial sands and gravels, although the vegetation was distinctly calcicolous due to the presence of free calcium. Pulsatilla vulgaris occurs on soils with a similar pH in Sweden and Denmark, but these are much more base-poor and consequently the vegetation is dominated by acidophiles such as Calluna vulgaris and Deschampsia flexuosa (Wells & Barling, 1971). Pulsatilla vulgaris probably once grew in similar acid communities in Breckland as a few former sites (e.g.

24 Cavenham Heath) support extensive areas of Festuca ovina–Agrostis capillaris–Rumex acetosella acid grassland (Erodium cicutarium-Teesdalia nudicaulis U1c sub-community), a species-rich types with close affinities to calcareous grassland (Rodwell, 1992).

Pulsatilla vulgaris tends to grow in short swards (7.5 ± 0.7 cm) though it can persist for long periods in taller grassland (>20 cm) in the absence of grazing, cutting or burning. However, recent population trends suggest that a sward height of between ca.5-10 cm is ideal and that in taller swards competitive exclusion by coarse grasses eventually leads to an overall decline in plant numbers (Fig. 11a). Consequently taller swards lead to a reduction in overall species diversity (Fig. 11b) and an increase of in the dominance of Bromopsis erectus (Fig. 11c). Bailey (1996) provides a useful list of species positively and negatively associated with the open conditions favoured by Pulsatilla vulgaris.

Figure 11 –Differences in (a) sward height (cm), (b) species diversity and (c) % cover of Bromopsis erectus (± 1 SE) on extant Pulsatilla vulgaris sites in England (n = 14) in relation to population trends, 1968-2006. Means with the same latter are not significantly different from one another (Walker et al., in press).

4.3 Summary of habitat requirements A number of habitat features are important to Pulsatilla vulgaris in England and these are summarized in Table 7.

Table 7 - A Summary of habitat features important to Pulsatilla vulgaris in England. Type Description Physical and • Lowland (<240 m) topographical • Escarpments, old quarries and earthworks • Moderately steep slopes with a southwesterly aspect • Insolation high (full sun) • Shallow soils (<15 cm) derived from calcareous substrates (chalk, limestone, calcareous sand) Vegetational and • Open CG2-5 calcareous grassland on chalk or limestone structural • Very open vegetation with 30% bare ground • Low vegetation ca.5(-10) cm with low cover of either Bromopsis erectus or Brachypodium pinnatum Processes • Ideally grazing by sheep and rabbits to reduce the dominance of coarse grasses (especially Bromopsis erectus) and to create bare

25 microsites for seed germination and seedling establishment • Transfer of seed between sites by herbivores and/or mowing machinery • Transfer of pollen between populations by insects Chemical • Soils with pH ca. 7.5 (formerly 5) • Infertile soils with high calcium carbonate content

5 Management implications

Pulsatilla vulgaris is a long-lived polycarpic perennial herb which mainly reproduces vegetatively, and rarely from seed. It is a poor competitor and therefore unable to persist in ungrazed, closed swards or amongst scrub where the general height of the vegetation exceeds 15 cm and there is a build-up of litter from coarse grasses, especially Bromopsis erectus and Brachypodium pinnatum. Its survival is therefore dependent on grazing, although short-term fluctuations in grazing intensity or short-term neglect are unlikely to be critical in the longer- term. For example, one of the largest populations in England survived 100 years of sheep grazing, 13 years of very heavy sheep grazing, 22 years of no grazing including a severe fire during the flowering season (Wells, 1968).

Management should aim to produce a sward of ca.5(-10) cm during the flowering period with up to 30% bare ground although there is much flexibility in how this can be achieved (Rich, 1997). The preferred management is sheep grazing from August to April (< 5 sheep ha-1), although low intensity grazing, including by cattle or horses, during the flowering season appears to have no ill-effect. All its current sites are also subject to moderate to high levels of rabbit grazing throughout the year and, although this can cause localized extinction where severe, it has probably been vital in maintaining open conditions on sites with intermittent or low levels of stock grazing. It has also survived a variety of cutting treatments ranging from cutting once a year in spring, summer or autumn, to three times a year as well as annual burning (‘swaling’) in February or March to reduce the dominance of coarse grasses such as Bromopsis erectus and Brachypodium pinnatum. On some sites it has also benefited from occasionally burning and trampling by humans which appears to stimulate the development of the deep-seated adventitious root buds.

On some sites where over-grazing, mainly by rabbits, is perceived to be a problem fencing exclosures have been erected although this appears to have been detrimental due to the build-up of coarse grasses.

Given the poor dispersal ability of Pulsatilla vulgaris and the high degree of isolation of many populations the movement of livestock and cutting machinery between extant and potentially suitable sites is likely to be critical in promoting gene-flow and in enabling colonization to take place.

7 Threats/factors leading to loss or decline or limiting recovery

In England Pulsatilla vulgaris has undergone a rapid and dramatic range contraction over recent millennia and its current distribution now represents just 27% and 14% of its former range at the 10-km and site-population scales respectively. A similar magnitude of decline has been reported for Pulsatilla vulgaris in central Germany (Hensen et al., 2005), Austria (Franz, 2005), Switzerland (Pfeifer et al., 2002) and Luxembourg (Colling, 2005) and for Pulsatilla patens in Finland where 60% of populations have been lost since the 1930s (Uotila, 1996;

26 Kalliovirta et al., 2006). There are also striking similarities with the decline of Orchis ustulata in England (Foley, 1992), which might be expected given that the two species formerly grew together on a number of sites (and still do at one site in Bedfordshire).

In England historical records show that Pulsatilla vulgaris has been declining since at least 1750 (Fig. 4; Table 8). The majority of the losses before 1900 (64%) were due to ploughing-up of common lands following Parliamentary Enclosure awards, mainly between 1750 and 1850 (Wells, 1968; Jones, 1969; Wells, 1969). These earliest losses were described most vividly by the Cambridgeshire botanist Charles Babington (1860), who noted that “Until recently (within 60 years) most of the chalk district was open and covered with a beautiful coating of turf, profusely decorated with Anemone Pulsatilla [Pulsatilla vulgaris], Astragalus Hypoglottis [Astragalus danicus], and other interesting plants. It is now converted into arable land, and its peculiar plants mostly confined to small waste spots by road-sides, pits, and the very few banks which are too steep for the plough.” Although this probably over-states its former abundance, it was certainly occurring in other parts of southern England (e.g. Druce, 1886, p.xxxii) due to increased demand for home-grown corn fuelled by a rapidly increasing urban population. During the same period many populations were also lost to quarrying and mining activities on coal fields in the Midlands and northern England (Table 8).

Table 8 – Reasons for the loss of Pulsatilla vulgaris populations in England between 1750 and 2000. % loss figures are based only on localities where the cause of loss is known and therefore exclude ‘Unknown’ and ‘Possible error/duplicate record’. 1750- 1801- 1851- 1901- 1951- Total Reason for loss 1800 1850 1900 1950 2000 (%) Ploughing 2 8 10 7 1 28 (42) Lack of grazing/scrub encroachment 1 1 1 14 17 (25) Quarrying/mining/mineral extraction 3 1 3 7 (10) Improvement/overgrazing 7 7 (10) Building/urban development 2 1 1 1 5 (7) Afforestation 1 1 2 (3) Landscaping of parkland 1 1 (1.5) Unknown 1 1 14 13 7 36 Possible error/duplicate record 2 3 5 Total 9 12 31 26 30 108 Rate of loss per decade 1.8 2.4 6.2 5.2 6.0 4.3

27

Figure 12 – Sites where Pulsatilla vulgaris is now extinct (all photos taken 2003-2006; year of last record indicated): (a) Fleam Dyke, Cambridgeshire (1973); (b) Shacklewell Hollow, Leicestershire (1992); (c) Hildersham Furze Hills, eastern (Sand) hill, Cambridgeshire (1990); (d) Honnington Camp, Lincolnshire (1992); (e) Pitstone Hill, Buckinghamshire (1996); (f) Southorpe Roughs, Northamptonshire (1990).

28 Losses to ploughing and quarrying continued into the twentieth century and by the 1960s only 29 populations remained (Wells & Barling, 1971). Losses since then have mainly been caused by increased above-ground competition, particularly with Bromopsis erectus, as a result of under-grazing (Walker et al., in press). Ironically this was first observed in grazing exclosures that were erected to protect populations from over-grazing (e.g. Carter, 1967; Wells, 1971). Of the 20 sites where Pulsatilla vulgaris has either declined or gone extinct since the 1960s, 16 have been ungrazed for over 40 years or have only received intermittent grazing, mowing or burning (Table 9). These include small areas of grassland on earthworks or steep banks that are now completely isolated within arable landscapes and are now partly or completely scrubbed-over (e.g. Fleam Dyke, Fig. 12a; Honnington Camp, Fig. 12d), small exclosures erected to exclude livestock, deer and rabbits on over-grazed sites (e.g. Aston Upthorpe Down, Fig. 13a) and privately managed nature reserves where resources for management have been limited (e.g. Ancaster Valley, Fig. 13).

