Biodiversity and Conservation 13: 1675–1698, 2004.

# 2004 Kluwer Academic Publishers. Printed in the Netherlands.

The impact of commercial harvesting on Warburgia

salutaris (‘pepper-bark tree’) in Mpumalanga,
South Africa

J. BOTHA1, E.T.F. WITKOWSKI1,* and C.M. SHACKLETON2

1
Restoration and Conservation Biology Research Group, School of Animal, Plant and Environmental
Sciences, University of the Witwatersrand, PO Wits, Johannesburg 2050, South Africa; 2Department of
Environmental Science, Rhodes University, Grahamstown 6140, South Africa; *Author for correspon-
dence (e-mail: ed@gecko.biol.wits.ac.za; fax: þ27-11-403-1429)

Received 15 July 2002; accepted in revised form 17 June 2003

Key words: Bark damage, Medicinal plants, Red Data species, Resource management, Resprouting/
coppicing

Abstract. Commercialisation often increases the difficulty in managing harvested plant populations sus-
tainably. The bark of the popular medicinal species, Warburgia salutaris (Bertol.f.) Chiov. (Canellaceae)
(‘pepper-bark tree’), is widely traded throughout southern Africa. The impact of commercial harvesting on
this Red Data species was assessed by comparing commercially harvested populations with populations
growing on private land or in protected areas (termed ‘protected populations’) in Mpumalanga and Limpopo
Province, South Africa. The basal diameters and heights of stems in commercially harvested populations were
significantly lower than those of the protected populations. The density of young/small plants was low in all
populations. W. salutaris is usually resilient to high levels of bark harvesting. In this study, 75% of heavily
harvested stems (>10% of the stem below 2 m) coppiced (resprouted). However, individuals that had been
affected by regular fires, or repeatedly harvested, appeared prone to a fungal disease and had a high percentage
mortality. The populations occurring on private land appeared the most vigorous. Habitat in one protected
area had been reduced through the construction of a dam. In another protected area, small W. salutaris
populations exhibited a shrubby growth form, probably due to frequent fires. Our current knowledge of this
species supports a global IUCN status of EN A4acd. Plant conservation needs to become a higher priority both
within and outside protected areas. Commercially harvested populations should be better managed through
improved harvesting techniques and monitoring. Cultivation levels urgently need to be increased. Further
research should be conducted on factors limiting regeneration, including the most appropriate fire regime.

Introduction

Southern Africa has a rich diversity of plants, with over 23,680 vascular plant
species having been identified in the subregion (i.e., the area south of the Kunene,
Okavango and Limpopo rivers) (Hilton-Taylor 1996). Increasing numbers of spe-
cies have become extinct or are under pressure, as habitats throughout the sub-
continent are transformed to meet the needs of people: 62 southern African plant
taxa are believed to be extinct, 277 endangered, 445 vulnerable and 1446 rare
(Hilton-Taylor 1997).
Commercialisation of wild plants often exacerbates the difficulty in managing
harvested populations sustainably, particularly when demand is high, and harvesters
lack tenure or strong usufruct rights and/or customary rules of uses have been
1676

eroded (Godoy and Bawa 1993; Dovie et al. 2002; Luoga et al. 2004a). For ex-
ample, favoured species such as Dalbergia melanoxylon have declined in both
Kenya and South Africa through harvesting to supply the woodcarving trade
(Shackleton 1993b; Cunningham 2000). Throughout Africa, numerous medicinal
plant species are becoming increasingly scarce due to a rise in trade to meet the
demand of growing urban populations (Marshall 1998). A decline of valued
medicinal plants in the central Himalayas resulted in a ban on harvesting and trade
(Farooquee and Saxena 1996).
Legislation has failed to curb illegal trade in medicinal species in South Africa,
where it is estimated that approximately 27 million consumers still rely on tradi-
tional medicine (Mander 1998). In a country where 34% of the population between
15 and 65 years of age has no fixed employment (Statistics South Africa 1998), the
medicinal trade makes an important contribution to livelihoods. Approximately 160
traders and 100 vendors traded medicinal plants on the Witwatersrand, Gauteng
province, in 1994 (Williams et al. 2000), and between 20,000 and 30,000 people are
estimated to derive an income from medicinal plants in some form in the province
of KwaZulu-Natal (Mander 1998).
Warburgia salutaris (Bertol.f.) Chiov. (Canellaceae), or the ‘pepper-bark’ (re-
ferring to the peppery taste of its bark and leaves), is a popular traditional
medicine that is utilised and traded throughout southern Africa (Marshall 1998).
The bark, rootbark and leaves have been recorded as being used for over 20
different purposes (Felhaber and Mayeng 1999). Although W. salutaris is available
in tablet form to treat bronchitis, ulcers, chest infections and thrush, this is un-
likely to alleviate the pressure on wild plant populations. Prices ranging from
US$5.85 for 60 tablets (http://www.vitalink.co.za) to US$12.80 for 30 tablets
(http://www.biogenesis.co.za) are beyond the reach of the majority of subsistence
sector consumers in developing countries. The spiritual and symbolic values of
plants are also important in traditional medicine and it is possible that, while
tablets may be acceptable for certain ailments, the raw product may be required to
treat other conditions.
Abundant species, particularly those that are resilient to the impact of harvesting
through high growth rates and/or resprouting/coppicing response, are more easily
able to withstand the impact of intensive harvesting (Cunningham 1992). W. sa-
lutaris is reported to be a fast growing species with vigorous coppicing ability
(Cunningham 1992), but is a rare constituent of evergreen forest (Codd 1976). It
also grows on wooded hillsides and ravines (Coates Palgrave 1990).
W. salutaris has been listed as a priority species for improved management and
propagation in Mozambique, Swaziland, Zimbabwe and South Africa (Marshall
1998). Despite this, 71% of vendors interviewed in informal markets in Mpu-
malanga Province between 1997 and 1999 believed that the bark of ‘isibaha’ (as
this species is known in Swazi and Zulu) is readily available, with 7% saying
that it was difficult to obtain and 22% that it is now rare (Botha et al. 2001).
This discrepancy is probably due to the relative ease with which vendors in the
Mpumalanga markets can still obtain W. salutaris. The bulk of stock on display
was imported from the Maputo markets of Mozambique, where concerns have
 1677

