Patterns of Endemism in the Limestone Flora of South African Lowland Fynbos

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Biodiversity and Conservation 5, 55–73 (1996)

Patterns of endemism in the limestone ﬂora of South African lowland fynbos

CHRISTOPHER K. WILLIS Botany Department, University of Venda, Private Bag X5050, Thohoyandou, South Africa

RICHARD M. COWLING* Institute for Plant Conservation, Botany Department, University of Cape Town, Rondebosch 7700, South Africa

AMANDA T. LOMBARD FitzPatrick Institute, University of Cape Town, Rondebosch 7700, South Africa

Received 15 November 1994; revised and accepted 8 February 1995

Taxonomic and biological aspects of endemism and Red Data Book status were studied amongst the limestone endemics of the lowland fynbos in the Cape Floristic Region, South Africa. Of the 110 limestone endemics, 1.8% are widely distributed in the Cape Floristic Region and 56.4% are regional endemics. Relative to flora of non-limestone lowland fynbos (n = 538 species), the families which were overrepresented in terms of limestone endemics included the Ericaceae, Fabaceae, Polygalaceae, Rutaceae and Sterculiaceae. The Restionaceae was the only underrepresented family. The local limestone endemics were not significantly different from regional endemics in terms of their biological attributes. An analysis of the frequency of the biological traits associated with the limestone-endemic flora established a biological profile for a limestone endemic: a dwarf-to-low shrub with soil-stored seeds which are ant or wind dispersed. In terms of the species richness of limestone endemics, the De Hoop Nature Reserve was the ‘hotspot’ within the region. Relative to the 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.

Keywords: Cape Floristic Region; lowland fynbos; limestone; endemism; conservation.

Introduction Within the south-western corner of Africa, the Cape Floristic Region (CFR) represents the smallest of the six ﬂoral kingdoms of the world (Takhtajan, 1986). Covering some 0.04% (89 000 km2) of the earth’s surface, it contains c. 8550 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 Lanariaceae, Penaeaceae, Grubbiaceae, Roridulaceae, Retziaceae, Stilbaceae and Geissolomataceae) are endemic. The CFR is dominated by fynbos, a sclerophyllous, heath-like shrubland associated with nutrient-poor soils which

*To whom correspondence should be addressed.

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56 Willis et al. cover most of the region (Cowling and Holmes, 1992a). These shrublands are fire-prone and usually burn at six to forty year intervals (Cowling and Holmes, 1992b). The coastal lowland areas of the CFR represent one of the most threatened regions of natural vegetation because of intensive agriculture, urbanization and alien-plant encroachment (Jarman, 1986). Amongst the lowland flora, limestone fynbos communities are particularly vulnerable, because of their edaphic specialization and restricted nature and they contain many threatened endemic species (Hilton-Taylor and Le Roux, 1989). Despite the flora being relatively well studied, patterns and determinants of endemism have been poorly examined in the CFR (Cowling and 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 et al., 1992). Although certain studies in the lowland floras of the CFR have shown that most endemics are edaphic specialists and that certain substrata (for example, limestone) harbour disproportionally high numbers of endemics (Cowling and Holmes, 1992a; Cowling et al., 1992), no studies have looked at these edaphic specialists per se. This study therefore represents the first attempt to analyse and characterize endemic vascular plants restricted to limestone substrata within the Cape lowland flora. Based on the distributions of limestone endemics within the lowland flora, J.P. Willis et al. (in press) 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 widespread within the CFR, or are endemic at the regional and local scales? (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? (vi) Do local limestone endemics differ from more widespread limestone species in terms of these traits?

Study area Geology, geomorphology and soils The study area comprises a gently rolling, coastal lowland landscape towards the southern tip of Africa from Hermanus in the west to the Gouritz River in the east, and it includes both the Agulhas (Cowling et al., 1988) and Riversdale coastal plains (Rebelo et al., 1991). See Fig. 1. As the entire area was inundated by transgressions during the mid-Miocene (15 Myr (million years)) and the early–mid-Pliocene (4 Myr), most sediments and soils postdate the regression (Hendey, 1983). Despite the low topographical diversity when compared with the mountainous regions of the fynbos biome, the area has numerous contrasting soil types and land systems (Thwaites and Cowling, 1988). Table Mountain Group sandstones and quartzites, Bokkeveld Group shales, limestones, remnant silcrete and ferricrete outcrops and calcareous coastal dunes are all represented in the area. Miocene–Pliocene limestones and associated colluvial deposits of the Bredasdorp Group form distinctive relief features in the coastal zone, and soils on the limestone bedrock are shallow, well-drained, calcareous sands (Cowling and Holmes, 1992a). The Riversdale Plain, deﬁned as the coastal plain south of the Langeberg Mountains between the Mendip Communications Ltd Job ID: BIO1----0057-1 383 - 57 Rev: 18-04-96 PAGE: 1 TIME: 15:40 SIZE: 55,10 OP: XX

Patterns of endemism in the limestone ﬂora of lowland fynbos 57 Duiwenhoks River in the west and the Gouritz River in the east, contains the largest development of Tertiary limestone in the fynbos biome. Further details on the geomorphology, geology and soils of the area are given by Malan (1987), by Thwaites (1987), by Rogers (1988) and by Thwaites and Cowling (1988).

