Plant Ecology 142: 105–120, 1999. 105 © 1999 Kluwer Academic Publishers. Printed in the Netherlands.

Plant form and function Biogeography of prostrate-leaved geophytes in semi-arid South Africa: hypotheses on functionality

Karen J. Esler1, Phillip W. Rundel2 &PietVorster1 1Department of Botany, University of Stellenbosch, Private Bag X1, Matieland, 7602 South Africa (e-mail: [email protected]); 2Department of Biology, University of California, Los Angeles, CA 90095, USA

Received 2 November 1998; accepted in revised form 20 November 1998

Key words: Amaryllidaceae, Biogeography, Geophylly, Leaf Orientation, Succulent Karoo

Abstract Nowhere is the species diversity of geophytes greater than in the five mediterranean-climate ecosystems of the world. Of these, the Cape mediterranean zone of South Africa is the most speciose. While the relative diversity and importance of geophytes of all of the other four mediterranean regions of the world drops off sharply as one moves into adjacent winter-rainfall desert regions, geophytes in the semi-arid to arid Succulent Karoo (including Namaqualand) remain a very important component of the flora, both in terms of abundance and diversity (com- prising 13 to 29% of the regional floras in this region). Apart from species richness, there are also a number of interesting geophyte growth forms in this region. One unusual growth form is geophytes with flattened leaves that lie prostrate on the soil surface. At least eight families (Amaryllidaceae, Colchicaceae, Eriospermaceae, Gerani- aceae, Hyacinthaceae, Iridaceae, Orchidaceae and Oxalidaceae) exhibit this growth form. While this growth form is relatively common in many geophyte lineages in the Succulent Karoo biome and the Cape mediterranean zone (Fynbos biome), and occurs infrequently through the summer-rainfall temperate regions of Africa, it is virtually absent in other regions worldwide. A null hypothesis is that the prostrate leaved trait is a neutral characteristic, however biogeographical data do not support this. A neutral trait would be unlikely to show such a clear pattern of distribution. Several alternative hypotheses on the adaptive significance of this growth form are discussed. These include: avoidance of herbivory, reduction in competition from neighbors, creation of a CO2 enriched environ- ment below the leaves, reduction of water loss around the roots, reduction of water loss through transpiration, precipitation of dew on the leaves and maintenance of optimal leaf temperatures for growth.

Introduction but nowhere are they more diverse and abundant than in the five mediterranean-climate ecosystems of the Geophytes are plants that possess underground resting world (Doutt 1994; Rundel 1996). Of these, the Cape buds attached to storage organs such as rhizomes, tu- mediterranean zone of South Africa is generally the bers, bulbs or corms. Although some geophyte species most speciose (Goldblatt 1978), with geophytes com- are evergreen, many of them survive periods of en- prising up to 40% (Nieuwoudtville Wild Flower Re- vironmental stress such as summer drought or winter serve, Snijman & Perry 1987) of some regional floras cold by dying back to these underground storage or- that have been disturbed by heavy grazing. It should gans (Dafni et al. 1981). They then resprout new fo- be noted, however that Pate & Dixon (1982) have liage in the following growing season. Inflorescences recorded that percentages as high as these for some may be produced before, during or at the end of the regional floras in southwestern and western Australia. vegetative growing season, a phenology that is con- The evolutionary success of geophytes in the Cape stant for most species. Biogeographically, geophytes Mediterranean zone of South Africa extends well into are widespread around the world in many habitats, the arid parts of this region. Geophytes of the semi- 106