also been raised about the high levels of exploitation (Marshall 1998), although a
limited quantity is harvested in Mpumalanga (Botha 2001). W. salutaris (known
as ‘mulanga’ in Venda and ‘xibaha’ in Tsonga) was reported to be difficult to
obtain in Limpopo Province. Despite its Red Data conservation status in
South Africa, bark is being exported from South Africa and Mozambique to
Zimbabwe, where it is now believed to be almost extinct in the wild (Veeman
et al. 2001).
W. salutaris is readily cultivated, but the current level of cultivation in South
Africa is not sufficient to meet demand. This urgently needs to be rectified.
However, with the time lag for trees to grow to a harvestable size, it is also
important to ensure that wild populations are adequately managed. This is more
readily achieved if there is an understanding of the impact of harvesting on wild
populations. Despite its high profile, there are little quantitative data on the extant
populations, apart from an assessment of the harvesting damage of W. salutaris in
KwaZulu-Natal Province in 1987 (Cunningham 1992) and a recovery plan (Church
and Scott-Shaw 2002).
Ecological sustainability may be assessed by directly measuring the rate of ex-
traction, and comparing it to the rate of natural replacement (Godoy and Bawa
1993; Luoga et al. 2002). This may often prove time consuming and expensive for
species with high longevity. Demographic studies are a cost effective means of
providing useful data on the impact of harvesting and other disturbances, con-
tributing to the development of effective management strategies (Geldenhuys and
van der Merwe 1988; Witkowski et al. 1994; Botha et al. 2002; Wilson and
Witkowski 2003) as well as providing quantitative data to ascertain whether further
in-depth research or monitoring is required.
This study aimed to assess the impact of commercial harvesting on W. salutaris by
comparing commercially harvested populations with populations that had received a
level of protection from harvesters (termed ‘protected populations’ in this paper).
The commercially harvested populations were located on the properties of com-
mercial forestry companies as well as on communal land. At the time of the study, the
latter fell under the jurisdiction of the local Tribal Authority. Tribal Authorities were
established by the previous South African government (Bantu Authorities Act of
1951), and were responsible for allocating local land use rights, adjudicating civil
disputes and co-ordinating local development prior to independence. These local
structures were often regarded as illegitimate, as traditional leaders were perceived to
have been co-opted by the apartheid government (Shackleton et al. 1998). The
protected W. salutaris populations occurred on private land (game farms) where
control of natural resources falls under the owner of the land as well as within
protected areas, which fell under the jurisdiction of conservation authorities.
The objectives of the study were to: (i) compare the population structures of
commercially harvested and protected populations, and (ii) assess the extent (i.e.,
the proportion of plants affected), degree (i.e., severity of the damage) and impact
of harvesting of W. salutaris growing under different land management regimes.
This forms part of a broader study on the trade of medicinal plants on the western
boundary of the Kruger National Park (Botha 2001).
 1678
Table 1. Characteristics of sample sites. Data from Cooper (1985) and Low and Rebelo (1996).
Populations Site Province Management Vegetation Number of Approximate Additional notes
regime type populations aerial size (ha)
of habitat;
mean  SE (range)

Commercially Communal Mpumalanga Communal Sour Lowveld 3 1.0  0.2 (0.6–1.3) Village of 20 families near
harvested land Bushveld the site, with a larger one
populations (800 people) approximately
10 km away. All W. salutaris
were assessed.
Forestry Mpumalanga Forestry Afromontane 1 187.0 Harvesters were accompanied
forest to locate the W. salutaris, and
all those that could be found
were assessed (three plots).
Forestry Mpumalanga Forestry Afromontane 1 131.0 Harvesters were accompanied
forest to locate the W. salutaris, and
all those that could be found
were assessed (one plot).

Protected Private land Mpumalanga Game farm Mixed Lowveld 1 5.0 W. salutaris were assessed
populations Bushveld on three plots.
Private land Limpopo Game farm North Eastern 1 20.0 W. salutaris were assessed
Mountain on two plots.
Bushveld
Table 1. (continued).
Populations Site Province Management Vegetation Number of Approximate Additional notes
regime type populations aerial size (ha)
of habitat;
mean  SE (range)

Private land Limpopo Game farm North East 1 20.0 W. salutaris were assessed
Mountain on three plots.
Bushveld
Protected Limpopo Protected area North Eastern 3 7.0  3.2 (0.5–30.0) W. salutaris were assessed
area A Mountain on eight plots, five of which
Sourveld, comprised <5 individuals.
Lowveld Sour
Bushveld
Protected Limpopo Protected area Low Soutpansberg 2 16.0  6.0 (10.0–22.0) W. salutaris were assessed on four
area B Mountain plots. Previously burnt every
Bushveld 2–3 years.

