Shrubland Restoration cesses.

Shallow and deep topsoil treatments yielded

high plant density, richness, and projected canopy cover,
but canopy cover was higher in deep topsoil plots

Following Woody Alien throughout the trial. Fertilizer addition increased can-
opy cover in untopsoiled and shallow topsoil plots via
an increase in alien annual species. Fertilizer addition
Invasion and Mining: ultimately may lead to increased native vegetation
cover in untopsoiled areas, but as it increased proteoid

Effects of Topsoil Depth, mortality on deep topsoil plots, it is not recommended

for sites where topsoil is available. A species-rich and
structurally representative fynbos community may be

Seed Source, and restored on topsoiled areas provided that the native
disturbance regime is simulated and seeds of major
structural guilds not present in the soil seed bank are
Fertilizer Addition included in the seed mix.

Key words: invasive alien plants, soil disturbance, soil-

Patricia M. Holmes1,2 stored seed banks, fynbos vegetation, seedling recruit-
ment, establishment and growth.

Abstract

Invasion by woody alien plants, construction, and

Introduction
mining operations are among the major disturbances
degrading vegetation in the Cape Floristic Kingdom,
South Africa. The aim of this study was to assess
whether native fynbos shrubland vegetation could be
T he Cape Floristic Kingdom of South Africa boasts
among the world’s highest concentrations of plant
species, of which about 80% are endemic (Cowling et al.
restored following dense alien invasion and distur-
1996, 1997). Fynbos vegetation is a major component of
bance by mining. An area supporting dense alien
the Cape Floristic Kingdom (Rebelo 1996) and occurs on
trees was cleared and topsoil was stripped and stock-
nutrient-poor substrata from the mediterranean-climate
piled to simulate mining disturbance. A field trial in-
west to the aseasonal temperate east.
vestigated the effects of topsoil depth, seed mix appli-
Remaining fynbos vegetation has been degraded by
cation, and fertilizer on native species recruitment
factors such as alien plant invasion, habitat fragmenta-
and vegetation development over a three-year period.
tion resulting from agricultural and urban develop-
Soil-stored seed banks contributed 60% of the species
ment, and inappropriate management practices (Rebelo
recruited, indicating that areas invaded for three de-
1992a, 1992b). In addition, disturbances of shorter dura-
cades have good restoration potential. The addition of
tion such as construction and mining activities have de-
a fynbos seed mix, which included serotinous over-
graded fynbos vegetation (Romoff 1986; Levitt 1997). In
story species, improved both the richness and struc-
the mountains, invasive alien trees and shrubs domi-
tural composition of the vegetation. Most species sown
nate thousands of hectares of natural vegetation, signif-
in untopsoiled plots established, but survival and
icantly altering communities and reducing diversity
growth was low compared to topsoil plots. Poor growth
and water run-off (Richardson et al. 1992; Le Maitre et
in combination with a lack of soil seed bank species,
al. 1996). At least 26% of natural vegetation in the
indicate that restoring a diverse and functional cover
mountains has been invaded at some stage (Richardson
of indigenous vegetation on subsoil is not possible in
et al. 1997). The realization that woody alien vegetation
the short-term. Soil amelioration is required to im-
uses more water than indigenous vegetation led to the
prove rooting conditions and initiate ecosystem pro-
initiation in 1995 of a multi-million dollar government
program to control invasive plants in catchment areas
(van Wilgen et al. 1997). The ultimate success of this
1 Institute for Plant Conservation, University of Cape Town,
program depends on a sustainable cover of fynbos veg-
Private Bag, Rondebosch 7700, South Africa
2 Address correspondence to P. M. Holmes, 23 Dreyersdal
etation being restored following alien clearing.
In the lowlands, a large proportion of the vegetation
Road, Bergvliet, 7945, Cape Province, South Africa, email
prebelo@mweb.co.za already has been transformed. Remaining vegetation
continues to be threatened as a result of increasing hu-
© 2001 Society for Ecological Restoration man pressures on the land: directly by agricultural and

MARCH 2001 Restoration Ecology Vol. 9 No. 1, pp. 71–84 71

Shrubland Restoration Following Alien Invasion and Mining
urban expansion and alien plant invasions, and indi-
rectly by habitat fragmentation and inappropriate man-
agement (Wood et al. 1994).
There is an increasing awareness of the need to re-
store vegetation that has already been degraded and to
lessen the impact of future developments (Anonymous
1997). Although little restoration research has been
done in fynbos, the recruitment dynamics, community
ecology, and functional ecology of fynbos have been
relatively well studied (Cowling 1992) and based on
this, protocols for restoration have been outlined
(Holmes & Richardson 1999). For example, it is known
that many fynbos species have long-lived propagules
stored in the soil, which can survive moderate-to-long
alien plant invasions (Holmes & Cowling 1997a, 1997b).
Germination of soil-stored fynbos species may be stim-
ulated by direct and indirect fire-related cues (e.g., heat
pulse, smoke compounds, and post-fire diurnal temper-
ature regime; Keeley & Bond 1997). Thus, if appropriate
germination cues are applied, persistent seed banks
may be used to assist in restoring native vegetation.
A proposal to mine kaolin near the boundary of the
Cape Peninsula National Park (an area of international
conservation importance; Trinder-Smith et al. 1996)
precipitated the need to investigate optimal methods
for restoring native vegetation following opencast min-
ing. In the past, alien grasses had been used to rehabili-
tate mined areas. As the proposed mine site supported
dense alien vegetation (predominantly Pinus pinas-
ter[cluster pine]) it provided a testing ground for resto-
ration, both following alien clearing and disturbance by
mining operations. Mining was simulated by stripping,
stockpiling, and respreading topsoil. Findings from this
study will assist in forming guidelines for the restora-
tion of mountain catchment areas following the clearing
of dense stands of alien trees, as well as for the restora-
tion of fynbos areas following disturbance by mining
and construction activities.
In view of the possibility of topsoil being unavailable
or in short supply following mining, a secondary aim
was to compare restoration without topsoil as well as
with two different topsoil depths. One of the aims of
revegetation following mining is to provide quick plant
cover to control soil erosion and create an aesthetically
pleasing landscape. Toward this end, different seed
mixes and a fertilizer treatment were tested for their ef-
ficiency in providing indigenous cover and diversity on
the various substrata.
The following key questions were addressed:
(1) Can fynbos be restored on untopsoiled substrata?
(2) Is topsoil depth an important factor in fynbos resto-
ration?
(3) Which seed mix application best restores Proteoid
Fynbos on the different substrata?
72
(4) Does the addition of fertilizer promote establish-
ment of fynbos vegetation?
Methods
Study Site
The restoration trial was set up on unmined land at the
Serina Kaolin Pty. Ltd. mine site at Noordhoek, on the
Cape Peninsula, South Africa (34⬚05⬘40⬙S 18⬚22⬘20⬙E).
The vegetation at the site originally was Proteoid Fyn-
bos (shrubland comprising ⬎10% non-sprouting pro-
teoid cover; Cowling & Holmes 1992), but was planted
to Pinus pinaster during the late 1950s (Jeremy Wiley per-
sonal communication, and aerial photographs). Planting
is a process analogous to invasion as young trees are
planted into burnt or young fynbos vegetation. The dense
alien overstory was dominated by P. pinaster, with occa-
sional individuals of Eucalyptus diversicolor (karri) present.
The understory comprised scattered Acacia saligna (Port
Jackson willow), A. cyclops (red eye), Hakea drupacea
(sweet hakea), and H. sericea (silky hakea) (all invasive
alien species) and was devoid of indigenous species. A
few indigenous species survived in gaps alongside ve-
hicle tracks. The site is situated on a gentle east-facing
slope. The topsoil is brown sandy loam, derived from
Table Mountain Sandstone colluvial material, which
overlies heavier subsoil with granite-derived clay be-
neath. Although these clay subsoils have a limited dis-
tribution, sandy loam topsoils are fairly common on
lower mountain slopes in the western Cape and often
support dense alien stands. The climate is Mediterra-
nean, with hot, dry summers and cool, wet winters. An-
nual rainfall was 670 mm during the first year of the
trial.
Seed Collecting
In January 1995, fynbos seed was collected from indige-
nous vegetation within a five-kilometer radius of the
trial site. This ensured that any introduced seed would
be of local origin. Seed was handpicked from plants
(predominantly the canopy-storage species, e.g., Protea
lepidocarpodendron [black-beard sugarbush] and Leuca-
dendron xanthoconus [sickle-leaf conebush) [Proteaceae])
and suction-harvested from under bushes and in the lit-
ter layer where the smaller-seeded species drop their
seed. The species composition of the suction-harvested
component was not directly assessed. The seed was
sun-dried for a week to release seeds from serotinous
cones; and then sorted into paper bags ready for the
trial. The insecticide Karbadust (Efekto, Silverton, South
Africa) was sprinkled into the bags to kill potential seed-
eating insects. Bags were stored in a cold room (4⬚C) in
order to minimize loss of viability until required for the
Restoration Ecology MARCH 2001

