Annals of Botany 85 (Supplement B): 3-15, 2000
doi:10.1006/anbo.1999.1054, available online at http://www.idealibrary.com on IDE4 l®
The Ecology of Bracken: Its Role in Succession and Implications for Control
R. H. MARRS*t, M. G. LE DUCt, R. J. MITCHELLtt, D. GODDARDT, S. PATERSONS
and R. J. PAKEMAN§
tSchool of Biological Sciences, University of Liverpool, PO Box 14, Liverpool L69 3BX, UK and §Macaulay Land
Use Research Institute, Craigiebuckler, Aberdeen AB15 8QH, UK
Received: 20 July 1999
Returned for revision: 7 September 1999
Accepted: 18 October 1999
Bracken (Pteridium) holds a pivotal role in succession, usually occurring in sequence between plagio-climax
communities such as heathland and woodland. It is at this interface that bracken causes problems for man, as the subseral communities are more valuable for agricultural use and most have a greater conservation value than brackendominated ones (there are a few exceptions). This paper examines the role of bracken in a series of successional
trajectories on lowland heaths; there is evidence that bracken occurs in a trajectory towards birch woodland in
Dorset. Whether the bracken stage is an intermediate stage towards woodland or acts as a 'mini-climax' in itself
remains to be demonstrated. Thereafter, the impact of bracken control on vegetation development is examined from
two successional viewpoints, succession reversal towards the early successional communities, and successional
accelerations towards woodland. A range of examples is provided from: (1) lowland heaths in England; (2) moorlands
in upland Britain where bracken has been treated with asulam; and (3) in North Wales where attempts have been
made to restock woodlands.
© 2000 Annals of Botany Company
Key words: Bracken, Pteridium, control, vegetation restoration, heathland, moorland, grassland, woodland,
succession, modelling.
INTRODUCTION
Bracken [Pteridium aquilinum (L.) Kuhn] is an almost
unique plant. It is extremely successful, and is the only
terrestrial fern that dominates large tracts of land outside
woodland in temperate climates. Originally a woodland
plant, it has managed to maintain high productivity outside
the woodland habitat, probably as a result of being able to
restrict its water loss more effectively than other ferns
(Pakeman and Marrs, 1992a). There are many reasons why
bracken is so successful, these include: (1) a very large
rhizome system containing large carbohydrate and nutrient
reserves, and many buds capable of producing new fronds;
(2) high productivity, which produces a frond canopy that
casts deep shade; (3) large accumulations of litter which
prevent other species from colonizing; (4) a range of toxic
chemicals within its tissues which can prevent it being eaten
or decaying, and possibly acting to prevent the ingress of
other species through allelopathy. As a result bracken is
regarded as a weed species, causing problems for a wide
range of land management options. However, simple weed
control, where only the target plant is considered, is
ineffective in the long-term; restoration to some other
community is essential. It is, therefore, essential to develop
an understanding of how bracken communities change
* For correspondence. Fax +44 (0) 151 794 4940, e-mail calluna
@liv.ac.uk
t Present address: Institute of Terrestrial Ecology Banchory
Research Station, Hill of Brathens, Banchory, Kincardineshire
AB31 4BY, UK.
0305-7364/00/0B0003 + 13 $35.00/00
through time, i.e. where bracken fits into a successional
framework, and how the communities develop once
bracken is managed.
We hypothesize that bracken-dominated communities
occupy a mid-successional position between early-successional, semi-natural communities such as grassland, heaths
and moors, and late-successional woodlands. From a land
manager's viewpoint there are two directions in which the
bracken community can be changed; either by reversing
succession towards early-successional communities, or by
promoting succession if woodland is to be developed. In the
former case the ecological problems include weed control,
establishment of appropriate vegetation, and its long-term
maintenance, and in the latter case, the establishment of
tree species.
The aim of this paper is to assess whether this hypothetical schema of bracken within a successional envelope is
valid, and then consider the successional problems that
occur when bracken is managed towards early- and latesuccessional communities.
WHERE DOES BRACKEN FIT INTO
SUCCESSION?
In a recent study we investigated a range of successions in
Dorset (UK) heathlands (an early-successional biotope),
and measured both species composition of the vegetation
and a range of soil chemical properties (Mitchell et al.,
1997). Low soil fertility is essential for the maintenance of lowland heath (Gimingham, 1992), and any
© 2000 Annals of Botany Company
Marrs et al.--Ecology of Bracken
4
increase in fertility during succession hinders heathland
regeneration. We selected six different successional stages:
heathlands with no succession, and heathlands that had
been invaded by five invasive, late-successional species:
Pteridium, Pinus sylvestris, Betula spp., Rhododendron
ponticum and Ulex europaeus. We then tested a range of
hypothetical multivariate successional models that could be
used to explain succession on these heaths. The models for
vegetation (see Fig. 1) were designed to show: (a) no
successional trend whatsoever, effectively the null model;
(b) site-dominated succession; (c) a single generalized
successional trajectory that accounted for all species; (d) a
multi-trajectory model, with each species dominant having
a different effect. The results for the vegetation data,
analysed using DECORANA, supported the multi-trajectory model (Fig. 2); i.e. each successional dominant species
changes the heathland in a different way, although there is a
possibility that bracken could occupy an intermediate
position in the Betula succession. When soil data were
included in a canonical correspondence analysis (CCA)
increasing bracken cover was associated with elevated soil
nitrogen concentrations (Mitchell et al., 1997).
We repeated this work on the Wirral (UK) (Goddard,
1999) and found considerable concordance between the
different successional phases in the two regions (Dorset and
Wirral). The successional stages were ranged on their
'proximity to heath', with the nearest to heath first.
