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Keywords:

  • communities;
  • conservation;
  • ecophysiology;
  • geographical and altitudinal distribution;
  • germination;
  • herbivory;
  • mycorrhiza;
  • reproductive biology;
  • soils

Summary

  1. Top of page
  2. Summary
  3. I. Geographical and altitudinal distribution
  4. II. Habitat
  5. III. Communities
  6. IV. Response to biotic factors
  7. V. Response to environment
  8. VI. Structure and physiology
  9. VII. Phenology
  10. VIII. Reproductive characteristics
  11. IX. Herbivory and disease
  12. X. History
  13. XI. Conservation
  14. Acknowledgements
  15. References

1. This account presents information on all aspects of the biology of Dryopteris carthusiana (Vill.) H. P. Fuchs, D. dilatata (Hoffm.) A. Gray, and D. expansa (C. Presl) Fraser-Jenk. & Jermy that are relevant to an understanding of their ecological characteristics and behaviour. The main topics are presented within the standard framework of the Biological Flora of the British Isles: distribution, habitat, communities, responses to biotic factors, responses to environment, structure and physiology, phenology, reproductive characteristics, herbivores, history, and conservation.

2. All three species are native deciduous ferns that are morphologically similar and genetically interrelated. Dryopteris dilatata, one of the commonest ferns in the British Isles, is found in many different habitats, but is above all a woodland species. Dryopteris carthusiana is less widely distributed, being mostly a species of wetlands and wet woodlands. Dryopteris expansa is the least common, mostly found in mountains, but also in wet woodlands at lower altitudes.

3.Dryopteris dilatata is mainly a species of semi-shade, and in the British Isles is considered to be the most shade-tolerant of the three. Dryopteris carthusiana occurs in a wide range of habitats, from exposed, well-illuminated to moderately shaded ones. Dryopteris expansa mainly grows in better illuminated habitats, often in the shade of sparse canopies or rocks. D. expansa is thus the most light-demanding species of the three.

4. The response to competition from neighbouring herbs has been shown to differ among the three species; D. expansa is clearly more vulnerable to competition than D. carthusiana and D. dilatata.

5.Dryopteris dilatata and D. carthusiana are both tetraploid, whereas D. expansa is diploid. Natural hybrids among all three species in the British Isles, as well as hybrids of D. carthusiana with D. filix-mas and D. cristata. The hybrid D. carthusiana × D. dilatata = D. × deweveri is the most common. The hybrids D. carthusiana × D. expansa D. × sarvelae and D. cristata ×D. carthusiana D. × uliginosa are extremely rare and at high risk of extinction.

6. Although not currently threatened, the distribution of all three species may be susceptible to continued habitat loss arising from changes in land use, management for control of Bracken and predicted climate change.

Dryopteridaceae. Dryopteris dilatata (Hoffm.) A. Gray (D. austriaca Woyn. ex Schinz & Thell. non Jacq.), the Broad Buckler-fern, is a polycarpic perennial hemicryptophyte. Rhizome short, erect to ascending or decumbent. Fronds tripinnate to quadripinnate, to 150(180) cm (Clapham, Tutin & Moore 1989; Stace 2010), arching, arranged in more or less funnel-shaped rosettes. Stipe 1/4 to as long as the lamina, fairly densely covered, especially at the base, with scales dark in the centre and pale brown at the margin or almost entirely dark. Lamina dark (olive or blue) green, slightly leathery in texture, ovate to triangular-ovate in outline. Pinnae triangular-ovate or lanceolate, short-stalked; up to 25 on each side (Clapham, Tutin & Moore 1989). Ultimate segments of pinnae linear-oblong, usually strongly convex above, with sharply serrated margins and spinulose teeth that curve downwards. Pinnae approximately equidistant throughout the lamina, lower pinnae asymmetrical, with basal basiscopic pinnules longer than acroscopic ones, basiscopic pinnules of the lowermost pinnae usually much less than half the length of their pinnae (Fig. 1a). Sori 0.5–1 mm in diameter (Clapham, Tutin & Moore 1989), usually in two rows on each pinnule, all over the underside of the lamina; indusia reniform, glandular (Stace 2010); spores blackish brown.

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Figure 1.  Silhouettes of the basal pinna, with the lowermost pinnule: (a) Dryopteris dilatata; (b) D. carthusiana; and (c) D. expansa.

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Dryopteris carthusiana (Vill.) H. P. Fuchs (D. lanceolatocristata (Hoffm.) Alston, Dspinulosa Kunze), the Narrow Buckler-fern, is a polycarpic perennial hemicryptophyte. Rhizome either short and decumbent or longer and more slenderly prostrate, occasionally branched (Page 1997). Fronds bipinnate-pinnatifid to tripinnate, stiffly erect, to 100(150) cm (Clapham, Tutin & Moore 1989; Stace 2010), in irregular groups. Stipe 1/4 to as long as the lamina, sparsely covered with uniformly pale brown scales without a central dark stripe. Lamina yellowish to mid-green, of firm but delicate texture; narrowly ovate-oblong. Pinnae triangular-ovate or lanceolate, short-stalked; up to 25 on each side (Fitter & Peat 1994); pinnules ± flat, segments oblong, with serrated margins and upwardly curving conspicuous spinulose teeth. Lower pinnae fairly distant and asymmetrical, often tilted to a nearly horizontal position, with basal basiscopic pinnules longer than acroscopic ones (Fig. 1b); upper pinnae closer and narrower, with tips pointing upwards. Sori on the lower side of the frond in one or two rows on each pinnule, orbicular, 0.5–1 mm in diameter (Clapham, Tutin & Moore 1989), covered with reniform indusia usually without glands (Stace 2010); lowermost pair of pinnae usually lacking sori. Spores dark brown.

Dryopteris expansa (C. Presl) Fraser-Jenk. & Jermy (D. assimilis S. Walker), the Northern Buckler-fern, is a polycarpic perennial hemicryptophyte. Rhizome short, erect to decumbent. Fronds to tripinnate or even quadripinnate at the base, to 100 cm (Stace 2010), rather stiffly spreading to only slightly arching, in ± regular sparse funnel-shaped rosettes. Stipe 1/2 to the same length as the lamina, fairly densely covered, especially at the base, with uniformly pale brown (tan) to distinctly reddish brown scales, sometimes having a darker central stripe or base. Lamina mid to yellowish green, soft in texture and triangular-ovate to broadly ovate, with the lowest pinna usually the longest. Pinnae triangular-ovate or lanceolate, short-stalked; all in one plane. Ultimate segments of pinnae ± oval, sharply serrated with softly short spinulose teeth, usually with flat margins. Lower pinnae usually more distant than upper ones, asymmetrical, with basal basiscopic pinnules longer than acroscopic ones, basal basiscopic pinnule of lowermost pinnae usually half or more of the length of its pinna (Fig. 1c). Sori orbicular, 0.5–1 mm in diameter (Clapham, Tutin & Moore 1989), covered with reniform glandular indusia (Stace 2010), usually in two rows on each pinnule, all over the underside of the lamina. Spores pale brown.

All three species may overlap in many characteristics, including plant height, shape and dissection of the lamina, as well in the shape and position of the sori. The best discrimination between species may be achieved using the colour and pattern of scales, the colour of spores and the presence of glands on the indusia. In similar habitat conditions, there are usually clear differences between D. dilatata and D. expansa, the former having the edges of pinnules all turned downwards, making these convex on the upper side (this is more obvious in young fronds; Crabbe, Jermy & Walker 1970); the latter has all pinnae in more or less one plane. Other characteristics such as the colour and texture of the lamina and the shape of ultimate segments may also be reliable. Those characteristics depend more than others on environmental conditions, for example illumination, and age or size of plants, and work best when comparing plants of the same size and age from a similar environment.

The three species (together with D. cristata (L.) A. Gray) are cytogenetically closely related and able to form hybrids; they have been treated as members of the Dryopteris carthusiana (D. spinulosa) complex (Manton 1950; Walker 1955). Dryopteris dilatata (Manton & Walker 1954) and D. carthusiana (Manton 1950) are tetraploids which originated through allopolyploidy by interspecific hybridization of diploid species followed by chromosome doubling (Walker 1955). Since the 1950s, several different ancestral diploid parental genomes have been proposed for each species on the basis of cytological and biochemical studies. Dryopteris expansa has been suggested as one parent of D. dilatata, with D. intermedia (Muhl. ex Willd.) A. Gray, D. intermedia ssp. maderensis (J. Milde ex Alston) Fraser-Jenkins or D. azorica (Christ) Alston as the other (Widén, Sorsa & Sarvela 1970; Gibby & Walker 1977; Gibby 1983). Dryopteris intermedia, D. intermedia ssp. maderensis or D. azorica have also been suggested as one parent of D. carthusiana and D. ludoviciana (Kunze) Small (Wagner 1970; Hickok & Klekowski 1975; Gibby, Widén & Widén 1978; Gibby 1983; Widén & Britton 1985) or a hypothetical unknown species named as D. ‘semicristata’ (Wagner 1970; Stein et al. 2010) or D. stanley-walkeri Fras.-Jenk. (Fraser-Jenkins 2001) as the other. Results of recent molecular research (nuclear pgiC and plastid trnL-F; Juslén, Väre & Wikström 2011) of Dryopteris species from Europe supported the hypothesis of allopolyploid origin of D. carthusiana (with D. intermedia and D. ludoviciana as diploid progenitors), but not for D. dilatata. The latter species may have originated by autopolyploidy from D. expansa.

Intraspecific taxa have been recognized for only D. expansa. According to Viane (1986), two varieties can be distinguished on the basis of the number of glands on the indusium: var. expansa (plants completely eglandular or with some glands on the indusium) is distributed in Greenland, North America and Japan; var. alpina (Moore) Viane from Europe is more glandular, with glands on the lamina surface and indusia. Later research has not supported the subdivision of the species based on these relative and inconsistent characters, and the subdivision has not been generally accepted (Fraser-Jenkins 1993; Montgomery & Wagner 1993; Stace 2010), except in Russia, where var. alpina has been considered to be a separate species, D. assimilis S. Walker (Tzvelev 2003).

In western Norway, individuals with dark-green fronds, black or black-green striped stipes, rachises and bases of the costae have been described as a (possible) endemic variety of the species D. expansa var. willeana (Lid) Elven (Sarvela 2000).

Genetic variation in populations of D. dilatata in ancient and recent forests has been studied in Germany (Reisch et al. 2007) using random amplified polymorphic DNA (RAPD) analysis. Ten primers were used for the analysis. Significant genetic variance was observed between ancient and recent forests (6%), and mean genetic diversity was higher in ancient than in recent forests.

All three species are native to the British Isles. Dryopteris dilatata is the most common and can be found in woodland and scrub, shaded grassland and heathland, on the margins of bogs, on hedgebanks, stone walls, quarry waste, sea cliffs, in rock crevices and block scree and on montane cliff ledges. Dryopteris carthusiana is a species of damp woodland and moorland habitats in areas of Britain and Ireland with acidic soils. Dryopteris expansa, the rarest, is characteristically found in open, damp woods and shady places on mountains; it is most frequent in Scotland, also occurs in Wales and northern England, but is absent from Ireland (Dines 2002a).

I. Geographical and altitudinal distribution

  1. Top of page
  2. Summary
  3. I. Geographical and altitudinal distribution
  4. II. Habitat
  5. III. Communities
  6. IV. Response to biotic factors
  7. V. Response to environment
  8. VI. Structure and physiology
  9. VII. Phenology
  10. VIII. Reproductive characteristics
  11. IX. Herbivory and disease
  12. X. History
  13. XI. Conservation
  14. Acknowledgements
  15. References

Dryopteris dilatata is mostly a European species, being most frequent in western and Central Europe. It belongs to the European temperate element (Preston & Hill 1997). D. dilatata is very common and widespread in the British Isles (Fig. 2), occurring over a wide range of altitude up to 1125 m in Scotland (Dines 2002c). Dryopteris dilatata is the most frequent fern after Pteridium aquilinum; it has been recorded in 3673 (95%) hectads (10 × 10-km squares; BSBI Maps Scheme: Hectad Maps 2011). In Central Europe (Fig. 3), it occurs in lowlands, although it is more common in mountains, and reaches 1700 m in the Tatras (Piękoś-Mirkowa 1991). In southern Europe, D. dilatata is less frequent, occurring mostly in mountains, for instance up to 2000–2200 m in the Alps (Dostál, Fraser-Jenkins & Reichstein 1984; Piękoś-Mirkowa 1991), and is absent from large Mediterranean and Black-Sea areas (Hultén & Fries 1986). Near the south-eastern border of its distribution in the Ukrainian Carpathian Mountains, D. dilatata is quite common (Tzvelev 2003), as is the case near the northern border of its distribution, in southern Scandinavia, where it is also one of the most common lowland and lower mountain ferns (Øllgaard & Tind 1993). Dryopteris dilatata becomes rarer in southern Finland (Sarvela 2000), where it reaches its north-eastern boundary. It is also rare in the Baltic States (Eglīte & Šulcs 2000; Patalauskaitė 2004; Kukk & Kull 2005) and in western Russia, where it is recorded in scattered localities to about 32° E (Tzvelev 2000, 2003). Dryopteris dilatata reaches the south-eastern border of its distribution in western Asia, in scattered localities between the Black and Caspian seas (Piękoś-Mirkowa 1977; Hultén & Fries 1986; Mazooji & Fallahian 2005).

