Review Article
Shifting Mosaics in Grazed Woodlands Driven by the Alternation of Plant Facilitation and Competition H. 01ff1, F. W. M. Vera2 J. Bokdam 1, E. S. Bakker 1, j• M. Gleichman 1, K. de Maeyer 1, and R. Smit1 1 Nature Conservation and Plant Ecology Group, Wageningen Agricultural University, Wageningen, The Netherlands 2 Ministry of Agriculture, Nature Management and Fisheries, Department of Ministers Office, Strategic Policy Division, Den Haag, The Netherlands Received: September 29, 1998; Accepted: January 13, 1999
Abstract: Free-ranging large grazers, such as cattle and horses,
are increasingly reintroduced to former agricultural areas in Western Europe in order to restore natural and diverse habitats. In this review we outline mechanisms by which large grazers induce and maintain structural diversity in the vegetation (mosaics of grasslands, shrub thickets and trees). This variation
in vegetation structure is considered to be important for the conservation of biodiversity of various plant and animal groups. The process of spatial association with unpalatable plants (associational resistance) enables palatable plants to establish in grasslands maintained by large grazers. In this way, short unattractive (thorny, low quality or toxic) species facilitate taller unattractive shrubs, which facilitate palatable trees, which in turn outshade the species that facilitated their recruitment. Established trees can, therefore, not regenerate under their own canopy, leading to cyclic patch dynamics. Since this cyclic dynamic occurs on a local scale, this contributes to shifting mosaics. The mechanisms involved in creating and maintaining the resulting shifting mosaics are described for temperate floodplain and heathland ecosystems, including the effects on nutrient transport within grazed landscapes. How grazing leads
to shifting mosaics is described in terms of plant functional types, allowing potential generalisation to other ecosystems.
Introduction Structural diversity of the vegetation has been shown to be
important both for plant diversity (01ff and Ritchie, 1998132]) and for animal diversity (Pianka, 1967; Root, 1973[; Cody,
19751441). Hence, for the conservation and restoration of biodiversity, it is important to gain insight into the processes maintaining variation in vegetation structure. 1975113]; Root,
In temperate ecosystems without large grazers or fire, succession usually quickly proceeds from grassland and shrub thickets to tall deciduous trees which can regenerate in their own shade (Bazzaz, 1979161; Pickett et al., 1987136]; Tilman, 19871521). Since the duration of the mature tree stage is the longest, closed forest is the prevailing vegetation structure under these conditions (see, e.g., Friend et al., 19931181; Pacala et
al, 1996[]), except where edaphic conditions do not sustain tree and shrub growth. Spatial variation in vegetation structure in these temperate woodlands is mainly maintained by so-called gap-phase dynamics. The driving force causing regeneration of trees is generally the death of mature trees which opens temporal opportunities for light-demanding, early seral woody species, which are in turn outcompeted by
The resulting interaction web of grasses, unpalatable forbs and
taller species able to regenerate in their shade (Shugart,
shrubs, palatable light-demanding trees and shade-tolerant
1984146]; Leibundgut, 1984128]; Remmert, 1991141]; Friend et al., 19931181; Pacala et al., 1996133]).
trees is discussed, and was found to contain various interesting direct and indirect effects. The key process contributing to spatial diversity in vegetation structure is the alternation of positive (facilitation) interactions between plant species at one life cycle stage, and competitive displacement at another stage.
Grazing thus causes directional successional sequences to change to shifting mosaics. The implications of this theory for nature conservation are discussed, including the relevant management problems, possible choices and practical solutions. We conclude that the theoretical framework outlined in this review provides helpful insights when coping with nature conservation issues in temperate woodland habitats.
However, most studies stressing the importance of this type
of gap-phase dynamics in temperate woodlands have focussed on ecosystems where man had already driven the naturally occurring large herbivores to extinction. Recently, Vera (1997160]) used historical evidence to argue that different successional patterns and spatial mosaics are expected when freeranging large herbivores are present. In this review, we will
summarise the arguments made by Vera and others about how woody species may regenerate in the presence of large grazers, and how their presence affects spatial and temporal variation in vegetation structure and biodiversity.
Key words: Herbivory, large herbivores, grazing, shifting mosaics, woodlands, cyclical succession competition, facilitation.
Knowledge of these processes is currently needed because restoration of ecosystems with free-ranging large grazers is increasingly being practised in Western Europe (de Bruin et al.,19871161; van Wieren, 19891581; Helmeretal., 19921221; Siebel,
Plant biol. 1(1999)127—137 © Georg Thieme Verlag Stuttgart. New York ISSN 1435-8603
1998147]; Piek, 19981351). In the Netherlands alone, about 50,000 ha of agricultural land (uniform pastures and arable fields) will be purchased for this purpose within the next 20
127
128 Plant blot. 1 (1999)
H. 01ff et al.
years by nature conservation organisations. The large-scale restoration of these systems requires a good knowledge of their natural functioning (Bakker, 1998; Van Wieren and
.0
Bakker, 19981591; WallisDeVries, 19981621), especially since her-
0-U)
bivores do not always favour diversity in every environment (01ff and Ritchie, 1998132]; Ritchie and 01ff, 19991421). We think
that the key processes to be understood in grazed woodlands are plant strategies in coping with herbivory, herbivore selectivity, and tree light requirements.
oo oc
o ocu — U)
Plants cope with herbivory by either avoidance (escape or defence) or tolerance (Grubb, 1992120]; Rosenthal and Kotanen,
.0
1994145]). Some species avoid being grazed by allocating most of their biomass out of reach (high in the air or below ground),
Ct
while others resist herbivory by having spines, thorns, or chemical defences, or by being otherwise unpalatable. Tolerance of grazing is found in species with rapid regrowth, large storage of reserves and/or physiological flexibility after biomass losses (Rosenthal and Kotanen, 1994145]). Such tolerant species are usually much more palatable to herbivores than species with defences. Avoidance and tolerance strategies not only vary between species but also between life cycle stages of the same species. Mechanical and chemical defences often need time to develop or build, which forces resistant species to try to avoid herbivory during early developmental stages.
