An ecological comparison between ancient and other forest plant species of Europe, and the implications for forest conservation

Biological Conservation 91 (1999) 9±22

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An ecological comparison between ancient and other forest plant species of Europe, and the implications for forest conservation Martin Hermy a,*, Olivier Honnay a, Les Firbank b, Carla Grashof-Bokdam c, Jonas E. Lawesson d a

K.U.Leuven, Department of Land Management, Laboratory for Forest, Nature and and Landscape Research, Vital Decosterstraat 102, B-3000 Leuven, Belgium b Institute of Terrestrial Ecology, Merlewood Research Station, Grange-over-Sands, Cumbria LA11 6JU, UK c Institute for Forestry and Nature Research (IBN-DLO), p.b. 23, 6700 AA Wageningen, The Netherlands d National Environmental Research Institute, dep. Landscape Ecology, GrenaÊvej 12, 841 Rùnde, Denmark Received 15 September 1998; received in revised form 3 March 1999; accepted 3 March 1999

Abstract An analysis is presented of the ecological characteristics of ancient forest plant species in deciduous forests of Europe. Twentytwo literature sources were used to generate a list of 132 ancient forest plant species, described from at least eight countries in Europe. The anity for ancient forests of these species di€ers considerably from country to country, but they have a de®nite ecological pro®le. There is a signi®cant di€erence in the response of the ancient forest plant species compared with other forest plant species for a variety of ecological characteristics, based on Ellenberg indicators, plant strategies and phytosociological associations. Ancient forest plant species tend to be more shade-tolerant than the other forest plant species; dry and wet sites are avoided. They are typical of forest sites with an intermediate pH and nitrogen availability. Geophytes and hemicryptophytes are more frequent amongst ancient forest plant species. The stress-tolerant plant strategy type is signi®cantly more abundant under the ancient forest species than expected when compared with other forest plant species and vice versa for the competitive plant strategy. This distinct ecological pro®le suggests that ancient forest plant species may be considered as a guild. The poor ability of these species to colonize new forest sites may be attributed to a complex of interacting variables: limited dispersal abilities (many have a short-distance dispersal strategy), low diaspore production and recruitment problems (e.g. low competitive ability). The regional variation in ancient forest plant species suggests that regional lists are more appropriate for assessing the nature conservation value of forests than one global European list. Due to their distinct ecological pro®le and low colonizing abilities, ancient forest plant species may be considered as important biodiversity indicators for forests. # 1999 Elsevier Science Ltd. All rights reserved. Keywords: Forest plant species; Ancient forests; Colonization capacity; Literature review; Species guilds; Historical ecology

1. Introduction In a fragmented, dynamic landscape, a species must be able to successfully colonize new habitats at least as fast as it is lost from existing habitats. Those species which are unable to do so, are threatened by extinction from the landscape. Such is considered to be the case for ancient forest plant species. While some plants can

* Corresponding author. Tel.:+32-16-329-757; fax:+32-16-329760. E-mail address: [email protected] (M. Hermy)

colonize new forests quickly, (e.g. Geum urbanum and Urtica dioica), other forest species may take centuries (Peterken, 1981; Peterken and Game, 1984). Such slow-colonizing species are termed ancient forest species, because their presence suggests a long continuous history for the habitat patch, and also because they therefoe may be indicative of more original forest conditions (Peterken, 1974; Rackham, 1980; Whitney and Foster, 1988). They are considered important in terms of nature conservation, because lists of ancient forest species combine both qualitative (forest quality) and quantitative (diversity) conservation criteria (Peterken, 1974, 1977, 1996; Honnay et al., 1999a). However,

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M. Hermy et al. / Biological Conservation 91 (1999) 9±22

what are the ecological characteristics of this group of plants, other than a tendency to be associated with old forests? Previously there has been no attempt at an ecological comparison between ancient forest plants species and other species at the European scale. Such an overview could inform the debate on forest biodiversity indicators and also help identify the conditions needed for the long-term persistence of these plants within European landscapes. The objective of this paper is to create a species list of ancient forest plants from the literature, and secondly to compare ecological attributes for species within this list with those for other plant species with forests. We then discuss the causes of failure of ancient forest plant species to colonize new forests and the consequences for nature conservation. 2. Methods 2.1. Identi®cation of European ancient forest plants A list of ancient forest plant species was developed from 22 publications, all from deciduous forests of northwestern and central Europe (Belgium, the Czech Republic, Denmark, Germany, Great Britain, the Netherlands, Poland, and Sweden, Table 1). The quality and nature of these publications vary considerably, from detailed, large scale studies (Rackham, 1980; Peterken and Game, 1984; Hermy, 1985; Wulf, 1994) to scattered and more anecdotical data on forest species (e.g. Roisin and Thill, 1952; Runge, 1959; van den Wijngaard, 1977; Stortelder and Hommel, 1990). Some data are derived from plots (e.g. Hermy, 1985; Brunet, 1994; Petersen, 1994), others from whole forests. Since most of these studies were not intended to present overviews of ancient forest species, it was not always easy to extract species lists from these sources. Within the sources, ancient forest is de®ned as forest that has existed continuously since at least a speci®ed date, but this date was originally selected on the availability of historical site information for the individual study [e.g. 1600, Peterken (1974); 1700, Rackham (1980); 1746±1786, Zacharias (1994); 1770±1800, Hermy (1985) and Petersen (1994); 1789, Lawesson et al. (1998); 1804±1805, HaÈrdtle (1994); 1812±1820, Brunet (1994); 1850, Grashof-Bokdam (1997a)], introducing an inevitable degree of inconsistency. Furthermore, most of the authors assume ancient forest species to be associated with the interiors of forests; in most of the studies, forest edges and clearings were not surveyed explicitly. Based on the phytosociological indication given in Ellenberg et al. (1991) and Oberdorfer (1970), we therefore omitted these species. The only exception to this was when the author(s) stated explicitly in the paper that the species had an optimum in the forest