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Figure 2.  The distribution of Dryopteris dilatata in the British Isles. Each dot represents at least one record in a 10-km square of the British National Grid: (○) pre-1970, (•) 1970 onwards. Mapped by Colin Harrower, using Dr A. Morton’s DMAP software, Biological Records Centre, Centre for Ecology & Hydrology, mainly from data collected by members of the Botanical Society of the British Isles.

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Figure 3.  The European distribution of Dryopteris dilatata on a 50-km square basis: (?) uncertain record. Dashed lines indicate the boundary of the mapped area. Reproduced from Atlas Florae Europaeae, vol. 1, by permission of the Committee for the mapping of the Flora of Europe and Societas Biologica Fennica Vanamo.

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Dryopteris carthusiana is a disjunctly holarctic, mostly boreal-temperate species that is widely distributed in Eurasia and North America (Montgomery & Wagner 1993). Dryopteris carthusiana is considered to belong to the Eurosiberian Boreo-temperate element of the British and Irish flora (Preston & Hill 1997). It is also widespread in the British Isles, although absent from many areas in lowland England, infrequent in southern Ireland and northern Scotland, and absent from Orkney and Shetland (Fig. 4). It occurs mostly at lower altitudes from sea level up to 330 m and seldom in mountains, up to 730 m (Page 1997; Dines 2002b). Dryopteris carthusiana has been recorded in 2136 (55%) hectads. In central and southern Europe (Fig. 5), D. carthusiana is found from close to sea level up to an altitude of 1700 m in the Tatra Mountains (Piękoś-Mirkowa 1991) and up to 2660 m in the Alps, although it is rare in the subalpine zone (Dostál, Fraser-Jenkins & Reichstein 1984). It is rarer in the Mediterranean, Black- and Caspian-Sea areas. In northern Europe, D. carthusiana grows up to subalpine regions in central parts of southern Scandinavia and is rare in higher mountains and absent in the northernmost part of the region (Øllgaard & Tind 1993). In Asia, its distribution stretches from the Ural Mountains to eastern Siberia (Czerepanov 1995; Tzvelev 2003); smaller isolated ranges are located in Turkey (Davis 1965), the Caucasus (Tzvelev 2003) and northern Iran (Mazooji & Fallahian 2005).

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Figure 4.  The distribution of Dryopteris carthusiana in the British Isles. Each dot represents at least one record in a 10-km square of the British National Grid: (○) pre-1970, (•) 1970 onwards. Mapped by Colin Harrower, using Dr A. Morton’s DMAP software, Biological Records Centre, Centre for Ecology & Hydrology, mainly from data collected by members of the Botanical Society of the British Isles.

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image

Figure 5.  The European distribution of Dryopteris carthusiana (east of the solid line incl. D. expansa & D. dilatata) on a 50-km square basis: (•) post-1930 records (×) pre-1930 records, (+) extinct, (○) introduction. Dashed lines indicate the boundary of the mapped area. Reproduced from Atlas Florae Europaeae, vol. 1, by permission of the Committee for the mapping of the Flora of Europe and Societas Biologica Fennica Vanamo.

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Dryopteris expansa has a disjunctly holarctic range, distributed in Eurasia and northern America (Montgomery & Wagner 1993) as well on Greenland and Iceland (Hultén & Fries 1986). It belongs to the Circumpolar Boreal-montane element of the British and Irish flora (Preston & Hill 1997). It occurs mostly in montane areas of the British Isles, being found in Wales and northern England, but most frequently in Scotland (Fig. 6). It also grows in Orkney and Shetland, but is not recorded in Ireland. Dryopteris expansa is most commonly found in lowlands from sea level up to 150 m and, in mountains, from 600 up to 1000 m; in the upper arctic-alpine zone, it is rarer (Page 1997). The most noticeable difference between the three species in the British Isles is the restriction of D. expansa to northern montane areas, where it is represented in only 292 (8%) hectads. In Central Europe (Fig. 7), it occurs mostly in mountains up to the alpine region, in the Tatras up to 2098 m (Piękoś-Mirkowa 1991), and in scattered localities in the lowlands. In southern Europe, it occurs only in mountains, up to 2660 m in the Alps (Dostál, Fraser-Jenkins & Reichstein 1984). In Scandinavia, D. expansa is widely distributed and is rarer only in the most northerly parts of the area (Øllgaard & Tind 1993). In eastern Europe, the frequency of distribution in the Baltic countries, for instance, varies; D. expansa is found in scattered localities throughout Estonia (Kukk & Kull 2005) and Lithuania (Patalauskaitė 2004), being more frequent in Estonia, but it is rare in Latvia (Eglīte & Šulcs 2000). In Russia, the distribution of the species extends from the northern and central part of western Russia to Siberia and Kamchatka (Tzvelev 1991; Czerepanov 1995), and in Asia the distribution extends to Mongolia (Dulamsuren et al. 2005) and Japan (Iwatsuki 1995). Smaller isolated localities have been found in the Caucasus (Piękoś-Mirkowa 1977), northern Iran (Mazooji & Fallahian 2005) and north-eastern Turkey (Kaynak, Benlioglu & Tarimcilar 1996).

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Figure 6.  The distribution of Dryopteris expansa in the British Isles. Each dot represents at least one record in a 10-km square of the British National Grid: (○) pre-1970, (•) 1970 onwards. Mapped by Colin Harrower, using Dr A. Morton’s DMAP software, Biological Records Centre, Centre for Ecology & Hydrology, mainly from data collected by members of the Botanical Society of the British Isles.

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image

Figure 7.  The European distribution of Dryopteris expansa on a 50-km square basis. Dashed lines indicate the boundary of the mapped area. Reproduced from Atlas Florae Europaeae, vol. 1, by permission of the Committee for the mapping of the Flora of Europe and Societas Biologica Fennica Vanamo.

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II. Habitat

  1. Top of page
  2. Summary
  3. I. Geographical and altitudinal distribution
  4. II. Habitat
  5. III. Communities
  6. IV. Response to biotic factors
  7. V. Response to environment
  8. VI. Structure and physiology
  9. VII. Phenology
  10. VIII. Reproductive characteristics
  11. IX. Herbivory and disease
  12. X. History
  13. XI. Conservation
  14. Acknowledgements
  15. References

(A) Climatic and topographical limitations

Temperature

The comparison of the overall distribution of the species in Europe (Figs 3, 5 and 7) and world-wide (Hultén & Fries 1986) with corresponding climatic data (Boucher 1987; Sedunov 1991) suggests that freezing temperatures should not limit either the altitudinal or latitudinal distribution of any of the three ferns in the British Isles. Mean January and July temperatures in British hectads occupied by D. dilatata are 3.5 and 14.4 °C, respectively (Hill, Preston & Roy 2004). The effect of winter temperature on the distribution of D. dilatata becomes evident in northern Europe, where the border of the species’ distribution follows the isotherm along which the coldest month is between −5 and −8 °C.

Mean January and July temperatures in the distribution of D. carthusiana are similar to D. dilatata, 3.3/14.6 °C (Hill, Preston & Roy 2004). In northern Europe, D. carthusiana could be limited by summer (mean July) temperature as its distribution border follows the isotherm between 8 and 10 °C; the limiting effect of winter (mean January) temperature is not so obvious, being between −8 and −16 °C.

Dryopteris expansa occurs in colder areas with mean January temperature of 1.7 °C and mean July temperature of 12.0 °C in the British Isles. In Central Europe, D. expansa has been used as an indicator of coolness, as it occurs mostly in the subalpine zone (Ellenberg et al. 1991). In the British Isles, D. expansa may be limited by summer temperature, as it is mostly distributed in areas where mean July temperature is lower than 15 °C. In northern Europe, D. expansa, like D. carthusiana, could be limited by summer (mean July) temperature.

Rainfall and humidity

Average annual precipitation in British hectads occupied by Dryopteris dilatata is 1114 mm (Hill, Preston & Roy 2004). This species occurs in the broadest range of humidity conditions, from open and relatively dry habitats to sheltered high-humidity habitats near running water.

Although D. carthusiana is often associated with high air humidity (Page 1997), the average annual precipitation in the hectads it occupies is 1075 mm, similar to that of D. dilatata (Hill, Preston & Roy 2004).

The soft, delicately textured fronds of D. expansa are characteristic of humid, cool habitats in lowland forests or mountains in the British Isles (Page 1997) with average annual precipitation for hectads of 1772 mm (Hill, Preston & Roy 2004), the highest among the three species.

Light flux

Dryopteris dilatata is a species of woodland semi-shade (Ellenberg value for light = 5; Hill, Preston & Roy 2004) that is rarely found in full light, but generally where there is more than 10% relative illumination when trees are in leaf (Grime, Hodgson & Hunt 1988; Page 1997). In the British Isles, D. dilatata is considered to be the most shade-tolerant of the three species. In Central Europe, the species’ optimum for light has been reported to be between 5 and 10% of relative illumination (Ellenberg value for light = 4; Ellenberg et al. 1991). In Scandinavia, D. dilatata grows in shaded as well as open habitats (Øllgaard & Tind 1993).

Dryopteris carthusiana occurs in a wide range of habitats, from exposed, well-illuminated ones in northern England and Scotland to moderately shaded habitats on woodland edges in lowlands (Page 1997). According to Hill, Preston & Roy (2004) the species has an Ellenberg value=6 for light, indicating that it is usually found in habitats with >10% relative illumination when the trees are in leaf. In Central Europe, D. carthusiana has been classified as a semi-shade plant (Ellenberg value for light = 5), that rarely grows in full light, although generally with more than 10% relative illumination when trees are in leaf (Ellenberg et al. 1991). In northern Europe, the species’ amplitude for light is broadest compared to the other two taxa (Øllgaard & Tind 1993).

Dryopteris expansa is a species of generally well-illuminated habitats (Ellenberg value for light = 7), but it also grows in partial shade (Hill, Preston & Roy 2004). Dryopteris expansa is the most light-demanding species of the three. Although the vegetation in the species’ habitats in Central Europe is quite similar to that in the British Isles (Dostál, Fraser-Jenkins & Reichstein 1984), its light optimum on the continent is considered to be lower (Ellenberg value = 4), and it can occur in microhabitats where relative illumination is 5–10% when trees are in leaf (Ellenberg et al. 1991). In northern Europe, D. expansa occurs in open and shaded habitats in the lowlands as well as in the mountains of Scandinavia (Øllgaard & Tind 1993).

Slope and aspect

Dryopteris dilatata can be found on slopes with various degrees of inclination, but more frequently in northern England on those of northern aspect (Grime, Hodgson & Hunt 1988), as in Scandinavia (Øllgaard & Tind 1993). In Central Europe (Tatra mountains), D. dilatata does not affect any particular inclination or aspect (Piękoś-Mirkowa & Miechŏwka 1992).

In Scandinavia, D. carthusiana can be found mainly on southern slopes of mountains, whereas in lowland forests it generally occurs on north-facing slopes, like the two other species (Øllgaard & Tind 1993). In Central Europe (Tatra mountains), D. carthusiana, similarly to D. dilatata, shows no preference for any particular inclination or aspect (Piękoś-Mirkowa & Miechŏwka 1992).