1679
1680

Study area

Commercially harvested populations were located through vendors trading tradi-

tional medicines in informal markets in Mpumalanga. Regional conservation of-
ficials assisted in the identification of the protected populations. Attempts were
made to locate harvested and protected populations in the same localities and
similar habitats, to minimise differences in environmental factors. However, as only
one protected W. salutaris population was located in Mpumalanga, four additional
protected populations were assessed in the neighbouring Limpopo Province. Site
descriptions are provided in Table 1. At the request of conservation managers,
localities of populations have been omitted. To distinguish between the two pro-
tected areas in the study, they are referred to as protected area A and protected area
B.
Rainfall in the study area is concentrated in the hot summer months (October–
May), with a distinct gradient from the Drakensberg escarpment in the west to the
Mozambique border in the east (>1000 mm/annum to approximately 500 mm/
annum), and to a lesser extent, from north to south. Winter is temperate and frost is
rare.

Methods

Five commercially harvested and 8 protected populations were sampled (Table 1).
A total count of the W. salutaris at a site or plot was conducted, depending on the
aerial size of the habitat. Plot sizes varied according to the distribution of the target
species, but were usually 20  40 m, or 20  30 m. The overall percentage of plants
sampled per population was 65  17% (mean  SE).
Heights and basal diameters were measured, the latter at 30 cm above the ground,
as some individuals branched below breast height. The number of coppice shoots of
each plant was recorded to obtain a measure of resprouting vigour. In the case of
multi-stemmed trees, each stem was measured and assessed. The external damage
to the stem was assessed on a scale adapted from Cunningham’s seven-point scale
for stem damage (Cunningham 1992) (Figure 1). The cause of damage was noted,
for example, harvesting or natural causes (fire, herbivory, elephant damage), as was
the state of health of the stem (alive, dead, appearance of physiological stress).
Stems classified as stressed showed signs of disease (rotting stems or branches) and/
or desiccation, but part of the plant was still living, or it was coppicing. Stems
classed as dead were desiccated or rotten, with no shoots or other signs of life.

Data and statistical analysis

The equivalent basal diameter of each tree was calculated. Stems with basal dia-
meters of 1 cm were termed young plants. Young plants are most likely to ori-
ginate from root suckering, although it is possible that some of them were
 1681

Figure 1. Scale used in the assessment of bark damage on a tree trunk. All assessments represent
the proportion of bark removed below 2 m, indicated by the dotted line (adapted from Cunningham
1992).

seedlings. Apart from size classes 1 (1 cm) and 2 (>1 and 5 cm), stem basal
diameter values were categorised into 5 cm increments.
Harvesting damage was summarised and displayed graphically according to land
use type (plots were pooled), to assess the difference in the extent, degree and
impact of harvesting of W. salutaris under different land management regimes.
Statistical analyses were performed using Systat 7.0 for Windows (1997) and
Excel 2000. Size class distributions were compared through Kolmogorov–Smirnov
Goodness of Fit tests. The percentages of plants of harvestable size were calculated
according to the size classes of trees that were currently commonly being harvested.
In the case of W. salutaris, this included trees from size class 2 upwards. Histograms
were used to compare the degree of harvesting in commercially harvested and pro-
tected populations. Chi-square analyses were used to compare the proportions of
trees of harvestable sizes in harvested and protected populations, as well as the
proportions of individuals that had survived after harvesting. Smaller size classes
were pooled to ensure a minimum number of five in each class. Non-parametric
statistics were used to compare basal diameter and height variations between har-
vested and protected populations (Kruskal–Wallis and Mann–Whitney U tests).
The quotients between the numbers of trees in successive diameter classes were
calculated and displayed graphically. Fluctuating quotients indicate an unstable or
fluctuating population, while in a stable population, quotients between the numbers
of trees in successive size classes approach a constant value (Meyer 1952; Harper
1977).
Simpson’s Index of Dominance (C) (Equation 1) and the Permutation Index (P)
(Equation 2) provide additional measures of population structure (Wiegand et al.
2000). The former describes the probability that any two trees drawn from the same
community are of the same size (Pielou 1977; Wiegand et al. 2000). Values above
0.1 show that the size frequency is steeper than would be expected from an
1682

exponentially declining population; those below 0.1 indicate that the size classes
are more evenly distributed.

1 Xk
C¼ Ni ðNi  1Þ ð1Þ
N ðN  1Þ i¼1

N is the total number of trees, Ni is the number of trees in class i, and k is the
number of size classes.
X
k
P¼ jJi  ij; Ji ¼ 1; 2; ::::::; k ð2Þ
i¼1

k is the number of size classes, Ji is the rank of size class i (i ¼ 1 for the smallest
trees), with the highest rank (Ji ¼ 1) given to the most frequent size class. Its
development was based on the idea that the size distribution of an undisturbed ideal
population should decline monotonically. In that case, the ranking is equivalent to
enumerating the size classes from the class representing the smallest (most fre-
quent) to that representing the biggest (least frequent) trees. When a size dis-
tribution is discontinuous, i.e., when bigger trees are more frequent than a
preceding size class, the ranking differs from enumeration, resulting in a greater
Permutation Index (Wiegand et al. 2000).

Results

All the W. salutaris populations had been harvested to some extent, although those
growing on protected sites had been harvested relatively lightly. Harvesting had
taken place more than 3 years prior to the survey in the majority of these popu-
lations (owners, managers and field rangers, personal communication, 1999).

