Download Plant succession: theory and applications

Plant succession:
theory and applications
by C.W.D. Gibson and V.K. Brown
’The most stable association (of plants) is never in complete equilibrium, nor is it
free from disturbed areas in which secondary succession is evident’ (Clements,
1916). In modern times, these ’most stable associations’ are the exception rather
than the rule, and are only found in the remoter parts of the world where undisturbed communities still exist. A natural state of change (such as after management
is abandoned by humans) is more usual. Indeed much of our farming, forestry,
land reclamation schemes and even nature conservation relies on preventing or in
some way directing this natural process of change. A good understanding of the
pinciples driving this natural succession, and their efficient application, is thus vital
to anyone involved in land management. A striking example, which is developed
later in this review, is provided by the reclamation of industrial waste tips; initial
safe construction or reconstruction is the province of engineers, physicists, hydrologists and soil chemists, whereas long-term stability and successful later use of the
land for agriculture and amenity, can only be achieved by applied ecologists using
the basic principles of plant succession (Bradshaw and Chadwick, 1980). Most
applications to date have been on land, so we have restricted this review to a
discussion of terrestrial successions, with apologies to those interested in the
application of succession theory to aquatic environments.
The term ’ecological succession’ is usually applied only to directional change
over a period of years; short-term cyclic seasonal changes and long-term climatic
changes are regarded as being imposed upon an underlying successional pattern.
Early observations of succession (e.g. Cowles, 1901; collation by Golley, 1977)
showed that change often proceeded through a series (sere) of recognizable plant
associations (seral stages) towards a state where little further change occurred
(climax) without outside disturbance. Such disturbance usually gives rise to a
repetition of some or all seral stages. Increasing numbers of observations and
theories about how succession works led to a vast number of technical terms (for a
review see Golley, 1977): those in common current use are defined in Table 1. The
time scale of a sere can vary considerably; in some cases an ecologist can hope to
see the whole process during a lifetime (e.g. Oosting, 1942), in others (e.g. Olson,
1958 on the sand dune vegetation of Lake Michigan - 1000 yr) there is the
potential for considerable genetic change among the smaller organisms in the
Downloaded from ppg.sagepub.com at PENNSYLVANIA STATE UNIV on September 20, 2016
474
Table 1
Some terms commonly used in the description of succession
community, and certainly for climatic change, before the ecological process has run
its course. By contrast, changes significant for management by humans can take
place very fast indeed (e.g. Jones, 1933 found that the species composition of
pasture leys could be changed drastically over a period of months).
Succession at the community scale is based on the interactions between individual plant species, animal species and their environment. We therefore start this
review by enumerating those types of interaction which have been shown to be
important in directing succession. There follows an explanation of some current
theories and models which attempt a general understanding of the process. The last
section is dominated by a series of examples to show the range of ways in which
succession theory has been applied to land management, and an indication of the
ways in which we believe such applications could usefully be extended in the
future.
I
Interactions
We have divided interactions important in succession into those to do with the
physical environment, those between different plant species and those involving
animals as well as plants. A further important distinction concerns the scale on
which succession is affected. This includes temporal scales (e.g. whether the whole
course of a succession is affected or only one part), spatial scales (e.g. regional
Downloaded from ppg.sagepub.com at PENNSYLVANIA STATE UNIV on September 20, 2016
475
climate vs microclimate under a bush or in the open), and effect scales (is an interaction strong enough to remove a species from consideration or so weak that it only
affects the growth rate of a few individuals?). We have attempted to show the
relative importance of different types of interaction in this section, in preparation
for the development of general models of succession.
1
Environmental influences
Regional climate
was
noted
as
being of such importance by Clements (1916) that
it formed the basis of his ’climatic climax’
as the most fundamental concept in
succession. However, applied ecologists will usually need to concentrate more on
the modifiers acting within this, i.e. factors resulting in further restrictions on the
species list allowed by regional climate.
These smaller scale variations can be very important. Although climatic change
on a regional scale is usually too slow to be within the scope of this review, local
variations in climate may appear to change the adaptive range of a species. For
instance, Pigott (1968) found that the calcicolous thistle Cirsium acaulon is restricted to south-southwest facing slopes in Yorkshire, the northern limit of its
European range, whilst in southern Britain it is found at all aspects. At its southern
limit in central Spain, it is again highly localized. This species needs regular temperatures of 20°-25°C to mature seeds and, whilst it is fairly drought-tolerant because
of its deep root system, it is no xerophyte and cannot tolerate very hot dry soils.
This effect is a product of the microclimate on the scale of the plant (within
the limits ultimately set by regional climate). The interaction between microclimate, climate and the plants themselves is well shown by the ecology of a
number of species in southern Britain. In East Anglia, plants such as the bluebell
Endymion non-scriptus and the primrose Primula vulgaris are restricted to woodland sites which are at least several centuries old, and disperse from these only very
slowly, under a relatively ’continental’ climate. In the ’Atlantic’ climate of western
Britain, the same species are quick colonizers of secondary woodlands and even of
pasture edge and hedgerow (Rackham, 1980). Thus the overall distribution and
the apparent position in succession (fast-dispersing early colonizers vs slowdispersing late colonizers) may be set by an interaction between regional climate,
microclimate modified by other species (e.g. shade) and the particular exaptations
(sensu Gould and Vrba, 1982) of the plant itself (a need for relatively high humidity
which is a characteristic of an individual rather than strictly an adaptation to its
local environment).
The incidence of fire as an ecological influence is dependent on regional climate
but at present fires are usually anthropogenic. The effects of fires, and the course
of postfire succession, depend considerably on the available plant species. In some
regions of the world, notably southwest Australia, many of the plant species
present are well adapted to fire, but in other places where fires have only been
regular for a relatively short time, such as in parts of the southwest USA, there are
fewer species which are specifically fire-adapted. In the Australian flora these
Downloaded from ppg.sagepub.com at PENNSYLVANIA STATE UNIV on September 20, 2016
476
specific adaptations include thick corky bark, the ability to form epicormic shoots,
regeneration from underground storage organs, and fruits which release their seeds
after being burnt on the outside (e.g. Carlquist, 1974, especially for Proteaceae).
Banksia
(Proteaceae)
seeds will also tolerate very
high temperatures (Siddiqui
et
al., 1976). As a result, most of the species which could occur in the plant community have propagules already present immediately after a fire: the subsequent
course and end-product of succession depends on the species present before burning and these species’ times of recovery (Purdie and Slatyer, 1976) and other lifetraits such as longevity. In some chapparal stands in southwest USA the
story is similar (Biswell, 1974) but other, forest, vegetation types such as ponderosa pine forests contain fewer fire-tolerant species and here the intensity and
frequency of burning and the ability of different species to recolonize a burnt
area have more critical significance (Weaver, 1974).