trial. One day before sowing, the suction-harvested
seed mix was given a smoke treatment to enhance ger-
mination response (Brown 1993).
Portions of the hand-collected seed and the suction-
harvested seed were combined to give the fynbos mix
(F) used in the trial. For the fynbos annual (FA) supple-
ment, fynbos seed harvested from a firebreak area was
added to F. Firebreak areas support more short-lived
species and should yield more annual and short-lived
perennial seeds than the mature veld. For the fynbos
commercial (FC) supplement, the commercially avail-
able indigenous seed of Cynodon dactylon (Bermuda
grass, Poaceae), Pelargonium capitatum and Geranium in-
canum (both sprawling perennial forbs, Geraniaceae)
were purchased and added to F. Cynodon was sown at a
rate of 300 seeds/m2 (half the recommended rate for
pastures), and Pelargonium and Geranium each at two
seeds/m2.
Experimental Design
The three main factors accommodated within the exper-
imental design were topsoil depth, seed treatment and
fertilizer. Substratum strips were prepared for the dif-
ferent topsoil treatments and the other factors were
nested within these. Topsoil depth treatments were un-
topsoiled (0 mm), shallow (100 mm), and deep (300
mm). Seed treatments were control (con: no seed
added), fynbos mix (F), fynbos plus annual supplement
(FA), and fynbos plus commercial supplement (FC).
Fertilizer was applied at one concentration level only,
and was applied to half of the seed treatment plots, ex-
cluding the seed control plots. The four different seed-
ing treatments and the fertilizer treatment were allo-
cated to the plots at random (total number of plots 105,
five replicates for each seed/fertilizer/topsoil treat-
ment).
Site Preparation
At the end of summer (March 1995) a 0.2 ha area of
dense alien vegetation was cleared for the trial. The
alien trees were felled, logs removed, and finer branches
chipped for use as mulch. Roots and stumps were bull-
dozed out of the soil and then the topsoil was stripped
and stockpiled to simulate disturbance by mining. Top-
soil was stockpiled until the site was cleared (a maxi-
mum of seven days). Substratum strips (4 m wide and
between 16 and 36 m long) were established downslope
in a west-to-east orientation on the cleared site. Untop-
soiled strips comprised the heavier subsoil layer (to
simulate the clay overburden substratum); shallow top-
soil blocks had 100 mm of the topsoil reapplied; and
deep topsoil blocks had 300 mm of the topsoil re-applied.
MARCH 2001 Restoration Ecology
Shrubland Restoration Following Alien Invasion and Mining
Sixteen meter square (4⫻4) plots were demarcated us-
ing logs pegged across the slopes, so one plot took up
the entire width of each substratum strip, and between
four and nine plots fitted along the length of each strip.
Logs also helped to stabilize the soil against surface
wash.
Seed was applied (12–13 April 1995) by broadcasting
over the entire plot, as evenly as possible. A thin layer
of wood-chip mulch (3–6 cm thick) was applied imme-
diately over this to prevent the seed from blowing away
and to ensure good contact between soil and seed. The
first application of fertilizer was done on 25 August
1995 following seed germination. Owing to the known
sensitivity of fynbos species to fertilizer addition, espe-
cially phosphorus (Witkowski 1991), a 0.5% solution of
the fish emulsion Seagro (Seagro, Cape Town, South
Africa) was used in the first year of establishment at a
rate of 1.2 L/m2. Undiluted Seagro contains 5.5% N,
0.75% P, and 1.6% K and trace elements. On 15 April
1996, the ultra-slow-release fertilizer Horticote 7:1:2 (27)
(Ocean Agriculture, Johannesburg, South Africa) was
applied at a low rate of 100g per m2 (100 g yields 18 g N,
2.6 g P, 6.6 g K, 1.2 g Mg, and small amounts of Fe, Mn,
Zn, Cu, B, and Mo). This ensured slow release of nutri-
ents over a 9–12 month period.
Monitoring
Five separate censuses of seedling recruitment were
done 3, 6, 12, 18, and 36 months following sowing. In
each of the 105 plots, four 1 m2 permanent quadrats
were positioned, two on each side of a transect bisecting
the plots, alternately above and below the transect.
Counts of all individuals in each growth-form guild
were made at the 3-, 6-, 12-, and 18-month censuses. At
the 18-month census, the numbers of species represent-
ing each growth-form guild and the numbers of alien
plants, were also recorded. Estimates of total projected
plant cover were recorded for each quadrat at each of
the censuses.
At 36 months, projected plant cover for each species
was estimated for the entire plot, and species richness
was recorded in one single 1 m2 quadrat placed at the
center of each plot. All species that flowered during the
trial were collected and identified.
In February 1997, ten months after the application of
the ultra-slow-release fertilizer, samples were taken
from fertilized and unfertilized plots in each topsoil
depth treatment (five replicates each), as well as three
samples from the adjacent undisturbed soil under
pines. Samples were analyzed for pH, resistance, and
nutrient concentrations, using standard techniques of
the Soil Science Division (Department of Agriculture:
Western Cape, Private Bag X1, Elsenburg 7607, South
Africa).
73
Shrubland Restoration Following Alien Invasion and Mining

Alien Plant Control

In September 1994, the biocontrol fungus (Uromycla-

dium tepperianum) was inoculated onto alien Acacia sali-
gna in the vicinity of the restoration trial site. This fun-
gus has been shown to weaken plants and reduce their
reproductive output (Morris 1999). Weeding of alien in-
vasive trees and shrubs recruiting from the soil seed
banks (Acacia species) and the seed rain (Pinus, Eucalyp-
tus and Hakea species) was done in January 1996, to pre-
vent these species from outgrowing and shading the
fynbos species. Alien seedlings were uprooted where
damage to indigenous species could be avoided; other-
wise, they were cut below ground level with secateurs
to prevent resprouting. Following this major weeding
intervention, very little follow-up control was required.

Data Analysis

Two-way analysis of variance (ANOVA; BMDP Pro-

gram 2V, Dixon 1992) was used to investigate the main
treatment effects and the interactions between depth
and seed, and depth and fertilizer treatments at various
stages in the development of the vegetation. Earlier
analyses indicated that the blocking factor (substratum
strip) influenced the variance less than the experimental
factors, and it was excluded to simplify the analyses.
Cover values and counts of plant density were square-
root-transformed to satisfy ANOVA homogeneity of
variance requirements.
Guild structure (by plant cover) in three-year-old
vegetation was investigated using contingency tables
(BMDP Program 4F, Dixon 1992). The null hypothesis
of independence between guild structure and topsoil
and seeding treatments was tested by chi-square. Ad-
justed standardized deviates (Haberman 1973) exceed-
ing 3.0 in absolute value were taken to indicate cells
with unusually large deviations from the expected. In-
digenous species were assigned to growth form, leaf
size, seed dispersal, seed storage, regeneration, and pol-
lination classes following Holmes & Cowling (1997a).

Figure 1. Indigenous plant density during the restoration trial

Results
Recruitment Pattern and Development of Plant Cover
Two-thirds of seedling recruitment occurred during the
first three months after sowing, and highest densities
were recorded at six months, when both perennial and
ephemeral (annual and geophyte) species were present
(Fig. 1). Plant density decreased over the first summer
as ephemerals died back and some perennial mortality
occurred. Mortality was most pronounced on untop-
soiled plots (Fig. 1). During the second winter there was
following different non-fertilized seeding treatments: (a) un-
topsoiled, (b) shallow topsoil, (c) deep topsoil (n ⫽ 20). No
seed addition (con), fynbos mix (F), F plus annuals (FA), F
plus commercial seed (FC).
a slight rise in plant density owing to the renewed ap-
pearance of some ephemerals.
In topsoil plots, plant cover developed rapidly over
the first 18 months (Fig. 2). By three years, dense vege-
tation (90% projected canopy cover) had developed on
deep topsoil plots and moderately dense vegetation

74 Restoration Ecology MARCH 2001

 Shrubland Restoration Following Alien Invasion and Mining

(Fig. 2). Within each topsoil depth, positive correlations

between plant cover and density were all highly signifi-
cant (r ⬎ 0.33, p ⬍ 0.001).

