REVIEWS Plant diversity in mediterranean-climateregions Richard M. Cowling, Philip W. Rundel, Byron B. Lamont, Mary Kalin Arroyo and Margarita Arianoutsou

he five mediterranean- The high plant diversity of mediterranean- regions except those in Australia climate regions of the world climate regions has attracted much and , where only a few (Fig. 1, Box 1) occupy less attention over the past few years. such species appear in the im- Tthan 5% of the Earth’s This review discusses patterns and mediate post-fire periodislr. The surface yet harbour about 48250 determinants of local, differential and average diversity of fynbos, kwon- known vascular plant species regional plant diversity in ail five regions. gan and mallee communities in the (Table l), almost 20% of the world Local diversity shows great variation within western regions, which are more total. These regions also have and between regions and explanations for nutrient-impoverished and have exceptionally high numbers of rare these patterns invoke a wide range of high winter rainfall, is similar to that and locally endemic plant+5 and hypotheses. Patterns of regional diversity in the less-seasonal and more-fertile include two recognized species are the result of differential speciation eastern regions of mediterranean flocks, one in southwestern Aus- and extinction rates during the South Africa and AustraliasJ8. tralia and the other in the south- Quaternary. These rates have been western Cape, South Africas. These influenced more by the incidence of Determinants patterns are of interest because fire and the severity of climate change A wide range of equilibrium they refute predictions on the rela- than by environmental heterogeneity. and non-equilibrium theories have tionships between diversity and Ail regions have a high number of rare been invoked to explain local di- area, productivity and latitude3a416. and locally endemic taxa that survlve as versity and species coexistence in There has been much interest small populations, many of which are mediterraneanclimate . recently in the patterns, determi- threatened by habltat transformation. These include differentiation along nants and function of biodiversity structural or growth-form niche in mediterranean-climate ecosys- axes3Jg, spatial variation in re- tems (e.g. Refs 6-8). Here, we re- Richard Cowling is at the Institute for Plant source availabilii$20, disturbances view patterns and determinants of Conservation, University of Cape Town, Private Bag, such as firen and grazing22, Rondebosch 7700, South Africa; Phil Rundel is at plant species diversity and rarity neighbourhood effectsigZ23,lottery the Laboratory of Biomedical and Environmental at various spatial scales. We also Sciences, University of , Los Angeles, processes iiJ4, and the influence of highlight aspects from research in CA 90024-1786, USA; Byron Lamont is at the School regional processe@. mediterraneanclimate regions that of Environmental Biology, Cur-tin University of Hustonr interprets the relative are salient to the evolution and con- Technology, PO Box U1987, Perth, WA 6001, diversity of mediterranean plant servation of plant biodiversity in Australia; Mary Arroyo is at the Dept of Biology, communities in terms of a general general. Faculty of Science, University of , Santiago, model where low rates of competi- Chile; Margarita Arianoutsou is at the Dept of Ecology tive displacement result from low Local diversity and Systematics, Faculty of Biology, University of soil nutrients and summer drought, Patterns Athens, 15784 Athens, Greece. coupled with a moderately high At the local scale (0.1ha or less), frequency of disturbance in the the vegetation of mediterranean- form of fire and grazing. There is climate regions is moderately species-rich by global stand- good evidence from several mediterranean-climate regions ards, on average less than half that recorded for tropical that plant diversity is a unimodai function of productivity or rainforests, but much richer than most other temperate other measures of nutrient supply9JiJ6. Most studies on communitieG. Within each region, there is great variation within-guild coexistence are for communities of proteoid in local diversity. Highest diversity occurs in frequently (Proteaceae) shrubs in fynbos and kwongan. Cody19found burnt open heath and scrub on nutrient-poor soils clear patterns of segregation into leaf-dimension niches, (Australian kwongan and South African fynbos), and the and evidence for character displacement, for proteoid heavily grazed shrublands and woodlands of the eastern shrubs in fynbos (see also Ref. 11). Using a null model to (Table 2, see Box 1 for description of generate a relationship between local and regional diversity vegetation types). Denser shrublands (e.g. ) and among southwestern Australian Banksiu (Proteaceae) woodlands (e.g. eucalyptus forest) have lower diversity. species, Richardson et al.25 recently showed that local di- However, diversity in the immediate post-fire year in chap- versity of real assemblages was rapidly saturated, suggest- arral, when a rich fire-ephemeral flora coexists with the re- ing that local-scale processes limit diversity. However, they sprouts and seedlings of long-lived shrubs, approximates could find no conclusive evidence that local assemblages that of mature fynbos and kwonganio. . are consistently structured by growth form or regeneration Growth form diversity is low in fynbos and kwongan, niche differentiation. instead, they argued that habitat spe- which include many structurally and functionally similar spe cialization of bank&s23 causes lower diversity than would ties, often belonging to the same genusii-13, but it is high in be predicted from niche differentiation and from the size of vegetation that seldom burns, for example, South African the regional species pool. scrub-forest13 and Chilean matorrali4. Annuals comprise 15% Few generalizations emerge from the many studies or more of the local floras in all the mediterranean-climate on local diversity in mediterranean vegetation. It appears,

