Acta Bot. Gallica, 2003, 150 (4), 373-382.

Are there herbaceous dryads in temperate deciduous forests ? by Guillaume Decocq1* et Martin Hermy2 1

Departement de Botanique, Université de Picardie Jules Verne, 1 rue des Louvels, F-80037 Amiens Cedex 1, France (phone : +33 322 827 761, fax : +33 322 827 469, e-mail : [email protected]) 2 Laboratory for Forest, Nature and Landscape Research, University of Leuven, Vital Decosterstraat 102, B-3000 Leuven, Belgique.

Abstract.- The concept of dryad (i.e. sedentary, structural, supportive species of mature forests) proposed by Van Steenis (1956) is extended to herbaceous plant species within the framework of temperate deciduous forests. A trait syndrome is derived for several forest herb species with similar dynamic behaviour within the silvigenesis. Three guilds are distinguished mainly according to the plant adaptations to photic stress : 1) shade-avoiders which are vernal geophytes, 2) shade-tolerants which are evergreen or wintergreen herbs or ferns, and 3) shade-adapted which are non-chlorophylian geophytes. Herbaceous species of these guilds are found to share many features such as a K-strategy, a long life span, a long juvenile period, a late sexual maturity, a low production of seeds, heavy barochoreous or myrmecochoreous diaspores, a lack of persisting seed banks and a capacity for vegetative multiplication and clonality.

Keywords : forest - guilds - herbaceous species – life history – succession. Résumé.- Le concept de dryade (i.e. espèce sédentaire et structurante des forêts matures) proposé par Van Steenis (1956) est ici appliqué aux espèces herbacées des forêts tempérées. Trois guildes sont distinguées en fonction du mode d’adaptation au stress photique : 1) les espèces évitant l’ombre, qui sont des géophytes vernales, 2) les espèces supportant l’ombre, qui sont des espèces sempervirentes (incluant des fougères), 3) les espèces adaptées à l’ombre, qui sont des géophytes non chlorophylliennes. Les espèces de ces trois guildes partagent de nombreux attributs, comme une stratégie K, une longévité élevée, une période juvénile prolongée, une maturité sexuelle tardive, une faible production de grosses graines barochores ou myrmécochores, une absence d’incorporation à la banque de graines du sol, une capacité élevée de multiplication végétative et de clonage. Mots clés : forêt – guildes – espèces herbacées – histoire naturelle – succession.

Commentaire :

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I. INTRODUCTION There is a growing interest in establishing non phylogenetic-based classifications of plant species for the understanding of ecosystem functioning. Nevertheless few studies about the dynamic behaviour of plant species have been published. Some “ eco-ethological ” classifications have been proposed, the greatest ones being those based on biological types (Raunkiaer, 1934), ecological groups (Duvigneaud, 1946 & 1974), method of diaspores dispersion (Ridley, 1930 ; Van der Pijl, 1972), morphological types (Barkman, 1988), adaptative strategies (Grime, 1977 ; Grime et al., 1988) and demographical strategies (Pianka, 1970). These classifications are sometimes labeled Plant-ecology-strategy schemes (PESS) since they have had as their goal predicting patterns in species distribution rather than predicting the effects of diversity on the provision or maintenance of ecosystem function (Westoby, 1998 ; Walker et al., 1999). New methods for classifying species have been recently developed ; they group species into types relating to the ecosystem-function role they performed. Such a categorization of species produces guilds or functional groups, called Plantfunction-type schemes or PFTS (see for example Walker et al., 1999 ; Weiher et al., 1999). It is noteworthy that this concept of guild has been initially introduced for plants, but is more largely used in animal ecology (Wilson, 1999). Within the scope of forest dynamics, few functional classifications have been proposed. Most of them deal with tropical forests and are often restricted to woody species (mainly trees, sometimes shrubs). The terms used for categorization were essentially based on life history and light requirements for germination, establishment and growth. Several classifications are bimodal like superior vs. inferior competitors (Connell, 1978), gap vs. non-gap species (Brokaw, 1985), primary vs. secondary species (Hubbell & Foster, 1986) or pioneer vs. climax species (Swaine & Whitmore, 1988). Others are much more complex -and often complicated- with numerous categories : 7 groups (pioneer - early successional - mid successional - late successional, with intermediary stages between each of these groups) according to Summerbell (1991) and 9 groups (3 pioneer - 3 “ building phase ” - 3 “ shade-tolerant ”) according to Condit et al. (1996). Less known but of strong interest is the “ ethological ” classification proposed by Van Steenis (1956), more recently taken up by Rameau (1987 & 1992). This was mainly defined for tree species, according to their dynamic behaviour and function within the silvigenesis in relatively undisturbed and non extreme environments. Three main categories have been distinguished : pioneer species which are high productive edificator species, like Populus spp., Salix spp. or Alnus spp., early successional (or late pioneer) species which are of intermediate properties, like Prunus spp., Fraxinus spp., Acer spp. or Quercus spp., and late successional (or successor) species, also called “ dryads1 ”, which are sedentary, structural, supportive species of the mature forest, like Fagus spp., Abies spp. or Picea spp. Of course pioneer species are able to become sedentary and structural in disturbed (Alnus glutinosa in floodplain forests for example) or stressed (Betula alba on oligotrophic soils for example) environments, but in such environments forest can not reach maturity and thus dryads are not able to establish themselves. The main criteria defining these categories are summurized in Table 1. Under certain conditions, late pioneer or even successor species may participate in pioneer communities (e.g. Quercus, Acer or Picea), according a stochastic process. Such opportunistic species were labelled “ nomadic ” species by Van steenis (1956). This scheme is very close to the more explicit one of Knapp (1974) who distinguished three main types too : edificator (= constructive) species, consolidating species and destructive species, a fourth type being also composed by opportunistic species.