In Dorset, when vegetation only was included: Ulex
and Pinus < Pteridium < Rhododendron and Betula, and
when soil data were added: Ulex < Pinus and Pteridium <
Rhododendron and Betula. On the Wirral the sequence for
vegetation was: Ulex < Pteridium and Quercus < Betula,
B
A
H\,B
PS
pA\U
-X
R
H
U
PS
U
PS
R
R
B
PA
U
H
/
/
//R
\\
PAU
PA
/
\
R
H
PS
P4/
PS
B
B
B
\
PA
H
B
U//PA
H
D
C
PSPS
B
//
/
/
/
B
PS
PS \PS
PS
B
\\
R/
/
PA// PA
U /U/
H//
PA
R
PA
A PA
PA
/
H>qLPA H\
IU
R
R
R
U
H/ H
FIG. 1. Hypothetical ordination diagrams illustrating results that might be obtained from DECORANA analysis of quadrat data obtained from
successional stages in Dorset heathlands. The arrows represent different possible successional trajectories (after Mitchell et al., 1997). H, Open
heathland; B, +B (Betula spp.) successional stage; PS, +PS (Pinus sylvestris) successional stage; PA, +PA (Pteridium aquilinum) successional
stage; R, +R (Rhododendron ponticum) successional stage; U, +U (Ulex europaeus) successional stage. A, No successional trajectory from the
heath to successional stages; a random distribution of quadrats from the different successional stages and sites; B, site effect. The major influence
over the successional trajectories is the site; C, only one successional trajectory along which a heathland site moves. In this example open heath
goes to +U to +PA to +R to +B and finally to +PS; D, several different successional trajectories along which a heathland site may move,
depending on the species which invades. In this case the +U stage is closest to the heathland, the +PS stage is furthest from the heathland and the
+PA, +R and +B stages are all similar in their distance from the heathland.
Marrs et al.--Ecology of Bracken
5
TABLE 1. A comparison of how successional stages differ
from each other in two English regions: the Dorset heaths
(Mitchell et al., 1997) and Thurstaston in Merseyside
(Goddard, 1999)
Thurstaston heath
Dorset heath
Ulex
Pteridium
Betula
4.222 (1)
4171 (1)
6.182 (2)
5.519 (2)
8.424 (3)
7.311 (3)
Ulex
Betula
Dorset
el
Thurstaston
.2
Heath
Pteridium
Ulex
Betula
Heath
Pteridium
0.515 (1)
0.777 (2)
1.458 (3)
9.100 (4)
The stages are compared using a Euclidean distance measure derived
from a canonical correspondence analysis (CCA), which included both
species composition and soil chemical data; the greater the distance,
the further apart are the stages in multidimensional space.
Axis 1
FIG. 2. Quadrats sampled from a range of successions on the Dorset
heathlands to test the hypotheses put forward in Fig. 1 and plotted by
their scores on the first two axes of a DECORANA analysis after
Mitchell et al. (1997). This illustrates how quadrats from the same
successional stages cluster together and the relationships between the
different successional stages. The postulated successional trajectories
are marked with arrows. (0) Open heathland; () Betula spp. is the
major invader; (+) Pinus sylvestris is the major invader; (x) Pteridium
aquilinum is the major invader; () Rhododendron ponticum is the
major invader; () Ulex europeaus is the major invader.
and for vegetation plus soils: Betula < Quercus <
Pteridium < Ulex. There is remarkable similarity in the
sequences when vegetation alone was considered, but the
juxtaposition of the ranks when the soils are included
suggests that successions may have different effects on the
environment in different situations. This supports the
individualistic concept in succession (Gleason, 1927), and
also suggests that subtle regional differences must be taken
into account when defining strategic land management
policies.
We have carried out a combined analysis of the Dorset
and Wirral data, including only those successional stages
common to both. In measurements of the multivariate
distance between the different successions in the two
regions, the bracken-dominated communities were intermediate in impact in both Dorset and Wirral, but the
bracken was further from the heathland in Wirral than in
Dorset (Table 1), again emphasizing regional differences.
The effects of succession on propagule banks have also
been considered in the Dorset heathlands (Mitchell et al.,
1998). Here the bracken-dominated communities of all the
successions studied were the least modified relative to
heathland. They had significantly lower numbers of heathland species than the heathland soils, but there were few
non-heathland species present. In the Rhododendron and
Betula communities, an increasing proportion of the
seeds was classified as non-heathland species. Clearly the
change in seed bank will reflect the time that the bracken
has been dominant but, at least in Dorset, bracken has had
only limited effect on the species composition of the
seedbank.
All these data suggest that our initial hypothesis that
bracken is a mid- to late-successional species is a reasonable
starting point, in that there has been a trajectory away from
our baseline site. However, bracken-dominated communities may or may not lie on a trajectory towards woodland,
and the soils under bracken appear to be changed in a
different way from other successions (Mitchell et al., 1997;
Goddard, 1999).
Mechanisms of successional change involving bracken
There are two ways that bracken influences succession:
(1) through invasion into early-successional communities;
and (2) through controlling the invasion of latersuccessional species.
