RESERVE SYSTEMS FOR LIMESTONE ENDEMIC FLORA

OF THE CAPE LOWLAND FYNBOS:

ITERATIVE VERSUS LINEAR PROGRAMMING

TECHNIQUES

Christopher K. Willis

Percy FitzPatrick Institute of African Ornithology

University of Cape Town

Rondebosch, 7701

Cape Town, South Africa.

Supervisors: Prof Richard Cowling, Dr Mandy Lombard

Thesis submitted in partial fulfilment of the requirements for the degree of Master of

Science in Conservation Biology, University of Cape Town.

June 1994

The copyright of this thesis rests with the University of Cape Town. No

quotation from it or information derived from it is to be published

without full acknowledgement of the source. The thesis is to be used

for private study or non-commercial research purposes only.

Univers

ity of

Cap

e Tow

n

Fonnat: Biological Conservation

RESERVE SYSTEMS FOR LIl\1ESTONE ENDEMIC FLORA OF

THE CAPE LOWLAND FYNBOS: ITERATIVE VERSUS LINEAR

PROGRAMMING TECHNIQUES

Christopher K. Willis

FitzPatrick Institute, University of Cape Town, Rondebosch 7700, South Africa

ABSTRACTi

"A comparj~on was made between two iterative algorithms and linear programming in determining the

ideal reserve configuration/or the limestone endemicjlora ofthe lowlandfynbos, Cape Floristic Region,

South Africa. Owing to thehighdegree oflocal endemism amongst theflora, thethree techniques sel~cted

the same number ofreserve sites, although a slightly different spatial configuration. ExceptforDe Hoop

andPauline Bohnen Nature Reserves, theexisting reserve configuration is inadequatefor theconservation

of limestone endemic plants. Recommendations are made as to where potential reserve sites should be

located, and which approaches should be developed to select reserves.

Running title: Conservation of limestone endemic flora, Cape Floristic Region.

Key words: Lowland fynbos, limestone, endemism, reserve selection algorithms, conservation.

INTRODUCTION

The Cape .Floristic Region (CFR) of South Africa is the smallest of the world's six floristic regions,

covering an area of approximately 89·000 km2• It has one of the highest known levels of plant species

endemism of any continental tropical or temperate area (Cowling & Holmes, 1992a). The region includes

seven endemic plant families, 198 endemic genera, and more than 8 550 vascular plant species of which

about 73% are endemic (Moll, 1990)~ The CPR has been, and is being, considerably transformed by

pastoral, agricultural, and urban development, and invasive alien plant encroachment (Richardson et al.,

1992). Indeed, the number of threatened vascular plants (ca 1500, or 17% of the entire vascular flora

of the region) in the CFR is,the highest recorded in the world,and is more than the entire flora of the

British Isles (Myers, 1990). In terms of plant endemism, Myers (1990) regards the CFR as one of the

"hottest" of all hot-spots. Considering the deterioration of natural vegetation, the present population

growth rate and development pressure, there is an urgent need to conserve unique fynbos vegetation

within a representative reserve configuration. Fynbos is the local term for the heath-like shrublands of

the CFR, whose distribution is determined both by soil nutrients and soil moisture (Cowling & Holmes,

1992b).

Within the south-western part of the CFR, the Agulhas and Riversdale Plains comprise a gently

rolling coastal lowland landscape dominated by fynbos shrublands whose floristic pattern is under strong

~edaphic control (Thwaites & Cowling, 1988; Cowling, 1990; Rebeloet al., 1991). Cowling et al. (1992)

have term~e coastal region of the southern Cape, which includes limestone-associated colluvial sandsA

and calcareous dunes, the Bredasdorp-Riversdale centre ofendemism (BRC) (Fig. 1). Limestone fynbos,

because' of the highly specialized and restricted nature of the communities, represents one of the most

threatened vegetation types in the CFR (Hilton-Taylor & Ie Roux, 1989).

Edaphicallyunusual substrata such as gypsum, serpentine, limestone, granite, dolomite and

quartzite provide a strong selective force for the evolution of neoendemic plant species throughout the

world (Kruckeberg & Rabinowitz, 1985; Kruckeberg, 1986; Matthews et al., 1993). Evidence for a large

neoendemic flora in the BRC, relative to the montane centres of endemism within the CFR (Oliver et al. ,

1983), arises from the fact that mostof the area was inundated by a marine transgression in the early to

mid-Pliocene (4 Myr B;'P.) (Thwaites & Cowling, 1988). The topography in the limestone landscape is

complex, the limestone hills or 'islands' rise to a maximum of 500 m above the coastal plain and have

2

small to large vertical cliff faces and a diversity of slope and aspect combinations. Soils on the limestone

bedrock areshallow, well-drained, calcareous sands (Cowling & Holmes, 1992a) with high organic

carbon and nitrogen content (Mustart & Cowling, 1993). Colluvial sands which surround the limestone

hills are deep, weakly acid and relatively infertile (Cowling, 1990; Mustart & Cowling, 1993). Further

details on the geology, geomorphology and soils of the BRC are given in Malan (1987), Thwaites (1987),

Rogers (1988) and Thwaites and Cowling (1988).

Reserve selection algorithms

Areas of protected natural habitat are the backbone of any strategy to maintain regional biological

diversity, which means they should include examples of as many natural features (species, communities,

landscapes) as possible. In reality, protected areas in South Africa have not been selected with this

objective in mind, but rather on an opportunistic or ad hoc basis (Siegfried, 1989; Lombard et al., 1992).

The selection is subjective, often depending on available land, and is influenced strongly by perceived

threat. Margules et al. (1988) have proposed a simple heuristic algorithm to identify the 'minimum' set

of sites in a given region, which together sample maximum biological diversity. This set of sites has been

termed a "nominal core reserve network" (Nicholls & Margules, 1993) or a "core natural area network"

(Margules & Meyers, 1993). Various applications of this or similar algorithms have been used in

conservation'biology(Pressey & Nicholls, 1989a, 1991; Vane-Wright et al., 1991; Bedward et al., 1992;

Rebelo & S~fried~ 1992; Margules & Meyers, 1993). Collectively, these heuristic algorithms have been

.4called iterative selection procedures because they iterate through a list of candidate sites, choosing the

best candidate at each step according to explicit rules (Nicholls & Margules, 1993). The 'non-negotiable'

configuration is seen as the 'minimum' set; it is the core of protected natural areas on which to build

regional nature conservation plans that may include more reserves as well as outside-reserve management

that promotes conservation goais.

Criticisms of heuristic algorithms have indicated that the solutions may not necessarily produce

the true mathematical 'minimum' or 'optimum' solution to a reserve problem. Underhill (in press) has

indicated thatalthoughiterative-algerithms raay produce the correct solution, they may also produce

suboptimal results. Optimality is, however, only one of the goals of the algorithms. Other advantages

in using heuristic procedures include being explicit (so reserve configurations chosen are more easily

3

defended), efficient and flexible (Margules et al., 1991; Nicholls & Margules, 1993). Using a

hypothetical example, Underhill (in press) has shown that the problem of minimizing the number of

reserves to conserveevery species is a straightforward application of a standard technique in operations,

namely integer linear programming. To our knowledge, no comparison of iterative algorithms and linear

programming, using a real world data set, has been published to date.

In this study we asked the following questions: (i) how do iterative algorithms and integer linear

programming compare in terms of efficiency and reserve location? (ii) how does the existing protected

area configuration compare with the proposed configuration?, and (iii) what approaches should be

developed to select reserves and to sustain them?

METHODS

Data base

Data on the distributions of 110 vascular plant taxa (species and intraspecific variants, henceforth referred

to as species) endemic to the limestone substrata in the BRC were obtained from several sources. These

included: PRECIS (pretoria National Herbarium Computerised Information System), a computerized data

bank managed by the National Botanical Institute (Gibbs Russell, 1985a; Gibbs Russell & Gonsalves,

1984); post-1960 monographs; Bond and Goldblatt's (1984) catalogue ofthe Cape flora; the Protea Atlas

Project database up to October 1993; the ISEP (Information System for Endangered Plants) data base,

managed b~Cape Nature Conservation, Jonkershoek; herbarium specimens in the Bolus Herbarium,

'!Universitf~of Cape Town; and the Compton Herbarium, Kirstenbosch National Botanic Gardens. This

information was supplemented by personal collections and observations made by professional botanists

familiar with the limestone flora.

Rebelo and Cowling (1991) have found a 7% error associated with Bond and Goldblatt's (1984)

catalogue, and 26-33 % error associated with the PRECIS data base, with endemic species under-

represented, for the CFR. For this reason, obvious errors in distributional data obtained from the various

sources were omitted. Additional distributional data were obtained from observations made and herbarium

specimens collected.duringa.field survey throughout the study area. During the survey, 15 areas were

surveyed for the presence of limestone endemics (Fig. 1). At each site, effort was made to sample the

range of physiognomic and topographical variation (such as north and south-facing slopes, cliff faces,

4

ridges, plateaus, recently burned and old veld). As an indication of how representative the sample was

at each site during the field survey, 38 out of an expected 58 (65.5%) limestone endemics were found

in the eighth-degree grid cell 3420ADD (part of De Hoop Nature Reserve). Although this value cannot

be extrapolated to other areas owing to topographical and physiographical variation between sites, it

nevertheless provides some indication of the robustness of the data base, since the missing species, such

as post-fire ephemerals, may be rare. Each site sampled during the survey was scored and ranked in

terms of its diversity in pre-defined categories of topography and soil types. The rank assigned to each

of the tied ranks was the mean of the ranks that would have been assigned to these ranks had they not

been tied (Zar, 1984: 141).