1dryad

: from the Latin dryas, -adis borrowed from the Greek druas, -ados, nymph of oak.

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Table I.- Criteria defining the eco-ethological groups (after Rameau, 1987 & 1992). Tableau I.- Critères de définition des groupes éco-éthologiques (d’après Rameau, 1987 & 1992) Environment Strategy Growth rate Fecondity Diaspore dispersion Wood Longevity Architecture

Pioneer species

Late-pioneer species

Dryads

lighted r rapid very high

medium r to K medium medium

shaded K low low

anemochoreous soft low (< 50 years) simple

highly variable medium to hard medium (> 100 years) variable

barochoreous hard high (> 200 years) complex

II. A SUBJECTIVE BUT USEFUL CONCEPT Even if this categorization of species is subjective (because it is based on observations of ecosystems in which it is taken for granted that functional types exist and that these can be defined inductively), it may be useful since it provides a basis for grouping the large number of species into a smaller number of functional types. Recently, Gitay et al. (1999) have found evidence of congruency between subjective classifications and dynamic data-driven ones and showed that the latter produced groups that match the intuitive interpretation of experts familiar with the forest. It is also an easy classification because it may be deduced from information that is readily available for most parts of the world. Finally it has the advantage of integrating both plant ecology-strategy and plant function attributes. Within this trimodal classification, the concept of dryad, much less used than the one of pioneer, presents a great heuristic interest. It may be particularly useful for multiple goals as it estimates the degree of maturity of a forest, verifies the integrity of a silvatic mosaic, indicates an inhibition in the forest succession, assesses the influence of forest management or other disturbances on vegetation, monitors a sustainable silviculture, and so on. That is why it is worthwhile trying to extend this concept to herbaceous species. In forest ecosystems herbs and grasses are important components because they may use a considerable part of the ecological production potential and so be indicators for the state of the whole forest (Oldeman, 1990). Moreover, by virtue of the differences in their sizes, longevity and living space, herbaceous species are supposed to react more quickly to environmental changes and disturbances than woody species do (Carlile et al., 1989 ; Decocq, 2000). There is a clear differential maturation among the different forest synusiae. The coenological saturation (steady state) usually occurs earlier within the herbaceous synusiae than in the woody ones as well as the occurence, abundance or dominance of dryad species (e.g. de Foucault et al., 1996). In this preliminary approach we would like to introduce the concept of dryad applied to forest herbaceous species, in advance of a complete typology of the dynamic behaviour of forest herbaceous species that would require further investigations. We restrict our considerations to European temperate deciduous forests, for which the concepts of tree dryad and shrub dryad have already shown their usefulness and efficiency in surveying forest mosaics (e.g. Rameau, 1987 &