Population parameters

The density of W. salutaris ranged from 12 to 475 trees/ha on commercially har-

vested sites (mean  S.E. ¼ 259  96/ha), and from 3 to 281 trees/ha in protected
populations (56  19/ha). There was no significant difference between the densities
(U5,14 ¼ 53; p > 0.05) or population sizes (U5,14 ¼ 42.0; p > 0.05) of commercially
harvested and protected populations (Table 2).
There was a highly significant difference between the size class distributions
based on basal diameters (Kolmogorov–Smirnov D106,517 ¼ 0.30; p < 0.005) (Fig-
ure 2a) as well as heights (Kolmogorov–Smirnov D170,667 ¼ 0.34; p < 0.005) of
plants from commercially harvested and protected populations. The basal diameters
and heights of commercially harvested populations were significantly lower than
those of protected ones (U106,517 ¼ 21,133.00; p < 0.005 and U170,667 ¼ 35,701;
p < 0.005, respectively; Table 2).
Table 2. Population parameters of harvested and protected W. salutaris populations (Mann–Whitney U test; *p < 0.01).
Estimated Population Recruit density Basal diameter Height Simpson’s Index Permutation
population density mean  SE mean  SE mean  SE of Dominance Index
size mean  SE (range) (range) (range) (C) (P)
mean  SE (range) (young plants/ha) (cm) (m)
(range) (trees/ha)

Commercially 34  12 (14–80) 259  96 (12–475) 15  5 (9–25) 7.9  0.7 (0.1–29.9) 2.3  0.2 (0.05–12.0) 0.31 4
harvested
Protected 49  20 (1–227) 56  19 (3–281) 6  2 (0–12) 12.9  0.6 (0.1–94.5) 4.0  0.1 (0.05–14.0) 0.20 10
p values >0.05 >0.05 >0.05 * *

1683
1684

Figure 2. Population structure of pooled commercially harvested and protected W. salutaris popula-
tions: (a) relative frequencies and (b) quotients between numbers of trees in successive size classes.
Apart from size classes 1 (1 cm) and 2 (>1 and 5 cm), stem basal diameter values were categorised
into 5 cm increments.

Size class 6–10 cm and size classes 16–25 cm in the commercially harvested
populations had frequencies of zero (Figure 3). Although the protected populations
also had size classes with frequencies of zero, these usually fell in the higher range
of basal diameters (>35 cm), apart from the protected area B populations (Figure
4d).
The densities of young W. salutaris plants were low on all sites, but tended to be
lower in protected populations than in those that had been commercially harvested,
although this was not significant (6  2 and 15  5 trees/ha, respectively)
(U5,14 ¼ 53.0; p > 0.05; Table 2). A significantly higher proportion of individuals
occurred in size class 0–1 cm in the commercially harvested populations, compared
with protected populations (28 and 10% of the total population, respectively)
(w2 ¼ 25.9; d.f. ¼ 1; p < 0.005). There were no young plants in one population
growing in protected area B. A population growing on private land in the Limpopo
Province had no individuals with basal diameters 5 cm, possibly due to fire and/or
herbivory.
 1685

Figure 3. Degree of stem damage to commercially harvested W. salutaris populations, through har-
vesting of bark below 2 m on the stem and chopping on (a, b) two forestry sites, and (c) communal land
in Mpumalanga. (d) Pooled commercially harvested sites. Apart from size classes 1 (1 cm) and 2 (>1
and 5 cm), stem basal diameter values were categorised into 5 cm increments.
1686

Figure 4. Degree of stem damage to protected W. salutaris through harvesting of bark below 2 m on
stems and chopping of individuals assessed on plots on (a, b) two private game farms; (c, d) two
protected areas in Limpopo Province; (e) a private game farm in Mpumalanga; and (f) pooled protected
populations. Apart from size classes 1 (1 cm) and 2 (>1 and 5 cm), stem basal diameter values were
categorised into 5 cm increments.
 1687

Figure 4. (continued).

The quotients between trees in successive size classes in both the commercially
harvested and protected populations fluctuated widely (Figure 2b). The Permutation
Indices were 4 and 10 for the commercially harvested and protected populations,
respectively (Table 2). The size class distributions of both the commercially har-
vested and protected W. salutaris populations were steeper than would be expected
from an exponentially declining distribution (Simpson’s Index of Dominance 0.31
and 0.20, respectively).

Harvesting

There was a significantly lower proportion of trees of harvestable size in the

commercially harvested populations (52  12%), compared with protected popu-
lations (74  8%) (w2 ¼ 6.2; d.f. ¼ 1; p < 0.05; Table 3). The extent of utilisation
was significantly higher in the former (w2 ¼ 116.8; d.f. ¼ 1; p < 0.0001) (65  9%
versus 12  3%).
All size classes had been harvested on the communal sites, including the lowest
basal diameters (0–1 cm) (Figure 3c). The smallest stem utilised had a basal
diameter of 0.3 cm. In the forest sites, both the extent and degree of harvesting were
1688

Table 3. Proportion of W. salutaris populations of harvestable size (stem diameter >1 cm), and status of
harvested stems (mean  SE) (w2 *p < 0.05; **p < 0.01).
Populations Percentage stems of Percentage Fate of harvested trees
harvestable size stems harvested
Dead (%) Alive (%) Stressed (%)