All distribution records (presence, not abundance) were plotted with reference to an eighth-degree

grid system (= cells, 11.5 Ian x 13.85 Ian). Several studies concerning the prioritization of conservation

areas and protection of the diversity of fynbos vegetation in the CFR have also used an eighth-degree

scale (Rebelo & Siegfried, 1990, 1992; Rebelo, 1992a,b; Rebelo & Tansley, 1993). This is a finer scale

than that generally adopted by botanists in southern Africa (Gibbs Russell, 1985b). The data base

comprised 110 species by 53 cells, and its accuracy was verified at an eighth-degree scale by Chris

Burgers (Cape Nature Conservation, Jonkershoek) using ARC/INFO version 3.4D+, a geographical

information system (GIS; Environmental Systems Research Institute, Redlands, California).

Iterative rrrve selection algorithms1 AThe algorithms developed by Margules et al. (1988) and the updated version of Nicholls & Margules

0993) were applied to the data base and compared. The latter 'adjacent' algorithm differs from the

former ('non-adjacent' algorithm) in that it is constrained by having to select sites that are close to one

another, when possible. It therefore attempts to identify a final configuration of areas that occur within

clusters, as opposed to being spatially independent of one another (Lombard et al., in press).

Linear programming algorithm

A non-heuristic linear programming algorithm (specifically, '0-1 integer programming') also was applied

to the data base. The 'public domain linear programming package LP_SOLVE (Michel Berkelaar,

Eindhoven University of Technology, Dept of Electrical Engineering, Design Automation Section, PO

5

Box 513, NL-5600 MB Eindhoven, Netherlands), which uses the mathematical branch-and-bound search

process, was used in the analysis. The method finds an "optimal solution" (see Underhill, in press) to

integer linear programming problems (Zionts, 1974; Nemhauser & Wolsey, 1989). The method has been

used by Cocks & Baird (1991) and Setersdal et al. (1993) to select potential nature reserves, and

minimises the value of an 'objective function' (Zionts, 1974).

Within the present study, the heuristic and non-heuristic algorithms were required to represent

each species one (xl), two (x2), three (x3), four (x4) or five (x5) times in the protected area

configuration. Efficiency of the reserve selections, as defined in equation 1 (from Pressey and Nicholls,

1989b), is a useful measure for comparing selection techniques. In equation 1, X is the number of cells

needed to protect all species a required number of times, and T is the total number of cells in the data

base (n = 53). Efficiency increases as X decreases.

Efficiency = 1 - (X/T)

Efficiency of the three methods was compared using equation (1).

(1)

Comparison with existing priority areas

Based on the' distribution of Proteaceae species, Rebelo and Siegfried (1990, 1992) have produced ideal

nature reserte configurations fot the CFR, using an eighth-degree grid. A comparison was made between

<1the ideal cinfiguration produced in this study, based on the distribution of limestone endemics, with that

o,t Rebelo and Siegfried (1990, 1992) for the same area.

RESULTS

Reserve selection algorithms

Each algorithm was equally efficient for each representation from xl to x5 (that is, the three algorithms

selected the same number of cells for each representation). For one representation of each endemic

species only (13 cells),theefficiency of each algorithm was 0 ..755. For five representations (38 cells),

efficiency was 0.283. Of the 13 cells (24.5% of the area covered by limestone endemics in the BRC)

selected by the three algorithms for one representation only, 11 cells (85%) were the same for each

6

algorithm (Fig. 2). In a comparison between linear programming and the adjacent algorithm, 12 cells

(92%) were the same.

Fig. 3 shows which of the selected cells contain existing protected areas (state forests and public

nature reserves). It should be noted that the presence of a reserve within a cell does not always ensure

that all taxa within the cell are adequately protected, especially with respect to limestone endemics. In

some cases, such as in the Hagelkraal and Bredasdorp areas, the existing reserves constitute only small

areas within the cells and do not include any limestone. Other cells (such as in De Hoop Nature Reserve)

fall entirely within reserves (see Fig. 1 for locations). For xl - x5 representations, between 47% and

62% of the selected cells presently contain reserves. In the case of the xl representation, 54-62% of the

selected cells contain reserves (that is, only five or six cells lack any protected natural habitat, depending

on the algorithm chosen). Of the 13 cells selected by the three algorithms for one representation only,

10 of these cells are irreplaceable if the entire limestone endemic flora is to be conserved (Fig. 4). The

areas that contain two or more unique species are Hagelkraal (four) and De Hoop Nature Reserve (three)

(Fig. 4). The importance of these sites is consistent with the rankings recorded for topographic and soil

diversity in these areas (fable 1).

, Although the selection algorithms are defined by a number of representations desired for each

species, the selected' set of cells will contain many more representations of some species than is required.

For 'example, most widely distributed species will be represented in many of the selected cells,

irrespectiv~1how many times they are required to be represented. Fig. 5 shows a frequency distribution

hf the number of limestone endemics that occur more than once in cells selected by the three algorithms,

where only one representation of each species is required. More than half of the 110 species was

represented at least three times, and more than one third of the species was represented at least five times

(irrespective of algorithm used). Summing the total species representations in Fig. 5 shows thatthe non­

adjacent and linear programming algorithms were equally successful (503 total species representations)

(Fig. 6), whereas the adjacent algorithm is only slightly less successful (492 total species representations).

However, this pattern was not repeated for the x2, x3, x4 and x5 representation analyses. For these, the

non-adjacent.and.adjacent algorithms were consistently more successful than linear programming (Fig.

6). In terms of total species representations, the three algorithms were not markedly different from one

another.

7

Comparison with existing priority areas

The only area of overlap between this study and the ideal nature reserve configuration of Rebelo and

Siegfried (1990, 1992) for the Proteaceae was the Hagelkraal area (Fig. 7).

DISCUSSION

A comparison of methods

This study is the first example in an endemic-rich area of the world of a comparison between heuristic

and non-heuristic reserve selection algorithms using a real world data base. Underhill (in press) considers

the non-adjacent and adjacent heuristic algorithms, developed by Margules et ale (1988) and Nicholls and

Margules (1993), respectively, as "suboptimal" reserve selection algorithms. The present study has shown

that using the limestone endemic data base, linear programming is no more efficient (as defined to mean

fewer cells needed to represent all species) at selecting a configuration of reserves than either the non­

adjacent or adjacent algorithms. Each algorithm selected the same number of cells, although in a

marginally different spatial configuration. Heuristic and non-heuristic solutions can be extremely sensitive

to starting conditions. The main reason for the similarity between methods used here is the relatively

large percentage of irreplaceable sites within the study area, as a result of high levels of local endemism

within the limestone flora. The three algorithms were thus forced into selecting a similar set of cells. A

more reliable comparative test of these three algorithms should use a data set which contains many

widespread,d fewspatially restricted species.

Efhciency of the three reserve selection algorithms used in this study is less than that found in

other studies (pressey & Nicholls, 1989b; Rebelo & Siegfried 1992; Lombard et al., in press). Reasons

for this may be as follows: efficiency (a) is highly dependent on the size of the geographical units used

in the selection exercise, and (b) may also vary with identical selection units according to whether the

target features are, for example, a few widespread and co-occurring vegetation types or many plant

species including narrow endemics which rarely co-occur (as shown in this study) (pressey et al., 1993).

The 13 cells (24.5% of the area) identified in this study represent the smallest number of sites required

to ronservealilimestoneendemicsinthe lowland fynbos. For comparison, published examples of the

minimum area required to conserve all species range from 11.7% for forest areas in southeastern

8

Australia (Nicholls & Margules, 1993) to 70% of remaining native vegetation in the croplands of South

Australia (Margules; 1989).

In terms of spatial configuration, main clusters of areas selected by the three algorithms include

the Hagelkraal-Awila area, the Soetanysberg, the Struisbaai area, Waenhuiskrans area, De Hoop Nature

Reserve, Wankoe-Blombos area and the Stilbaai-east area. The Hagelkraal area and De Hoop Nature

Reserve are particularly important, considering that they both contain more than one unique limestone

endemic. In addition to unique limestone endemics, .Willis et al. (Bot. J. Linn. Soc., submitted) have

shown that De Hoop represents the 'hotspot' in terms of limestone endemic species richness, and that

Hagelkraal, relative to species richness, contains a higher than predicted number of critically rare Red

Data Book limestone endemics.

While heuristic algorithms and mathematical programming solutions can be valuable as.indicative

tools, they do have limitations for real world planning. For example, while they can usefully indicate

how much land or how many sites are needed to achieve a reservation goal, they do not reveal much

about the potential value of all the sites in a study area. An advantage of iterative algorithms.is, however,

flexibility. Aspects such as socio-economic factors and neighbourhood effects can be incorporated into

iterative algorithms, although this was not done in our study. Stochastic dynamic programming (H.

Possingham, personal communication), which can be used to take uncertainties into account, has been

suggested as 'an alternative approach to the reserve selection problem.