interior. The frequency with which each remaining species occurred among the 22 studies was recorded (Table 2). 2.2. Identi®cation of European forest plants A total list of plant species associated with all European forests, ancient and recent, was compiled including all species from forests and forest edges. The latter was achieved using the phytosociological anity as given in Ellenberg et al. (1991): it includes all species from forest edges (Classes: Trifolio-Geranietea, Epilobietea, Betulo-Adenostyletea), along with species of coniferous forests (Classes: Erico-Pinetea, PulsatilloPinetea, Vaccinio-Piceetea) and deciduous forests (DF) (Classes: Salicetea purpureae, Alnetea, Quercetea roboripetraeae, Querco-Fagetea). To this list were added two species with no clear phytosociological behaviour (indicated by an x in Ellenberg l.c.), because they occur commonly in forests. For comparison purposes a second list, taking into account only the species from deciduous forests (DF), was compiled (see later). 2.3. Ecological characteristics of the forest plant species The ecological characteristics of the species were examined using the Ellenberg scores of response to abiotic factors (Ellenberg et al., 1991) and the assessment of the plant's ecological strategy (Hodgson et al., 1995). The Ellenberg indicator values (Ellenberg et al., 1991) o€er autecological information on the ®eld response of some 2000 species to a range of climatic and edaphic factors in central Europe. While the intuitive nature of the Ellenberg indicator values has been criticised (Thompson et al., 1993), they remain the most wide ranging source of ecological plant species information available in Europe. There is evidence that they are robust (Thompson et al., 1993; Runhaar et al., 1994) and it appears that the values are broadly applicable even to Britain, with its distinctive Atlantic climate (M.O. Hill, pers. comm.). Three species were not included in the Ellenberg lists; information for Isopyrum thalictroides and Ruscus aculeatus was obtained from Landolt (1977); while for one other species, Cardamine glandulifera (mentioned in Dzwonko and Loster, 1989), we did not ®nd any information, so it was excluded from further ecological analysis. Since species of young forests have been described as being weedier and more aggressive than many ancient forest species (Whitney and Foster, 1988), we also looked for di€erences in plant strategies, both in the established phase and in the regenerative strategies (Grime et al., 1988). We therefore classi®ed species (n=107), to the level of the seven basic types, using the data tables of Hodgson et al. (1995). Data on the dispersal mode of the ancient forest plants were compiled

B D B GB GB GB NL GB B GB B D CS PO NL D D D DK D D S

Roisin and Thill (1952:20...) Runge (1959 in Wulf 1994) Froment and Tanghe (1967:348±350) Pigott (1969) Pollard (1973:350±351) Pigott (1977:65) van den Wijngaard (1977:73±75) Rackham (1980) Hermy and Stieperaere (1981) Peterken and Game (1984)+Peterken (1974:240) Hermy (1985:106) GoÈdde et al. (1985 in Wulf 1994) Kubicova (1987:165) Dzwonko and Loster (1989:80-84) Stortelder and Hommel (1990:104,119) Dinter (1991 in Wulf 1994) Wulf (1994: Table 4) +Wulf (1997) Wulf (1994: Table 4) Petersen (1994: Table 11 and 17) Zacharias (1994:Table 3) HaÈrdtle (1994:Table 1) Brunet (1994:Table1)

Between Court-St.Etienne and Gembloux (Belgium) Westfalen (Germany) Blaimont near Chimay (Belgium) Derbyshire (Great Britain) Huntingdon and Peterborough (Great Britain) Neighbourhood of Rothamsted (Great Britain) Veluwe (the Netherlands) Eastern England (Great Britain; sand, loess and clay; pH: 3.1±8.0) Flemish Sand area south of Bruges (Belgium) Central Lincolnshire (Great Britain; sand, loams, clay, peaty clay) Flanders (except Polders; sand, loess, clay, peat) MuÈnster (Germany) Central Bohemia (around Prague, Czechoslovakia) Wierzbanowka valley (W. Carpath. foothills; SW of Krakow)(Poland) Utrecht hill area (Rhenen to Hilversum; the Netherlands) Nordrhein-Westfalens (Hiesfelder Waldes, Germany) Niedersachsen (Elbe-Weser triangle: 760,000 ha; sand, loam and clay; Germany) Northeastern Brandenburg (1,014,000 ha; Germany) Résnñs peninsula (Sjñlland; 3000 ha; gravel, sand and clay; Denmark) Harzvorland (Niedersachen, 321,600 ha; silty and clay soils; Germany) Schleswig-Holstein (Germany) SkaÊne province (S. Sweden)

Area Anec Anec Anec Anec Hedges Anec Anec Forest Plots Forest Plots Forest Forest Forest Plots Anec Forest Forest Plots Forest Forest Plots

Data typea

7 2 15 5 10 14 1 38 13 49 29 4 33 52 5 4 80 78 27 39 14 29

Number of ancient forest spp.

a Results based on: Anec: anecdotal; based on experience rather than a quantitative study or other purpose paper; Forest: ¯oristical species lists per forest; Plots: ¯oristical species list per plot; hedges: ancient hedges, mostly derived from forests.