In Britain, Dryopteris expansa occurs mainly on north-facing, but also east-facing, scree slopes of mountains (Page 1997). In Scandinavia (Øllgaard & Tind 1993) and Central Europe (Tatra mountains), D. expansa usually occurs on north-facing slopes of varying inclination (Piękoś-Mirkowa & Miechŏwka 1992).

(B)Substratum

Dryopteris dilatata typically grows in deep, humus-rich, moderately fertile, mineral soils (Hill, Preston & Roy 2004) derived from a wide range of rock types (sandstones, slates, granites, grits and shales), although it also occurs in moderately fertile, peaty soils (Grime, Hodgson & Hunt 1988). Dryopteris dilatata can additionally be found as an epiphyte on fallen trunks, rotting stumps or tree bark. In skeletal habitats of rocky areas, D. dilatata grows in humus that accumulates in crevices and in holes on top of boulders. The species can also be found in anthropogenic habitats, for example in old brick basements and at the bases of old walls and bridges (Page 1997). In the mountains of Central Europe, D. dilatata grows in fertile (Ellenberg et al. 1991), loose sandy-stony loam soils or in rubble soils (Dostál, Fraser-Jenkins & Reichstein 1984). In the Tatra Mountains, D. dilatata grows in various types of soils with high humus content that are rich in available magnesium, medium-rich to poor in potassium and medium-rich in phosphorus (Piękoś-Mirkowa & Miechŏwka 1992).

In the British Isles, D. carthusiana grows in wet mineral or peaty soils (Dines 2002b) of relatively low fertility (Hill, Preston & Roy 2004). It is most successful in peaty alluvial soils and is absent from the most mineral-poor sites (Page 1997). Habitats with peaty soils are common for D. carthusiana in Central Europe (Dostál, Fraser-Jenkins & Reichstein 1984). However, it prefers more or less infertile (Ellenberg et al. 1991) sandy, clayey or loamy mineral soils, or grows as a epiphyte on fallen, rotting tree trunks and stumps (Seifert 1992), or on living trees, as in Fennoscandia (Sarvela 2000). In Fennoscandia, D. carthusiana also grows in oligotrophic to mesotrophic mineral soils in lowlands, in rock crevices and screes on mountains, and also as a weed on stone walls (Sarvela 2000). In the Tatra Mountains, D. carthusiana grows in soils with a high content of humus, mostly rendzinas, calcareous cambisols and eutric cambisols. These soils are poor in available magnesium and potassium and very poor in phosphorus (Piękoś-Mirkowa & Miechŏwka 1992).

In lowland areas in the British Isles, D. expansa grows in peaty and mineral soils, but it can be also found around rock outcrops. On mountains, D. expansa grows in the rocky cavities of mountain scree, but is most successful in pockets of block-scree slopes of mica schist (Page 1997). The requirement for soil fertility of D. expansa is the lowest of the three species (Ellenberg et al. 1991; Hill, Preston & Roy 2004). In Scandinavia, the habitats of D. expansa are described as mesotrophic, and on mountains the species grows among large boulders in scree and at the bases of large banks of creeping soil (Øllgaard & Tind 1993). Dryopteris expansa has also been found growing as a weed on stone walls and in crevices of lava-flows in Iceland (Sarvela 2000). In the Tatra Mountains, D. expansa grows mostly in dystric cambisols, podzolic rankers, orthic podzols and dystric histosols. These soils have developed from acidic parent rock (granites, gneisses) or peat, have a high humus content, and are poor in available potassium and phosphorus, whereas the magnesium content varies widely (Piękoś-Mirkowa & Miechŏwka 1992).

Height and seasonal variation of the water-table

Dryopteris dilatata occurs mostly in habitats with permanently moist but not wet soils (Hill, Preston & Roy 2004). In wet woodlands and mires with high water-tables, D. dilatata grows in raised microhabitats, with better drainage (hummocks). In high air humidity, D. dilatata can become epiphytic on trees (Page 1997; Dines 2002c). In Scandinavia, the amplitude for soil moisture is broader; D. dilatata grows not only in moist soils, but also in drier habitats, including stone walls (Øllgaard & Tind 1993). In Central Europe, the ecological optimum of D. dilatata for moisture is similar to that of the British Isles, growing mostly in moist or damp soils (Ellenberg et al. 1991).

Dryopteris carthusiana is characteristic of a seasonally fluctuating or permanently high groundwater level in the British Isles. Its ecological optimum lies between constantly moist or damp and wet habitats (Hill, Preston & Roy 2004), suggesting that the high water-table conditions are required for optimal growth and reproduction. In Scandinavia and Central Europe, D. carthusiana occurs over a broader soil moisture range. In southern Europe, the species can also be found in drier habitats, such as stone walls (Dostál, Fraser-Jenkins & Reichstein 1984; Øllgaard & Tind 1993), or as an epiphyte on trees (Sarvela 2000).

Dryopteris expansa is mostly distributed in moist or damp soils, with a permanently high level of groundwater, or in moist rock fissures in mountains (Page 1997; Hill, Preston & Roy 2004). The ecological amplitude of D. expansa for moisture appears to be even narrower than that of D. carthusiana, although towards the drier end of the gradient (Page 1997). In colder climates (e.g. Scandinavia), D. expansa occurs not only in moist but well-drained soils (Øllgaard & Tind 1993), but also in drier habitats, such as stone walls (Sarvela 2000). In Central Europe, D. expansa occurs mainly in habitats with moist rather than wet soils (Ellenberg et al. 1991) as in the British Isles.

Soil pH

The ecological optima for soil reaction of the three species in the British Isles are different (Hill, Preston & Roy 2004), with that of D. dilatata lying between the other two species (Ellenberg value for pH = 4); it is most frequent and abundant in acidic soils with pH < 5.0 and is rare in soils with pH above 6.5 (Grime, Hodgson & Hunt 1988). Dryopteris carthusiana grows mainly in moderately acidic soils (Ellenberg value for pH = 5). Dryopteris expansa is mainly a species of acidic soils (Ellenberg value for pH = 3).

In Central Europe, all three species inhabit acidic soils (Dostál, Fraser-Jenkins & Reichstein 1984); the ecological optima of D. carthusiana and D. expansa are at lower pH than in the British Isles. The Ellenberg indicator value for soil pH for D. carthusiana is 4 (favouring acidic to moderately acidic habitats) and that for D. expansa is 2 (indicative of very acidic to acidic soils; Ellenberg et al. 1991). In the Tatra Mountains, the species’ distribution pattern is similar and all three species have their highest frequency in acidic soils with pH < 4.5 (Piękoś-Mirkowa & Miechŏwka 1992).

Organic matter content

The organic carbon content of soils collected from habitats of Dryopteris species in the Polish Tatra Mountains has been studied colorimetrically. The frequency of all three species was highest in soils with a content of 2.5–12.0% of organic C in the rhizosphere and lower in soils with higher (>12%) contents of organic C (Piękoś-Mirkowa & Miechŏwka 1992).

III. Communities

  1. Top of page
  2. Summary
  3. I. Geographical and altitudinal distribution
  4. II. Habitat
  5. III. Communities
  6. IV. Response to biotic factors
  7. V. Response to environment
  8. VI. Structure and physiology
  9. VII. Phenology
  10. VIII. Reproductive characteristics
  11. IX. Herbivory and disease
  12. X. History
  13. XI. Conservation
  14. Acknowledgements
  15. References

Although in the British Isles D. dilatata can be found in very different communities, from woodlands to open habitats, it is primarily a woodland species, which occurs in most woodland community types (Rodwell 1991a). The species has been recorded in a total of 18 woodland, two heath, four montane, two swamp and one open habitat community types, and in altogether 58 subcommunities (Rodwell 1991a,b, 1992, 1995, 2000; Table 1). In most of these subcommunities, D. dilatata is scarce or occasional, being a constant species in only five subcommunities, and common in seven subcommunities.

Table 1.   British plant communities and subcommunities in which Dryopteris carthusiana (C) and D. dilatata (D) have been recorded; I–V are constancy classes (20% intervals), and approximate Domin ranges are presented in parentheses (after Rodwell 1991a,b, 1992, 1995, 2000). CORINE biotype types are also presented; these are cross-referenced to the main communities (Hill 1996)
NVC  Main communitySubcommunityCORINE biotype
ClassSpeciesDescriptionabcdef
Woodlands and scrub (W)
 W1C Salix cinereaGalium palustre woodlandI (4–6)      C44.921
 W2C Salix cinereaBetula pubescensPhragmites australis woodlandI (1–4)I (3–4)II (1–3)    C44.921
 W2D Salix cinereaBetula pubescensPhragmites australis woodlandII (1–4)II (1–4)II (2)    C44.921
 W3D Salix pentandraCarex rostrata woodlandII (1–3)      C44.923
 W4C Betula pubescensMolinia caerulea woodlandI (2–6)I (3–6)I (2)I (2)   C44.A1
 W4D Betula pubescensMolinia caerulea woodlandII (1–9)IV (4–9)I (1)I (1–3)   C44.A1
 W5C Alnus glutinosaCarex paniculata woodlandI (1)I (1)I (1)I (1)   C44.911
 W5D Alnus glutinosaCarex paniculata woodlandIII (1–4)III (1–4)IV (1–4)III (1–4)   C44.911
 W6D Alnus glutinosaUrtica dioica woodlandII (1–7)I (1–4)II (1)II (1–7)III (2–6)  C44.911 C44.121(b) C41.C2(d)
 W7D Alnus glutinosaFraxinus excelsiorLysimachia nemorum woodlandIII (1–6)I (1–4)II (1–3)IV (1–6)   C44.31
 W8D Fraxinus excelsiorAcer campestreMercurialis perennis woodlandI (1–4)I (1–4)I (1–5) I (1–3)I (1–4)I (1–3)C41.32 C41.41(e) C41.233(f)
 W9D Fraxinus excelsiorSorbus aucupariaMercurialis perennis woodlandII (1–6)III (1–6)I (1–3)    C41.31
 W10D Quercus roburPteridium aquilinumRubus fruticosus woodlandII (1–8)II (1–7)I (2–5)II (1–6)I (1–5)III (1–8) C41.21
 W11D Quercus petraeaBetula pubescensOxalis acetosella woodlandI (1–9)III (1–9)I (1)I (1–5)   C41.532
 W12D Fagus sylvaticaMercurialis perennis woodlandI (1–4)I (1–4)     C41.1311
 W14D Fagus sylvaticaRubus fruticosus woodlandI (2–4)      C41.121
 W15D Fagus sylvaticaDeschampsia flexuosa woodlandI (1–3)II (1–3)I (3)    C41.121
 W16D Quercus spp.–Betula spp.–Deschampsia flexuosa woodlandII (1–8)I (1–6)III (1–8)    C41.52 C41.525(a)
 W17D Quercus petraeaBetula pubescensDicranum majus woodlandI (1–6)I (1–6)II (1–4)I (1–4)I (1–5)  C41.532
 W19D Juniperus communis ssp. communisOxalis acetosella woodlandI (1–4)II (1–4)I (2–4)    C31.88
 W20D Salix lapponumLuzula sylvatica scrubII (1–3)      C31.622
 W25D Pteridium aquilinumRubus fruticosus underscrubI (1–4)I (1–4)I (2)    C31.831
Mires (M)
 M25C Molinia caeruleaPotentilla erecta mireI (3–6)  I (3–6)   C37.312
Heaths (H)
 H18D Vaccinium myrtillusDeschampsia flexuosa heathI (1–4)I (1–4)I (1–3)I (1–3)   C31.212
 H22D Vaccinium myrtillusRubus chamaemorus heathI (1–3)I (1–3)I (1)    C31.2122
Calcifugous grasslands and montane communities (U)
 U13D Deschampsia cespitosaGalium saxatile grasslandI (1–4)II (1–4)     C36.1123
 U16D Luzula sylvaticaVaccinium myrtillus tall-herb communityII (1–4)IV (1–4)I (1–3)I (1–3)   C31.63
 U17D Luzula sylvaticaGeum rivale tall-herb communityI (1–4) I (1)I (1–3)I (1–4)  C31.64
 U18D Cryptogramma crispaAthyrium distentifolium snow-bedII (2)      C36.1125
Swamps and tall-herb fens (S)
 S3D Carex paniculata sedge–swamp Caricetum paniculataeII (2–3)      C53.217
 S6D Carex riparia swamp Caricetum ripariaeI (1)      C53.213
Vegetation of open habitats (OV)
 OV27D Epilobium angustifolium communityI (1–7) I (2–3)IV (1–7)II (1–7)  C87.2 C31.87(c,d)

In the Dryopteris dilatataRubus fruticosus subcommunity (W4a) of Betula pubescensMolinia caerulea woodland (W4), which is co-dominated and protected by Rubus fruticosus, D. dilatata reaches a very high local abundance, up to 90%. In the Dryopteris dilatataDicranum majus subcommunity (U16a), of the Luzula sylvatica–Vaccinium myrtillus community (U16), D. dilatata is a scarce species with patchy distribution, the subcommunity being co-dominated by Vaccinum myrtillus, Oxalis acetosella and Deschampsia cespitosa. In the Rubus fruticosus agg.–Dryopteris dilatata subcommunity (OV27c) of the Epilobium angustifolium community (OV27), D. dilatata is locally abundant, co-dominant with Chamerion (Epilobium) angustifolium and Rubus fruticosus agg.