Associational Resistance to Herbivory A special type of grazing avoidance is found in plant communi-
ties containing both resistant (species with defences) and palatable plant species. Various authors have recognised that individuals of one plant species may, instead of being a competitor, have a net positive effect on another species by reducing the amount of herbivory the other species experiences (Root,
a)
Ct ICt
Unpalatable plant (% of biomass)
b)
°too 0.
a)
Large herbivore
AP
o—
Small herbivore
Oct
Palatable plant (% of biomass) Fig.1 (a) The proportion of a palatable plant consumed by a highly selective, small herbivore (dashed line) and a less selective, large her-
bivore (solid line) as dependent on the proportion of unpalatable plants in the local vegetation patch. The difference between these two lines is shaded and denotes the advantage to the palatable plant due to associational resistance (AR). (b) The proportion of an unpalatable plant consumed by a highly selective, small herbivore (dashed line) and a less selective, large herbivore (solid line) as dependent on the proportion of palatable plant species in a local vegetation patch. The difference between the two lines (shaded area) denotes the disadvantage to the unpalatable plant due to associational palatability (AP).
19731431, 19751441; Atsatt and O'Dowd, 197612]; Burrichter et al., 198Oa111; Huntly, 1991126]; Callaway, 19921121). Such facilita-
Various plant defence strategies may lead to associational re-
tion, or positive interactions (Callaway, 19921121), between species has been termed associational resistance (Huntly, 19911261; WahI and Hay, 1995161]), a defence guild (Atsatt and O'Dowd, 197612]; McNaughton, 1978129]) or a defence association (Quen-
McNaughton (19781291) showed that the plant species Themeda
ga-Kerr and Paul, 1995138]). We adopt the first term here. We
think associational resistance is of key importance in understanding the dynamics of grazed temperate woodlands and will describe this process in more detail.
sistance. For example, a study in the Serengeti grasslands by tnancira lost a smaller proportion of its biomass to buffalo and
wildebeest in plots with higher abundance of less palatable plant species, such as the pungent Cymbopogon excavatus. However, this resistance was not effective against more selective vertebrate herbivores such as zebra and Thompson's gazelle. In a dry Mediterranean oak savanna with high deer herbivory, Callaway (1992112]) found that two Quercus species
could only establish within unpalatable shrubs where they Associational resistance causes palatable plants to be proportionally less grazed by large herbivores when unpalatable spe-
cies reach higher relative abundances (Fig,la). This means that the palatable plant species is less grazed towards lower densities of its own biomass (a positive density dependence in its per capita loss rate). The inverse effect is also found: un-
palatable species may be proportionally more grazed when palatable species reach higher relative abundances (Fig. I b). This means that the unpalatable species is less grazed when its biomass increases (a negative density-dependence in its per capita loss rate). It should be noted that associational resistance only operates when the herbivores lack the ability for small-scale discrimination between palatable and the unpalatable species, or when the grazers are physically hindered by the unpalatable species. Therefore, it is more likely to operate with large grass/bulk feeders (like cattle and horses), than with small species and concentrate feeders (browsers) (Fig.1).
were protected from herbivory.
A well-documented example of associational resistance is found in floodplain woodlands along lowland rivers in western
Europe, where thorny shrubs facilitate the establishment of palatable trees, leading to characteristic vegetation structures in a cyclical turnover (Vera, 19971601). We will use this ecosystem as a case study to elaborate some of the processes and mechanisms involved, and discuss the important community and ecosystem consequences of large herbivores and associational resistance. After this, we will discuss its possible operation in other ecosystems.
Case Study: Temperate Floodplain Woodlands Temperate lowland floodplains are frequently inundated dur-
ing the winter, resulting in a naturally fertile soil, and hence sustain a relatively high primary productivity. Large native
Shifting Mosaics in Grazed Woodlands Driven by the Alternation of Plant Facilitation and Competition
herbivores which occurred in the North Western European lowland before agriculture became widespread include aurochs (Bos primigenius, the extinct ancestor of cattle) and tarpan (Equis przwalski qmelini, wild horse). These grazers are
thought to have preferred the floodplain areas along rivers due to the high quantity and quality of primary production (Vera, 19971601).