Country

Authors

Table 1 Chronological list of publications on ancient woodland species, used in the review

M. Hermy et al. / Biological Conservation 91 (1999) 9±22 11

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M. Hermy et al. / Biological Conservation 91 (1999) 9±22

Table 2 Ancient forest plant species in Europe, mentioned in the literature (Table 1). Plant species from forest edges have been omitted, except when explicitly mentioned as forest interior species in the publication. Nomenclature follows Ellenberg et al. (1991) Species

Dispersal typea

No of citations in 22 publications

Acer campestre Actaea spicata Adoxa moschatellina Allium ursinum Anemone nemorosab Anemone ranunculoides Asarum europaeum Asperula odorata Athyrium felix-feminac Berberis vulgaris Brachypodium sylvaticum Bromus benekenii Campanula latifolia Campanula trachelium Cardamine glandulifera Carex digitata Carex laevigata Carex pallescens Carex pendula Carex pilosa Carex remotad Carex strigosa Carex sylvaticad Chrysosplenium alternifolium Chrysosplenium oppositifolium Circaea alpina Circaea lutetiana Circaea x intermedia Clematis vitalba Conopodium majus Convallaria majalis Cornus mas Cornus sanguinea Corydalis cava Corydalis solida Corylus avellana Crataegus laevigatae Dactylis polygamac Dactylorhiza fuchsii Daphne mezereum Dentaria bulbifera Dentaria glandulosa Dryopteris carthusiana Dryopteris pseudo-mas/®lix-mas Elymus caninus Epilobium montanum Epipactis purpurata Equisetum hyemale Equisetum sylvaticum Euonymus europaeus Euphorbia amygdaloides Euphorbia dulcis Festuca altissima Festuca gigantea Festuca heterphylla Gagea luteab Gagea spathacea Geum rivale Gymnocarpium dryopteris Helleborus viridis Hepatica nobilis

ANEw END END MYR MYR MYR MYR EPI ANEd END EPI EPI UNSP ANE BAR MYR UNSP UNSP HYD UNSP HYD HYD MYR UNSP UNSP UNSP EPI UNSP ANEw MYR END END END MYR MYR END END UNSP ANEd END UNSP UNSP ANEd ANEd EPI ANE ANEd ANEd ANEd END MYR MYR UNSP EPI UNSP MYR MYR EPI ANEd UNSP MYR

3 4 4 7 14 4 3 9 3 2 2 4 4 9 1 4 2 2 5 1 6 5 8 7 6 3 4 2 1 2 10 1 4 1 1 6 5 3 2 3 1 1 1 3 3 3 2 2 4 7 3 1 2 4 1 2 3 5 4 3 8 (continued)

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Table 2 (continued) Species

Dispersal typea

No of citations in 22 publications

Hieracium fuscocinereum Hieracium sabaudum Hordelymus europaeus Hyacinthoides non-scripta Hypericum hirsutum Hypericum montanum Hypericum pulchrumb Ilex aquifolium Isopyrum thalictroides Lamium galeobdolon Lathraea squamaria Lathyrus montanus Lathyrus vernus Lilium martagon Listera ovata Lonicera periclymenum Lonicera xylosteum Luzula luzuloidesf Luzula pilosa Luzula sylvatica Lysimachia nemorumd Maianthemum bifolium Malus sylvestris Melampyrum nemorosumc Melampyrum pratensis Melica nutans Melica uni¯ora Melittis melisophyllumc Mercurialis perennis Mespilus germanica Milium e€usum Narcissus pseudonarcissusf Neottia nidus-avis Orchis mascula Oxalis acetosella Paris quadrifolia Phyteuma spicatumf Platanthera chorantha Poa nemoralis Polygonatum multi¯orumc Polystichum aculeatumc Potentilla sterilis Primula elatiorb Primula vulgarisc Pteridium aquilinum Pulmonaria obscura Pulmonaria ocinalis Pyrus commune Ranunculus auricomus Ranunculus lanuginosus Rhamnus catharticus Ruscus aculeatus Sanicula europaea Scrophularia nodosa Sorbus torminalis Stachys sylvatica Stellaria holostea Stellaria nemorum Symphytum tuberosum Tamus communis Thelypteris phegopteris Tilia cordata Tilia platyphyllos Ulmus laevis

UNSP ANE UNSP BAR ANE ANE ANE END BAR MYR MYR UNSP AUT MYR ANEd END END MYR MYR MYR ANE END END MYR MYR MYR MYR BAR MYR END ANE BAR ANEd ANEd AUT END ANE ANEd ANE END ANEd UNSP ANE MYR ANEd MYR MYR END EPI EPI END END EPI ANE END EPI BAR HYD MYR END ANEd ANEw ANEw ANEw

