# The forest regeneration puzzle: biological mechanisms in humus layer and forest vegetation dynamics

Jean-François Ponge, Jean André, Olle Zackrisson, Nicolas Bernier, Marie-Charlotte Nilsson, Christiane Gallet

► To cite this version:

Jean-François Ponge, Jean André, Olle Zackrisson, Nicolas Bernier, Marie-Charlotte Nilsson, et al. The forest regeneration puzzle: biological mechanisms in humus layer and forest vegetation dynamics. Bioscience, 1998, 48 (7), pp.523-530. 10.2307/1313314. hal-00505386

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# The forest regeneration puzzle

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## Biological mechanisms in humus-layer and forest-vegetation dynamics

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Jean-François Ponge, Jean André, Olle Zackrisson, Nicolas Bernier, Marie-Charlotte Nilsson and Christiane Gallet

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Jean-François Ponge is professor at the National Museum of Natural History of Paris and Nicolas Bernier is associate professor in the same institution. They work at the Laboratory of General Ecology, 4 avenue du Petit-Chateau, 91800 Brunoy, France. Jean André and Christiane Gallet are both associate professors at the University of Chambery. They work at the Laboratory of Mountain Ecosystem Dynamics, CISM, 73376 Le Bourget du Lac Cédex, France. Olle Zackrisson is professor and Marie-Charlotte Nilsson is associate professor at the Swedish University of Agricultural Sciences. They work at the Faculty of Forestry, Department of Forest Vegetation Ecology, 901 83 Umeå, Sweden.

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## E-mail addresses:

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J.F. Ponge: jean-francois.ponge@wanadoo.fr

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J. André: jean.andre@univ-savoie.fr

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O. Zackrisson: olz@nana.slu.se

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M.C. Nilsson: marie-charlotte Nilsson@svek.slu.se

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C. Gallet: gallet@univ-savoie.fr

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## Introduction

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The tendency for managed coniferous forests to fail to regenerate naturally is a worldwide problem, especially in areas with severe climates, such as mountain and boreal zones (Sirén 1955, Mayer 1976). Because most of these ecosystems produce high levels of field- and cryptogamic-layer biomass (Persson 1980, Grier et al. 1981), it has been suggested that failure of coniferous forests to regenerate is somehow related to the ground vegetation and the related soil organic components. Although

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neglected by theoreticians, we may also assume that ground and below-ground organisms are

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involved in the processes by which disturbances and the resulting plant successions maintain these

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ecosystems (Finegan 1984).

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Forest ecosystem dynamics have long been explained by changes in floristic composition (Foster

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1988) and nutrient availability (Vitousek 1984). The passage from pioneer to late-successional plant

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communities has frequently been modelled (McCook 1994) and in a few instances studied

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experimentally (Facelli and Facelli 1993). Generally interactions between plants (including their

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immediate environment as a passive partner) have been considered responsible for forest succession.

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However, the below-ground components of any given ecosystem must also be taken into account

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before successional and steady-state patterns in plant communities can be fully understood (Cromack

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1981, Miles 1985; Nilsson 1994). A new emphasis on the study of forest ecosystem dynamics is

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emerging, in which new field and laboratory techniques are used to study biological processes related

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to plants and their interactions with soil. Although most of these studies bear only upon particular

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aspects of forest regeneration, we have tried to assemble these pieces into an integrated view of the

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regeneration puzzle. We focus mainly on European forests, because some major traits of American

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forests, for example the absence of native lumbricid earthworms (Fender and McKey-Fender 1990),

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may have a far-reaching influence on their dynamics.

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## The framework of forest dynamics

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Forest regeneration, the establishment of a new tree cohort, normally occurs during succession that

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involves plants, animals and microbes (Watt 1947, Cromack 1981, Finegan 1984, Oldeman 1990,

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Bernier and Ponge 1994). The first stages of the life of a tree (the seedling and the sapling stages) are

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dominated by strong environmental influences: intra- and inter-specific competition, and environmental

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stresses. Once the tree is firmly established, it increasingly influences its own environment, both

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above-ground, by shading and by intercepting rain, and below-ground, by absorbing water and nutrient

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ions, and releasing other ions and organic chemicals. Softwood as well as hardwood trees tend to

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acidify the soil because proton production, due to uptake and storage of nutrients by trees, exceeds

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proton consumption, due to mineral weathering, mineralization of organic matter, and nitrogen fixation

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in the soil (Ulrich 1986, Binkley and Richter 1987). The development of moder humus, that is, the
accumulation of organic matter in the form of the faeces of invertebrates deposited at the surface of
the soil profile, occurs as forest trees go through the phase of intense growth, the pole stage (Bernier
and Ponge 1994, Ponge and Delhaye 1995). At this time in their growth, most tree species may be
classed as soil acidifiers, except those that are able to reverse acidification through symbiotic nitrogen
fixation (Tarrant and Miller 1963) or by producing litter that decomposes at a high rate (Tamm 1990).