Invasion of early-successional communities. Bracken
colonizes semi-natural habitats either through the
spore -- prothallus pathway or by rhizome invasion from
adjoining land. Records of colonization through the
spore -- prothallus pathway are few, even though they
must occur; colonization can therefore be assumed to be
irregular, and perhaps controlled by combinations of
circumstances or extreme events. Most invasions probably
come from rhizome invasion. Rhizomes can invade
6
Marrs et al.-Ecology of Bracken
adjacent land, but rates which have been measured are at
most a few m year-' (0-36-0-46 m year-' at Ramsley Moor,
Derbyshire, UK and Levisham Moor, North York Moors,
UK; Pakeman unpubl. res.); but this must depend on the
competitive ability of the adjacent vegetation. Watt (1955)
in his classic study of the relationship between Calluna and
bracken suggested that both species exhibited cyclic
regeneration (sensu Miles, 1979), and there was an interdigitation along bracken-Calluna fronts, with bracken
invading pioneer and degenerate Calluna, and retreating
from building and mature phases. Calluna showed a similar
response with respect to the bracken growth cycle. Similar
processes have been described by Ninnes (1995), who
showed that moorland was more likely to be lost to bracken
invasion if it had not been burnt, that is if it had not been
maintained in its most vigorous condition with maximal
time in the building phase. He stated that 'the competitive
vigour of the dwarf shrub heath under a regular burning
regime appears to outweigh the risk of bracken invasion
immediately following fire'. This is important because
bracken, with its large store of underground buds on the
rhizome, is able to withstand fire.
Invasion by late-successional communities. Given that a
tree canopy can suppress bracken, it is reasonable to expect
a grass/heath/moor--bracken--woodland succession. This
could be accommodated in many models of succession,
facilitation, inhibition, tolerance, resource-ratio etc. One
school of thought holds that bracken, once established,
inhibits further colonization by other species including trees
(sensu Niering and Goodwin, 1974; Connel and Slatyer,
1977). If this is so then natural colonization by latesuccessional tree species can only occur under two
conditions, either at the start of the succession when
bracken is also invading and at relatively low vigour (either
Initial Floristic Composition model, Egler, 1951; Tolerance
model, Connel and Slatyer, 1977), or if the bracken is
established, then some factor(s) cause(s) the bracken to
diminish, even if only temporarily.
There is no doubt that bracken inhibits the invasion of
other species, either by direct shading or by the physical
presence of litter (Miles and Kinnaird, 1979a,b; Marrs,
1988). However, Marrs (1987a) found low densities of
Betula seedlings (one seedling 200m - 2) invading plots
where the bracken canopy had remained untreated. In a
second experiment (Marrs, 1987b), Betula seedling densities
were excluded at densities > 21 fronds m-2 and restricted
to 0.25 seedlings m- 2 when frond densities were between
11-21 fronds m- 2 . Pinus sylvestris seedlings could apparently persist where frond density was 28 fronds m- 2, but
were restricted to single colonists in plots with frond
densities > 20 fronds m-2 . Marrs and Hicks (1986) in a
study at Lakenheath Warren, UK showed that 5.5 + 2.1
(mean + s.e.) Pinus sylvestris seedlings invaded sparse
bracken (39 + 2 fronds m-2 ; mean height 40 + 1 cm),
and about half that number (2.5 + 1-1 m-2 ) invaded dense
bracken (33 + 13 fronds m-2 ; height 89 + 5 cm). Pine
saplings (>0 5 m tall) also showed differences in their sizeclass distribution; two size classes were derived: class
I = 0.5-3 m, and class II > 3 m. The sparse bracken
community had greater densities of class I plants (25 vs.
4 per 300 m2) but lower densities of class II plants (7 vs.
17 per 300 m2) than the dense bracken. Marrs and Hicks
(1986) suggested that these results were brought about by
previous fluctuations in the bracken canopy density. On
balance, the evidence suggests that tree seedlings are
inhibited to some extent by dense bracken.
There is a tendency to believe that once bracken is
established it is there for evermore. However, there is good
evidence from both long-term studies and remote sensing
that bracken in some areas exhibits some form of cyclic
regeneration. This hypothesis was first put forward by Watt
(Watt, 1945, 1976), and substantiated on the same site by
Marrs and Hicks (1986). Moreover, where the bracken
cover, especially the litter layer, is disturbed, for example by
animal tracks, there can be rapid tree invasion. In a study at
Holme Fen, near Peterborough, UK, 76 Betula and six
Salix saplings invaded a 2-m wide pathway cut into tall,
dense bracken (30 fronds m-2 ; 2.5-3 m tall, with a 05 m
litter depth); no saplings colonized the uncut, dense bracken
areas (Marrs and Pakeman, 1995).
It is possible that almost all of the proposed successional
models operate some of the time. Marrs (1988) suggested a
generalized model that allowed the inhibition model of
succession (Connel and Slatyer, 1977) to operate against (a)
the cyclic model for bracken proposed by Watt (1945,
1976), and (b) an inhibition threshold (Fig. 3). This model
allows all of the observations noted above to operate in
different ways in different places and at different times. If
the relationship fluctuates around the threshold then tree
seedlings can invade, if the relationship is always above the
threshold then invasion never occurs, and more complex
models are possible. If this model were valid it could
account for the wide variety of responses found under field
conditions as a result of differential responses around the
threshold through time at individual sites or between
bracken clones.
It is also possible that tree seedling invasion into bracken
areas is prevented by external factors, for example a lack of
appropriate seed sources, or the effects of herbivores, which
can prevent the ingress of trees into many semi-natural
communities (Miles, 1979). In order to answer some of the
outstanding issues associated with the transition between
bracken to woodland, the effects of these external factors
must be separated from the inhibitory effects of bracken on
its own.
MANAGEMENT TO REVERSE SUCCESSION
Over a 20-year period of studying management to reverse
succession on bracken-dominated sites we have used a
range of approaches which have provided both successes
and failures. We have (1) monitored vegetation development on long-term study plots, where the bracken and
the vegetation have been managed at the plot scale, (2)
assessed vegetation recovery after bracken control using a
chronosequence approach on a countrywide scale, and (3)
developed a multivariate modelling approach to assess how
successful initial vegetation management has been, and to
monitor continuing success.