In Alnus-woodland communities, Alnus glutinosaCarex paniculata (W5) and Alnus glutinosaFraxinus excelsiorLysimachia nemorum woodlands (W7), D. dilatata reaches its highest frequency, being common throughout both communities and locally constant in Lysimachia vulgaris (W5b) and Deschampsia cespitosa subcommunities (W7c). Dryopteris dilatata occurs occasionally in various woodland communities, summarized in Table 1.

Dryopteris dilatata is a very frequent species in conifer plantations in the British Isles, where it may sometimes be dominant or the only species in deep shade (Chater 2010). In swamps (S3 and S6), felled woodland (OV27), montane heaths, grasslands and ungrazed cliff ledges (H18, H22, U13, U16, U17, U18), D. dilatata is a sparse species with a low frequency, although it can also be locally frequent (U16a, OV27c), as described above.

In Central Europe, in contrast to the British Isles, D. dilatata is most common not only in montane Fagus sylvatica (Fagion sylvaticae) and Abies alba (Vaccinio-Abietion) woodlands, but also in Picea abies (Vaccinio-Piceion) woodlands, Pinus cembra and mountain dwarf shrub heaths (Rhododendro-Vaccinion), and in tall perennial herb and shrub communities (Adenostylion alliariae). In lowlands, D. dilatata is less common, and it is rare in xerothermic communities (Dostál, Fraser-Jenkins & Reichstein 1984; Ellenberg 1988). In planted Pinus sylvestris and Quercus robur forests in The Netherlands, D. dilatata is among most frequent herb species (Dirkse & Daamen 2004). In the Polish Tatra Mountains, D. dilatata occurs in Fagus sylvatica (Dentario glandulosae-Fagetum), Picea abies and Abies alba coniferous forests (Abieti-Picetum, Polysticho-Piceetum and Plagiothecio-Piceetum) (Piękoś-Mirkowa & Miechŏwka 1992).

Dryopteris carthusiana is also primarily a species of woodland communities in the British Isles (Rodwell 1991a,b). It occurs in five communities and nine subcommunities (Table 1), but in most of those it is scarce, with sparse abundance. All communities in which D. carthusiana has been recorded are in the range of damp to wet, mostly with organic soils. D. carthusiana reaches its highest abundance, up to 33%, although with low frequency, in the Salix cinereaGalium palustre woodland community (W1), in the Dryopteris dilatataRubus fruticosus subcommunity (W4a) of Betula pubescensMolinia caerulea woodland (W4) and in the Angelica sylvestris subcommunity (M25c) of Molinia caeruleaPotentilla erecta mire (M25). In the Sphagnum spp. subcommunity (W2b) of Salix cinereaBetula pubescensPhragmites australis woodland (W2), D. carthusiana has the highest frequency (occasional) of occurrence in all subcommunities. In the Alnus glutinosaFilipendula ulmaria subcommunity (W2a) of this community, in the Juncus effusus (W4b) and Sphagnum spp. (W4c) subcommunity of Betula pubescensMolinia caerulea woodland (W4) and in the Alnus glutinosaCarex paniculata woodland community (W5), D. carthusiana is a scarce species with low abundance. It is also recorded in conifer plantations (French, Murphy & Atkinson 1999; Chater 2010), and it even grows on dry soils in Pinus plantations (Crawley 2005).

Outside woodland, D. carthusiana is also found in damp pastures, on wet heathland or moorland, often in flushes, and in blanket bogs; Juncus spp. and Molinia caerulea are characteristic associates in these habitats (Woods 1993; Halliday 1997; French, Murphy & Atkinson 1999; Abbott 2005; Chater 2010).

In Central Europe, D. carthusiana has been recorded in different woodland communities, primarily dominated by Alnus glutinosa (Alnion glutinosae), Alnus incana and Ulmus laevis (Alno-Ulmion), and also in Quercion robori-petraeae and Luzulo-Fagion (Dostál, Fraser-Jenkins & Reichstein 1984; Ellenberg 1988).

In the Polish Tatra Mountains, D. carthusiana is most common in Fagus sylvatica (Dentario glandulosae-Fagetum) forests, but also occurs in coniferous forests with Picea abies and Abies alba (Abieti-Picetum, Polysticho-Piceetum and Plagiothecio-Piceetum), and deciduous forests with Alnus incana (Alnetum incanae and Caltho-Alnetum) (Piękoś-Mirkowa & Miechŏwka 1992).

In planted Pinus sylvestris and Quercus robur forests of The Netherlands, D. carthusiana, like D. dilatata, is among the most frequent herb species (Dirkse & Daamen 2004).

In Finnish deciduous and mixed boreal herb-rich forests, Dryopteris carthusiana has high constancy and reaches its highest frequency in mesic mixed forests dominated by Alnus incana (Hokkanen 2003).

There is insufficient information about the distribution of D. expansa in communities in the British Isles; it is not listed in the floristic tables of Rodwell (1991a,b, 1992, 1995, 2000) because of its low frequency (<5%) or its absence from the samples collected from the communities under study. The low frequency of D. expansa may also to some degree be due to the difficulties of identification of the species (Dines 2002a). D. expansa has frequently been found in Scotland, in communities similar to McVean’s Tall herb association, growing with Athyrium distentifolium (McHaffie 2005). The closest NVC communities to this are the Luzula sylvaticaVaccinium myrtillus tall-herb community (U16), Dryopteris dilatataDicranum majus subcommunity (U16a), and the Cryptogramma crispaAthyrium distentifolium snow-bed community (U18).

In Central Europe, D. expansa is a montane species, spreading up to the subalpine zone, but it occurs mainly in woodlands with Picea abies, Abies alba (Vaccinio-Piceion) and Fagus sylvatica (Fagion communities) (Dostál, Fraser-Jenkins & Reichstein 1984; Ellenberg 1988). In the Polish Tatra Mountains, D. expansa is most common in coniferous woodland communities (Vaccinio-Piceetea) (Piękoś-Mirkowa & Miechŏwka 1992). In Northern Europe, D. expansa occurs in lowlands; for example in Finland the species occurs with high frequency in deciduous and mixed boreal herb-rich forests, and is used as an indicator species for moist, fern-rich Picea abies-dominated forests (Hokkanen 2003).

IV. Response to biotic factors

  1. Top of page
  2. Summary
  3. I. Geographical and altitudinal distribution
  4. II. Habitat
  5. III. Communities
  6. IV. Response to biotic factors
  7. V. Response to environment
  8. VI. Structure and physiology
  9. VII. Phenology
  10. VIII. Reproductive characteristics
  11. IX. Herbivory and disease
  12. X. History
  13. XI. Conservation
  14. Acknowledgements
  15. References

Competitive ability

In the only competition experiment performed with Dryopteris spp. (Rünk, Moora & Zobel 2004), young sporophytes of D. expansa had smaller biomass, frond number and frond length than D. carthusiana and D. dilatata. The response to competition from neighbouring Deschampsia flexuosa individuals differed among the fern species. In D. expansa, a decrease in biomass and frond length was observed at even a low density of neighbours, whereas in D. carthusiana and D. dilatata a negative response occurred only at a high density of competitors. Dryopteris expansa was more vulnerable to competition than D. carthusiana and D. dilatata. Dryopteris carthusiana had a larger biomass allocation to rhizome and to below-ground biomass (rhizome + roots) in general than the other two species, and larger allocation to roots than D. dilatata. For D. expansa and D. dilatata, allocation to below-ground parts decreased at high neighbour density, while in D. dilatata the relative length of the stipe also increased. The rapid decrease in the relative below-ground biomass of D. expansa and D. dilatata with a high density of neighbours may be connected with the relative increase in competition for light under high plant density. Dryopteris carthusiana lacked such a response, perhaps because of tolerance of competition for light. In general, D. dilatata seems to represent the ‘foraging type’ of competitive response (Keddy, Fraser & Wisheu 1998), manifested as the increase in stipe length in the most crowded and shaded conditions. Dryopteris carthusiana evidently represents the transition between the ‘foraging type’ (increased allocation to roots in crowded conditions) and the ‘persistence type’ (high allocation to the rhizome in all neighbour densities).

Allelopathy

Allelopathic effects of sporophyte-frond leachate of Osmunda cinnamomea L. on Dryopteris carthusiana were studied in USA (Wagner & Long 1991). No significant effect on spore germination or on gametophyte survival and growth rate was found.

Relationship with bryophytes

The effect of bryophyte competition may be critical for the survival of fern gametophytes (Gilbert 1970; Cousens, Lacey & Kelly 1985). A three-year study of Dryopteris dilatata, D. carthusiana and Dexpansa sporophytes at boreo-nemoral forest sites showed a differential response of Dryopteris species to bryophyte cover (Rünk, Moora & Zobel 2006). The site with the highest bryophyte cover was the most unfavourable for biomass production all three Dryopteris species, but especially for D. expansa. The population density of D. expansa was lowest at high bryophyte cover, and immature (non-sporulating) individuals were almost absent from the population.

V. Response to environment

  1. Top of page
  2. Summary
  3. I. Geographical and altitudinal distribution
  4. II. Habitat
  5. III. Communities
  6. IV. Response to biotic factors
  7. V. Response to environment
  8. VI. Structure and physiology
  9. VII. Phenology
  10. VIII. Reproductive characteristics
  11. IX. Herbivory and disease
  12. X. History
  13. XI. Conservation
  14. Acknowledgements
  15. References

(A) Gregariousness

Vegetative reproduction in D. dilatata has been shown to be limited in the British Isles (Grime, Hodgson & Hunt 1988), and thus a clumped distribution of young sporophytes can mostly be attributed to availability of ‘safe sites’ for all three life-history stages: spores, gametophytes and sporophytes. A study of D. dilatata in woods near Derby showed clear clumping of sporophytes resulting from environmental heterogeneity, probably associated with the distribution of shrubs (Willmot 1985).

Clumps of sporophytes of D. dilatata and D. carthusiana on small mounds on the forest floor and of D. dilatata around dead wood have been recorded in Switzerland (Seifert 1992). The environmentally mediated clumping of D. expansa has also been observed in Scandinavia (Øllgaard & Tind 1993) and in the case of all three species in eutrophic boreo-nemoral forests in Estonia.

(B) Performance in various habitats

In the British Isles, differences in habitat quality are most easily detectable through effects on the length of fertile fronds in D. dilatata, which may vary considerably, from 7 to 150(180) cm (Clapham, Tutin & Moore 1989), although they are usually 30–100 cm long (Page 1997; Stace 2010). In old woodlands with thin soil and humus layers, atypically small crowns of fertile individuals of D. dilatata occur with short fronds and a long-creeping rhizome with pale scales (Page 1997). In colder climates, near the north-western edge of its distribution (Finland), D. dilatata usually has shorter fronds (to 85 cm long; Widén, Sarvela & Ahti 1967), than in the British Isles.

Lowland plants of D. expansa are the largest (to 100 cm), whereas in montane conditions mature plants of D. expansa with very short fronds, 10–25 cm or even less, have been recorded (Page 1997), as in northern Finland (Widén, Sarvela & Ahti 1967).

The effect of light availability on the size of all three species has been reported, especially for D. expansa, the size of which varied mainly with the degree of exposure in a montane area (Page 1997). Plants were smaller in less vegetated and hence better illuminated habitats.