Climate The climate of the area is relatively uniform. The average annual temperature is in the range 15–17.48C, depending on the locality. Along the coast, the mean annual rainfall ranges from 454 mm at Gansbaai to 400 mm at the Gouritz River mouth. Higher values would be recorded in the hills but data are lacking. Rainfall seasonality is typical of a Mediterranean-type climate, with most of the annual precipitation falling in the winter months.

Limestone fynbos 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). The term used to describe the vegetation associated with limestone in the BRC has varied according to the classification used. Moll et al. (1984) described the vegetation as ‘limestone fynbos’, whereas Cowling and Holmes (1992b), based on Campbell’s (1985) use, classified the vegetation as ‘proteoid fynbos’. Leucadendron meridianum I.J. Williams and Protea obtusifolia Bueck ex Meissner dominate the limestone areas within the proteoid fynbos, with Leucospermum truncatum (Bueck ex Meissner) Rourke and Leucodendron muirii E. Phillips co-dominant in this community where limestone outcrops have skeletal soils (Rebelo et al., 1991). We regard the vegetation endemic to limestone substrata as limestone fynbos. Fifty-four per cent (1100 km2 of the 2030 km2) of the limestone fynbos occurs in and immediately adjacent to the Riversdale coastal plain (Moll et al., 1984; Bohnen, 1986). Details of other vegetation categories in the area are given by Cowling et al. (1988) and by Rebelo et al. (1991).

Methods Categories and centres of endemism Three categories of endemism were recognized in the BRC: (i) CFR endemics 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 subcentres (such as the Bredasdorp Centre) within the BRC (Weimarck, 1941; Midgley, 1986; Oliver et al., 1983). All of the local endemics considered in this study occupy ranges of less than 2000 km2 (2.2% of the Cape Floristic Region); some ranges are less than 5 km2.

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-1960 monographs; Bond and Mendip Communications Ltd Job ID: BIO1----0058-1 383 - 58 Rev: 18-04-96 PAGE: 1 TIME: 15:40 SIZE: 55,10 OP: XX

58 Willis et al. Goldblatt’s catalogue (1984) of the Cape flora; the Protea Atlas Project database (Botany Department, University of Cape Town); the ISEP (Information System for Endangered Plants) database, managed by Cape Nature Conservation, Jonkershoek; herbarium specimens in the Bolus Herbarium (BOL), University of Cape Town and in the Compton Herbarium (COM), 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 catalogue (1984), and a 26–33% error associated with the PRECIS database, with endemic species particularly underrepresented, 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 from herbarium specimens collected, during a field survey throughout the study area. During the survey, 15 areas were surveyed for the presence of limestone-endemic plant species. At each site, efforts were 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 vegetation) within the area concerned. All distribution records (presence, not abundance) were plotted on an eighth-of-a- degree grid (that is, in cells, 11.5 × 13.85 km2). Using this information, the accuracy of the herbarium databases was verified on an eighth-of-a-degree scale by Chris Burgers (Cape Nature Conservation, Jonkershoek) using the ARC /INFO program, 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-endemic flora from the Agulhas Plain in the western sector of the study area. This flora comprised an independent sample of 538 vascular plant species (R.M. Cowling, unpublished data).

Biological aspects of endemism A comparison was made of the association between endemism and the biological attributes of the species in order to determine whether limestone-endemic plants were a random assemblage with respect to growth form, woody-plant height, dispersal distance, seed storage, degree of endemism and woody-plant pollination. The categorization of species with respect to biological attributes was based on data from Bond and Slingsby (1983), Bond and Goldblatt (1984), Rebelo et al. (1985), Rebelo (1987) and our own unpublished observations. In some cases the categories were possibly too broad to be meaningful (for example, soil-stored seed, insect pollination) but data were unavailable for ﬁner subdivisions. Similar comparisons have been made by Cowling and Holmes (1992a), by Cowling et al. (1992) and by McDonald and Cowling (1994). For the comparison between limestone-endemic plants and the non-limestone-endemic ﬂora, eight growth-form categories were recognized: 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, Mendip Communications Ltd Job ID: BIO1----0059-1 383 - 59 Rev: 18-04-96 PAGE: 1 TIME: 15:40 SIZE: 55,10 OP: XX

Patterns of endemism in the limestone ﬂora of lowland fynbos 59

Figure 1. A map of the study area showing the Bredasdorp–Riversdale centre of endemism (shaded) within the CFR relative to Weimarck’s major centres of endemism (Weimarck, 1941). SW = South Western, L = Langeberg. The inset shows the position of the study area within South Area.