In old-growth forests, mull humus, defined by the abundance of earthworm faeces in mineral horizons
and rapid incorporation of litter, has been detected under adult trees, even under acidifying species
such as Norway spruce or European beech (Page 1974, Bernier and Ponge 1994, Ponge and Delhaye
1995). This change in organic matter decomposition is a key component of regeneration patterns. Any
process by which the accumulated forest organic matter is decomposed before the trees die, thus
making nutrients available to seedlings, will facilitate forest renewal. The low light intensities that limit
understory growth will diminish as large trees fall and gaps open in the canopy, which will improve
photosynthesis and thus growth rates of seedlings and saplings. However, a delay in the establishment
of new tree cohorts, for instance during unfavourable weather, might allow more competitive plant
communities to develop, including heath, grass, fern, or moss carpets, which generally impede the
establishment (Figure 1) or even the growth of tree species (Messier and Kimmins 1990, Ohlson and
Zackrisson 1992, Bernier and Ponge 1993, Dolling 1996, Zackrisson et al. 1997).

Thus important mechanisms influencing forest renewal operate through the soil system, including leaf
litter, and through ground vegetation (Nilsson et al. 1996). Knowledge of these mechanisms can
improve the ability of models to predict forest dynamics and climate-ecosystem interference (Wissel
1991, Andersson et al. 1996).

Soil microorganisms

Trees of nearly all species have their roots sheathed with soil ectomycorrhizal fungi, which play an
important role in nutrient and water uptake. The need for ectomycorrhizal symbiosis for the trees to
establish and grow well has long been known (Handley 1963). More recently, it has become clear that
the predominant ectomycorrhizal fungal species tend to change throughout the successional
development of forest stands (Mason et al. 1983, Gibson and Deacon 1988).
Changes in humus form during forest development may explain the accompanying succession of mycorrhizal fungi. For instance successions of mycorrhizal toadstools have been observed during the colonization of calluna heathland by birch trees, together with a shift from mor (slowly decaying litter with a poor comminution by fauna) to moder humus (Miles 1985). Temperate-zone late-successional forest trees such as spruce (Picea abies) and beech (Fagus sylvatica) often regenerate on mull humus (Ponge and Delhaye 1995, Bernier and Ponge 1994). By contrast, rapidly growing trees (the pole stage of these species) are commonly associated with moder humus. This association may explain why early stage fungi (which normally live in mull humus) are succeeded by other species during stand development. The fine root system of trees in moder humus is nearer the soil surface than is found in mull humus (Meyer and Göttsche 1971), which probably selects for ectomycorrhizal fungal strains that are able to live preferentially within litter layers (Rose et al. 1983). The physical disturbance of horizons resulting from the burrowing activity of earthworms and associated animals (moles, small rodents) observed under mature trees (Bernier and Ponge 1994, Ponge and Delhaye 1995) may help to explain the return of early successional mycorrhizal fungi.

Only few species and genotypes of fungi that can live symbiotically with trees as ectomycorrhizae are reported in ericaceous heathland with mor humus (Read 1991). This reduction in the ectomycorrhizal pool, despite sufficient dispersal of spores by wind or animals, will contribute to impede forest tree establishment when ericaceous species are present (Handley 1963, Zackrisson et al. 1997) and thus will preclude or considerably delay the renewal of forest ecosystems when gaps are invaded by these species (Dighton and Coleman 1992).

## Biochemical interactions

The growth and well-being of plants, animals and microbes can be favoured or inhibited by biochemical interactions with secondary metabolites. Vascular plants generally produce cocktails of different organic compounds, some of which may be waste products though many may be produced deliberately to make the plants unpalatable or toxic to herbivores (Zucker 1983). These compounds can be excreted (e.g., oils, waxes, resins), incorporated into cell walls (e.g., lignin, bark tannins), or enclosed in vacuoles within living cells (e.g. soluble tannins). When the plant tissues and organs die,
these organic compounds are liberated in the course of decomposition. In the meantime other inputs of
secondary metabolites occur by leaching of living parts. Certain of these compounds can affect other
organisms directly, and all can undergo biochemical reactions which alter humus properties. Below-
ground processes involving secondary compounds seem to be important in multi-species interactions
(Christy 1986, Hester et al. 1991). Thus seed germination and seedling growth can both be inhibited or
stimulated by organic compounds produced by living vegetation (Nilsson and Zackrisson 1992, Gallet
1994) or by litter and humus layers (Alvarez et al. 1979, Mallik and Newton 1988). These effects have
been assessed in laboratory experiments in which root competition effects were controlled for (Nilsson
1994). This biochemical control primarily affects the development of the root system of young tree
seedlings, but also ectomycorrhizal fungi and other soil microorganisms (Robinson 1972, Baldwin et al.
1983, Nilsson et al. 1993). Phenolic compounds, which are particularly abundant in the Ericaceae and
their allies, have often been implicated in these interactions, and their effects can be indirect, through
the binding of protein or other nitrogenous compounds (Howard and Howard 1990).