Figure 1. Large, broad, prostrate-leaves of (A) Massonia sp. (Hyacinthaceae Leaf size = 15 × 25 cm) and (B) Brunsvigia sp. (Amaryllidaceae Leaf size = 12 × 24 cm). arid to arid Succulent Karoo (a winter-rainfall desert the flora of the Goegap Nature Reserve near Springbok adjacent to the true mediterranean zone and incorpo- where geophytes make up 16% (and petaloid mono- rating Namaqualand) remain a very important compo- cots, 13%) of the flora (Van Rooyen et al. 1990). In the nent of the flora, both in terms of abundance and di- Karoo Garden Reserve near Worcester they comprise versity (Snijman 1984; Goldblatt 1986; Duncan 1988; approximately 29% of the flora (Perry et al. 1979). Hilton-Taylor 1996). The remarkable diversity of geo- In contrast, the relative diversity and importance of phytes in the Succulent Karoo can be seen clearly in geophytes in all of the other four mediterranean re- 107 gions of the world drops off sharply as one moves Methods into winter-rainfall desert regions (Rundel 1996). Geo- phytes comprise only about 1% of the floras of the The relative and absolute species diversity of na- winter rainfall zone of the Mojave and the Sonoran tive geophytes within the five mediterranean floras of Desert in North America, and similarly small frac- the world was extracted from a variety of published tions of the winter-rainfall Atacama Desert of Chile, data sources (Table 1). Within the southern African northern Sahara Desert, and desert areas of Western flora, an analysis of the biogeographical patterns of Australia (Rundel 1996). geophytes with prostrate leaves was conducted on Not only is the species diversity of geophytes in species in the families Amaryllidaceae, Colchicaceae, the Succulent Karoo remarkable, but so is the growth Eriospermaceae, Hyacinthaceae, Iridaceae and Orchi- form diversity. In addition to typical monocot geo- daceae. Species were considered to be prostrate-leaved phyte growth forms with upright rosettes of basal if they possessed broad leaves adpressed (or more-or- leaves, there is an unusual growth form that is rela- less adpressed) to the soil surface. In addition to per- tively rare elsewhere. These are geophytes with leaves sonal communications from A. Le Roux & C. Boucher that lie fully pressed against the soil surface (‘geo- and P. Goldblatt & J. Manning, the following source phylly’ (sensu Eller & Grobbelaar 1982), referred to material was referenced: Adamson & Salter 1950; as ‘prostrate-leaved geophytes’ in this paper). This Bond & Goldblatt 1984; Snijman 1984; Le Roux growth form is distinct from the basal rosettes com- & Schelpe 1988; Du Plessis & Duncan 1989; Jeppe monly found in North American desert annuals (Mul- 1989; Arnold & De Wet 1993 and Shearing & Van roy & Rundel 1977). Prostrate geophyte leaves are Heerden 1994. Species described as prostrate or more- frequently large and broad, in contrast to North Amer- or-less prostrate in at least part of their distribution ican basal rosettes of desert annuals that have multiple were included in the lists (Appendix 1). The prostrate small and thin leaves. The prostrate-leaf growth form, leaf character, although often highly consistent within which often includes one or two broad leaves ori- a species (e.g., in Ammocharis coranica), can also be ented 180◦ from each other (although there can be variable in some species. Species were included in up to five leaves arranged in a basal rosette), can be the analysis if they were prostrate in at least part of found in at least eight Succulent Karoo families. These their distribution. A complete study was conducted on include species from petaloid monocotyledonous fam- the Amaryllidaceae, however for other families, the ilies but remarkably this characteristic is also noted lists provided should not be considered exhaustive. in dicotyledonous geophytes, including species from Nomenclature was obtained from the TURBOVEG the Oxalidaceae and Geraniaceae (not included in this 9.42 program (South African Version). analysis). Commonly encountered prostrate-leaved For each of the above-mentioned families, locali- geophytes in the Succulent Karoo include Brunsvigia ties, habitat descriptions and leafing times were com- and Haemanthus (Amaryllidaceae); Lachenalia, Mas- piled and summarized. Numbers of species falling into sonia and Whiteheadia (Hyacinthaceae); Eriosper- the winter-, summer- or all-year rainfall regions were mum (Eriospermaceae); and Satyrium and Holothrix determined (Figure 2). If a species fell into two or (Orchidaceae). more rainfall regions, it was scored for both regions. In this paper, we provide a biogeographical analy- Specific emphasis was placed on the family sis of the southern African prostrate-leaved geophytes. Amaryllidaceae that has the highest number of species We ask the questions: Why are there so many geo- of flat-leaved geophytes of the eight families under phytes in the Succulent Karoo compared to other investigation. For this family, detailed habitat descrip- winter-rainfall deserts? What selective pressures have tions were compiled, as well as flowering and leafing resulted in the high incidence of the prostrate leaf times. For each genus in the family Amaryllidaceae, form among geophytes in the winter-rainfall region of the distribution of species with and without prostrate southern Africa? Despite their charismatic appearance leaves was mapped at a 1-degree grid scale (100 km × (Figure 1), very little research has been conducted on 100 km). these plants, although a variety of hypotheses relating to the functional significance of this unusual growth form exist. These are reviewed and discussed. 108 ureau (1986). Selected climate data for stations in winter, summer and all-year rainfall regions of South Africa. Data for climate diagrams obtained from Weather B Figure 2. 109

Table 1. Absolute and relative diversity of geophytes in floras from the five regions with metiterranean-type ecosystems. Table partially compiled from Rundel (1996).

