Area, geography and diversity patterns
Spanning three continents, the MB is the largest mediterranean-climate biome in terms of area (2,300,000 km2, Fig. 1), being 25 times larger than the CFR (90,000 km2), the smallest of the five regions. At large spatial scales (10–106 km2), the slope of species–area relationships (SARs) for mediterranean regions is homogenous (c. 0.2 for a power model; Kier et al., 2005), and therefore the intercepts can be directly compared. At this scale, the CFR clearly displays a higher density of species, as shown by the fact that the intercept of the SAR for this region is 2.2 times higher than that for the MB (Cowling et al., 1996). The high diversity of the CFR was clearly evidenced when we fitted a power-model SAR to the five mediterranean-climate regions (Fig. 2). Although the diversity of both the CFR and the MB falls above the SAR, the CFR is over twice as diverse as expected for its area (Fig. 2). As an illustration of this, the mediterranean part of continental Greece (9 × 104 km2; Médail & Quézel, 1997) is of roughly the same area as the CFR, but harbours fewer than half as many plant species (c. 4000 species vs. c. 9000; Médail & Quézel, 1997).
Figure 2. Species–area relationship of plant species for the five mediterranean-climate regions of the planet. The best-fit line of the power function is plotted, ln(number of species) = 0.50 ln(area) + 2.58, R2 = 0.497, F = 2.96, P = 0.18, n = 5. Confidence intervals of regression are shown: 90%, dashed lines; 75%, dotted lines. Data from Cowling et al. (1996). CFR, Cape Floristic Region; MB, Mediterranean Basin.
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The CFR is also more diverse than the MB at the point scale (1 m2; Keeley & Fotheringham, 2003). However, at the 1000-m2 community scale, the shrublands and woodlands in the eastern MB were in fact more diverse than both CFR fynbos and renosterveld communities (Keeley & Fotheringham, 2003). The fact that the CFR presents a much higher diversity at regional and point scales but often a lower diversity at intermediate scales when compared with the MB suggests that beta diversity is a major contributor to the overall plant species richness in the CFR. Indeed, several studies seem to support the fact that species turnover between habitats is exceptionally high in the CFR (Simmons & Cowling, 1996; Linder, 2003).
Overall, the MB is more geographically heterogeneous than the CFR, as it is typified by sea barriers, straits, islands and archipelagos (Rosenbaum et al., 2002), all of which are lacking in the CFR. The Mediterranean Sea, the largest inland sea in the world, is the most significant geographical barrier for plant dispersal (Escudero et al., 2008b), but the region is also dotted with important mountain chains, reaching elevations over 2500 m (e.g. Atlas, Betic, Olympus, Taurus). A pattern of high plant endemism associated with geographical barriers is strongly manifested within the circum-Mediterranean region (Thompson, 2005). Several of the most species-rich MB clades display a high level of taxonomic turnover across different archipelagos, islands, peninsulas and mountains, often with little ecological differentiation; for example Anthemis (Lo Presti & Oberprieler, 2009), Antirrhinum (Vargas et al., 2009), Centaurea (Font et al., 2009), Cistus (Guzmán et al., 2009), Dianthus (Balao et al., 2010) and Nigella (Bittkau & Comes, 2009). These patterns suggest that diversity has been strongly driven by allopatric speciation in this region.
With no sea barriers, the CFR region is geographically more homogeneous and compact. The major barrier to biological movements in this territory is the Cape Folded Belt, a series of moderately elevated mountains that delimits coastal, intermontane and inland plains (Cowling et al., 2009). Certain clades display high numbers of single-mountain endemics, such as Iridaceae (Goldblatt & Manning, 1998) and Proteaceae (Rebelo, 2001), implying a role of geographical isolation in speciation at least in these groups. However, the best predictors of reproductive isolation in the CF seem to be ecological rather than geographical (see ‘Ecological setting’ below).
In short, the abundant sea and orographical barriers in the large MB have promoted allopatric speciation, whereas small areas have been the arena for speciation in the CFR.
Geomorphic and climatic history
Since the Oligocene, the history of the MB has been more unstable and complex than that of the CFR in terms of both geomorphic and climatic events (Thompson, 2005; Cowling et al., 2009). Situated at the convergence of the African, Arabian, Eurasian and Iberian tectonic plates, the circum-Mediterranean region has undergone constant and dramatic geomorphic mutation. The late Oligocene and the Miocene were periods of important horizontal and vertical movements of land masses, with the break-up of continents, orogenesis, and volcanic activity in both the east and west of the MB (Robertson, 1998; Rosenbaum et al., 2002). In the late Miocene, the closing of marine passages between the Atlantic Ocean and the Mediterranean Sea led to increasing desiccation, culminating in the Messinian salinity crisis (5.3–5.9 million years ago, Ma; Duggen et al., 2003; Krijgsman et al., 2010). Subsequently, the Pliocene and Pleistocene were periods of island formation and intense orogenesis (particularly in the central MB; Rosenbaum et al., 2002). This complex history has most certainly led to high rates of isolation and speciation, but also to extinction, and possibly to the repeated extirpation of floras in areas of similar size to the CFR.