The variety of dispersal mechanisms among plants means that any discussion
history
of colonizing abilities is inextricably linked with interactions between plant species
and with plant-animal pollination and seed dispersal mechanisms, outside the scope
of this general review (but see Faegri and van der Pijl, 1966). However, purely
physical barriers can be extremely important in determining the importance of
colonization to the community scale. On oceanic islands, dispersal of some types
can take so long that evolution has produced plants of similar ecology from earlier
colonists (Carlquist, 1974). In more familiar regions, the problem is best illustrated
by a contrast between the much-studied ’old-field’ successions (abandonment after
agriculture) in temperate regions and studies in undisturbed forests. In most cases
where succession has been studied in a relatively small patch left undisturbed in
the midst of agricultural land, the successional process is manifested as a replacement series in which colonization is very important, especially in the later stages, in
combination with biotic modification of the soil (for a review see Golley, 1977).
At the other extreme, Piroznikow (1983), working in the largest area of virgin forest
left in Europe (Bialowieza), found that even the soil seed bank was restricted and
contained only forest species; after a small disturbance these late successional
species, and only these, would be available for recolonization. In a range of habitats
not including virgin forest, Thompson and Grime (1979) found results intermediate
between these extremes. Clearly, material for germination in any particular place
comes from immigrants (colonization), the immediately preceding seed rain and the
seed bank as determined by seed longevity and past factors (individual species range
from a requirement for immediate germination to an ability to survive many
decades (Gross and Werner, 1978)). Interactions between these factors determine
what happens in a given habitat (Thompson and Grime, 1979).
Edaphic factors (connected with soil environment) put further constraints on
the potential species list in a given habitat. pH, soil structure, water levels, temperature, and the concentrations of key nutrients all provide limits to which plant
adaptations vary in degree and in the part of the spectrum over which they can
survive. However, plant’s resource spectra are usually labile, being influenced by
other biotic factors, e.g. by other plants which modify the soil environment,
Downloaded from ppg.sagepub.com at PENNSYLVANIA STATE UNIV on September 20, 2016
477
resources, or by animal-induced stresses, and
cussed below in the context of these biotic interactions.
by direct competition for
2
are
dis-
Interactions between plant species
Competition between plant populations is well attested (Jackson, 1981) although
its precise importance in relation to other factors is understood in only a few
communities. Most pertinent to the present review are those studies which show
competition giving rise to the replacement of plant species by others, rather than
demonstrating stable coexistence. In some cases, ’early successional’ species need
open soil patches (e.g. Aphanes arvensis - Grubb, 1976) or even light reaching the
seeds (e.g. Verbascum thapsus - Gardner, 1921; Gross and Werner, 1978) for
germination. Annuals and biennials such as these are usually denied such microsites for seed germination by the closed litter cover established by perennial grasses
after a few years of old-field succession, but they may persist in local conditions
of shallow soil or when seeds are exposed by the scrapes of burrowing animals
(Grubb, 1976). Later on in succession, although germination may take place,
seedling establishment, reproduction and/or dispersal may be affected by direct
shading. Such factors contribute to the depleted seed bank found in old European
forests. Piroznikow (1983) noted that the surviving forest floor species were those
capable of persisting by vegetative reproduction under deep shade and that some
of these were not represented in the seed bank. In Britain, although Primula vulgaris
can survive in deep shade, it cannot set seed, and new seeding depends on disturbances to the forest canopy such as coppicing or natural tree fall (Rackham,
1980).
Soil characters can also modify the outcome of competition between plants.
Nutrients and water are both obtained from the soil, and it is virtually a tautology
to say that competition, where important at all, is for the limiting soil factor(s).
The position is not always so simple. Many plants only tolerate restricted pH
ranges: among these, ’calcicoles’ are confined to chalk or limestone soils, and
’calcifuges’ to more acid sites. Despite these field restrictions, many species tolerate
a much wider range when grown in culture (Rorison, 1969). Plants are often
restricted to acid soil by the interference of Ca++ ions with the plant’s ability to
take up Mn, Fe, P and other essential nutrients. Conversely, acid soils can hold
large quantities of A1+++ and Fe+++ ions in solution, which are both directly toxic
(Al +++) and tend to precipitate H2po4, preventing uptake by the plant. In acid
waterlogged soils, lack of oxygen near the roots must also be overcome, e.g. by
enhanced transport from the aerial parts (Fitter and Hay, 1981).
Differences between field and laboratory conditions can often be explained
by the modifying effects of competition from species better at one extreme or the
other (Tansley, 1917; Rorison, 1969). Such interactions between soil conditions,
plant competitors and the effects of plant on the soil can give rise to succession
by nucleation (Austin and Belbin, 1981; Game et al., 1982) where initial patches
Downloaded from ppg.sagepub.com at PENNSYLVANIA STATE UNIV on September 20, 2016
478
start systems of concentric
rings of vegetation types which eventually coalesce: in
circumstances these patches can cyclically replace each other in time and
space (Godwin and Conway, 1939; Watt, 1947).
A special case of competition is when plants produce substances which are toxic
to other plants (allelopathy). Many species produce such substances (classic examples come from American chaparral e.g. Biswell, 1974; Harborne, 1977) but
there has been argument over the function of these allelopathic chemicals - are
they substances produced by one plant to poison another, or are they merely waste
metabolites which are unavoidably produced and happen to have this effect (e.g.
Harper, 1977)? In one sense this is immaterial; such chemicals are produced, they
do have inhibiting effects on most plants, often including the individual which
produced them, and they are destroyed by fire, releasing successional stages more
diverse and productive and with a higher biomass than this ’allelopathic climax’
particular
(Biswell, 1974).
.
In direct contrast are cases in which one plant alters the environment to the
benefit of another species. Nitrogen fixing by bacteria in root nodules (e.g. Hansen
and Dawson, 1982) can not only accelerate succession, but also produce plant
species which would be unlikely in other circumstances (see ’Applications’ below).
Hodgkin (1984) found a simpler, but less intuitive, mechanism operating during
scrub establishment on Welsh sand dunes. Hawthorn (Crataegus monogyna) bushes
establishing in phosphorus-poor dune grassland have deep roots which access phosphate sources unavailable to the usual grassland plants. Seasonal leaf fall gradually
enriches the topsoil and subsequently other plants demanding high phosphate levels
can establish at the expense of the original flora, even if the scrub is removed.
However, the initial scrub establishment often depends on interactions with grazing
animals, and an explanation needs an understanding of the next level of interactions.