Commercially 51.6  12.2 64.6  9.2 28.6  12.5 64.8  14.6 13.8  6.0
harvested
Protected 74.0  8.3 11.5  3.4 0.3  0.3 91  8.2 8.8  8.2
p values *(d.f. ¼ 1) **(d.f. ¼ 1) **(d.f. ¼ 4)

high. Stems from size class 6–10 cm onwards had been harvested at levels >25% of
the bark below 2 m in both communal and forestry areas (Figure 3). Ringbarking
and chopping had occurred, the latter particularly at the communal sites.
Harvesting had occurred on private land in Limpopo Province and Mpumalanga,
as well as in protected areas, but not as extensively (1–25%) (Table 3) or to the
same degree (Figure 4) as in the commercially harvested populations. The majority
of these trees had been harvested at rates of < 25% of the stem below 2 m. A W.
salutaris with a basal diameter of 26.8 cm had been chopped in 1958 in protected
area B (M. Khoza, personal communication, 1998). Although coppicing, this tree
showed signs of disease (a fungal pathogen), with sections of the main stem rotting.
There was no significant difference between the number of stems per individual
in plants from commercially harvested and protected populations (U106,517 ¼
27,660; p >0.05) (1.9  0.2 and 1.8  0.1, respectively). There was, however, a
significant difference between the proportion of multi-stemmed trees in commer-
cially harvested and protected populations (w2 ¼ 5.3; d.f. ¼ 1; p < 0.05), with 51%
of the plants from commercially harvested and 37% of those from protected po-
pulations having coppiced (Table 4). Within the commercially harvested popula-
tions, the proportion of utilised individuals that were coppicing was significantly
higher than the proportion of unharvested trees that were coppicing (82 and 32%,
respectively) (w2 ¼ 17.3; d.f. ¼ 1; p < 0.0001).
The opposite was true for the protected populations. The proportion of harvested
individuals coppicing was significantly lower than the proportion of unharvested
trees that were multi-stemmed (28 and 41%, respectively) (w2 ¼ 4.22; d.f. ¼ 1;
p < 0.05).
Where chopping had occurred there was no relationship between the height of
the harvested stem and the number of resprouts (r2 ¼ 0.017; d.f. ¼ 8; NS), or the
heights of the coppices (r2 ¼ 0.018; d.f. ¼ 10; NS), although data were limited.
There was also no relationship between the basal diameters of chopped stems and
the number of coppices (r2 ¼ 0.30; d.f. ¼ 10; NS).
There was a highly significant difference in the proportions of healthy, dead and
stressed W. salutaris occurring in the commercially harvested populations, and
those in the protected populations (w2 ¼ 30.5; d.f. ¼ 4; p < 0.0001) (basal diameters
>5 cm) (Table 3). The populations growing on private land had the highest
percentage of healthy trees (98%), with 90% of those growing in protected areas
 1689

Table 4. Proportion of commercially harvested and protected W. salutaris populations that were
coppicing or single stemmed (w2 d.f. ¼ 1; *p < 0.05; **p < 0.01).
Populations Category % Coppicing % Single p values
stemmed

Total population Commercially harvested individuals 51 49

Protected individuals 37 63 *
Commercially Harvested individuals 82 18
harvested Unharvested individuals 32 68 **
Protected Harvested individuals 28 72
Unharvested individuals 41 59 *

appearing healthy. The percentage of healthy individuals dropped to 77% in the

harvested populations growing on communal land, with 10% showing signs of
stress and 13% dead. The harvested populations in forestry areas fared better, with
89% of the trees appearing healthy.
In the protected populations, a significantly higher proportion of individuals
appeared healthy after harvesting compared with those in the commercially har-
vested populations (w2 ¼ 25.0; d.f. ¼ 1; p < 0.0001) (91  8 and 65  15%, re-
spectively), where relatively high proportions of the harvested stems appeared
stressed. However, W. salutaris appeared prone to disease in protected area B. In
one plot, 63% of plants had been damaged by fire or elephants, and 60% of these
plants also appeared stressed. In a second plot, disease had affected 45% of the
damaged W. salutaris. Few of the undamaged stems appeared to be stressed: 12% at
the first site and 10% at the second. In this area, W. salutaris tended to have a
shrubby growth form, probably as a result of fires every 2–3 years (M. Khoza,
personal communication, 1998).
Of the individuals that had been ringbarked (old harvest), 29% of those on the
communal site were still alive, with 21% appearing stressed. The only ringbarked
individual on the forestry site had died, a large tree with a basal diameter of 30 cm
and height of 7 m.

Discussion

Populations of species of anthropogenic importance are often characterised by a

reduction in frequencies in larger size classes, a decreased number of size classes
(Rao et al. 1990; Shackleton et al. 1994) and also regeneration bottlenecks (e.g.
Wilson and Witkowski 2003). The basal diameters and heights of W. salutaris were
significantly lower in the commercially harvested populations than in the protected
ones, and there were fewer size classes. The proportion of chopped W. salutaris
stems was relatively low, suggesting that the growth rate of individuals may have
been inhibited through physiological stress resulting from harvesting. A decrease in
mature trees diminishes the sexual reproductive potential of a population through a
1690

lowering of seed production. Although W. salutaris is able to regenerate success-