Region Mm Number of species Percentage (%) Total Monocot Geophyte Monocot Geophyte Geo/Mono Source

California

Santa Monica Mountains 250–550 644 96 18 14.9 2.8 18.8 Rundel (1996) Eastern Mojave Desert 140–340 717 85 10 11.9 1.4 11.8 Rundel (1996) Total Flora – 4844 823 262 18.2 5.4 31.8 Hickman (1993)

Chile

Total Flora – 4877 892 261 18.3 5.4 29.3 Marticorena (1990)

Western Mediterranean

Alicante 275 1582 270 67 17.1 4.2 24.8 Rigual (1984)

Western Australia

Perth Region 600–1400 1510 462 190 30.6 12.6 41.1 Marchant et al. (1987)

South Africa

Cape Hangklip 718–955 1407 460 216 32.7 15.4 47.0 Boucher (1977) Nieuwoudtville 342 299 114 119 38.1 39.8 104.4 Snijman & Perry (1987) ∗ Goegap 162 441 114 56 25.9 13.0 49.1 CNC unpubl. spp. list Port Nolloth 70 300 54 42 18.0 14.0 77.8 Desmet (1997)

∗ CNC = Cape Nature Conservation.

Results see Pate & Dixon 1982) is also low in comparison with the mediterranean flora of South Africa (Table 1). Geophytes are an important component of the floral di- In southern Africa, at least seven monocotyle- versity throughout the winter-rainfall region of South donous and two dicotyledonous families (the Oxali- Africa. At the mesic end of the gradient in the Cape daceae and Geraniaceae, not dealt with in this paper) mediterranean zone, geophytes represent 15 (Cape have geophyte species with prostrate leaves (Table 2, Hangklip) to 40% (Nieuwoudtville) of the flora and as Appendix 1). Prostrate-leaved monocots are over- mean annual rainfall declines into the mediterranean whelmingly concentrated in the winter-rainfall region desert to the northwest (Succulent Karoo biome, in- of southern Africa (40 to 100%, Table 2, Figures 3 and cluding Namaqualand), geophytes maintain their im- 4a–f). In the Amaryllidaceae, which has the largest portance (Table 1). Geophytes can represent from 13 concentration of prostrate-leaved species (at least 50 (Goegap) to 14% (Port Nolloth) of the flora in the species from 8 genera), 79% are found within the Succulent Karoo (Table 1). In general, these pro- winter-rainfall region (Figure 2, Table 2). In contrast, portions are 3 to 7 times that of geophytes in the non prostrate-leaved species in the same genera do not mediterranean region floras of California, Chile, or exhibit this clear biogeographical pattern. There are the western Mediterranean Basin (Table 1). The repre- two centers of diversity associated with the prostrate- sentation of monocotyledonous geophytes in the flora leaved species in the Amaryllidaceae in the Namaqua- of California is 5%, but ranges from 3% in arid land region of the Succulent Karoo. The first (9 species mediterranean ecosystem regions to only 1% in the per 1 degree grid square) is in the Springbok grid winter-rainfall zone of the Mojave Desert (Table 1). (2917), south of the Orange river, and the second, a The representation of geophytes in the Chilean, west- larger area (from 9 to 16 species per 1 degree grid ern Mediterranean and western Australian floras (but square) lies south of the Olifants river and runs down the coast to Langebaan (3118; 3119; 3218; 3219). This 110

Figure 3. Distribution of prostrate-leaved species within the family Amaryllidaceae. Numbers of prostrate-leaved species are indicated at a resolution of a 1 degree grid square (100 × 100 km).

Table 2. Diversity and distribution of prostrate-leaved geophytes Table 3. Absolute number and proportion of species in genera in seven southern African plant families. of the family Amaryllidaceae that have prostrate (or more-or-less prostrate) leaves. Family Diversity Distribution (%) # genera # spp. Winter All year Summer Genus Total spp Prostrate spp % Prostrate spp rainfall rainfall rainfall Ammocharis 21 50 Amaryllidaceae 8 50 79 9 12 Apodolirion 62 33 Colchicaceae 1 8 73 27 0 Brunsvigia 17 11 65 Eriospermaceae 1 10 50 42 8 Crossyne 2 2 100 Hyacinthaceae 14 30 67 23 10 Cybistetes 1 1 100 Iridaceae 10 21 100 0 0 Gethyllis 35 9 26 Orchidaceae 5 9 50 43 7 Haemanthus 22 9 41 Strumaria 23 10 44