3
Animal-plant interactions
.
profound and varied effects of grazing on vegetation dynamics are well known
(e.g. Harper, 1977), and the current characteristics of some plant communities may
reflect their history of grazing pressures (Duffey et al., 1974). However, the impact
of herbivory on the establishment and development of natural vegetation is seldom
documented. Traditionally, many botanists have believed that small herbivores (e.g.
insects) have little impact on succession, and that large animals are best regarded
The
interrupting the process rather than radically changing its dynamics. Animal
pollination and seed dispersal have been accepted as important in special cases
(e.g. Godwin, 1936).
It is becoming apparent that even small herbivores may change the course and/
or dynamics of succession, while large grazers may set plant communities on a wide
variety of paths, dependent on the timing and intensity of succession and the
particular herbivore species. In a classic early study Jones (1933) was able experimentally to direct sown agricultural leys towards grass swards, clover swards or high
diversity (’weedy’) mixtures by varying the intensity, and more especially the
as
Downloaded from ppg.sagepub.com at PENNSYLVANIA STATE UNIV on September 20, 2016
479
timing, of sheep grazing. Major changes took months rather than years. Sheep can
also set the form and persistence of micro-patterns within the sward (Bakker et
al., 1983). The pattern of change in upland vegetation on acid soil in Britain is also
influenced by the intensity of sheep grazing (Miles, 1978). Under low grazing
pressures succession to woodland takes place via grassland (often with bracken) or
heath phases. When grazing pressures are increased the regeneration of shrubs and
tree saplings is prevented either by grazing impeding competition with herbaceous
species or by mechanical damage. The secondary effects of vertebrate grazing can
be considerable (e.g. Spedding, 1971). The influence of grazing on the plant succession of rangeiands is reviewed by Ellison (1960) and the dangers of overgrazing in
arid lands cited as an example of interruption/disturbance of the normal successional pattern. In woodlands there is less evidence for the effect of browsers, except as
negative influences which prevent regeneration in most years (Adams, 1975), but
the potential for browsers in determining forest species composition is suggested
by the known feeding preferences of these animals among tree saplings (Peterken,
1981; Rackham, 1980).
While the effects of vertebrates on plant succession may be assessed by either
intuitive observation or enclosure/exclosure experiments, the effects of insect
grazers can be studied by experimental application of insecticides (to which grasslands and early successional associations are more amenable than forest) and by
examining the effects of natural outbreaks of forest defoliators (usually the only
course with forest insects). Among the few grassland studies, both McBrien
al. (1983) and research by Brown and coworkers (reviewed in Brown, 1984)
demonstrated strong effects. In the latter work, the exclusion of insects by the
regular use of non-persistent insecticides permitted direct comparison between
insect-grazed and insect-free plots. (Grazing by other herbivores was prevented.)
In the absence of insect herbivory, plant species accumulated more rapidly, the
vegetation cover was greater, grasses invaded (and replaced herbs) earlier and the
structural complexity of the vegetation was higher. Recent single plant species
studies in natural early successional grassland (e.g. Brown, 1985) have indicated
a significant reduction in number of individual plants, a decrease in growth rate
and a lowering of reproductive potential when exposed to ’natural’ populations of
insect herbivores. The reduction in number of plants was mainly due to seedling
mortality. Whelan and Main (1979) have indicated that insect attack on seeds
and seedlings (the most vulnerable stage in the life history of a plant (see Harper,
1977)) may influence plant succession as can rodents in a similar system (Bond,
1984). Bews (1920) suggested that seed predation by insects in the coastal forest
of Natal might alter the course of succession by the release of previously suppressed tree species. The experimental manipualtions by McBrien et al. showed that
the domination of old-field successions by Solidago spp (goldenrods) could be
broken by herbivorous beetle outbreaks, thus accelerating succession towards
forest conditions. This effect was experimentally reversed by killing beetles on
insecticide plots.
Among forest successions, Bess et al. (1947) showed that gipsy moth outbreaks
possible
et
Downloaded from ppg.sagepub.com at PENNSYLVANIA STATE UNIV on September 20, 2016
480
could either accelerate or decelerate succession depending on outbreak intensity.
At moderate intensities, late-successional tree species, which happen to be less
palatable to the moth, gained an advantage due to defoliation of overshading
earlier successional species. At very high intensities, all tree species were defoliated,
allowing the light-demanding but fast-growing successional saplings to reestablish
a new succession. The purist might argue that this represents the behaviour of
an introduced pest, not a natural succession. Among native insects in native forests,
tree death caused by mountain pine beetle (Dendroctenus ponderosae) in the
western USA had different effects according to interactions with fire and the
natural climax forest of particular regions (Amman, 1977). In natural stands of
mixed lodgepole pine, subalpine fir and Douglas fir, frequent fires hold the forest
at a lodgepole pine stage. Less frequent fires allow outbreaks of the beetle in
mature lodgepole pines, permitting the shade-tolerant juveniles of the other tree
species to take over. In some regions which differ in both soil and climate, the
pattern is again changed, and pure lodgepole stands persist in whatever circumstances, but with their age class distributions set by fire and beetles. In Europe,
succession of alpine larch forests towards a larch/cembran pine mix is delayed
or accelerated by larch budmoth (Zeiraphera diniana) in a similar manner to the
gipsy moth system described above (Baltensweiler, 1975; Baltensweiler et al.,
1977).
Although
have concentrated on the effects of grazing animals on plant
succession, it must be stressed that plants have an important bearing on the nature,
diversity and abundance of the animal species present at any particular stage in
succession. Among the possible mechanisms for these plant-animal effects, plant
architectural changes during succession have at least as much influence on the
associated succession of animal species as do changes in plant species composition
we
(e.g. Southwood et al., 1979).
II
Modelling successsion
From the above it is clear that no single model could explain or predict all plant
successions. Despite this, there are several ways in which general models can help
the ecologist. Conceptual models can be used to identify sets of general patterns
likely to be found under particular, predictable, circumstances. Detailed models
(often referred to as ’component models’ - see Southwood, 1978) can predict
the outcome of a particular treatment in a particular place. Much simpler models,
nevertheless containing the most important features of a system, can be used in a
strategic manner to explore the possible range of consequences of a particular
feature of a system or treatment of it. In practice, component models are usually
too expensive (because of the complexity of data gathering and analysis) for most
applied uses of plant succession, and only conceptual models and simple mathematical frameworks are discussed below.
Downloaded from ppg.sagepub.com at PENNSYLVANIA STATE UNIV on September 20, 2016
481
1
Conceptual models
For many years the field of plant succession was a battleground between the
proponents of different single models which purported to explain the whole field.