This decline of grazing frequency and intensity on many sites has been due to the reduced profitability of livestock farming in arable areas since the 1950s which has made it difficult to sustain appropriate grazing management on unproductive sites (Nisbet & Shere, 2006). On mixed farms the conversion of grassland to arable has made farmers less committed to grazing small areas, whereas their inaccessibility has deterred potential graziers because of increased transport and infrastructure costs. Even on livestock farms these problems have prevented the grazing of small fragments of semi-natural grasslands perceived to be unproductive and/or difficult to manage. In addition, there has been a decline in rabbit grazing since the spread of myxomatosis in 1953 which is known to have caused dramatic successional changes, especially on sites with no history of livestock grazing (Sumpton & Flowerdew, 1985).

Table 9 - Management of Pulsatilla vulgaris populations in relation to trends in abundance, 1968-2006. 1-5 represent a decline in the intensity of grazing management. Extant Extinc Management since 1968 Increas Total Stable Decline t e 1. Winter + some spring/summer/autumn grazing 3 2 - - 5 2. Winter grazing (since 1980) 2 1 - - 3 3. Irregular grazing, mowing, burning - 4 2 2 8 4. Over-grazed then under-grazed - - 2 3 5 5. Ungrazed for over 40 years - - - 7 7 6. Improved/destroyed - - - 4 4 7. Unknown - 1 - - 1

Over the last 40 years many grassland sites have also been agriculturally improved and reseeded to increase productivity. Other threats have included the digging-up of plants for horticulture including over 1000 from Knocking Hoe in 1948 (Hope-Simpson, 1948) and more recently at Barton Hills (M. Gurney, pers. comm.). In addition, the last known plants were dug-up at two former sites (Broughton Far Wood, Fleam Dyke; Marren, 1999) although other factors were more important in causing declines. Other direct threats, including forestry, building developments, etc. have only caused a few losses, including the dumping of rubble on the last Leicestershire colony. More recently there has also been concern, but no direct evidence, that atmospheric nitrogen deposition may be adversely affecting some populations through eutrophication of infertile grassland (Crawley, 2005; Rich et al., 1993).

29 The current range of Pulsatilla vulgaris in England is characterised by a high level of fragmentation, since numbers and size of populations have declined considerably over the past 40 years. During this time the average distance between neighbouring populations has increasing from 8 km to 22 km. Most significantly eight populations are now separated by more than 10 km, five by more than 35 km and the most isolated site, Ledsham in Yorkshire, by 102 km. Consequently, gene-flow between populations is likely to be very low or none existent making populations vulnerable to genetic drift and inbreeding depression, and therefore local extinction due to genetic, demographic or environmental problems (Schaffer, 1987; Lande, 1988). In these circumstances a decrease in genetic diversity is to be expected (Soulé, 1986) accompanied by a reduction in reproductive performance as shown for Pulsatilla vulgaris in central Germany, as well as a number of other European grassland species that have suffered similar declines (e.g. Oostermiejer et al., 1995; Ouburg & van Treuren, 1995; Vergeer et al., 2003). The results from the German study suggests that due to life-history characters Pulsatilla vulgaris may have maintained higher levels of genetic variation than would be expected for a declining species, although small populations are likely to display lower levels of genetic variation than larger ones, even where gene exchange is occurring between sites in close proximity. As the distance between half of English populations is well beyond the foraging radius of most pollinators (>10 km) we would expect to see a significant differentiation between isolated or outlying populations, both in terms of genetic variation and reproductive performance. Further work is needed to test these hypotheses.

7 Current Conservation Measures

7.1 In Situ Measures Pulsatilla vulgaris is currently classed by as Vulnerable using IUCN criteria but is not currently included in Schedule 8 of the Wildlife and Countryside Act, 1981 (Cheffings & Farrell, 2005). It was also included as a priority Biodiversity Action Plan species in 2007 (NERC Act 2006) and is listed as one of 47 priority Crop Wild Relatives in the UK for which action plans have been produced (Maxted et al., 2007).

With the exception of Taylor’s Hill, Gloucestershire, all extant populations of Pulsatilla vulgaris occur on SSSIs or NNRs (Table 10). Seven sites appear to be in favourable condition from the perspective of Pulsatilla vulgaris (but not necessarily for other designated site features), with some form of grazing management to maintain calcareous grassland features of interest including Pulsatilla vulgaris. Populations have therefore increased in size or remained stable over the past 40 years. Seven sites appear to be in poor condition or are recovering from poor condition due to the introduction of management. These include sites that were under-grazed for a long period and have recently been cleared of scrub and grazing re-introduced. The most dramatic example is Ancaster Valley, South Lincolnshire (Fig. 13). By 1981 dense Ulex europaeus scrub had eradicated most of the Pulsatilla vulgaris population (as well as Carex ericetorum) and only a few plants remained. Since then the scrub has been completely removed and the condition of the grassland improved through winter sheep- grazing. A similar project to stock-proof and reintroduce grazing to the Devil’s Dyke in Cambridgeshire is also benefiting Pulsatilla vulgaris largely through the reduced dominance of Bromopsis erectus (Fig. 14d). The recent re-introduction of grazing is also having positive results at Rodborough Common (cattle) and Deacon Hill, where a ‘flying flock’ of Hebridean sheep are used to graze a number of Pulsatilla vulgaris sites managed by the Wildlife Trust.

Table 10 - Extant populations of Pulsatilla vulgaris in England. Site Cons Condition

30 .

(a) Sites in good condition, grazing regime ideal Barnack Hills and NNR Good condition, population temporary fenced to reduce Holes disturbance Barnsley Wold SSSI Good condition Warren Barton Hills NNR Good condition, flowering poor in some years due to over- grazing Bourton Down SSSI Good condition, seedlings present Hornsleasow SSSI Good condition, some parts under-grazed Roughs Knocking Hoe NNR Good condition, severe rabbit disturbance in some years Therfield Heath SSSI Good condition, some parts under-grazed

(b) Sites in poor condition or recovering from poor condition Ancaster Valley SSSI Scrub clearance and grazing reintroduced Deacon Hill SSSI Under-/over-grazed in the past; severe rabbit disturbance Devil's Dyke SSSI Under-grazed but grazing introduced to some areas Beaumonts Hay SSSI Grazing irregular Taylor’s Hill - Grazing irregular Rodborough SSSI Under-grazed Common Swinstead Valley SSSI Under-grazed, encroachment by Brachypodium pinnatum

(c) Sites in poor condition, plant likely to go extinct Aston Upthorpe SSSI Most plants in ungrazed exclosure; rest of site overgrazed Down Ledsham SSSI Only a single plant; likely to go extinct Ravensburgh Castle SSSI Ungrazed; likely to go extinct Steps Hill SSSI Undergrazed, threatened by scrub encroachment

As noted above, exclosures have been erected at a few sites to protect populations from over- grazing (e.g. Aston Upthorpe, Knocking Hoe, Pitstone Hill) but in general these had lead to declines due to increased growth of Bromopsis erectus. At Aston Upthorpe annual mowing has been introduced to counter this and maintain sward heights at the appropriate height (Fig. 14a). At Therfield Heath temporary fencing is used to rotationally graze common land and to ensure that areas containing Pulsatilla vulgaris are grazed appropriately. At Barnack Hills and Holes single strand fencing is used to reduce disturbance by visitors during the flowering period (Fig. 14b). At the most recently discovered site, Swinstead Valley, a temporary grazing exclosure erected during the flowering period led to an increase from 4 flowers in 2009 to 18 in 2010.

31 1981 1992

1999 2006

Figure 13 – The restoration of Pulsatilla vulgaris habitat at Ancaster Valley, South Lincolnshire. The extant population is located on the left hand slope covered in Ulex europaeus in 1981. The scrub was cleared in the 1980s and winter-grazing reintroduced.

Table 11 – Details of translocations of Pulsatilla vulgaris in England. Site No. % Year(s) of Source surviv Details of translocation attempt of intro plan of seed al ts Aston Upthorpe, 1999 87 56 Aston Augmentation of existing colony. Berkshire (2009) Upthorp Plants protected within exclosure e but few flower due to predation by rabbits or voles. Hartslock, 1998 78 80 Barnack Experimental introduction to Oxfordshire (2008) investigate translocation techniques (Warden, 2001). Southorpe 1999 12 0 Barnack Re-introduction to a former site. Paddock, Plants failed to survive more than 2 Northamptonshir years. e Ancaster, South 1992- 68 32 Ancaster Augmentation of existing colony. Lincolnshire 2002 (2005) Plants protected by wire cages during the flowering period. Copper Hill 1994- 68 0 Ancaster Re-introduction to a former site.

