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Changes to the global climate system are anticipated from the accumulation of CO2 and other greenhouse gases in the atmosphere since preindustrial times. This accumulation has had a discernible influence on global temperature and is predicted to cause further warming in this century (IPCC, 2001). Direct and dramatic ecological responses to global warming are expected (Peters & Lovejoy, 1992; Thomas et al., 2004), as are feedback effects whereby ecological responses generate additional climatic impacts by modifying transfer rates of energy, water, and trace greenhouse gases at the planetary surface (Rosenberg et al., 1983; OIES, 1992). These prospects are supported by long-term monitoring studies, which indicate that recent climatic and atmospheric trends are inconsistent with past climatic variation and are already affecting the phenology, physiology and distribution of plant species (Hughes, 2000; Parmesan & Yohe, 2003). Concerns have been amplified because rates of vegetation change are expected to occur much faster than past successional processes and species dispersal rates (Pastor & Post, 1988; Overpeck et al., 1991).
Various climate futures focusing on regional mean temperature and rainfall changes in different seasons have been predicted for the African continent (Hulme et al., 2001). They draw upon different draft emission scenarios prepared for the Intergovernmental Panel on Climate Change (IPCC, 2001) and have been incorporated into bioclimatic models to predict ecosystem responses to climate change (Rutherford et al., 1999). The application of these models in vulnerability and adaptation assessments in a South African Country Study on Climate Change predicted future warming and aridity trends sufficient to cause large reductions in species richness in Mediterranean-climate Fynbos and Succulent Karoo biomes (Midgley et al., 2002, 2003). These biodiversity changes accompanied by the displacement of the Succulent Karoo biome southward along the west-coast and interior coastal plain (Hannah et al., 2002), a feature of glacial-interglacial climatic oscillations of the Pleistocene (Midgley et al., 2001). The predictions concur with the purported particular sensitivity of Mediterranean-climate ecosystems globally to changes in biodiversity induced by the five major drivers of biodiversity at the global scale, with climate change rated only second to land use as the driver with the largest effect on biodiversity when all ecosystems are averaged (Sala et al., 2000). They are also supported by local observations, which indicate that the population demographies of some large succulents, such as Aloe dichotoma, have already begun responding to anthropogenic induced climate change in a manner projected by bioclimatic models (Foden, 2002). Such changes are of concern for biodiversity conservation in the region, since both the Fynbos and Succulent Karoo biomes are characterized by exceptionally high species richness and endemism (Cowling et al., 1989, 1998; Hilton-Taylor, 1996), the Succulent Karoo biome especially possessing the highest species diversity recorded for an arid vegetation type worldwide (Hilton-Taylor, 1996) and listed among 25 global biodiversity hot spots (Myers et al., 2000). Despite these features, these biomes are not yet represented in a network of 32 ecosystem warming research sites currently representing Forest, Grassland, high and low latitude/altitude Tundra biomes (Rustad et al., 2001).
The ability of bioclimatic models to elucidate biodiversity responses to climate change has been questioned (Woodward & Beerling, 1997), and is certainly limited by a paucity of empirical information from field and laboratory trials. Experimental tests are urgently required to validate and refine bioclimatic model extrapolations, since this remains one of the few methods able to generate predictions of climate impacts on large numbers of individual species (Thomas et al., 2004). In this paper, we report on initial responses of some endemic succulent species in a southern African biodiversity hotspot to experimental warming approximating a future climate scenario (Hulme et al., 2001). For this and logistic and engineering reasons, we focused on specialized dwarf and shrubby leaf succulents occurring on sandy-loam substrates covered by quartz gravel in the Knersvlakte centre of endemism in the Succulent Karoo biome, an area of great ecological significance and conservation value (Schmiedel & Jürgens, 1999; Schmiedel, 2001, 2002).
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Ambient air temperatures at our experimental sites during the 4-month treatment period did essentially represent average conditions for study area. This supported by the similar average daily maximum air temperatures recorded in our control plots and at the closest meteorological station at Clanwilliam. However, there were 3 d with abnormally high ambient temperatures at our experimental sites in which monthly diurnal air temperature maxima in the control plots did slightly exceed those recorded over a 28-yr span at the Clanwilliam meteorological station.
Daily maximum air temperatures in the centres of our open-top chambers, which averaged 5.5°C above ambient over the 4-month treatment period (Fig. 1c), approximated temperature increases of between 4.5 and 5.0°C (means of 7-GCM experiments) predicted (SRES A2-high climate sensitivity scenario) for the geographic coordinates 30° S to 31° S, 19° E to 20° E in the year 2080 (Hulme et al., 2001). The observed close correspondence between ratios of highest recorded monthly temperature against corresponding average daily temperature maxima in our open-top chambers, control plots and at the Clanwilliam meteorological station indicated that the temperature extremes accompanying the average daily maxima in our open-top chambers also provided a rational analogue of the predicted climate change.