The current view is that there are several broad types of succession which dominate
under recognizable circumstances. The development of these ideas was due to many
people (see Golley, 1977) but most current ideas are encompassed by the works of
Drury and Nisbet (1973), Egler (1954), Horn (1974) and Connell and Slatyer
(1977) (Table 2). In all these models the presence of a wide range of life history
strategies is acknowledged (see e.g. Grime, 1979; Horn, 1978; Southwood, 1978;
Stearns, 1977; 1983 for a variety of views on their generation). Among these, very
early successional species have a short life span, high seed production and are good
dispersers, whilst very late successional species tend to have the converse traits.
The most extreme general succession model in one direction (Table 2, column 1)
is one in which most of the species are present from the start and the course of
succession depends solely on their relative growth rates, generation times, persistence and other life history traits. The ’initial floristic composition’ model is most
likely to apply under secondary succession initiated by small disturbances in a large
area of climax vegetation (e.g. Piroznikow, 1983 - although here early successionals may be absent altogether), or under larger-scale disturbances where most species
are well adapted to the disturbance and can persist as seeds or other propagules
(e.g. Purdie and Slatyer, 1976).
Connell and Slatyer (1977) envisaged three other types of successional sequence
in all of which ’early successional’ species are important. In a ’facilitation’ succession (Table 2, column 2), equivalent to Clements’s (1916) ’relay floristics’,
the early stages are dominated by species which change soil conditions, by soil
formation or debris trapping, by changing drainage properties and/or by nutrient
enrichment (Crocker and Major, 1955; Lawrence et al., 1967). Such changes inevitably make the site less suitable for the pioneer plant, but happen to make it more
suitable for other plant species - these are the later successionals. Such succession
proceeds until and if the final colonists change the soil conditions little and/or
make the substrate suitable for themselves alone. These processes are likely to be
especially important in primary successions where soil formation takes place, and
in some cases may generate cyclic changes when no species can stabilize the system
(e.g. Godwin and Conway, 1939).
Connell and Slatyer’s second model (‘tolerance’ - Table 2, column 3) is one in
which early successionals are merely the first colonists and subsequent behaviour is
directed solely by competitive behaviour under the same soil conditions. These
authors stated that ’there is little evidence’ for this model; in many ways it is the
most parsimonious of the four and could be resorted to in cases where nothing
special appears to be happening! It would seem to be thoroughly inappropriate for
primary successions, but might be found where only a small disturbance has taken
place but nevertheless not all the actors in succession are present from the start, or
encompass a wide range of life histories even when present from the start (Pickett,
1982.
Downloaded from ppg.sagepub.com at PENNSYLVANIA STATE UNIV on September 20, 2016
rr-
I
*.
.v
U)
1
’o
c
Cd
C6
u
za
_fG
7i
0
CD
U
1
E
a)
r
Q)
0
U
C
f0
T3
-2
I
u
,I:$
tl
1J
c~
0.
x
f0
’C~
E8%
x
0
.2
’Gl
Q)
......
C)
u
u
1J
C
co
all
i5
w
’
0
4
C
:J
~#
en
u
o
0
Q)
E
a.
~3
f
z
x
m
LZ.
u
U
E
c
i5
0
Q)
U
’5
en
N
r4
t0
U
.2
.0CO
t0
C
H
Downloaded from ppg.sagepub.com at PENNSYLVANIA STATE UNIV on September 20, 2016
483
The final model (Table 2, column 4) is an ’inhibition’ process, where even
the first colonists are good competitors and will not be replaced until they die
of other causes. They are only replaced at all by virtue of their relatively short
natural lifespans. Subsequent establishing species are even more intransigent and
the community is eventually dominated by those species which combine a long
lifespan with an ability to replace themselves in conditions of harsh intra and
interspecific competition. The best examples come from the chaparral systems
discussed earlier, in which the ’moribund’ climax vegetation is usually broken
periodically by fires; otherwise productivity and regeneration of even the climax
vegetation continue to decline (Biswell, 1974). It is difficult to imagine primary
successions working like this, and secondary successions resembling the model
could best be looked for under conditions of naturally low productivity and
nutrient/water stress. Grime (1979) noted the same phenomenon and thought it
worthwhile to erect a special category of life history strategy (’stress tolerator’)
to describe species similar to Connell and Slatyer’s (1977) climax species for
inhibition successions.
2
Simple mathematical frameworks
It can be argued that a good mathematical model is one which is simple to use and
which is wrong in helpful ways i.e. the manner in which it breaks down helps us to
form new theories about what is really going on. Mathematical models which are
right are usually too complex to use cheaply and apply only in restricted circumstances.
Starting with the interactions between plant species, there are several appropriate
starting formats for modelling plant succession. Shugart et al. (1973) examined
succession as a series of linear differential equations describing the component
interactions between plant species. They were restricted to a linear framework by
the rapidly-increasing complexity of including non-linear effects. Although this
line of modelling has proved extremely powerful for exploring the more general
field of community stability (for a review see Pimm, 1982), there has been little
subsequent use in the field of plant succession. A major problem is that it is difficult to collapse the interactions between collections of associated plant species
into single linear differential equations, and without this simplification a vast
number of separate equations are usually involved and the interaction between
each species pair must be determined - a task of impossible complexity.
Difference equations, although a useful tool in building theories about population dynamics (May, 1981), have not been used in succession modelling. As
well as the problem mentioned above, there is a difficulty in matching the time
frames of each plant species which would restrict their use.
Succession can, however, be regarded as a process by which each plant species,
or closely associated set of species, has a particular chance of replacing an individual
belonging to any other particular species (or species group). Thus matrix models in
which the base matrix is a table of probabilities of replacement of each plant
Downloaded from ppg.sagepub.com at PENNSYLVANIA STATE UNIV on September 20, 2016
484
are an intuitively attractive way of representing plant
an
added
There
is
succession.
advantage in that the time frame is flexible: the time
of
the
matrix
can
be
step
adjusted to e.g. the shortest generation time of any plant
of
or
species set species.
If replacement probabilities are fixed, depending only on the species involved,
the model forms a Markov chain, whose mathematical properties are well understood (Bailey, 1964). Horn (1976) pointed out that these models could mimic
many of the features found in real successions (Table 1), depending on the values
given to different replacement probabilities (Figure 1). Disturbances from other
sources such as fire, grazing, tree falls or agriculture could be regarded as changing
either species composition, followed by the same replacement probabilities, or
changing the probabilities themselves (Figure 1(5)).