Ba~ on the results produced by the algorithms, many reserves are required in the BRC owing

1to the higltpercentage of narrow or local endemism in the area. The existing protected area configuration

i~t,inadeCluate for the conservation of limestone endemics. Reasons for this are as follows: (a) apart from

De Hoop, De Mond and Pauline Bohnen nature reserves, most of the protected areas are coastal state

forests which do not contain limestone endemics and have been planted with invasive alien acacias to

stabilize drift sand; and (b) limestone endemics have very localized habitats, and have not been

considered in the proclamation of nature reserves. The proclamation of De Hoop Nature Reserve was,

for example, not based on floristic criteria. However, the importance of De Hoop Nature Reserve to the

conservation of the limestone endemictlora of the Cape lowland fynbos contradicts the statement

previously made by Rebelo and Siegfried (1990) that "De Hoop Nature Reserve might be a prime

9

candidate for Siegfried's (1989) proposal for the deproclamation of certain nature reserves and the

exchange of their land for new reserves" .

Comparison of the spatial configuration of reserves based on the distributional data of Proteaceae

(Rebelo & Siegfried 1990, 1992) with that obtained in this study (using the same scale), indicate that the

Proteaceae are not as representative of the diversity of fynbos vegetation, as is indicated by correlations

based on species richness at the quarter-degree scale (Rebelo & Siegfried, 1990). These results emphasize

the dangers inherent in prioritizing areas for protection using data from only a single family. In terms

of ideal reserve configurations, any areas of overlap among sites selected by reserve selection algorithms

for different taxa, such.as in the Hagelkraal area, should be given special attention in reserve design. In

addition to limestone endemics, the Hagelkraal area also includes acid substrata with many endemic

Proteaceae. The state-owned protected area in this part of the BRC is Walker Bay State Forest, a coastal

state forest which was historically planted with Australian invasive acacias in order to stabilize the sand

dunes. Considering that Walker Bay State Forest contains neither limestone endemic vegetation nor

endemic Proteaceae, there is an urgent need to conserve the topographical complexity and vegetation

associated with the limestone hills in the Hagelkraal-Awila area and to prevent the spread of alien acacias

into these areas.

~

Towards a reserve configuration

There is a~ to investigate all'cells selected in the ideal reserve configuration in terms of the followingA.

criteria: degree ofdisturbance, land use in adjacent habitats, presence ofother substrata, size of limestone

outcrops and land ownership. Reserves should be selected in limestone areas that have not been heavily

invaded by alien vegetation, and include intact habitats adjacent to. limestone patches. By including

adjacent undisturbed habitats and different soil types, the beta diversity of the reserve would be enhanced

due to an increased number of habitats and the turnover of species among them. Shmida and Wilson

(1985) have suggested that habitat diversity is the ultimate determinant of beta diversity. Rates of species

turnover will, however, differ depending on the historical processes associated with the evolution of

habitatspecialists(C()Wlillgefill. , 1992). Reserves containing complex mosaics of edaphic environments

would represent important selective regimes and be conducive to rapid speciation in these areas.

10

The size of reserves was not specifically addressed in this study, as "there is little point in

prescribing minimum or optimal reserve sizes before a configuration of reserves has been designated"

(Rebelo & Siegfried, 1992). The area-specific results of an empirically based study on the limestone

fynbos 'islands' of the Agulhas Plain have, nevertheless.' shown that the minimum reserve size needed

to avoid species losses (including local endemics) in the region is about 4-15 ha (Cowling & Bond,

1991). This is encouraging for the conservation of diversity in south-western Cape lowland fynbos where

natural vegetation is confined to scattered fragments, and where 90% of existing reserves in the south-

western Cape lowland fynbos are larger than 15 ha (Jarman, 1986). Because the limestone 'islands' are

exposed to the same disturbance regimes as, and share pollinators and seed dispersers with, acid sand

fynbos (Cowling & Bond, 1991), these minimum areas are only applicable to reserves in which

disturbance regimes are maintained (specifically fire), and which have access to pollinators and seed

dispersal agents (Rebelo 1992b).

Managers and landowners within the lowland fynbos should adopt an integrated landscape

management approach (Hobbs, 1993; Hobbs et al., 1993; Saunders et al., 1993), which links the

disciplines of landscape ecology and conservation biology, and entails the cooperation between different

managers and owners. In order to conserve the remnant limestone fynbos patches and ecosystem

processes within the BRC, there is a need to recognise the impact of the surrounding landscape elements

bnthe patches, and to develop a holistic approach, even though it may involve many landowners and

manageme~/bodi~ .. Within the integrated landscape management approach, different interests and

4managemeit·activities need to be considered and accommodated in the lowland fynbos. These include

c9nservation, ecotourism, wildflower harvesting, limited grazing and appropriate fire management.

Conservation management within reserves must be linked with management outside reserves, which seeks

to reduce or reverse the current trends of landscape degradation. A large portion of the BRC resides in

private hands or under the control of local authorities, and the local communities should become involved

with its management. Providing that a regional perspective can be built into local actions, and that a

conservation ethic can be built up, devolution of responsibility for conservation to a local level may be

more successfuLthancurrent centralised structures (Hobbs et al., 1993).

Landscapes within the BRC are becoming increasingly fragmented, and there is an urgent need

for conservation biologists to move towards reconciliation with landowners. This could be promoted

11

within the lowland fynbos through the proclamation of private nature reserves and/or contractual national

parks. De Hoop Nature Reserve and Hagelkraal should serve as the core areas for the conservation of

limestone endemics in lowland fynbos. Other areas within the BRC that would qualify for contractual

parks include the Soetanysberg-Geelrug, Struisbaai, Waenhuiskrans, Vermaaklikheid-Blombos and

Stilbaai-east areas.

In conclusion, results presented here should be seen as the first stage in the development of a

regional approach to identifying areas for protection of limestone endemic flora of the Cape lowland

fynbos. Limestone endemics are only a very small portion of the total biodiversity (defined as the entire

range of regional biological variation, both within and between species) present within the CFR, and if

the entire range of species is to be conserved, then the present data base needs to be expanded to

encompass a larger sample of the regional biota. Several studies have shown that patterns of species

richness and endemism differ both between taxa (Ryti & Gilpin, 1987; Pagel et al., 1991) and within taxa

(Siegfried & Brown, 1992). This study thus forms one small piece in the jigsaw of conserving

biodiversity (both patterns and processes) within the CFR. Regional diversity and regional configurations

are emphasized because it is the regional complement of species which should be represented in reserves.

Compromises will have to be made and hard decisions will have to be taken concerning which taxa or

functional groups ate to be used in reserve design. Managers and landowners must take cognizance of

"the fact that 'the long-term conservation of the exceptional limestone endemic flora in the Cape lowland

fynbos wil~e achievable only through the adoption of an integrated landscape management approach to

" Athe reglorf

ACKNOWLEDGEMENTS

My grateful appreciation is expressed to supervisors, Richard M. Cowling and Amanda T. Lombard for

their guidance and encouragement. Fieldwork was greatly facilitated through the enthusiastic assistance

of Barry J. Heydenrych (Flora Conservation Committee, Botanical Society of South Africa) and Chris

J. Burgers (Cape Nature Conservation, Jonkershoek). The Director (Research) of the National Botanical

Institute is thanked for the use of distributional and habitat data produced by the Pretoria Nationa

Herbarium Computerized Information System (PRECIS). I gratefully acknowledge the assistance of

Jemery Day and Hugh Possingham (Department of Applied Mathematics, University of Adelaide,

12

Australia) for running the linear programming package LP SOLVE, Nick Nicholls (CSIRO,. Canberra,

Australia) for running the heuristic algorithms, and Andrea Plos for her help with the preparation of the

illustrations. My sincere appreciation is extended to the Institute for Plant Conservation (University of

Cape Town), University of Venda, Foundation for Research Development and Flora Conservation

Committe of the Botanical Society of South Africa for their financial support during the study. Richard

Cowling, Amanda Lombard, Chris Burgers, Barry Heydenrych and Peter Ryan provided valuable

comments on earlier drafts of this manuscript. Lastly I would like to thank my family and my wife,

Carla, for their understanding and support throughout the study. Co-authors on this paper are, in order:

Amanda T. Lombard, Richard M. Cowling, Barry J. Heydenrych and Chris J. Burgers.

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17

Fig. 1.

Fig. 2.

Fig. 3.

Fig. 4.

F· S'ig, ~'

Fig. 6.

Fig. 7.

FIGURE LEGENDS

Map of the study area, showing the approximate boundary of the Bredasdorp­Riversdale Centre (shaded) which includes limestone fynbos, and the locationof sites sampled during the field survey: 1, Korsika; 2, Hagelkraal; 3,Soetanysberg; 4, Heuningrug; 5, AgulhaslStruisbaai; 6, Kars River; 7, DeHoop Nature Reserve; 8, Vermaaklikheid; 9, Arbiterskop; 10, Kransfontein;11, Melkhoutfontein; 12, Pauline Bohnen Nature Reserve; 13, Canca seLeegte; 14, Gouriqua; 15, Kalkberge. The insets show the position of thestudy area relative to Africa and South Africa. The map is overlaid by aneighth-degree grid system.

The distributions of reserve sites (solid cells) selected by the reserve selectionalgorithms, for one representation of each limestone endemic species only. (a)Non-adjacent algorithm; (b) adjacent algorithm; (c) integer linearprogramming. Shaded cells represent those cells that contain limestoneendemics but were not selected by the respective algorithms.

The distributions of reserve sites selected by the reserve selection algorithms,in relation to existing protected areas within the limestone fynbos. Solid cellsdenote areas that contain existing reserves (public nature reserves and/or stateforests), whereas shaded cells do not contain reserves. (a) Non-adjacentalgorithm; (b) adjacent algorithm; (c) integer linear programming.