According to the results of a garden pot experiment on a light-availability gradient (10, 25, 50 and 100% of full daylight), sporophytes of D. carthusiana, D. dilatata and D. expansa grown together performed differently in different light conditions (Rünk & Zobel 2007). D. dilatata was morphologically the most plastic species of the three. Its more plastic biomass allocation strategy could probably underlie the ability of the species to exploit a wider range of light environment, as well as different substrate and humidity conditions than other two species.

The performance of the three species has been investigated in a field experiment (Rünk, Zobel & Zobel 2010), which was performed in three localities in a boreo-nemoral forest in Estonia: the first locality inhabited naturally only by D. carthusiana (soil i), the second by D. carthusiana and D. expansa (soil ii), and the third by all three species (soil iii). Young even-sized sporophytes of the three species were planted in pots in soil from each of the three experimental sites at each locality, giving nine soil × species combinations. The flux of indirect radiation had a positive effect on the performance (mean total biomass) of all three species; plants grew larger under better illumination. Although locality and soil origin had significant effects on the experimental plants, only the soil origin had species-specific effects: it had no effect on growth of D. dilatata, but had significant effects on D. carthusiana and D. expansa, producing more than two-fold differences in growth. Since D. carthusiana grows in all three experimental soils naturally, the specific soil properties, although causing differences in growth, probably do not limit its local distribution. Similarly, soil properties obviously do not limit the local distribution of D. dilatata, as it grew with equal success in all three soils. In contrast, soil origin seems to be most important for D. expansa– its growth was significantly poorer in soil from the site where it was naturally absent. Vulnerability of D. expansa to edaphic conditions may not only limit its performance, but also its local distribution.

(C) Effects of frost, drought, etc

Frost

The three species tolerate a seasonally cold climate differently. Dryopteris dilatata may be winter-green in the British Isles (Clapham, Tutin & Moore 1989), although the fronds usually remain green until the end of October, then die down by December, and plants overwinter with foliage in a senescent condition (Grime, Hodgson & Hunt 1988; Page 1997), as is also the case in Central Europe (Dostál, Fraser-Jenkins & Reichstein 1984) and Scandinavia (Øllgaard & Tind 1993). Developmental stages of the species may show different cold tolerance; in the same habitat, the fronds of large D. dilatata plants were more sensitive to cold and died in late autumn–early winter, while small plants remained winter-green (Willmot 1989). In Central Europe, Fennoscandia (Øllgaard & Tind 1993) and the Baltic States (Eglīte & Šulcs 2000), the fronds covered by snow may stay green through the winter (Dostál, Fraser-Jenkins & Reichstein 1984). On the other hand, spring frost damage has been reported in young fronds (Seifert 1992) in Switzerland, whereas in Estonia late spring frosts may kill all young current year fronds of the species.

In the British Isles, the fronds of D. carthusiana are the least cold-tolerant of the three species, usually dying rapidly with the first frosts in October, and overwinter in a senescent condition (Page 1997). In Scandinavia and the Baltic States, D. carthusiana may be partly winter-green, with fertile fronds usually withering in the autumn, and sterile ones mostly overwintering (Widén, Sarvela & Ahti 1967; Eglīte & Šulcs 2000; Sarvela 2000). Again, in Switzerland, spring frost damage has been reported in young fronds of D. carthusiana (Seifert 1992).

Dryopteris expansa is thought to be the most cold-tolerant of the three species in the British Isles (Page 1997); its rhizome has survived −30 °C and its soft-textured fronds −7 °C (Sato & Sakai 1981). In the British Isles, the cold tolerance of fronds often enables D. expansa to remain green longer than other two species, perhaps until the November or in very sheltered sites even through the winter (Rich & Jermy 1998), although usually the fronds overwinter in a senescent condition (Page 1997). In the colder climate of Fennoscandia (Øllgaard & Tind 1993; Sarvela 2000) and in the mountains of Central Europe (Dostál, Fraser-Jenkins & Reichstein 1984), the fronds die back in the autumn, after the first frost. In Norway and southern Finland, however, the fronds may remain green until spring (Sarvela 2000). In northern Japan (Hokkaido), fertile plants of D. expansa are summer-green (Sato 1982), but die away in October, as in Central Europe. Small individuals can remain green in winter (Sato 1983), similar to D. dilatata in the British Isles.

Drought

The three species are differentially sensitive to soil moisture and atmospheric humidity. The laminae of D. dilatata are more drought-tolerant than the other two species (Øllgaard & Tind 1993). The susceptibility of D. carthusiana to low air humidity is probably connected with its preference for habitats with a high ground water level (Page 1997; Dines 2002b), although it has thicker fronds than D. expansa and in short droughts is probably less sensitive to drying. Thin, membranous and delicate laminae make D. expansa highly sensitive to drying.

Fire

Although fire may kill the fronds of D. carthusiana and D. expansa, rhizomes of both species are able to survive single fire events (Ahlgren 1960; Neumann & Dickmann 2001). Investigation of the long-term effects of fire on the boreal forest understory (Québec, Canada) has shown that D. carthusiana was generally more abundant in the earlier stages of post-fire succession (De Grandpré, Gagnon & Bergeron 1993).

The effect of fire depended greatly on the season, the frequency and intensity of burning and the presence of additional disturbances. Clear-cutting and yearly spring burning over eleven years killed D. expansa in all experimental plots in a Picea glauca × P. engelmannii forest (British Columbia, Canada) and prevented its re-establishment. Conversely, it survived in autumn-burned plots, and there was no difference in its cover between unburned and autumn-burned plots after eleven years of treatment (Hamilton & Peterson 2003). D. expansa is known to survive fire and reproduce vegetatively after a single slash-burn (Hamilton 2006a,b). A decrease in the cover of D. expansa during the 5 years following a fire may still occur, probably because of a competitive effect from the regeneration of woody plants (Oliver 1981).

VI. Structure and physiology

  1. Top of page
  2. Summary
  3. I. Geographical and altitudinal distribution
  4. II. Habitat
  5. III. Communities
  6. IV. Response to biotic factors
  7. V. Response to environment
  8. VI. Structure and physiology
  9. VII. Phenology
  10. VIII. Reproductive characteristics
  11. IX. Herbivory and disease
  12. X. History
  13. XI. Conservation
  14. Acknowledgements
  15. References

(A) Morphology

The rhizome

The rhizomes of all three species are covered with persistent stipe bases and triangular-lanceolate scales of similar shape (Crabbe, Jermy & Walker 1970), but of different colours. Dryopteris dilatata has a short, erect, ascending or decumbent stocky rhizome, with a domed growing point and many crosiers (young, unexpanded fronds). It usually has scales with pale brown edges and a broad dark-brown or blackish central longitudinal stripe (Clapham, Tutin & Moore 1989; Page 1997; Rich & Jermy 1998). The anatomical structure of rhizomes of all three species includes intracellular spaces with internal hairs, 80–100 μm long in the case of D. dilatata (Widén, Sarvela & Ahti 1967). Rhizomes of D. carthusiana are either small, short and decumbent or longer and more slenderly prostrate with occasional branching. The growing point of the rhizome is flat and usually supports four bright green crosiers in a cruciate arrangement (one above, one below and one to each side). Rhizome scales of D. carthusiana are uniformly pale brown without a central dark stripe, as on the stipe (Clapham, Tutin & Moore 1989; Page 1997; Rich & Jermy 1998). The rhizome internal hairs are 80–100 μm long (Widén, Sarvela & Ahti 1967). D. expansa has an erect, short, sturdy rhizome, similar to that of D. dilatata, which in older individuals may be ascending or decumbent. Scales of D. expansa are typically uniformly reddish brown, occasionally with a darker central stripe or base. The rhizome growing point of D. expansa is domed, with many crosiers (Clapham, Tutin & Moore 1989; Page 1997; Rich & Jermy 1998). Its rhizome internal hairs are shorter than those of the other two species at 60–80 μm, but more frequent (Widén, Sarvela & Ahti 1967).

Fronds

Under laboratory conditions, the first fronds in all three species appeared approximately 28 weeks after the sowing of spores. It took more than another 14 weeks for fronds of species-specific morphology to emerge (Fig. 8).

image

Figure 8.  Silhouettes of successive early fronds, from first frond to age 14 weeks: (a) Dryopteris dilatata; (b) D. carthusiana; and (c) D. expansa.

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The arching fronds of D. dilatata are arranged quite regularly, forming more or less funnel-shaped groups, so-called ‘shuttlecocks’ (Rich & Jermy 1998). The stipe length in D. dilatata may range from 1/4 of lamina length to the whole lamina length (Page 1997; Stace 2010). Laminae of D. dilatata are usually olive- or blue-green and slightly leathery in texture. The stipes are covered with scales, which are very dense at the base and less dense above. The scales are broadly ovate-deltate with long acuminate apex, almost uniformly dark brown (blackish) or usually bicoloured, with a distinctive wide dark brown or blackish longitudinal stripe in the centre and pale brown edges (Page 1997; Rich & Jermy 1998). However, in juveniles such as small upland plants (Crabbe, Jermy & Walker 1970; Stace 2010) or in offshoots, the scales may be uniformly pale and more flaccid (Page 1997). In Fennoscandia, the scale margins are fringed with short-stalked glands (Sarvela 2000). The laminae are covered with trichomes (glands and/or glandular hairs) and scales of varying density. In Fennoscandia, in D. dilatata the lower surface of the laminae is covered quite densely with narrow, fibrillose scales (Widén, Sarvela & Ahti 1967; Øllgaard & Tind 1993; Sarvela 2000). Dryopteris dilatata has stomata 48.5–54.2 μm long on average (Piękoś-Mirkowa 1979; Seifert 1992).

The fronds of D. carthusiana are the most irregularly arranged of the three, forming sparse to thick groups, not ‘shuttlecocks’. Erect to ascending individual fronds usually have slightly backward-arching apices. The stipe length of D. carthusiana may range from 1/4 of lamina length to the whole lamina length. Laminae may vary from yellowish to mid-green, with a firm, but delicate texture. The stipes are covered with thin, uniformly pale brown, broadly lanceolate scales, often with incurved margins; sometimes stipes are more scaly at the base, with only scattered or sparse scales on the upper part and rachis (Rich & Jermy 1998). In Fennoscandia, the scale margins are fringed with short-stalked glands (Sarvela 2000). The laminae are covered with trichomes and scales of varying density. In Fennoscandia, narrow fibrillose scales on the lower surface of the laminae have also been sometimes recorded in D. carthusiana (Widén, Sarvela & Ahti 1967; Øllgaard & Tind 1993; Sarvela 2000). It has the longest stomata of the three species, 54.2–57.1 μm on average (Piękoś-Mirkowa 1979; Seifert 1992). The stomatal length of D. carthusiana has been shown to increase with elevation (Holland & Richardson 2009).

The fronds of D. expansa arise in regular sparse ‘shuttlecocks’ of rigidly ascending to spreading, only slightly arched fronds (Page 1997; Rich & Jermy 1998). The stipe length may range from 1/2 to whole lamina length (Page 1997; Stace 2010). D. expansa has soft laminae, which are usually mid to yellowish green. The stipes are densely scaly at the base but more sparsely so above. Scales are broadly ovate-deltate often with abruptely acuminate apex, and variable in colour, from uniformly tan (but not as pale as in D. carthusiana; Page 1997) to more typically reddish brown, or bicoloured, with a darker brown central stripe or base (Rich & Jermy 1998). Bullate scales have also been found on the stipes of D. expansa (Crabbe, Jermy & Walker 1970). In Fennoscandia, the scale margins are fringed with short-stalked glands (Sarvela 2000). The laminae are covered with trichomes and scales of varying density. Scattered narrow fibrillose scales on the lower surface of the laminae have been recorded D. expansa (Widén, Sarvela & Ahti 1967; Øllgaard & Tind 1993; Sarvela 2000). Dryopteris expansa has the shortest mean stomatal length (47.0–47.6 μm) of the three species (Piękoś-Mirkowa 1979; Seifert 1992).