In undisturbed floodplain areas, the lowest, most frequently inundated but well-aerated zones contain forest patches of softwood broadleaved forest dominated by Salix ssp. and P0pulus spp., while Alnus glutinosa dominates on the wettest sites with impeded drainage (Harms et al., 1993[2U). These trees produce many small seeds which are dispersed by wind and water and need bare soil to germinate and establish. Local
Plant biol. 1 (1999) 129
tively low densities for at least the past few centuries. These areas have never been ploughed or fertilised (Burrichter et a!., 19801111), and livestock may have gradually replaced the native large herbivores utilising such areas. These areas are now protected and low-stocking grazing is continued as a nature man-
agement practice. The vegetation of these areas consists of mosaics of grasslands, shrub thickets and woodland. We think that herbivores prevent the formation of a closed forest in this system and that they mediate a shifting mosaic of grasslands, shrub thickets and woodland patches. We suggest that these shifting mosaics are driven by the alternation of facilitation
(associational resistance) and, competitive displacement. These hardwood floodplain woodland remnants may be the last fragments of an ecosystem type which was once much more widespread. Such areas thus provide an opportunity to
erosion and sedimentation during winter inundations therefore provide establishment opportunities for Salix and Populus (Van Splunder et al., 19951571). Once established, they are toler-
study natural processes that have now disappeared from most of our landscape.
ant to frequent inundation (Siebel, 19981471) and may reproduce by clonal propagation. The palatable Salix and Populus are rather attractive to large grazers and browsers (like moose, Alces alces), but are also tolerant of herbivory. Individual ramets can recover after having been heavily browsed for many subsequent years. Traditional human use of willows in floodplains involves regular coppicing for wood harvesting.
Alternation of Facilitation and Competition
Alluvial woodland patches on somewhat higher, less frequently inundated soils are dominated by the deciduous hardwood trees Quercus robur and Fraxinus excelsior with some Ulmus minor and Tilia sp. In contrast to the softwood species, Quercus and Fraxinus have large seeds that are mainly dispersed by animals (Eurasian jay IGarrulus glandanus] and woodmouse [Apodemus sylvaticus]) and have poor clonal propagation. Juveniles of these hardwood trees are all palatable to large herbivores and not very grazing tolerant. They need a "window of
opportunity" without severe browsing of about 5—10 years, after which they will have grown enough to be out of reach for large herbivores. This implies that whenever herbivores are present, these trees will not establish in open, grazed grassland or in a closed forest (with little understorey). Associational resistance to herbivory seems to be an important process allowing the regeneration of palatable trees in this community. Various authors have reported that Prunus spinosa and Crataegus monogyna, both thorny shrubs, are able to facilitate the establishment of Quercus and Fraxinus by protecting
We will now outline in more detail how facilitation/competition alternations exactly lead to shifting mosaics in grazed woodlands. Previous studies in hardwood floodplain woodland remnants, such as the Junner Koeland (the Netherlands) and Borkener Paradies (Germany), suggest that vegetation mosaics in these areas are maintained for a long period because each patch goes through a repeated cyclic succession yielding a shifting mosaic of vegetation structural types (Burrichter et al., 19801111; Coops, 19881141; Pott and HUppe, 19931371; Annema,
1997111; Vera, 1997160]). Fig. 2a shows a schematic cross-view of
the spatial mosaic in vegetation structure that is currently found in these areas and a proposed cyclic succession of individual patches that leads to such a shifting mosaic (Fig. 2b). The dynamics of this system will be contrasted with the spatial patterns and transitions in vegetation structure in the absence of large grazers (Figs. 2c,d). We will describe this cyclic succession both in terms of plant functional types and plant species. For this, we propose a broad classification of plant functional types according to growth form, light requirement and palatability to large grazers (Table 1). Species were assigned to a functional group based on our own field observations. We will discuss later whether the same general mechanism with the same functional types, but with different species, also operates in other ecosystems.
et al., 19801111; Sloet van Oldruitenborgh, 19821401; Coops,
The underlying cyclic succession in the presence of large grazers is driven by the alternation of positive (associational re-
19881141; Pott and Huppe, 19931371; Vera, 1997160]). Despite the
sistance) and negative (competitive) interactions between
effectiveness of mature Prunus and Crataegus in protecting palatable trees from grazing, they face problems in establishing themselves, since their thorns are not yet developed during the early stages in their life cycle. Our own field observations indicate that Prunus and Crataegus may occasionally establish from seed within patches of clonal, more grazing resistant herbaceous species which are poorly palatable (Juncus spp.), spiny (Cirsium spp.) or stinging (Urtica spp.).
plant species. Short unattractive species facilitate the establishment of taller unattractive species, which facilitate palatable trees, which in turn outshade the species that facilitated their recruitment, leading to cyclic patch dynamics (Fig. 2b).
them from grazing (Watt, 19191631; Tansley, 19221511; Burrichter
This process of associational resistance leads to interesting vegetation mosaics. This is illustrated by a number of floodplain areas along the rivers Overijsselse Vecht (the Netherlands) and Ems (Germany). These areas are former communal rangelands
that have been saved from the intensification of agricultural practices and remained grazed by cattle and horses at rela-
On soils which are sufficiently productive to sustain large herbivore populations, various direct (biomass removal) and indirect effects (e.g. nutrient recycling) can result in the formation of grass lawns, which are generally uniform in structure (McNaughton, 19841301; Bakker, 1989131). The recruitment of most deciduous trees in such grasslands is generally difficult since the seedlings are generally sensitive to browsing damage and suffer from competition by the grasses (Smit and 01ff, 19981501). Associational palatability (Fig. I b) may contribute to the persistence of grassland stages, where saplings of thorny
130 Plant biol. 1 (1999)
H. 01ff et al.
without large grazers
With large grazers
c) observed spatial mosaic
a) Observed spatial mosaic
I
—f.m
I i.S.—t
**** 44 3 thud TtitE?1 sl 111 1 4
b) Dynamics of individual patches
d) dynamics of individual patches
7-, F
Sr
_.i1Ii IL. HCst /0 D
3ls13
Ttit I
A
.%, t— 1
gg
L+P+ grasses
L+Pforbs
L+Pshrubs --
L+P+
L+P+forbs
A
- -r
L+P+fr
S L-P+ frees
Fig. 2 Observed spatial mosaic (a) as mediated by local cyclic succession of plant functional types (b) in temperate woodlands with free-ranging large grazers, such as cattle and horses. Associational resistance to herbivory is an important mechanism causing this type
of dynamics (see text). Without large grazers, a different spatial mosaic (c) and patch dynamics (d) are observed. See Table 1 for explanation of plant functional types.