graminoids and vines. The dispersal-mode categories recognized were: wind, bird (or vertebrate), ant, ballistic and passive/unknown. The dispersal distance was categorized 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. The pollination of woody plants (shrubs) was categorized as: bird, insect or wind pollinated. For the analysis of the limestone flora alone, several of these categories were excluded because of the low species numbers in the cells of the contingency table. The relationships were investigated using two-way frequency tables (BMDP program 4F; Dixon, 1988). Chi-square analysis was used to test for independence among the variables. Adjusted standardized 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 program (Willis and Hill, 1992) was used to show the relative differences between the two samples. Star diagrams may have three to eight adjacent quadrilaterals, emanating from the centre of a circle, whose areas are proportional to the data values of the selected variables. The quadrilaterals extend beyond the circumference of the circle when this is dictated by the data values (Willis and Hill, 1992). Chi-square analyses were performed using the Statgraphics 5.0 program (Statistical Graphics Corporation, US). Nodes of rare species relative to species richness Using an eighth-of-a-degree grid, the richness of rare species (as defined by Hall and Veldhuis, 1985) per cell was compared with the total species richness for the limestone- endemic flora. Regressions were performed separately for threatened (vulnerable or endangered taxa), critically rare and total rare species (both threatened and critically rare) according to the International Union for Conservation of Nature and Natural Resources Mendip Communications Ltd Job ID: BIO1----0060-1 383 - 60 Rev: 18-04-96 PAGE: 1 TIME: 15:40 SIZE: 55,10 OP: XX

60 Willis et al. (IUCN) categories determined by Hall and Veldhuis (1985). A square-root transformation was used for rare species, as were data counts (Zar, 1984). Grid cells found to lie outside the upper 95% prediction limits for the limestone species were interpreted as having signiﬁcantly more rare species than expected. Based on the eighth-of-a-degree-grid cell distributions, isoﬂor maps of the total species richness and of the rare limestone endemics were drawn using the Kriging method within the graphics program SURFER (1989). The Kriging method uses geostatistical techniques to calculate the autocorrelation between data points and to produce a minimum-variance unbiased estimate.

Results One-hundred and ten species were defined as limestone-endemic species in the BRC (these species are listed in Appendix 1). Of these, two species (1.8%) were widespread in the CFR (but endemic there), 62 (56.4%) were regional endemics confined to the BRC and 46 (41.8%) were local endemics confined to subcentres within the BRC (Table 1).

Table 1. The frequency of local and regional limestone endemics and of non-limestone ﬂora in the Bredasdorp–Riversdale centre of endemism. The CFR limestone endemics (n = 2) are excluded from the analysis. The chi-square analysis (χ2) 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

Non-limestone Limestone endemics

Regional Local

Family Number Percentage Number Percentage χ2 Signiﬁcancea

All 538 62 57.4 46 42.6 Asteraceae 62 9 64.3 5 35.7 0.18 NS Campanulaceae 6 2 66.7 1 33.3 1.81 NS Cyperaceae 27 1 100.0 0 0 3.63 NS Ericaceae 35 4 23.5 13 76.5 10.36 P , 0.01 Fabaceae 26 8 72.7 3 27.3 4.77 P , 0.05 Iridaceae 39 1 33.3 2 66.7 2.96 NS Liliaceaeb 25 2 100.0 0 0 1.76 NS Lobeliaceae 2 1 50.0 1 50.0 3.20 NS Poaceae 25 2 100.0 0 0 1.75 NS Polygalaceae 9 6 75.0 2 25.0 11.54 P , 0.01 Proteaceae 29 5 83.3 1 16.7 0.01 NS Restionaceae 55 4 100.0 0 0 4.61 P , 0.05 Rhamnaceae 6 2 66.7 1 33.3 1.81 NS Rutaceae 12 9 45.0 11 55.0 50.68 P , 0.001 Sterculiaceae 3 2 66.7 1 33.3 4.82 P , 0.05

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Patterns of endemism in the limestone ﬂora of lowland fynbos 61 Table 2. Family statistics of limestone endemics in the Bredasdorp–Riversdale centre of endemism (see Appendix 1 for more detail)

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 Scrophulariaceae 1 2 Cyperaceae 1 1 Penaeceae 1 1 Rosaceae 1 1 Rubiaceae 1 1

Total 49 110

Taxonomic aspects The four families with the largest number of limestone endemics were the Rutaceae, Ericaceae, Asteraceae and Fabaceae (Table 2). The genus Erica (12 species) contained the most endemics, followed by Agathosma (9), Aspalathus (8) and Muraltia (7). The Ericaceae, Fabaceae, Polygalaceae, Rutaceae and Sterculiaceae were significantly overrepresented, relative to a non-limestone flora, in the limestone-endemic flora (Table 1). The Restionaceae was the only underrepresented family. The remaining families were not significantly different from the non-limestone flora. Among the larger genera (.5 species), 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 the growth form, the χ2-tests were non-signiﬁcant for all endemic-class–biological-attribute relationships within the limestone ﬂora (Table 3). Within the growth-form category, there were no biological attributes that were overrepresented for either the local or the regional limestone endemics. An analysis of Mendip Communications Ltd Job ID: BIO1----0062-1 383 - 62 Rev: 18-04-96 PAGE: 1 TIME: 15:40 SIZE: 55,10 OP: XX