Effect of Topsoil Depth on Plant Density and Cover

The ANOVAs run for the different censuses yielded

similar results; those for the 18-month census are pre-
sented (Table 1). Most of the variance attributed to the
topsoil depth factor is associated with the untopsoiled
treatment. Plots without topsoil had significantly lower
indigenous plant density and cover, and lower alien
plant density, compared to topsoil plots across all seed
and fertilizer treatments (Figs. 1–4).
Differences between the shallow (100 mm) and deep
(300 mm) topsoil treatments took longer to develop.
There were few differences at six months, but by 18
months density was higher in most of the shallow top-
soil plots (Fig. 1). Plant cover without fertilizer addition
was higher in deep than in shallow topsoil plots by 18
months, and this difference increased after three years
(Fig. 2).

Effect of Seed Treatments on Plant Density and Cover

The addition of seed significantly increased both plant

density and cover over the unseeded controls (Table 1;
Figs. 1 & 2). Without seed addition, there was virtually
no plant recruitment in untopsoiled plots. In topsoil
plots, the soil seed bank contributed one-third of the
seedlings during the main recruitment phase of the first
winter (Fig. 1). In topsoil plots at three years, differ-
ences in plant density between control and seed mix

Table 1. Results of ANOVAs for indigenous plant density,

projected canopy cover, and herbaceous alien density, 18
months after sowing.
Indigenous Density Canopy Cover Alien Density
Source df F F F
Figure 2. Projected plant canopy cover during the restoration
trial following different non-fertilized seeding treatments: (a) Experimental factors topsoil depth (depth) and sowing
untopsoiled, (b) shallow topsoil, (c) deep topsoil (n ⫽ 20, ex- treatment (seed)
cept for 36 months, where n ⫽ 5). No seed addition (con), fyn- Depth 2 236.4*** 754.4*** 49.4***
Seed 3 54.0*** 44.1*** 15.1***
bos mix (F), F plus annuals (FA), F plus commercial seed (FC).
Depth ⫻ seed 6 4.5*** 0.8ns 3.0**
Error 408
Experimental factors topsoil depth (depth) and fertilizer
(fert)
Depth 2 157.2*** 818.5*** 40.4***
(75% projected canopy cover) on shallow topsoil plots. Fert. 1 0.1ns 94.8*** 65.5***
Depth ⫻ fert. 2 1.1ns 40.8*** 2.8ns
However, on the sown untopsoiled plots, cover de-
Error 354
creased during the first summer owing to plant mortal-
ity, and remained relatively low (20%) after three years ns ⫽ not significant. *p ⬍ 0.05. **p ⬍ 0.01. ***p ⬍ 0.001.

MARCH 2001 Restoration Ecology 75

Shrubland Restoration Following Alien Invasion and Mining
Figure 3. Effect of fertilizer addition on (a) alien plant density
and (b) percentage projected canopy cover, at 18 months for
the different topsoil depths (n ⫽ 20). Fynbos mix (F), F plus
annuals (FA), F plus commercial seed (FC).
treatments were still evident, whereas differences in
cover were insignificant (Figs. 1 & 2).
Differences among the three seeded treatments were
relatively small. On shallow topsoil, the fynbos-plus-
annual seed mix performed better than the other two
seed mixes in the early stages of restoration, in terms
both of indigenous density and cover (Figs. 1 & 2).
However, there was little benefit in this treatment after
the first year. The grass Cynodon dactylon, which was
sown as part of the commercial seed mix, did not ger-
minate well, and its establishment was poor. The peren-
nial forbs, sown as part of the commercial seed mix,
contributed little to plant density or cover.
At the six-month census, seed treatment had no effect
on herbaceous alien density: 97% of seedlings derived
from the topsoil or seed rain. The significant effect of
seed treatment on alien density at 18 months (Table 1)
relates to an indirect effect on open space for recoloni-
zation by these aliens.
76
Figure 4. Effect of seed source on native growth-form distribu-
tion: (a) by plant density at the peak of recruitment (6 months;
n ⫽ 20), (b) by species richness at 18 months (n ⫽ 20), and (c)
by percentage projected canopy cover at 36 months (n ⫽ 5).
No seed addition (con), fynbos mix (F), F plus annuals (FA), F
plus commercial seed (FC).
Effect of Fertilizer Treatment on Plant Density, Cover, and
Soil Variables
Application of the ultra-slow-release fertilizer did not
alter indigenous plant density, but caused a large in-
crease in alien herbaceous plant density after the sec-
ond winter (Table 1; Fig. 3a). The relative increase in
alien density was highest in untopsoiled plots.
Fertilizer addition had no effect on plant cover in the
deep topsoil plots, but caused an increase in cover in
shallow topsoil and untopsoiled plots after the second
winter (Fig. 3b). Most of this increase could be attrib-
uted to an increase in herbaceous, predominantly alien,
plant recruitment.
Although signs of stress (red leaf coloration) and die-
back in proteoid shrubs were observed following the
ultra-slow-release fertilizer application, no negative
long-term impacts on total plant density or cover were
found. In deep topsoil plots, proteoid mortality was sig-
nificantly higher in fertilized plots (␹2 ⫽ 17.4, p ⬍ 0.0001),
but there was no such effect in the other two soil treat-
ments.
Fertilizer addition caused little change to soil nutrient
status and pH measured ten months after the ultra-
slow-release fertilizer application (Table 2). Resistance
decreased significantly in fertilized untopsoiled plots,
Restoration Ecology MARCH 2001
 Shrubland Restoration Following Alien Invasion and Mining

Table 2. Soil pH, resistance, and nutrient concentrations 10 months after fertilizer application in fertilized and unfertilized plots at
the restoration trial and in neighboring undisturbed soil under pines (mean ⫾ SD, n ⫽ 5, except for undisturbed soil n ⫽ 3). Units
are ohms (resistance), mg/kg (Na, P, K), me% (Ca, Mg), and % (C). Results of 1-way ANOVAs and post-tests for unfertilized soil
are presented.
ANOVA
Topsoil Undisturbed (Unfertilized Only)
Depth (Pines) 0 mm 0 mm 100 mm 100 mm 300 mm 300 mm F(3,17)
Fertilizer No No Yes No Yes No Yes Tukey-Kramer

pH 4.4 ⫾ 0.1 4.8 ⫾ 0.3 4.5 ⫾ 0.4 4.7 ⫾ 0.2 4.6 ⫾ 0.1 4.5 ⫾ 0.1 4.6 ⫾ 0.2 1.79ns
Resistance 1,840 ⫾ 125 1,986 ⫾ 838 882 ⫾ 203a 2,540 ⫾ 832 2,266 ⫾ 369 3,910 ⫾ 499 2,128 ⫾ 654 8.60** pines,0,
100 ⬍ 300
Na 78 ⫾ 19 72 ⫾ 28 86 ⫾ 15 67 ⫾ 30 44 ⫾ 10 33 ⫾ 4 36 ⫾ 12 3.46*
P 3.3 ⫾ 0.6 2.0 ⫾ 0.7 1.2 ⫾ 0.4 2.8 ⫾ 1.6 3.8 ⫾ 1.6 2.4 ⫾ 0.9 3.2 ⫾ 1.1 1.05ns
K 59 ⫾ 16 25 ⫾ 6 28 ⫾ 7 33 ⫾ 18 46 ⫾ 16 40 ⫾ 11 41 ⫾ 10 4.40* 0 ⬍ pines
Ca 4.4 ⫾ 1.6 0.7 ⫾ 0.2 0.7 ⫾ 0.1 3.0 ⫾ 0.6 2.7 ⫾ 0.7 3.1 ⫾ 0.8 2.4 ⫾ 0.8 14.6*** 0 ⬍ pines,
100,300
Mg 1.3 ⫾ 0.5 0.4 ⫾ 0.1 0.4 ⫾ 0.1 0.9 ⫾ 0.2 0.8 ⫾ 0.2 0.9 ⫾ 0.2 0.7 ⫾ 0.3 7.97*** 0 ⬍ pines,
100,300
C 2.2 ⫾ 0.4 0.4 ⫾ 0.1 0.5 ⫾ 0.1 1.6 ⫾ 0.8 2.0 ⫾ 0.5 1.8 ⫾ 0.7 2.1 ⫾ 0.4 6.57*** 0 ⬍ pines,
100,300
a Significantly different to unfertilized equivalent (p ⬍ 0.05, Welch’s approximate t-test); ns ⫽ not significant. *p ⬍ 0.05. **p ⬍ 0.01. *** p ⬍ 0.001.