32 Quarry, Ancaster 1996 Most scratched out by rabbits and pheasants within a few days of planting. Four plants survived for two years. Ledsham, Mid- 2000 1 0 Barnack A single plant was introduced to west Yorkshire encourage cross-pollination of the sole remaining plant in northern England. This died within a couple of years. In England attempts to re-introduce Pulsatilla vulgaris to former sites or augment existing populations have been carried out at six sites with variable success (Table 11). Transplants have survived at Aston Upthorpe, Ancaster and Hartslock plants within protective exclosures where the surrounding vegetation has been removed to reduce competition (Fig. 14c) and the surrounding vegetation has been mown or grazed. However, at both Aston Upthorpe and Hartslock very few plants manage to set seed due to predation by rabbits or voles (Warden, 2009). All other attempts have been failures with plants only surviving for one or two years. This included an attempt to translocate a single plant to within 4 metres of the sole surviving plant in northern England (at Ledsham) to encourage cross-pollination (A. Headley, pers. comm.). Similar high rates of translocation failures have been reported for Switzerland (Pfeifer et al., 2002).

Figure 14 – Examples of in situ conservation work for Pulsatilla vulgaris in England: (a) fencing to exclude livestock, Aston Upthorpe Down, Berkshire; (b) temporary fencing to

33 reduce trampling by visitors, Barnack Hills & Holes, Northamptonshire; (c) cages to protect transplants from rabbits (note clearance of vegetation from around the plant), Ancaster Valley, South Lincolnshire; and (d) effects of the reintroduction of grazing to the Devil’s Dyke, Cambridgeshire, following the erection of stock-proof fencing.

7.2 Ex situ Measures Plants of wild origin are known to be cultivated in the Oxford Botanic Garden and Kew’s garden at Wakehurst Place. Plants originating from Barnack Hills and Holes were also grown by Terry Wells at Monks Wood Experimental station between 1970 and 1980 for the purposes of research, some of which were transferred to his garden in Upwood. Many plants originating from wild British populations are likely to be cultivated in other private gardens. A small amount of viable seed is currently stored in the Kew Millennium Seed Bank at Wakehurst Place (Royal Botanic Gardens Kew, 2008).

Pollen from the single Ledsham plant has been used to cross-pollinate five plants from Barnack Hills and Holes, with the intention of growing on plants for reintroduction to the wild site, but without success (A. Headley, pers. comm.).

7.3 Research Data Research is urgently required to assess genetic variation within English populations and the extent to which small population size, limited gene-flow (due to extreme population fragmentation), genetic drift and inbreeding depression are affecting the performance of English populations. Likewise studies that assess dispersal and pollination mechanisms, in particular the potential for dispersal via livestock and machinery, may provide valuable insights into gene-flow and how best to conserve Pulsatilla vulgaris in the future. Studies on the genetic relationships between British and continental populations would also be useful help to inform European conservation priorities.

Research on the regeneration niche of Pulsatilla vulgaris is needed in order to establish the optimum conditions under which field germination and seedling establishment takes place. Further work is also needed to assess factors controlling the abundance of Pulsatilla vulgaris, in particular the affects of the removal of competitive dominance in grassland swards e.g. responses to environmental perturbations and the removal of dominant species and leaf litter (Bailey, 1996).

Figure 15 – Fluctuations in the number of Pulsatilla vulgaris in fixed plots at Barnack Hills and Holes, Northamptonshire. Data supplied by Chris Gardner (Natural England).

34 7.4 Monitoring and the Common Monitoring Standard Traditionally Pulsatilla vulgaris has been monitored by simple counts of flowering ‘crowns’ or estimates based on densities in small areas (e.g. Tarpey, 1999). These provide an overall assessment of year to year variation but are limited for a number of reasons. First, ‘crowns’ do not represent discrete genets due to the production of offshoots close to parents. The total count is therefore likely to overestimate the total size of the population possibly by orders of magnitude. Second, grazing can have a marked influence on estimates especially on sites where livestock are present during the flowering period. Third, such counts do not take into account the life-stage structure of the population or whether recruitment is taking place through the production of seed, presence of juveniles, etc.

Possible alternative approaches include counts within fixed plots as has been carried out at Barnack Hills and Holes in Northamptonshire since 1975 (Fig. 15). This should preferably include a number of demographic parameters, including the individuals in different life- stages, flowering performance, seed production etc., and relate these environmental variables such as sward height, % cover of bare ground, ‘hits’ on dominant grasses, etc. Simple counts of rosettes rather than flower stems is probably a more preferable performance parameter given the dramatic fluctuations in the numbers of flowers observed on some sites (e.g. Fig. 15). These are less affected by seasonal factors and grazing and therefore provide a more accurate assessment of the size of populations (Bailey, 1996). However, all these approaches are likely to be time consuming to carry-out and therefore dependent on available expertise, time and resources.

8 References

Abbott, P.P. 2005. Plant Atlas of Mid-west Yorkshire. Yorkshire Naturalists’ Union. Aichele, D. & Schwegler, H.W. 1957. Die Taxonomie der Gattung Pulsatilla. Feddes Repertorium 60, 1-230. Akeroyd, J. 1993. Pulsatilla Miller, in T.G. Tutin, N.A. Burges, A.O. Chater, J.R. Edmondson, V.H. Heywood, D.M. Moore, D.H. Valentine, S.M. Walters, D.A. Webb (eds) Flora Europaea, Volume 1, Psilotaceae to Platanaceae, second edition. Cambridge University Press, Cambridge. Babbington, C.C. 1860. Flora of Cambridgeshire. J. van Voorst, London. Baker, J.G. 1906. North Yorkshire: Studies of its Botany, Geology, Climate and Physical Geography. Longmans, London. Bailey, C. 1996. An investigation into the factors influencing the distribution, relative abundance and genetic variation of Pulsatilla vulgaris at two sites in Bedfordshire. Unpublished MSc thesis, Imperial College, Wye. Böcher, T.W. 1934. Beiträge zur Zytologie der Gattung Anemone. Botanisk Tidsskrift 42, 183- 206. Bowen, H. 1968. The Flora of Berkshire. Holywell Press, Oxford. Bowen, H. 1997. Observations on Pulsatilla vulgaris. BSBI News 76, 37. Bowen, H. 2000. The Flora of Dorset. Pisces Publications, Newbury. Brewis, A., Bowman, P. & Rose, F. 1996. The Flora of Hampshire. Harley Books, Colchester. Campbell, B.D., Grime, J.P. & Mackey, J.M.L. 1992. Shoot thrust and its role in plant competition. Journal of Ecology 80, 633-641. Carter, H.H. 1967. Juniper Valley: some observations and problems. Reading Naturalist 19, 21-29.

35 Cheffings, C. & Farrell, L. et al. 2005. The Vascular Plant Red Data List for Great Britain. Species Status 7, 1-116. Joint Nature Conservation Committee, Peterborough. Colling, G. 2005. Red List of the Vascular Plants of Luxembourg. Ferrantia 42, 1-77. Compton, G. 2010 onwards. Cambridgeshire flora records since 1538. Part one (rare species). Accessed online: http://www.mnlg.com/gc/index2.html. Crawley, M.J. 2005. The Flora of Berkshire. Brambley Books, Harpenden. Druce, G.C. 1886. The flora of Oxfordshire. First edition. Parker and Co., Oxford and London. Edwards, B. & Pearman, D.A. 2004. Dorset Rare Plant Register. DERC, Dorchester. EUNIS, 2004. European Nature Information System. Species factsheet for Pulsatilla vulgaris Mill. http://eunis.eea.europa.eu/species/177065. Everett, S. 1988. Rare Vascular Plant Survey of Southern England. CSD Report Number 23, Nature Conservancy Council, Peterborough. Foley, M.J.Y. 1992. The current distribution and abundance of Orchis ustulata L. (Orchidaceae) in the British Isles - an updated summary. Watsonia 19, 121-126. Franz, E. 2005. Population development, habitat preference and causes of endangerment of the Pasque Flower (Pulsatilla vulgaris MILL.) in Austria between 1991 and 2005. Linzer Biologische Beitraege 37, 1145-1176. Gärdenfors, U. (ed.) 2010. The 2010 Red-list of Swedish Species. ArtDatabanken. Greves, S. 1997 A Species Action Plan for pasqueflower (Pulsatilla vulgaris) in Berkshire, Buckinghamshire and Oxfordshire. English Nature, Thatcham. Grose, D. 1957. The Flora of Wiltshire. The Natural History Section & Wiltshire Archaeological and Natural History Society, Devises. Grubb, P.J. 1990. Demographic studies on the perennials of chalk grassland, in S.H. Hillier, D.W.H. Walton, & D.A. Wells (eds.) Calcareous Grasslands – Ecology and Management. Proceedings of the Nature Conservancy Council and British Ecological Society Symposium, University of Sheffield, 14-16th September 1987. Bluntisham Books, Bluntisham, pp. 207-255. Hantula, J., Uotila, P., Saura, A. & Lokki, J. 1989. Chloroplast DNA variation in Anemone s. lato (Ranunculaceae). Plant Systematics and Evolution 163, 81-85. Hensen, I., Obeprieler, C. & Wesche, K. 2005. Genetic structure, population size, and seed production of Pulsatilla vulgaris Mill. (Ranunculaceae) in Central Germany. Flora 200, 3-14. Hill, M.O. & Preston, C.D. 2002. New Atlas genera in their natural orders. BSBI News 91, 18- 23. Hope Simpson, J. 1948. Management Plan: Knocking Hoe, Appendix IV. Nature Conservancy Council, Peterborough. Jalas, J. & Suominen, J. (eds) 1989. Atlas Florae Europaeae. Distribution of Vascular Plants in Europe. 8. Nymphaeaceae to Ranunculaceae. The Committee for Mapping the Flora of Europe & Societas Biologica Fennica Vanamo, Helsinki. Jarvis, C.E., Spencer, M.A. & Cafferty, S. 2005. Typification of Linnaean Plant Names in Ranunculaceae. Taxon 54, 467-471. Jefferson, R.G. & Walker, K.J. 2010. An over-looked population of Pulsatilla vulgaris Mill. In South Lincolnshire (v.c.53). Watsonia 28, 79-81. Jones, E.F. 1969. The decrease of Pulsatilla vulgaris in England. Biological Conservation 1, 327-328. Jonsell, B. (ed.) 2001. Flora Nordica. Volume 2. Chenopodiaceae to Fumariaceae. The Bergius Foundation, Stockholm. Jonsson, O., Rosquist, G. & Widén, B. 1991. Operation of dichogamy and herkogamy in five taxa of Pulsatilla. Holarctic Ecology 14, 260-271.