Reserve sites that cannot be substituted if they are to preserve their constituentspecies (irreplaceable sites). The two solid cells uniquely preserve four and

< three unique species respectively, whereas the shaded cells uniquely preserveonly one species.

Total number of representations of limestone endemics in three differentreserve systems selected by the three algorithms, The three reserve systemsare shown in Fig. 2. The graph depicts the case where only one representationof each species is required.

Comparison of the sums of the total species representations using the threealgorithms.

Comparison of the areas selected for reserves in this study with those in thestudy area (Fig. 1) selected by Rebelo and Siegfried (1990, 1992) for the CapeFloristic Region, based on the distribution of Proteaceae species. The solidcell represents the area of overlap between the two studies whereas shaded~llsr~pJ:'~~Ilttllose cells selected. in Rebelo and Siegfried (1990, 1992) thatwere not selected in this study. The striped squares represent those selectedin this study (all three methods combined) that were not selected by Rebeloand Siegfried (1990, 1992).

ooN

190 E(a)

~(c)

Fig. 2.

/'"

jj1~111j1111~jJ(: ~-~

r-5 r--~r-,

./. 1~j1~j1j11j1~11 ~11111j11~j1~11 j'--...11~~111~111~11

;~

1~11~11~111~11~ ~~~i~::~~11~11~

(a) 190 E

(b)/"

;1j~~~1I~1111J(: ~-I---...

h5 --~r-,/ ~~j1~111~1~1~1~ ~1~1~1~1~1j1~1~ ./-

j~1~1~j1j~1j11j j~l~j~j~j~jjj~~IV

~~;~~i;;Ij~j~~

(c) 1/Ii

/'

~j~~j~~~1~~jj~~1J(: >- I.- .-'-:-.

l5 -........f--..K~j11~1~~~I~~~~1./. j~111~~j~111~; ./.........

~111111111j11~1:rv

~;;~i~:~~~11j111~,

Fig. 3.

II

I~

11\oO-+--t--+--f---j-------f:=:'~___\__+______l

,C'l

(

po

Table 1. Habitat (topographic) diversity and soil types present in selected sites sampled during the field survey within theBredasdorp-Riversdale centre of endemism.

il,

II,.s::

II II I IHabitat .diverslty"~ , Soilst Sum Rank

I I R F P St C ,N So ~c8SITMS~F/sl I I"

Korsika~ • • • • • • • • • • • • 12 1.5

Hagelkraal • • • • • • • • • • • 11 3

Soetanysberg • • • • • • • • • 9 5

Heuningrug • • • • • • • 7 11.5,

StruislAgulhas • • • • • • • 7 11.5

Kars River • • • • • • • 7 11.5

DeHoopNR • • • • • • • • • • • • 12 1.5

Vermaaklikheid • • • • • • • • • 9 5

Arbiterskop • • • • • • • 7 11.5

Kransfontein • • • • • • • • • 9 5

Melkhoutfontein • • • • • • • • 8 7.5

Pauline Bohnen NR • • • • • • • 7 11.5

Canca se Leegte • • • • • • 6 15

Gouriqua • • • • • • • 7 11.5

Kalkberge • • • • • • • • 8 7.5

• R = Ridges; F = Flats; P = Plateau (limestone); St =Steep slopes; C = Cliffs; N = North-facing slopes; So = South-facing slopes.t Sh = Shale/loamy soils (transition to Renosterveld); D = Dune sands (recently formed); Cas = Colluvial acid sand;TMS = Table Mountain sandstone; CI = Colluvium from limestone; F/S = Ferricrete/silcrete.

35

30

o.! 25.e(I)Q.o 20....o'-(I) 15.cE~ 10Z

5

o

~

<~

.. ~ Non-adjacent

. [JAdjacent

• Linear programming

1 2 3 4 5 6 7 8 9 10 >10

Total number of representations

Fig. S.

1200 ..U) I

"!»

S10501053

~

.- I,c~... ,

as... 900e(I)

-0750(I)

l-e.(I)

600I-

0(I)-- 450e(I)Q.0 300-as...0 150t-

O1 2 3 4 5

Number of representations

~ Non-adjacent [JAdjacent • Linear programming

Fig. 6.

I,~

o~ +-----j---I-~I+__-I___+_-_+_-t_______J

N

oo +----f--+---+-----+~~~~~--1N

Format: Botanical Journal of the Linnean Society

Patterns of endemism in the limestone flora of South

African lowland fynbos

CHRISTOPHER K. WILLIS

FitzPatrick Institute. University of Cape Town. Rondebosch 7700. South Africa

vi.~..

Running title: Patterns of endemism in the limestone flora of lowland fynbos.

WILLIS, C.K., 1994. Patterns of endemism in the limestone flora of South African lowland fynbos.

Taxonomic and biological aspects of endemism and Red Data Book status were studied amongst the

limestone endemics of the lowland fynbos, Cape Floristic Region, South Africa. Of the 110 limestone

endemics, 56.4% were regional endemics, 41.8% were local endemics and 1.8% were endemic to the

Cape Floristic Region. Families which were over-represented in terms of endemics included the

Ericaceae, Fabaceae, Polygalaceae, Rutaceae and Sterculiaceae. The Restionaceae was the only under­

represented family. Local limestone endemics were not significantly different from regional endemics in

terms of biological attributes. An analysis of the frequency of biological traits associated with the

limestone endemic flora enabled the establishment of a biological profile of a limestone endemic: a dwarf

to low shrub with soil-stored seeds which are ant or wind dispersed, and/or form symbiotic relationships

with microbes. In terms of species richness of limestone endemics, De Hoop Nature Reserve was the

'hotspot' within the region. Relative to total species richness, the Hagelkraal and Stilbaai areas contained

higher than predicted numbers of rare species. These areas require urgent attention if the unique floral

diversity associated with limestone substrata within the Bredasdorp-Riversdale centre of endemism is to

be conserved.

ADDITIONAL KEY WORDS:- Cape Floristic Region - lowland fynbos - limestone - endemism ­

conservation

2

CONTENTS

Introduction

Study area

Geology, geomorphology and soils

Climate

Limestone fynbos

Methods

Categories and centres of endemism

Data collection

Taxonomic aspects of endemism

Biological aspects of endemism

Nodes of rare species relative to species richness

Results

Taxonomic aspects

Biological aspects

Rare species

Discussion

... Taxonomic aspects of limestone endemism

Biological aspects of limestone endemism

Rare.limestone endemics-t.

Conclusions

Acknowled~mentS~

References

AppendEc 1

3

INTRODUCTION

Within the southwestern corner of Africa, the Cape Floristic Region (CFR) represents the

smallest of the six floral kingdoms of the world (fakhtajan, 1986). Covering some 0.04% (89 000 km")

of the earth's surface, it contains ca 8 550 species of vascular plants, of which 73% are endemic to the

CFR (Moll, 1990). Of the 957 genera, 198 are endemic and seven families, namely the Bruniaceae,

Penaeaceae, Grubbiaceae, Roridulaceae, Retziaceae, Stilbaceae and Geissolomataceae are endemic

(Goldblatt, 1978). The CFR is dominated by fynbos, a sclerophyllous, heath-like shrubland associated

with nutrient-poor soils which cover most of the region (Cowling & Holmes, 1992a). These shrublands

are fire-prone and usually burn at six to 40 year intervals (Cowling & Holmes, 1992b). The coastal

lowland areas of the CFR represent one of the most threatened regions of natural vegetation owing to

intensive agriculture, urbanization and alien plant encroachment (Jarman, 1986). Amongst the lowland

flora, limestone fynbos communities, because of their edaphic specialization and restricted nature, are

particularly vulnerable and contain many threatened endemic species (Hilton-Taylor & Ie Roux, 1989).

Despite the flora being relatively well studied, patterns and determinants of endemism have been

poorly examined in the CFR (Cowling & Holmes, 1992a). For conservation management, it is important

to know whether or not an endemic flora constitutes a random assemblage with respect to taxonomy,

habitat preference and biological attributes. If not, then the peculiar characteristics of the endemic flora

can be used as a guide for management. Unfortunately, studies that seek to characterize endemics in

terms-of these attributes represent a major gap in the literature for all endemic-rich areas (Cowling,

Holmes & Rebelo, 1992)., Although certain studies in the lowland floras of the CFR have shown that

most endemics ate edaphic specialists, and that certain substrata ~.g. limestone) harbour-,(

disproportionally high numbers of endemics (Cowling & Holmes, 1992a; Cowlinget al., 1992), no

studies havti'ooked. at these ed~phic specialists~ see This study therefore represents the first attemptA .

at analyzing and characterizing endemic vascular plants restricted to limestone substrata within the Cape

lowland-flora. Based on the distributions of limestone endemics within the lowland flora, Willis et ale

(submitted) have attempted to determine the ideal configuration of reserves for their conservation.

We addressed the following questions: (i) how many limestone endemics are there? (ii) how many

of these species are CFR, regional and local endemics? (iii) how many endemics are listed in the Red

Data Book? (iv) what are the patterns of species richness across the landscape? (v) do the limestone

endemics differ in terms of taxonomic and biological traits from non-limestone flora in the Cape

lowlands", and (vi) do local limestone endemics differ from more widespread limestone species in terms

of these traits?