The elevated temperatures in our open top chambers were associated with a 3.5- to 4.9-fold increase in plant and canopy mortality among the specialized dwarf succulents A. pearsonii and C. spissum, and a 2.1-fold increase in canopy mortality in the shrubby succulent D. diversifolium (Table 1). These substantial reductions in live standing succulent biomass seemingly contrasted with results of a meta-analysis of plant productivity responses to experimental warming in 20 of 32 global sites representing Forest, Grassland, high and low latitude/altitude Tundra biomes (Rustad et al., 2001). The meta-analysis found a 19% productivity increase in response to an average 2.4°C of experimental warming among the 20 sites distributed in cooler regions at latitudes above 35° N (Rustad et al., 2001). However, relative productivity responses to experimental warming declined with increasing site mean annual temperature (Rustad et al., 2001) implying that productivity could be expected to decrease with experimental warming at lower latitude subtropical and tropical sites not included in the meta-analysis. Noteworthy, was the abrupt rather than gradual temperature increase in our open top chambers on commencement of the study, which may have precluded natural plant acclimation to the increased heat stress, thereby contributing to the extraordinarily high mortalities observed. Indeed, an analysis of the age and size distribution of surviving and deceased A. pearsonii in the control plots and open-top chambers revealed that the live plants were significantly older (Fig. 2d) and larger than the deceased plants (Table 1); possibly indicative of past selection for heat resistant ecotypes.
An examination of the distribution patterns of surviving dwarf succulents in our open-top chambers revealed that live C. spissum and A. pearsonii individuals particularly were restricted to cooler microhabitats in more ventilated areas at the edges of the chambers (Fig. 2b) and shaded refuges beneath the skeletons of larger succulents such as Salsola spp. (Fig. 2c). These distribution patterns supported our perception that lethal temperature thresholds were exceeded in the open-top chambers, though ostensibly less severely in the cooler microhabitats. Indeed, diurnal temperature extremes in our open-top chambers were closely proximate to the upper temperature limit of 55°C considered tolerable by most vascular plants (Larcher, 1980; Kappen, 1981). However, there are reports of much higher lethal temperature thresholds in a diverse array of dwarf succulents. These, based on the ability of chlorenchyma cells to uptake a vital stain (Onwueme, 1979), ranging from 66.4°C to 66.9°C in rosette leafed Haworthia species (H. retusa and H. turgida), 68.3°C to 68.7°C in spherical leafed Lithops species (L. leslie and L. turbiniformis), and 69°C to 70°C in seedlings of Ferocactus (F. covillei and F. wislizenii) and in detached stem segments of Opuntia (O. ficus-indica) species (Smith et al., 1984; Nobel et al., 1986; Nobel, 1989). Nevertheless, lethal temperature thresholds in the majority of southern African dwarf succulent taxa may be lower, since they occur at high densities virtually exclusively on quartz-fields with milder thermal regimes (Schmiedel & Jürgens, 2002, 2004). Indeed, maximum daily soil temperatures during summer have been measured up to 10°C lower on highly reflective quartz substrates than on adjacent brown shales, and up to 3°C lower leaf temperatures have been measured in A. pearsonii growing inside quartz fields compared with the same species growing on neighbouring soils without quartz cover (Schmiedel & Jürgens, 2004). Similarly, another earlier study reported that leaf surface temperatures in a dwarf Argyroderma species on a quartz-covered substrate remained close to an ambient air temperature of 35°C whereas those of a shrubby Ruschia species on adjacent brown shale exceeded 45°C (von Willert et al., 1992).
Common physiological responses to experimental warming observed among the surviving dwarf and shrubby succulents in the open-top chambers included diminished foliar water contents and starch concentrations, the shrubby succulents also exhibiting altered foliar chlorophyll levels. Relocation of carbon reserves to secondary phenylpropanoid compounds was apparent in D. diversifolium where reduced foliar starch concentrations corresponded with increased anthocayanin levels. Nevertheless, the physiological changes observed in the surviving succulents did imply moisture limitations in the open-top chambers. Moisture deficits modify leaf conductance, transpiration and carbon assimilation rates (Ni & Pallardy, 1992) resulting in a degradation of stored non-structural carbohydrate reserves (Dunn et al., 1987), with small stature species with limited root extension and carbon reserves particularly sensitive to low soil water potentials (Donovan & Ehleringer, 1991; Flanagan et al., 1992). Indeed, a higher fraction of small leaves with a lower mass leaves were observed in the canopy of live D. diversifolium (Table 1), suggesting an acclimation to reduce transpiration loss under the warmer conditions in the open-top chambers. In this regard, it is known that shallow rooted dwarf succulents of the Mesembryanthemaceae require frequent though small amounts of water for survival, and the role of supplementary precipitation by fog and dew, estimated at as much as 38% of annual hydrological input (Dawson, 1998), is an important factor in ameliorating summer water deficits in semiarid and arid Mediterranean-climate ecosystems and preventing thermoregulation problems due to reduced transpiration (von Willert et al., 1992; Turner & Picker, 1993). This supplementary precipitation accrued on leaf surfaces drips, or is funnelled via stem-flow, onto the soil (Hutley et al., 1997) where it can be absorbed by plant root systems or directly by leaves from their wetted surfaces (Yates & Hutley, 1995; Martin & von Willert, 2000) or from the vapour-saturated atmosphere (Breazeale et al., 1950). Indeed, the interception of such supplementary precipitation by the open-top chambers and its channelling to the chamber edges could also partly explain the observed prevalence of surviving dwarf succulents in these locale.
In conclusion, it does seem likely that current thermal regimes are closely proximate to tolerable extremes for many of the 1563 almost all endemic succulent species included in the subfamily Ruschioideae which diversified rapidly in the region during the cool Pleistocene (Klak et al., 2004). Anthropogenic warming could therefore significantly exceed their thermal thresholds resulting in localized extinctions of particularly those specialized species range-restricted to specific habitats. However, further investigation is required to elucidate the importance of associated moisture deficits in these passive warming experiments, a potential consequence of supplementary precipitation interception by open-top chambers and higher evaporation therein, to allow reliable assessment of potential extinction losses under a range of climate change scenarios, and to match these with the predictions on the increasingly useful bioclimatic modelling approach.