362 0 1996, Elsevkr Science Ltd PII: SOlSS-5347(96)10044-6 TREE uof. I I, no. 9 September 1996 REVIEWS however, that in frequently burnt shrublands on nutrient- poor soils (fynbos and kwongan), relatively low growth rates and the reshuffling of competitive hierarchies owing to differential post-fire regeneration, allows the coexistence of many seemingly equivalent shrubs and long-lived graminoidsl3Js. On more fertile soils, where fire-free inter- vals are longer (chaparral, , phrygana), shorter- lived species are rapidly excluded by the developing shrub canopyiOJ7. In Chilean and grassy shrublands and woodlands in the eastern Mediterranean Basin, both of which seldom burn, grazing by livestock permits the coexist- ence of both short-lived and long-lived speciesi4J7J2.

Differentiation diversity Differentiation diversity refers to compositional change along habitat gradients (beta diversity) and along geo- Fig. 1.The five mediterranean-climate regions of the world. graphical gradients (gamma diversity)z. High differentiation diversity is largely the product of the evolution of habitat specialists and geographical vicariants2a3. Comparable and exceptionally high levels of differen- western Australiad. A similar explanation has been invoked tiation diversity, amounting to almost complete turnover of for the species-rich but topographically and climatically fire-killed shrub species along edaphic and geographical uniform lowlands of the southwestern Capes. gradients, have been recorded in the strongly winter rainfall Cowling et al.3 have suggested that regional diversity in zones of southwestern Australia and the southwestern mediterranean-climate regions is the product of local diver- Cape394Js.In the southeastern zones of these regions, which sity and differentiation diversity in relation to environmen- experience more summer rain, differentiation diversity is tal heterogeneity. Thus, regions with high local diversity much lower3Js. In California, high turnover is associated and high turnover associated with long habitat and geo- mainly with predominantly fire-killed shrub lineages (Arcto- graphical gradients will support species-rich landscapes and and short-lived herbs or annu- sfaphylos Ceanothus) (Table 3). The driving force is rapid speciation and/or low al&21.29.A similar pattern occurs in the Mediterranean Basin extinction rates of habitat specialists and geographical where the shrub lineages include and Astragalus, Genista vicariant@. This would explain why regional diversity and the herbs are mainly annual members of the Cistus, converges in small areas of the southwestern Cape and Leguminosae, Compositae and Gramineae’7JO.In Chile, high southwestern Australia, which have similar heterogeneity and turnover is concentrated in suffrutescent shrubs and per- ennial herbs belonging to many genera including Senecio, Adesmia, Oxafis and Cafceolarial4J5. The tall shrub and tree floras that have persisted since the Tertiary in all regions ex- Box 1. Plant life in mediterranean-climate regions cept Australia, and that regenerate mainly from vertebrate- dispersed propagules in the absence of fire, have wide gee- Five geographically remote regions (Pig. 1, Table 1) have mediterranean-type cli- mates with warm, dry summers and cool, wet winters. By agricultural standards, all graphical distributions and contribute little to turnover3J5Jg. these regions have infertile soils, especially in southwestern Australia and the southwestern Cape of South Africa (Table 3). These two areas also differ from the Regional diversity others in that they are ancient and relatively subdued landscapes on sheared con Regional diversity (at a scale of IO-106kmz) in mediter- tinental margins; the landscapes of the Mediterranean Basin, California and Chile are in subduction zones and are consequently much younger and topographically ranean-climate regions ranks among the highest in the complex-here, mountain building has occurred as recently as the late Tertiary and world3,15(Fig.2). The southwestern zone of the Cape has the Quaternary*. highest diversity at this scale: for a given area, this region Before the onset of global cooling and aridification in the Pliocene, all five has, on average, 1.7 times the diversity of southwestern regions were clothed in subtropical forest 15J6J7, These forests were subsequently Australia, about 2.2 times the diversity of the southeastern replaced by sclerophyllous vegetation and dry woodlands, especially during the Quaternary when seasonal mediterranean-type climates developed. At the same Cape, California and the Mediterranean Basin, and 3.3 times time, fire became a significant factor in all regions except Chile, although contem the diversity of Chile3Js. Fox18suggests that regional diver- porary natural fire regimes vary regionally (Table 3). Although the frequency of sity in the southeastern zone of mediterranean Australia is Quaternary climatic cycles was probably similar for all regions, glacial conditions considerably lower than in the southwest although detailed were more severe in the northern than southern hemisphere areasa6. The contemporary vegetation of mediterranean-climate regions comprises an data are lacking. Diversity in small areas (>30 km2) of south- admixture of floras derived from relic subtropical forest and recent drought- and fire- western Australia is not significantly different from similar adapted lineages, with the latter predominating in all regions, especially in Australia areas of the southwestern Capes. and the Cape4.15.17.33.35.37.The typical vegetation type is evergreen, sclerophyllous In California and in the Cape, regional diversity peaks in or heathland, namelychaparral in California; matorral in Chile: matorral, topographically diverse areas that have high rainfall, provid- maquis and garrigue in the Mediterranean Basin; kwongan and mallee in Australia; and fynbos and renosterveld in South Africas. However, most regions also sup ing support for the favourableness and environmental hetero port extensive areas of forest, woodland and xeric, droughtdeciduous and semi- geneity hypotheses, respectively31Jz. The high topographical succulent shrubland. and climatic heterogeneity of Chile and the Mediterranean The sclerophyllous shrublands of mediterranean-climate regions show varying Basin (Table 3) might similarly explain their relatively high degrees of ecological convergence8. The most striking is between kwongan and fynbos. They are distinguished from other shrublands by their relatively open shrub (at least at a global scale) regional diversityi5Jr. However, cover, high shrub species diversity, and the highest incidence in the world of oblig southwestern Australia, the second richest region, remains ate post-fire reseeders, canopy seed storage (serotiny), and ant seed dispersal an exception since topographic heterogeneity is low and cli- (myrmecochory)~OJ6. The remaining shrublands have denser shrub canopies; burn matic heterogeneity is only moderate (Table 1). Edaphic at much longer intervals; and have their diversity concentrated in short-lived herbs complexity and associated specialization has been invoked and subshrubsl5,17.*1. as the principle determinant of the high diversity of south-