4

STUDY AREA

Geology, geomorphology and soils

The study area comprises a gently rolling, coastal lowlandlandscapetowards the southern tip of

Africa from Hermanus in the west to the Gouritz River in the east, and includes both the Agulhas

(Cowlinget al., 1988) and Riversdalecoastal plains (Rebelo It it., 1991)(Fig. 1). As the entire area was

inundatedby transgressionsduring the mid-Miocene (15 Myr) and the early-mid-Pliocene (4 Myr), most

sediments and soilspostdatethe regression(Hendey, 1983).Despitethe low topographical diversitywhen

compared with the mountainous regionsof the fynbosbiome, the area has numerous contrastingsoil types

and land systems (fhwaites & Cowling, 1988). Table Mountain Group sandstones and quartzites,

Bokkeveld Groupshales, limestones, remnantsilcreteandferricreteoutcropsand calcareous coastaldunes

are all represented in the area. Mio-Pliocene limestones and associated colluvial deposits of the

BredasdorpGroup form distinctiverelief features in the coastal zone, and soils on the limestonebedrock

are shallow, well-drained, calcareous sands (Cowling & Holmes, 1992a). The Riversdaleplain, defined

as the coastal plain south of the Langeberg Mountains between the Duiwenhoks River in the west and

the GouritzRiver in the east, contains thelargest development of Tertiary limestonein the fynbosbiome.

Further detailson the geomorphology, geologyand soils of the area are given in Malan (1987), Thwaites

(1987), Rogers (1988) and Thwaites & Cowling (1988).

Climate

The climateof the area is relativelyuniform. Averageannual temperature ranges between 15 and

J7.4PC;'dependin~ 'on locality. Along the coast mean annual rainfall ranges from 454 mm at Gansbaai

to 400 mm at the Gouritz.River mouth. Higher values wouldbe recordedin the hills but data are lacking.

Rainfall se~nality is typicalof a mediterranean-type climatewith mostof the annualprecipitationfalling

'"in the winter months.

Limestone (ynbos

The term used to describe the vegetation associated with limestone in the BRC has varied

according to the classification used. Moll et ale (1984) described the vegetationas "limestonefynbos" ,

whereas Cowling & Holmes (1992b), based on Campbell (1985), classified the vegetation as "proteoid

fynbos". Leucadendron meridianum I.I. Williams and Protea obtusifoliaBuek ex Meissner dominatethe

limestoneareas within the proteoid fynbos, with Leucospermum truncatum (Buek ex Meissner)Rourke

and LeucadendronmuiriiB...Phillips.co-dominant. in this community where limestone outcrops have

skeletalsoils (Rebelo et ~., 1991).We regard the vegetationendemic to limestonesubstrata as limestone

fynbos. Fifty-four per cent (1 100 km2 of the 2 030 knf) of limestone fynbos occurs in and immediately

5

adjacent to the Riversdale coastal plain (Moll ~ al., 1984; Bohnen, 1986). Details on other vegetation

categories in the area are given in Cowlinget al. (1988) and Rebelo et al. (1991).

METHODS

Categories and centres of endemism

The study was conducted in the Bredasdorp-Riversdale centre of endemism (BRC) (Cowling et

al., 1992), a well-defined centre for the calcicole fynbos taxa confined to the Bredasdorp formation

limestone and associated colluvial deposits which have their maximum exposure in this area (Fig. 1).

Three categories of endemism were recognized in the BRC: (i) CFRendemics confined to the CFR; (ii)

regional endemics confined to Weimarck's (1941) South Western Centre and the BRC (Fig. 1) (Cowling,

et al., 1992); and (iii) local endemics, arbitrarily recognized as taxa confined or nearly confined to

individual centres or subcentres (such as the Bredasdorp Centre) (Weimarck, 1941; Midgley, 1986;

Oliver, Linder & Rourke, 1983). All of the local endemics considered in this study occupy ranges. less

than 2 000 km2 (2.5% of the Cape Floristic Region); some less than 5 km".

Data collection

Data on the distribution of the vascular plant taxa (species and intraspecific variants, henceforth

referred to as species) endemic to limestone substrata in the BRC (Appendix 1) were obtained from

several sources. These included: PRECIS (pretoria National Herbarium Computerised Information

System), a computerized data bank managed by the National Botanical Institute (Gibbs Russell, 1985);

-post.1960monogr~phs; Bond and Goldblatt's (1984) catalogue of the Cape flora; the Protea Atlas Project

data base (Botany Department, University of Cape Town); the ISEP (Information System for Endangered

Plants) dat/base, 'managed by' Cape Nature Conservation, Jonkershoek; herbarium specimens in the~ .

Bolus Herbarium (BOL), University of Cape Town, and the Compton Herbarium (COM), Kirstenbosch

rjational Botanic Gardens. This information was supplemented by personal collections and observations

made by professional botanists familiar with the limestone flora. Rebelo and Cowling (1991) have found

a 7% error associated with Bond and Goldblatt's (1984) catalogue, and 26...33% error associated with the

PRECIS data base, with endemic species particularly under-represented, for the CFR. For this reason,

obvious errors in distributional data obtained from the various sources were deleted.

Additional distribution data were obtained from observations made and herbarium specimens

collected during a field survey throughout the study area. During the survey, 15 areas were surveyed for

the.presence of lilllestone•endemic plant species. At each site, effort was made to sample the range of

physiognomic and topographical variation (such as north and south-facing slopes, cliff faces, ridges,

plateaus, recently burned and old veld) within the area concerned.

6

All distribution records (presence, not abundance) were plotted in accord with an eighth-degree

grid (= cells, 11.5km x 13.85km). Using this information, the accuracy of the herbarium data bases

was verified on an eighth-degree scale by Chris Burgers (Cape Nature Conservation, Jonkershoek) using

ARC/INFO version 3.4D +, a geographical information system (GIS; Environmental Systems Research

Institute, Redlands, California).

Taxonomic aspects of endemism

Are limestone endemic plants a taxonomically heterogeneous group or do certain taxa have a

higher than expected probability of being endemic? We addressed this question by using contingency

tables. Chi-square analysis was used to test the hypothesis that the frequency of endemics within a family

would not be significantly different from the frequency for the non...limestone flora (an independent

sample comprising 538 vascular plant species; R.M. Cowling, unpublished data).

Biological aspects of endemism

A comparison was made of the association between endemism and biological attributes of species

in order to determine whether limestone endemic plants were a random assemblage with respect to

growth form,woody plant height,dispersal mode, dispersal distance, seed storage, degree of endemism

and woody plant pollination. The categorization of species with respect to biological attributes was based

on data in Bond and Slingsby (1983),. Bond and Goldblatt (1984), Rebelo, Siegfried & Oliver (1985),

Rebelo (1987) and our own unpublished observations. In some cases the categories were possibly too

broad to be.meaningful ~.g. soil-stored seed, insect pollination) but data were unavailable for finer

subdivisions. Similar comparisons have been made by Cowling and Holmes (1992a), Cowling et ale

(1992) and~cDonald and Co~ling (submitted).I ~

For the comparison between limestone endemic plants and the non-limestone flora of the SW

Gape lowland fynbos, eight growth form categories were recognised: dwarf shrubs (less than 0.25 m),

low shrubs (0.25 - 1 m), medium shrubs (1 - 2 m), tall shrubs (2 - 5 m), geophytes, forbs, graminoids

and vines. The dispersal mode categories recognised were: wind, bird (or vertebrate), ant, ballistic and

passive/unknown. Dispersal distance was categorised as short (less than 10 m), medium (10 -50 m) and

long (greater than 50 m). Seed storage categories included soil, canopy and non-storage, whilst the

pollination of woody plants (shrubs) was categorised as bird, insect or wind pollinated. For the analysis

of the limestone flora alone, several of these categories were excluded because of the low numbers in

the flora.

Relationships were investigated using two-way frequency tables (BMDP Program 4F; Dixon,i

1988). Chi-square analysis was used to test for independence among the variables. Adjusted standardized

7

deviates (Haberman, 1973) exceeding 3.0 in absolute value were taken to indicate cells with unusually

large deviations from the expected value. Three-way frequency tables were computed to examine how

some of these variables interact.

The biological attributes of the limestone endemic species and those of an independent sample

of non-limestone flora (538 species) were compared using simple two-way contingency tables. Chi-square

analysis was used to test for significant difference in the frequency of each trait with respect to the two

sets of species. The 'STARS' graphics programme (Willis & Hill, 1992) was used to show the relative

differences between the two samples. Star diagrams may comprise from three through eight adjacent

quadrilaterals, emanating from the centre of a circle, whose areas are proportional to the data values of

selected variables. The quadrilaterals extend beyond the circumference of the circle when the data values

dictate this (Willis & Hill, 1992). Chi-square analyses were performed using Statgraphics 5.0 (Statistical

Graphics Corporation, U.S.).

Nodes of rare species relative to species richness

Using an eighth-degree grid, the richness of rare species (as defined in Hall & Veldhuis, 1985)

per cell was compared with the total species richness for the limestone endemic flora. Regressions were

performed separately for threatened (vulnerable, endangered or recently extinct taxa), critically rare and

total rare species (both threatened and critically rare) according to the IUCN categories determined by

Hall & Veldhuis (1985). A square-root transformation was used for rare species, as data were counts

(Zar, 1984). Grid cells found to lie outside the upper 95% prediction limits for the limestone species

were interpreted' as,Iiaving significantly more rare species than expected. Based on the eighth-degree grid

cell distributions, isoflor maps of total species richness and rare limestone endemics were drawn using

the Krigingiethod:Within the g;aphics program SURFER (1989). Kriging uses geostatistical techniquesA

to calculate the autocorrelation between data points and produce a minimum variance unbiased estimate.

f

RESULTS

110 species were defined as limestone endemic species in the BRC (listed in Appendix 1). Of

these, 62 (56.4%) were regional, endemics and 46 (41.8%) were local endemics (Table 1).