In contrast, the late Cenozoic in the CFR has been characterized by a comparatively stable geomorphic evolution. The region had a period of tectonic stability in the Oligocene, which was followed by cycles of orogenic uplift in the Miocene and Pliocene associated with the Post-African I and II erosion cycles (Partridge & Maud, 2000; Cowling et al., 2009). In the Quaternary there have been no major geomorphic phenomena in the CFR (Cowling et al., 2009), which suggests that rates of extinction may have been low.
The climatic histories of the two regions also differ. Most importantly, the onset of a true mediterranean climate took place earlier in the CFR. In southern Africa, progressive aridification of the climate began in the mid-Miocene (10–15 Ma), associated with the establishment of the Benguela upwelling system (Zachos et al., 2001; Cowling et al., 2009; Dupont et al., 2011). Approximately 10 Ma, the seasonal summer-dry climatic regime found in the present day in the CFR was established (Krammer et al., 2006; Roters & Henrich, 2010). The progressive aridification and the opening of new niches in the CFR in the last 10 million years (Myr) have been hypothesized to have triggered rapid speciation in several CFR clades (Verboom et al., 2009). Plant groups that have been shown to have diversified since the onset of the mediterranean climate in the CFR include Ehrharta (9.8–8.7 Ma; Verboom et al., 2003), Heliophileae (< 4 Ma; Mummenhoff et al., 2005) and Phylica (7–8 Ma; Richardson et al., 2001). However, not all species-rich CFR clades have experienced a speciation burst since the onset of aridification (see Appendix S1 in Supporting Information). Phylogenetic studies of clades such as Crotalarieae p.p. (46.3 Ma; Edwards & Hawkins, 2007), Pelargonium (30.5 Ma; Bakker et al., 2005) and Restionaceae (> 41–38 Ma; Linder et al., 2005) have shown that these clades had an ancient origin in this biome that clearly pre-dates the onset of the mediterranean-type climate.
In the MB, the profound climatic alterations that led to the modern climate took place much later than those in the CFR. Strong seasonality and aridification began by the mid–late Pliocene (c. 3.6 Ma), and only by the end of this period (c. 2.8 Ma) did the contemporary summer-drought regime stabilize (Suc, 1984; Suc & Popescu, 2005). These abrupt climatic changes caused the extinction of moisture-adapted lineages (Jiménez-Moreno et al., 2007), and have been shown to have coincided with diversification bursts of lineages that were pre-adapted to arid environments (Bell et al., 2012; Fiz-Palacios & Valcárcel, 2013), such as Antirrhinum (< 4.1 Ma; Vargas et al., 2009), the Cistus–Halimium complex (1.0 Ma; Guzmán et al., 2009), Dianthus (1.9–7 Ma; Valente et al., 2010a), Erodium (< 3 Ma; Fiz-Palacios et al., 2010) and Tragopogon (1.7–5.4 Ma; Bell et al., 2012). On the other hand, clades such as Cyclamen (29.20–30.10 Ma; Yesson et al., 2009), Linaria sect. Versicolores (6.45–16.53 Ma; Fernández-Mazuecos & Vargas, 2011), Narcissus (18.1–29.3 Ma; Santos-Gally et al., 2012) and Ruta (26.65–63.53 Ma; Salvo et al., 2010) are much older and seem to have survived the filtering processes associated with climatic change in the region.
The climatic history of the CFR and the MB has also differed significantly in the Quaternary. The severity of the temperature and moisture oscillations associated with Pleistocene glaciations was higher in the Northern Hemisphere than in the Southern Hemisphere (Markgraf et al., 1995; Jansson, 2003). Indeed, strong evidence suggests that long-term Quaternary climatic stability and summer-drought reliability were much higher in the CFR than in the MB (Cowling et al., 2004), which could have led to important differences in extinction and speciation rates. In the MB, clades such as Cedrus, Platanus and Syringa have been shown to have been severely affected by extinctions caused by Quaternary climate fluctuations (Postigo-Mijarra et al., 2010). In contrast, studies in the large CFR clades Gladiolus (Valente et al., 2011) and Pentaschistis (Galley et al., 2007a) have found evidence for low rates of extinction in the CFR in the Quaternary, in agreement with the hypothesis of high climatic stability for this region (Cowling et al., 2004; Galley et al., 2007a).
We conclude that the time-lag in the establishment of summer-drought climatic regimes in the CFR (10 Ma) compared with the MB (3.6 Ma), in combination with the more unstable climatic and geomorphic history in the MB, may have enabled more time for lineage accumulation with lower extinction rates in the CFR.