Biochemical interactions among organisms can thus help to explain successional patterns nearly as
well as do changes in resource availability, which are well-established theoretically (Heard 1994) but
poorly documented experimentally. However, in terms of biochemical control between plants, it can be
difficult to extrapolate results from laboratory to field conditions, because the properties and
persistence of biochemical compounds are strongly influenced by the soil conditions. For instance,
humus condition and fires can modify biochemical interactions between plants. Also, some plant
secondary compounds detrimental to other plant species or soil organisms can be adsorbed on soil
particles with a high surface area such as clay (Mortland et al. 1986), which may explain why soil
biological activity and plant growth may be enhanced by the artificial (Salonius 1983) or natural (Haimi
et al. 1992) disturbance of soil horizons. Similarly the decreased biochemical interference after a
forest-fire may partly be explained by the production of charcoal which, like clay particles, acts as a
detoxifier and a catalyzer in soil (Zackrisson et al. 1996).

Decaying wood and regeneration of coniferous species

The importance of rotting wood as a rooting medium for the establishment of coniferous trees such as
spruce (Picea spp.) and hemlock (Tsuga spp.) has been widely documented for different ecosystems,
especially under harsh climatic conditions (McCullough 1948, Harmon and Franklin 1989, Hofgaard 1993, Hörnberg 1995). Rotting wood has the remarkable property to adsorb or fix small organic molecules. This phenomenon stems from the aromatic nature of its main constituent, lignin, which becomes less bonded to cellulose as decomposition proceeds (Highley and Kirk 1979) and thus becomes open to chemical reactions. Despite structural changes with time, lignin remains polymerized (Kirk and Chang 1975) and acts as a binding agent for water-soluble phenolics (Bariska and Pizzi 1986), thus alleviating the inhibitory effects of phenolics on soil organisms and roots. Nitrogenous compounds such as ammonia, amino-acids and proteins, have also a strong chemical affinity for decaying wood (Mortland and Wolcott 1965). Because decaying wood fixes atmospheric nitrogen (Cornaby and Waide 1973), it can be considered as a reserve of nitrogen that increases during the course of wood decomposition (Graham and Cromack 1982). Decaying wood is also a reserve for water. Its high surface area and the capillary system formed by open xylem vessels create a strong water-retention capacity, which increases as decomposition progresses (Käärik 1974).

There are strong similarities between well-rotten wood and mull humus, despite their different chemical composition. Both strongly adsorb water and nutrients and have a high capacity for polymerizing phenolics and other organic metabolites, because of their high surface area and electronegativity. Indirect evidence of properties in common between decaying wood and mull humus is the fact that the widespread early-stage mycorrhizal fungus, *Thelephora terrestris* (Mason et al. 1983) occurs both as a mycorrhizal symbiont on trees rooting in mull humus (for instance in nurseries) and as a free-living saprophyte in rotting wood (Lanier et al. 1978, Bunnell et al. 1980). Thus decaying wood can be considered as another kind of humus favourable to the establishment of coniferous seedlings. But whereas mull humus is scarce in subalpine and boreal zones decaying wood is abundant (Sirén 1955, Bernier 1996). Thus, in the long-term management of forests in severe climates, it is probably desirable to maintain an abundance of large woody debris, such as dead trunks (Ponge et al. 1994).