shrubs are grazed together with the attractive grasses. How-
here and Malaisse, 19941171). Since uprooting tillers of seed-
ever, when dung is deposited or when the grassland is otherwise locally disturbed and/or enriched, such short grassland can be locally invaded by herbivore-resistant herbaceous species which have spines (thistles), are toxic, or otherwise unpalatable (Silvertown and Smith, 1989148]; Milton et al., 19971311)
lings of thorny shrubs are poorly defended against herbivores (Rackham, 1980[1), they may require unpalatable herbaceous plants for protection during the first years of their establishment. An important feature of grazed mosaics of open grasslands and thorny shrubs is that most unpalatable herbaceous
(Fig.2b, transition A to BI). The grazers may then avoid these
plants (thistles, tall grass) occur at the fringe (transition of
patches. This can provide an opportunity for thorny woody species to invade by establishing from seed (Fig.lb, BI to C). Almost all thorny shrubs in this habitat have berries, so birds are likely to be their main dispersal vector. Such "windows of opportunity" will especially occur when the grazers occur in
shrubs to grasslands, Fig. 2a). This is probably due to mutual protection against grazers that young shrubs and unpalatable herbaceous species provide to each other. This enforces the establishment of new tillers of the shrubs adjacent to existing
such a low density that not every location in the area is grazed each year. In many instances, however, the grazers will convert patches with less attractive herbaceous species back to short grassland before shrubs can establish (Fig. 2b, B1 to A), which makes the grassland stage persistent. So the sequence A to BI to A (Fig.2b) is the rule, A to BI to C is a rare event. Once es-
tablished, the thorny species may expand in area, invading neighbouring grassland patches (Fig. 2b, B2). Especially clonal, uprooting species such as Prunus spinosa and Rubus spp. show this behaviour (Burrichter et al., 19801111; Coops, 1988114]; Du-
thickets, and enforces spatial patterns, once present. Birds foraging on the berries of these shrubs break seed dormancy, and excrete the seeds while foraging, leading to seed deposition under or close to the shrubs. Indeed, steep seed shadows have been observed (Van Groenendael et al., 1982 a]541) and short-range clonal propagation will further enforce this effect. Shrub thickets can thus invade open grassland in two ways: either from seed (A to B1 to C, Fig.2b) or by clonal invasion from neighbouring patches (A to B2 to C, Fig.2b). Establish-
ment of unpalatable shrubs from seed in grassland without existing shrubs may be an important bottleneck to get shrub
Shifting Mosaics in Grazed Woodlands Driven by the Alternation of Plant Facilitation and Competition
Plant biol. 1 (1999) 131
Table 1 Proposed classification of plant functional types according to growth form, light requirement for growth and palatability to large grazers (e.g., cattle, horses). Not all possible types (combinations of traits) are listed, only plant types which play a role in one of grazed woodland mosaics described in the text are given
Palatability to large grazers (P)
Functional type code
Examples of plant species 1
(L)
Graminoid
High
High
L+P+ graminoids
Lolium perenne, Festuco rubro, Deschampsio flexuosci
Tall herbaceous species
High
Low
L+P— herbaceous species
juncus effusus, Cirsium spp., Carduus ssp., Urtico ciloica
Tall herbaceous species
High
High
L+P+ herbaceous species
Dwarf shrubs Shrubs
High
L+P— dwarf shrubs
High
Low Low
Chomaenerion angustifolium. Eupatorium connabinum Ca/Juno vulgoris, Erico tetrauix
Trees
High
High
L+P+ Trees
Trees
Low
High
L—P+ Trees
Growth form
Light requirement
L+P— shrubs
Prunus spinoso, Crotoegus monogyna, Rubus spp. Quercus robur, Froxinus excelsior, Ulmus minor Fagus sylvatica
1 only examples of potential dominants in Western European mixed woodlands are given
thickets established, especially at higher densities of large grazers. The fact that birds mainly transport seeds of thorny
pled, grasses and forbs will be able to establish on the remaining nutrient rich humus layer. Removal of the crown or whole
shrubs between thickets, but much less to the grassland, contributes to this. But once generative establishment has happened (e.g., during herbivore crash) clonal growth and protection from grazing by unpalatable plants at the edges of existing shrub thickets reinforce these patterns of grassland and shrubs and contribute to their persistence.
dead tree, e.g., by river inundation or by humans collecting
Established thorny shrub thickets may provide safe recruitment sites for palatable trees (associational resistance), such
firewood, will also prevent the branch-cage effect. The productive (forest gap) grassland patches will attract grazers, which
prevent establishment of shrubs and trees. During this stage, associational palatability (Fig.1) may delay the spreading of unpalatable species, prolonging the grassland stage. Only after disturbance, and/or when grazers temporarily neglect a patch, unpalatable herbaceous plant species may invade locally, and the cyclical turnover may start again (Vera, 19971601).