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1992) as well as in monitoring or simulating forest dynamics (e.g. Burgmann, 1996). Here we try to derive a trait syndrome (sensu Chapin et al., 1993, i.e. a repeated attribute combination) that defines the status of dryad for several forest herb species with similar dynamic behaviour in the silvigenesis. For this purpose we use a set of morphological and life-history characters based on theoretical considerations (looking for inter-synusiae invariants in the behaviour of species and making analogies with woody dryads), personal field experience and available data from the literature. For the latter, we firstly analyze some community ecology studies to select some species which were potential dryads. Different kind of studies were used : those comparing understorey composition between ancient and recent forests (see for example Peterken, 1974 ; Honnay et al., 1998 ; Hermy et al., 1999), others concerning either primary or secondary successions, and focusing on the establishment and maturation of forest communities (see for example de Foucault et al., 1996 ; Elgersma, 1998), and also studies on primary forests or, at least, forests protected from a significant anthropogenic pressure for many centuries (see for example Williamson, 1975 ; Lemée, 1978 ; Falinski, 1986 ; Koop & Hilgen, 1987). Secondly, we have reviewed the autoecological data avalaible on each species selected in order to derive a “ dryad syndrome ” for forest herbaceous species (e.g. Sernander, 1906 ; Ridley, 1930 ; Salisbury, 1942 ; van der Pijl, 1972 ; Al-Mufti et al., 1977 ; Bierzychudek, 1982 ; Grime et al., 1988 ; Crawley, 1990 ; Packham et al., 1992).

III. WHAT IS EXPECTED A HERBACEOUS DRYAD TO BE ? A dryad characterizes mature forests (particularly the biostatic phase of the climax forest) of non extreme environments i.e. 1) undisturbed forests which are only submitted to natural silvigenetic cycles without any significant anthropogenic influence since a long time (a few centuries for a temperate deciduous forest considered at the level of the whole forest mosaic), 2) forests where the succession is not impaired by one or more “ inhibiting factors ” such as too extreme climatic conditions, an extreme pH or nutrient content, severe erosion, or important herbivory. As distinct synusiae fit different kinetics of maturation, the herbaceous synusiae should theorically reach the climatic “ equilibrium ” before the woody synusiae (see for example Decocq et al., 1996 ; de Foucault et al., 1996). Consequently, herbaceous dryads may be associated with late pioneer or even pioneer woody synusiae. A herbaceous dryad should be a true forest species, strongly adapted to the stressing forest environment. The forest understorey environment is characterized by four kind of stress : severe shading, low temperatures, deposition of leaf litter and depletion of mineral nutrients and water in the soil (Grime, 1977 ; Oldeman, 1990 ; Packham et al., 1992). In our opinion, the most selective ecological factor for understorey vegetation into forest ecosystems is shading, because soil-related stress factors and temperature are strongly determined by light avalaibility (for example, the accumulation of humus is favoured by the lack of light, particularly on acid soils under oceanic influence). Moreover many ecophysiological processes, like photosynthesis or germination for example, depend on the quantity and quality of the light that are let through by canopies. So, we conclude that herbaceous dryads must be plant species firstly adapted to shading environments but also able to develop on soils with a more or less thick layer of humus. We found three pathways for the plant species adaptation to photic stress (Table 2). • Plants may adapt their vegetative cycle to the seasonal variations of forest climate in order to benefit from the maximum of light when it occurs. In this case, the plant is a vernal species

377 Table II.- Features of the different guilds of herbaceous dryads in temperate deciduous forests. RGR : relative growth rate (g / g x week). Tableau II.- Caractéristiques des différentes guildes de dryades herbacées des forêts tempérées caducifoliées. RGR : taux de croissance relatif (g/g x semaine) Shade-avoiders Biological type ( sensu Raunkiaer) Phenology/biology Established strategy ( sensu Grime) Demographical strategy ( sensu Pianka) Growth rate Reproduction Sexual maturity Fecondity