## Scaling processes: from humus layers to ecosystem dynamics

At first sight it may seem unrealistic to extrapolate from the scale of tiny organisms such as field- and bottom-layer plant species, soil animals, and microbes, to the scale of the whole forest. However, the many feed-back processes involving trees and smaller plants, animals and microbes, lead logically to
such synthesis. Humus layers are the seat of major processes such as plant litter decomposition, nutrient and water uptake. As noted earlier, the establishment of a young tree or of a group of trees may determine changes in the immediate environment (e.g. shading, soil acidification) as its branch and root systems develop, and these in turn influence soil biological processes. Even though a tree is subjected to a strong selection from its own environment in the first years of its life, its influence becomes more and more prominent, and increases in space as its crown and root system enlarge and eventually fuse with those of other individuals. Similar effects may be observed with herbaceous and woody ground vegetation, especially when a single species becomes dominant and resistent (Emmer 1994, Bernier and Ponge 1994). In turn, humus layers built during the development of particular kinds of ground vegetation or of tree stands may influence the subsequent course of forest dynamics through their selective action on seedling establishment. Although these ideas were put forward a half-century ago by Watt (1947) for vascular plants, they have been neglected in modelling complex ecosystem dynamics and trying to understand the transition from small-scale to large-scale processes (Coleman et al. 1992).

In order to understand better the transition from small-scale to large-scale processes, the time required for the development of a given component of the forest should be taken into account. The colonization of regeneration niches (Grubb 1977) by individuals of plant species with strong competitive and phytotoxic properties may be considered as a starting point for long-term changes in the community (Messier and Kimmins 1991). Similarly important event is the colonization of the humus profile by individuals of species that have a strong influence on decomposition processes (such as some white-rot fungi of litter) or on humus-forming processes (such as burrowing earthworm species). Colonization by bracken (Pteridium aquilinum) and some heath and grass species, can lead to their spreading clonally to form large patches (Watt 1956, Maubon et al. 1995), unless conditions preclude such local dominance (Watt 1976, Hester et al. 1991). If such a patch appears, where the plant biomass is mostly of just a single species, then a new structural unit has appeared in the ecosystem. Locally, this structural unit will change environmental conditions (e.g. microclimate, humus), but nothing else may happen at the level of the ecosystem except when the eventual regeneration of the forest on this patch is impeded by competition, or because of the presence of a humus form unfavourable to tree seedling establishment, perhaps because of phytotoxic properties. The transition to a larger scale is, again, a question of repetitiveness. A patch of a clonal species may have only a temporary or small effect on a
limited part of the ecosystem. However, if this patch fuses with others similar in accompanying features (including soil communities), then the ecosystem may change locally to the extent that it must be classed as a new type (Figure 2). This has been shown in spruce (*Picea abies*) forests in France, where the development of mor humus inside patches of *Vaccinium myrtillus* prevented the establishment of spruce seedlings (Bernier et al. 1993, Bernier and Ponge 1994, Maubon et al. 1995). In the same way post-fire dominance of crowberry (*Empetrum hermaphroditum*), in Sweden has been shown to have long-term effects where it can lead to accumulation of mor humus and ultimately to a failure of Scots pine (*Pinus sylvestris*) stands to regenerate themselves as illustrated by Figure 1 (Zackrisson et al. 1997, Wardle et al. 1997).

## The landscape: competition between ecosystems at the edge of the forest

Altitudinal or latitudinal limits of forest ecosystems are generally viewed as transitions that relate the presence of tree species to climatic conditions (Sirois 1992) or to the influence of human activities (Zackrisson 1985). Recent research about the role of interactions between plants, animals and microorganisms in ecosystem dynamics gives a more detailed picture of the processes involved in the formation of the upper forest limit.

In mountain spruce (*Picea abies*) forests of the Alps, the establishment of spruce seedlings depends on the presence of mull humus or decaying wood (Ponge et al. 1994). In either case establishment occurs only when two processes are dominant in the ecosystem: the transformation of moder humus to mull through the development of burrowing earthworm populations (followed by active mineralization), and the decomposition of wood by fungi. We propose to name this, when mineralization exceeds photosynthesis, the heterotrophic phase. In contrast, during what we call the autotrophic phase, the growth of trees is characterized by carbon accumulation, increased uptake of nutrients, and the development of moder humus in the topsoil, thus photosynthesis exceeds mineralization. Both these phases show a de-coupling of the ion cycle of the ecosystem, i.e. are departures from equilibrium (Ulrich 1986). Any process by which the autotrophic phase restricts subsequent tree regeneration will degrade the forest, and in the long-term a treeless ecosystem may develop (Bernier 1996). The restriction of the regeneration niche by autotrophic processes creates a dynamic forest limit (Figure 3). When a severe climate limits the activity of decomposer organisms,
mull-forming processes may be impeded and, under even more extreme conditions, wood decay also
slows down. Other events such as atmospheric pollution, wide-scale deforestation, fires, or climate
changes, can also result in the loss of the heterotrophic phase (Zackrisson et al. 1995) and thus
degeneration of the forest ecosystem (Figure 1). Such degradation processes were described by Sirén
(1955) for boreal forests of northern Europe.