as Quercus, Fraxinus, Tilia and Ulmus (C to D, Fig.2b). Recruit-
ment of Quercus just besides young shrub ramets may be facilitated by Eurasian jays (Garrulus glandarius) which use shrub stems at fringes as a landmark when cachirLg acorns between the vegetation (Bossema, 1979110]). Similarly, Johnson (1997127]) found that blue jays (Cyanocitta cristata) cached acorns preferentially in regenerating woodland and edge habitats while usually avoiding grassland habitats. The oak trees quickly grow taller than the shrubs (within 5 to 10 years) and will then start to outshade them (D to E, Fig. 2b). In this phase the trees are sufficiently tall to be no longer damaged by large grazers. Once the protection from the shrubs has disappeared, the trees will be unable to regenerate on that patch (stage F, Fig. 2b). The grazers will prefer the vicinity of the trees, for shelter and scouring, especially when there is little woodland available, resulting in complete seedling and sapling mortality beneath their canopy. Furthermore, the shade from the parent trees may be unfavourable for seedling establishment. This mechanism implies that, once established in shrub thickets, small groups of trees finally remain in open grassland without
Summarising, the spatial association with unpalatable plants
enables palatable trees to establish in ecosystems with large grazers. The trees then outshade the species that earlier facilitated their recruitment, and the resulting lack of recruitment under their own canopy leads to cyclical turnover. Random causes of tree mortality, spatial heterogeneity in soils, clonal growth of shrubs, and establishment of trees at the transitions of shrubs to grassland, probably prevent synchronous succession over large areas, leading to shifting mosaics of vegetation structural types. This leads to a very different spatial pattern in
grazed woodlands (Fig.2a) than in ungrazed woodlands (Fig. 2c). Fig. 2d summarises the cyclical succession of gap phase dynamics without large grazers. In this type of cyclical succession, the mature tree phase (stage A in Fig. 2d) has the longest duration, and lacks a persistent grassland stage. Hence, the prevailing vegetation structure will be a closed forest.
Stage-dependent Shifts in Competition/Facilitation Balance
much undergrowth (Vera, 19971001). The resulting interaction web of large herbivores, palatable Once the trees die of old age, disease or storm (F ito C, Fig. 2b)
grasses, unpalatable herbaceous plants, thorny shrubs and
two different processes are possible. The branches of the fallen
trees is depicted in Fig. 3. The characteristic shifting mosaics arise because plant species have indirect positive interactions in one life cycle stage (through associational resistance), while one of the species is competitively superior in another stage. This holds both for the interaction between thorny shrubs and palatable trees, and for the interaction between thorny shrubs and unpalatable forbs. We suggest that these facilitatio n/corn-
tree may provide protection against large grazers for a few years, and facilitate establishment of palatable trees (G to H to F, Fig. 2b). This protection has been called the "branch-cage
effect" and has been suggested to play a role in temperate deciduous forests with high deer densities (Van de Veen, 1975153]). However, when the wood decomposes or is tram-
132 Plant biol. 1 (1999)
H. 01ff et al.
____________
fl
are then invaded by early successional trees and shrubs (Pious
sylvestris, Betula pendtila, and Rubus spp.) followed by Quercus robur and Sorbus aucuparia. These trees are finally replaced by the taller and more shade-tolerant Fagus sylvatica. This succes-
sion is attended by increasing plant biomass and increasing nutrient availability due to organic matter accumulation in the soil (Berendse, 199O; Van Oene et al., 1998[]).
— — EIIiIilIIiuiiiii
V
• t$_ -
In the presence of large grazers, the vegetation succession in this system does not follow this directional pathway, but consists more of a shifting mosaic of different vegetation states (Fig.4). This seems to be due to the joint operation of associational resistance with nutrient transport by the grazers within these mosaics. Calluria is not only replaced by Deschampsia, but the reverse is also possible, due to the preference of the grazers for the latter, due to local soil impoverishment in heavily grazed grass patches, and because Calluna has a compe-
titive advantage when nutrients are limiting (Berendse, 199418]). Sorbus
Negative direct effect
W Positive direct effect — — — * Negative indirect effect
— — -. Positive indirect effect Fig. 3 Interaction web of plant functional types and large grazers in temperate hardwood floodplain woodlands, with stage-dependent shifts in competition/facilitation balance. Only interactions that are important for the dynamics of the system outlined in Fig. 2 b are given. Indirect interactions operate either through associational resistance (AR) or associational palatability (AP). See Fig. 2 and Table 1 for explanation of plant functional types.
and Quercus, both highly palatable species, may establish in the presence of large grazers due to the protection by unpalatable Pinus and Rubus spp. These species, in turn, seem to establish especially between the less palatable dwarf shrubs and much less in the palatable Deschampsia. Once Quercus has established, it will eventually outshade P1nus, Betula and Rubus. Further succession to Fagus is inhibited because its seedlings in the forest understorey are easily accessible to the grazers. Mortality of mature trees hence leads to the return to grassland patches, which may impoverish to
heath (Fig.4c). It may be clear from this description that grazed heathiand/woodland mosaics on sandy soils have much more structural diversity in the vegetation than their ungrazed counterparts.
Operations in Other Systems The definition of this type of cyclic succession in terms of plant
petition alternations are an important interaction structure
functional types (Table 1, Figs. 2b,3, and 4) allows us to inves-
Weissing, 19941251; Huisman et a!., 19991241). Associational pal-
tigate if it also operates in other ecosystems than the aforementioned floodplain and heathlands. Table 2 summarises the ecosystems for which the literature provides first evidence for its operation. The few studies available show that it may occur on both dry and wet, and infertile and fertile soils. All
atability (Fig.lb) is probably important in maintaining the
ecosystems reported in Table 2 lack fire as an important factor.
that has been little explored yet. It will especially arise if species show a strong asymmetric type of competition, meaning that small initial differences in resource capture rates are mag-
nified towards later developmental stages (Huisman and grassland stage, since it induces an indirect negative effect of grasses on shrubs and trees (Fig. 3). It should be noted that all
important indirect effects operate through the herbivore (Fig. 3), showing its importance for the characteristic dynamics of these kinds of systems.