The MB is situated between three continents (Africa, Asia and Europe) and has thus been considered a ‘tension zone’ for plant lineages from different biogeographical origins (Comes, 2004). Several floristic regions are now known to have frequently acted as sources of species to the Mediterranean region (and vice versa), and its contemporary flora is rich in Irano-Turanian, Saharo-Arabian, Holarctic and subtropical African elements (Zohary, 1973; Quézel, 1978, 1985), with some clades often invading the region multiple times mostly from the east (Mansion et al., 2008) or from the south (Buerki et al., 2012). In contrast, the exceptional level of plant endemism in the CFR and its location at the southernmost tip of Africa have led to the suggestion that this continental region is ‘island-like’, with lower levels of connectivity than typical mainland areas (Kier et al., 2009). In several groups, migration out of the CFR into neighbouring summer-rainfall regions (namely the Drakensberg) has occurred more frequently than has migration into the CFR (Galley & Linder, 2006; Galley et al., 2007b; Valente et al., 2010b, 2011). Nevertheless, a recent study in Hyacinthaceae found that there have been a large number of independent colonizations of the CFR from sub-Saharan Africa (Buerki et al., 2012).
Plant movements have also taken place repeatedly between the two biomes and other mediterranean-climate regions (Burtt, 1971; Quézel, 1978). The MB has particularly strong affinities with California, with over 25 groups exhibiting a disjunct pattern between the two regions (Kadereit & Baldwin, 2012), whereas the CFR shares several groups with south-western Australia (e.g. Aizoaceae, Geraniaceae, Haemodoraceae and Proteaceae; Hopper & Gioia, 2004; Galley & Linder, 2006). Connections have also taken place several times between the CFR and the MB, leading to a considerable number of plant clades presenting an intriguing CFR–MB disjunct pattern (Tables 1 & 2). Possible land routes of connection between the two territories have been proposed, through the Sahara via the mountainous corridors of the central Mahgreb or near the Red Sea coast, and through tropical and summer-rainfall southern Africa via Afromontane arid tracks (Wickens, 1976; Quézel, 1978). In certain CFR–MB disjunct clades, however, long-distance dispersal mediated by birds has not been ruled out (e.g. Senecio; Coleman et al., 2003).
In summary, the MB presents a high level of connectivity with other regions, whereas the CFR appears to be comparatively more ‘island-like’, which has translated into its exceptional levels of endemism. Lineage exchange has occurred often between the two regions.
There is a significant turnover of species among numerous microhabitats in the MB (Naveh & Whittaker, 1979), suggesting that rapid local adaptation in association with allopatry may have been an important driver of speciation events. In the CFR, total microhabitat diversity may be lower overall, but some studies suggest that microhabitat heterogeneity within small areas may be unusually high (Simmons & Cowling, 1996). The two most common vegetation communities in the CFR – fynbos and renosterveld – are both typified by steep ecological gradients, particularly in terms of soil and hydrology (Linder, 2003; Silvertown et al., 2012). The fact that these gradients are associated with species turnover supports a role for ecological speciation processes in the CFR, at least for some of the largest clades, including Iridaceae, Orchidaceae, Proteaceae and Restionaceae (van der Niet & Johnson, 2009; Rymer et al., 2010).
One of the major hypotheses that has been put forward to explain the high species richness in the CFR highlights the role of edaphic specialization in generating diversity (Linder, 2003). Using phylogenetic sister-species comparisons, Schnitzler et al. (2011) identified soil type as the best predictor of speciation in Babiana, Moraea and Protea. However, it remains unclear why edaphic shifts should be more common here than in other regions (Barraclough, 2006). For instance, some areas in the MB, such as the southern Iberian Peninsula, display a similarly high diversity of soils, but harbour far fewer species than areas of similar size in the CFR (Ojeda et al., 2001).
The differences in angiosperm diversity between the CFR and the MB have also been hypothesized to be associated with regional differences in plant–pollinator interactions (Valente et al., 2012). One of the main hypotheses to explain the high plant diversity in the CFR proposes that a high percentage of speciation events within several lineages may have been driven by pollinator shifts (Johnson, 2010; Waterman et al., 2011; Valente et al., 2012). This hypothesis is supported by the fact that several of the species-rich CFR clades exhibit a high diversity of floral characters and pollination systems (Johnson, 1996). Examples of such clades include Babiana (Schnitzler et al., 2011), Disa (Johnson et al., 1998), Gladiolus (Valente et al., 2012) and Moraea (Goldblatt et al., 2002). In addition, it has been shown that a high percentage of species in southern Africa are typically pollinated by a single animal species (Johnson & Steiner, 2003). In contrast, the majority of plant species in the MB exhibit a generalist pollination strategy (Johnson & Steiner, 2000; Thompson, 2005), and large genera in the region possess a relatively low diversity of pollination systems (e.g. Astragalus, Antirrhinum). The lower diversity of specialized pollination systems in the MB could potentially be linked with the lower diversity of the specific pollinator clades that are associated with high floral specialization in the CFR (rather than with a lower total pollinator species density per se; Valente et al., 2012). For instance, the diversity of the most important pollinator group in both regions (long-tongue bees, Apidae) is higher in the CFR (Kuhlmann, 2009; Linder et al., 2010). In addition, several of the specific animal pollinator clades that are associated with high diversification in the CFR (Goldblatt & Manning, 2006) are completely absent in the MB (sunbirds, long-proboscid nemestrid and tabanid flies, hopliine beetles, among others).
Considered together, this evidence suggests that ecological speciation appears to have been more frequent in the CFR than in the MB, and that interactions with specific pollinator classes that are more prone to causing reproductive isolation in plants could have been more common in the former.