Unfortunately, if these transition probabilities change, the model becomes an
order more complex and the conveniences of matrix algebra are lost. Usher (1979;
1981) and Austin and Belbin (1981) found that, in all successions where suitable
data had been gathered, individual transition probabilities changed with time (the
process is non-stationary) and/or with past cover states (the process is higher than
first order). These authors concluded that not only did Markovian models give an
inadequate description of succession, but the necessary data gathering for their
more complex structure was too cumbersome to be useful when the biology of the
individual plant species was known or could be assessed.
Under some circumstances these models can be of practical use. On the one
hand, the original demonstration by Horn (1976) that many of the classic patterns
in succession could be explained by very simple processes stimulated ecologists to
examine the real processes involved in a new light (e.g. Austin and Belbin, 1981;
Game et al., 1982; van Hulst, 1979). On the other hand, one is often faced with a
situation where little is known about the component plant species or their interactions, and the way in which a first-order, stationary, model breaks down can
give useful insights into the possible processes involved. Gibson et al. (1983) studied
succession after release from giant tortoise grazing on Aldabra atoll. The succession
was both non-stationary and high-order, but the manner in which the simple
models broke down, and the possible range of consequences of this, showed that
succession accelerated with time, due to both colonization and facilitation effects,
that individual species groups could both facilitate and inhibit others, depending
on the receiver species, and that previous fears that giant tortoises overgrazing
would devastate the island’s vegetation (Hnatiuk et al., 1976; Merton et al., 1976)
were probably unjustified as the vegetation types thought vulnerable were part
of a completely different successional series to those suffering high grazing
pressure.
Thus although there is, and probably will be, no simple general model which
explains all plant succession, there are a number of tools available to the applied
ecologist which can help identify the processes most important to the problem and
goals in hand.
species by each plant species,
Downloaded from ppg.sagepub.com at PENNSYLVANIA STATE UNIV on September 20, 2016
Figure 1 A variety of transition matrices which mimic a variety of successions
(all contain four possible states). 1 ) A slow but constant rate set of transitions from
early to late - a possible format for a tolerance model. 2) Here we have mixed
fast early stages with a very slow late one - there could be facilitation by A and B
followed by inhibition by C. 3) This is a polyclimax version - climax states C and
D are equally stable and equally likely to be entered from B. 4) Cyclic change - in
practice the oscillations will eventually damp down to an even mixture of all four
states. 5) One way of modelling a continuing disturbance such as grazing. Before
grazing (5a), the succession resembles (1) but with a climax at C not D. Grazing
changes the transition probabilities themselves (5b) such that C is now a transient
state on the way to D and can indeed be bypassed by going straight from B to D.
Grazing has also increased the chance of the early states being replaced. This is by
no means the limit of the models’ versatility - it only serves to illustrate the range.
Equally, the mimicking ability does not mean that the models are true (see text).
Downloaded from ppg.sagepub.com at PENNSYLVANIA STATE UNIV on September 20, 2016
486
III
Applied uses of succession
To the inhabitants of industrial nations, a number of spectacular examples of
succession theory applied to practical problems are in easy reach, although the
layman may not recognize them as such. Ideally, they will not be recognizable successful applications to the revegetation of industrial waste tips, stabilization of
sand dunes, reservoir and new construction landscaping will present themselves as
indistinguishable from the surrounding agricultural and seminatural landscape.
The ecology of land restoration is now a well-established field and an extensive
literature is developing on the subject (see e.g. Bradshaw and Chadwick, 1980;
Cairns et al., 1976; Goodman and Chadwick, 1978; Holdgate and Woodman,
1976). Although the practical transition from a bare, unsightly and often dangerous
landscape to something more useful to people often involves a great deal of intricate and difficult research, the theoretical answer can be quite simple: a means
must be found to initiate and accelerate primary succession from conditions inimical
to most forms of life.
Two examples will suffice to illustrate the general point. Open-cast kaolin (china
clay) workings in southwest Britain (Cornwall) left conical tips of micaceous waste
which supported only a sparse vegetation even after a century of abandonment
(Skeffington and Bradshaw, 1982). Modern disposal produces tips of waste and
overburden which are better designed for stability, but some of the older tips had
to be reshaped before ecological work could begin (Allaby, 1983). The key problems in the establishment of succession were identified as nutrient (especially
nitrogen) shortages and the free leaching properties of the original waste i.e. although
seed could be sown mixed with fertilizer, repeat applications would be prohibitively
expensive unless an effective nitrogen cycle could be established within the tips.
This was achieved using the exotic (to Britain) tree lupin (with a very high rate of
nitrogen fixation by associated bacteria in root nodules) in combination with
initial mulching and later sowing of other species. In a very few years a sward
develops which helps stabilize the tip surface, starts to build soil structure and can
now support sheep grazing as well as starting to accumulate a wide variety of other
plant and animal species.
Wastes contaminated with heavy metals pose a further problem; it is not enough
to identify the key nutrients limiting the start of primary succession, for the wastes
are often toxic enough to kill most plant species. If the associated engineering
problems can be solved; it is sometimes possible to seal the wastes in with a suitable
layer of overburden (Bradshaw and Chadwick, 1980). In Welsh lead workings, a
cheaper and equally effective method has been adopted (Bradshaw et al., 1978).
They fould that on some of the older workings with very high lead concentrations
(due to less effecient extraction processes in the past), one or two plant species
could be found growing in very high lead concentrations. On examination these
were found to be genetically resistant strains, and by pooling the species from a
large number of spoil heaps around the country, several dozen species could be
accumulated (Smith and Bradshaw, 1979). Unfortunately, few of these species
Downloaded from ppg.sagepub.com at PENNSYLVANIA STATE UNIV on September 20, 2016
487
had nitrogen-fixing symbionts, and so establishment of a viable sward and the
initiation of soil formation had to be accompanied by applying fertilizers and/or
sewage sludge. Thus the problem was partially solved by artificially enhancing
colonization (bringing the plants in) combined with identifying the key nutrients
involved in initiating succession. The solution is not perfect; although the lead tips
so treated are no longer unsightly and are safe for amenity purposes, the lead
levels in tolerant plant species are too high to permit agricultural use (Bradshaw
and Chadwick, 1980).
Low-input agriculture and forestry worldwide is plagued by problems caused
by inadequate understanding and/or application of processes of plant community
change. We feel that this is a neglected area of research and one in which investigation of particular problems would reap enormous dividends. Such problems are
most likely to be encountered in third world countries where social, economic or
environmental conditions make the high-input agriculture of the developed world
difficult or inappropriate. To date, we know of few studies where particular problems have been solved (but see Kruger, 1984) and a general example is worked
out below to indicate the sort of applications that are possible.