62 Willis et al. Table 3. The association between the endemism and the biological attributes of limestone-endemic plants in the Bredasdorp–Riversdale centre of endemism. The percentage contributions within each endemic category are listed in parentheses; LE, local endemics; RE, regional endemics

(a) Growth form Dwarf Low Medium shrub shrub shrub Geophyte Forb Graminoid (,0.25 m) (0.25–1 m) (1–2 m) LE 31 (67.4) 10 (21.7) 2 (4.3) 2 (4.3) 1 (2.2) 0 (0) RE 26 (41.9) 24 (38.7) 2 (3.2) 3 (4.8) 0 (0) 7 (11.3) χ2 = 12.3, p , 0.05 (b) Dispersal mode Wind Ant Ballistic Passive/unknown LE 15 (32.6) 19 (41.3) 3 (6.5) 9 (19.6) RE 21 (33.9) 24 (38.7) 7 (11.3) 10 (16.1) χ2 = 0.9, p . 0.10 (c) Dispersal distance Short Medium (,10 m) (10–50 m) LE 29 (63) 17 (37) RE 40 (64.5) 22 (35.5) χ2 = 0.025, p. 0.10 (d) Seed storage Canopy Soil LE 0 (0) 46 (100) RE 3 (4.8) 59 (95.2) χ2 = 2.29, p . 0.10

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-dispersed and 42% for ant-dispersed endemics. All of the local endemic shrubs, 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 to degree of endemism (Fig. 2). Within the growth-form classes, dwarf and low shrubs were overrepresented as limestone endemics. Endemism in medium–high shrubs (1–2 m) was not significantly different from the non-limestone flora. Limestone endemics were underrepresented in all other growth-form classes (Fig. 2). Limestone endemics were significantly overrepresented as ballistic and ant-dispersed species and they were underrepresented as passive/unknown and vertebrate-dispersed species. The limestone endemics were also overrepresented as local and regional endemics, and they were signficantly underrepresented in the CFR-endemic and widespread categories (Fig. 2). In terms of seed storage, limestone endemics were overrepresented in the soil-stored seed category and underrepresented with respect to canopy-stored seeds. There was no significant difference between Mendip Communications Ltd Job ID: BIO1----0063-1 383 - 63 Rev: 18-04-96 PAGE: 1 TIME: 15:40 SIZE: 55,10 OP: XX

Patterns of endemism in the limestone ﬂora of lowland fynbos 63

Figure 2. Star plots comparing the proportion of limestone endemic (n = 110) and non-limestone flora (independent sample, n = 538) with respect to the endemism and the biological attributes within the following 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, (f) seed storage, and (g) woody-plant pollination (non-limestone flora, n = 259; limestone endemics, n = 97). Chi-square (χ2) analyses were performed on the untransformed data. The percentage contribution of the major segment to each plot is indicated next to the relevant segment. Mendip Communications Ltd Job ID: BIO1----0064-1 383 - 64 Rev: 18-04-96 PAGE: 1 TIME: 15:40 SIZE: 55,10 OP: XX

64 Willis et al. limestone endemics and the non-limestone ﬂora in the type of plant pollination in woody species, and both sets of species (92% and 82%, respectively) were predominantly insect pollinated (Fig. 2).

Rare species Of the limestone endemics, 29 (26%) have been listed, following IUCN-threatened-status criteria, in the South African Red Data Book for plants of the fynbos and Karoo biomes (Hall and Veldhuis, 1985). Seventeen (15% of all limestone endemics) of these plants listed in the Red Data Book may be considered as rare (that is, in the categories endangered, vulnerable or critically rare). Relative to the species richness, only two cells showed a higher than expected number of rare species. One cell was selected for both total rare species and threatened rare species, namely the Melkhoutfontein/Stilbaai area east of the Kafferkuils River (six threatened; two critically rare species) (Fig. 3). The other cell that contained higher than expected critically rare species was the Hagelkraal area (one threatened; three critically rare species) (Fig. 3). The area richest in species for limestone endemics was in the De Hoop Nature Reserve (Fig. 3). 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 The high percentage of local endemism prevalent amongst the limestone endemics of the Cape lowland fynbos is due to the edaphic specialization of this calcicole ﬂora (Mustart and Cowling, 1993) and the fragmented nature of the limestone habitats in a ‘sea’ of acid substrata. Assuming that the limestone fynbos covers approximately 2030 km2 within the fynbos biome (Rebelo et al., 1991), then it contains 54.2 endemic species per 103 km2. This probably represents the richest concentration of limestone endemics in the world. Ninety taxa endemic to limestone in the Greek mountains have been recorded by Papanicolaou et al. (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, paticularly in the Agulhas Plain, indicates that edaphic factors are a major force in speciation (Cowling et al., 1992). Examples in the Proteaceae include Leucospermum cordifolium (quartzite), L. patersonii (limestone) (Rourke, 1972), Protea obtusifolia (limestone), P. susannae (neutral sand) (Rourke, 1980), Leucadendron meridianum (limestone) and L. coniferum (neutral sand) (Williams, 1972).