Seeds

Diaspore dispersion Longevity Architecture

Ecology

Phylogenetics

Examples

Geophyte

Shade-tolerants Chamaephyte or geophyte

vernal

Shade-adapted

Hemicryptophyte or geophyte

Geophyte non-chlorophylian (saprophytic or parasitic)

Evergreen or wintergreen

SR -> CSR

S -> CS

SC

SC -> C

K

K

K

K

low (RGR* < 0,5)

low (RGR* < 0,5)

rather low (no data)

very low (?) fungi-dependant

vegetative and/or generative

mainly vegetative

mainly vegetative

vegetative and generative

late (> 5 years)

variable

late (> 5 years)

late (> 5 years)

high seed production but low germination rate

low seed production

high spore production but effectiveness unknown

not well known and fungidependant

a few ( 25x40µm) persistance unknown

barochory and/or myrmecochory

myrmecochory, barochory or autochory

autochory (anemochory ?)

many centuries ? (coloniarity)

many centuries ? (coloniarity)

many centuries ? (coloniarity) possible reiteration

very complex (modular herbs)

possible reiteration

ancient coppice-woods on productive sites

ancient forests on more or less productive sites

large but optimum in ravine forests

Monocots, sometimes dicots Hyacinthoides non-scripta Anemone nemorosa Scilla liliohyacinthus

Dicots Vinca minor Lamium galeobdolon Galium odoratum Oxalis acetosella

Ferns Dryopteris spp. Polystichum spp. Asplenium scolopendrium

heavy seeds (> 2 mg) persistance unknown barochory and/or myrmecochory long (many decades ?) no data old oak-beech forests with a thick humus layer Monocots or dicots Neottia nidus-avis Epipogon aphyllum Monotropa hypopytis

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(“ shade-evader ” sensu Packham et al., 1992 or “ phenological avoider ” according to Weiher et al., 1999) which avoid severe shading by accomplishing the totality or most of its cycle in the off season, between the end of winter (when the thermic stress becomes less strong) and the end of spring (when the photic stress becomes maximal because of the foliation of overstorey vegetation). But the deep shade is not the only constraint for vernal species. Litter has been found to be an important factor limiting vernal herbs whose full expansion coincides also with the seasonal minimum in litter density (Al-Mufti et al., 1977 ; Sydes & Grime, 1981). We must therefore consider that the vernal strategy is an adaptation to both light and, to some extent, also litter stress. The most important characteristic of the vernals is their ability to exploit temporary periods during the spring in which there are opportunities for the growth of species of low competitive ability ; that is why they are sometimes labeled as “ perennial ephemeroids ” (Al-Mufti et al., 1977) or “ stesstolerant ruderals ” (Grime et al., 1988). Most of them are adapted to coppicing so that they are sometimes considered as species linked to a certain type of silviculture rather to a natural periodicity in the forest environment. But we rather understand this “ shade-evading ” strategy as a strong adaptation to the stressing forest environment and see vernal species as true forest species, even if their frequent dominance into the understorey vegetation is unambiguously favourized by the coppice treatment. Numerous species develop such a strategy, particularly on fertile soils : for example, Adoxa moschatellina, Narcissus pseudonarcissus, Hyacinthoides non-scripta, Scilla bifolia, Anemone nemorosa, Cardamine heptaphylla, Dentaria pinnata. Most of these species are geophytes with very specialized underground strategies (i.e. bulbs, rhizomes). They usually form large colonies. Following the classification of Grime et al. (1988), they may be considered as intermediary between the SR and the CSR strategies. A lot of these species are also slow-growing and their sexual maturity quite often occurs late in the life cycle (no neotony i.e. no appearance of adult characters in juvenile organisms, see Oldeman 1990) that allows a comparison with the K strategy of Pianka (1970). Making an analogy with arborescent dryads, these species usually have a rather low seed production (with exceptions like Hyacinthoides non-scripta). Moreover the seeds have usually a weak longevity (no incorporation in the seed bank) and a bad dispersal capacity (mainly barochoreous, less often myrmecochoreous). Vegetative regeneration usually predominates on sexual reproduction. A few species are also able to reiterate, which is an exceptional phenomenon for monocots (Oldeman, 1990). • Plants may provide ecophysiological and metabolism adaptations to the low light levels that characterize the understorey environment (“ abaptation ” sensu Begon et al., 1996). Two contrasted ways in plant adaptation may be distinguished : species not requiring a lot of light because of their high content of chlorophyll (“ shade-tolerant ” species like Vinca minor, Galium odoratum, Lamium galeobdolon, Oxalis acetosella, etc.) and the non-chlorophylian species which are not light-dependent (“ light-independent ” species like Neottia nidus-avis, Epipogon aphyllum, Monotropa hypopytis, Lathraea squamaria, etc.). Chlorophyll high-containing species are usually chamaephytic, evergreen or wintergreen perennial species which are able to build more or less large colonies. Such species usually present many other physiological adaptations : a spongy mesophyll with very large air spaces and palissade cells in leaves, a thin cuticle, a low vein density, large epidermal cells, etc. (Packham et al., 1992). They possess low metabolic rates which lead to low light compensation points. Moreover light saturation is attained at low levels. All of them are Dicots. Their behaviour is close to the strategy K of Pianka since the construction of the colony by vegetative multiplication seems to have priority on sexual reproduction. They are intermediate between the S and the CS groups of Grime. Vegetative multiplication is the main mechanism of plant propagation, usually thanks to stolons that allow the formation of long-lived creeping carpets of plagiotropic stems and cover quite large areas before dispersing seeds. Sexual reproduction may be lacking. When it occurs, barochory or myrmechory are the main ways for seed dispersion. Vitality of the seeds is not well known.