In fact, when fires occur frequently, the protective effect of thorny and unpalatable species is likely to be reduced in importance, and forest establishment becomes delayed or inhibited by other mechanisms.
It should be noted that the operation of shifting mosaics in Case Study: Temperate Dry Heathiands Shifting mosaics driven by facilitation/competition alterna-
tions (Figs. 2b and 3) not only operate in fertile habitats like floodplains, but also seem to be important in less productive systems. Bokdam (1998191) suggests that this mechanism plays
an important role in heathlands grazed by free-ranging cattle (Fig. 4). He describes this process for heathlands on dry sandy soils, as found in the Netherlands, northwest Germany and Denmark. Disturbances such as sod cutting (an old agricultural practice) or sand drift may initiate succession. In the absence of large grazers, this succession proceeds from lichens and mosses to dwarf shrubs (Calluna vulgaris, Enca tetralix) to grasses (Deschampsia flexuosa). The dwarf shrubs and grasses
grazed ecosystems is yet only supported by observational evidence. Experiments are needed to establish its real importance in the ecosystems listed in Table 2, and to justify the proposed classification of plant functional types.
Important Herbivore and Plant Traits Based
on the arguments outlined in Fig.1, shifting mosaics
mediated by sequential associational resistance are only likely to be found when large, relatively unselective grazers are the main herbivores. The principle of associational resistance does not work with smaller, more selective herbivores simply because they can "pick out" the palatable species from the cooccurring unpalatable ones. In fact, field observations in var-
Shifting Mosaics in Grazed Woodlands Driven by the Alternation of Plant Facilitation and Competition
a) with large grazers, functional groups
heathlands with large grazers (a) and with-
0
syl vest ris
.0
Rubus'p
0.
vuIgans'4 L+P-
Po!vtrichum
mosses, lichens
L-P+
trees
L+P+ k._)
U)
(0
L+P- fl trees
E
0
trees ,
// L+P- shrubs
/
L+P-/
dwarf
shrubs'L+P+
L+Pmosses, lichens
/
out large grazers (b) and transitions between dominant species with large grazers (c) and without large grazers (d). Modified after Bokdam (1998[I). See Table 1 for explanation of plant functional types.
Deschampsia flexuosa
Distumance
b) without large grazers, functional groups
.0 C 0.
plant functional types in dry temperate
Quercus robur Sorbus aucuparia
Pinus
L+P-
E
Fig. 4 Vegetation state transitions between
c) with large grazers, species
L+P+
U) U)
Plant biol. 1 (1999) 133
grasses
Disturbance
nutrient availability
d) without large grazers, species
Fagusy1va
Pinus sylvestris
robur
Quercus Sorbus aucupana
//us5PP.
Cal! una
vulgaris'4.
Pa! ytri chum
Deschampsia floxuosa
CIadon,a Distuance nutrient availability
ious grazed floodplains along the river Overijsselse Vecht (The
Netherlands) show that Quercus robur regeneration was impossible during years with high rabbit densities. The same may apply to years with high vole or mice densities. An exception may occur in years when seed and seedling predators are suddenly saturated by a mast year of the trees. Crawley (1995(15]) showed that rabbits and wood mice destroyed most acorns in years of low seed production, but not in mast years. Furthermore, plant features that repel large herbivores may attract smaller herbivores. Dense, thorny shrub thickets may provide protection for small to intermediate sized vertebrate herbivores (voles, rabbits, deer) against their predators, increasing the rate of seed and seedling predation of palatable trees within these thickets. On the other hand, the positive effect of seed caching by wood mice within shrub thickets may outweigh the negative effect of increased seed predation. Finally, associational resistance is expected to work better against grazers (as cattle and horses) than against browsers (as roe deer). For browsers, the advantages of the good quality of thorny shrubs may outweigh the disadvantages of their mechanical defence. Differences in morphology (smaller bite size and biting with teeth) will further contribute to the use of thorny species by browsers and mixed feeders. We clearly need more experimental data to evaluate the role of different herbivore species in maintaining shifting mosaics in grazed woodlands.
and other factors, and which conditions lead to the highest spatial variation in vegetation structure. Table 3 lists some hypothesised relationships and optimal levels, but more work is needed to test and quantify these predictions along gradients of environmental conditions and herbivore assemblages.
The degree of spatial variation in vegetation structure is expected to be highest at sites with intermediate productivity, with free-ranging large grazers grazing year-round with a sufficiently large area available, not too many small herbivores such as rabbits, with soil and nutrient conditions leading to intermediate productivity and at intermediate disturbance regimes by wind and water (Table 3).On productive but inaccessible (e.g., very wet) sites, succession is expected to go fast, reducing spatial variation. At accessible, productive sites, high herbivore densities will be found, causing a uniform, short vegetation structure. In large-scale natural systems predator control and spatial variation in predation risk may further con-
tribute to spatial vegetation mosaics (Hughes and Ward, 1993(231). Furthermore, very
unproductive (dry, poor) sites will be avoided by the large herbivores, but succession will proceed so slowly that only few successional stages co-occur. At sites
with very frequent and extensive disturbances, only ruderal, short-living plant species will be able to maintain their populations (Grime, 1979119]).