Taxonomic aspects of limestone endemism The tendency of many of the families listed in Table 2 to produce local endemics is also evident in other fynbos floras (Cowling et al., 1992; McDonald and Cowling, 1994). Several analyses have indicated than endemics are unequally divided among plant families (for example, Tolmachev, 1974a in Major, 1988; Cowling and Holmes, 1992a; Cowling et al., 1992). Relative to non-limestone flora, limestone endemics are not a random assemblage in terms of their taxonomic attributes. Amongst the limestone-endemic flora, the overrepresentation of the Ericaceae and the Rutaceae conforms to patterns found in these families for endemic fynbos in the Agulhas Plain, Cape Peninsula and the Humansdorp regions of the CFR (Cowling et al., 1992). The overrepresentation of Fabaceae is consistent with the results taken from four endemic floras in extra-tropical Eurasia (Tolmachev, Mendip Communications Ltd Job ID: BIO1----0065-1 383 - 65 Rev: 18-04-96 PAGE: 1 TIME: 15:40 SIZE: 55,10 OP: XX

Patterns of endemism in the limestone ﬂora of lowland fynbos 65

Figure 3. The distribution of species richness of limestone-endemic vascular plants in the Bredasdorp–Riversdale centre of endemism, according to the eighth-of-a-degree grid system used in this study. The 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 (endangered, vulnerable and critically rare) and threatened (endangered and vulnerable only) and (B) critically rare species than expected, relative to the total species richness.

1974a,b in Major, 1988), while the overrepresentation of the Polygalaceae follows the patterns shown in the endemic flora of the Agulhas Plain (Cowling and Holmes, 1992a). The overrepresentation of the Sterculiaceae is an interesting phenomenon, since this has not been recorded in the published results of any endemic flora. However, the sample sizes are very low for this particular family, and this may have influenced the results. Despite the significant species–richness correlations found by Rebelo and 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 overrepresented within the limestone-endemic flora. Hence, reserve systems identified on the basis of this family are unlikely to represent limestone endemics (Willis et al., in press).

Biological aspects of limestone endemism In terms of their 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, and further subdivision into local and regional endemics is Mendip Communications Ltd Job ID: BIO1----0066-1 383 - 66 Rev: 18-04-96 PAGE: 1 TIME: 15:40 SIZE: 55,10 OP: XX

66 Willis et al. unnecessary. When 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 and Cowling, 1994). They are mainly dwarf–low shrubs with short dispersal distances and soil-stored seeds. In terms of their dispersal mode, the fact that the seeds tend to be either wind or ant dispersed, is consistent with results from the Agulhas Plain for the local and regional endemics combined (Cowling et al., 1992). Compared with the overall flora of the Agulhas Plain, limestone endemics tend to be overrepresented with respect to ballistic seed dispersal. Wind and ballistic dispersal of seeds appear to be the only successful alternatives to myrmecochory in fynbos (Johnson, 1992). Although a survey conducted during 1983 showed the absence of the Argentine ant, Iridomyrmex humilis (Mayr), in the BRC (De Kock and Giliomee, 1989), this alien invertebrate remains a possible threat to the limestone-endemic fynbos, since invasion by this ant may expose seeds of myrmecochorous endemic fynbos, particularly within the families Polygalaceae, Proteaceae (Bond and Slingsby, 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 the fynbos 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 et al., 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 when these species are subjected to catastrophic events, such as too frequent fires, which reduce population sizes and thus promote population fragmentation and isolation. Cowling and Bond (1991) have shown that shrubs with ant-dispersed seeds were the species group most vulnerable to local extinction on small limestone-habitat fragments. Management should be sensitive to the fact that non-sprouters are vulnerable to fire-induced local extinction. In addition, because many limestone endemics have short dispersal distances, resilience by migration (dispersal) is unlikely.

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 and Tansley, 1993). The concentration of a higher than expected number of rare limestone-endemic species in the Stilbaai and Hagelkraal areas supports the recommendations made by Willis et al. (in press), using iterative and linear-programming techniques, for these areas to be given greater conservation status. We acknowledge, however, that any conservation strategy which is 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 protection for many other organisms. A holistic conservation strategy, based on both patterns and processes, should be developed for the Cape lowland fynbos (see Rebelo, 1992). 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 and Gaston, 1993). More information on rare limestone endemics is required, particularly with regard to the processes that maintain the Mendip Communications Ltd Job ID: BIO1----0067-1 383 - 67 Rev: 18-04-96 PAGE: 1 TIME: 15:40 SIZE: 55,10 OP: XX

Patterns of endemism in the limestone ﬂora of lowland fynbos 67 populations and communities, before informed decisions can be made for their effective management. On 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 (it could be used for several different taxa), has been described by Hall (1993). In the ﬁrst stage the criteria are aspects of the need for conservation of the species, and in the second the criteria are their biological and practical ease of conservation.