fully vegetatively (by suckering; Cunningham 1992; Johnson et al. 1995), a loss of
sexual reproduction in a population could result in lowered genetic diversity, which
may negatively affect long-term persistence. Indeed, clusters of trees in KwaZulu-
Natal are generally all clones, and no seedlings have been found in this province
(Scott-Shaw 1999).
The densities of young plants of certain species decrease with increasing human
disturbance, though they may increase in other species, for example, pioneers
(Shackleton et al. 1994; Chandrashekara and Sankar 1998; Luoga et al. 2002). The
density of young plants was low in the majority of W. salutaris populations, but
particularly in the protected populations. There were no individuals with basal
diameters of less than 5 cm in one of the protected populations, and no individuals
in size class 0–1 cm of another. Due to higher levels of coppicing, there were
significantly higher proportions of individuals in size class 0–1 cm in the harvested
populations compared with those in the protected populations. This indicates that
harvesting per se has not impacted recruitment, despite the altered size class profile.
The typical W. salutaris fruiting season is from October to January (Coates
Palgrave 1990). In May 1999, 6% of the protected area A population and in July
1999, 2% of a population growing on private land in Limpopo Province were both
still bearing fruit, which suggests that a lack of fruiting is not the cause of low
recruitment in these populations. The low levels of recruitment of young plants
could be due to most fruit aborting early, and high levels of seed parasitism, which
have been reported in Kwazulu-Natal (Cunningham 1992; Johnson et al. 1995;
Scott-Shaw 1999).
A study of the regeneration potential of W. salutaris was beyond the scope of this
study, but the numbers of mature trees capable of producing seed provide an
indication of the potential resilience of populations. W. salutaris in cultivation at the
Silverglen nursery in KwaZulu-Natal started fruiting when approximately 3–5 m
high (approximately 10 years of age) (Johnson et al. 1995). A W. salutaris in
cultivation at Phindulwane nursery, Mpumalanga, produced seed at 1 m (approxi-
mately 4 years of age) (G. Strydom, personal communication, 2000). Time to
reproductive maturity under field conditions is very likely much greater than these
times would indicate. Recognising that the reproductive potential of a tree varies
according to climatic and environmental conditions as well as its coppicing ability,
42% of the W. salutaris in the harvested populations were >2 m in height, while
66% of the protected populations were >2 m. The highest frequencies of mature W.
salutaris were found on private land, with between 55 and 83 individuals >2 m
occurring on the plots on private land in Limpopo Province and Mpumalanga. In
protected area A, 32 individuals were >2 m, and only seven individuals in protected
area B were >2 m. However, many of the W. salutaris in the latter reserve exhibited
a shrubby growth form due to the effects of fire.
The fluctuating quotients and the Permutation Indices indicate that both the
commercially harvested and protected populations were discontinuous, which is
relatively common in woody species experiencing wide climatic fluctuations, fire,
herbivory and anthropogenic disturbance (Walker et al. 1986; Shackleton 1993a).
 1691

Simpson’s Index was higher in the commercially harvested populations than in the
protected ones, showing that the size frequency distributions were steeper in the
former through the impact of selective harvesting of trees in higher size classes.
A key attribute of the resilience and productivity of savannahs is the ability of
damaged trees to regrow from the remaining stump. In this study, 89% of the W.
salutaris were coppicing. The basal diameter of the stem and the height at which a
stem was chopped may affect coppicing success and the regrowth rate of certain
species, which is important from a management perspective (Shackleton 2000;
Luoga et al. 2004b). In this study, 75% of the W. salutaris that had been heavily
harvested (>10% of the stem below 2 m) were coppicing. There was no relationship
between harvesting height and the heights of coppice shoots in W. salutaris, or
between the basal diameter and number of resprouts.
As anticipated, the proportion of harvested W. salutaris that were coppicing
within the commercially harvested populations was significantly higher than the
proportion of unharvested individuals that were coppicing. However, the opposite
was true of the protected populations. The relatively low proportion of harvested
W. salutaris that were coppicing in the protected populations may be due to the
combined effects of several factors. The individuals that had been utilised on
the private and protected area sites were significantly larger than those from the
commercially harvested populations (stem diameters 19.1  1.6 and 9.5  0.7 cm,
respectively; t ¼ 1.98; d.f. ¼ 98; p < 0.001). They had also been harvested to a
lesser degree. In addition, few signs of other disturbances were noted on the
commercially harvested sites; 4  3% of the W. salutaris had been affected by
fire and the natural breakage of stems. Signs of disturbance in the protected
populations were higher (23  11%), and included fire, elephant damage and road
construction. The overall harvesting impact on the larger individuals in private
and protected areas was thus less than the effects of other forms of disturbance
across all size classes, resulting in higher levels of resprouting amongst the
unharvested W. salutaris. Other large browsing herbivores such as black rhino-
ceros and kudu also utilise W. salutaris in KwaZulu-Natal Province (Scott-Shaw
1999).
The population sizes of the majority of commercially harvested W. salutaris
populations were low, as were the majority of those occurring in the two protected
areas. The sizes of the two populations assessed in protected area B were 8 and 25.
We were unable to find W. salutaris at a third site in protected area B where it had
previously occurred, despite an intensive search with an experienced ranger, who
was familiar with its previous location. Only one population (n ¼ 62) in protected
area A fell within the same range as those growing on private land (n ¼ 59–148).
The remainder ranged from 1 to 10 individuals. One population (n ¼ 10) was
growing above the flood line of a dam on a mountainside, where there was limited
space for additional population growth. W. salutaris was also located on the banks
of a dam (two groups, n ¼ 3 and 4), again suggesting that larger populations had
been flooded after the construction of the dam. An individual W. salutaris and two
groups (n ¼ 4 individuals at both sites) growing in protected area A were unusual in
that they occurred in flat, open woodland rather than on the slopes of hills or
1692