area covers a range of vegetation types from the true Succulent Karoo vegetation of sparsely distributed winter-rainfall species (81%) were associated with dwarf succulent shrubs, to the more mesic mediter- low, open vegetation and/or exposed areas (sometimes ranean shrubland, Strandveld, which is associated created by fire in the Fynbos biome). Species occur- with the sandy coastal zone. ring in the non-seasonal or summer-rainfall zones are Common to all of these areas is the presence of more commonly associated with sheltered or shady open gaps in vegetation where these species are of- habitats (60%), as are most of the prostrate-leaved ten found growing. In an analysis of the habitats species that occur in the tropics (Lock in press). of prostrate-leaved Amaryllidaceae, the majority of Despite the clear biogeographical patterns of prostrate-leaved geophytes in the winter-rainfall re- 111

Figure 4. Distribution of prostrate-leaved species in (A) Apodolirion,(B)Brunsvigia,(C)Crossyne,(D)Gethyllis,(E)Haemanthus and (F) Strumaria in the family Amaryllidaceae. The entire distributions (prostrate and non-prostrate) of each genus are shaded. Numbers of prostrate-leaved species are indicated at a resolution of a 1 degree grid square (100 × 100 km).

Figure 4. Continued. 112

Figure 4. Continued.

Figure 4. Continued. 113

Figure 4. Continued.

Figure 4. Continued. 114 gion of South Africa, there are some species which oc- drought and no rain at all in summer are not a rare cur in the summer-rainfall regions of southern Africa occurrence in California (MacMahon & Wagner 1985) and even the drier parts of tropical Africa (Lock in and Chile (Hajek & di Castri 1975; di Castri & Ha- press). These include Costus spp. (Costaceae formerly jek 1976). This can lead to early growth stimulation Zingiberaceae), Chlorophytum spp. (Anthericaceae) in geophytes but leaving insufficient soil moisture to (both from monocotyledonous genera that are absent allow these plants to complete flowering and to set or poorly represented in the winter-rainfall region of seed in the spring. Such years would have a nega- South Africa) as well as a variety of species in the tive impact on geophytes by draining the carbohydrate Orchidaceae. Notable exceptions to the general pattern reserves in their below-ground storage organs (Rossa in the Amaryllidaceae are Brunsvigia burchelliana and & von Willert 1998). Climatic comparisons between Haemanthus humilis ssp. humilis, both of which have the South African and North American winter-rainfall very wide distributions in the summer-rainfall zone of deserts (Esler et al. 1999; Esler & Rundel 1999) have southern Africa. These species account for much of shown that in the Succulent Karoo, relatively mild the pattern in the summer-rainfall zone seen in Fig- temperatures and highly predictable rains during the ures 4b and 4e. Despite these exceptions, it is clear winter season as well as the high incidence of rains that, nowhere else are prostrate-leaved species found outside winter, allow early initiation of growth in au- in such diversity or abundance as in the Cape mediter- tumn but also minimize the risk of not allowing a ranean zone and the adjacent winter-rainfall, semi-arid complete growth cycle to occur. Under these condi- to arid Succulent Karoo biome. In fact, this growth tions in the Cape Region where rainfall is both higher form is virtually absent in other desert areas of the and more predictable, geophytes can persist as they world. do. With this scenario, it is possible to explain the In the Amaryllidaceae, there are clear phenolog- abundance of geophytes in the semi-arid to arid Suc- ical differences between summer- and winter-rainfall culent Karoo, but it does not address the more vexing prostrate-leaved species. Species in the winter-rainfall question of diversity. region do not retain their leaves during the hot, dry The second question is what selective pressures summer months (November – February) while some have resulted in the high incidence of the prostrate-leaf species in the summer-rainfall region retain their form among geophytes in the winter-rainfall region of leaves throughout the year (Figure 5). southern Africa? When placed in a broad systematic framework, it is possible to argue that the character may have evolved only a few times in any lineage. For Discussion example, in the Amaryllidaceae, Haemanthus, Geth- yllis and Apodolirion are all placed in the tribe Hae- The first question that we ask is why are there so mantheae, while Brunsvigia, Crossyne and Strumaria many geophytes in the Succulent Karoo compared to are sister genera in the tribe Amaryllideae. While there other winter-rainfall deserts? While ecophysiological are specific lineages within some families in which investigations might provide some ideas as to the suc- prostrate leaves have evolved, it is striking that a di- cess of this life form in the region, the question of versity of families display this characteristic. These speciation is less easy to answer. Some ecophysio- groups are all ecologically successful in the winter logical data exist, investigating the seasonal growth rainfall regions. Many of the genera with prostrate- activities and physiological traits of geophytes in the leaves also have upright or intermediate-leaf forms. Cape mediterranean zone (Ruiters et al. 1993a, b; This emphasizes the importance of selection (ecophys- Ruiters 1995), but less is known about geophytes in iological selection as we argue later) and the possibil- the Succulent Karoo. However, Rossa & von Willert ity that prostrate-leaf morphology is a homoplasy in (1998), in a study of physiological characteristics of many groups. geophytes in Namaqualand, show how aseasonal rain- While the prostrate leaf form has been described fall can replenish the water content of below-ground for some species in the summer-rainfall parts of Africa storage organs. They suggest, as we have (Esler et al. (Lock in press), it is clear that there is some functional 1999), that the poor success of geophytes in other significance attached to this unusual growth form in comparable desert regions appears to relate to the un- the winter-rainfall region. It is tempting to suggest predictability of spring growing conditions. Climatic that all prostrate-leaved species have evolved under the patterns such as early rains followed by late winter same selective pressures but the answer may not be so 115