1 4 4 7 5 1 2 2 1 9 5 4 3 1 3 1 1 4 10 4 6 9 3 5 4 6 9 2 11 1 8 3 7 8 10 12 5 4 1 11 3 3 11 7 5 4 3 3 8 5 3 1 10 1 5 4 6 1 2 1 2 4 1 2 (continued)

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Table 2 (continued) Species

Dispersal typea

No of citations in 22 publications

Ulmus minor Vaccinium myrtillusb Veronica montana Viburnum opulus Vinca minor Viola mirabilis Viola reichenbachiana

ANEw END MYR END MYR MYR MYR

2 4 6 2 3 1 8

a

Dispersal type: MYR: dispersal by ants (myrmecochores); END: dispersal by animals and birds via digestion (endozoochores and ornithochores); EPI: dispersal by adhesion on animals (epizoochores); BAR & AUT: passive and active dispersal by plant itself (baro- and autochores); UNSP: unspeci®ed, uncertain or unknown; HYD: dispersal by water (hydrochores); ANEw: diaspores winged or ¯attened; ANEd: diaspores minute (orchids, ferns and horsetails); ANE: dispersed by wind but heavier than ANEd and not winged. b Sometimes in old grasslands or heathlands, on former forest sites. c Sometimes in wood edges. d Often along forest rides. e Petersen includes also Crataegus monogyna and the hybrids in this taxon. f Sometimes in grasslands, particularly in Central Europe.

from Grime et al. (1988), supplemented by Dzwonko and Loster (1989) and Hermy (1985). 2.4. The comparison of the ecology of ancient forest and other forest plant species The phytosociological groupings given by Ellenberg et al. (1991) were used to assess the phytosociological characteristics of ancient forest species compared with those of all forest species. For the other comparisons, given the available literature sources, it was considered more appropriate to use only species of deciduous forests and to exclude species of edges and clearings. Contingency tables were constructed to show di€erences between ancient and non-ancient species with respect to the selected Ellenberg characteristic, and the chi-square statistic was computed. Finally, the plant strategy distribution of ancient forest plant species compared to other forest plant species was tested. A similar comparison for the dispersal characteristics has not been attempted, as not enough unambiguous literature data were available. All statistical analyses were performed with SPSS version 6.0 and 6.1 (Norusis, 1993). 3. Results 3.1. Lists of ancient forest species and total forest ¯ora A review of the literature produced a list of 132 forest plant species considered to have a clear anity for ancient forests (Table 2), out of a list total of 627 forest species including the two species with non-speci®c behaviour. Note that ®ve ancient forest species indicative of grasslands and heathlands according to Ellenberg et al. (1991) were not omitted (Table 2), because they are associated with forests in western Europe.

The total list of all forest species can be divided into ®ve groups (Table 3): 1. 383 species from deciduous forest communities [deciduous forest communities and related scrub communities, classes: Salicetea purpureae (12 spp.), Alnetea glutinosae (18 spp.), species from Querco-Fagetea-communities (306 spp.), and 47 species with no clear phytosociological anity, but clearly forest species]; 2. 83 species from coniferous forests; 3. 154 species from edges and clearings; 4. 5 species from heathlands and grasslands; 5. 2 non-classi®ed species. If all the 132 ancient forest species are included, and all the species from coniferous forests, from clearings and edges, grasslands and heathlands are excluded, the resulting list has 391 forest species of deciduous forests, further referred to as deciduous forest interior species. 3.2. Plant communities containing the ancient forest plant species Of these 627 forest species, 21% have been mentioned as ancient forest species in one or more sources. As a group, ancient forest plant species di€erentiate the higher order phytosociological syntaxa; since these syntaxa are common in northwestern and central Europe, it suggests that they are relatively common species (Fig. 1). The majority (56%) of these ancient forest species are typical of Fagetalia-forest communities, and a further 16% characterize Querco-Fagetea-forests in general (Table 3), more than expected by chance in comparison with all forest species (2=171.1, p<0.01). Ancient forest plant species were scarce in other classes; only seven Quercetalia robori-petraeae-species were

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Table 3 The signi®cance of di€erences in the phytosociological behaviour of ancient forest plant species and other forest species (Chi2-value=171.1, p<0.01) Community group

Deciduous forest+related scrub

Coniferous forest Forest edges+ clearings Grasslands Totals a b

Syntaxon

Querco-Fagetea (8.4)a Quercetalia robori-petraeae (8.41) Quercetalia pubescentis (8.42) Fagetalia (8.43) Prunetalia (8.44) Salicetetalia arenariae (8.45) Alnetea glutinosae (8.2) Salicetea purpureae (8.1) Not de®ned+indi€erent(x) Erico-Pinetea (7.1) Pulsatillo-Pinetea (7.2) Vaccinio-Piceetea (7.3) Trifolio-Geranietea (6.1) Epilobietea (6.2) Betulo-Adenostyletea (6.3) Nardo-Callunetea (5.1) Molinio-Arrhenatheretea (5.4) Non-classi®ed species