A common problem in semiarid areas has been the reversion of grasslands and
savanna to woodland following use as grazing range by domestic stock. Walker
al. (1981) proposed a model which accounts for this process and suggests relatively simple solutions. They showed that the balance between water permeability
properties of the soil, deep-rooted plants such as most of the woody species, and
shallow-rooted ones such as the pasture grasses, and grazing pressure, resulted in
two alternative equilibria. Given a range of semiarid seasonal rainfall regimes,
under light grazing the grasses formed an extensive shallow-root mat which effectively suppressed most shrub seedlings and prevented water from reaching the
deeper layers of the soil where established shrub roots lay. If grazing pressure
was increased, there came a point where the shallow grass root mat is weakened
and more water (also probably leached nutrients) reached deeper layers of the
soil. Young grasses cannot establish because of the grazing pressure, but young
woody plants manage to burst past the grazing levels because of their increased
access to water underneath. Once the woodland is established, it will remain as
by this time the canopy has closed and most water passes through the regions
where young grass roots lie. The system can only be broken by artificial removal
of the shrub cover (e.g. by burning) combined with the exclusion of herbivores
and possibly reseeding: the season of the year at which this is done is also crucial
(Kruger, 1984). The problem need never arise if stocking densities are carefully
managed at the start.
Even in intensive agriculture, an understanding of the interactions between
different types of grazers and the development of the sward can be important
in devising the most efficient management. Moore and Clements (1984) found
that frit fly (especially Oscinella frit) infestations were lower when a ryegrass
ley was cut than when it was rotationally grazed by sheep. Grazing produced
higher numbers of tillers, and the individual tillers were more susceptible to frit fly
et
Downloaded from ppg.sagepub.com at PENNSYLVANIA STATE UNIV on September 20, 2016
488
attack, for reasons which remain uncertain. The natural succession after sowing a
ley has always been an expensive problem; either from the need for frequent
reseeding or from the decline in productivity associated with a more diverse sward.
In many areas of Britain modern practice is to keep grazing animals off during the
spring and summer months, taking hay or silage cuts instead. The pastures are only
grazed from later on in the summer. This is a direct outcome of work such as that
described above and going back to Jones (1933). His findings showed, among other
things, that the traditional practice of pasturing as many sheep as the area could
hold during the winter and leaving the same number on in the summer quickly
turned grass/clover mixture into high diversity, weedy, low productivity swards.
Pure ryegrass or clover-ryegrass mixtures could be maintained by changing the
phenology of grazing to match the phenology of the desired species, as is done now.
Wildlife conservation, especially in areas with a long history of human use, is
often a matter of the manipulation of habitats to accord with a particular
successional stage. Here it is rarely enough to know only a few key processes in the
succession; the rarity of a species and/or a particular community may depend on
the fine details of a relationship between climate, edaphic factors, the species
available for colonization, and past human management. Two studies in the conservation of butterflies in Britain, one unsuccessful, the other a qualified success,
serve to illustrate the point. The native Large Blue (Maculinea arion) is now extinct
in Britain, the Adonis Blue (Lysandra bellargus) persists in a few places. Both
species’ larvae start life as phytophages of common plants of limestone grasslands
(Thymus drucei and Hippocrepis comosa respectively). The Large Blue is then
taken into a nest of Myrmica sabuleti by foraging worker ants, wherin it completes
its development as an ant predator. The Adonis Blue remains phytophagous but is
tended by ants of several species (Thomas, 1983) and may pupate in an ants’ nest.
In both systems, the animal part is dependent on the microclimate of short, heavily
grazed limestone swards in the south of England: the Adonis Blue is further
restricted to southfacing slopes. Changes in farm economy in the early twentieth
century were followed by the removal of heavy rabbit grazing by myxomatosis in
the 1950s. The consequent decline in both butterfly species was noted early, but
conservation efforts were frustrated by inadequate knowledge of the unusual
plant communities and grazing management on which they and their ant associates
depended (Thomas, 1980; 1984). By the time that this was understood, the Large
Blue had declined to a point where a combination of years with atypical weather
drove it extinct (Thomas, 1980). The vegetation needed by both species can be
recreated, and has been, by reimposing the right grazing regime in the right place,
but remaining colonies of the Adonis Blue are usually too scattered for effective
colonization; this has been done successfully by artificial means (Thomas, 1984
and personal communication).
This story of particular species reflects both i) the need to understand the
processes behind change in the whole community for conservation to be effective
and ii) the potential for restoration of any community whose component species
are still available provided that the mechanisms which drive secondary succession
Downloaded from ppg.sagepub.com at PENNSYLVANIA STATE UNIV on September 20, 2016
489
(e.g. on abandoned agricultural land) towards it are well understood and can be
reapplied. We see this as one of the areas within succession study with great potential for future applications, which are only beginning to be used. Great potential for
future development also lies in the management of low-input systems of agriculture
and forestry, especially in third world countries where reliance on continued input
of fertilizers and pesticides from outside can be too expensive or not feasible for
social reasons. Studies we have such as Walker et al.’s (1981) and Jones’s (1933) have
direct implications for the way in which sustained productivity of land can be
maximized with the minimum need for expensive external
inputs.
Department of Zoology, University of Oxford, UK
Imperial College at Silwood Park, Ascot, UK
Acknowledgements
C.W.D.G. thanks the Animal Ecology Research Group for providing facilities,
and Julie Hamilton for reading an early draft and putting in the commas. V.K.B.
thanks Clive Stinson for his active participation in the early experiments on the
effects of insect herbivores on plant succession referred to on p. 479.
N
References
Adams, S.N. 1975: Sheep and cattle grazing in forests: a review. Journal of Applied
Ecology 12, 143-52.
Allaby, M. 1983: The greening of the Cornish alps. New Scientist 98, 138-41.
Amman, G.D. 1977: The role of the mountain pine beetle in lodgepole pine ecosystems : impact on succession. In Mattson, W.J., editor, The role of arthropods
in forest ecosystems, Berlin: Springer-Verlag, 3-18.
Austin, M.P. and Belbin, L. 1981: An analysis of succession along an environmental
gradient using data from a lawn. Vegetatio 46, 19-35.
Bailey, N.T.J. 1964: The elements of stochastic processes, with applications to the
natural sciences. Chichester: Wiley International.
Bakker, P., de Leeuw, J. and van Wieren, S.E. 1983: Micro-patterns in grassland
vegetation created and sustained by sheep grazing. Vegetatio 55, 151-61.
Zeiraphera
Baltensweiler, W. 1975: Zur Bedeutung des Grauen Lärchen wiclden (
diniana Gn) für die Lebensgemeinschaft des Lärchen-Arvenwaldes. Mitteilungen der Schweizerischen entomologischen Gesellschaft 48, 5-12.