(B) Mycorrhiza

The sporophytes of all three species have arbuscular mycorrhiza (AM). Hyphae, arbuscules and vesicles have all been observed in roots collected from different forest sites in Estonia during one growing season in 2004. In the British Isles, AM have been found in the roots of D. dilatata (Harley & Harley 1987). AM have been observed in D. carthusiana in southern Ontario, Canada (Berch & Kendrick 1982) and in France (Boullard 1951). The mycorrhiza of D. carthusiana has been studied in greater detail in Poland (Truszkowska 1953; Dominik & Pachlewski 1956; Boullard & Dominik 1960; Dominik 1961; Dominik & Wojciechowska 1961; Unrug & Turnau 1999). This work has indicated that D. carthusiana is facultatively mycorrhizal, with a varying degree of root colonization. Two morphotypes of AM, Arum-type and Paris-type, were observed. Additionally, hyphal connections have been found between the roots of D. carthusiana and the gametophytes of liverworts (Conocephalum conicum and Pellia endiviifolia), via Glomus tenuis (Turnau, Ronikier & Unrug 1999). AM have also been observed in D. expansa in southern Ontario, Canada (Berch & Kendrick 1982). Benefit from mycorrhizal infection, in terms of shoot growth in phosphorus-deficient soils, has been demonstrated experimentally in another member of genus Dryopteris, D. filix-mas (Cooper 1977).

(C) Perennation: reproduction

Although production of spores is common (Grime, Hodgson & Hunt 1988; Page 1997), and D. dilatata produces them in large numbers, establishment of ferns is not a frequent event, because of the high mortality of spores and gametophytes (Page 2002). Young sporophytes of D. dilatata also have a high mortality, and even those few individuals that survive to maturity may only live for a short time. The large number of young sporophytes found in populations of D. dilatata in the British Isles demonstrates the significance of sexual reproduction for the species, even if the recruitment of young sporophytes does not take place every year. Vegetative reproduction, notably the development of small secondary crowns, is less usual for this species (Willmot 1985). In Switzerland, D. dilatata produces rhizome branches and stolons. Closely situated secondary crowns develop from rhizome branches, and elongated stolons give rise to offspring (Seifert 1992). In Estonia, in a 2-year pot experiment vegetative propagation has been observed in young sporophytes of D. dilatata and D. carthusiana; in the case of D. dilatata, this amounted to 0.07 vegetative offspring per individual (Rünk & Zobel 2009).

In Central Europe, similar vegetative propagation of D. carthusiana has been recorded, producing secondary crowns and offspring (Seifert 1992). In Estonia, in a pot experiment the mean number of vegetative offspring per individual was 1.07, higher than in D. dilatata (Rünk & Zobel 2009).

(D) Chromosomes

Two different forms of D. dilatata were examined by Manton (1950): the tetraploid, so-called ‘normal British’ form with 2= 164, and diploid forms from Switzerland and Scandinavia with 2n = 82. The same chromosome number (2n = 82) for British diploid material (D. dilatata var. alpina) from Scotland was confirmed by Walker (1955). This diploid form subsequently was separated from D. dilatata (2= 164) as a new taxon (Walker 1961) and has been recognized as D. expansa (2n = 82) since 1977 (Fraser-Jenkins & Jermy 1977). Manton (1950) first recorded 2n = 164 in the sporophyte of D. carthusiana. Numerous cytological studies carried out on material from different regions of Europe (Manton & Walker 1954; Walker 1955; Döpp 1958; Sorsa 1958, 1963; Döpp & Gätzi 1964; Simon & Vida 1966; Widén & Sorsa 1966, 1969; Sorsa & Widén 1968; Piękoś & Passakas 1973; Piękoś-Mirkowa 1979; Gibby 1983) and North America (Manton & Walker 1953; Walker 1961; Tryon & Britton 1966) have confirmed tetraploidy (2n = 164) in D. dilatata and D. carthusiana, as well as diploidy in D. expansa (2n = 82).

(E) Physiological data

Response to shade

The results of a study in which the three species were grown on a light-availability gradient in an experimental garden (Rünk & Zobel 2007) were generally in agreement with the distribution of the three species in the British Isles (see II A). There were clear interspecific differences in total plant growth and biomass allocation in different shade treatments. Furthermore, two distinct strategies of biomass allocation in response to shade were shown by D. dilatata and D. carthusiana, with D. expansa demonstrating intermediate behaviour. The main differences between the species were in the fractions of biomass stored in fronds and rhizomes (or below-ground organs).

Dryopteris dilatata was the most shade-tolerant, with growth not significantly affected by shade. Specific leaf (lamina) area (SLA) showed the expected plastic responses to shade – laminae grew thinner and had a relatively larger area under decreased light flux. However, the stipe length increased and the lamina/stipe length ratio decreased with increased level of shade, in this species only. This was associated with a plastic switch towards decreased resource storage in its rhizome (and other below-ground biomass) and simultaneous increase in relative frond biomass with increased shade. It was able to reduce its allocation to rhizomes more than two-fold from 50 to 10% light.

Dryopteris carthusiana performed better than the other two species in less shaded conditions (50 and 25% daylight), but not in deeper shade (10%), where its biomass production was only 34–40% of that in higher light. SLA again showed the usual plastic response to shade. Dryopteris carthusiana, unlike D. dilatata, allocated a near-constant share of resources to its rhizomes and progressively increased relative root and below-ground biomass with decreasing light (on account of decreasing relative frond biomass).

Dryopteris expansa was the least shade-tolerant species. Its biomass production was highest in 50% light but decreased sharply in more shaded conditions (25% light) and remained similarly low in the stronger shade (10% light). SLA showed a plastic response to shade similar to other two species. In D. expansa, a more or less constant proportion of biomass was allocated to fronds and below-ground organs, the increase in relative root mass with decreased light being compensated by a slight decrease in relative stipe and rhizome mass.

The three species differed also in their ontogenetic morphological plasticity in response to shade. When the effect of plant size (biomass) was removed, D. dilatata appeared to be the most plastic of the three. In four traits (rhizome mass, frond/below-ground biomass ratio, stipe length and SLA), its degree of ontogenetic plasticity was significantly higher than that of D. expansa and D. carthusiana (Rünk & Zobel 2007).

Energy content

The energy content of D. dilatata fronds varied from 19.4 to 20.9 kJ g−1 dry matter in response to different soil, light and vegetation conditions in four different types of natural Picea abies forest of the Tatra Mountains (Kukla, Kuklová & Schieber 2004).

(F) Biochemical data

Secondary compounds

Since the 1960s, the phloroglucinol composition of D. dilatata, D. carthusiana and D. expansa has been studied for systematic and evolutionary significance (see references in Widén et al. 1999). The presence or absence of phloroglucinols (a mixture of phenolic compounds, most of which have antihelminthic activity; Widén, Sarvela & Britton 1983) produced by the internal glands of rhizomes or the petiolar bases of the plants appeared to be a taxonomic characteristic of Dryopteris species in Europe, northern America and Asia (Widén, Sarvela & Ahti 1967; Widén & Britton 1969, 1971a,b,c; Widén, Sorsa & Sarvela 1970). The phloroglucinols detected in the three species are summarized in Table 2.

Table 2.   The reported composition of the main phloroglycinols of Dryopteris dilatata, D. carthusiana and D. expansa
Phloroglycinol derivative D. carthusiana D. dilatata D. expansa
Albaspidin1, 2*, 32*, 4, 51, 2*, 6, 7, 8, 9, 10, 11
Aspidin1, 2*, 3, 51, 2*, 4, 5, 12*1, 2*, 5, 8, 9, 11
Aspidinol1, 2*, 3, 51, 2*, 4, 51, 2*, 5, 8, 9
Desaspidin1, 2*, 31, 5, 12*1, 2*, 6, 7, 8, 9, 10, 11
Filixic acid 1, 58
Flavaspidic acid1, 2*, 3, 51, 2*, 4, 5, 12*1, 2*, 5, 6, 7, 8, 9, 10, 11
Para-aspidin2*, 32*, 42*, 8, 9, 10, 11
Phloropyron2*, 32*, 41, 2*, 8, 9
Trisdesaspidin2*, 3 2*, 8, 9, 10, 11
Trisflavaspidic acid  10

Flavonoid compounds have been found in the fronds of D. dilatata (cyanidin and delphinidin) and D. carthusiana (cyanidin) collected from Sweden (Fredga & Bendz 1966) and in both species (leucoanthocyanins and kaemferol) from the Alps (Voirin 1967). Additionally, the latter survey found traces of quercetin in D. carthusiana. One of the three known betaine lipids diacylglyceryl-N,N,N-trimethylhomoserine (DGTS) has been reported in the fronds of D. carthusiana from the Samara region of Russia (Rozenstvet et al. 2001). Kaemferol and quercetin at low concentrations have also been reported in D. carthusiana in northern America (Petersen & Fairbrothers 1983), as well as a derivative of caffeic acid in D. expansa fronds there (Bohm 1968). Various hydrocarbons, fatty acids and terpenoids have been detected in the excretions of the internal glandular hairs of D. carthusiana and D. expansa (Huhtikangas, Huurre & Partanen 1980; Huhtikangas et al. 1983). D. carthusiana is reported to have been used as an antihelminthic in the Baltic countries (Maizīte 1937; Vaga & Eichwald 1960), as has D. expansa (Vaga & Eichwald 1960).

Cyanogenesis

Cyanogenesis is apparently absent in D. dilatata (Ottosson & Anderson 1983a) and D. carthusiana (Harper, Cooper-Driver & Swain 1976).

VII. Phenology

  1. Top of page
  2. Summary
  3. I. Geographical and altitudinal distribution
  4. II. Habitat
  5. III. Communities
  6. IV. Response to biotic factors
  7. V. Response to environment
  8. VI. Structure and physiology
  9. VII. Phenology
  10. VIII. Reproductive characteristics
  11. IX. Herbivory and disease
  12. X. History
  13. XI. Conservation
  14. Acknowledgements
  15. References

Appearance and growth of shoots

In the British Isles, new fronds on large plants of D. dilatata appear all together in a single cohort (Willmot 1989) from April to May and mature by June (Page 1997). There may be 40–50 frond primordia ready to develop in a terminal bud of a large sporophyte of D. dilatata (Wardlaw & Sharma 1963). In an average year, approximately 10 fronds develop fully, that is, in any year there is a reserve of fronds for the next 4–5 years. Pinna primordia of the next year’s fronds are already distinguishable in January, and those of pinnules at the end of February. At the same time, sporangia in the current year’s circinnate fronds are developing. The next year’s fronds continue developing during the spring and summer, and sori begin to form in September. Although the formation of sori continues until March, most of the next year’s fronds and even the fronds of the year after next are able to uncoil in the current summer in the event of defoliation (by herbivory, freezing etc.). The size and fertility of those fronds depend on the extent of the loss of the current year’s fronds (Wardlaw & Sharma 1963).

The growth of D. carthusiana begins in the second half of May, and the new fronds have usually matured by the end of June. The growth of D. expansa begins in the second half of May, like in D. carthusiana, while the new fronds expand over a longer period, from May to late July (Page 1997).

In Central Europe, D. dilatata and D. carthusiana have tightly coiled crosiers on the rhizome in autumn that are ready for growth (Seifert 1992). Most of them uncoil the next spring. In the case of abnormal weather conditions in autumn (mild autumn with abnormally high air temperature), old fronds remain green for a longer period and the young, next year’s fronds, begin to uncoil. The same phenomenon has been observed in all three species in Estonia.

Sporulation

The three species differ in the timing of spore ripening and shedding. Dryopteris dilatata sheds its spores over a period of two and a half months: spores ripen by July and have usually been shed by the beginning of September (Page 1997). In Central Europe, D. dilatata largely sheds its spores in the same period as in the British Isles, that is in July and August (Dostál, Fraser-Jenkins & Reichstein 1984). The sori on the same frond may ripen gradually, and there may be ripe and unripe sori at the same time (Seifert 1992).

Dryopteris carthusiana sheds its spores over two and a half months, similarly to D. dilatata, but about a month later, from the end of July to the middle of October (Page 1997). In Central Europe, spores of D. carthusiana may be ripe earlier than in the British Isles, as early as July (Dostál, Fraser-Jenkins & Reichstein 1984). Gradual ripening of the spores has also been recorded in D. carthusiana (Seifert 1992). Although most of the spores probably disperse soon after ripening, in D. carthusiana in northern America there may still be spores in sori that are able to germinate by March (Farrar 1976).

Dryopteris expansa sheds its spores over the shortest period, approximately 2 months, from August to October (the latest of the three species). In Central Europe, spores of the species may be ripe by July (Dostál, Fraser-Jenkins & Reichstein 1984). In northern Japan (Hokkaido), the spore dispersal period of D. expansa is in July and August (Sato 1982).