All forest species

Ancient forest species

Other forest species

number

%

numberb

%

numberb

%

47 21 40 157 40 1 18 12 47 25 12 46 90 24 40 2 3 2 627

7.5 3.3 6.4 25.0 6.4 0.2 2.9 1.9 7.5 4.0 1.9 7.3 14.4 3.8 6.4 0.3 0.5 0.3 100.0

21(10) 7(4) 4(8) 74(33) 7(8) 0(0) 1(4) 0(3) 11(10) 0(5) 0(3) 0(10) 0(19) 1(5) 0(8) 2(0) 2(1) 2(0) 132

15.9 5.3 3.0 56.1 5.3 0.0 0.8 0.0 8.3 0.0 0.0 0.0 0.0 0.8 0.0 1.5 1.5 1.5 100.0

26(37) 14(17) 36(32) 83(124) 33(32) 1(1) 17(14) 12(9) 36(37) 25(20) 12(9) 46(36) 90(71) 23(19) 40(32) 0(2) 1(2) 0(2) 495

5.3 2.8 7.3 16.8 6.7 0.2 3.4 2.4 7.3 5.1 2.4 9.3 18.2 4.6 8.1 0.0 0.2 0.0 100.0

Numbers refer to the hierarchical codes in Ellenberg et al. (1991). Between brackets the expected number of species in that category under the hypothesis of no di€erence in phytosociological behaviour.

present in the list. Eleven ancient forest species had no de®nite anity for a forest higher order syntaxon. Since the higher forest syntaxa clearly have environmental optima (cf. Ellenberg, 1978), these results suggest that ancient forest species tend to be associated with relatively rich soils and not wet soils (only 1 Alnion-species: Carex laevigata). Of the deciduous forest interior species (n=391), 34.5% are recorded as ancient forest plant species. 3.3. The ecological characteristics of ancient forest species Ancient forest species tend to be shade- or semi-shade tolerant plants (Fig. 2). They are more likely to be shade-tolerant plants than other forest plants (Table 4). Relative light intensity is usually lower than 5% (cf. Ellenberg et al., 1991), although the species may occur in more sunny stands. The temperature and continentality ®gures both show that ancient forest species prefer the mild conditions of the lowlands to the submontane stages from oceanic to suboceanic parts of Europe. Ancient forest species are signi®cantly concentrated in the mid part of the moisture gradient, and they avoid both dry and wet sites (Fig. 2 and Table 4). Their preference for ``fresh'' to moist soils, is also re¯ected in the phytosociological anities (Fig. 1). A similar, but less signi®cant, response is observed for soil acidity; weakly acid to neutral soils are especially favoured. Ancient forest species are typical of soils with

intermediate nitrogen availability (N-indicator values). There is a preponderance of hemicryptophytes (Fig. 3), and geophytes are signi®cantly more frequent than expected. Nanophanerophytes are less frequent than expected. The majority of ancient forest species are summergreen (61%), although 22% have some overwintering foliage. The preponderance of geophytes also a€ects the higher frequency of vernal species. Wintergreen species are also more frequent than expected, although the proportion of evergreen species is similar to the non-ancient forest ¯ora. Twenty-four per cent of the ancient forest species are dispersed by ants (myrmecochores). However, the total number of species considered to be dispersed by wind (anemochores) is considerable (25%) (Fig. 4). The proportion of the anemochores having very minute seeds or spores and probably the highest dispersal abilities (e.g. orchids, ferns and horsetails) is only 11.4%. In terms of plant strategies in the established phase, 39% of the ancient forest plant species are stress-tolerant; the two other primary strategies (competitors and ruderals) are rarely represented (Table 5). Of the secondary strategy types, the stress-tolerant competitor scores highest (22%). Compared to other forest plant species, the group of ancient forest plant species has a signi®cantly higher proportion of stress-tolerant species and lower proportion of competitive species (Table 5). In terms of regenerative strategies, however, no signi®cant di€erences were observed (therefore not presented here).

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Fig. 1. Phytosociological distribution of the ancient forest plant species (n=132). Hierarchical classi®cation system (see Ellenberg et al. 1991): Classes: Querco-Fagetea (Quercus-Fagus forests); Alnetea glutinosae (Alnus glutinosa forests); Order: Quercetalia robori-petraeae (Quercus robur and Q. petraea forests); Quercetalia pubescenti (Quercus pubescens forests), Fagetalia (Fagus sylvatica forests); Prunetalia (Prunus spinosa scrub); Nardetalia (Nardus stricta grassy heath); Molinietalia (Molinea caerulea grasslands); Arrhenatheretalia (Arrhenaterum elatior grasslands); Alliance: Quercion robori-petraeae (Quercus robur and Q. petraea forests); Fagion sylvaticae (Fagus sylvatica forests); Carpinion betuli (Carpinus betulus forests); Alno-Ulmion (Alnus glutinosa-Ulmus minor alluvial forests); Tilio-Acerion (Tilia platiphyllos-Acer pseudoplatanus gully forests); Pruno-Rubion (Prunus spinosa-Rubus spp. scrub); Atropion (Atropa belladonna forest edge and clearing communities).