Baltensweiler, W., Benz, G., Boney, P. and Delucchi, V. 1977: Dynamics of larch
bud moth populations. Annual Review of Entomology 22, 79-100.
Bess, H.A., Spurr, S.H. and Littlefield, E.W. 1947: Forest site conditions and the
Gypsy Moth. Harvard Forestry Bulletin No. 22. Harvard University.
Bews, J.W. 1920: The plant ecology of the coastal forest of Natal. Annals of the
Natal Museum 4, 367-469.
Biswell, H.H. 1974: Effects of fire on chaparral. In Kozlowski, T.T. and Ahlgren,
C.E., editors, Fire and ecosystems, London: Academic Press, 321-65.
Downloaded from ppg.sagepub.com at PENNSYLVANIA STATE UNIV on September 20, 2016
490
1984: Fire survival of Cape Proteaceae - influence of fire season and
seed predators. Vegetatio 56, 65-74.
Bradshaw, A.D. and Chadwick, M.J. 1980: The resoration of land. Studies in
Ecology No. 6, Oxford: Blackwell Scientific.
Bradshaw, A.D., Humphreys, M.O. and Johnson, M.S. 1978: The value of heavy
metal tolerance in the revegetation of metalliferous mine wastes. In Goodman,
G.T. and Chadwick, M.J., editors, 1978, 311-34.
Brown, V.K. 1984: The ecology of secondary succession: insect-plant relationships. Bioscience 34, 710-16.
1985: Insect herbivores and plant succession. Oikos 44, (in press).
Cairns, J., Dickson, K.L. and Herricks, E.E. 1976: Recovery and restoration of
Bond, W.J.
damaged ecosystems Charlottesville: University of Virginia Press.
Carlquist, S. 1974: Island biology. New York: Columbia University Press.
Clements, F.E. 1916: Plant succession: analysis of the development of vegetation.
Publication of the Carnegie Institute, Washington No. 242.
Connell, J.H, and Slatyer, R.O. 1977: Mechanisms of succession in natural communities and their role in community stability and organisation. American
Naturalist 111, 1119-44.
Cowles, H.C. 1901: The physiographic ecology of Chicago and vicinity. Botanical
Gazette 31, 145-82.
Crocker, R.L. and Major, J. 1955: Soil development in relation to vegetation and
surface age at Glacier Bay, Alaska. Journal of Ecology 43, 427-48.
Drury, W.H. and Nisbet, I.C.T. 1973: Succession. Journal of the Arnold Arboretum,
Harvard University 54, 331-68.
Duffey, E., Morris, M.G., Sheail, J., Ward, L.K., Wells, D.A. and Wells, T.C.E. 1974:
Grassland ecology and wildlife management. London: Chapman and Hall.
Egler, F.E. 1954: Vegetation science concepts. I: Initial floristic composition, a
factor in old-field vegetation development. Vegetatio 4, 412-17.
Ellison, L. 1960: Influence of grazing on plant succession of rangelands. Botanical
Review 26, 1-78.
Faegri, K. and Pijl, L. van der 1966: The principles of pollination ecology. Oxford:
Pergamon Press.
Fitter, A.H. and Hay, R.K.H. 1981: Environmental physiology of plants. London:
Academic Press.
and Hotrabhavandra, T. 1982: Patch dynamics of plant
abandoned surface coal mines; a case history approach. Journal
of Ecology 70, 707-20.
Gardner, W.A. 1921: Effect of light on the germination of light-sensitive seeds.
Botanical Gazette 71, 249-88.
Gibson, C.W.D., Guilford, T.C., Hambler, C. and Sterling, P.H. 1983: Transition
matrix models and succession after release from grazing on Aldabra atoll.
Game, M., Carrell, J.E.
succession
on
Vegetatio 52, 151-59.
Godwin, M. 1936: Studies in the ecology of Wicken Fen III. The establishment
and development of fen scrub.
Journal of Ecology 24, 82-116.
H.
and
1939: The ecology of a raised bog near Tregaron,
V.M.
Godwin,
Conway,
Cardiganshire. Journal of Ecology 27, 313-59.
Golley, F.B. editor, 1977: Ecological succession. Benchmark Papers in Ecology
Vol. 5, Stroudsburg, Pennsylvania: Dowden, Hutchinson and Ross.
Downloaded from ppg.sagepub.com at PENNSYLVANIA STATE UNIV on September 20, 2016
491
Chadwick, M.J. 1978: Environmental management of mineral
Sijthoff and Nordhoff.
Gould, S.J. and Vrba, E.S. 1982: Exaptation - a missing term in the science of
form. Paleobiology 8, 4-15.
Grime, J.P. 1979: Plant strategies and vegetation processes. Chichester: John Wiley.
Gross, K.L. and Werner, P.A. 1978: The biology of Canadian weeds 28. Verbascum
thapsus L. and V. blattaria L. Canadian Journal of Plant Sciences 58, 401-13.
Grubb, P.J. 1976: A theoretical background to the conservation of ecologically
distinct groups of annuals and biennials in the chalk grassland ecosystem.
Biological Conservation 10, 53-76.
Harborne, J.B. 1977: Introduction to ecological biochemistry. London: Academic
Goodman, G.T.
and
wastes. Leiden:
Press.
Hansen, E.A.
and Dawson, J.O. 1982: Effects of Alnus glutinosa on hybrid Populus
height growth in a short-rotation intensively cultivated plantation. Forest
Science 28, 49-59.
Harper, J.L. 1977: Population biology of plants. London: Academic Press.
Hnatiuk, R.J., Woodell, S.R.J. and Bourn, D.M. 1976: Giant tortoise and vegetation
interactions on Aldabra atoll. Part 2: Coastal. Biological Conservation 9, 305-
16.
Hodgkin,
S.E. 1984: Shrub encroachment and its effect on soil fertility on
borough Warren, Anglesey, Wales. Biological Conservation 29, 99-119.
New-
and Woodman, M.J. 1976: The breakdown and restoration of
ecosystems. New York: Plenum Press.
Horn, H.S. 1974: The ecology of secondary succession. Annual Review of Ecology
and Systematics 5, 25-37.
1976: Succession. In May, R.M., editor, Theoretical ecology: principles and
applications, Oxford: Blackwell Scientific, 187-204.
1978: Optimal tactics of reproduction and life history. In Krebs, J.R. and
Davies, N.B., editors, Behavioural ecology, Oxford: Blackwell Scientific,
411-29.
Hulst, R. van 1979: On the dynamics of vegetation: Markov chains as models of
succession. Vegetatio 40, 3-14.