VIII. Reproductive characteristics

  1. Top of page
  2. Summary
  3. I. Geographical and altitudinal distribution
  4. II. Habitat
  5. III. Communities
  6. IV. Response to biotic factors
  7. V. Response to environment
  8. VI. Structure and physiology
  9. VII. Phenology
  10. VIII. Reproductive characteristics
  11. IX. Herbivory and disease
  12. X. History
  13. XI. Conservation
  14. Acknowledgements
  15. References

(A) Reproduction of sporophyte

The undersides of all pinnae of fertile fronds of D. dilatata are generally covered by sori (Page 1997). In Central Europe, D. dilatata is more fertile than D. carthusiana– it has more fertile individuals, more fertile fronds per individual and more sori per frond (Seifert 1992). Near the edge of its distribution in northern Europe, 3 years of observations in permanent plots showed a similar result: D. dilatata had significantly more fertile fronds per generative individual than D. carthusiana (Rünk, Moora & Zobel 2006).

Weak frond dimorphism has been observed only for D. carthusiana; fertile individuals frequently have some sterile fronds alongside the fertile ones (Page 1997), which are usually slightly smaller (Øllgaard & Tind 1993). Also, up to three basal pairs of pinnae might lack sori completely (Dostál, Fraser-Jenkins & Reichstein 1984; Seifert 1992).

In D. expansa, the undersides of all pinnae of fertile fronds are generally also entirely covered by sori (Øllgaard & Tind 1993; Page 1997).

(B) Discharge and dispersal of spores

Although D. dilatata produces c. 13.5 million wind-dispersed spores per frond (Page 1979), and D. carthusiana 150 million spores per plant in the USA (Peck, Peck & Farrar 1990), most of them are deposited within 3 m of the source sporophyte (Glaves 1991). According to a study performed in Iowa, USA (Farrar 1976), not all spores of D. carthusiana are shed by winter or even by the next spring. Sporangia continue to open and shed spores during the winter, until the following March. D. carthusiana had 10 000–100 000 spores per frond in December, and the number was approximately the same in overwintered fronds in March.

(C) Germination of spores

Spores of D. dilatata and D. carthusiana (originating from Switzerland) had similar germination percentages on agar after 1 year of storage at room temperature (85 and 87% respectively). Treatment with hypochlorite affected the germination of spores differently and depended on the timing of the treatment. Germination decreased in D. carthusiana and increased in D. dilatata as a result of treatment with sodium hypochlorite (Seifert 1992).

Different germination rates of D. carthusiana spores collected at different times were observed in an experiment performed in Iowa, USA (Farrar 1976). Spores of D. carthusiana collected in December had a germination probability of 52%, while those collected the following March had a germination probability of 84%. Spores of D. carthusiana (collected from USA, Cincinnati) also survived a brief low temperature treatment with liquid nitrogen and were able to germinate afterwards (Pence 2000).

An experimental study of D. expansa (Sheffield et al. 2001) revealed an effect of germination media on spore germination rates. The germination of 2-year-stored spores of D. expansa (collected from the British Isles) was 58% on media without sucrose, 61% on media containing 0.05 m sucrose and significantly higher (66%) if germinated on media containing higher concentration, 0.2 m sucrose.

(D) Gametophyte morphology

The spores of Dryopteris dilatata are blackish brown to black, those of D. carthusiana brown to dark brown, whereas those of D. expansa are pale or straw-coloured to reddish amber-brown (Dostál, Fraser-Jenkins & Reichstein 1984; Grime, Hodgson & Hunt 1988; Sarvela 2000). All three species have similar monolete, elliptical (ovoid to bean shaped) spores (Dostál, Fraser-Jenkins & Reichstein 1984) with a perispore variably folded and covered with protuberances. The spores are highly variable in size: D. dilatata spores (with perispore) range from 30–52 × 38–70 μm; D. carthusiana 20–52 μm × 38–70 μm and D. expansa 31–56 × 44–75 μm (Widén, Sarvela & Ahti 1967; Piękoś-Mirkowa 1979; Dostál, Fraser-Jenkins & Reichstein 1984; Grime, Hodgson & Hunt 1988; Seifert 1992).

In all three species, a uniseriate, elongated, multicellular filament develops first from the spore. Subsequent planar growth leads to a flat, cordate gametophyte (Piękoś-Mirkowa 1979). The growth and development of the gametophyte (prothallus) of D. carthusiana and D. dilatata has been studied extensively in culture (Seifert 1992). The continuing growth of a young gametophyte (cordate form) leads to the formation of marginal proliferations, first small and slightly lobed (lobed form), which eventually become numerous plate-like convoluted outgrowths forming a rosette-shaped thallus (Seifert 1992). After 20 weeks of growth on soil, isolated gametophytes of D. dilatata had a width of c. 10 mm, and those of D. carthusiana 8 mm.

(E) Reproduction of gametophyte

Isolated prothalli (gametophytes) D. dilatata and D. carthusiana develop antheridia first, that is, all small gametophytes are male. All the gametophytes of both species growing on agar have archegonia by the ninth week after spore sowing, whereas archegonia appear later on soil and wood substrates. The new sporophytes of both species appear most rapidly on wood, and development on agar and soil takes longer. Vegetative reproduction and dorsal stalk-like outgrowths of gametophytes have been recorded in both species (Seifert 1992). In D. carthusiana, the effect of the substrate on the development of gametophytes has also been found in natural conditions (Flinn 2007).

Gametophytes of homosporous ferns are potentially hermaphroditic, that is able to produce both archegonia and antheridia. Antheridiogens are hormone-like substances produced by the mature female gametophyte that stimulate the development of antheridia on neighbouring immature gametophytes (Schneller 2008). Experimental results for D. dilatata show a possible response to antheridiogen (Barker 1988). However, neither D. carthusiana (Seifert 1992) nor D. expansa produce or respond to antheridiogens (Voeller 1964).

High intragametophytic selfing (78%) has been observed in D. carthusiana but it was lower (35%) in D. dilatata (Seifert 1992). Intragametophytic selfing rates in D. carthusiana reported from North America are variable, ranging from 14 to 86% (Cousens 1975; Peck 1985; Flinn 2006; Somer et al. 2010). Enzyme electrophoresis studies of D. expansa in the USA (Soltis & Soltis 1987) revealed substantial variation in the inbreeding coefficient (or fixation index, F) among natural populations, from −0.014 to 0.745 (mean = 0.335). F values, can range from −1 (indicating extreme heterozygote excess) to +1 (indicating no observed heterozygotes). On the basis of the statistically significant F values (from 0.262 to 0.745) indicating heterozygote deficiencies and the possibility of inbreeding, it has been suggested that D. expansa has a mixed mating system (neither outcrossing nor selfing predominates; Lande & Schemske 1985). Substantial variation in F values among natural populations investigated in this study (Soltis & Soltis 1987) has been considered an indicator of high interpopulational variation in mating system. Furthermore, the proportion of outcrossing and selfing is related to sporophyte density – the higher the density of sporophytes, the more outcrossing. Simple polyembryony (more than one sporophyte on a gametophyte, each derived from a separate archegonium) has also been observed in D. dilatata and D. carthusiana in experimental conditions (Seifert 1992).

(F) Ecology of gametophyte

Seifert (1992) has shown that development of new sporophytes in D. dilatata and D. carthusiana is possible in the same autumn as release the spores. In this case, young sporophytes will overwinter, still attached to the gametophytes. In overwintered gametophytes, fertilization may occur in spring and sporophytes will form subsequently. Gametophytes of D. dilatata and D. carthusiana growing on wood have been seen to successfully overwinter in Central Europe. High frost resistance of gametophytes of D. expansa has been noted in Japan (Sato & Sakai 1981; Sato 1982).

As in any species with free-living alternating generations, the distribution of D. dilatata is determined by the environmental requirements of both generations, but primarily of the gametophytes (Grime, Hodgson & Hunt 1988). The size of gametophytes in D. dilatata and D. carthusiana is negatively density-dependent. Seifert (1992) reported that the growth media and the density of gametophytes affected sex expression, gametophyte development rate and the intragametophytic selfing rate. Spore-sowing experiments with D. carthusiana (Flinn 2007) demonstrated a positive effect of elevated humidity on the production and growth of gametophytes in the wild. Mineral soil has been reported as the best substrate for gametophyte formation and growth, followed by humus and leaf litter.

(G) Hybrids

Natural hybrids between all three species, as well as hybrids of D. carthusiana with D. filix-mas (L.) Schott and D. cristata (Table 3), occur in the British Isles (Stace 2010). Hybrids are morphologically generally intermediate between the parental species (Page 1997) or more similar to the parent of higher ploidy (Sarvela 2000), D. dilatata, D. carthusiana, D. cristata or D. filix-mas.

Table 3.   Hybrids of Dryopteris carthusiana, D. dilatata and D. expansa
Parental speciesHybrid nameAuthorityCommon nameNumber of 10 × 10-km squares recorded for the British Isles
  1. The square counts are taken from the BSBI Vascular Plant Database, Biological Records Centre, and are based on a recent revision of hybrid records by D.A. Pearman and C.D. Preston.

D. dilatata D. expansa D. × ambroseaeFraser-Jenk. & JermyGibby’s Hybrid Buckler-fern 21
D. carthusiana D. dilatata D. × deweveri(J.T. Jansen) Jansen & Wacht.Hybrid Narrow Buckler-fern243
D. carthusiana D. expansa D. × sarvelaeFraser-Jenk. & JermyKintyre Buckler-fern  4
D. filix-mas D. carthusiana D. × brathaicaFraser-Jenk & Reichst.Brathay Fern  1
D. cristata D. carthusiana D. × uliginosa(A. Braun ex Döll) Kuntze ex DruceHybrid Fen Buckler-fern 19
D. dilatata × D. expansa = D. × ambrosae

Plants are triploid (2n = 123), forming 41 bivalents and 41 univalents at meiosis (Walker 1955; Gibby & Walker 1977). Spores are deformed and entirely abortive, and often the whole sporangia appear sparse and abortive as well (Page 1997; Sarvela 2000). The hybrid has been found in scattered localities in Scotland and northern England, as scattered individuals in mixed populations of both parents (Page 1997).

D. carthusiana × D. dilatata = D. × deweveri

Plants are tetraploid (2n = 164). At meiosis, they show 41 bivalents and 82 univalents and spores are mostly abortive. The hybrid is not uncommon throughout the British Isles and can be found in scattered localities in mixed populations of both parents (Page 1997).

D. carthusiana × D. expansa = D. × sarvelae

Plants are triploid (2n = 123). No pairing occurs at meiosis and spores are entirely abortive (Page 1997; Sarvela 2000). This hybrid is known only from four localities (Table 3), in damp woodland in Scotland and northern England, but at one of these sites is the dominant taxon with about 100 individuals (M. Gibby, pers. comm.).

D. filix-mas × D. carthusiana = D. × brathaica

Plants are tetraploid (2n = c. 164), showing only a little pairing at very irregular meiosis (Manton 1950). The spores are entirely abortive (Page 1997). This extremely rare natural hybrid has only ever been found once, in c.1854 in Brathay Wood on the NW side of Lake Windermere, in Cumbria (Fraser-Jenkins & Reichstein 1977).

D. carthusiana × D. cristata = D. × uliginosa

Plants are tetraploid (2n = 164) chromosomes, showing c. 41 bivalents and 82 univalents at meiosis. The spores are totally abortive (Page 1997; Sarvela 2000). This hybrid, though always rare in the British Isles, was once more widely distributed but is now restricted to a small area in Norfolk (Cheffings & Farrell 2005), in a shaded fenland habitat similar to that of D. cristata (Page 1997).