Marrs et al.-Ecology of Bracken
Three
Three
Three
Pioneer
Building
Mature Degenerate
FIG. 3. Hypothetical relationships between inhibition of succession to
woodland around a threshold, and the regeneration cycle of bracken,
showing inhibition only in the competitive building and mature phases
(A), complete inhibition throughout the bracken's life cycle (B), and
incomplete or variable inhibition throughout the bracken's life cycle
(C) (after Marrs, 1988).
The long-term plot approach
This study was done at Cavenham Heath in the Brecklands region of East Anglia, UK. A randomized block, fully
factorial experiment was set up in 1978 on an area of dense
bracken (Lowday and Marrs, 1992a). The treatments
TABLE
7
applied were designed to test a range of bracken control
and heathland restoration strategies (Table 2). Treatment
application was continued with modifications for 18 years
(Table 2) and the treatment effects on both bracken and the
developing heathland vegetation monitored (summarized in
Marrs, Johnson and Le Duc, 1998a,b).
The effects on bracken were considerable, but no
treatment eradicated the bracken. Cutting continuously
either once or twice yearly for 18 years reduced bracken
frond biomass to 6 and 3% of untreated levels, respectively.
Application of the herbicide asulam was initially the most
effective treatment, but there was relatively rapid recovery;
repeat applications produced similar responses (Fig. 4).
An important result was the relatively rapid recovery of
the bracken after the treatments stopped. Some treatments
recovered to control levels after a further 12 years. The most
successful treatment was cutting twice yearly for 6 years;
frond biomass had reached only 40% of untreated levels
12 years after the last cut (Fig. 4) (Marrs et al., 1998a).
There were several important conclusions derived from
this experiment. First, bracken is extremely difficult to
eradicate from a patch of land, indeed it may be impossible
unless there is a complete change of land use, e.g. to
cultivated agriculture. Second, even to sustain a long-term
reduction in bracken infestation may require continuous
applications of control treatments. Finally, all control
treatments applied in this study proved effective to some
extent, and there may be considerable scope for applying
them in combination; a combination of treatments might
provide a synergistic effect which is cost effective. Studies
to test some potential treatment combinations are currently
in progress in the British uplands (Le Duc et al., this
volume).
However, bracken control was only part of the investigation, the main objective of the study was to reverse
succession and restore Calluna-dominated heathland. The
species likely to develop in the new early successional
community are outlined according to their value for
conservation management of the site in Table 3. Calluna
was clearly desirable; species typical of Breck grass
2. Treatment history in the 18-year experiments to test various bracken control and heathlandrestorationstrategies at
Cavenham Heath in Breckland
Experimental information
Phase 1 (1978-1984)
Phase 11 (1985 1996)
Bracken control treatments
i.
ii.
iii.
iv.
v.
vi.
As Phase I, but experimental blocks pooled from
n = 4 to n = 2
Two further treatments applied:
i. No further bracken control treatment
ii. Bracken control treatments continued as
Phase I. Asulam applied on 6 year cycle
(1984 and 1990)
Heathland restoration treatments
Replication
Vegetation sampling years
Model
Untreated control
Cut once/year
Cut twice/year
Asulam 1978
Asulam 1978 + 1979
Asulam 1978 plus cutting once/year
from 1979
i. No treatment, natural colonization
ii. Addition of Calluna seed
Four replicate blocks (n = 4)
1978, 1979, 1980, 1981, 1982, 1983, 1986
Four blocks x six bracken control x two
restoration = 48
All treatments were applied in factorial combination (after Marrs et al., 1998a,b).
n = 2
1986, 1988, 1990, 1991, 1993, 1996
Two blocks x six bracken control x two
restoration x two continued/stopped = 48
8
Marrs et al.--Ecology of Bracken
A
B
C
---
800
600
_
400
200
l
E
xi
--
'V
n
A
,5
78808284868890929496
r
-0
Cl
D
E
F
0
16
78808284868890929496
Year
or stopped after 6 years (--- ) on frond
FIG. 4. Effects of five bracken control treatments applied either continuously for 18 years (-)
- 2
biomass (g m ) at Cavenham Heath between 1978 and 1996: A, untreated; B, cutting once yearly (late July); C, cutting twice yearly (midJune and late July) (note no data were recorded in 1978); D, asulam initially applied once (in 1978), and in the continuous treatment applied
thereafter on a 6 year cycle; E, asulam initially applied twice (in 1978 and 1979), with continuous treatment as in D; and F, asulam applied once
(in 1978) and bracken cut once yearly thereafter. Means (n = 8 until 1984, n = 4 thereafter) and 2 x pooled s.e. are presented as vertical bars
(after Marrs et al., 1998a).
heaths (Watt, 1981a,b; Dolman and Sutherland, 1994),
were deemed desirable; clonal species such as Carex
arenaria and Calamagrostis epigejos were thought to be
possibly problematic; woody species typical of late-successional communities were deemed undesirable. Initial results
were promising (Marrs and Lowday, 1992), with good
establishment by seedlings in plots where Calluna seed
had been applied, and where there had been disturbance of
the litter layer. The role of litter disturbance was confirmed in subsequent experiments at the same site (Lowday
and Marrs, 1992b). After 10 years there was Calluna cover
in all bracken-treated plots (Fig. 5), with between 10 and
40% cover on seeded plots and best results where the
bracken was cut twice yearly (Fig. 5). Thus, the overall
strategies for succession reversal appeared to have been
successful.