but no significant changes were detected for any other
measured soil variable.
Soil variable comparisons between the unfertilized
plots and the undisturbed soil around the restoration site
(currently under pines) indicated significantly higher
resistance for deep topsoil samples, but no other differ-
ences. Subsoil from the untopsoiled plots was lower in
many essential plant nutrients (e.g., K, Ca, Mg) and carbon
than the undisturbed soil and topsoil plots (Table 2).
Effects of Treatments on Species Composition and Guild Structure
Species richness was significantly lower in untopsoiled
compared to topsoil plots across all seed treatments
(Table 3). Over the three-year monitoring period, an av-
erage of ten species colonized the unseeded, untop-
soiled plots, both from seed drift during the initial sow-
ing and localized dispersal of early-maturing species.
There was no significant difference in richness among
seeded, topsoil plots at quadrat (1 m2) or plot (16 m2)
scales (Table 3). Among topsoil plots, seed controls had
the lowest richness; on average, seed treatments con-
tributed an additional three species per 1 m2 or five spe-
cies per plot. Topsoil contributed a minimum 60%, and
the seed mix 15%, of all species recorded at the restora-
tion trial site (Table 4).
Vegetation structure differed between untopsoiled
and topsoil plots and between control and seeded treat-
ments. Density, richness, and cover of all growth forms
were lower for untopsoiled plots (Fig. 4). Proteoid
shrubs (with canopy-stored seeds) were virtually ab-
sent in control plots, as they do not recruit from soil

Table 3. Species richness at quadrat (1 m2) and plot (16 m2) scales in three-year old vegetation following
different topsoil and seeding treatments (mean ⫾ SD, n ⫽ 5); no seed addition (Control), fynbos mix (F), F
plus annuals (FA), F plus commercial seed (FC). Results of 1-way ANOVAs for seed treatments are
presented.
0 mm 100 mm 300 mm
Seed Treatment 1 m2 16 m2 1 m2 16 m2 1 m2 16 m2

Control 0.2 ⫾ 0.4a 10.2 ⫾ 3.6a 9.4 ⫾ 1.5a 25.8 ⫾ 4.7 9.2 ⫾ 2.4a 22.8 ⫾ 5.3
F 6.2 ⫾ 1.9b 16.6 ⫾ 2.9ab 13.4 ⫾ 1.3b 31.2 ⫾ 5.9 12.6 ⫾ 1.1ab 30.0 ⫾ 3.7
FA 6.0 ⫾ 1.4b 16.2 ⫾ 3.8ab 11.8 ⫾ 0.4ab 30.2 ⫾ 3.4 12.6 ⫾ 1.3ab 30.0 ⫾ 6.7
FC 6.2 ⫾ 1.3b 17.0 ⫾ 0.7ab 11.0 ⫾ 1.0ab 29.2 ⫾ 3.9 11.8 ⫾ 2.9ab 29.0 ⫾ 2.0
F ⫹ fertilizer 4.6 ⫾ 1.3b 16.6 ⫾ 4.3ab 12.8 ⫾ 1.1b 27.4 ⫾ 5.6 11.6 ⫾ 1.5ab 28.8 ⫾ 5.8
FA ⫹ fertilizer 6.6 ⫾ 2.9b 18.4 ⫾ 4.2b 13.0 ⫾ 1.9b 32.0 ⫾ 5.0 14.0 ⫾ 2.1b 30.0 ⫾ 4.8
FC ⫹ fertilizer 5.8 ⫾ 1.9b 16.6 ⫾ 4.8ab 13.8 ⫾ 2.6b 35.2 ⫾ 4.4 13.6 ⫾ 2.1b 27.8 ⫾ 4.2
F(6,28) 8.34*** 2.54* 5.05** 2.10ns 3.12* 1.41ns
ns ⫽ not significant. *p ⬍ 0.05. **p ⬍ 0.01. ***p ⬍ 0.00. Within columns different letter superscripts denote a significant difference (Tukey-

Kramer, p ⬍ 0.05).

MARCH 2001 Restoration Ecology 77

Shrubland Restoration Following Alien Invasion and Mining

Table 4. The number of indigenous species* recorded at the had a relatively low proportion of shrub (especially eri-
restoration trial site by growth form and propagule source. The coid) cover and a relatively high proportion of grami-
third column includes species deriving from both the soil and noid cover compared to deep topsoil plots. Species with
seed mix, and those species which could not be assigned with soil-stored seeds, especially ericoid shrubs and those
certainty to either source (mostly ephemeral species which had
dispersed by ants, were under-represented in untop-
died back before species counts were done in plots).
soiled plots. Short-lived seeder species with wind-dis-
Source Soil Seed Mix Both/Unknown Total persed seeds and insect-pollinated flowers typified the
Proteoid shrub 0 6 0 6 untopsoiled plots. Among seed treatments on topsoil
Ericoid shrub 24 5 5 34 plots, unseeded controls had a relatively low propor-
Other shrub 22 6 5 33 tion of graminoid cover and a relatively high propor-
Graminoid 20 2 8 30 tion of shrub (especially ericoid) cover. On topsoil plots,
Forb 4 2 17 23 the guild structure of unseeded controls was character-
Geophyte 15 0 1 16
Total 85 21 36 142 ized by an over-representation of species with soil-
stored seeds, particularly shrubs with ericoid leaves
* Species list available from author. and passive or ballistic seed dispersal.
Restored plant communities on seeded topsoil plots
resembled Proteoid Fynbos in general structure, with a
seed banks. In topsoil plots, richness was significantly well-developed proteoid shrub overstory layer and
lower for control than sown plots for all growth forms mixed ericoid shrub-graminoid understory layer at
except geophytes (Fig. 4; Table 5). Richness of growth- three years (Fig. 5).
forms did not differ among the different seeded treat-
ments (Table 5). Graminoid density (predominantly
Costs and Benefits of the Various Treatments
Poaceae and Cyperaceae) was higher in the fynbos-
plus-annual treatment in the untopsoiled and 100 mm The costs incurred in the restoration trial were extrapo-
topsoil plots (Table 5). By three years, geophytes and lated to give general estimates for different aspects of
forbs contributed insignificant cover (Fig. 4). the restoration program (Table 6). Costs of initial alien
Analysis of the different native guild components in- tree clearing were excluded, as this would be a prereq-
dicated significant differences among topsoil depth and uisite before any mining or vegetation restoration oper-
seed treatments for all the guilds tested (Appendix 1). ations. Earthmoving costs also were excluded, as this
Among topsoil depth treatments, shallow topsoil plots forms part of general mining operation costs.