Figure 5. Leafing phenology of prostrate-leaved Amaryllidaceae (see Appendix 1 for species list) occurring in the summer and winter rainfall regions. simple. There are apparent differences in the types of this hypothesis might be reasonable for a few species, habitats and vegetative phenology of prostrate-leaved it does not explain the distinct distribution pattern species occurring in the summer versus winter-rainfall of the majority, since herbivory is a selective force regions. The majority of winter-rainfall species are throughout southern Africa (Owen-Smith & Danck- associated with low, open vegetation and/or exposed werts 1997). Many of the prostrate-leaved species areas and having a distinct winter growth period, while of Amaryllidaceae and Colchicaceae are known to species in the non-seasonal or summer-rainfall regions contain toxic alkaloids in their leaves (Watt & Breyer- are more commonly associated with sheltered or shady Brandwijk 1962) which generally deter mammals, al- habitats and have an evergreen or summer growth though apparently not all domestic livestock (S. Todd, period. We restrict our discussion to the far more pers. comm.). Insects, which are often resistant to abundant species concentrated in the winter-rainfall plant chemical defenses, would not necessarily be regions, however we recognize that the different habi- physically deterred by this particular plant form. tats of prostrate-leaved species may provide insights to (2) Prostrate leaves reduce competition from neigh- explain the biogeographical patterns observed. bors. While we can find no reference to this in the A variety of hypotheses have been proposed to literature, reduction of competition from neighbors explain the prostrate-leaf growth form, and future re- may well be a selective factor for the summer-rainfall search may well allow us to highlight the important species that are found in grassland vegetation. How- factors. A null hypothesis is that the prostrate-leaved ever, it does not explain the abundance of prostrate- trait is a neutral characteristic, however biogeograph- leaved species in the winter-rainfall region where ical data do not support this. A neutral trait would be grasses (and neighbors in general) are less abundant. unlikely to show such a clear pattern of distribution. Many of the winter-rainfall species grow in fairly ex- What follows is a brief synopsis and discussion of posed areas with little herb cover away from shrub existing hypotheses, to which we add our own. canopies. (1) Avoidance of herbivory. Eller & Grobbelaar (3) Prostrate leaves create a CO2 enriched envi- (1982), who worked on Ledebouria ovatifolia (Hy- ronment below the leaves (Lock in press). A moist acinthaceae), one of the summer-rainfall prostrate- environment under leaves (see hypothesis 4) could leaved species, suggested that leaves adpressed to the encourage activity of microorganisms, which in turn soil surface are more difficult for herbivores to reach produce CO2. ACO2-enriched environment might in- and thus protect the plants against herbivory. While crease photosynthetic CO2 uptake, which is generally 116 low in Namaqualand geophytes (Rossa & von Willert in the early morning hours (K.J.E. & P.W.R., un- 1998). While this would certainly provide an advan- publ. data). This cooling is frequently sufficient to tage for prostrate-leaved species with stomata on their reach dew point temperature with the condensation lower leaf surfaces, this hypothesis is not consistent of droplets of water on the leaf surfaces. Such local- with the biogeographical patterns noted for prostrate- ized dew condensation is common, especially since leaved species, as it does not explain why their diver- relatively humid air masses are frequently present sity is low in the summer-rainfall region. Vorster & over much of the Succulent Karoo, and would logi- Spreeth (1996), in a study of the leaf anatomy of South cally provide an important source of soil moisture for African Amaryllidaceae, noted much variation in the these species. While direct water absorption is un- positioning of stomata. Brunsvigia and Strumaria had likely, dew on the leaves could funnel down to the mostly abaxial stomata, while some species of Hae- center of the plants close to the bulb. Alternatively, manthus had abaxial stomata and others had an equal a moist environment around the leaves would reduce distribution on both surfaces. evapotranspiration gradients significantly, providing While hypotheses 1 to 3 could potentially explain an indirect advantage to the water balance of these aspects of the evolution of the prostrate-leaf form, species. We are presently investigating this hypothesis all of them fail to explain the predominance of these using a variety of approaches including modeling of species in the arid to semi-arid winter-rainfall region. micro-meteorological data and stable isotope analysis The following hypotheses, while not mutually exclu- of source water pools as well as measurements made sive, could provide a better insight into the distribution in the field. It is interesting to note that in contrast of these species. These have two primary themes to the winter-rainfall species, most of the summer- (a) water economy (hypotheses 4–6) and (b) energy rainfall prostrate-leaved Amaryllidaceae grow under balance (hypothesis 7). bushes where dew is uncommon. (4) Prostrate leaves reduce the rate of water loss (7) Prostrate leaves track soil temperatures, thereby around the roots. Lovegrove (1993) suggested that raising leaf temperatures during mid-day and main- prostrate leaves act as water-trapping umbrellas, re- taining optimal leaf temperatures for growth. Broad, ducing the rate of water loss, and creating favorable flat leaves that are closely pressed to the soil sur- microclimates for growth. Water loss through tran- face track soil temperatures during the day rather than spiration could be reduced significantly if saturated air temperature. Under winter growth conditions, this air is trapped below prostrate leaves, but this would could provide a second advantage. The soil surface, only hold for species that have stomata mostly on the and thus, the leaf tissue, heats up several degrees undersurface of the leaves. over air temperature, providing leaf temperatures more (5) Prostrate leaves have a significant boundary layer favourable for photosynthesis on cool winter days than effect. Ground-hugging leaves have the advantage of would otherwise occur. We are currently testing this reduced wind-speeds and increased boundary layers, hypothesis using micro-meteorological modeling and factors that could lower transpirational loss signifi- field measurements. The prediction is that since the cantly. While this hypothesis has yet to be tested on mild winter temperatures of Namaqualand allow a species in the winter-rainfall region, results from a winter growth phenology which is distinct from the field investigation on a summer-rainfall species, Lede- spring growth which characterizes plant activity in bouria ovatifolia (Eller & Grobbelaar 1982) suggest North American deserts (where winter temperatures that boundary layers do not necessarily reduce transpi- are lower, Esler & Rundel (1999)), morphological and rational loss. This hypothesis may hold especially for physiological adaptations which might further aid this such species of Brunsvigia, Strumaria, Massonia and winter growth (e.g., Rundel et al. 1995) would be an Eriospermum that have evolved wind dispersed fruits advantage for species growing in this environment. and seeds and are situated in exposed, windy habitats In contrast, raised leaf temperatures for the summer (D. Snijman, pers. comm.). rainfall species would be maladaptive, and that would (6) Prostrate leaves track soil temperature, allowing explain the understory habitats of these species. plants to drop below dew point temperature in the Galil (1958 in Galil 1980) notes that a rapid change early mornings, thereby precipitating dew. Our obser- in ambient soil temperature may stimulate contrac- vations on species in the winter-rainfall region show tile root formation in geophytes. A further possibility, that prostrate-leaved geophytes tracking soil tempera- therefore, is that prostrate leaves may maintain the tures can cool several degrees below air temperature burial depth of bulbs with increased insulation by the 117 leaves thus minimizing the quantity of food materials Appendix 1 required for new shoots to reach the soil surface if bulbs move deeper into the soil. How this relates to Appendix 1. List of petaloid monocot species with the habitat of prostrate-leaved species has yet to be ∗ prostrate and more-or-less prostrate ( ) leaves in south- determined. ern Africa. Numbers after the names indicate distrib- The arid mediterranean zone of southern Africa ution; 1 = winter rainfall; 2 = all year rainfall; 3 = contains a wealth of species that have an unusual summer rainfall. suite of growth form characteristics. Prostrate-leaved Family Colchicaceae geophytes provide the opportunity to investigate what selective forces might have played a role in the evolu- Androcymbium capense (L.) K.Krause 1/2 tion of the region’s geophyte flora. Having discussed Androcymbium ciliolatum Schltr. & K.Krause 1 a range of hypotheses, and identified possible in- Androcymbium cuspidatum Baker 1 consistencies with the observed biogeographical pat- Androcymbium dregei C.Presl 1 terns, we are able to generate testable predictions, Androcymbium eucomoides (Jacq.) Willd. 1/2 some of which we are currently investigating. We be- Androcymbium irroratum Schltr. & K.Krause 1 lieve, however, that the mild winter temperatures and Androcymbium melanthioides Willd. 1/2 Androcymbium pulchrum Schltr. & K.Krause 1 predictable rainfall characteristics of this region are central to the explanation as to why prostrate-leaved Family Eriospermaceae species are so abundant in this area. Eriospermum breviscapum Marloth ex P.L.Perry 1 Eriospermum capense (L.) T.M. Salter 1/2 Eriospermum cooperi Bak. 3 Acknowledgements Eriospermum cordiforme Salter 1/2 Eriospermum dyeri Marloth ex Archibald 2 John Manning, Peter Goldblatt, Dee Snijman, Alison Eriospermum nanum Marloth 1 van der Merwe and Ernst van Jaarsveld provided in- Eriospermum porphyrium Archibald 2 formation used to compile the list of prostrate-leaved Eriospermum pustulatum Marloth ex A.V.Duthie 1 geophytes, for which we are grateful. Ulli Buratti Eriospermum subincanum P.L.Perry 1 and Michelle Collins assisted in compiling the lists. Eriospermum zeyheri R.A.Dyer 2 Richard Cowling and Dee Snijman provided useful comments on the manuscript. This work was sup- Family Hyacinthaceae ported by the Foundation for Research and Devel- Albuca cooperi Baker 1 ∗ opment, under the research project ‘Plant Form and Amphisiphon stylosa W.F. Barker 1 Function in an extraordinary desert: the western suc- Androsiphon capense Schltr. 1 culent Karoo’. This article is a publication of the Daubenya aurea Lindl. 1 ∗ 1995 and 1996 South African International Arid Lands Eucomis regia (L.) L’Her.´ 1 ∗ Expeditions. Lachenalia angelica W.F.Barker 1 Lachenalia congesta W.F.Barker 1 Lachenalia kliprandensis W.F.Barker 1 Lachenalia latifolia Tratt. 1/2 ∗ Lachenalia polypodantha Schltr. ex W.F.Barker 1 Lachenalia pusilla Jacq. 1 Lachenalia stayneri W.F.Barker 1 Lachenalia trichophylla Baker 1 Ledebouria ovatifolia (Bak.) Jessop 3 Ledebouria undulata (Jacq.) Jessop 1 Massonia depressa Houtt. 1/2 Massonia echinata L.f. 1/2 Massonia grandiflora Lindl. 1 Massonia jasminiflora Burch. ex Baker 3 Massonia pustulata Jacq. 1/2 118