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short-lived herbs or fire-sensitive shrubs with high numbers Table 1. Plant species diversity and conservation status of sexually produced generations - attributes that would of mediterranean-climate regions invariably lead to high rates of genetic recombinations and rapid speciation3J1929. Area Native Threatened Major Region (106km2) floraa taxab threatsa Speciation California 0.32 4300 718 urbanization, Speciation models in mediterranean-climate regions usu- (35) agriculture ally invoke climate change as the driving force for geo- 0.14 2400 ? deforestation, graphic speciation in topographically heterogeneous (23) grazing, environments4J3. Cowling et ~1.3suggest that sympatric spe- agriculture ciation could occur when disruptive selection operates on Mediterranean 2.30 25000 4251 deforestation, populations that have been isolated by fire or climate change, Basin (50) agriculture, in habitats (usually soil types) that differ from those of the grazing, larger populations of the parent species. There are numer- urbanization ous examples of edaphically differentiated sister taxa in the Cape 0.09 8550 1300 invasive alien plants, Capes, southwestern Australia4 and California33.Since many (68) agriculture, urbanization of these neoendemics are short-lived and have discrete gen- erations, speciation rates may have been very rapid3!4. SW AustraliaC 0.31 8000 1451 agriculture, What do these models tell us about the evolution of (75) deforestation, introduced pathogens regional diversity in the different mediterranean-climate regions? These patterns can be interpreted in terms of aData from Refs 3-5,17 and2l. Percentage endemic is shown in brackets. differential speciation and extinction rate.+. In Chile, for bData from Ref. 1. CData for SE Australia are unavailable. example, the absence of fire as a natural factor and the rela- tive mildness of Quaternary climates, owing to low conti- nentality, resulted in the persistence of many long-lived and slow-evolving Tertiary forest lineages’s. Although there has speciation histories28. But why does Chile, which has high been considerable diversification of herbaceous lineages in topographical and climatic heterogeneity, and California, response to aridification since the late Tertiary, limited spe- where these forms of heterogeneity combine with edaphic ciation within woody genera has occurredl5. Environmental complexity to produce an enormous diversity of habitatsz1J9, conditions in California and the Mediterranean Basin are have lower regional diversity than featureless landscapes of intermediate between those in Chile and those in South southwestern Australia and the ancient, worn-down ‘hills’of Africa/Australia (Table 3). During the Quaternary, a reason- the southwestern Cape? Why does the southwestern Cape ably large flora of persistent Tertiary forest species would have more than twice the species of similar-sized and equally have been supplemented by moderate diversification of heterogeneous landscapes of the southeast? We return to annuals and fire-adapted shrubs33.35.However, relatively these questions in the section on speciation. extreme glacial conditions36 would have resulted in high extinction rates, thereby depressing regional diversity. Rarity In the Cape and Australia, two factors would have com- Mediterranean-climate regions generally include very bined to elevate speciation rates and to depress extinction high numbers of rare taxa most of which are locally endemic rates of their mediterranean floras: (1) high fire frequencies, habitat (principally edaphic) specialists associated with a which are a consequence of low soil fertility and associated limited number of lineage+4J3. Levels of endemism and rar- high flammabilityl6, and (2) relatively mild Quaternary cli- ity are most pronounced in the southwestern Cape and mates - a result of strong maritime influences35. Although southwestern Australia, where many hundreds of species the incidence of frequent, high-intensity fires resulted in the occur naturally in limited numbers of populations (each large-scale extinction of many Tertiary forest lineageGJ7, ~100 individuals)z-4. In these regions, range-restricted, rare this loss was offset by the massive diversification within taxa are overrepresented among fire-killed shrubs with short a limited number of predominantly fire-sensitive shrub dispersal distance@J4. A possible (and testable) gener- lineageG8. This, coupled with the persistence of many spe- alization regarding local endemics from all mediterranean- cies (often in very small populations), has produced the re- climate regions is that they are invariably poorly dispersed, markable species-flocks of the fynbos and kwongan floras. Why then is regional di- versity in the southwestern Cape higher than that in the Table 2. Patterns of local plant diversity in mediterranean-climate region@ southeastern Cape and south- Shrublands Woodlands and forest western Australia? The exist- ence of greater topography nb lm2 1000 m2 nb lm2 1000 m2 in the Cape may have pro- moted greater geographical California 13 7f6 31flO 18 14f3 56f9 speciation than in topographi- Central Chile 3 8f2 lOOf 1 7 25 cally uniform Australia3J8. Mediterranean Basin 29 14flO 70f54 8 llf7 64f50 There is good evidence that Cape 54 16f6 70f21 11 lOf4 56f21 glacial climates in the south- SW Australia 33 13flO 68f20 10 7f3 33f13 eastern Cape were harsher than those in the southwest, Qata from Refs 3,38 and 39. and that this resulted in the bn is the number of plots sampled. widespread disappearance of fynbos (and consequently in