Table 5. ANOVA and post-test results by growth-form guild for density (plants/m2) at 6 months, richness (species/m2) at 18
months, and projected canopy cover (%) at 36 months; no seed addition (Con), fynbos mix (F), F plus annuals (FA), F plus
commercial seed (FC).
Tukey-Kramer Tukey-Kramer Tukey-Kramer
Guild F (p ⬍ 0.05) F (p ⬍ 0.05) F (p ⬍ 0.05)

Density F(df: 3,79) 0 mm topsoil 100 mm topsoil 300 mm topsoil

Proteoid 38.2*** Con ⬍ F,FA,FC 60.9*** Con ⬍ F,FA,FC 53.5*** Con ⬍ F,FA,FC
Ericoid 16.5*** Con ⬍ F,FA,FC 5.9** Con ⬍ F 5.7** Con ⬍ FA,FC
Graminoid 20.8*** Con ⬍ F,FA,FC; F⬍FA; FC⬍FA 6.4*** Con ⬍ FA; F⬍FA 3.4* Con ⬍ FC
Forb 11.8*** Con ⬍ F,FA,FC 9.6*** Con ⬍ F,FA,FC 7.7*** Con ⬍ FA,FC
Geophyte 10.8*** Con ⬍ F,FC; FA⬍F,FC 2.4ns 1.2ns
Richness F(df: 3,79)
Proteoid 26.5*** Con ⬍ F,FA,FC 42.6*** Con ⬍ F,FA,FC 55.0*** Con ⬍ F,FA,FC
Ericoid 5.70** Con ⬍ FC 3.40* F ⬍ FA 3.4* Con ⬍ FA
Other shrub 3.36* Con ⬍ FC 2.74* 4.6** Con ⬍ FC
Graminoid 12.2*** Con ⬍ F,FA,FC; F⬍FA 5.19** Con,F ⬍ FA 4.6** Con ⬍ FA
Forb 9.9*** Con ⬍ F,FA,FC 13.4*** Con ⬍ F,FA,FC; F⬍FA 7.5*** Con ⬍ F,FA,FC
Geophyte 10.2*** Con ⬍ F,FA,FC 1.12ns 2.2ns
Cover F(df: 3,19)
Proteoid 2.76ns 5.04* Con ⬍ F,FA 7.73** Con ⬍ FA,FC
Ericoid 4.75* Con ⬍ F,FC 1.27ns 1.29ns
Other shrub 2.66ns 0.31ns 0.73ns
Graminoid 4.6* Con ⬍ FA,FC 0.66ns 1.54ns
Forb 0.92ns 0.18ns 0.94ns
ns ⫽ not significant. *p ⬍ 0.05. **p ⬍ 0.01. *** p ⬍ 0.001.

78 Restoration Ecology MARCH 2001

 Shrubland Restoration Following Alien Invasion and Mining

useful in accelerating restoration in untopsoiled areas,

via the promotion of herbaceous species and the initia-
tion of nutrient-cycling processes. Woody alien species
recruited well and would have formed a dense stand
overtopping the fynbos vegetation, had a follow-up
program not been implemented. Regular follow-up
control of woody alien species is therefore an essential
component of restoring fynbos vegetation.

Discussion

Despite the complete absence of fynbos vegetation be-

Figure 5. General view of the Noordhoek restoration trial site,
with three-year-old restored Proteoid Fynbos vegetation in
the foreground and alien invasive vegetation in the back-
ground (Pinus pinaster dominant).
By 1996 the fungus (Uromycladium tepperianum) was
widespread on Acacia saligna around the restoration site,
and by 1998 the infected plants were heavily galled. As a
result of the successful spread of this biocontrol agent,
the reproductive output of this alien and the amount of
follow-up control required are expected to decline.
The most cost-effective way of promoting fynbos res-
toration was to apply the general fynbos seed mix
which included the major structural component miss-
ing from the soil-stored seed banks (overstory proteoid
shrubs). The fynbos annual supplement added a small
benefit to restoration during the first year on untop-
soiled and shallow topsoil plots, but incurred nearly
twice the cost in seed-collecting time. Fertilizer pro-
vided no benefit in deep topsoil areas. However, it was
fore the initiation of restoration, it has been possible to
restore topsoiled areas to a locally species-rich and
structurally representative fynbos community. Casual
observations at the trial site indicate that the indigenous
fauna also is returning, including reptiles, amphibians,
and invertebrates.
The trial has demonstrated that restoration succeeds if
an ecologically sound conceptual framework is followed
(Holmes & Richardson 1999). In most systems, key fac-
tors contributing to a conceptual framework include the
processes leading to degradation, and the recruitment
dynamics, community structure, ecosystem function,
and disturbance regime of the native ecosystem (Hobbs
& Norton 1996; Primack 1996; Dobson et al. 1997; Palmer
et al. 1997; Holmes & Richardson 1999). Invasive alien
trees had completely altered the structure and function-
ing of the vegetation at the site. By removing the alien
trees and controlling their recruitment, fynbos species
were able to re-establish, predominantly from in situ per-
sistent seed banks, but also from sown seed.
Recruitment in fynbos vegetation is almost entirely
coupled to fire (Le Maitre & Midgley 1992), and germi-
nation cues are directly or indirectly linked to fire (Kee-

Table 6. Costs and benefits associated with various treatments applied in the restoration trial. Benefits are
rated in a relative way: N ⫽ none or detrimental, ⫹ small benefit, ⫹⫹ moderate benefit, ⫹⫹⫹ large benefit.
Cost
Treatment man-days/ha US$/ha Benefit

Site preparation (earthworks excluded, as it is part of mining operation)

Biocontrol a – 167 ⫹⫹
Seed mixes
Fynbos mix 40 – ⫹⫹⫹
Fynbos annuals 30 – ⫹
Commercial seed – 448 N
Fertilizer
Fish emulsion ⬍1 146 N
Horticote ⬍1 1,587 ⫹b
Follow-up alien control
Pine & Hakea 7.5c – ⫹⫹⫹
Acacia & Eucalypt 27.5 – ⫹⫹⫹
a Rust fungus Uromycladium tepperianum which was inoculated onto Acacia saligna in September 1994. Biological control generally works

by lowering the reproductive output of the aliens and ultimately the amount of follow-up control required.
b Of small benefit to untopsoiled areas only.
c Would have been unnecessary had mulch been prepared without pine and hakea seed.

MARCH 2001 Restoration Ecology 79

Shrubland Restoration Following Alien Invasion and Mining
ley & Bond 1997). By clearing the site in late summer
and giving suction-harvested seed a smoke treatment
before sowing, many of the natural post-fire conditions
were simulated. Smoke and smoke extracts have been
shown to stimulate germination in a wide range of spe-
cies from fynbos and other mediterranean-climate
shrublands (De Lange & Boucher 1990; Dixon et al.
1995; Brown & Van Staden 1997; Keeley & Fothering-
ham 1998). Smoke treatment has been used successfully
in stimulating recruitment in fire-prone vegetation fol-
lowing bauxite mining in Western Australia (Roche et
al. 1997). The only natural germination cue omitted was
a heat pulse, which occurs during fire and is known to
stimulate some species with soil-stored seeds (Jeffery et
al. 1988; Musil & de Witt 1991; Kilian & Cowling 1992).
Seeds of these refractory species could persist in the
dormant state at the trial site.
Despite three decades of dense pine invasion, the soil
seed banks contributed 60% of all species recruiting,
representing 70% of species present in three-year-old
restored vegetation. Many fynbos species have long-
term, persistent seed banks (Holmes & Cowling 1997a,
1997b), and this result emphasizes the important contri-
bution of topsoil in restoring such vegetation (Putwain &
Gillham 1990; Ward et al. 1997; Holmes & Richardson
1999). The relatively high level of recruitment recorded
in topsoiled, unseeded areas suggests that soil distur-
bance warrants further investigation as a method of
stimulating germination.
Restored community structure and composition may
be compared to that of a native community to assess
whether restoration objectives have been met (Dobson
et al. 1997; Palmer et al. 1997; Holmes & Richardson
1999). The aim of returning Proteoid Fynbos to the site
was attained on topsoil plots. All major functional
groups were also present, although resprouting guilds
may be under-represented compared to undisturbed
native communities. Structural and functional composi-
tion is relevant in assessing most restoration outcomes
in floristically complex regions such as the Cape Floris-
tic Kingdom. The extremely high turnover in species
along environmental and geographical gradients (Cowl-
ing et al. 1992; Simmons & Cowling 1996) renders floris-
tic comparisons between restored and native communi-
ties problematic.
Implications for Restoring Alien-Invaded Sites
The transformation of fynbos vegetation to dense
stands of alien trees is analogous to the conversion of
native forests to agricultural and then degraded land:
without intervention, an “extinction debt” of species is
created (Dobson et al. 1997). Because of the localized
distribution of many rare and endemic species in the
Cape Floristic Kingdom (Cowling et al. 1992), invasions
80
pose a real threat to the conservation of biodiversity
(Rebelo 1992b). This study has demonstrated that fyn-
bos areas supporting dense aliens for three decades
may be restored to native vegetation; therefore, such ar-
eas should never be written-off for nature conservation
purposes. Although many fynbos species have long-
term persistent seed banks (Holmes & Cowling 1997a,
1997b) which can survive average-to-long fire intervals
(15–45 years, van Wilgen et al. 1992), these seed banks
eventually decline in the absence of seed rain. The in-
tensity of restoration intervention required is propor-
tional to the duration and the number of fire-cycles of
dense alien invasion, and invaded sites should be cleared
as soon as possible. In order to maximize recruitment
from persistent fynbos seed banks, clearing treatments
should be planned to maximize germination of soil-
stored seeds. The risk of a damaging, high-intensity fire
through dense, alien slash should be minimized either
by removing large, felled biomass or by burning the
aliens standing. In areas of extensive alien invasion, seed
of local serotinous species should be sown after burning
the site. Regular follow-up control is essential to pre-
vent the reestablishment of an alien stand.
Implications for Restoration After Mining and Construction
Can Fynbos Be Restored on Untopsoiled Substrata? The few
species that established on subsoil derived from the
seed mix. Those sown species which established rela-
tively consistently (e.g., Protea lepidocarpodendron, Berze-
lia lanuginosa, and Athanasia crithmifolia) are able to
grow in heavier soil.
Plant cover and vegetation development were re-
tarded in untopsoiled plots, indicating that restoration of
a fully diverse and functional cover of fynbos on subsoil
or mine overburden substrata is unlikely to be achieved
in the short-term. In addition to providing soil-stored
seed banks, topsoil has better water-absorbing and hold-
ing capacity than subsoil, and contains important plant
growth nutrients, and the micro-flora and fauna essential
for nutrient-cycling processes (Brady 1974). Thus, even a
thin layer of topsoil would greatly ameliorate subsoil
conditions by enabling nutrient-cycling processes to be
initiated. Proteaceae survival and growth were lower on
a rehabilitated sand mine than in nearby scrub heath
communities in Western Australia. A major problem at
the rehabilitation site was impedance between surface
and subsurface soils, which prevented normal taproot
development (Enright & Lamont 1992).
If possible, some topsoil should be spread over the
site. If topsoil is not available, subsoil or overburden
should be ripped to reduce compaction and increase wa-
ter penetration. Ecosystem processes should be initiated
by applying mulch and sowing non-invasive, fast-grow-
Restoration Ecology MARCH 2001