36 Kalliovirta, M., Ryttäri, T. & Heikkinen, R.K. 2006. Population structure of a threatened plant, Pulsatilla patens, in boreal forests: modeling relationships to overgrowth and site closure. Biodiversity & Conservation 15, 3095-3108. Kratochwil, A. 1988. Zur Bestäubungsstrategie von Pulsatilla vulgaris Mill. Flora 181, 261-324. [The flowering phenology of Pulsatilla vulgaris] Lande, R. 1988 Genetics and demography in biological conservation. Science 241, 1455-1460. Leslie, A. 2004. Vascular plant records. Nature in Cambridgeshire 46, 89. Lindell, T. 1998. Breeding systems and crossing experiments in Anemone patens and in the Anemone pulsatilla Group (Ranunculaceae). Nordic Journal of Botany 18, 549-561. Linnaeus, C. 1753. Species Plantarum. (Facsimile edition 1957, Ray Society, London). Marren, P. 1999. Britain’s Rare Flowers. T. & A.D. Poyser, London. Maxted, N., Scholten, M., Codd, R. & Ford-Lloyd, B. 2007. Creation and use of a national inventory of crop wild relatives. Biological Conservation 140, 142–159. Miller, P. 1768. The Gardeners Dictionary. John and Francis Rivington, London. Mitchley, J. 1988. Control of relative abundance of perennials in chalk grassland in southern England. II. Vertical canopy structure. Journal of Ecology 76, 341-350. Mitchley, J. & Willems, J.H. 1995. Vertical canopy structure of Dutch chalk grasslands in relation to their management. Vegetatio 117, 17-27. Moser, D.M., Gygax, A., Bäumler, B., Wyler, N. & Palese, R. 2002. Rote Liste der gefährdeten Arten der Schweiz. Farn- und Blütenpflanzen. Swiss Agency for the Environment, Forests and Landscape (SAEFL), Berne, and Centre du Réseau Suisse de Floristique (CRSF), Chambésy. Nisbett, A. & Shere, P. 2006. The Environmental Impacts of Changes in Livestock Farming in England. Rural Development Service (Defra), Exeter. Olivier, L., Galland , J.P. & Maurin , H. (eds) 1995. Red Book of threatened flora of France. Volume I: Species priority. Natural Heritage Collection (Series Genetic Heritage). No. 20. SPN-IEGB/MNHN, DNP/Environment Department, CBN Porquerolles, Paris. Oostermeijer, J.G.B., van Eijick, M.W., van Leeuwen, N.C. & den Nijs, H.C.M. 1995. Analysis of the relationship between allozyme heterozygosity and fitness in the rare Gentiana pneumonanthe L. Conservation Biology 12, 1042-1053. Osborne, J.L., Martin, A.P., Carreck, N.L., Swain, J.L., Knight, M.E., Goulson, D., Hale, R.J. & Sanderson, R.A. 2008. Bumblebee flight distances in relation to the forage landscape. Journal of Animal Ecology 77, 406–415. Ouberg, N.J. & van Treuren, R. 1995. Variation in fitness-related characters among small and large populations of Salvia pratensis. Journal of Ecology 83, 369-380. Pfeifer, E., Holderegger, R., Matthies, D. & Rutishauser, R. 2002. Investigation on the population biology of a flagship species of dry meadows: Pulsatilla vulgaris Mill. in north-eastern Switzerland. Botanica Helvetica 112, 153-171. Plants for a Future (accessed 2010) Plants for a Future database: Pulsatilla vulgaris Mill. (http://www.pfaf.org/database/plants.php?Pulsatilla+vulgaris). Pigott, C. D. & Walters, S.M. 1954. On the interpretation of the discontinuous distributions shown by certain British species of open habitats. Journal of Ecology 42, 95-116. Preston C.D. & Hill M.O. 1997. The geographical relationships of British and Irish plants. Botanical Journal of the Linnean Society 124, 1-120. Preston, C.D., Pearman, D.A. & Dines, T. 2002. New Atlas of the British and Irish flora. Oxford University Press, Oxford. Rassi, P., Alanen, A., Kanerva, T. & Mannerkoski, I. (eds) 2001. The Red List of Finnish Species. Ministry of the Environment & Finnish Environment Institute, Helsinki.

37 Rich, T.C.G. 1997. The Management of Semi-natural Lowland Grassland for Selected Rare and Scarce Vascular Plants. English Nature Research Report No. 216. English Nature, Peterborough. Rich, T.C.G., Cooper, E.A., Rodwell, J.S. & Malloch, A.J.C. 1993. Effects of Climate Change and Air Pollution on British Calcicolous Grasslands. Final report to UK Department of the Environment. Röder, D. & Kiehl, K. 2006. Population structure and population dynamic of Pulsatilla patens (L.) Mill. in relation to vegetation characteristics. Flora 201, 499-507. Rodwell, J. 1992. National Vegetation Classification. Volume 2. Grassland and montane communities. Cambridge University Press, Cambridge. Rodwell, J., Morgan, V., Jefferson, R.G. & Moss, D. 2007 The European Context of Lowland Grasslands. JNCC Report, No. 394. Rose, F. 1957. The importance of the study of disjunct distribution to progress in understanding the British flora, in J.E. Lousley (ed.) Progress in the Study of the British Flora. Botanical Society of the British Isles, London, pp. 61-78. Ross-Craig, S. 1948. Drawings of British Plants. Part I. Ranunculaceae. G. Bell & sons Ltd., London. Royal Botanic Gardens Kew. 2008. Seed Information Database (SID). Version 7.1. Available from: http://data.kew.org/sid/ (May 2008) Schaffer, M.L. 1987. Minimum viable populations: coping with uncertainty, in M.E. Soulé (ed.) Viable Populations for Conservation. Cambridge University Press, Cambridge, pp.69- 86. Smith, J. 1996, In search of the Pasque Flower. Bulletin: The Alpine Gardener 64, 380-381. Soulé ME 1986 Viable Populations for Conservation. Cambridge University Press, Cambridge. Steffan-Dewenter, I. & Kuhn, A. 2003 Honeybee foraging in differentially structured landscapes. Proceedings of the Royal Society of London Series B-Biological Sciences 270, 569–575. Sumpton, K.J. & Flowerdew, J.R. 1985. The ecological effects of the decline in Rabbits (Orctolagus cuniculus L.) due to myxomatosis. Mammal Review 15, 151-186. Tackenberg, O. 2001. Methoden zur Bewertung Gradueller Unterschiede des Ausbreitungspotentials von Pflanenarten. [Methods for evaluation of degree differences in the propagation potential of plant species]. Dissertationes Botanicae 347. J. Cramer, Berlin, Stuttgart. Tackenberg, O., Poschlod, P. & Bonn, S. 2003. Assessment of wind dispersal potential in plant species. Ecological Monographs 73, 191-205. Tarpey, T. 1999. Pasqueflower Count: Church Hill. Unpublished survey report to the Conservators of Therfield Heaths and Greens. Thompson, K., Bakker, J. & Bekker, R. 1997. The Soil Seed Banks of North West Europe: Methodology, Density and Longevity. Cambridge University Press, Cambridge. Trist, P.J.O. 1988. Hildersham Furze Hills. Nature in Cambridgeshire 30, 4-12. Uotila, P. 1996. Decline of Anemone patens (Ranunculaceae) in Finland. Symbolae Botanicae Upsalienses 31, 205-210. Vergeer, P., Rengelink, R., Copal, A. & Ouburg, N.J. 2003. The interacting effects of genetic variation, habitat quality and population size on performance of Succisa pratensis. Journal of Ecology 91, 18-26. Walker, K.J., Wells, T.C.E. & Pinches, C.E. In press. Reduced grazing and the decline of the threatened grassland herb Pulsatilla vulgaris Mill. (Ranunculaceae) in England, UK. Biological Conservation.