Marrs et al.--Ecology of Bracken
TAB LE
9
3. Ranking of species on the basis of their conservation value in the bracken control-heathlandrestoration experiment
at Cavenham Heath (Marrs et al., 1998b)
Conservation importance
Species
Comments
'Essential'
'Desirable'
Calluna
Agrostis capillaris, Dicranum scoparium, Festuca ovina,
Dominant species at Cavenham Heath
Major components of Breck grass heath, minor
Galium saxatile, Rumex acetosella
Deschampsiaflexuosa
components of Calluna heath
Calamagrostisepigejos, Carex arenaria
Betula spp., Pinus sylvestris, Rubus fruticosus
Clonal and found on grass heaths
Woodland species
'Problematic'
'Undesirable'
In the following 8 years, however, there were marked
changes to vegetation composition. The mo st noticeable was
the almost complete death of Callunain 19990 and 1991, and
on from Callunaa complete change in community composition
dominated heath to either (a) Breck gra ss heath (Watt,
1981a,b), (b) areas covered by the clonal do minants, and (c)
limited invasion of woody species (Marrss et al., 1998b).
Subsequent studies using variation pa.rtitioning have
isolated the importance of each environmentntal explanatory
variable or set of variables in influencin g the vegetation
change; the explanatory variables includ ed management
treatment, spatial position on site, rablbit disturbance,
bracken recovery, climate and nitrogen deposition. This
approach identifies the amount of variation accounted for by
each set of explanatory variables on theiir own, and the
amount of overlap with others. In the fitrst phase of this
study (1978-1986), three factors contribut ed to vegetation
change-time, bracken control treatmer its, and spatial
effects (essentially the invasion of the clon al species). However, in the second phase (1986-1996), braacken treatments
were less important, with the effects of space, weather,
bracken recovery, and differential disturbance by rabbits
increasing in importance (Marrs and Le Duc, 2000).
Thus, successional stages currently occupied by dense
bracken can be reversed to an earlier stage, but it may not
be the one intended. Factors outside the control of the
vegetation manager may impinge on vegetation development, and there may be change towards an undesirable
community in the medium- to long-term.
The chronosequence approach
The chronosequence approach was first developed by
Jenny (extensively updated in the review by Jenny, 1980),
and it assumes that vegetation/ecosystem development is
entirely controlled by time. Usually the changes are inferred
using a space-for-time substitution approach. For the
assessment of vegetation change following bracken control,
this means using sites treated at different times as if they
were part of the same vegetation succession. We accept that
this approach is not as reliable as a study of individual sites
continuously charted through time, but it does allow trends
to be assessed which can be verified independently.
Pakeman and Marrs (1992b) first used this approach in a
pilot study of vegetation development after bracken control
by aerial application of asulam on the North York Moors.
Aerial applications of asulam are one of the most
commonly used bracken control techniques in the British
uplands. The conclusions from this study were that it was
S
o
possible to derive apparently sensible, and statisticallyc
significant, relationships using this approach.
In the North York Moors, vegetation development
after spraying was slow, about half of that found in the
o
0
Breckland plots discussed above. Two problems were
highlighted. First, of the 7% increase in vegetation cover
per annum, approximately half was accounted for by the
increasing cover of bryophytes, especially Campylopus
introfiexus. The dominance of bryophytes can delay or
even inhibit the colonization of heath and grass species
(Clement and Touffet, 1990). Second, reduction in the cover
U
Al
A2
AC
Cl
C2
of bracken litter was slow (7% per annum) probably as a
Treatment
result of its slow decomposition (Frankland, 1976). As
bracken litter is an impediment to plant establishment, litter
FIG. 5. Effects of bracken control and heathland restoration treatments
persistence was identified as a major constraint on
on the cover (%) of Calluna in the Cavenham Heath experiments in
1988. U, Untreated; Al, asulam once; A2, asulami twice; AC, asulam
vegetation succession after asulam application.
once plus cut once yearly; Cl, cut once yearly; C'2, cut twice yearly;
applied In order to provide a nationwide overview of vegetation
in factorial
factoriarly;
(Il) unseeded; (U) seeded with Calluna. Treatments applied in
response after asulam application the chronosequence
combination. Vertical bars represent the LSD (P < 0.05) (after Marrs
approach was extended to cover 117 sites across Britain.
and Lowday, 1992).
Marrs et al.--Ecology of Bracken
10
TABLE
4. Summary of the locations and attributes of the 117 sites across the UK used in the chronosequence study
Number
Country
Region
Scotland
Skye
Deeside
Strathclyde (Loch Fyne and Oban)
Southern Uplands (Bowhill, Eskdale,
Manor Valley)
Wales
North Wales (Lleyn Peninsula,
Snowdonia)
England
NE (Cheviot, Yorkshire Dales)
NW (Bowland Fells, Lake District)
North York Moors
W Midlands (Peak District,
S Staffordshire)
SW (Exmoor)
Elapsed time since
Number of sites
in each NVC
of sites
Altitude (m)
Aspect ()
Slope (°)
spraying (years)
vegetation type
3
3
9
12
30-70
230-330
30-80
210-375
150-225
120-135
110-330
61-320
10-16
11 18
5-29
10-26
0-2
4 5
0 5
0 10
3U
3U
7U; IW; ICG
7U; 4H; ICG
5
70-350
26-190
7 23
0-8
5U
25
16
22
12
200 460
110-405
135 345
95-330
4-345
5-345
5-310
60-330
6-30
4-28
2-28
4-20
0-16
1 19
0-11
0 7
22U; 3H
13U; 3H
18U; 3H; 2W
9U; 2H; 2W
10
147
10-320
4-17
05
3U; 3H; 4W
The site vegetation types are those defined within the British National Vegetation Classification (Rodwell, 1991a,b, 1992): U, upland grassland:
H, heaths; W, woodland; CG, calcareous grassland; MG, mesotrophic grassland.