mountains. Similar data were reported for KwaZulu-Natal Province (Scott-Shaw

1999) with four sub-populations (IUCN terminology) locally extinct, seven extant
sub-populations of >20 plants and two with <20 plants.
Although the W. salutaris growing in protected area A appeared vigorous, the
fact that a species occurs in a protected area does not guarantee its long-term
persistence (e.g. Pfab and Witkowski 1999). Plant conservation often takes second
place to other management considerations. In this study, for example, suitable W.
salutaris habitat in protected area A had been reduced by the construction of a dam,
the building of which started in 1969 after the reserve was promulgated in 1965. In
addition, conservation has traditionally focussed on the management of charismatic
animals and their habitats. While this is changing, the majority of conservation
agencies in developing countries are also experiencing severe financial and human
resource cutbacks. The effect of ecological factors such as metapopulation dy-
namics, which are often poorly understood and require long-term autecological
studies, also need to be considered in the management of rare or pressurised species
(Meffe and Carroll 1994).
An integrated management strategy is thus essential, incorporating the
continued protection of those W. salutaris populations growing within protected
areas with extensive cultivation and the improved management of harvested
populations.
In the face of increasing financial constraints, it may be tempting to reduce
research and monitoring of plants. However, this often results in the further decline
of the species, incurring higher expense if salvage operations are attempted
(Schemske et al. 1994). Determining appropriate harvesting quotas combined with
adequate monitoring of populations has proven crucial in the long-term manage-
ment of commercially important species (Cunningham and Mbenkum 1993; Wit-
kowski et al. 1994; Lamont et al. 2001). Furthermore, attempts to reintroduce plants
into new or historically inhabited areas have met with mixed results (Schemske
et al. 1994; Witkowski et al. 2001). In a review of recovery plans of 98 endangered
species in the USA, for example, Schemske et al. (1994) found that the majority
lacked the biological information to assess the dynamics of populations or meta-
populations. Similar problems have been experienced in South Africa (Witkowski
et al. 1997). However, attempts at ex situ conservation of W. salutaris are being
implemented, with recovery plans to augment sub-populations (e.g., Church and
Scott-Shaw 2002). If financial resources, technical skills and time are limited,
assessing population structures and monitoring trends in absolute densities of po-
pulations within a broad area provides valuable information on the changes in the
metapopulation and the relationships between metapopulations, as well as within-
population dynamics (Schemske et al. 1994). Further research also needs to be
conducted on factors limiting the extent of reproduction and establishment of W.
salutaris in the wild. Apart from natural factors such as parasitism, inappropriate
fire regimes (too frequent burning, for example) may kill young plants and saplings.
The results of these studies need to be communicated to managers of protected
areas, private landowners and communities responsible for managing W. salutaris
to enable them to care for these populations as effectively as possible.
 1693

Within communal areas, conservationists could assist people to improve the

management of their wildlife resources by helping them develop viable monitoring
systems and cultivation programmes. A pilot programme initiated in southeastern
Zimbabwe showed that the cultivation of W. salutaris by small scale farmers and
traditional healers had the potential to offer considerable social and economic
benefits, and was well received by participants (Veeman et al. 2001). Traditional
healers, vendors and traders in Mpumalanga, Limpopo Province and KwaZulu-
Natal were also eager to cultivate this and other medicinal species (personal
observation).
Propagation material needs to be made available to people in the subsistence
sector as part of an integrated programme to improve health and food security.
While people in rural areas are often skilled farmers, training and extension ser-
vices may be required to augment local knowledge and experience, as certain
medicinal species require specialised propagation techniques, many of which have
already been developed at facilities such as the Silverglen medicinal plant nursery
in KwaZulu-Natal. W. salutaris is difficult to propagate from seed due to a lack of
availability of seed through high predation levels as well as loss of viability during
conventional storage methods (Symmonds and Crouch 2000). Tissue culture has
proven challenging due to high phenolic content, although an in vitro technique has
been developed (Kowalski and van Staden 2001). The species has been successfully
bulked up for cultivation projects using shoot-tip cuttings (Symmonds and Crouch
2000).
W. salutaris has been found to be susceptible to insect infestations such as
Imbrasia wahlbergi (Boisduval) (Lepidoptera, Saturniidae), Lichtensia carissae
(Brain) (Hemiptera, Coccidae) and Parasaissetia nigra (Nietner) (Hemiptera,
Coccidae) (Crouch and Crouch 2001). Management of pests and disease is thus
likely to be needed, preferably using organic techniques rather than chemical
pesticides, considering the user market. Further research on pest management is
required.
Although a full analysis of communal management of natural resources is be-
yond the scope of this discussion, the development of sustainable harvesting me-
chanisms has to include addressing issues of land and resource tenure. In South
Africa, many of the medicinal plant harvesters come from outside harvesting areas,
often collecting in bulk to supply traders in urban centres. In southern Africa, as in
many parts of the world, local institutions and customary resource management
systems are being eroded, resulting in an often rapid decrease in natural resources
(Shackleton et al. 1998; Letsela et al. 2004). Despite this, harvesters from Mpu-
malanga and Limpopo Province always obtained permits from the local Tribal
Authority when collecting plants on communal land, whereas they seldom re-
quested permission to collect plants on private farms or forestry plantations (Botha
2001).
W. salutaris is one of the few species in which bark regrows vigorously after
intensive harvesting, with individuals having been observed to survive total bark
removal and a complete regrowth of bark (Cunningham and Mbenkum 1993). In
this study, W. salutaris that had been affected by natural disturbance (e.g., fire in
1694