Forests may include patches of dwarf-shrub vegetation that may share several features with
ecosystems found above tree lines such as humus condition (Bernier and Ponge 1994) or mycorrhizal
systems (Read 1991). In a patchwork ecosystem, the different patches may variously interfere with one
another by plant-plant interactions, incompatibility between mycorrhizal systems, humus form, shading,
and other mechanisms, as illustrated by Figure 4. Thus the forest boundary should be viewed rather as
a fragmented and fluctuating limit influenced but not directly controlled by climatic conditions or
management.

These new ideas about the altitudinal or latitudinal limit of forests (the tree line) may have bearings
upon the more general concept of the ecotone (Van der Maarel 1990). An ecotone, defined as the
borderline between two distinct ecosystems, should be viewed as the zone in which ecosystems,
including soil organisms and ground flora, compete. Decreases in the competitive ability of forest
ecosystems, in particular in their renewal processes, may explain why changes in climate or human
activities may lead to profound changes difficult to reverse, such as desertification.

## Acknowledgements

The authors are greatly indebted to Pr. J. Miles, The Scottish Office, Edinburgh, UK, for its thorough
examination of the manuscript and improvement of the language and of clarity of the story.

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Fig. 1. The degraded boreal forest in northern Sweden. The ground vegetation is dominated by cowberry (Empetrum hermaphroditum) which impeds the renewal of the native Scots pine (Pinus sylvestris) forest through biochemical interactions. Cutting operations during the past two centuries have favoured this degradation.

Fig. 2. The transition from inter-species competition to competition between ecosystems in woody areas. A = forest structural species (single or multiple); B = heath structural species with clonal development; 1 to 6 = steps from A-dominated ecosystem to B-dominated ecosystem.

Fig. 3. Schematic representation of the dynamic forest limit on a northern slope (northern French Alps). A = autotrophic phase; H = heterotrophic phase (see text). Holorganic faeces are faeces of animals (enchytraeids, litter-dwelling earthworms, arthropods) consuming organic matter only, generally distributed in a horizon underlying recognizable leaf litter horizons. Their accumulation characterizes moder humus forms. Organo-mineral faeces are faeces of animals (mostly soil-dwelling earthworms) consuming organo-mineral material (endogeic species) or mixing organic matter to mineral matter (anecic species). Their accumulation characterizes mull humus forms. Leached organic matter is made of colloidal organic particles which can be leached through the soil profile and may chelate metals (podzolization). Mineral horizons are mainly composed of mineral particles. They underlay the biologically active part of the humus profile. Under 1000 m altitude, mull humus is dominant throughout the forest cycle, with a weak accumulation of organic faeces of small animals (moder humus) during the pole phase. Regeneration (of Norway spruce, silver fir) through seedling establishment after gap opening is easy, whatever the size of openings. Heath patches of bilberry (Vaccinium myrtillus) occupy small areas, with a thick mull humus, where regeneration is impossible. Between 1000 and 1800 m altitude, the forest cycle is characterized by strong changes in humus forms, with the appearance of a dysmoder humus (moder with a thick layer of organic faeces) during the pole phase, being progressively transformed into a dysmull (mull with imperfectly incorporated organic matter) in the mature phase, then in a true earthworm mull in gap openings provided a bilberry heath is not established before regeneration occurs (gaps of a sufficient size). The
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regeneration niche (of spruce) is restricted to places with a mull humus and decaying wood (multiple gaps). Bilberry heath occupies small gaps (mostly favoured at this elevation by badly-adapted silvicultural practices), with a mull humus not conducive to the establishment of spruce seedlings. Above 1800 m altitude, mull humus is always present, whether in coniferous thickets (Norway spruce, European larch, cembro pine) or in ericaceous heath (bilberry, rhododendron). Regeneration occurs through the establishment of seedlings on decaying wood and through layering only at the upper forest limit.

<caption>Fig. 4. Diagram (a) illustrating the separation of an altitudinal gradient into space-time processes.</caption>

Heath competes with forest at mid elevation where both can establish themselves in similar ecological conditions (gap openings, mull humus). This creates a dynamic equilibrium (inner forest limit), which can be strongly influenced by silvicultural practices (cutting operations) and natural disturbances (storms, avalanches). Diagram (b) showing favourable microsite conditions (mull humus) for the establishment of both tree seedlings (seed rain) and bilberry heath (development of subterranean parts) at mid elevation, and the fate of humus profiles under forest (moder) or heath (mor) ecosystems.
<figure><img src="image_2.png" /><figcaption>Fig. 1</figcaption></figure>

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<caption>Fig. 4</caption>