364 TREE vol. II. no. 9 September 1996 REVIEWS high extinction rates) during much of the Quaternarys. A similar scenario may apply to the southeastern zone of mediterranean Australia**. An important point is that the “T 0 differences and similarities in patterns in regional diversity among mediterranean-climate regions are not the product of chance (cf. Ref. 38), but the deterministic outcome of the effects of slightly different selective forces on speciation and extinction rates of phylogenetically disparate florasl5J8. The interesting implication of these comparisons is that environmental heterogeneity per se is an unsatisfactory predictor of regional diversity patternsGJ9. Given certain conditions (stable climates, predictably frequent fires and periodic drought, which promote generation turnover and diversification-prone lineages), natural selection will result in a very fine-scale discrimination of habitatse. This is pre- cisely what has happened in the southwestern Cape and southwestern Australia: rapid speciation, coupled with low 2J extinction rates, has produced extremely species-rich land- -0.5 0.5 1.5 2.5 3.5 4.5 5.5 6.5 scapes in otherwise relatively homogeneous areas. Here, Log area (km*) botanists have identified a multitude of edaphic habitat+4 that may well be the product of rapid speciation leading to Fig. 2. Species-areacurves and regressions from mediterranean-climate regions. high diversity: in Rosenzweig’sGwords, ‘Species diversity is Diamonds, SW Australia; filled squares, Cape (SW); unfilled squares, Cape (SE); the horse; habitat diversity is the cart’ (p. 176). crosses, Mediterranean Basin; unfilled circles, Chile; filled circles, California. Medi- terranean Basin data are from the lberian Peninsula. All slopes are homogeneous but intercepts (k-values) vary. Relative diversities of the different regions (see text) Threats are ratios of their respective h-values. Data from Refs 3, 1.5 and 42. The mediterranean-climate regions of the world com- prise a substantial portion of the world’s vascular plant flora (Table l), including many ancient and taxonomically distinctive taxa; thousands of recently evolved species; Australia), they are probably accelerating in the Cape, Chile 26 200 endemic species; many hundreds of endemic genera; and the African zone of the Mediterranean Basin’. several endemic families; and the Cape Floristic Region (the world’s smallest floral kingdom)‘-4. The conservation status Conclusions of these regions is, however, very poor, and biodiversity is Mediterranean ecosystems provide many opportunities under severe and rapidly escalating threat&j. for the comparative study of the determinants of plant di- Agriculture and animal husbandry have been practised versity at local and regional scales. In particular, they offer in the Mediterranean Basin for 10 000 years, and most eco- unique potential for evaluating the effects of mediterranean- systems are now ‘human-modified’l7. Extensive transfor- type climates and recurrent fire (both relatively recent se- mations of the other regions began only after colonization lective forces) on coexistence and diversification in phylo- by Europeans, about 500 years ago in Chile (earliest), and genetically unrelated floras (true replicates). Moreover, the only 170 years ago in southwestern Australia (latest)s. All of existence of richly diversified genera in each of the regions the regions have very high concentrations of rare plant taxa, [e.g. Carex (126 spp.) and Erigeron (82 spp.) in California; whose survival is threatened mainly by clearing for agricul- Senecio (109 spp.), Adesmia (82 spp.) in central Chile; ture and urbanization, but also by alien plants and patho- Asfralagus (450 spp.), Silene (365 spp.) in the Mediterranean gens (Table 1). With the exception of the montane areas of Basin; Erica (526 spp.), Aspalathus (245 spp.) in the Cape; the Cape, the current reserve networks in mediterranean- Acacia (>400 spp.), Eucalyptus (>300 spp.) in southwestern climate regions are inadequate@. Currently, some 142 vas- Australia]3,4,15,17,33provide excellent material for the com- cular plant taxa from these regions are presumed extinct, 55 parative study of ecological variation within monophyletic of these from southwestern Australia’. Although extinction lineages. The large numbers of naturally rare species that rates may have peaked in some regions (e.g. California, have persisted for tens to hundreds of thousands of years