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Although reiteration ability is rare among herbs, it seems to be more frequent within the species tested. Neotony is also lacking. The field impression is that these modular herbs forage extensively for light : they mobilize all their energy in the construction of a foliar area as large as possible to capture the maximum of light. Consequently, flowering and fruiting are secondary preocupations and are not so rhytmic with the seasons. Therefore the flowering of these species seems to be proportional to solar irradiation : species like Vinca minor or Lamium galeobdolon do not flower in the most shaded environment although they abundantly flower in clearings or after a clear-cut. These field observations suggest that such species only flower when they have an excess of energy they can not spend in the construction of the colony. Because they are evergreen or wintergreen perennial species, they may be able to capture light whatever the season, the limiting factor becoming temperature. They may be considered as “ capitalists ” (sensu Mac Leod, 1894 in Hermy & Stieperaere, 1985) since there is a “ continuous and rapid reinvestment of captured resources (capital) in new leaves and roots in order to gain access, monopolize and exploit new reserves of ressources ” rather than allocating ressources to reproductive activities. Some fern species are also wintergreen (for example Asplenium scolopendrium, Polystichum aculeatum, etc.) and may be considered as dryad species. But further investigations are still needed because of the lack of knowledge on the autoecological characteristics of most of the species (longevity, spore dispersal and incorporation in the seed bank). Such species also often build more or less large colonies under certain mesoclimatic conditions, particularly in ravine forests where the herbaceous environment is highly shaded and moist. Vegetative multiplication is assumed by other types of specialised organs, like propagules, adventicious buds on roots or epiphyllous prothalles. Plant species without chlorophyll (or with little or non-functionnal chlorophyll) are not or poor light-dependant. So they are able to establish themselves in the most shaded environments. They develop two ways of life : saprophytism or parasitism. Saprophytic species feed on dead organic matter, so that they require forest soils with a thick humus layer as in beech forests for example. This could also be understood as an adaptation to the edaphic stress as evoked above. Nutrition depends on a symbiotic association with other organisms, mainly fungi. This implies complex relations between different organisms within the forest ecosystem that may be understood as a proof of the stability of the system. Such species are usually geophytic Monocots like orchids (For example Neottia nidus-avis, Epipogon aphyllum, Coralorhiza trifida, etc.). Parasitic species develop an extreme strategy since their life depends on the durability of the relationship with their host. This implies that the forest ecosystem must not be disturbed. Such species are usually geophytic Dicots like Orobanchaceae (for example Monotropa hypopytis, Lathraea squamaria).