So, in conclusion, there are many signi®cant di€erences between the ecological responses of the 132 ancient forest species and the other 259 forest interior species selected for comparison (Table 4). 4. Discussion 4.1. The list of ancient forest plant species and regional variation While our list of ancient plant species is informative, it must be interpreted with caution for several reasons. The absence of an ancient forest species from a certain list may mean that the species was simply unrecorded (particularly with anecdotal sources, see methods section), that it was not present in the studied forests, or that it was present but was not considered to be an ancient forest species. No exact conclusion can be reached from the available literature without further data. However, excluding the anecdotal information on ancient forest plants would mean the loss of valuable

qualitative information of experienced scientists. Furthermore there is a large di€erence in areas sampled (see Table 1) and some parts of the environmental gradient may be somewhat underrepresented (e.g. peaty soils); but at least in some publications (e.g. Peterken 1974; Rackham 1980; Hermy 1985; Wulf 1994) the full gradient from sandy, silty, clay and peaty soils was available. Therefore we think the list of ancient forest plant species is largely representative for western and northwestern Europe. In some regions, a species may belong to the ancient forest species category, but in others it may be more capable of colonizing recent forests. In Denmark, Anemone nemorosa, Convallaria majalis, Melica uni¯ora, Mercurialis perennis, Primula elatior and Sanicula europaea are not restricted to ancient forest (J.E. Lawesson, pers. comm.); they are found more or less in all forests. In eastern England Primula vulgaris is a good indicator of ancient forest (Rackham, 1980), but in Ireland it is a grassland species (B.N.K. Davis, pers. comm.). Variation in the validity of the lists may also be quite local in pedologically and geologically diverse areas. For

M. Hermy et al. / Biological Conservation 91 (1999) 9±22

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Fig. 2. Distribution of the ancient forest plant species (n=132) in relation to various indicator scores of Ellenberg et al. (1991). Observed (obs. freq.) number of species and the expected (exp.freq.) number of species is given under the hypothesis that ancient forest species do not di€er from the other forest species in their ecological response. Signi®cance of di€erence is shown in Table 4. Ranks go from 1 to 9 (-: unclassi®ed species) and de®nition follows Ellenberg et al. (1991): (a) Light: l, shadow plant (relative light intensity usually <2%); 3, shadow plant; 5, half shadow plant; 7, half light plant; 9, full light plant (rarely receiving <50% of full daylight). (b) Temperature: distribution in relation to latitudinal and altitudinal belts; 3: mostly in cold climates (e.g. montane to subalpine); 5: intermediate, i.e. concentrated in the submontane belt of Central Europe; 7: mostly in warm climate (rare in Central Europe); 9: only in very warm climate (Mediterranean). (c) Continentality ®gure; main distribution in relation to degree of continentality; 1: euocenanic (reaching Central Europe only in extreme west; 2: oceanic; 4: suboceanic (main area in whole Central Europe); 6: subcontinental (main area in eastern Central Europe). (d) Soil moisture: 3: in dry soils; 5: in ``fresh'' soils; 7: in moist soils; 9: in wet, often not well aerated soils. (e) Soil acidity: 1: only on very acid soils; 3: mostly on acid soils; 5: on intermediate soils; 7: mostly in neutral soils, but also in acid and alkaline ones; 9: only in neutral or alkaline soils. (f) Soil nitrogen: occurrence in relation to ammonia or nitrate supply; 1: only on soils very poor in nutrients; 3: mostly in poor sites; 5: mostly in intermediate soils; 7: mostly in soils rich in nutrients; 9: nitrogen indicators. The nitrogen ®gure is considered indicative of the total nutrient status of the soil.

example, in Flanders, it may be observed that a plant species is con®ned to ancient forests in the sandy region (northern part), whereas the same species also occurs in recent forests in the loamy region some 50 km southward,

e.g. Primula elatior (Hermy, 1985). Mercurialis perennis, usually an ancient forest plant species in the forests of central Lincolnshire (Peterken and Game, 1981), abundantly colonized recent forests in the Derbyshire Peak

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M. Hermy et al. / Biological Conservation 91 (1999) 9±22

Table 4 The signi®cance of di€erences in the relationships between ancient forest (n=132) and other forest interior species (n=259) for various ecological variables on the basis of the Ellenberg indicator values, life forms and leaf persistence (see also Figs. 2 and 3) Ecological variable

MIVa ancient forest species

Chi2-value

Signi®canceb

Cramer's V

Signi®canceb

Light Temperature Continentality Moisture Soil acidity Nitrogen

4.33 5.48 3.40 5.46 6.24 5.32

55.2(n=381) 12.8 (n=323) 25.7 (n=367) 51.5 (n=362 15.6 (n=342) 31.9 (n=347)

*** * *** * * ***

0.37 0.19 0.24 0.20 0.20 0.30

*** * ** *** n.s. ***

33.6 (n=391) 16.9 (n=391)

*** **

0.28 0.21

*** **

(4) (5) (3) (5) (7) (5)

Raunkiaer life form Leaf persistence a b

MIV=mean indicator value, between brackets=median. Signi®cance:*p<0.05;**, p<0.01;***, p<0.001.

Fig. 3. Life forms and leaf persistence in the ancient forest plant species (n=132). Observed (obs freq.) number of species and the expected (exp.freq.) number of species is given under the hypothesis that ancient forest species do not di€er in their response from other forest species (n=259). Signi®cance of di€erence is shown in Table 4. (a) Raunkiaer life forms: hCH: herbaceous chamaephytes; G: geophytes; H: hemicryptophyte; NPh: nanophanerphyte; Ph: other phanerophyte; Th: therophyte; wCH: woody chamaephyte; -: unclassi®ed species. (b) Leaf persistence: season during which most of the photosynthetic organs are active; I: evergreen; S: summergreen; V: spring to early summer; W: overwintering foliage.