Taxonomic aspects

The four families with the largest number of limestone endemics were the Rutaceae,Ericaceae,

Asteraceae and Fabaceae Cfable2).ThegenusErica (12 species) contained the most endemics, followed

by Agathosma (9), Asp~athus (8) and Muraltia (7). The Ericaceae, Fabaceae, Polygalaceae, Rutaceae

and Sterculiaceae were significantly over-represented amongst the limestone endemic flora (Table 1). The

8

Restionaceae was the only under-represented family. The remaining families were not significantly

different from the non-limestone flora in the SW Cape lowlands. Among the larger genera (> 5 spp.),

higher than -average (> 48 %) levels of regional endemism were recorded for Muraltia (polygalaceae)

(71.4%) and Aspalathus (Fabaceae) (62.5%). High levels of local endemism (> 52%) were recorded for

Erica (Ericaceae) (75%) and Agathosma (Rutaceae) (66.7%).

Biological aspects

With the exception of growth form, the X2 tests were non-significant for all endemic class­

biological attribute relationships within the limestone flora (fable 3). Within the growth form category,

there were no biological attributes that were over-represented for either the local or regional limestone

endemics. An analysis of three-way frequency tables showed that 32 % of local endemic dwarf-low shrubs

(comprising 89% of all local endemics) were wind dispersed and 44% were ant-dispersed. For regional

endemics (dwarf-low shrubs comprised 81% of all regional endemics), the respective values were 24%

for wind- and 42 % for ant-dispersed endemics. All of the local, and 96% of regional endemic dwarf-low

shrubs had soil-stored seed banks. Furthermore, 54% of local and 60% of regional endemic dwarf-low

shrubs had short-dispersal distances.

When compared with non-limestone flora, the limestone endemics were not a random assemblage

with regard to biological attributes and degree of endemism (Fig. 2). Within the growth form classes,

dwarf-and low shrubs were over-represented as limestone endemics. Endemism in medium-high (1-2 m)

shrubs was not significantly different from the non-limestone flora. Limestone endemics were under­

represented In 'all other growth form classes (Fig. 2). Limestone endemics were significantly over-, .~ .,{

represented as ballistic and ant-dispersed species and under-represented as passive/unknown and

vertebrate~persed'species. The limestone endemics were also over-represented as local and regionalA

endemics.Iand significantly under-represented as CFR and wide endemics (Fig. 2,3). In terms of seed

s~rage"limestone endemics were over-represented as having soil-stored seeds and under- represented

with respect to canopy-stored seeds. There was no significant difference between limestone endemics and

the non-limestone flora in the type of woody plant pollination. Both sets of species (92 % and 82%

respectively) were predominan~yinsect-pollinated (Fig. 2).

Rare species

Of the limestone endemics, 29(26%) have been listed, following IUCN threatened status criteria,

in the South African Red DataBookforplantsofthefynbos andKaroo biomes (Hall & Veldhuis, 1985).

Seventeen (16% of all limestone endemics) of these plants listed in the Red Data Book may be consideredi

as rare a.~. in the categories extinct, endangered, vulnerable or critically rare). Relative to species

9

richness, only two cells showed a higher than expected number of rare species (Fig. 4, 5). One cell was

selected for both total-rare species and threatened-rare species, namely the MelkhoutfonteinlStilbaaiarea

east of the Kafferkuils River (six threatened; two critically rare species) (Fig. 5b). The other cell that

contained higher than .expected critically-rare species was, the Hagelkraal area (one threatened; three

critically rare species) (Fig. '5b). The most species-rich area for limestone endemics was in De Hoop

Nature Reserve (Fig. 5a). Apart from a small concentration of endemics around the Stilbaai area, the

greatest concentration of endemics appears to be in the region stretching from the Soetanysberg through

to the Breede River.

DISCUSSION

Taxonomic aspects of limestone endemism

l ',fhe tendency of many of the families listed in Table 2 to produce endemics is also evident in

other parts of the CFR in,general (McDonald & Cowling, submitted), and coastal regions in particular

(Cowling et al., 1992). Several analyseshave indicated that endemics are unequally divided among plant

families @.g. Tolmachev, 1974a in Major, 1988; Cowling & Holmes, 1992a; Cowling et al., 1992;-~

McDonald & Cowling, submitted). Relative to non-limestoneflora, limestone endemics are not a random

assemblage in terms of taxonomic attributes. Amongst the limestone endemic flora, over-representation

of the Ericaceae and the Rutaceae conforms to patterns found in these families for endemic fynbos in the

Agulhas Plain, Cape Peninsula and theHumansdorp regions of .the CFR (Cowling et al., 1992). The

over-representation of Fabaceae is consistent with the results taken from four endemic floras in extra-(

tropical Eurasia (Tolmachev, 1974a,b in Major, 1988), while the over-representation of the Polygalaceae

The high percentage of local endemism prevalent amongst the limestone endemics of the Cape

lowland fynbos is due to the edaphic specialization and patchiness of the limestone habitats within the

region. Assuming that limestonefynbos covers approximately2 030 km2 within the fynbos biome (Rebelo

et al., 1991), limestone fynbos contains 54.2 endemic species per 1()3 krn', This probably represents the

richest concentration of limestone endemic vegetation in the world. Ninety taxa endemic to limestone in

the Greek mountains have been recorded by Papanicolaou, Babalonas & Kokkini (1983), although no

density values were provided for comparison. The presence of closely related endemics, or vicariads

(sensu Rourke, 1972), occurring on limestone and non...limestone soil types, particularly in the Agulhas

plain.dndicates that edaphic factors are a major force in speciation (Cowling et al., 1992). Examples are

Leucospermum cordifolium (quartzite), L. patersonii (limestone) (Rourke, 1972); Protea obtusifolia

llimestolle), P. 'susannae (neutral sand) (Rourke, 1980); Leucadendron meridianum (limestone), and L., ,

coniferum (neutral sand) (Williams, 1972).vi '

,~

10

follows the patterns shown in the endemic flora of the Agulhas Plain (Cowling & Holmes, 1992a). The

case ofthe Sterculiaceae being over-represented is an interesting result, having not been recorded as over­

represented in the published results of any endemic flora. However, as the sample sizes are very low for

this particular family, it may just be an artefact of the sampling procedure.

Despite significant species richness correlations found by Rebelo & Siegfried (1990) between the

Proteaceae and selected families and genera in the CFR, such as the Ericaceae, Rutaceae, Aspalathus and

Muraltia, the Proteaceae were not over-represented within the limestone endemic flora.

Biological aspects of limestone endemism

In terms of biological attributes, the local and regional limestone endemics were not significantly

different from one another. Limestone endemics, therefore, may.be considered as a distinct group, with

further subdivision into local and regional endemics unnecessary. Compared with the non-limestone flora,

limestone endemics are not a random assemblage in terms of biological attributes. The limestone

endemics of the BRC show similar trends to the endemics of the Agulhas Plain, Humansdorp (Cowling

et al., 1992) and Langeberg floras (McDonald & Cowling, submitted). They are mainly dwarf-low shrubs

with short dispersal distances and soil-stored seeds. In terms of dispersal mode, the fact that the seeds

tend to be either wind- or ant-dispersed, is consistent withresults from the Agulhas Plain for local and

regional endemics combined (Cowling et al., 1992). Compared with the overall flora of the Agulhas

Plain, .limestone endemics tend to be over-represented with respect to ballistic seed dispersal. Wind and

ballistic dispersal of seeds appear to be the only successful alternatives to myrmecochory in fynbos

4Johnson; 1992}'. Although a survey conducted during 1983 showed the absence of the Argentine ant,.. ~

Iridomyrmex humilis (Mayr), in the BRC (De Kock & Giliomee, 1989), this alien invertebrate remains

. a possible -'eat tothe limest~ne endemic fynbos, since invasion by this ant may expose seeds ofl

myrmecochorous endemic fynbos, particularly within the families Polygalaceae, Proteaceae (Bond &

Sljngsby, 1984) and Rutaceae, to granivorous rodent predation.

An attribute that is strongly associated with endemism is microsymbiont specificity (Cowling et

al., 1992). Both the fynbos Ericaceae and Fabaceae have specific microbe-mediated nutrient-uptake

strategies (ericoid mycorrhizal and rhizobia respectively), and it has been suggested that specificity for

microbes could explain edaphic specialization and speciation in these groups (Cowling,Straker &

Deignan, 1990). Although these biological attributes may be associated with speciation (non-sprouters

have a greater potential for speciation than sprouters), they can also be conducive to local population

extinction whenthesespecies are subJectedto catastrophic events such as too frequent fires, which reduce

population sizes and thus promote population fragmentation and isolation. Cowling and Bond (1991) have

11

shown that shrubs with ant-dispersed seeds were the species group most vulnerable to local extinction

on small limestone habitat fragments.

Despite the preponderance of insect pollination amongst the fynbos taxa, pollination biology has

never been an important research theme in the region. Within the BRC, some species ofIong-proboscid

flies (mainly Tabanidae and Nemestrinidae) are important pollinators of certain plant species ~.g. Erica

species) (Johnson, 1992) and could be critically important for maintaining the natural functioning and

integrity of many limestone endemics. Since long-proboscid flies, and midges, are particularly common

in the BRC during certain seasons, urban expansion along the coast holds the potential threat that control

measures may be implemented. This may include the application of pesticides to control the Tabanidae

larvae in the freshwater vleis along the coast (Burgers, 1993). Although fynbos pollination biologists are

still largely at the stage of identifying pollinators, this is nevertheless an important field in which much

basic research still needs to be addressed, and many questions appropriate to the long term persistence

of limestonefynbos communities need to be answered.