38 Warden, K. 2001. An investigation into techniques for the propagation and augmentation of a wild population of pasqueflower, Pulsatilla vulgaris, Miller, including observations on the reproductive biology of the species. Unpublished MSc thesis, University of Reading. Warden, K. 2009. Pulsatilla vulgaris. Ashmolean Natural History Society of Oxfordshire Rare Plants Group 2009 Newsletter, 7. Wells, T.C.E. 1968. Land use changes affecting Pulsatilla vulgaris in England. Biological Conservation 1, 37-44. Wells, T.C.E. 1969. The decrease of Pulsatilla vulgaris in England – A reply to Dr. E.F. Jones. Biological Conservation 1, 328-329. Wells, T.C.E. 1971. A comparison of the effects of sheep grazing and mechanical cutting on the structure and botanical composition of chalk grassland, in E. Duffey & A.S. Watt (eds) The Scientific Management of Animal and Plant Communities for Conservation. Blackwell Scientific Publications, Oxford, pp. 497-515. Wells, T.C.E. 1994. Pulsatilla vulgaris Miller, in A. Stewart, D.A. Pearman & C.D. Preston (eds) Scarce Plants in Britain. Joint Nature Conservation Committee, Peterborough, pp.344- 346. Wells, T.C.E. 2003. A Flora of Huntingdonshire and the Soke of Peterborough. Privately published, Huntingdon. Wells, T.C.E. & Barling, D.M. 1971. Biological Flora of the British Isles no. 44. Pulsatilla vulgaris Mill. (Anemone pulsatilla L.). Journal of Ecology 59, 275-292. Welsh, J. 1983. Survey of Pulsatilla vulgaris populations in Bedfordshire. Unpublished MS held by the author. Widén, B. & Lindell, T. 1996. Flowering and fruiting phenology in two perennial herbs, Anemone pulsatilla and A. pratensis (Ranunculaceae). Symbolae Botanicae Upsaliensis 31, 145-158. Wójtowicz, W. 2001. Pulsatilla vulgaris Mill. Sasanka zwyczajana. In: Kazmeirczakowa, R. & Zarzycki, K. (eds), Polska czerwona ksiega roslin. Polska Akademia Nauk, Krakow, pp.138-139.

39 9 Contacts

Botanical Society of the British Isles 97 Dragon Parade Harrogate Kevin Walker - [email protected] North Yorkshire HG1 5DG. Plantlife International The Wild Plant Conservation Charity 14 Rollestone Street Salisbury Tim Wilkins - [email protected] Wiltshire SP1 1DX. Tel: 01722 342730

10 Links

ƒ BSBI Maps Scheme: http://www.bsbimaps.org.uk/atlas/main.php

ƒ Records via NBN Gateway: http://www.nbn.org.uk

ƒ Global Biodiversity Information Facility: http://www.gbif.org

ƒ Pasqueflower is a Species of Principal Importance in England (S41 of NERC Act 2006): http://www.ukbap.org.uk/NewPriorityList.aspx

ƒ The UK list of threatened (red listed) vascular plants is maintained by JNCC: http://jncc.defra.gov.uk/page-3354

40 11 Annex 1 – site descriptions

Descriptions of the 34 English population of Pulsatilla vulgaris thought to be extant in the 1960s including 29 included in Wells & Barling (1971) and five discovered subsequently. With the exception of Swinstead Valley (discovered in 2009) all have been resurveyed by Walker et al. (in press) since 2000. Sites are listed in vice-county and then alphabetical order. Conservation designations are given in parentheses. † Denotes where Pulsatilla vulgaris is thought to be extinct.

HERTFORDSHIRE (v.c.20)

Aldbury Nowers (SSSI)† During the 1960s a few plants were recorded in rank Bromopsis erectus grassland (CG3b) and scrub overlying chalk adjacent to an Iron Age camp. The site was ungrazed for many years and consequently scrubbed over (recently cleared) except in a few places where small fragments of chalk grassland remain. Pulsatilla has not been seen at this site since 1969 despite repeated searches (Trevor James, pers comm.).

Therfield Heath (SSSI) The second largest British colony largely confined to very short, rabbit grazed turf on the steep south to southwest-facing slopes of a narrow chalk spur known locally as ‘Church Hill’ (TL332395). A few plants also occur in rank Bromopsis erectus grassland (CG3a) on the adjacent Pen Hill (TL332397) and to the east of the tumuli marked on the OS map (TL332399). All occur on common land in the ‘roughs’ of a golf course which were ungrazed for many years. Church Hill has a long history of heavy rabbit grazing and in the 1980s small areas were also mown in late February or early March using a tractor and ‘Flymo’. Since 1986 rotational winter grazing has been carried out across much of the site using temporary grazing compartments and, on Church Hill at least, this has led to an increase in overall population numbers, which now exceed 60,000 and up to 12 rosettes m-2 (Tarpey, 1999). Recreation pressures include trampling on the spine of Church Hill and the occasional removal of flowers or whole plants. The population near the tumuli may have originated from seed spread by a local farmer (W.H. Darling) in 1953/54.

BERKSHIRE (v.c.22)

Aston Upthorpe Down (SSSI) The sole relic of a once extensive population that stretched along the Berkshire Downs (Druce, 1886; Crawley, 2005). By the 1960s around 300 plants were confined to a northwest-facing chalk slope although flowering was limited due to heavy grazing by rabbits. As a consequence, a small exclosure was erected in 1961 with an inner fence to exclude rabbits (repaired 1976 and replaced in 1998). This resulted in a gradual decline in the numbers of Pulsatilla vulgaris due to increased competition from coarse grasses and the grazing off of inflorescences by wood mice (Carter, 1967). The population continued to decline into the 1970s and 1980s despite occasional mowing/burning to control the growth of Bromopsis erectus. Mowing was re-introduced in 1996 and this led to an increase in flowering performance although by this time only around 13 plants remained (Warden, 2001). Only a few plants have been recorded outside this exclosure since 1994 due to very heavy rabbit grazing. Eighty-seven plants grown from Aston Upthorpe seed were planted inside the new exclosure in October 1999 (Warden, 2001); 55 (63%) were still present in 2004 (Kathy Warden, pers. comm.).

41 Lockinge† In 1962 two plants were discovered in rough grassland above Lockinge. It has apparently been seen again since 1987 (Crawley, 2005) but no plants or suitable habitat could be located by the author in 2005 (SU427846).

Unhill Bottom† This site was the remnant of an extensive population, possibly totalling over 55,000 plants, which spread over much of the adjacent chalk downland of Dean’s Bottom (Crawley, 2005). Much of this area was used for military training during the 1939-45 war and was subsequently ploughed-up. The population had declined to around 5000 plants by the late 1950s (Bowen, 1968) and then to around 750 plants by 1967 when Pulsatilla was confined to a small area of ungrazed Festuca rubra grassland (CG6) on a NNW-facing slope. It apparently survived in this locality till at least 1978 but eventually disappeared when the grassland was improved and intensive sheep grazing was introduced (Warden, 2001).

BUCKINGHAMSHIRE (v.c.24)

Clipper Down (SSSI)† In the 1960s a few plants were recorded on a steep SSW-facing chalk slope which was being heavily grazed by sheep from November until April. The intensity of grazing was increased during the 1970s and 1980s (excluding November to March) leading to deterioration in the condition of the site (Everett, 1988). The population was fenced (c.1986) for a number of years until grazing levels were reduced on the surrounding slope. The last reliable record was in 1976 although there are unconfirmed records of flowering in 1986 and more recently as vegetative plants (Greves, 1997). No plants have been found in recent years despite repeated searches during the flowering period (L. Trowbridge, pers., comm.). This site currently falls within the Ivinghoe Hills SSSI complex and is managed favourably by a tenant farmer for the National Trust.

Pitstone Hill (SSSI)† In the 1960s a few plants occurred on the steep S-facing slope of a mediaeval ditch in relatively short Bromopsis erectus grassland. It persisted in tightly-grazed grassland although plants were very difficult to locate in the mid-1980s due to heavy grazing pressure. An exclosure was erected around the site in 1986 and this has led to the build up of coarse grasses and scrub. The last record was at the top of the S-facing bank in 1996; it has not been recorded since despite repeated searches.