Table 3. Relative environmental characteristics and plant diversity components in mediterranean-climate regions _ Topographic Climatic Modal natural fire Differentiation Regional Soil fertilitya heterogeneityb heterogeneityb frequency (yr)” Local diversityd diversitye diversity’

California moderate high very high 40-60 low-moderate moderate moderate Central Chile high very high high fire-free low-?high low-moderate? low Mediterranean Basin high-moderate high very high 25-50 low-vety high moderate? moderate Cape (SW) very low-moderate moderate-high high 10-20 moderate-high high high Cape (SE) low-moderate moderate high 10-20 moderate-high moderate moderate SW Australia very low-low low moderate 10-15 low-high high high

Qata from Ref. 8; bdata from Refs 8 and 15; cdata from Refs 8,18 and 40; dsee Table 2; edata from Refs 2-4; fsee Fig. 2.

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in small, fluctuating and poorly dispersed populations rep- 18 Fox, M.D. (1994) AustraIian medlterranean vegetation: intra- and resent a challenge to population geneticists and conser- intercontinental comparisons, in Ecology and Biogeography of vation biologists4. However, without significant progress in Mediterranean Ecosystems in Chile, California and Australia (Arroyo, M.T.K.,Fox, M.D. and Zedler, P.H., eds), pp. 137-159, halting the transformation and degradation of natural habi- Springer-Verlag tats in mediterranean-climate regions, many of these popu- 19 Cody, M.L.(1986) Siructmal niches in plant communities,in Communily lations will soon disappear. Ecology (Diamond, J. and Case, T.J., eds), pp. 381-405, Harper&Row 20 Aronson, J. and Shmida, A. (1992) Plant species diversity along a Acknowledgements Mediterranean-desert gradient and its correlation with Many thanks to Mike Rosenzweig for stimulating discussions interannual rainfall fluctuations, J. Arid Environ. 23,235-247 and to Fernando Ojeda for help with the literature. Dave 21 Keeley, J.E. and Swift , CC. (1995) Biodiversity and ecosystem Richardson provided critical comments on an earlier draft. functioning in mediterranean-climate California, in Meditemmean- Type Ecosystems. The Function of Biodiversity (Davis, G.W. and References Richardson, D.M.,eds), pp. 121-183, Springer-Verlag 22 Naveh, Z. and and Whittaker, R.H. (1979) Structural and floristic 1 Greuter, W. (1994) Extinction in Mediterranean areas, Philos. diversity of shrublands and woodlands in northern Israel and Trans. R. Sot. London Ser. B 344,41-46 other mediterranean areas, Vegetatio 41, 171-190 2 Cody, M.L. (1986) Diversity, rarity and conservation in 23 Lamont, B.B., Enright, N.J. and Bergl, SM. (1989) Coexistence and mediterranean-climate regions, in Conservation Biology. 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