District (Merton, 1970). Pteridium aquilinum has a clear anity for ancient forests in central Lincolnshire on Kimmeridge Clay and Boulder Clay, but in other regions Pteridium is indi€erent to forest origin (Peterken and Game, 1984) and it covers vast areas of open moorland in north England and Wales. These case studies suggest that lists of ancient forest plants may di€er across regions with a variety of environmental conditions and that they may be more associated with ancient forests when at the (local) limits of their distribution area. Therefore, probably none of the ancient forest plant species is con®ned to ancient forest throughout its natural distribution area. We can conclude that signi®cant progress on the identi®cation of ancient forest plant species will therefore only come from detailed, regional and well designed studies. Regional lists of ancient forest plant species are the most appropriate for use in local conservation studies. Until now, data on ancient forest

plant species are available only for a limited number of countries. However, we suspect that more information is available but published in (to us) less accessible (language problem) and very local journals (distribution problem). 4.2. The ecological pro®le of ancient forest plant species From the statistical comparison of the 132 ancient forest plant species with the other forest plant species (Tables 3±5, Figs. 2,3 and 4), a clear ecological pro®le emerges. Ancient forest plant species tend to be more shade-tolerant than the other forest plant species; they avoid dry and wet sites. They are typical of forest sites with an intermediate pH and nitrogen availability. Geophytes, vernal and wintergreen species are more frequent amongst ancient forest plant species than expected. The stress-tolerant plant strategy type is more abundant among ancient forest species than expected

M. Hermy et al. / Biological Conservation 91 (1999) 9±22

and vice versa for the competitive plant strategy. It suggests that this group of plant species forms a cluster of species which may be referred to as a guild: a group of species ``that exploit the same class of environmental resources in a similar way'' and thus brings together species ``that overlap signi®cantly in their niche requirements'' (Root, 1967; Putman, 1994). 4.3. Bottlenecks in colonization by ancient forest plant species The diculty for ancient forest species to colonize recent forests has been attributed to limited dispersal abilities, low amounts of diaspore production and recruitment problems (Peterken and Game, 1984; Whitney and Foster, 1988; Matlack, 1994; Honnay et al. 1999b).

Fig. 4. Dispersal categories in ancient forest plant species (n=132). ANEd: Anemochores with minute diaspores; ANEw: Anemochores with winged or ¯attened diaspores; ANE: Anemochores; HYD: Hydrochores; END: Endozoochores; EPI: Epizoochores; AUT: Autochores; MYR: Myrmecochores; BAR: Barochores; UNSP: Unspeci®ed or uncertain.

19

Probably the latter follows from di€erences in soil conditions (e.g. higher amount of nutrients in recent forest soils) (e.g. Koerner et al., 1997; Honnay et al., 1999b; Verheyen et al., 1999). Dispersal is important, as it is a prerequisite to establishment, but it is by no means the only explanation for the phenomenon of ancient forest plant species. Grashof-Bokdam (1997b) found a mean maximum dispersal value of about 1 m yearÿ1 based on 16 forest plant species. Colonization rates for endo- and exozoochores are usually higher than those of species having short distance dispersal like myrmecochores and species lacking an active mechanism of dispersal (Matlack, 1994; Grashof-Bokdam, 1997a). For some endozoochores (e.g. Maianthemum bifolium) however, a low berry production is common; furthermore the fruits may be quite inconspicuous on the shaded forest ¯oor (Hermy, 1985). Van Dorp and Kalkhoven (1988) also pointed to the fact that the dispersal distance of plants by birds of late successional forest habitat might also be quite limited, as these territorial birds have small home ranges and do not cross large open landscapes. Also the success of wind dispersal for ®eld layer species in forests is disputable and probably limited. So the importance of short distance dispersal (topochory) in ancient forest plant species is, therefore, more important than suggested by Fig. 4. Yet some species, that are dispersed by ant (e.g. Glechoma hederacea, Viola odorata, Moehringia trinervia) are usually good colonizers of recent forests. Of the eight kinds of species identi®ed as particularly vulnerable to the e€ects of fragmentation (Noss and Csuti, 1994) ancient forest plant species may thus fall into at least three categories: species with limited powers of dispersal, species with low reproductive potential, and species of habitat interiors. There is no single mechanism which explains completely the low colonization abilty of ancient forest plant species, and no distinctive

Table 5 The signi®cance of di€erences in the relationships between ancient forest plant species (n=54), and other forest plant species (n=53) for the plant strategies in the established phase (Chi2-value=31.46; p<0.01) Abbr.