Neobakeria angustifolia (L.f) 1 Strumaria discifera Marloth ex Snijman ssp. bulbifera ∗ Neobakeria comata (Baker) Schltr. 2/3 Snijman 1 ∗ Neobakeria heterandra Leight. 1 Strumaria discifera Marloth ex Snijman ssp. discifera 1 Neobakeria namaquensis Schltr. 1 Strumaria gemmata Ker- Gawl. 1 ∗ Ornithogalum fimbrimarginatum Leight. 1/2 Strumaria karooica (W.F.Barker) Snijman 1 ∗ Ornithogalum graminifolium Thunb. 1/2 Strumaria leipoldtii (L.Bolus) Snijman 1 ∗ Ornithogalum unifolium Retz. 1 Strumaria massoniella (D.& U.Müll.-Doblies) Snijman 1 Polyxena ensifolia (L.f.) Schonland 1/2 Strumaria merxmuelleriana Rhadamanthus platyphyllus B.Nord. 1/2/3 (D.& U.Müll.-Doblies) Snijman 1 Whiteheadia bifolia (Jacq.) Baker 1 Strumaria salteri W.F.Barker 1 Strumaria villosa Snijman 1 Family Amaryllidaceae Strumaria watermeyeri L.Bolus ssp. botterkloofensis Ammocharis coranica (Ker Gawl.) Herb. 3 (D.& U.Müll.-Doblies) ∗ Apodolirion amyanum D.Müll.-Doblies 1 Snijman 1 ∗ Apodolirion lanceolatum (L.f.) Benth. 2/3 Strumaria watermeyeri L.Bolus ssp. watermeyeri 1 ∗ Brunsvigia appendiculata Leight. 1 Family Iridaceae Brunsvigia bosmaniae Leight. 1 Brunsvigia burcheiliana Herbert 1/2/3 Freesia caryophyllacea (Burm.f.) N.E.Br. 1 Brunsvigia comptonii W.F.Barker 1 Freesia fergusoniae L.Bolus 1 ∗ Brunsvigia gregaria R.A.Dyer 1/2 Galaxia grandiflora Andrews 1 Brunsvigia herrei Leight. ex W.F.Barker 1 Galaxia luteo-alba Goldblatt 1 Brunsvigia marginata (Jacq.) Aiton 1 Galaxia ovata Thunb. 1 ∗ Brunsvigia minor Lindl. 1 Galaxia stagnalis Goldblatt 1 ∗ Brunsvigia orientalis (L.) Aiton ex Eckl. 1 Galaxia variabilis G.J.Lewis 1 Brunsvigia radula (Jacq.) Aiton 1 Galaxia versicolor Salisb. ex Klatt 1 ∗ ∗ Crossyne flava (Snijman) D & U.Müll.-Doblies 1 Geissorhiza bolusii Baker 1 ∗ Crossyne guttata (L.) D & U.Müll.-Doblies 1 Geissorhiza corrugata Klatt 1 ∗ Cybistetes longifolia (L.) Milne-Redh. Schweick. 1 Geissorhiza ovalifolia R.C.Foster 1 Gethyllis barkerae D. Müll.-Doblies 1 Geissorhiza ovata (Burm.f.) Asch. & Graebn. 1 ∗ Gethyllis hallii D.Müll.-Doblies 1 Geissorhiza parva Baker 1 Gethyllis lata L.Bolus ssp. lata 1 Gynandriris pritzeliana (Diels) Goldblatt 1 Gethyllis lata L.Bolus ssp. orbicularis D.Müll.-Doblies 1 Hesperantha montigena Goldblatt 1 Gethyllis linearis L.Bolus 1 Micranthus alopecuroides (L.) Rothm. 1 ∗ ∗ Gethyllis oliverorum D.Müll.-Doblies 1 Moraea serpentina Baker 1 ∗ Gethyllis pectinata D.Müll.-Doblies 1 Moraea tortilis Goldblatt 1 ∗ Gethyllis roggeveldensis D.Müll.-Doblies 1 Sparaxis caryophyllacea Goldblatt 1 ∗ Gethyllis uteana D.Müll.-Doblies 1 Syringodea derustensis M.P.de Vos 1 ∗ Gethyllis villosa (Thunb.) Thunb. 1/2 Xenoscapa fistulosa (Spreng. ex Klatt) Goldblatt 1 ∗ Haemanthus albiflos Jacq. 1/2/3 & J.C.Manning ∗ Haemanthus amarylloides Jacq. ssp. amarylloides 1 Haemanthus amarylloides Jacq. ssp. toximontanus Snijman 1 Family Orchidaceae Haemanthus carneus Ker-Gawl. 3 ∗ Bartholina burmanniana (L.) Ker Gawl. 1/2 Haemanthus coccineus L. 1 ∗ Bartholina etheliae Bolus 1/2 Haemanthus deformis Hook.f. 3 ∗ Habenaria dregeana Lindl. 2 Haemanthus humilis Jacq. ssp. humilis 3 Holothrix aspera (Lindley) Reichb.f. 1 Haemanthus lanceifolius Jacq. 1 ∗ Holothrix secunda (Thunb.) Reichb.f. 1 Haemanthus pubescens L.f. ssp. arenicola Snijman 1 Liparis capensis Lindl. 2/3 Haemanthus pubescens L.f. ssp. leipoldtii Snijman 1 Satyrium bicorne (L.) Thunb. 1/2 Haemanthus pubescens L.f. ssp. pubescens 1 Satyrium erectum Sw. 1/2 Haemanthus sanguineus Jacq. 1 Satyrium humile Lindley 1 Strumaria chaplinii (W.F.Barker) Snijman 1 119

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