Implications for Nature Conservation
Transition Rates and Relative Abundance of Vegetation States
Both the landscape and the herbivore assemblage of temperate
In a shifting mosaic, the degree of spatial variation in vegetation structure depends on the intensity, extent arid frequency of disturbances (destruction of shrub and woodland patches),
mising the harvest of renewable products. During the last century especially, this has led to a loss of biodiversity from these habitats. We think that the theory reviewed in this paper can be helpful when designing management strategies to cope with these biodiversity losses (see also Van Wieren
the possible vegetation transitions, and the rate of displacement between vegetation states. We are only just beginning to understand how these factors are affected by soil conditions, geomorphology, the nature and density of herbivores
woodlands have been extensively modified by man for maxi-
and Bakker, 1998(591; WallisDe Vries, 1998(62]). When doing
this, we have to identify relevant problems (what's wrong),
of cyclic succession
2
Thin soils overlying chalk bedrock
Horse,
mesotrophic to oligotrophic
Sheep3
Horse, (Tarpan),
(Aurox).
Cattle,
Sheep3
Arenaria serpy!lifolia, Agrostis vinea/is, Festuca ovina
Festuca spp., Ammophila arenaria, Carex arenaria, Colamagrostis epige]os
Carex flacca, Brachypodium pinnatum, Bromus erectus
Deschampsia flexuosa, Agrostis spp., Festuca ovina
herbaceous
Potentilla fruticosa
Cirsium spp., Echium vu/gare, Ononis spinosa, Rubus caesius, Urtica diolca, Anchusa officmnalis
Dipsacus spp., Cirsium spp., Car/ma vulgaris, Carduus spp.
Ononis spinosa,
Calluna vulgaris, Nardus stricta, Genista spp., Juniperus communis
Juncus spp., Deschampsia caespitosa, bynchium campestre, Urtica dioica
Cirsium spp., Carduus spp.,
species
L+P—
See Table 1
for codes Herbivoresgone extinct in a system are denoted between brackets, their domesticated replacements are given in italics Sheep probably do not have a native ancestor iii these systems
Baltic alvar
Scandinavian and
(Aurox), (Tarpan), (Red deer),
Cattle,
Sheep3
Horse, (Tarpan), Red deer,
(Aurox),
Cattle,
calcareous soils,
Dry calcareous soils, mesotrophic to oligotropic
Northwest European chalk grassland
Sheep3
Horse, (Tarpan), Red deer, Roe deer,
(Aurox),
Cattle,
Arrhenaterumelatius
Agrostis spp., Holcus Ianatus,
Horse, (Tarpan), (Red deer)
Festuco rubra,
(Aurox),
L-+-P+ graminoids
Functional type
Cattle,
Large herbivores2
1
spp.
Juniperus communis, Pinus sylvestris, Prunus spinosa
Crataegus monogyna, Hippophae rhamnoides, Rosa spp., Rhamnus catharticus
Rosa
Crataegus monogyna, Rhamnus catharticus,
Rubus spp., young Pinus sylvestris, Ulex europaeus
Prunus spinosa, Crataegus monogyna, Rhamnus catharticus. Rosa spp., Rubus spp.
L+P— shrubs
through facilitation/competition alternation (see text) in different ecosystems
Dry to wet sandy,
Dry (loamy) sand, acid, mesotrophic to oligotrophic
Northwest European fluvioglacial and aeolic upland areas (heathiand/pine woodland mosaics)
Northwest European coastal dunes
Loamy sand, wet, neutral pH, eutrophic
Northwest European lowland floodplains, irregularly inundated
Soil conditions
Possible examples
Ecosystem Type
Table 2
Quercus robur, Sorbus intermedia
Populus alba, Papulus tremula, Quercus robur
Quercus robur, Tilia spp., Carpinus betulus, Corylus avelana
Quercus robur, Quercus petraea, Betuia pendula, Fagus sylvatica, Sorbus aucuparia
Quercus robur, Fraxinus excelsior, Ulmus minor
L+P+ trees
1 9971601
et a!.,
1996141
1992['; Bakker
Zobel and Kant,
Rejmanek and Rosen, 19921401;
van Leewen, 1973[ss]; Van Groenendael et al., 19821541
Malaisse, 19941171; Coops, 1988114]
Duliere and
Bokdam, 1998191, ID: 3391
Vera,
Oldruitenborgh, 19821491 Pott and HOppe, 1993l3];
19801111; Sloet van
Burrichter et al.,
Reference
(0
0
0 0
P
Shifting Mosaics in Grazed Woodlands Driven by the Alternation of Plant Facilitation and Competition
Plant biol. 1 (1999) 135
Table 3 Proposed determinants of spatial variation in grazed shifting mosaics, important influences on these determinants, and conditions leading to the highest levels of spatial variation
Determinant of spatial variation in vegetation structure
Affected by:
Highest variation in vegetation structure expected at:
Disturbance frequency
Herbivore species and abundance
Intermediate abundances of large grazers Intermediate disturbance frequency Soil and geomorphological conditions intermediately sensitive to disturbances
Flooding and wind regime Geomorphology, soil characteristics
Extent of disturbances
Herbivore species and abundance
Flooding and wind regime Geomorphology, soil characteristics
Rate of successional replacement
Intermediate abundances of large grazers Intermediate intensity of disturbances Soil and topography intermediately sensitive to disturbances
Primary productivity (nutrient inputs, rainfall and soil characteristics)
Intermediate primary productivity
Intensity of herbivory
Intermediate intensity of herbivory
Associational resistance
Herbivore species and abundance
Intermediate abundances of large grazers, low abundances of browsers
Number of successional stages
Number of functional types in local species pool1
Large number of plant functional types
Number of possible successional pathways
Number of functional types in local species pool
Large number of plant functional types
1 Dependent on spatial variation in site conditions and biogeographical history of the area
balance management options (what do we want) and management forcing variables (how can we get there) (Table 4). Not only is loss of biodiversity a problem, we also face the loss of ecosystem functions and services, and are quickly losing at-