IX. Herbivory and disease

  1. Top of page
  2. Summary
  3. I. Geographical and altitudinal distribution
  4. II. Habitat
  5. III. Communities
  6. IV. Response to biotic factors
  7. V. Response to environment
  8. VI. Structure and physiology
  9. VII. Phenology
  10. VIII. Reproductive characteristics
  11. IX. Herbivory and disease
  12. X. History
  13. XI. Conservation
  14. Acknowledgements
  15. References

(A) Animal feeders and parasites

Arthropods

Of these three species of Dryopteris, in the British Isles the greatest number of arthropod herbivores, all oligophagous fern-feeders, has been found in D. dilatata (BRC Database of Insects and their Food Plants 2011). The adults and larvae of the heteropteran bug Monalocoris filicis (L.) (Hemiptera: Miridae) and the larvae of moth Psychoides filicivora (Meyrick) (Lepidoptera: Tineidae) feed on fern sporangia and sori. Monalocoris filicis occurs on D. dilatata from the end of June to September, whereas Psychoides filicivora attacks for a shorter time, only in July. Eupteryx filicum (Newman) (Hemiptera: Cicadellidae), a leafhopper bug, and Chirosia parvicornis (Zetterstedt) (Diptera: Anthomyiidae), a fly, are leaf-eating insects. Adults of Eupteryx filicum attack plants in August, and damaged white areas are observable on fronds. Chirosia parvicornis larvae occur on D. dilatata from June to August, damaging frond-tips and creating galls (Ottosson & Anderson 1983a,b).

Dryopteris carthusiana has been recorded in the British Isles as a host only of the micro-moth Udea decrepitalis (Herrich-Schaffer) (Lepidoptera: Pyralidae), whose larvae feed on the fronds (Emmet 1979; Emmet & Heath 1991).

Two different aphid species (Hemiptera: Aphididae), Utamphorophora filicis Miyazaki and Amphorophora ampullata Buckton, have been found to feed on D. expansa fronds in Japan (Miyazaki 1968, 1971) and one, Macrosiphum dryopteridis, in Central Europe, in the Czech Republic (Holman 1959; Fauna Europaea 2011). All three species are oligophagous fern-feeders.

Birds and mammals

A comparative study of grazed and ungrazed semi-natural woodlands in northern Ireland showed that D. dilatata was one of the more substantially grazed species and it was suggested as an indicator species of ungrazed woods (McEvoy, Flexen & Mcadam 2006). On Rum, it is locally frequent or dominant in plantations where it is protected from grazing by red deer (Cervus elaphus) but confined to rocky areas and sea cliffs elsewhere on the island (Pearman et al. 2008). In Shetland, ungrazed rock ledges and ‘holms’, small rocky islands in lochs, are characteristic habitats that provide a refuge from sheep-grazing (Spence 1979; Scott & Palmer 1987).

D. carthusiana was strongly defoliated as a result of grazing by traditional local cattle in wood pastures in south-west Finland (Malkamäki & Hæggström 1997). In North America, D. carthusiana is also grazed by livestock (Dambach 1944), caribou (Rangifer tarandus) (Ferguson, Bergerud & Ferguson 1988) and elk (Alces alces) (Belovsky & Jordan 1978). In contrast, the species is known to be unpalatable to white-tailed deer (Odocoileus virginianus) or tolerant of their grazing (Carson et al. 2005).

Selective grazing of D. expansa has also been recorded in Britain; it is grazed by red deer (Cervus elaphus), but not by mountain hare (Lepus timidus) (Page 1997). In North America (Alaska), rhizomes of D. expansa are important winter forage for Sitka black-tailed deer (Odocoileus hemionus sitkensis), making up 30% of their December diet. Fiddleheads in early spring and green fronds in spring and summer were also consumed by this species (Parker et al. 1999). In Norway, D. expansa is one of the preferred food species of elk (Sæther & Heim 1993). In Alaska, D. expansa is also grazed by elk (LeResche & Davis 1973; Hanley & Mckendrick 1985) and mountain goat (Oreamnos americanus) (Fox & Smith 1988), and in western North America by sooty grouse (Dendragapus fuliginosus) and dusky grouse (D. obscurus) (Stewart 1944).

(B) Plant parasites: fungi

A parasitic fungus, Taphrina vestergrenii Giesenh. (Ascomycota, Taphrinaceae), has been observed on D. carthusiana fronds in Slovakia (Bacigálová, Mułenko & Prillinger 2002).

X. History

  1. Top of page
  2. Summary
  3. I. Geographical and altitudinal distribution
  4. II. Habitat
  5. III. Communities
  6. IV. Response to biotic factors
  7. V. Response to environment
  8. VI. Structure and physiology
  9. VII. Phenology
  10. VIII. Reproductive characteristics
  11. IX. Herbivory and disease
  12. X. History
  13. XI. Conservation
  14. Acknowledgements
  15. References

Fossil records indicate that in Britain, ferns with Dryopteris carthusiana-type spores (including D. carthusiana, D. dilatata, D. cristata and Cystopteris dickieana; Birks 1973) were present in the Late Weichselian, c. 15 000 radiocarbon years before present (Godwin 1975).

The history of the taxonomy of all three Dryopteris species has been complicated. Over the past 200 years, the species have been affiliated to different genera including Aspidium, Lastrea, Lophodium, Nephrodium, Polypodium, Polystichum or Thelypteris. Dryopteris dilatata is a distinctive species that was first recorded in Britain by John Goodyer ‘on the moist shadowie rockes by Maple-durham in Hampshire’ (Brewis, Bowman & Rose 1996), a record published by Johnson (1633). According to the National Biodiversity Network Taxonomic and Designation Information (NBN 2012), 25 different binomials have been used for D. dilatata. In recent decades, two main names, Dryopteris dilatata (Hoffm.) A. Gray (Gray 1848) and D. austriaca (Jacq.) Woyn. ex Schinz et Thell. (Schinz & Thellung 1915), have been used. According to Fraser-Jenkins (1980), the name D. austriaca cannot be used for the taxon, because the basionym Polypodium austriacum Jacq. applied in fact to Pteridium aquilinum (L.) Kuhn, and therefore lectotypes selected for the new combination Dryopteris austriaca were not valid. The name D. dilatata, based on Polypodium dilatatum Hoff., and first used by A. Gray (1848), could, on the contrary, be clearly typified and has therefore been more acceptable and more frequently used in modern floras (e. g. Fraser-Jenkins 1993; Montgomery & Wagner 1993; Stace 2010).

Dryopteris carthusiana (Vill.) H. P. Fuchs (Fuchs 1958), first described by Dominique Villars (1786) as Polypodium carthusianum Vill., has long been known as D. spinulosa (O. F. Müller) O. Kuntze (Kuntze 1891). The first record is difficult to identify because of confusion with other Dryopteris species but the description and illustration of Polipodium cristatum in Bolton (1785) is clearly D. carthusiana (J. Edgington, pers. comm.) and Withering (1796) reported it from Britain as Polypodium spinulosum. The species was not well-understood until recent decades and the distribution map published by Perring & Walters (1962) was only provisional. Sixteen different binomials have been used for D. carthusiana according to the NBN (2012) Taxonomic and Designation Information. In 1957, a different name, Dryopteris lanceolatocristata (Hoffm.) Alston (1957), was published and used (e.g. Clapham, Tutin & Warburg 1957). Since authentic Villars’ material of Polypodium carthusianum was absent, the identity of D. carthusiana was newly verified and a neotype selected in 1978 (Fraser-Jenkins 1980).

Dryopteris expansa (C. Presl) Fraser-Jenk. & Jermy was first published by C. Presl (1825) as Nephrodium expansum C. Presl. Until 1950, the species was considered a variety of D. dilatataLastrea dilatata C. Presl var. alpina T. Moore (Moore 1855). As a result of cytological studies of D. dilatata (Manton 1950; Walker 1955), a new diploid species was separated from tetraploid D. dilatata and described as D. assimilis S. Walker (Walker 1961). The valid name combination of D. expansa has been used since 1977, when the priority of the epithet ‘expansa’ was recognized (Fraser-Jenkins & Jermy 1977). According to the NBN (2012), seven different binomials have been used for D. expansa.

XI. Conservation

  1. Top of page
  2. Summary
  3. I. Geographical and altitudinal distribution
  4. II. Habitat
  5. III. Communities
  6. IV. Response to biotic factors
  7. V. Response to environment
  8. VI. Structure and physiology
  9. VII. Phenology
  10. VIII. Reproductive characteristics
  11. IX. Herbivory and disease
  12. X. History
  13. XI. Conservation
  14. Acknowledgements
  15. References

Dryopteris dilatata, D. carthusiana and D. expansa have all been included in The Vascular Plant Red Data List for Great Britain (Cheffings & Farrell 2005), in the category of ‘Least concern’. Dryopteris dilatata has the least complicated taxonomic history, and trends in its distribution are easiest to assess. Its ‘change index’ (which measures relative change in British range size from 1930–69 to 1987–99) is 1.32, which Dines (2002c) interpreted as indicating a stable distribution in northern and western Britain accompanied by an expansion in eastern England. Dryopteris dilatata showed a significant increase in a number of vegetation plots in Bedfordshire between an initial survey in 1949–51 and a resurvey in 2003–04; the increase in mean abundance within the plots was not statistically significant (Walker, Preston & Boon 2009). Kirby et al. (2005) noted a significant increase in the cover of D. dilatata/carthusiana within woodland plots between 1971 and 2001 (records of the two species were aggregated in their survey). The main causes of the increase in the east are believed to be an increase in broad-leaved woodland following the reduction in management and hence more shaded and humid conditions (Perring et al. 1964; James 2009) and a spread in conifer plantations (Sanford & Fisk 2010). James (2009) suggests that it might also have responded to eutrophication. Nevertheless, the current stable/expansive distribution of D. dilatata in the British Isles may become threatened in the future as it has been predicted that, because of climate change, it may disappear from the southern part of its distribution area in the Britain by 2050 (Bakkenes et al. 2002).

Dryopteris carthusiana has been under-recorded until recently and this is the reason for a ‘change index’ value of 1.06. Its comparatively narrow ecological amplitude and loss of habitat caused by human impact (drainage of wetlands, forestry and agricultural improvement) may underlie the decrease in its distribution apparent in Fig. 4 (Page 2001; Dines 2002b).

Although D. expansa may be under-recorded because of identification problems, its distribution in montane localities is assumed to be relatively stable (Dines 2002a). The species was first mapped by Jermy et al. (1978), and no comparative change index has been calculated since. Climatic change is also considered to be the most important possible threat to D. expansa (Page 2001). Overgrazing by domestic and wild animals in upland communities may be the reason why D. expansa, mostly a mountain species, can be frequently found only in habitats which are inaccessible to grazing mammals. The susceptibility of D. expansa to herbicide spraying to control Bracken (Pteridium aquilinum) and the loss of ancient woodlands could also be possible causes of its continuing decline (Page 2001). Two extremely rare hybrids, D. × sarvelae (D. carthusiana × D. expansa) and D. × uliginosa (D. cristata × D. carthusiana), which occur in only a very few locations and in very small populations in Great Britain, are therefore considered to be at a high risk of extinction; both have been included in The Vascular Plant Red Data List for Great Britain in the category of ‘Vulnerable’ (Cheffings & Farrell 2005). D. × brathaica (D. filix-mas × D. carthusiana) has not been seen since the original 19th century collection, but survives in cultivation.

Acknowledgements

  1. Top of page
  2. Summary
  3. I. Geographical and altitudinal distribution
  4. II. Habitat
  5. III. Communities
  6. IV. Response to biotic factors
  7. V. Response to environment
  8. VI. Structure and physiology
  9. VII. Phenology
  10. VIII. Reproductive characteristics
  11. IX. Herbivory and disease
  12. X. History
  13. XI. Conservation
  14. Acknowledgements
  15. References

We gratefully acknowledge Mary Gibby, Chris Preston, Michael Proctor, David Streeter and Michael Usher who kindly provided helpful comments on the text, and advice and additional information that significantly improved this account. We are most grateful to Tony Davy for substantive editorial assistance and useful comments on the text. We thank John Edgington and David Pearman for information on the first British records of Dryopteris carthusiana. We also thank Colin Harrower for providing the maps for Figs 2, 4 and 6; Mikko Piirainen for granting permission to reproduce the European distribution maps (Fig. 3, 5 and 7) and Alexander Harding for linguistic assistance. This work was supported by ETF grants 7576 and 9269, University of Tartu SF0180119s08 and European Regional Development Fund (Centre of Excellence FIBIR).

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  1. Top of page
  2. Summary
  3. I. Geographical and altitudinal distribution
  4. II. Habitat
  5. III. Communities
  6. IV. Response to biotic factors
  7. V. Response to environment
  8. VI. Structure and physiology
  9. VII. Phenology
  10. VIII. Reproductive characteristics
  11. IX. Herbivory and disease
  12. X. History
  13. XI. Conservation
  14. Acknowledgements
  15. References
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