Jackson, J.B.C. 1981: Interspecific competition and species distributions: the
ghosts of theories and data past. American Zoologist 21, 889-902.
Jones, M.G. 1933: Grassland management and its influence on the sward. Empire
Journal of Experimental Agriculture 1, 43-57, 122-28, 223-34, 361-67.
Kruger, F.J. 1984: Effects of fire on vegetation structure and dynamics. In Booysen,
P. de V. and Tainton, N.M., editors, Ecological effects of fire in South African
ecosystems, Berlin: Springer-Verlag, 219-43.
Lawrence, D.B., Schoenike, R.E., Quispel, A. and Bond, G. 1967: The role of
Dryas drummondi in vegetation development following ice recession at Glacier
Bay, Alaska, with special reference to its nitrogen fixation by root nodules.
Journal of Ecology 55, 793-813.
May, R.M. 1981: Theoretical ecology: principles and applications, second edition.
Oxford: Blackwell Scientific.
McBrien, H., Harmsen, R. and Crowder, A. 1983: A case of insect grazing affecting
plant succession. Ecology 64, 1035-39.
Holdgate, M.W.
Downloaded from ppg.sagepub.com at PENNSYLVANIA STATE UNIV on September 20, 2016
492
Merton, L.F.H., Bourn, D.M. and Hnatiuk, R.J. 1976:
Giant tortoise and
vegetation
interactions on Aldabra atoll. Part 1: inland. Biological Conservation 9, 293316.
Miles, J. 1978: In Heal, O.W., editor, Upland land use in England and Wales,
Countryside Commission Publication No. 111.
Moore, D. and Clements, R.O. 1984: Stem-borer larval infestations of rye-grass
swards under rotationally grazed and cut conditions. Journal of Applied
Ecology 21, 581-90.
Olson, J.S. 1958: Rates of succession and soil changes in southern Lake Michigan
sand dunes. Botanical Gazette 108, 125-70.
Oosting, H.J. 1942: An ecological analysis of the plant communities of Piedmont,
North Carolina. American Midland Naturalist 28, 1-126.
Peterken, G.F. 1981: Woodland conservation and management. London: Chapman
and Hall.
Pickett, S.T.A. 1982: Population patterns through twenty years of old-field succession. Vegetatio 49, 45-59.
Pigott, C.D. 1968: Biological flora of the British Isles No. 111: Cirsium acaulon
(L.) Scope. Journal of Ecology 56, 597-612.
Pimm, S.L. 1982: Food webs. London: Chapman and Hall.
Piroznikow, E. 1983: Seed bank in the soil of stabilised ecosystem of a deciduous
forest (Tilio-Carpinetum) in the Bialowieza National Park. Ecologia Polska
31, 145-72.
Purdie, R.W. and Slatyer, R.O. 1976: Vegetation succession after fire in sclerophyll
woodland communities in southwestern Australia. Australian Journal of
Ecology 1, 223-36.
1980: Ancient woodland. London: Edward Arnold.
Rackham, O.
Rorison, I.H. 1969: Ecological inferences from laboratory experiments on mineral
nutrition. In Rorison, I.H., editor, Ecological aspects of the mineral nutrition
of plants, British Ecological Society Symposium No. 9, Oxford: Blackwell
Scientific, 155-75.
Shugart, H.H., Crow, T.R. and Hett, J.M. 1973: Forest succession models: a
rationale and methodology for modelling forest succession over large regions.
Forest Science 19, 203 -12.
Siddiqui, M.Y., Myerscough, P.J. and Carolin, R.C. 1976: Studies in the ecology of
coastal heath in New South Wales. Australian Journal of Ecology 1, 175-83.
Skeffington, R.A. and Bradshaw, A.D. 1982: Nitrogen accumulation in kaolin
mining wastes in Cornwall IV: Sward quality and the development of a nitrogen cycle. Plant and Soil 62,439-51.
Smith, R.A.H. and Bradshaw, A.D. 1979: The use of metal-tolerant plant populations for the reclamation of metalliferous wastes. Journal of Applied Ecology
16, 595-612.
Southwood, T.R.E. 1978: Ecological methods, second edition. London: Chapman
and Hall.
Southwood, T.R.E., Brown, V.K.
and Reader, P.M. 1979: The relationship of
plant and insect diversities in succession. Biological Journal of the Linnaean
Society 12, 327-48.
Spedding, C.R.W. 1971: Grassland ecology. Oxford: Clarendon Press.
Downloaded from ppg.sagepub.com at PENNSYLVANIA STATE UNIV on September 20, 2016
493
Stearns, S.C. 1977: The evolution of life history traits. Annual Review of Ecology
and Systematics 8, 145-71.
editor, 1983: The interface between life history evolution, whole organism
ontogeny and population genetics. American Zoologist, 23, 1-125.
G. hercynium
Tansley, A.G. 1917: On competition between Galium saxatile L. (
Weig.) and G. sylvestre Poll. (
G. aspera Schreb.) on different types of soil.
Journal of Ecology 7, 173-79.
Thomas, J.A. 1980: Why did the Large Blue become extinct in Britain? Oryx 15,
243-47.
1983: The ecology and conservation of Lysandra bellargus (Lepidoptera:
Lycaenidae) in Britain. Journal of Applied Ecology 20, 59-83.
1984: The behaviour and habitat requirements of Maculinea nausithous (the
Dusky Large Blue butterfly) and M. teleius (the Scarce Large Blue) in France.
Biological Conservation 28, 325-47.
Thompson, K. and Grime, J.P. 1979: Seasonal variation in the seed banks of
herbaceous species in contrasting habitats. Journal of Ecology 67, 893-921.
Usher, M.B. 1979: Markovian approaches in ecological succession. Journal of
Animal Ecology 48, 413-26.
1981: Modelling ecological succession, with particular reference to Markovian
models: Vegetatio 46, 11-18.
Walker, B.H., Ludwig, D., Holling, C.S. and Peterman, R.M. 1981: Stability of semiarid savanna grazing systems. Journal of Ecology 69, 473-98.
Watt, A.S. 1947: Pattern and process in the plant community. Journal of Ecology
35, 1-22.
Weaver, H. 1974: Effects of fire on temperate forests. In Kozlowski, T.T. and
Ahlgren, C.E., editors, Fire and ecosystems, London: Academic Press, 279-319.
Whelan, R.J. and Main, A.R. 1979: Insect grazing and post-fire succession in
southwest Australian woodland. Australian Journal of Ecology 4, 387-98.
Downloaded from ppg.sagepub.com at PENNSYLVANIA STATE UNIV on September 20, 2016