ing annuals and indigenous legumes and hardy peren-
nial species. After germination, organic or low concen-
trations of ultra-slow-release fertilizer should be applied
to improve the soil nutrient status and promote the de-
velopment of plant cover. In this way primary succes-
sion may be accelerated (Dobson et al. 1997). Inorganic
fertilizers that contain high levels of phosphate should
be avoided, as fynbos species are particularly sensitive
to this nutrient (Stock & Allsopp 1992). Alien herba-
ceous species are promoted by fertilizer addition, but
should decline once a dense perennial cover develops.
Is Topsoil Depth an Important Factor in Restoring Fynbos?
Shallow and deep topsoil treatment differences were of
a much lower magnitude than those between topsoiled
and untopsoiled treatments for all the measured vari-
ables. Thus, replacing a little topsoil is far better than no
topsoil, when restoring a site to fynbos.
Plant density was generally higher in the shallow
topsoil treatment, which suggests that a larger propor-
tion of its soil seed bank was stimulated to germinate
compared to the deep topsoil treatment. Differences in
density were more marked at 18 months than at six
months, indicating that there was more recruitment
during the second winter in shallow than in deep top-
soil. This may relate to the lower canopy cover in shal-
low topsoil, which could impact both seed germination
and recruitment.
Plant canopy cover remained highest in deep topsoil
throughout the three-year trial. The deeper topsoil
probably provided a more favorable growing environ-
ment for the establishing plants, including a longer
growing season than shallow topsoil. Therefore, the
more topsoil returned to a restoration site, the faster
will be the development of plant cover. However, care
should be taken when stripping topsoil to ensure that
the layer containing the viable seed bank (0–100 mm in
fynbos) is stockpiled separately from deeper layers be-
fore respreading, to prevent the seed bank being di-
luted (Putwain & Gillham 1990).
Which Seed Mix Best Restores Fynbos on the Different Sub-
strata? Seed addition is essential for any indigenous re-
cruitment to occur on untopsoiled sites, because subsoil
and overburden are devoid of native seeds. On topsoil
plots, however, the seed mixes improved the richness
and structural composition of the vegetation. Proteoid
shrubs form an overstory layer in many fynbos commu-
nities and are an important structural component of the
vegetation (Cowling & Holmes 1992). Furthermore, this
overstory layer has been shown to maintain community
diversity in the long-term (Vlok 1996). As proteoids are
predominantly serotinous, and are eliminated by alien
invasions and mining operations, they must be sown
back into the community.
MARCH 2001 Restoration Ecology
Shrubland Restoration Following Alien Invasion and Mining
During the first year, on both untopsoiled and shal-
low topsoil plots, the fynbos-plus-annual seed mix in-
creased the density of graminoids compared to the
general fynbos mix. No other growth-form differed
among the seed treatments on any of the substrata. In
most situations a general fynbos mix containing the lo-
cal serotinous species and a variety of non-serotinous
species adequately complements the soil-stored seed
bank in restoring fynbos diversity, structure, and
cover. In situations where it is essential to have rapid
development of plant cover (for example, if topsoil is
of poor quality or soil erosion is a threat), it may be ap-
propriate to collect additional seed from a fire-belt
area to boost the graminoid component. However, the
result may not justify the additional expense of doing
this: nearly twice the seed-collecting time. The results
indicate a high correlation between plant density and
cover. Therefore, to ensure good initial cover, it is nec-
essary to sow at a reasonably high rate (40–70 seeds/m2,
depending on the predicted soil-stored component).
Seed of the commercially available cultivar of Cynodon
dactylon (Bermuda grass) failed to establish well and
therefore did not fulfil its potential role of providing
early plant cover.
The importance of topsoil in successfully restoring
fynbos at the restoration trial site emphasizes the need
to manage this resource extremely carefully. If possible,
topsoil should be spread on another area immediately
after stripping to minimize the death of buried indige-
nous propagules. It has been shown that even short pe-
riods of topsoil stockpiling may result in death of plant
propagules (Hargis & Redente 1984).
Does Fertilizer Addition Promote Fynbos Establishment? On
deep topsoil plots the addition of fertilizer increased
mortality in proteoid shrubs that have sensitive cluster
roots, and imparted no benefit in terms of increased
plant cover. Vegetation cover increased following fertil-
izer addition in untopsoiled and shallow topsoil plots.
This increase in plant growth, coupled with a lack of
nutrient enrichment in the soil, suggests that nutrients
were assimilated by the vegetation. As most of the plant
cover increase was attributable to alien herbaceous spe-
cies, fertilization is not recommended as a means of
promoting fynbos establishment where topsoil is avail-
able. However, in areas devoid of topsoil, such as
eroded areas or soil slips, the application of ultra-slow-
release fertilizer, together with mulch and indigenous
seed, may accelerate nutrient-cycling processes and the
re-establishment of vegetation cover.
Future Management
To ensure a sustainable ecosystem in the long-term, it is
important to reinstate the native disturbance regime. To
81
Shrubland Restoration Following Alien Invasion and Mining
do this, invasive plants must be controlled and the site
burned on a 15–45 year cycle (depending on local con-
ditions; van Wilgen et al. 1992). Without burning, the
vegetation eventually will become moribund and a po-
tential fire hazard. If fire is excluded, secondary succes-
sion to coastal thicket or Afromontane forest could oc-
cur (Cowling & Holmes 1992). However, biodiversity
would be lost in this process and it is recommended
that areas successfully restored to fynbos be managed
for fynbos conservation. Burning the site also would
provide a test of the ecological sustainability of the res-
toration in the long-term (Palmer et al. 1997).
Acknowledgments
I wish to thank Janet Barker of the Environmental Evalua-
tion Unit at the University of Cape Town for facilitating
the study, and John Butterworth of Serina Mines Pty. Ltd.
for supporting the research, arranging the site prepara-
tion and research finance, and monitoring rainfall at the
site. John Jordaan, Fiona Powrie, and Lee Jones gave ad-
vice on seed collecting, seed storage, and fertilizer addi-
tion, and Jaana Ball and Fatima Parker assisted with mon-
itoring. I thank Tony Rebelo, Dave le Maitre, and an
anonymous reviewer for commenting on the manuscript.
LITERATURE CITED
Anonymous. 1997. White paper on the conservation and sustain-
able use of South Africa’s biological diversity. South African
Government Gazette. Vol. 385, Number 18163.
Brady, N. C. 1974. The nature and properties of soils. 8th edition.
Macmillan Publishing Co. Inc., New York.
Brown, N. A. C. 1993. Promotion of germination of fynbos seeds
by plant-derived smoke. New Phytologist 123:575–583.
Brown, N. A. C., and J. Van Staden. 1997. Smoke as a germination
cue: a review. Plant Growth Regulation 22:115–124.
Cowling, R. M., editor. 1992. The ecology of fynbos: nutrients, fire
and diversity. Oxford University Press, Cape Town.
Cowling, R. M., and P. M. Holmes. 1992. Flora & vegetation. Pages
23–61 in R. M. Cowling, editor. The ecology of fynbos: nutri-
ents, fire and diversity. Oxford University Press, Cape Town.
Cowling, R. M., P. M. Holmes, and A. G. Rebelo. 1992. Plant di-
versity and endemism. Pages 62–112 in R. M. Cowling, edi-
tor. The ecology of fynbos: nutrients, fire and diversity. Ox-
ford University Press, Cape Town.
Cowling, R. M., P. W. Rundel, B. B. Lamont, M. K. Arroyo, and M.
Arianoutsou. 1996. Plant diversity in mediterranean-climate
regions. Trends in Ecology & Evolution 11:362–366.
Cowling, R. M., D. M. Richardson, and P. J. Mustart. 1997. Fyn-
bos. Pages 99–130 in R. M. Cowling, D. M. Richardson, and
S. M. Pierce, editors. Vegetation of southern Africa. Cam-
bridge University Press, Cambridge.
De Lange, J. H., and C. Boucher. 1990. Autecological studies on
Audouinia capitata (Bruniaceae). I. Plant-derived smoke as a
germination cue. South African Journal of Botany 56:700–703.
Dixon, K. W., S. Roche, and J. S. Pate. 1995. The promotive effect of
smoke derived from burnt native vegetation on seed germina-
tion of Western Australian plants. Oecologia 101:185–192.
Dixon, W. J. 1992. BMDP statistical software manual. University
of California Press, Berkeley.
82
Dobson, A. P., A. D. Bradshaw, and A. J. M. Baker. 1997. Hopes
for the future: restoration ecology and conservation biology.
Science 277:515–522.
Enright, N. J., and B. B. Lamont. 1992. Survival, growth and water
relations of Banksia seedlings on a sand mine rehabilitation
site and adjacent scrub-heath sites. Journal of Applied Ecol-
ogy 29:663–671.
Haberman, S. J. 1973. The analysis of residuals in cross-classified
tables. Biometrics 29:203–229.
Hargis, N. E., and E. F. Redente. 1984. Soil handling for surface
mine reclamation. Journal of Soil & Water Conservation 39:
300–305.
Hobbs, R. J., and D. A. Norton. 1996. Towards a conceptual
framework for restoration ecology. Restoration Ecology 4:
93–110.
Holmes, P. M., and R. M. Cowling. 1997a. Diversity, composition
and guild structure relationships between soil-stored seed
banks and mature vegetation in alien plant-invaded South
African fynbos shrublands. Plant Ecology 133:107–122.
Holmes, P. M., and R. M. Cowling. 1997b. The effects of invasion
by Acacia saligna on the guild structure and regeneration ca-
pabilities of fynbos shrublands. Journal of Applied Ecology
34:317–332.
Holmes, P. M., and D. M. Richardson. 1999. Protocols for restora-
tion based on recruitment dynamics, community structure
and ecosystem function: perspectives from South African
fynbos. Restoration Ecology 7:215–230.
Jeffery, D. J., P. M. Holmes, and A. G. Rebelo. 1988. Effects of dry
heat on seed germination in selected indigenous and alien le-
gume species in South Africa. South African Journal of Bot-
any 54:28–34.
Keeley, J. E., and W. J. Bond. 1997. Convergent seed germination
in South African fynbos and Californian chaparral. Plant
Ecology 133:153–167.
Keeley, J. E., and C. J. Fotheringham. 1998. Smoke-induced germi-
nation in California chaparral. Ecology 79:2320–2336.
Kilian, D., and R. M. Cowling. 1992. Comparative seed biology
and co-existence of two fynbos shrub species. Journal of
Vegetation Science 3:637–646.
Le Maitre, D. C., and J. J. Midgley. 1992. Plant reproductive ecol-
ogy. Pages 135–174 in R. M. Cowling, editor. The ecology of
fynbos: nutrients, fire and diversity. Oxford University
Press, Cape Town.
Le Maitre, D. C., B. W. van Wilgen, R. A. Chapman, and D. H.
McKelly. 1996. Invasive plants and water resources in the
Western Cape Province, South Africa: modelling the conse-
quences of a lack of management. Journal of Applied Ecol-
ogy 33:161–172.
Levitt, M. 1997. Putting fynbos back: the rehabilitation of Du
Toitskloof. Veld & Flora 83:81–83.
Morris, M. J. 1999. The contribution of the gall-forming rust fun-
gus Uromycladium tepperianum (Sacc.) McAlp. to the biologi-
cal control of Acacia saligna (Labill.) Wendl. (Fabaceae) in
South Africa. African Entomology Memoir No. 1:125–128.
Musil, C. F., and D. M. de Witt. 1991. Heat stimulated germina-
tion in two Restionaceae species. South African Journal of
Botany 57:175–176.
Palmer, M. A., R. F Ambrose, and N. L. Poff. 1997. Ecological the-
ory and community restoration ecology. Restoration Ecology
5:291–300.
Primack, R. B. 1996. Lessons from ecological theory: dispersal, es-
tablishment and population structure. Pages 209–233 in D.
A. Falk, C. I. Millar, and M. Olwell, editors. Restoring diver-
sity: strategies for reintroduction of endangered plants. Is-
land Press, Washington D. C.
Putwain, P. D., and D. A. Gillham. 1990. The significance of the
Restoration Ecology MARCH 2001