protected area B) or heavily harvested (the commercially harvested population on

communal land) appeared prone to disease and a higher percentage of mortalities.
Many species are vulnerable to fungal or borer attack once bark has been removed,
as damaged surfaces provide pathogens with an entry point to the plant (Knowles
and Witkowski 2000). Harvesting has been known to exacerbate this problem, as
healthy individuals are infected through the use of contaminated knives and other
tools used for harvesting (e.g., Witkowski et al. 1991). One way of ameliorating the
problem would be to train harvesters to use flame sterilised equipment in suscep-
tible populations. In addition, sealant could be painted on the affected area. This
could be achieved by including traditional healers and tribal authorities living in the
area in the management of the species.
Using the old (pre-1994) IUCN categories, W. salutaris had a status of Vulner-
able (VU) for South Africa (and Swaziland; Hilton-Taylor 1996), although
categorised as Endangered (EN) in KwaZulu-Natal and ‘Transvaal’ (a pre-1994
province which included Mpumalanga and Limpopo province). Using the then
updated IUCN (1994) categories (version 2.3), Scott-Shaw (1999) lists it as EN
A1acd for KwaZulu-Natal. Considering other southern African countries in which
it is located, it is given as EN A1acd for Malawi (Msekandiana and Mlangeni
2002), VU A2cd for Mozambique (it is fairly common in southern Mozambique,
but heavily utilised) (but EN globally; Izidine and Bandeira 2002), Critically
Endangered (CR) A1bcd for Swaziland (Dlamini and Dlamini 2002) and CR
A1dB1B2abcdeC1C2aD for Zimbabwe (Mapaura and Timberlake 2002). Using the
latest IUCN (2001) categories (version 3.1), a South African and global status of
EN A4acd is consistent with our present understanding of the distribution, history,
biology and threats to this species.
The increased use of leaves as a substitute for bark should be encouraged, as the
two biologically active ingredients, warburganal and polygodial, are present in both
the leaves and the bark (Drewes et al. 2001). Traditional healers already use leaves
to treat certain ailments (personal communication, 1999) but if this could be carried
out on a wider scale by drying and packaging the leaves for the mass market, more
sustainable levels of harvesting could be achieved from both wild and cultivated
populations. Simultaneously, consumer awareness needs to be raised regarding the
phytochemical basis for this alternative as well as the need to improve the man-
agement of the resource base. This could be achieved by working with the many
traditional healer organisations active throughout southern Africa.
The population structures of commercially harvested W. salutaris populations
differed substantially from protected populations. The mean basal diameters and
heights of the former were significantly lower than those of the latter. There was
also a decrease in the number of size classes in the commercially harvested po-
pulations. While the survival rate of damaged W. salutaris was relatively high,
populations subject to high natural (fire) and anthropogenic degrees of disturbance
were prone to disease and higher rates of mortality. A higher proportion of W.
salutaris growing on private land appeared vigorous (98%) than in protected areas
(90%) and on commercial forestry property (89%), but only 77% of the trees
assessed on communal land appeared vigorous. A similar trend was found with the
 1695

status of trees that had been harvested or subjected to natural disturbance, with the
exception of W. salutaris growing in protected area B, where individuals appeared
prone to disease after elephant and fire damage. Although the high numbers of
people participating in the medicinal trade in South Africa are daunting, experience
in Kenya, where approximately 60,000 woodcarvers are involved in carving co-
operatives, has shown that it is possible to initiate improved resource management
strategies with large numbers of resource users (Cunningham 2000). Traditional
healers, vendors and traders in southern Africa have proven more than willing to
cultivate valued plants. In particular, communities living in communal areas in
which W. salutaris is growing should be encouraged to propagate this species, both
for their own needs as well as to meet future requests by outside harvesters. The
forestry sector could contribute to the protection of the populations growing on
their plantations by establishing orchards of medicinal species such as W. salutaris,
Catha edulis, Rapanea melanophloeos and Bersama tysoniana, as well as providing
subsistence sector resource users with propagation material. The improvement of
harvesting techniques is also important, accompanied by consistent monitoring. In
1992, Cunningham reported that all the large W. salutaris individuals (>5 cm DBH)
assessed outside protected areas in KwaZulu-Natal were heavily debarked. Today
this species is extinct outside conservation areas in this province (Mander 1998). If
we are not able to improve the management of a fast growing, resilient species such
as W. salutaris, how are we going to conserve the many slow growing medicinal
species facing similar pressures?

Acknowledgements

This project was one component of The Green Trust funded Kruger National Park
Traditional Healers Programme. South African National Parks and the University of
the Witwatersrand are thanked for logistical support. The following people are
thanked for assistance with field surveys: Mr. Mervyn Lötter, Ms. Sonnette
Krynauw, Mr. Marc Stalmans, Ms. Jenny Neuhingham, Mr. Jerry Theron, Mr. Nick
Zambatis, Mr. Million Khoza, Mr. Peter Scott, Mr. Louis Luke, Mr. Dup Du Plessis,
Mr. Elijah Lekhulene, Ms. Josephina Hloliwe Silinda, Mr. Jameson Mthimkhlulu,
Mr. Peter Hume, Mr. Dale Guthrie, Mr. Warren McLelland, Mr. King Khoza, Mr.
Andries Mathonsi, Mrs. Angel Ndlovu and Mr. Mashale. Ms. Zodwa Mashele
provided invaluable assistance in the field.

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