Conclusion Some general conclusions can be made regarding endemism in limestone fynbos. The highest concentration of limestone endemics is in the De Hoop Nature Reserve, with higher than expected numbers of rare species in the Hagelkraal and Stilbaai areas. Limestone endemics are characterized by very high levels of regional and local endemism. Taxonomically, families such as the Ericaceae, Polygalaceae and Rutaceae are significantly overrepresented as endemics. In terms of their biological attributes, limestone endemics are most likely to be dwarf-to-low shrub with soil-stored seeds which are ant or wind dispersed and/or to form symbiotic relationships with microbes. The taxonomic and biological profiles of the largely neoendemic flora in the lowland areas of the CFR are broadly similar, indicating similar speciation processes across the region (Cowling et al., 1992). The patterns that have been observed in this study indicate that more attention should be given to the overrepresented 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 limestone endemic shrubs in the Rutaceae and Ericaceae should provide useful insights into the ecosystem processes in the region. There are many still unanswered questions in limestone fynbos. 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 the inherent structure and function of limestone communities? Which species (or kinds of species) are the most important to ecosystem function? How much or how little redundancy is present in the biological composition of limestone fynbos? Conservation of species is not the total solution. We must also conserve the processes, defined by species interactions within ecosystems, and we must maintain the evolutionary potential of the organisms which are protected. Although conservation biologists must act immediately, there is a need at the same time to build up long-term data series that can be used to develop specific management recommendations. The conservation of limestone fynbos in an area of the world that contains an extraordinary number of local and regional endemics is no simple task. If we are to ensure the long-term persistence of limestone fynbos, cooperation between conservation biologists, taxonomists, managers and landowners will be required.

Acknowledgements Barry J. Heydenrych (Flora Conservation Committee, Botanical Society of South Africa) and Chris Burgers (Cape Nature Conservation, Jonkershoek) provided valuable Mendip Communications Ltd Job ID: BIO1----0068-1 383 - 68 Rev: 18-04-96 PAGE: 1 TIME: 15:40 SIZE: 55,10 OP: XX

68 Willis et al. assistance during the ﬁeld survey. We gratefully acknowledge James Willis (Department of Geological Sciences, University of Cape Town) for guidance in using the STARS program, and Andrea Plös for her help with the preparation of the illustrations. We would also like to thank June Juritz, Jacqui Sommerville and Roger Haylett for their help and advice with the statistical analyses. We thank the Director (of research) of the National Botanical Institute for the use of distributional and habitat data produced by the Pretoria National Herbarium Computerized Information System (PRECIS). Finally, we thank the Institute for Plant Conservation (UCT), University of Venda, Foundation for Research Development and the Flora Conservation Committee of the Botanical Society of South Africa for their ﬁnancial support.

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70 Willis et al. areas in the Cape Floristic Region: the need to standardize for total species richness. S. Afr. J. Sci. 89, 156–61. Rebelo, A.G., Siegfried, W.R. and Oliver, E.G.H. (1985) Pollination syndromes of Erica species in the south-western Cape. S. Afr. J. Bot. 51, 270–80. Rebelo, A.G., Cowling, R.M., Campbell, B.M. and Meadows, M. (1991) Plant communities of the Riversdale plain. S. Afr. J. Bot. 57, 10–28. Rogers, J. (1988) Stratigraphy and geomorphology of three generations of regressive sequences in the Bredasdorp Group, southern Cape Province, South Africa. In Geomorphological studies in Southern Africa (G.F. Dardis and B.P. Moon, eds) pp. 407–34. Rotterdam: Balkema. Rourke, J.P. (1972) Taxonomic studies on Leucospermum R.Br. J. S. Afr. Bot. Suppl. Vol. 8, 1–194. Rourke, J.P. (1980) The Proteas of Southern Africa. Johannesburg: Purnell. SURFER (1989) Version 4. Golden Colorado: Golden Software Inc. Takhtajan, A. (1986) Floristic Regions of the World. Berkeley: University of California Press. Thwaites, R.N. (1987) Preliminary investigations into the geomorphological history of the Agulhas plain. S. Afr. Geogr. J. 69, 165–68. Thwaites, R.N. and Cowling, R.M. (1988) Soil-vegetation relationships on the Agulhas plain, South Africa. Catena 15, 333–45. Weimarck, H. (1941) Phytogeographical groups, centres and intervals within the Cape flora. Acta Univ. Lund 37, 5–143. Williams, I.J.M. (1972) A revision of the genus Leucadendron. Contr. Bolus Herbarium 3, 1–425. Willis, J.P. and Hill, D.R.H. (1992) ‘Star’ plots – diagrams with strong visual impact for simultaneously displaying variations in four to nine sample characteristics. In Elemental Analysis of Coal and its By-products (G. Vourvopoulos, ed.) pp. 75–79. Singapore: World Scientific Publishing. Willis, C.K., Lombard, A.T., Cowling, R.M., Heydenrych, B.J. and Burgers, C.J. (in press). Reserve systems for limestone endemic flora of the Cape lowland fynbos: iterative versus linear programming. Biol. Conserv. Zar, J.H. (1984) Biostatistical Analysis, 2nd edn. New Jersey: Prentice-Hall. Mendip Communications Ltd Job ID: BIO1----0071-1 383 - 71 Rev: 18-04-96 PAGE: 1 TIME: 15:40 SIZE: 55,10 OP: XX

Patterns of endemism in the limestone ﬂora of lowland fynbos 71 Appendix 1 List of the vascular plants considered as limestone endemics in this study, their Red Data Book status and individual ratings in the categories: endemism, growth form, dispersal mode, dispersal distance, seed storage and pollination type. The pollination type is listed for woody plants only.