IV. A TRAIT-SYNDROME FOR HERBACEOUS DRYADS These three guilds of species, 1) shade-avoiders, 2) shade-tolerants and 3) lightindependents, are potentially dryads. They share many features : a K strategy (sensu Pianka), a life span quite long, a long juvenile period and a late sexual maturity, a low production of heavy seeds, a mainly barochorous dispersal, no or a very short dormancy, no persisting seed banks. All of them mainly reproduce vegetatively which results in clones of individuals, but only the two first types are able to build more or less large colonies. We consider this result of major importance for three main reasons. Firstly, there is a correlation between clonality and longevity in plant species (Cook, 1985). Arborescent dryads usually have a long life span and a low rate of growth. They are also able to build complex architectures to increase their biomass (K strategy sensu Pianka). By making an

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analogy, herbaceous dryads should be searched for within slow growing species having a high longevity. But even if most of the species tested are able to reiterate, herbs are unable to build complex architectures to increase their biomass. An alternative may be the ability to establish colonies which is strongly linked to the capacity for a vegetative multiplication. Secondly, extensive integration has been suggested to be an adaptation to the low average availability of one or more resources during the growing season (Jonsdottir & Watson, 1997). It appears to benefit to plants in resource-poor environments by providing them with a means of conserving scarce resources, facilitating a developmental division of labour between ramets of different generations, and exploiting patchily distributed resources at multiple sites, as well as providing a mechanism for strong intraclonal control of ramet production through apical dominance. By staying interconnected and maintaining physiological integration between ramets, clonal fragments can capture unpredictable pulses in a resource-poor environment (d’Hertefeldt & Jonsdottir, 1999). Exploitation of these pulses through morphological responses may be too slow or too costly for the plant in these environmental conditions. Therefore, a “ sit-and-wait strategy ”, where old but functional stems and leaves are already widely distributed and ready to exploit such unpredictible pulses, can be highly adaptative (d’Hertefeldt & Jonsdottir, 1999). Even if these features were mainly reported for resources like water or soil nutrients in ecosystems, we think that they may be also possible for light within forest ecosystems. Such a strategy of foraging for light seem to characterize “ shade-tolerant ” species. Thirdly, generative reproduction imposes the recruitment of matter of vital importance for the plant individual, its growth and vegetative multiplication. Flowering is maximal in the most hostile environments where increasing biomass is impaired by the lack of avalaible water or nutrients as well as by the excess of light or heat. Generative reproduction is a chance for a plant individual 1) to produce new genotypes better adapted to the new environmental conditions, 2) to migrate toward a better environment thanks to seed production (Reichholf, 1993). In undisturbed forest ecosystems, these plant species spend all their energy in vegetative multiplication and construction of the colony since generative reproduction is not of vital importance. Consequently herbaceous dryads are expected not to abundantly flower under optimal environmental conditions. Nevertheless, nearly all these species flower and produce seeds regularly although they replace themselves primarily vegetatively (Bierzychudek, 1982). Further investigations are needed 1) to reach an accurate definition of dryads in the scope of temperate deciduous forests that implies a quantification of most of the features mentioned above, 2) to extend this concept to other types of forest, 3) to get a complete classification of herb species according to their dynamical behaviour. Such a classification would show a great heuristic interest and should probably be generalized to all types of forest. This also emphasizes the lack of objective differences between PESS and PFTS since ecology-strategy traits and functional traits are strongly linked, both contributing to the dynamic behaviour of plant species. Aknowledgements - We would like to thank Eddy van der Maarel for his very helpful comments on the initial draft.