tractive landscapes for recreation. Meanwhile we face high management costs when trying to counteract such losses. We think that the theory outlined in this paper may provide helpful insights in nature management decisions. It may be used for predicting which and how many vegetation states will be found in an area. However, we would like to stress that it still remains an open question whether the current strategy of releasing free-ranging large grazers in former agricultural areas will really counteract the ongoing loss of biological diversity (van Wieren, 19891581; Bakker, 199815]; WallisDe Vries, 19981621). Current restoration projects have started too recently
to draw this conclusion or have been poorly evaluated. Some issues concerning the management of these areas are therefore hotly debated, especially in the Netherlands (Table 4).This involves questions such as: i) which and how many descendants of extinct large grazers should be introduced? ii) what is the optimal size and spatial configuration of grazing areas? iii) what degree of self-regulation is desirable and possible? Large grazers such as aurochs and tarpan have been driven to extinction, so the ecological role they once fulfilled in natural ecosystems has also been lost. Given that these species went extinct centuries ago, we do not know exactly what this role was, in which habitats they occurred and at which densities, or how important they were in the preservation of the biodi-
versity of other animal and plant species (their ecosystem
functions). We can only look for ecological analogies in func-
tioning of their descendants, as cattle and horses (Vera,
Table 4 Nature conservation problems, management options and management forcing variables with regard to free-ranging large grazers in natural areas (see: van Wieren and Bakker, 1998]]; Piek, 1998135])
Problems Loss of biodiversity Loss of ecosystem functions and services Loss of landscape attractivity High management costs
Management goals/options — Which degree of self-regulation? — How much area of natural habitats? — What landscape spatial structure? — How much biodiversity (how many and which communities and species)?
Management forcing variables — Which herbivores to be introduced? — Which average stocking rate? — Temporal removal of large herbivores (to mimic herbivore crashes?)
— Apply local and temporal exclusion of herbivores through fencing? — Seasonal or year-round grazing? — Should naturally occurring herbivores (rabbits, hares, deer) be controlled in their densities? — External food and water supply to the herbivores, yes or no? — Where to supply food and water? — What is the optimal size and spatial arrangement of new (restored) habitats? — How many, which and what area of landscape units (communities) should be included in a grazing area? — What forest management (tree logging, removal of fallen trees or not, planting trees or not)?
H. 01ff et al.
136 Plant biol. 1 (1999) 1997[601), and
Bakker,J. P. (1998) The impact of grazing on plant communities. In Grazing and conservation management (Wallisde Vries, M. F., Bakker, J. P., and van Wieren, S. E., eds.), Dordrecht: Kluwer Academic Publishers, pp.137 —184. Bazzaz, F. A. (1979) The physiological plant ecology of plant succession. Annual Review of Ecology and Systematics 10,351—371.
study their functioning under free-ranging con-
ditions. The theory outlined in this paper may provide some first (qualitative) insights into optimal management strategies aimed at preservation of biodiversity. Given the current level of knowledge and the space available here, we can only be brief at this
stage. For this, we will link the management variables listed in Table 4 to our conclusions on determinants of vegetation structure from Table 3. To maximise the degree of variation in vegetation structure, which seems beneficial for animal diversity, it seems wise to (re-)introduce grazers (cattle, horses) and not only browsers. The grazers should be introduced at moderate densities, matched with the primary productivity (rate of succession) of the area. Year-round grazing should be preferred over summer grazing. External food should not be provided, since this maintains the herbivore densities at unnaturally high levels, hindering the regeneration of woody species. When external food is not supplied, extreme climatic years may lead to population crashes, allowing windows of opportunity for woody species to establish. In areas with just summer grazing and managed densities, such crashes may be simulated by incidental removal of the animals for a few years. Unpalatable species (e.g., Pinus in heathlands, orJuniperus in Alvar or chalk grassland) and dead trees should not be removed, since their removal inhibits the recruitment opportunities for palatable trees, and hence may even contribute to their local expansion (their successional displacement is prevented). A newly grazed area should contain a sufficiently high ratio of shrubs and woodland to grassland, since otherwise the
animals will destroy the woody species and hence the seed sources. If this is not possible, temporal variation in herbivore density may be applied. Temporal removal of large herbivores is only useful when small herbivores (rabbits, voles) are not at
a population peak. Planting of palatable trees is unwanted, since fencing would have to be used to protect them from grazers. It is better to allow the natural fences (the unpalatable forbs and shrubs acting as barb wire [van Leeuwen, 1973 a[55l]) to establish. Grazing areas should be sufficiently large so that
spatial variation in grazing intensity occurs, allowing local recruitment of unpalatable (protective) species.
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H. 01ff Nature Conservation and Plant Ecology Group Wageningen Agricultural University Bornsesteeg 69 6708 PD Wageningen The Netherlands E-mail:
[email protected] Section Editor: R. Aerts