Rare limestone endemics

A limited number of species-rich areas do not guarantee effective conservation for rare and

restricted organisms, many of which occur outside species-rich areas (prendergast et al., 1993; Rebelo

& Tansley, 1993). The concentration of.ahigher than expected number of rare limestone endemic species

inthe-Stilbaai and Hagelkraal areas supports the recommendations made by Willis et ale (submitted),

using iterative and linear programming techniques, for these areas to be given greater conservation status.

We. acknowledge, however, that any conservation strategy based solely on the criteria of diversity

(species richness) and rarity, and on only one or a limited number of taxa,may fail to provide adequate

protectionIe many other org~sms. A holistic conservation strategy, based on both patterns and

processes.ishould be developed for the Cape lowland fynbos (see Rebelo, 1992).

I The term 'rare' describes a wide array of spatial and temporal patterns of abundance, from

sparsely populated species with wide geographic ranges to "point" endemics with dense local populations

(Kunin & Gaston, 1993). More information on rare limestone endemics is required, particularly with

regard to the processes that maintain the populations and communities,before informed decisions can be

made as regards their effective management. On the average, geographically restricted taxa also tend to

have small local populations, potentially making them doubly vulnerable to outside threats (Lawton,

1993). A potentially useful two-stage analytical method, using the Uniter computer program, for setting

conservation priorities for rare and threatened species (can potentially be used for several different taxa),

has been described by Hall (1993). In the first stage, the criteria are aspects of the need for conserving

the species, and in the second, their biological and practical ease of conservation.

12

CONCLUSIONS

Some general conclusions can be made regarding endemism in limestone fynbos. The highest

concentration of limestoneendemics is in De Hoop Nature Reserve, with higher than expectednumbers

of rare species in the Hagelkraal and Stilbaaiareas. Limestoneendemics are characterized by very high

levelsof regionaland local endemism. Taxonomically, limestoneendemics are not a random assemblage.

Familiessuchas the Ericaceae, Polygalaceae andRutaceaeare significantly over-represented as endemics.

Limestone endemics are also not random assemblages with respect to biological attributes. A limestone

endemic is most likely to be a dwarf to low shrub with soil-storedseeds which are ant or wind dispersed

and/or form symbiotic relationships with microbes. The possession of some of these traits, although

adaptive at the organism level, may incidentally cause lineage turnover and the multiplication of species

(Cowling et al., 1992). The taxonomic and biologicalprofiles of endemics in the lowland areas of the

CFR are broadly similar, indicating similarspeciationprocesses across the region. The patterns that have

been observed in this study indicatethat more attentionshould be given to the over-represented families

within limestone areas to guide management principles. An evaluation of the effects of fire, the most

practical management option in the fynbos, on dwarf-low limestoneendemic shrubs in the Rutaceae and

Ericaceae should provide useful insights into ecosystem processes in the region.

There are many still unanswered questions in limestonefynbos. For example, with many areas

being threatened by alien invasion, agriculture and urban expansion, what kinds and amounts of

biological simplification lead most readily to significant or irreversible changes in inherent structure and .

functionof limestone communities? What species (or kinds of species) are most important to ecosystem

function?" How 'm~ch or how little redundancy is present in the biological composition of limestone

fynbos? Are there 'drivers' or 'passengers' within the communities, with some species being perhaps

more impo~t than others in f system functioning? This is a very difficult question, as apparentl

'passengers', at one time scale, may be infrequentdeterminants at another. Conservingspecies is not the

tojalsolution. W~ must also conserve the processes, defined by species interactions within ecosystems,

and maintain tire evolutionary potential of organisms protected. Although conservation biologists must

act now, there is a need at the same time to build up.long-term data series that can be used to develop

specificmanagement recommendations, Conserving limestone fynbos in an area of the world that contains

an extraordinarynumber of local and regional endemics, is no simple task. If we are to ensure the long­

term persistence of limestone fynbos, the cooperation between conservation biologists, taxonomists,

managers and landowners will be required.

13

ACKNOWLEDGEMENTS

My grateful appreciation is expressed to my supervisors, Richard M. Cowling and Amanda T.

Lombard for their guidance and encouragement. Fieldwork was greatly facilitated through the enthusiastic

assistance of Barry J. Heydenrych (Flora Conservation Committee, Botanical Sociey of South Africa) and

Chris J. Burgers (Cape Nature Conservation, Jonkershoek). The Director (Research) of the National

Botanical Institute is thanked for the use of distributional and habitat data produced by the Pretoria

National Herbarium Computerized Information System (PRECIS). I gratefully acknowledge the assistance

of Jemery Day and Hugh Possingham (Department of Applied Mathematics, University of Adelaide,

Australia) for running the linear programming package LP_SOLVE, Nick Nicholls (CSIRO, Canberra,

Australia) for running the heuristic algorithms, and Andrea Plos for her help with the preparation of the

illustrations. My sincere appreciation is extended to the Institute for Plant Conservation (University of

Cape Town), University of Venda, Foundation for Research Development and. Flora Conservation

Committee of the Botanical Society of South Africa for their financial support during the study. Richard

Cowling, Amanda Lombard, Chris Burgers, Barry Heydenrych and Peter Ryan provided valuable

comments on earlier drafts of this manuscript. Lastly I would like to thank my family and my wife,

Carla, for their understanding and support throughout the study. Co-authors on this paper are, in order:

Amanda T. Lombard, Richard M. Cowling, Barry J. Heydenrych and Chris J. Burgers.

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17

APPENDIX 1

List of the vascular plants considered as limestone endemics in this study.

Family

MONOCOTYLEDONS

Cyperaceae

Iridaceae

Liliaceae

Poaceae

Restionaceae

DICOTYLEDONS

Aplaceae

Asteraceae

I,~

Campanulaceae

Ericaceae

Ficinia truncata (Thunb.) Schrader

Freesia elimensis L. BolusHesperantha juncifolia Goldbl.Watsonia fergusoniae L. Bolus

Haworthia variegataBolusLachenalia muirii Baker

Pentaschistis calcicola Linder var. calcicola*P. calcicola Linder var. hirsuta Linder"

Thamnochortus fraternus Pill.T. muirii Pill.T. paniculatus MastersT. pluristachyus Masters

Centella pottebergensis AdamsonPeucedanum sp. nova

Berkheya coriacea HarveyEuryops hebecarpus (DC.) B. NordenstamE. Iinearis HarveyE. muirii C.A. SmithFelicia canaliculata GrauF. ebracteata GrauF. nordenstamii GrauHelichrysum chlorochrysum DC.Metalasia calcicola Karls"M.' erectifolia Pillans t

M. luteola Karist

Oedera steyniae (L. Bol.) Anderb. & Bremer"Osteospermum subulatum DC.Stoebe muirii Levyns

Lightfootia calcarea AdamsonL. microphylla AdamsonL.sgtiariosa AdamsonRoella compacta Schltr.

Acrostemon schlechteri N.E. Br.

RDB category"

Critically RareEndangered

Critically RareVulnerable

Vulnerable

Endangered

Uncertain

Critically Rare

Vulnerable

Indeterminate

UncertainUncertain

18

Fabaceae

Lobeliaceae

Mesembr7hell1aceae

;-\>J

Penaeaceae

I'Polygalaceae

Proteaceae

A. vernicosus msErica berzelioides Guthrie & BolusE. calcareophila E. OliverE. curtophylla Guthrie & BolusE. excavata L. BolusE. gracilipes Guthrie & BolusE. oblongiflora Benth.E. occulta E. OliverE. propingua Guthrie & BolusE. pulvinata Guthrie & BolusE. saxicola Guthrie & BolusE. scytophylla Guthrie & BolusE. uysii H.A. BakerPlatycalyx pumila N.E. Br.Scyphogyne calcicola E. OliverThoracosperma muirii L. Guthrie"

Amphithalea alba GranbyAspalathus aciloba R. DahlgrenA. calcarea R. DahlgrenA.· candidula R. DahlgrenA. pallescens Ecldon & ZeyherA. prostrata Ecldon & ZeyherA. repens R. DahlgrenA. salteri L. BolusA. sanguineaThunb. subsp. sanguinea*Indigofera hamulosa Schltr.Lebeckia sessilifolia (Ecklon & Zeyher) Benth.

Lobelia barkerae F. WimmerL. valida L. Bolus

Braunsia vanrensburgii (L. Bolus) L. BolusRuschia calcicola (L. Bolus) L. Bolus

Brachysiphon mundii Sonder

Muraltia barkerae LevynsM. calycina HarveyM. 'depressa DC.M. lewisiae LevynsM.:. pappeana HarveyM. salsolacea ChodatM. splendens LevynsPolygala meridional is Levyns

Leucadendron muirii E. PhillipsLrmeridianum I.J. WilliamsLeucospermum patersonii E. PhillipsL. truncatum (Buek ex Meissner) RourkeMimetes saxatilis E. Phillips

Uncertain

Critically Rare

Vulnerable

Uncertain

Uncertain

Endangered

Indeterminate

Critically Rare

VulnerableVulnerable

19

Rhamnaceae

Rosaceae

Rubiaceae

Rutaceae

ScrOPhuta,ceae, '

,~

Sterculiaceae

Protea obtusifolia Buek ex Meissner

Phylica laevigata Pill.P. selaginoides SonderP. sp. nova

Cliffortia burgersii Oliver & Fellingham!