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REFERENCES Al-Mufti M.M., C.L. Sydes, S.B. Furness, J.P. Grime & S.R. Band, 1977.- A quantitative analysis of shoot phenology and dominance in herbaceous vegetation. J. Ecol., 65, 759-791. Barkman J.J., 1988.- New systems of plant growth forms and phenological plant types. In: Plant form and vegetation structure. M.J.A. Werger, P.J.M. van der Aart, H.J. During & J.T.A. Verhoeven (eds.), SPB Academy Publications, The Hague, 944. Begon M., J.L. Harper & C.R. Townsend, 1996.Ecology: individuals, populations and communities, 3rd ed. Sunderland, Sunderland. Bierzychudek P., 1982.- Life histories and demography of shade-tolerant temperate forest herbs: a review. New Phytol., 90, 757-776. Brokaw N.V.L., 1985.- Trefalls, regrowth and community structure in tropical forests. In: The ecology of natural disturbance and patch dynamics. S.T.A. Pickett & P.S. White (eds.), Academic Press, New York, 53-69. Burgmann H., 1996.- Functional types of trees in temperate and boreal forests: classification and testing. J. Veg. Sci., 7, 359-370. Carlile D.W., J.R Skalski., J.E. Batker, J.M. Thomas & V.I. Cullinan, 1989.- Determination of ecological scale. Landscape Ecol., 2, 203-213. Chapin F.S.III, K. Autumn & F. Pugnaire, 1993.Evolution of suites of traits in response to environmental stress. Am. Natur., 142, 78-92. Condit R, S.P. Hubbell & R.B. Foster, 1996.Assessing the response of plant functional types to climatic change in tropical rain forest. J. Veg. Sci., 7, 405-416. Connell J.H., 1978.- Diversity in tropical rain forests and coral reefs. Science, 199, 1302-1310. Cook R.E., 1985.- Growth and development in clonal plant populations. In: Population biology and evolution of clonal organisms. J.B.C. Jackson, L.W. Buss & R.E. Cook (eds.), Yale University Press, New Haven, 259-296. Crawley M.J., 1990.- The population dynamics of plants. Phil. Trans. R. Soc. Lond. B., 330, 125-140. Decocq G., B. de Foucault & J.P. Amat, 1996.- Flore et végétation impliquées dans la recolonisation de l’ancien fort de Mayot (Aisne, France). In: Sociétés humaines et milieux humides en Picardie. E.P. Désiré & R. Regrain (eds.), Editions du CTHS, Paris, 171-182. Decocq G., 2000.- The “ masking effect ” of silviculture on substrate-induced plant diversity in oak-hornbeam forests from northern France. Biodiv. Conserv., 9, 1467-1491. Duvigneaud P., 1946.- La variabilité des associations végétales. Bull. Soc. Roy. Bot. Belg., 78, 107-134. Duvigneaud P., 1974.- La synthèse écologique. Doin, Paris, 296p.

Elgersma A.M., 1998.- Primary forest succession on poor sandy soils as related to site factors. Biodiv. Conserv., 7, 193-206. Falinski J.B., 1986.- Vegetation dynamics in temperate lowland primeval forests. Geobotany, 8, 1-537. Foucault B. (de), J.R. Wattez, J.P. Amat & M.A. Valke, 1996.- Observations sur la reconstitution du tapis végétal après les combats de la Grande Guerre (1916) dans la région d’Albert (Somme). In: Sociétés humaines et milieux humides en Picardie. E.P. Désiré & R. Regrain (eds.), Editions du CTHS, Paris, 147-170. Gitay H., I.R. Noble & J.H. Connell, 1999.- Deriving functional types for rain-forest trees. J. Veg. Sci., 10, 641-650. Grime J.P., 1977-. Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary theory. Am. Natur. 111, 1169-1194. Grime J.P., J.G. Hodgson & R. Hunt, 1988.Comparative plant ecology, a functionnal approach to common british species. Unwin Hyman Ltd, London. Hermy M. & H. Stieperaere, 1985.- Capitalists and proletarians (Mac Leod 1894): an early theory of plant strategies. Oikos, 44, 364-366. Hermy M., O. Honnay, L. Firbank, C. GrashofBokdam & J.E. Lawesson, 1999.- An ecological comparison between ancient and other forest plant species of Europe, and the implications for forest conservation. Biol. Conserv., 91, 9-22. d’Hertefeldt T. & I.S. Jonsdottir, 1999.- Extensive physiological integration in intact clonal systems of Carex arenaria. J. Ecol., 87, 258-264. Honnay O., B. Degroote & M. Hermy, 1998.- Ancientforest plant species in western Belgium : a species list and possible ecological mechanisms. Belg. J. Bot., 130, 139-154. Hubbell P.S. & R.B. Foster, 1986.- Biology, chance and history of the structure of tropical rain forest tree communities. In: Community ecology. J. Diamond. & T.J. Case (eds.), Harper & Row, New York, 314-329. Jonsdottir I.S. & M.A. Watson, 1997.- Extensive physiological integration : an adaptative trait in ressource-poor environments ? In: The ecology and evolution of clonal plants. H. de Kroon & J. van Groenendael (eds.), Backhuys Publishers, Leiden, 109-136. Knapp R., 1974.- Some principles of classification and of terminology in successions. In: Vegetation dynamics. R. Knapp (ed.), Junk, The Hague, 167177. Koop H. & P. Hilgen, 1987.- Forest dynamics and regeneration mosaic shifts in unexploited beech (Fagus sylvatica) stands of Fontainebleau (France). For. Ecol. Manage., 20, 135-150. Lemée G., 1978.- La hêtraie naturelle de Fontainebleau. In: Problèmes d’écologie: structure