Family Speciesa RDBb Ec GFd DISPe DISTf Sg Ph

MONOCOTYLEDONS Cyperaceae Ficinia truncata (Thunb.) Schrader 2 4 3 1 2 Iridaceae Freesia elimensis L. Bolus CR 1 2 5 1 2 Hesperantha juncifolia Goldbl. E 1 2 5 1 2 Watsonia fergusoniae L. Bolus 2 2 1 2 2 Liliaceae Haworthia variegata Bolus 2 2 1 2 2 Lachenalia muirii Baker 2 2 3 1 2 Poaceae Pentaschistis calcicola Linder var. calcicolai 24 1 2 2 P. calcicola Linder var. hirsuta Linderi 24 1 2 2 Restionaceae Thamnochortus fraternus Pill. CR 2 4 1 2 2 T. muirii Pill. V 2 4 1 2 2 T. paniculatus Masters 2 4 1 2 2 T. pluristachyus Masters V 2 4 1 2 2 DICOTYLEDONS Apiaceae Centella pottebergensis Adamson 1 1 3 1 2 2 Peucedanum sp. nova 11 5 1 22 Asteraceae Berkheya coriacea Harvey 2 1 1 2 2 2 Euryops hebecarpus (DC.) B. Nordenstam 2 1 1 2 2 2 E. linearis Harvey 1 1 1 2 2 2 E. muirii C.A. Smith E 1 1 1 2 2 2 Felicia canaliculata Grau 2 1 1 2 2 2 F. ebracteata Grau U 2 1 1 2 2 2 F. nordenstamii Grau 2 1 1 2 2 2 Helichrysum chlorochrysum DC. 21 1 2 22 Metalasia calcicola Karisj 21 1 2 22 M. erectifolia Pillansj CR 21 1 2 22 M. luteola Karisj 11 1 2 22 Oedera steyniae (L. Bol.) Anderb. and Bremerk V111222 Osteospermum subulatum DC. 1 3 3 1 2 Stoebe muirii Levyns I 2 1 1 2 2 2 Campanulaceae Lightfootia calcarea Adamson 2 1 5 1 2 2 L. microphylla Adamson U 1 1 5 1 2 2 L. squarrosa Adamson U 2 1 5 1 2 2 Roella compacta Schltr. 3 1 5 1 2 2 Ericaceae Acrostemon schlechteri N.E. Br. 1 1 1 2 2 2 A. vernicosus sp. nova 11 1 2 22 Erica berzelioides Guthrie and Bolus U 2 1 1 2 2 1 E. calcareophila E. Oliver 1 1 1 2 2 2 E. curtophylla Guthrie and Bolus 2 1 1 2 2 3 E. excavata L. Bolus 1 1 1 2 2 2 E. gracilipes Guthrie and Bolus 1 1 1 2 2 2 E. oblongiﬂora Benth. 1 1 1 2 2 2 E. occulta E. Oliver CR 1 1 1 2 2 2 Mendip Communications Ltd Job ID: BIO1----0072-1 383 - 72 Rev: 18-04-96 PAGE: 1 TIME: 15:40 SIZE: 55,10 OP: XX