dormant viable seed bank in the restoration of heathlands.
Biological Conservation 27:1–16.
Rebelo, A. G. 1992a. Preservation of biotic diversity. Pages 309–344
in R. M. Cowling, editor. The ecology of fynbos: nutrients,
fire and diversity. Oxford University Press, Cape Town.
Rebelo, A. G. 1992b. Red Data Book species in the Cape Floristic
Region: threats, priorities and target species. Transactions of
the Royal Society of South Africa 48:55–86.
Rebelo, A. G. 1996. Fynbos biome. Pages 62–74 in A. B. Low and
A. G. Rebelo, editors. Vegetation of South Africa, Lesotho
and Swaziland. Department of Environmental Affairs and
Tourism, Pretoria.
Richardson, D. M, I. A. W. Macdonald, P. M. Holmes, and R. M.
Cowling. 1992. Plant and animal invasions. Pages 271–308 in
R. M. Cowling, editor. The ecology of fynbos: nutrients, fire
and diversity. Oxford University Press, Cape Town.
Richardson, D. M, I. A. W. Macdonald, J. H. Hoffmann, and L.
Henderson. 1997. Alien plant invasions. Pages 535–570 in R.
M. Cowling, D. M. Richardson, and S. M. Pierce, editors.
Vegetation of southern Africa. Cambridge University Press,
Cambridge.
Roche, S., J. M. Koch, and K. W. Dixon. 1997. Smoke enhanced
seed germination for mine rehabilitation in the Southwest of
Western Australia. Restoration Ecology 5:191–203.
Romoff, N. 1986. Revegetation of disturbed areas in the fynbos
biome – the current status. Veld and Flora 72:46–48.
Simmons, M. T., and R. M. Cowling. 1996. Why is the Cape Pen-
insula so rich in plant species? An analysis of the indepen-
dent diversity components. Biodiversity & Conservation 5:
551–573.
Stock, W. D., and N. Allsopp. 1992. Functional perspective of eco-
systems. Pages 241–259 in R. M. Cowling, editor. The ecol-
MARCH 2001 Restoration Ecology
Shrubland Restoration Following Alien Invasion and Mining
ogy of fynbos: nutrients, fire and diversity. Oxford Univer-
sity Press, Cape Town.
Trinder-Smith, T. H., R. M. Cowling, and H. P. Linder. 1996. Pro-
filing a besieged flora: endemic and threatened plants of the
Cape Peninsula, South Africa. Biodiversity and Conserva-
tion 5:575–589.
van Wilgen, B. W., W. J. Bond, and D. M. Richardson. 1992. Eco-
system management. Pages 345–371 in R. M. Cowling editor.
The ecology of fynbos: nutrients, fire and diversity. Oxford
University Press, Cape Town.
van Wilgen, B. W., P. R. Little, R. A. Chapman, A. H. M. Gorgens,
T. Willems, and C. Marais. 1997. The sustainable develop-
ment of water resources: history, financial costs, and benefits
of alien plant control programmes. South African Journal of
Science 93:404–411.
Vlok, J. H. J. 1996. The role of overstorey proteoid shrubs in main-
taining species richness in a southern Cape mountain fynbos
community. M.Sc. Thesis. University of Natal, Pietermar-
itzburg, South Africa.
Ward, S. C., J. M. Koch, and C. D. Grant. 1997. Ecological aspects
of soil seed-banks in relation to bauxite mining. I. Unmined
jarrah forest. Australian Journal of Ecology 22:169–176.
Witkowski, E. T. F. 1991. Growth and competition between seed-
lings of Protea repens (L.)L. and the alien invasive Acacia sali-
gna (Labill.)Wendl. in relation to nutrient availability. Func-
tional Ecology 5:101–110.
Wood, J., A. B. Low, J. S. Donaldson, and A. G. Rebelo. 1994.
Threats to plant species diversity through urbanization and
habitat fragmentation in the Cape Metropolitan Area, South
Africa. Pages 259–274 in B. J. Huntley, editor. Botanical di-
versity in southern Africa. Strelizia 1, National Botanical In-
stitute, Pretoria, South Africa.
83
Shrubland Restoration Following Alien Invasion and Mining