Steps Hill (SSSI) In the 1960s over 100 plants were recorded in short, Festuca ovina turf on a steep SW-facing spur of chalk downland above Incombe Hole. The site was formerly very heavily grazed by sheep and cattle leading to localised poaching and the removal of most of the flowerheads during the spring (R. Maycock, pers. comm.). Grazing levels were subsequently reduced and this led to a gradual increase in Bromopsis erectus (CG3). Sheep now lightly graze the site from autumn to early spring (Greves, 1997) and as a result vegetation remains fairly rank (>15 cm). In 2005 there approximately 50 plants were located in a limited area (20 × 15-m) surrounded by hawthorn scrub and many freely regenerating whitebeams.

CAMBRIDGESHIRE (v.c.29)

Devil’s Dyke (SSSI)

42 Historically Pulsatilla has been recorded sporadically along 7 km of an Anglo-Saxon chalk ditch and bank between Burwell and where the Cambridge-Newmarket railway crosses the dyke to the SE. The majority of plants are confined to the SW-facing banks particularly where the grassland has been kept open by rabbits, infrequent mowing or burning. A few plants also occur on the top of the dyke, where grass growth is reduced by trampling, and on the adjacent Newmarket Heath which is cut fortnightly, although no plants have been recorded from the heath since 1984. The dyke itself was not grazed for many decades leading to the development of a thick sward of Bromopsis erectus. Accidental burning of one section in the 1970s led to a dramatic increase in flowering numbers although numbers subsequently declined to pre-1970 levels. Since then localised mowing has led to localised increases on some sections (e.g. adjacent to Newmarket Heath) and in 2003 the introduction of winter- sheep grazing (and stock-fencing) led to increased flowering on the southern section. In the same year four plants appeared (with Himantoglossum hircinum) on the steep SE-facing bank of the A14 c. 300m to the N of the nearest plants on the Dyke itself (TL603632; Leslie, 2004). These presumably established from seed dispersed to the site on mowing machinery.

Fleam Dyke (SSSI)† In the 1960s a small population was recorded on an ungrazed SW-facing bank of a mediaeval chalk ditch and bank immediately to the NW of a small tumulus. It was last seen in April 1973 when the plants were dug-up by the farmer in order to reduce the number of botanists visiting the site (Marren, 1999).

Hildersham Furze Hills (SSSI)† A small population formerly grew (with Dianthus deltoides) on the spine of the easterly (Sand) hill on a sandy soil (pH 5.2) derived from glacial sands and gravels (Wells & Barling, 1971). During the 1950s there were never more than 3-4 clumps with 20-30 flowers (Trist, 1988). Annual rabbit damage was intense, especially during droughts, although this declined following the advent of myxomatosis in 1954. Three plants survived on the spine of the hill into the mid-1980s despite the spread of rank grasses and blackthorn scrub (Trist, 1988). By 1990 only one, non-flowering plant remained and it has not been recorded since despite improvements in the condition of the grassland and the removal of scrub (Compton, 2010 onwards).

BEDFORDSHIRE (v.c.30)

Barton Hills (NNR) Several large sub-populations occur towards the S end of this reserve in exceptionally rich chalk downland turf on steep, predominantly S- to SW-facing slopes and spurs where soils are very shallow and competition from coarse grasses is restricted (Wells, 1968; Welsh, 1983). A few plants also occur on ancient field systems at the N end of the reserve where grazing is more variable. Historically the site was heavily grazed by sheep but management was neglected from 1934 to 1954 resulting in the development of a dense sward of Bromopsis erectus (Wells, 1968). This was burnt-off in 1954 and sheep grazing re-introduced for nine months of the year (2-3 ac-1), although rabbit grazing declined dramatically due to myxomatosis. Since the mid-1980s the site has been grazed by rabbits all year (although populations have increased in recent years) and sheep (0.4 ha-1) from May to December (inclusive) although this has been relaxed in recent years due to a rise in the rabbit population (Bailey, 1996). This has resulted in an increase in the flowering population to over 5,000 crowns although flowering is suppressed in some years by heavy grazing (G. Bellamy, pers. comm.). The Barton population of Pulsatilla is well known and attracts many visitors during

43 the flowering period. In the past many flowers were traditionally gathered at Easter, although this activity it is much less common today. However, in 2006 around 70 plants were illegally removed (M. Gurney, pers. comm.).

Deacon Hill (SSSI) Since 1960 small numbers of Pulsatilla have been recorded sporadically from several localities in the vicinity of Deacon Hill on steep, SW to NW-facing chalk downland slopes and spurs: (1) the NE slope of Barn Hole (TL119294); (2) narrow spur adjacent to Pegsdon Firs (TL121297); (3) combe NE of Pegsdon Firs (TL123296); and (4) the celtic field system below Deacon Hill itself (TL12SP98). Historically the northern half of the site (Deacon Hill) has been heavily grazed by sheep and rabbits. In contrast, grazing has been much lower in the southern half of the reserve leading to a decline as a result of scrub encroachment and build-up of coarse grasses from the 1950s onwards. In recent years, scrub clearance and the reintroduction of grazing have led to an improvement in the quality of the grassland although no plants have been found in Barn Hole despite repeated searches.

Knocking Hoe (NNR) Between 500-1000 plants grow on the SW-facing slope of a small chalk hill (‘the Hoe’; TL130139) in exceptionally rich calcareous turf with a number of other national rarities (Hypochaeris maculata, Orchis ustulata, Seseli libanotis and Tephroseris integrifolia). A few plants also occur on a Celtic field system (within a grazing exclosure) just to the east (‘Spiranthes bank’; TL131308), and more sporadically within an abandoned exclosure on a steep S-facing slope to the W of Tingley Wood (TL132306). It was lost from other parts of the reserve that were ploughed for a short period in 1956 but it has not re-colonised this area. The site was sheep grazed throughout the nineteenth century although this declined after 1931 and since then it has had periods of heavy and light grazing by sheep, rabbits and cattle with occasional mowing and raking of cut material to maintain a tight sward. Few plants were recorded during the 1970s due to the decline in the rabbit population and the growth of coarse grasses (Bromopsis erectus). However, the population increased dramatically following the introduction of mowing and the recovery of the rabbit population in the 1980s although these caused severe localised erosion in places (e.g. Spiranthes Bank) (Bailey, 1996). The Hoe itself is currently heavily-grazed by rabbits with additional winter sheep grazing and management is now considered to be ideal with over 1000 flowers counted in 2005 (G. Stevens, pers. comm.). In contrast, numbers within the two less heavily grazed exclosures remain low due to greater competition with coarse grasses. The site receives few visitors but there are reports of over 1000 plants being dug-up in the past (Hope-Simpson, 1948).

Ravensburgh Castle (SSSI) In the 1960s two sub-populations were recorded from adjacent chalk slopes of an Iron Age hill fort dating back to 400BC. The smaller of the two populations occurred immediately below the fort on a steep W-facing slope (TL098295); the larger colony extended eastwards from a S- facing spur overlooking the first site (TL097296). Over 300, mainly vegetative plants were recorded on this slope in 1981 and 30 below the hill fort (Welsh, 1983). In 1964 the grassland was very rank but by 1980 the vegetation was very short with much bare chalk due to heavy grazing by sheep and rabbits. It has not been grazed since and is now dense Bromopsis erectus grassland with scattered hawthorn scrub. As a consequence, no plants have been seen on the W-facing slope for many years and only a few plants survive on the S-facing spur where the grassland is more exposed and the soils are very shallow.

Smithcombe Hill (SSSI)†

44 In the 1960s a small population occurred in rank Bromopsis erectus grassland (CG3a) surrounded by scattered Viburnum lantana scrub on a steep SSE-facing chalk slope. By the 1980s the scrub had become very dense and only a single vegetative rosette could be found (Welsh, 1983). It has not been recorded since despite scrub clearance and the introduction of goat grazing.

NORTHAMPTONSHIRE (v.c.32)

Barnack Hills and Holes (NNR) Many thousands of plants (>20,000) occur over a large area of mediaeval limestone quarry workings where they are confined to shallow soils on S and SW-facing slopes. Grazing ceased in 1914 and by the 1960s the grassland was very rank Bromopsis erectus-Brachypodium pinnatum grassland with a dense layer of leaf litter. Sheep grazing (September to late- December) was re-introduced in 1978 resulting in a dramatic increase in flowering. Monitoring in fixed plots showed an increase from 260 in 1978 to 4,727 crowns by 2005. The entire population is now estimated to exceed 20,000 crowns (C. Gardiner, pers. comm.). The management is now considered ideal (Rich, 1997) and as a result P. vulgaris has spread to new areas of the reserve where it may have established from seed (C. Gardiner, pers comm.).

Southorpe Paddock (SSSI)† In the 1960s a small colony was recorded in rough Brachypodium pinnatum grassland. The site has received variable amounts of grazing in the past and the last confirmed record was in 1995. In 1999 12 plants originating from Barnack seed were planted out but none survived for more than a year (C. Gardner, pers. comm.).