The sites were selected solely on the basis that they had all
been sprayed once with asulam in a known year. The use of
a large number of sites surmounts some of the criticisms of
the chronosequence methodology. A summary of the site
geographic distribution, along with ranges of environmental factors and vegetation types are shown in Table 4.
These data have been analysed using constrained ordinations (ter Braak and Smilauer, 1998) in two ways, firstly
using the entire dataset, and second where the vegetation
was partitioned into four upland communities: (1) acidic
lowland woodland; (2) Agrostis/Festuca/Pteridiumcommunity; (3) moorland grass; and (4) montane heather moorland (Bunce et al., 1999). Previous analyses indicated that
this classification system was more appropriate than the
National Vegetation Classification (NVC) for these data.
The first analysis showed that geographic location
affects the response; easting, northing and distance from
the sea (the latter being a surrogate measure for oceanicity)
were important variables controlling vegetation succession.
When easting and northing were factored out as covariables, distance from the sea, non-bracken litter,
altitude, animal excrement (cover estimate of excreta of all
grazing animals at the time of survey used as an extremely
simple surrogate measure for grazing intensity), time and
bracken litter were significant (Table 5). When soil factors
were also included extractable P, pH, and exchangeable concentrations of Ca and Mg were also important (Table 5).
The four community types indicate that there is a
reasonable range of endpoint communities being established over the UK. Thus asulam use in one situation may
give a different response from the same treatment in
another. The subsets of data based on Bunce et al.'s
(1999) classification were then used in a HOF analysis
(Huisman, Olff and Fresco, 1993); this modelling approach
relates species response along the vectors of the environmental variables detected in the constrained ordination.
Examples of species responses of the montane heather
moorland class of Bunce et al. to two environmental
5. Results of the constrained ordinations of the
chronosequence data indicating those environmental variables
that explained most of the variation in the dataset
TABLE
Axis
Eigenvalue
Significant environmental variables
A
Analysis I: using all environmental variables except soil
1
0.33
Easting, northing, plant litter
2
0.29
Northing, distance from sea, easting
3
0-28
Animal excrement, distance from sea, plant litter
4
0-13
Altitude, distance from sea, aspect
Analysis 11: as Analysis I but with northing and easting as covariables
1
0.19
Distance from sea, plant litter, altitude
2
0.13
Altitude, animal excrement, elapsed time since
spraying
3
0-11
Plant litter, elapsed time since spraying, altitude
4
0.09
Distance from sea, animal excrement, bracken
litter recovery
Analysis III: as Analysis I, including soils analyses but with northing
and easting as covariables
1
0.33
Extractable P, soil pH, elapsed time since spraying
2
0-30
Soil pH, extractable P, exchangeable Ca
3
0.26
Exchangeable Ca, bare ground, extractable P
4
0.22
Distance from sea, bare ground, exchangeable Mg
B
Montane heather moorland
1
2
3
0.29
0.23
0-22
4
0.18
Distance from sea, altitude, northing
Northing, easting, elapsed time since spraying
Surface water, distance from sea, elapsed time since
spraying
Plant litter, altitude, elapsed time since spraying
Agrostis/Festuca/Pteridium community
1
0.33
Surface water, northing, distance from sea
2
0-26
Northing, distance from sea, altitude
3
0-22
Plant litter, northing
4
0.16
Distance from sea, casting, northing
A, All data, but analysed with different sets of explanatory variables;
B, only those sites classified as montane heather moorland and
Agrostis/Festuca/Pteridiumcommunity (Bunce et al., 1999).
Marrs et al.--Ecology of Bracken
variables are shown (Fig. 6). Essentially development of
vegetation cover after bracken spraying depends on many
interacting variables, and the response to each may be
complex (Fig. 6).
11
A
J~
Multivariate models to judge success
We have already described the multivariate modelling
developed by Mitchell et al. (1997) for assessing the
successional status of a range of late-successional vegetation, including bracken on Dorset heaths. We have
extended the use of this approach to assessing the success of
management studies to reverse succession. The rationale
behind this approach is first to develop a successional
framework within a successional sequence (Fig. 1), and then
to view the late-successional site as the 'start point' and the
early-successional site as the 'target'. Various scenarios are
possible when late-successional sites are managed. The
managed vegetation at the 'start point' could remain where
it was (resistance is high), it could move direct to the 'target'
and stay there (resistance is low and resilience is low), and it
could move to the 'target' and then recover quickly to the
'start point' (resistance is low and resilience is high).
Alternatively, the vegetation could move off in a completely
different trajectory as a result of invasion of new species.
Mitchell et al. (1999) document a range of other
possibilities.
The use of this modelling approach has been tested for
bracken sites in Dorset. Of the eight heathland sites used to
derive the original model, bracken has been controlled on
four of them, although at one site in two separate areas.
The bracken had been controlled by applying asulam,
sometimes in conjunction with cutting, and at one site the
litter had been bulldozed clear. The vegetation that
developed on these treated sites was surveyed, and the
data incorporated into the multivariate model (Mitchell
et al., 1999). The resulting plot for the bracken (Fig. 7)
showed that there has been some success in that most sites
moved some way towards the 'target', but they have not
moved very far, and are now tending to move away from
the target. Two indices of success were derived from the
model: (1) the distance between the treated site and the
'target'; and (2) an index derived using Euclidean geometry
to indicate the displacement of the site from the ideal linear
trajectory between 'start' and 'target'. When comparing the
bracken sites with other late-successional communities
(Table 6), it is clear that some bracken communities are
relatively resistant to change compared to other latesuccessional communities, because they have not moved
very far from the start positions and do not achieve their
target. Moreover, they also tend to move the furthest away
from the straight-line trajectory.