Appendix 1. The association between biological guilds and (a) topsoil depth and (b) seed treatments in three-year-old restored
fynbos. The relative percentages of each guild, based on cover values, are listed with adjusted standardized deviates (ASD) in
parentheses. ASD absolute values exceeding 3.0 indicate cells with unusually large deviations from the expected. Seed treatments
are: Control (no seed added), F (fynbos mix), FA (F & annuals), FC (F & commercial seed); Reseeder-sl is short-lived (⬍5 yr), -ll is
long-lived (⬎4 yr).

(a) Topsoil depth: all plots

Growth form ␹2 ⫽ 81*** Regeneration mode ␹2 ⫽ 221***
Geophyte Graminoid Forb Shrub Resprouter Reseeder-sl Reseeder-ll
0 mm 0.1 (1.0) 14.2 (⫺1.2) 0.3 (0.9) 85.4 (1.0) 0 mm 10.9 (⫺3.4) 12.6 (10.8) 76.6 (⫺2.9)
100 mm 0.1 (1.4) 19.5 (8.3) 0.3 (2.3) 80.1 (⫺8.6) 100 mm 19.0 (9.3) 5.3 (0.9) 75.7 (⫺8.8)
300 mm 0 (⫺2.0) 12.7 (⫺7.4) 0.1 (⫺2.8) 87.2 (7.9) 300 mm 12.1 (⫺7.1) 3.3 (⫺7.3) 84.6 (10.3)
Leaf size ␹2 ⫽ 781*** Seed storage mode ␹2 ⫽ 200***
Leptophyll Nanophyll Microphyll Mesophyll Canopy Soil None
0 mm 27.7 (⫺22.6) 32.5 (22.9) 28.4 (11.8) 11.4 (0) 0 mm 51.4 (13.4) 48.5 (⫺13.4) 0.1 (0.1)
100 mm 68.5 (5.1) 8.1 (⫺3.2) 12.3 (⫺3.7) 11.1 (⫺0.6) 100 mm 26.7 (⫺7.9) 73.1 (7.8) 0.1 (1.0)
300 mm 69.6 (8.7) 5.9 (⫺10.7) 12.8 (⫺3.5) 11.6 (0.6) 300 mm 31.3 (⫺0.3) 68.6 (0.4) 0.1 (⫺1.0)
Seed dispersal mode ␹2 ⫽ 294*** Pollination mode ␹2 ⫽ 141***
Wind Vertebrate Ant Ballistic Passive Bird Insect Wind
0 mm 59.6 (13.5) 0.1 (0.1) 1.7 (⫺15.2) 2.3 (0.8) 36.4 (⫺0.9) 0 mm 7.2 (⫺4.9) 77.9 (11.8) 14.8 (⫺9.3)
100 mm 35.7 (⫺4.5) 0.1 (1.0) 23.4 (3.4) 2.0 (0.4) 38.7 (1.5) 100 mm 12.8 (0.8) 58.0 (⫺2.1) 29.2 (1.8)
300 mm 36.7 (⫺3.6) 0.1 (⫺1.0) 24.1 (5.8) 1.8 (⫺0.9) 37.3 (⫺0.9) 300 mm 13.2 (2.2) 56.8 (⫺5.0) 30.0 (3.8)
(b) Seed treatments: topsoil plots only
Growth form ␹2 ⫽ 24*** Regeneration mode ␹2 ⫽ 17*
Geophyte Graminoid Forb Shrub Resprouter Reseeder-sl Reseeder-ll
Control 0.0 (0) 17.5 (⫺3.3) 0.9 (1.8) 81.6 (3.0) Control 18.4 (⫺2.0) 12.8 (0.1) 68.8 (1.7)
F 0.0 (0) 26.7 (2.5) 0.2 (⫺0.9) 73.1 (⫺2.4) F 23.6( 1.3) 12.4 (⫺0.3) 64.0 (⫺1.0)
FA 0.0 (0) 20.7 (⫺2.1) 0.3 (⫺0.6) 79.1 (2.2) FA 18.3 (⫺2.7) 13.3 (0.5) 68.4 (2.0)
FC 0.0 (0) 26.6 (2.3) 0.4 (0) 73.1 (⫺2.2) FC 25.8 (3.0) 12.4 (⫺0.3) 61.8 (⫺2.4)
Leaf size ␹2 ⫽ 227*** Seed storage mode ␹2 ⫽ 54***
Leptophyll Nanophyll Microphyll Mesophyll Canopy Soil None
Control 93.7 (12.6) 3.3 (⫺7.7) 2.5 (⫺6.2) 0.5 (⫺4.5) Control 7.2 (⫺5.9) 92.6 (5.9) 0.2 (0)
F 56.2 (⫺5.5) 25.5 (6.4) 14.9 (2.4) 3.5 (⫺2.6) F 16.3 (⫺0.5) 83.6 (0.6) 0.1 (⫺0.7)
FA 63.4 (⫺1.0) 11.7 (⫺4.1) 14.1 (1.7) 10.8 (6.5) FA 23.7 (5.8) 76.0 (⫺5.8) 0.3 (0.4)
FC 58.0 (⫺4.1) 23.0 (4.2) 13.6 (1.2) 5.4 (0) FC 16.5 (⫺0.3) 83.2 (0.2) 0.3 (0.3)

Seed dispersal mode ␹2 ⫽ 92*** Pollination mode ␹2 ⫽ 19**

Wind Vertebrate Ant Ballistic Passive Bird Insect Wind
Control 15.0 (⫺7.3) 0.2 (0) 22.4 (0.5) 10.5 (4.2) 51.8 (4.3) Control 14.3 (⫺0.5) 58.5 (3.2) 27.1 (⫺3.1)
F 33.7 (3.2) 0.1 (⫺0.7) 19.6 (⫺1.7) 4.8 (⫺1.9) 41.8 (⫺0.5) F 14.4 (⫺0.7) 49.9 (⫺1.1) 35.7 (1.7)
FA 29.2 (⫺0.2) 0.3 (0.4) 18.6 (⫺2.3) 6.3 (0.1) 45.7 (2.0) FA 15.9 (0.7) 53.4 (1.1) 30.7 (⫺1.8)
FC 33.6 (2.9) 0.3 (0.3) 26.2 (3.6) 5.0 (⫺1.6) 35.0 (⫺4.9) FC 15.5 (0.3) 47.6 (⫺2.6) 37.0 (2.5)

***p ⬍ 0.05. ***p ⬍ 0.01. ***p ⬍ 0.005.

84 Restoration Ecology MARCH 2001