Southorpe Roughs (SSSI)† A few plants formerly occurred in rank Bromopsis erectus-Brachypodium pinnatum grassland in an area of old quarry workings. The site was not grazed for many years and by the 1980s plants were very difficult to locate amongst the rank grass and invading scrub. It was apparently last seen by Franklyn Perring in 1990 (L. Farrell in litt. to T.C.E. Wells). It has not been seen since despite the recent reintroduction of sheep grazing (2004) and tree felling to reduce shade.

Sutton Heath† A single flowering plant was discovered on a small ridge of limestone turf close adjacent to Sutton Bog in 1972 (Wells, 2003) where it was seen again in 2003. The grassland shows signs of agricultural improvement and is heavily grazed. No plants have been found since despite repeated searches, although Astragalus danicus still occurs on the same ridge.

EAST GLOUCESTERSHIRE (v.c.33)

Barnsley Wold Warren (SSSI) The largest population in the UK with the majority of plants occurring at high density in exceptionally rich limestone turf on a steep (c.20º) SW-facing slope where soils are very shallow and there is much bare soil and rubble. Small numbers of plants have also occurred sporadically on a W-facing slope nearby. Historically the site has been heavily grazed by sheep, cattle and horses and the vegetation burnt (‘swaled’) in February or March. This practice was abandoned in 1971; since then the site has been grazed by sheep, at high density, between February to March and then from June onwards. This management has

45 resulted in an increase from around 50,000 to an estimated 75,000 crowns (D. Barling, pers. comm.).

Beaumonts Hay (SSSI) This site forms part of the Brassey Reserve and Windrush Valley SSSI and supports a small population of Pulsatilla on a relatively steep SW-facing limestone slope. Grazing has been increased in recent years producing a much shorter, species-rich sward.

Bourton Down (SSSI) Around 500 plants are restricted to a small area of sheep-grazed, W-facing downland with extremely shallow soils. Historically the site has been heavily grazed by sheep, although since 1982 stock have been removed from March to late summer in order to allow Pulsatilla to flower and currently the population appears stable. This management is similar to Barnsley Wold but with more variable winter grazing (Rich, 1997). In the 1966 two patches of Pulsatilla were recorded in ungrazed Brachypodium pinnatum grassland about 1 km to the NW of the reserve (SP132321) but this area is now dense hazel scrub.

Hornsleasow Roughs (SSSI) At this site Pulsatilla is scattered across a large area of former limestone quarries (“hills and holes”) that have had periods of heavy (1960s) and light grazing (1970-80), mostly by sheep but with a few cattle. It is currently lightly grazed by sheep (<3 ha-1) for most of the year (excluding March-May) and although this is not considered ideal management there are still around 100 plants scattered over a hectare of grassland but at low density. Since the relaxation in grazing the grassland changed from tightly grazed (c.2 cm) Festuca ovina turf (CG2d) to moderately rank (c.6 cm) but species-rich Bromopsis erectus grassland (CG3).

Sweetslade Farm† The majority of this site was ploughed-up in 1966. However, a small area of short limestone grassland (CG5a) was preserved to protect a few plants of Pulsatilla on WNW-facing slope. There are no subsequent records and the site is now completely covered by gorse scrub (M.A.R. and C. Kitchen, pers comm.).

Taylor’s Hill Although this population was originally discovered in 1847 it was not seen again until C.S. Downer found a few plants growing on a SW-facing limestone slope in 1971 (Holland, 1986). These had increased to 110 plants by 1982 whereas only 15 were located over a 200 m stretch of downland in 1996 (SP003157 to SP005156) (M.A.R. and C. Kitchen, pers comm.). This site currently has no conservation designation.

WEST GLOUCESTERSHIRE (v.c.34)

Rodborough Common (SSSI) In the 1960s Pulsatilla was recorded from two adjacent limestone slopes on Bear Hill (SO849027 and SO847029) and in rough grassland below the Iron Age hill fort on Rodborough Hill (SO848038). One of the colonies on Bear Hill still survives amongst rough Brachypodium pinnatum grassland (CG4) on a gentle S-facing slope. The other sites were lost due to scrub encroachment and lack of grazing (M.A.R. and C. Kitchen, pers comm.). Historically there has been light grazing by sheep and cattle and occasionally burnt (‘swaling’) in February or March by commoners but both practices have declined in recent decades. As a consequence the Bear Hill slope was mown in the 1990s and since 1999 winter grazing by cattle has been re-

46 introduced by the National Trust leading to a reduction in the cover of Brachypodium pinnatum and a gradual increase in the numbers of Pulsatilla.

SOUTH LINCOLNSHIRE (v.c.53)

Ancaster Valley (SSSI) A small colony occurs in lightly grazed limestone grassland (CG3) on an E-facing slope of a narrow limestone valley. The site was not grazed for many years leading to the development of rank Brachypodium pinnatum grassland and dense gorse scrub. The latter was removed during the late 1980s and the site has subsequently been annually winter-grazed by c.30 sheep (J. Welhan, pers. comm.). Due to improvement in the condition of the grassland 68 plants (originating from Ancaster seed) were re-introduced to the same slope (in 1992, 1993, 1998 and 2002) where they are protected by wire cages during the flowering period. All plants have been monitored annually since the early 1990s; in 2005 6 native plants and 22 (32%) introduced plants remained.

Holywell Mound (SSSI)† In the 1960s around 200 plants were present in species-rich limestone turf on a SW-facing slope although few plants flowered due to heavy grazing and the occasional ‘picking’ of flowers by local school children (J. Gibbons in litt. to T.C.E. Wells). In the 1960s the grassland was very short, herb-rich Bromopsis erectus-Brachypodium pinnatum grassland (CG5) with abundant Thesium humifusum. A few plants survived into the 1980s although the site was subsequently sprayed and partially improved. Pulsatilla has not been recorded for many years and the grassland is now a species-poor Bromopsis erectus grassland (CG3b) with few herbs.

Honington Camp (SSSI)† In the 1960s a small colony occurred in rank Bromopsis erectus grassland (CG3d) on the W- facing outer embankment of an Iron Age hill fort surrounded by arable land. The site has been infrequently grazed leading to the development of a thick sward of Brachypodium pinnatum amongst scattered Crataegus scrub. No plants have been seen since 1992 despite repeated searches.

Swinstead Valley (SSSI) On 25th April 2009, a single flowering plant of Pulsatilla vulgaris was discovered at a new site by Richard Jefferson and Fiona Hart in Swinstead Valley, South Lincolnshire (Jefferson & Walker, 2010). Subsequent searches revealed a total of four “plants” in 2009 and 18 in 2010, following the erection of a temporary grazing exclosure. This population is located on a moderately steep (c.30º) west-facing slope (280-310ºN) of limestone grassland on the east side of a narrow valley where the vegetation had been kept very short by rabbit and sheep grazing. The vegetation is species-rich Brachypodium pinnatum-Bromus [Bromopsis] erectus grassland (74% fit to CG5a, typical sub-community) with abundant Bromopsis erectus, Festuca ovina, Helianthemum nummularium, Sanguisorba minor and Thymus polytrichus and Astragalus danicus growing close-by.

NORTH LINCOLNSHIRE (v.c.54)

Broughton Far Wood (Clap-gate Pit) (SSSI)† In the 1960s 3-4 plants were recorded amongst ungrazed grassland and scrub in an abandoned limestone quarry. The plants were last recorded in 1969 when they were dug-up (I. Weston, pers. comm.).

47

LEICESTERSHIRE (v.c.55)

Shacklewell Hollow (SSSI) † In the 1960s a small colony was recorded in species-rich limestone grassland (CG5a) on a shallow SW-facing slope. Three plants were re-discovered at this site in 1992 when the grassland was very rank due to the lack of grazing. However, the population was subsequently destroyed when the farmer dumped rubble over the area (D. Isaac, pers. comm.).

MID-WEST YORKSHIRE (v.c.64)

Ledsham (SSSI) In 1984 a single plant was discovered in heavily grazed limestone grassland (CG4a) on a SE- facing limestone bank. For many years flower heads were grazed-off and so cages were placed around the plant to protect it from rabbits. In 1997 the plant was hand-pollinated with pollen collected (the same day) from Barnack Hills and Holes but the plant failed to set seed due to predation by slugs. As a result pollen from the Ledsham plant (male parent) was used to cross- pollinate five plants from Barnack (site 4) but without success (A. Headley, pers. comm.). A single Barnack plant was then translocated to within 4 metres of the Ledsham plant in order to encourage pollination but disappeared within a couple of years.

48 13 Annex 2 – changes in population size, 1960-2006

Changes in the numbers of Pulsatilla vulgaris on 33 sites included in Walker et al. (in press). Totals are the maximum number of crowns recorded in any one year for each decade and were derived from a variety of sources.