C SC R CR SR S CSR Totals

Plant strategy typea

Competitor Stress-tolerant competitor Ruderal Competitive ruderal Stress-tolerant ruderal Stress-tolerator CSR strategist

All forest speciesb

Ancient forest species

Other forest species

number

%

numberc

%

numberc

%

18 31 2 5 9 29 13 107

16.8 29.0 1.9 4.7 8.4 27.1 12.1 100.0

4(9) 12(16) 0(1) 2(3) 7(5) 21(15) 8(7) 54

7.4 22.2 0.0 3.7 13.0 38.9 14.8 100.0

14(9) 19(15) 2(1) 3(2) 2(4) 8(14) 5(6) 53

26.4 35.8 3.8 5.7 3.8 15.1 9.4 100.0

a The following intermediate strategy types were interpreted as follows: C/CR=C; C/CSR=C; C/SC=C; CR/CSR=CR; R/CR=R; R/ CSR=R; R/SR=R; S/CSR=S; S/SC=S; S/SR=S; SC/CSR=SC; SR/CSR=SR. b Strategy types according to Hodgson et al. (1995) only available for 107 forest species out of the 391 forest interior plant species. c Between brackets the expected number of species in that category is given under the hypothesis that ancient forest plant and other forest plant species have the same strategy types.

20

M. Hermy et al. / Biological Conservation 91 (1999) 9±22

suite of dispersal characteristics which separates them from all other plant species of forests; limited dispersal abilities, low amounts of diaspore production, recruitment and isolation e€ects in new forests act synergistically. Another factor which is important for the colonization of new forests, and for persistence in existing ones, is the availability of cover and the degree of competition from other plants. Some ferns, such as Pteridium aquilinum, produce large amounts of small spores in warm summers, but require open ground for germination (Convay, 1957; Page, 1976), which is often not available in recent forests. In many forests in western Europe, species like the highly competitive Urtica dioica and, Rubus fruticosus agg. have expanded considerably due increasing disturbance and/or pollution (such as Ndeposition) (e.g. Diekmann and Dupre, 1997). These competitive species hamper the survival and development of many forest interior species, as is suggested by the negative correlation between the cover of U. dioica and the number of ancient forest plant species (Hermy, 1994) and also by the high proportion of stress-tolerant species among the ancient forest plant species (Table 5). In a recent study on the impact of habitat quality on forest plant species colonization, Honnay et al. (1999b) found that the number of ancient forest plant species was negatively a€ected by the soil phosphate content, and that soil phosphate stimulates a vigorous growth of competitive plant species (see also Pigott, 1971, 1982). The competitive power of stress-tolerant species, the most common plant strategy under ancient forest plant species, is usually lower under circumstances of nutrient enrichment (see Pigott, 1982; Grime et al., 1988). 4.4. Migration of ancient forest plant species The low colonization capacity of ancient forest species severely restricts the possibilities of habitat re-creation. In addition, most ancient forest species do not have persistent seed banks (Brown and Oosterhuis, 1981), suggesting that even temporal land use changes may have dramatic e€ects on the survival of the ancient forest ¯ora, and reduces the probability of successful restoration of degraded habitats. This will particularly hold for areas with a fragmented forest distribution, like Belgium, The Netherlands and England. However, it does not mean that migration is totally impossible. Under certain conditions, colonization of new sites has occurred (e.g. Primula elatior in Hayley wood, Rackham, 1975; Hyacynthoides non-scripta in ZonieÈn forest, De Meyer and and Langohr, 1984; Mercurialis perennis in some woods of Lincolnshire, Peterken and Game, 1981). Migration is most likely to be successful when ancient forests or other habitats with ancient forest plant species [e.g. relict hedges (Pollard, 1973)] directly borders on recent forest (Matlack, 1994: migration rates: 0±2.3 m yearÿ1; Brunet and Von Oheimb, 1998:

0±1.3 m yearÿ1); Honnay et al., 1999b: 0.28±0.55 m yearÿ1). Since a slow migration of ancient forest plant species occurs, the di€erences in habitat quality between ancient and recent forests, and the dependence of a number of forest plant species on ancient forests, may to some extent be interpreted in terms of source and sink dynamics (Pulliam and Dunning, 1994). Ancient forests are then good habitats (sources) for the survival and reproduction of ancient forest plant species, whereas recent forests generally may be considered as poor habitats for establishment (sinks) because of their higher nutrient loadings and the increased competition from other species. Although more appropriate for animal species, it is perhaps worthwhile to study ancient forest plant species in terms of source-sink population dynamics. 4.5. Conservation implications Ancient forests are of high importance for forest conservation, in particular because re-creation takes centuries (e.g. Peterken 1977, 1996). Peterken (1974) called ancient forest plant species extinction-prone. The main reason for this is their slow colonization abilities, so once they have disappeared or have declined for whatever cause, they only recover extremely slowly. Forest management, therefore, should aim at favouring ancient forest plant species by maintaining traditional deciduous forest management systems and reducing competitive plant species. The increase in the latter is favoured by nitrogen deposition and fertilizer drift from surrounding land uses, so ancient forest plants may in the long run bene®t from less intensive agriculture. The a€orestation policy of the EU should, in terms of ancient forest plant species, aim at expansion of existing forests, rather than isolated a€orestation. Increasing the size of forests o€ers better opportunities to the colonization by ancient forest plant species than the creation of new isolated forests. Acknowledgements This work is part of the Landeconet project, an EC funded research project on landscape ecology in changing agricultural landscapes (contract EV5VCT940528). Thanks to Kris Verheyen, an anonymous referee and Dr. Jean-Luc Dupouey for comments on the manuscript.

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