This approach is still in its infancy. In order to be
successful as a monitoring tool the survey of the managed
sites needs to be repeated several times to give accurate
measurements of ecosystem resistance and resilience. This
has not yet been done; however, even at this stage it has
provided useful comparative assessments on the status of
bracken-dominated communities with respect to management success.
0
0
Distance from the sea (kmin)
B
or
45
40
35
.
30
25
g
20
15
10
5
0
50
100
150
200 250 300 350 400 450
Altitude (m asl)
FIG. 6. The response of a range of species after asulam treatment of
the CVS montane heather moorland vegetation type (Bunce et al.,
1999) to two environmental variables: distance from the sea (A), and
altitude (B). Response curve developed from a combination of CCA
modelling and the fitting of a suite of response surfaces (Huisman,
et a., 1993).
MANAGEMENT TOWARDS LATESUCCESSIONAL COMMUNITIES
There is no doubt that a dense bracken cover reduces tree
colonization and performance under certain circumstances,
but once saplings are established there appears to be
ambiguity as to the effect of bracken on survivorship. In
forestry it is accepted that vigorous bracken can kill trees
(Biggin, 1982), however, the same author suggests that 'it is
not always necessary to weed, i.e. reduce the bracken
infestation'. In many situations, the forester accepts that the
bracken will check growth for some time, but once the trees
overtop the bracken they will start shading the bracken and
eventually grow well. In other situations, where the bracken
has been reduced successfully by pre-planting herbicide,
significant increases in tree volume were found (Dutkowski
and Boomsma, 1990). These authors recommended preplanting sprays rather than post-planting sprays to achieve
a reduction in bracken, primarily to achieve good bracken
control before the trees were established, but also because
there was the ability to use appropriate surfactants, which
might damage establishing trees. Another method for
reducing bracken infestation to assist tree establishment is
12
Marrs et al.--Ecology of Bracken
A
2
4az
.5
-a
0
Year
B
800
-1
600
,n
W400
-2
200
= 200
0
Q
-1
0
1
2
Axis 1
FIG. 7. A simplified canonical ordination diagram (CCA) using both
vegetation and soils data (Mitchell et al., 1999), showing the response
of bracken-dominated sites (START) after management towards a
lowland heath (TARGET). The TARGET and START positions are
shown as the mean centroids of all sites with s.e. bars, the managed
sites are shown as individual sites (after Mitchell et al., 1999).
to apply the non-selective herbicide dicamba in concentrated strips between the tree planting lines; this approach
reduces the competition from bracken, especially for light,
and allows the trees to grow better (Palmer, 1988).
We assessed the effects of various treatments to reduce
bracken vigour on the establishment of oak seedlings within
a natural oak woodland at Blaen Nanmor, within the
Snowdonia National Park (Paterson, 1996). The saplings
were transplanted in 1992 with the aim of regenerating the
woodland; tree shelters 0-6 m tall were used to protect the
saplings. Starting in August 1993, four bracken control
treatments were applied to two replicated plots, the
treatments were: (1) untreated 'control'; (2) bracken fronds
cut once yearly; (3) bracken fronds cut twice yearly; and (4)
a single application of asulam in early August 1993. The
bracken heights in August between 1993 and 1995 are
shown (Fig. 8A); cutting twice yearly and asulam use
reduced the bracken height below that of the tree shelters,
and cutting once yearly had an intermediate effect, with
similar effects on frond biomass in 1995 (Fig. 8B). No
significant increases in sapling height were found between
bracken control treatments in this short study, although
oaks growing on plots where the bracken had been cut were
Treatment
C
200
0
150
a 100
a
n
v
Treatment
FIG. 8. Effects of bracken control treatments on frond height between
1993 and 1995 in relation to tree shelter height (A), frond biomass in
1995 (B) and oak leaf number in August 1995 in an experiment to
assess impact of bracken control on oak sapling performance at Blaen
Nanmor, Snowdonia (C). Bars with the same letter are not significantly
different; LSD = 296 g m-2 ; P < 005. U, Untreated; Cl, cut once
yearly; C2, cut twice yearly; Al, asulam once (after Paterson, 1996); ts,
tree shelter height.
consistently taller. However, there was an increase in
sapling vigour where bracken was controlled. By 1995,
3 years after planting, the trees in cut plots had at least three
times the number of leaves compared to untreated plots.