Site-population 1960-69 1970-79 1980-89 1990-99 2000-06 (a) Increasing Barnack Hills and Holes 2000 1300 14200 15000 20000 Barnsley Wold 50000 50000 50000 50000 75000 Barton Hills 1100 685 4000 5000 5000 Knocking Hoe 300 50 460 300 1000 Therfield Heath 1000 2897 ? 60000 60000

(b) Stable Ancaster Valley1 6 5 16 11 6 Beaumonts Hay <100 ? 25 ? 10 Bourton Down 500 ? 500 ? 471 Deacon Hill 1 ? 5 7 1 Devil’s Dyke 250 1500 1000 500 250 Hornsleasow Roughs 200 ? ? 100 100 Taylor’s Hill ? 42 110 15 ? Ledsham 3 ? ? 2 2 1

(c) Declining Aston Upthorpe2 300 101 35 10 26 Ravensburgh Castle 39 0 300 5 4 Rodborough Common 300 3 ? 40 37 Steps Hill 500 100 30 10 52

(d) Extinct Aldbury Nowers 17 0 0 0 0 Broughton Far Wood 9 0 0 0 0 Clipper Down 15 1 ? ? 0 Fleam Dyke 25 2 0 0 0 Hildersham Furze Hills 4 14 5 1 0 Holywell Mound 200 ? 1 ? 0 Honington Camp 53 ? 10 1 0 Lockinge 2 ? ? ? 0 Pitstone Hill 1 1 ? 2 0 Shacklewell Hollow 56 ? ? 3 0 Smithcombe Hill 30 ? 1 0 0 Southorpe Paddock 8 2 3 5 0 Southorpe Roughs 5 6 10 Present 0 Sweetslade Farm 7 ? ? 0 0 Sutton Heath ? 1 ? ? 0 Unhill Bottom 750 3 0 0 0 1 Excludes 68 plants introduced since 1992. 2 Excludes 87 plants introduced since 1999.

49 14 Annex 3 – associates

Vegetation composition and structure of Pulsatilla vulgaris populations in England (in 16 of the 18 extant populations - Taylor’s Hill & Swinstead Valley not included). For associates figures are frequency in quadrats (n = 62) with the mean % cover given in parentheses. Species recorded in <10% of quadrats are listed after the table. Constant species (> 80 % of quadrats) are highlighted in bold. For composition and structure variables figures are means with ± 1SE in parentheses. Figures are presented for (a) all 16 sites and for (b) limestone and (c) chalk sites only (n = 7 and 9 respectively).

All sites Limestone only Chalk only

(a) Associates Pulsatilla vulgaris V (4.2) V (3.6) V (4.9) Bromopsis erectus V (24.2) V (24.7) V (23.7) Festuca ovina V (12.9) IV (8.5) V (17.6) Sanguisorba minor V (8.8) V (8.7) V (8.9) Helianthemum nummularium V (6.0) V (7.2) IV (4.7) Carex flacca V (4.2) V (3.7) V (4.7) Cirsium acaule V (4.2) V (5.3) V (3.1) Leontodon hispidus IV (2.8) IV (2.8) IV (2.9) Pilosella officinarum IV (2.5) IV (3.2) III (1.8) Briza media IV (1.5) IV (1.9) III (1.0) Helictotrichon pratense IV (1.3) III (0.6) V (2.0) Koeleria macrantha IV (1) III (0.6) V (1.4) Carex caryophyllea IV (0.9) IV (0.9) IV (0.9) Brachypodium pinnatum III (5.1) V (7.4) I (2.7) Ctenidium molluscum III (3.6) III (3.4) III (3.7) Lotus corniculatus III (1.2) III (1.6) III (0.8) Campanula rotundifolia III (0.9) II (0.9) V (1.0) Scabiosa columbaria III (0.8) III (1.1) II (0.5) Plantago lanceolata III (0.7) III (0.7) III (0.6) Scleropodium purum II (2.0) III (3.5) II (0.3) Filipendula vulgaris II (1.6) I (0.5) IV (2.9) Thymus polytrichus II (1.0) III (1.8) I (0.1) Thymus pulegioides II (1.0) II (1.0) III (1.0) Centaurea nigra II (0.8) II (0.4) III (1.3) Plantago media II (0.6) II (0.9) III (0.4) Polygala calcarea II (0.6) II (0.9) I (0.3) Hippocrepis comosa II (0.6) I (0.5) III (0.8) Campyliadelphus chrysophyllus II (0.5) II (0.2) I (0.9) Campanula glomerata II (0.5) I (0.2) II (0.8) Viola hirta II (0.3) III (0.3) II (0.3) Homalothecium lutescens II (0.3) II (0.4) I (0.1) Asperula cynanchica II (0.2) II (0.2) II (0.2) Ranunculus bulbosus II (0.2) II (0.3) II (0.2) Carlina vulgaris II (0.2) II (0.3) I (0.1)

50 Annex 3 continued.

All sites Limestone only Chalk only Pimpinella saxifraga II (0.2) II (0.2) I (0.2) Linum catharticum II (0.1) III (<0.1) II (0.1) Crataegus monogyna II (0.1) II (0.1) II (0.2) Galium verum II (0.1) II (<0.1) I (0.2) Anthyllis vulneraria I (0.6) II (1.1) Primula veris I (0.4) II (0.9) Fissidens sp. I (0.3) II (0.3) I (0.2) Thesium humifusum I (0.2) II (0.4) I (<0.1) Fissidens cristatus I (0.2) I (0.1) I (0.3) Succisa pratensis I (0.2) I (<0.1) I (0.4) Tephroseris integrifolia I (0.2) II (0.5) Taraxacum officinale agg. I (0.1) II (0.1) I (<0.1) Prunella vulgaris I (0.1) I (<0.1) II (0.2)

(b) Vegetation composition/structure Vegetation height (cm) 7.5 (0.7) 7.0 (0.8) 7.9 (1.1) Bare ground (%) 6.2 (1.2) 7.0 (1.7) 5.3 (1.6) Number of species 23.0 (0.7) 23.1 (1.1) 22.8 (1.0) Number grasses & sedges 6.2 (0.2) 6.4 (0.3) 6.0 (0.2) % cover of grasses & sedges 49.1 (1.9) 46.0 (3.0) 52.0 (3.0) Number herbs 14.6 (0.6) 14.0 (0.9) 15.2 (0.9) % cover of herbs 44.1 (2.1) 46.0 (3.0) 42.0 (3.0) Diversity 1.0 (0.0) 1.1 (0.1) 1.0 (0.0) Evenness 0.7 (0.0) 0.8 (0.0) 0.7 (0.0) % cover of Bromopsis erectus 24.2 (2.4) 24.7 (3.8) 23.7 (2.8) Number of positive indicators 10.2 (0.4) 10.4 (0.5) 10.0 (0.5) % cover of positive indicators 63.3 (2.5) 69.1 (3.8) 57.1 (3.0) % fit to CG3 or CG5 60.5 (2.0) 54.7 (2.7) 66.8 (2.5)

Sites and number of quadrats recorded (1968, 2006): Ancaster Valley (2,1), Aston Upthorpe (1,1), Barnack Hills and Holes (4,3), Barnsley Wold (3,2), Barton Hills (2,4), Beaumonts Hay (2,1), Bourton Down (3,2), Devil's Dyke (2,2), Hornsleasow Roughs (1,2), Knocking Hoe (3,1), Knocking Hoe - Spiranthes Bank (1,1), Ravensburgh Castle (2,1), Rodborough Common (4,1), Steps Hill (1,1), Therfield Heath – Pen Hill (2,1), Therfield Heath - Church hill (3,1). Species recorded in less than 10% of quadrats: Aceras anthropophorum, Arrhenatherum elatius, Blackstonia perfoliata, Carex ericetorum, Centaurea scabiosa, Cerastium fontanum, C. pumilum, Cirsium arvense, C. vulgare, Cladonia sp., Cynosurus cristatus, Dicranum scoparium, Euphrasia nemorosa, Festuca rubra, Galium aparine, G. mollugo, Gentianella amarella, Gymnadenia conopsea, Helictotrichon pubescens, Heracleum sphondylium, Hieracium exotericum, Himantoglossum hircinum, Hylocomium splendens, Hypnum cupressiforme, Hypochaeris maculata, H. radicata, Leucanthemum vulgare, Luzula campestris, Medicago lupulina, Neckera complanata, Onobrychis viciifolia, Ononis repens, Ophrys apifera, Orchis mascula, O. morio, Pastinaca sativa, Phleum bertolonii, Picris hieracioides, Poa compressa, Polygala vulgaris, Polytrichum sp., Prunus spinosa, Quercus robur, Rhamnus cathartica, Rhinanthus minor, Rhytidiadelphus squarrosus, R. triquetrus, Rosa canina, Seligeria sp., Senecio jacobaea, Serratula tinctoria, Seseli libanotis, Sonchus asper, Thuidium assimile, Trifolium pratense, T. repens, Trisetum flavescens, Veronica chamaedrys, Weissia sp.

51

Written by Kevin Walker, BSBI Edited by Plantlife International First draft dated Sept 2010 Last revised 19 April 2011

52