382 et fonctionnement des écosystèmes terrestres. M. Lamotte & F. Bourlieu (eds.), Masson, Paris, 75128. Oldeman R.A.A., 1990.- Forest: elements of silvology. Berlin, Springer-Verlag, 624p. Packham J.R., D.J.L. Harding, G.M. Hilton & R.A. Stuttard, 1992.- Functional ecology of woodlands and forests. Chapman & Hall, Cambridge, 407p. Peterken G.F., 1974.- A method of assessing woodland flora for conservation using indicator species. Biol. Conserv., 6, 239-245. Pianka E.R., 1970.- On r and K selection. Am. Natur., 104, 592-597. Rameau J.C., 1987.- Contribution phytoécologique et dynamique à l'étude des écosystèmes forestiers. Applications aux forêts du nord-est de la France. Thesis, University of Besançon, Besançon, 340p. Rameau J.C., 1992.- Dynamique de la végétation à l'étage montagnard des Alpes du sud. Première approche d'une typologie des hêtraies et hêtraiessapinières. Les applications possibles au niveau de la gestion. Rev. Forest. Franc., 44, 393-429. Raunkiaer C., 1934.- The life forms of plants and statistical plant geography. Collected papers. Clarendon, Oxford, 632p. Reichholf J., 1993.- Comeback der Biber: Ökologische Überraschungen. Verlag CH Beck, München. Ridley H.N., 1930.- The dispersal of plants throughout the world. L. Reeve and Co, Ashford. Salisbury E.J., 1942.- The reproductive capacity of plants. Bell, London, 244p. Sernander R., 1906.- Entwurf einer Monographie der Europäischen Myrmecochoren. Almquist, Uppsala. Summerbell G., 1991.- Regeneration of complex notophyll vine forest (humid subtropical rainforest) in eastern Australia - a review. Cunninghamia, 2, 391-409. Swaine M.D. & T.C. Whitmore, 1988.- On the definition of ecological species groups in tropical rain forests. Vegetatio, 75, 81-86. Sydes C.L. & J.P. Grime, 1981.- Effects of tree leaf litter on herbaceous vegetation in deciduous woodland. 1. Field investigations. J. Ecol., 69, 237248. Van der Pijl L., 1972.- Principles of dispersal in higher plants. Springer, Heidelberg, 162p. Van Steenis C.G.J., 1956.- Basic principles of rain forest sociology. Study of tropical vegetation. Actes du colloque de Kandy, 195, 159-165. Walker B., A. Kinzig & J. Langridge, 1999.- Plant attribute diversity, resilience, and ecosystem function : the nature and significance of dominant and minor species. Ecosystems, 2, 95-113. Weiher E., A. van der Werf, K. Thompson, M. Roderick, E. Garnier & O. Eriksson, 1999.Challenging Theophrastus: a common core list of plant traits for functional ecology. J. Veg. Sci., 10, 609-620. Westoby M., 1998.- A leaf-height-seed (LHS) plant ecology strategy scheme. Plant Soil, 199, 213-227.

Williamson G.B., 1975.- Pattern and serial composition in an old growth beech-maple forest. Ecology, 56, 727-731. Wilson J.B., 1999.- Guilds, functional types and ecological groups. Oikos, 86, 507-522.