The oaks in asulam-treated plots were intermediate
(Fig. 8C). These findings were similar to those of Humphrey
and Swaine (1997), who showed that where bracken fronds
13
Marrs et al.--Ecology of Bracken
6. Distances in four dimensions of managed sites or areas within sites from heath (target, T) and successional
(start, S) sites and of start site from target (distances calculated from CCA analysis II, managed sites treated as
passive samples)
TABLE
Distance of managed site
from
TargetT
Starts
Distance of
start from
target
Sopley & Ramsdown
Trigon
AHCP
Merritown
7.32
5.28
5.93
1.96
8.11
1.07
1.23
241
5.96
5.52
6.15
3.67
PS
Grange
Arne (d)
E. Holton (a)
AHCP (a)
E. Holton (b)
Merritown
Sopley & Ramsdown
Blackhill
Arne (a)
Arne (b)
Arne (c)
AHCP (b)
Trigon
Arne (e)
3.87
2.91
2.79
2.64
3.67
2.46
3.46
3.24
1.71
4.31
3.49
3.08
2-36
4.62
3.00
4.29
3.77
2.28
1.76
3.16
3.79
2.91
4-67
6-52
5.00
2.53
3.96
7.45
PA
Cranborne
Blackhill (a)
Blackhill (b)
Trigon
Arne
5.19
7.12
7.96
3-26
2-65
Arne
Sopley & Ramsdown (a)
Trigon
Blackhill
Sopley & Ramsdown (b)
3.62
3.63
3.68
2.61
3-70
Stage
Area
B
R
Ranking, closest to heath
Ranking, closest to
straight line
Within stage
Overall
9.47
0.84
1.05
0.70
4
2
3
1
27
24
25
2
4
2
3
1
4.00
4.99
4.33
4.57
4.32
3.89
4.65
4.28
4.99
4.99
4.99
4.57
3.63
4.99
2-87
2-22
2.23
0.35
1.09
1.74
2.60
1.87
1.40
5.92
3.51
1.04
2.69
7-09
12
6
5
4
11
3
9
8
1
13
10
7
2
14
20
9
8
6
17
4
13
11
1
21
14
9
3
22
11
7
8
1
3
6
9
5
4
13
12
2
10
14
2.29
4.67
5.79
1.58
2.58
4.53
3.68
3.68
4.16
5.14
2.95
8.10
1007
0.68
0.10
3
4
5
2
1
23
26
28
12
7
3
4
5
2
1
4.86
2.28
2.17
2.03
2.31
3.53
3.39
2-88
2.93
3-39
4.95
2.53
2.97
1.7
2.62
2
3
4
1
5
15
16
18
5
19
5
2
4
1
3
A value*
Within stage
Overall
27
4
6
3
19
12
13
2
7
10
15
11
9
24
22
5
17=
25
t 20
26
28
17=
1
23
14
21
8
15
*A measure of whether this trajectory (start to managed to target) is a straight line is provided by the A value which is calculated as (distance
from managed site to target) + (distance from managed site to start) - (distance from start to target); the closer this value is to zero the closer the
trajectory is to a straight line. The managed sites are ranked by distance from the heath target and by how close they are to a straight line
trajectory.
were cut continuously or over the winter there was a marked
increase in total seedling biomass, net total leaf area and a
decrease in root: shoot ratio. The most striking results were
an increase in total seedling biomass from 079 g in
untreated plots, to 1.12 g where fronds were removed over
winter, and to 3.52g when fronds were continuously
removed; results for total leaf area are 59, 95 and
227 cm 2 . Thus, it appears that the reduction in bracken
fronds increases the photosynthetically available radiation
reaching the seedlings, reduces competition and allows the
seedlings to increase their leaf area, biomass and hence
hopefully their long-term performance.
Thus, there appears to be some threshold of bracken
vigour above which tree mortality is high and saplings do
not thrive. However, below this threshold bracken reduces
tree performance, and any reduction in bracken improves
tree growth. Unfortunately, this threshold has not been
identified yet. Where bracken has a variable effect on tree
establishment it is worth speculating whether it is worth
the effort of treating the bracken if some of the trees
will eventually survive and mature. In Australian forestry
trials, Dutkowski and Boomsma (1990) showed that it was
economical to control bracken post-planting as site quality
increased and the annual rate of return was estimated to be
at least 10%, sufficient to justify the cost of bracken control.
However, where trees are being planted for non-economic
reasons, for example to improve or maintain the landscape,
then it may not be possible to justify the costs of control, it
may be more cost-effective to accept increased mortality,
poorer growth and a slower woodland development.
There is a paucity of research on the effects of bracken on
woodland development; this is unfortunate because in
many situations in upland Britain a woodland ecosystem
may be the most appropriate sustainable land use given
Biodiversity Action Plan targets.
OUTLOOK
Bracken is an unusual fern and it plays a major ecological
role in many biotypes. Synthesis of evidence suggests that
it is a mid-successional plant that usually occupies a
niche between plagio-climax heaths/moors/grasslands and
woodland. This was confirmed by multivariate analyses of
soil and vegetation and seedbanks in lowland heaths.
14
Marrs et al.-Ecology of Bracken
However, bracken can also persist for long periods,
probably because of the direct competitive effects it has
on regenerating trees, although this may be enhanced by
allelopathy, herbivory from grazers and dispersal processes
of the trees. Different responses occur in different localities
and a model has been put forward which accounts for at
least some of the reported successional relationships
between bracken and other successional stages.
Reversal of succession is possible given appropriate
management; however, it is difficult to eradicate bracken
and the resulting community may not be the one that is
desired. Trajectories through time may be complicated by a
range of processes in complex interactions the processes
may include management, site characteristics, soils, and
climate, and all of these may change through time.
The path of least resistance in terms of management
outcomes may be to accelerate the succession towards
woodland. Woodland is a suitable target in many areas of
upland Britain, and it may be the most cost-effective.
ACKNOWLEDGEMENTS
We thank the former Nature Conservancy Council, Nuclear
Power plc, the former Department of the Environment, the
Institute of Terrestrial Ecology, the University of Liverpool,
the Royal Society for the Protection of Birds and the
Ministry of Agriculture, Fisheries and Food for financial
support over the last 20 years. The senior author thanks
present and former colleagues at the University of
Liverpool including the late Dr A. S. Watt FRS, Dr M.
Auld, the late Sue Bdrtsch, Dr A. Britton, Mr R. BrandHardy, Dr C. Evans, Mr S. Johnson, Mr J. Lowday,
Dr A. L. Milligan, Dr K. M. Owen, Dr C. S. R. Snow and
Dr T. Parr for their contributions to the bracken and
succession research programme.
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