72 Willis et al.

Family Speciesa RDBb Ec GFd DISPe DISTf Sg Ph

E. propinqua Guthrie and Bolus 2 1 1 2 2 2 E. pulvinata Guthrie and Bolus 1 1 1 2 2 2 E. saxicola Guthrie and Bolus 1 1 1 2 2 2 E. scytophylla Guthrie and Bolus 1 1 1 2 2 2 E. uysii H.A. Baker V 1 1 1 2 2 2 Platycalyx pumila N.E. Br. 1 1 5 2 2 3 Scyphogyne calcicola E. Oliver 1 1 5 2 2 3 Thoracosperma muirii L. Guthriek 21 5 2 22 Fabaceae Amphithalea alba Granby 2 1 3 1 2 2 Aspalathus aciloba R. Dahlgren U 2 1 4 1 2 2 A. calcarea R. Dahlgren 2 1 4 1 2 2 A. candidula R. Dahlgren U 1 1 4 1 2 2 A. pallescens Ecklon and Zeyher 2 1 4 1 2 2 A. prostrata Ecklon and Zeyher E 2 1 4 1 2 2 A. repens R. Dahlgren 1 1 4 1 2 2 A. salteri L. Bolus 1 1 4 1 2 2 A. sanguinea Thunb. subsp. sanguineak 21 4 1 22 Indigofera hamulosa Schltr. 2 1 4 1 2 2 Lebeckia sessilifolia (Ecklon and Zeyher) Benth. 2 1 4 1 2 2 Lobeliaceae Lobelia barkerae F. Wimmer 1 1 5 1 2 2 L. valida L. Bolus I 2 1 5 1 2 2 Mesembryanthemaceae Braunsia vanrensburgii (L. Bolus) L. Bolus 1 1 5 1 2 2 Ruschia calcicola (L. Bolus) L. Bolus 2 1 5 1 2 2 Penaeaceae Brachysiphon mundii Sonder CR 1 1 3 1 2 2 Polygalaceae Muraltia barkerae Levyns V 1 1 3 1 2 2 M. calycina Harvey V 1 1 3 1 2 2 M. depressa DC. 21 3 1 22 M. lewisiae Levyns 2 1 3 1 2 2 M. pappeana Harvey 2 1 3 1 2 2 M. salsolacea Chodat 2 1 3 1 2 2 M. splendens Levyns 2 1 3 1 2 2 Polygala meridionalis Levyns 2 1 3 1 2 2 Proteaceae Leucadendron muirii E. Phillips 2 1 3 1 1 2 L. meridianum I.J. Williams 2 1 3 1 1 2 Leucospermum patersonii E. Phillips 2 1 3 1 2 1 L. truncatum (Bueck ex Meissner) Rourke 2 1 3 1 2 1 Mimetes saxatilis E. Phillips 1 1 3 1 2 1 Protea obtusifolia Bueck ex Meissner 2 1 1 2 1 2 Rhamnaceae Phylica laevigata Pill. U 2 1 3 1 2 2 P. selaginoides Sonder 2 1 3 1 2 2 P. sp. nova 11 3 1 22 Rosaceae Cliffortia burgersii Oliver and Fellinghaml 11 3 1 23 Rubiaceae Galium bredasdorpense Puff 2 1 5 1 2 2 Rutaceae Acmadenia densifolia Sonder 2 1 3 1 2 2 A. heterophylla Glover 3 1 3 1 2 2 A. mundiana Ecklon and Zephyr 1 1 3 1 2 2 Adenandra rotundifolia Ecklon and Zeyher 2 1 3 1 2 2 Agathosma abrupta Pill. I 1 1 3 1 2 2 A. eriantha Steudel V 2 1 3 1 2 2 A. ﬂorulenta Sond.k 11 3 1 22 Mendip Communications Ltd Job ID: BIO1----0073-1 383 - 73 Rev: 18-04-96 PAGE: 1 TIME: 15:40 SIZE: 55,10 OP: XX

Patterns of endemism in the limestone ﬂora of lowland fynbos 73

Family Speciesa RDBb Ec GFd DISPe DISTf Sg Ph

A. geniculata Pill. 2 1 3 1 2 2 A. riversdalensis Dummer 2 1 3 1 2 2 A. sedifolia Schldl. 1 1 3 1 2 2 A. sp. nova 1113122 A. sp. nova 2113122 A. sp.nova 3113122 Diosma demissa I.J. Williams 1 1 3 1 2 2 D. echinulata I.J. Williams 2 1 3 1 2 2 D. guthriei Glover 11 3 1 22 D. haelkraalensis I.J. Williams CR 1 1 3 1 2 2 Euchaetis intonsa I.J. Williams CR 2 1 3 1 2 2 E. laevigata Turcz. 1 1 3 1 2 2 E. longibracteata Schltr. 2 1 3 1 2 2 E. meridionalis I.J. Williams 2 1 3 1 2 2 Scrophulariaceae Sutera calciphila Hilliardk 21 5 1 22 S. subspicata (Benth.) Kuntze 2 1 5 1 2 2 Sterculiaceae Hermannia concinnifolia I. Verd. I 2 1 5 1 2 2 H. muirii Pill. ex I. Verd. 1 1 5 1 2 2 H. trifoliata L. I 2 1 5 1 2 2

aAuthors of species follow Bond and Goldblatt (1984), except where indicated otherwise. bRed Data Book categories based on Hall and Veldhuis (1985): CR = critically rare, E = endangered, V = vulnerable, U = uncertain, I = indeterminate. cCategory of endemism: 1 = local, 2 = regional, 3 = Cape Floristic Region. dGrowth form: 1 = shrub, 2 = geophyte, e = forb, 4 = graminoid. eDispersal mode: 1 = wind, 2 = vertebrate, 3 = ant, 4 = ballistic, 5 = passive/other. fDispersal distance: 1 = short (passive and ant), 2 = medium (wind), 3 = long (vertebrate). gSeed storage type: 1 = canopy, 2 = soil, 3 = none. hWoody-plant pollination type: 1 = bird, 2 = insect, 3 = wind. iLinder and Ellis (1990, p. 83). jKaris (1989). kArnold and De Wet (1993). lOliver and Fellingham (1991).