Galium bredasdorpense Puff

Acmadenia densifolia SonderA. heterophylla GloverA. mundiana EckIon & ZeyherAdenandra rotundifolia EckIon & ZeyherAgathosma abrupta Pill.A. eriantha SteudelA. florulenta Sond.*A. geniculata Pill.A. riversdalensis DummerA. sedifolia Schldl.A. sp. nova 1A. sp. nova 2A. sp. nova 3Diosma demissa I.J. WilliamsD. echinulataI.J. WilliamsD. guthriei GloverD. haelkraalensis I.J. WilliamsEuchaetis intonsa IJ. WilliamsE. laevigata Turcz.E. longibracteata Schltr.E. meridionalis I.J. Williams

Sutera calciphila Hilliard*S. subspicata (Benth.) Kuntze

Hermannia concinnifolia I. Verd.H. muirii Pill. ex I. Verd.H. trifoliata L.

Uncertain

IndeterminateVulnerable

Critically RareCritically Rare

Indeterminate

Indeterminate

a Authors of species follow Bond & Goldblatt (1984) except where indicatedb Red Data Book categories based on Hall and Veldhuis (1985)t Karis (1989):I: Linder & Ellis (1990: 83)§ Oliver & Fellingham (1991)* Arnold &de Wet (1993)

20

TABLE 1.

TABLE 2.

TABLE 3.

LEGENDS TO TABLES

The frequency of local, regional limestone endemics and non-limestone flora in the

Bredasdorp-Riversdale centre of endemism. CFR limestone endemics (n = 2) are

excluded from the analysis. The chi-square (x2) tests the null hypothesis that the

frequency of species in the limestone endemic (regional and local combined) and non­

limestone categories would not be different from the frequency of the whole flora,

excluding the family. NS = Not significant, * = p < 0.05, ** = p < 0.01, *** = p

< 0.001.

Family statistics of limestone endemics in the Bredasdorp-Riversdale centre of endemism

(see Appendix 1 for details).

The association between endemism and biological attributes of limestone endemic plants

in the Bredasdorp-Riversdale centre of endemism. Percentage contributions within each

endemic category are listed in parentheses. LE, Local endemics; RE, Regional endemics.

TABLE 1

Non-limestone Limestone Endemics

TABLE 2

Family Genera Species

Rutaceae 5 21

Ericaceae 5 17

Asteraceae 8 14

Fabaceae 4 11

Polygalaceae 2 8

Proteaceae 4 6

Campanulaceae 2 4

Restionaceae 1 4

Iridaceae 3 3

Rhamnaceae 1 3

Sterculiaceae 1 3

Apiaceae 2 2

Liliaceae 2 2

Mesembryanthemaceae 2 2

Lobeliaceae ' 1 2~

··Poaceae 1 2

scroPhuraceae" 1 2

Cyperaceae 1 1

penaeaceae 1 1

Rosaceae 1 1

Rubiaceae 1 1

Total 49 110

"

TA

BL

E3

".~. -,-:

:,

(a)

Gro

wth

form

~

DW

arf

shru

b«,

O.2

Sm)

LE

3L(6

7.4)

RE

26'(4

1.9)

(b)

Dis

pers

alm

ode

Low

Med

ium

shru

bsh

rub

(O.2

S-lm

)(I

-2m

)10

(21.

7)2

(4.3

)24

(38.

7)2

(3.2

)X-

=12

.3,P

<0.

05

Geo

phyt

e

2(4

.3)

3(4

.8)

For

b

1(2

.2)

0(0

)

Gra

min

oid

0(0

)7

(11.

3)

LE

RE

Win

d15

(32.

6)21

(33.

9)

Ant

Bal

listic

19(4

1.3)

3(6

.5)

24(3

8.7)

7(1

1.3)

X-=

0.9,

P>

0.10

Pas

sive

lUnk

now

n9

(19.

6)10

(16.

1)

(c)D

ispe

rsal

dist

ance

(d)

Seed

stor

age

Can

opy

Soil

LE

RE

Sho

rtM

ediu

m«

10m

)(lo

-SO

m)

29(6

3)17

(37)

40(6

4.5)

22(3

5.5)

x2=

0.02

5,P

>0.

10

LE

RE

o(0

)46

(100

)3

(4.8

)59

(95.

2)x2

=2.

29,

P>

0.10

Figure 1.

Figure 2.

Figure 3.,fl:O

...Figure 4.

Figure 5.

LEGENDS TO FIGURES

Map of the study area showing. the Bredasdorp-Riversdale centre of endemism (BRC)

(shaded) within the Cape Floristic Region relative to Weimarck's (1941) major centres

of endemism. SW = South Western, L = Langeberg. The inset shows the position of

the study area within South Africa.

Star plots comparing the proportion of limestone endemic (n = 110) and non-limestone

flora (independent sample, n = 538) with respect to endemism and biological attributes

within specific categories: (a) growth form, (b) woody plant height (non-limestone flora,

n = 259; limestone endemics, n = 97), (c) dispersal mode, (d) degree of endemism, (e)

dispersal distance, (t) seed storage and (g) woody plant pollination (non-limestone flora,

n = 259; limestone endemics, n =97). Chi-square~ analyses were performed on

untransformed data. The percentage contribution of the major segment to each plot is

indicated next to the relevant segment.

Bar graph showing the number of limestone endemic species per eighth-degree grid cell

in the Bredasdorp-Riversdale centre of endemism.

Linear regression of the number of rare limestone endemic species (square root

I;.·transformed) versus the total number of limestone endemic species per eighth-degree grid

,;, . cell (n = 53). The dashed lines represent the 95% confidence limits (innermost) and the

. 95 % prediction limits of the regression (outermost). 'Threatened species' indicate Red

l?ata Book categories of extinct, endangered and vulnerable, whereas 'Critically Rare

species' comprise that category alone (Hall & Veldhuis, 1985).

The distribution f 40f species richness of limestone endemic vascular plants in the

Bredasdorp-Riversdale centre of endemism, according to the eighth-degree grid system

used in this study. Isoflor maps represent (a) the entire limestone endemic flora, and (b)

the rare limestone endemics only. The two sites indicated on map (b) represent those

areas with significantly more (A) rare (extinct, endangered, vulnerable and critically rare)

and threatened (extinct, endangered and vulnerable only) and (B) critically rare species,

than expected relative to the total species richness (see Fig. 4).

190

E

..... 200

/0

FIG

UR

E1B

RC

210

o3

0lo

nI

I

Indi

anO

cean

N t

340

S

LIMESTONE

1I1l1I!!!!!!!1 Canopy__ Soil

~~""l Non-storageChi-square = 11.46

P < 0.01

mmImm Bird__ Insect

~ WindChi-square = 5.63

NS

Shtub11111111111111 Geophytef:/00/~ Forb~ GraminoidW//ffi Vine

Chi-square =59.9p < 0.0001

DwarfIIIIIllIlIIlI1 LowWAg Medium.~~ Tall

Chi-square = 15.12p < 0.01

f&%\1 WindV/$//3 BirdIIII1II1!!1I11 Antw/--01 Ballistic

Passive / unknown

Chi-square = 33.46p < 0.0001

Local11111111111111 Regional

~ CPRWPM Wide

Chi-square = 235~9

p < 0.0001

Short( < 10m)

W$l Medium ( 10 - SOm )11111111111111 Long ( > 50 m)

Chi-square = 8.99p < 0.05

64.5

NON-LIMESTONE

(f)

(g)

(a)

(b)

(c)

(d)

FIGURE 2

20

1818

16

0 14.!oCI) 12Q.0'I-

100:-CI).Q 8

E::s

6Z,..

Number of grid cells

1II1II. Limestone endemics

FIGURE 3

3 / /'- All species / /'V) »: / ../

= / / /"/ -: ../

+ ///4

/"/ A4 /"

/ /" /II / »:/.....-. 4 4/ 4 /" ./-g 2 /" »:./ / /" ./

c.e / ~ 4,/ 4 /GI'2 / / /" »:

'S/ / /" /

/. 4_/ ./" • /"/ »: /"

fa»: »:

/ // ./

I"'::4 ...

/ / /1 / / /

/ //' / Y = 0.72 + 0.03 X- - ....... .........-

~»: 2/ R = 68.2 %»:

CI /tI.l /

P < 0.0001-:0 /

0 20 40 60 80Number of species

3- Threatened speciesV) »>= --~

+ .---

1 .----- ~/"

/"2 -- /"--- /"... ... - /"/"

GI'2 -- ~

'S - /"-- ... ...-- --i - -- ---~

4 4 4 • . .~---- --~...---- -Z -- --- _.A ........ 4~-

~ - _-- Y = 0.72 + 0.02 X-- 2CI _--- R = 36.2 %tI.l

0 --- p < 0.0001

0 20 40 60 80~ Number of species

I 3- Critically Rare SpeciesV);~/ = »>.--

+II ~./

r /4-l 2 /"/

• At"/"

GI'2 /" - ~/

'S ~/" ... _- .--- --ks - ~.--

I 1-~ Y = 0.67 + 0.02 X

2CI R = 75.2 %tI.l

0 P < 0.0001

0 20 40 60 80Number of species

FIGURE 4

... ..f .........:.......

\-De Hoop NatureReserve

: :. .: ~ .

----------------------------J..35°

(b)

I Hagelkraal

FIGURE 5