Comparative ecophysiology of the leaf-succulents Augea capensis (C3) and Malephora purpureo-crocea (CAM) in the Knersvlakte, Succulent Karoo, South Africa
Introduction
The vegetation of the arid and semi-arid winter rainfall region of the southern Namib Desert and the Succulent Karroo in southern Africa is particularly characterised by a high biodiversity of succulents (Mooney et al., 1977; Milton et al., 1997; van Jaarsveld and van Wyk, 2005). These succulent plants own various functional traits allowing them to survive long periods of drought (Veste and Jürgens, 2004); in most of these succulents Crassulacean acid metabolisms (CAM) had evolved (von Willert et al., 1992; Veste and Thiede, 2004). An early case study in the winter rainfall region of southern Africa showed that approx. 35% of the species and up to 70% of the total vegetation performed the CAM pathway (Werger and Ellis, 1981).
Crassulacean acid metabolism (CAM) plants, which are mostly succulents, are characterised by their ability to assimilate carbon dioxide into organic acids and store these in the vacuoles at night, but subsequently release and decarboxylate them during daytime. The release of the intermediately “stored” CO2 rapidly and largely increases the plant internal concentration of this gas, which, in turn, induces stomatal closure and, thus, reduces transpirational water losses. As a consequence, CAM performing plants often show higher water use efficiency than those relying on C3 photosynthesis only. For this reason, CAM is assumed to be an important strategy of drought adaptation of plants growing in arid habitats (Kluge and Ting, 1978; Osmond, 1978; Herrera, 2009; Winter et al., 2015).
Gas exchange patterns of CAM plants can, however, be expressed very diversely in different species, ranging from that of a “typical” C3-type to nearly exclusive night-time CO2 uptake. This range of extremes may be found within one species during progressing plant development and/or as a response to changes in environmental conditions or in different species within the same environment (De Santo and Bartoli, 1996; Herppich et al., 1996, 1998; Veste et al., 2001; Martin, 2010; Martin et al., 2019; Winter, 2019).
On the other hand, von Willert et al. (1992) concluded from the results of numerous long-term studies in the Namib Desert and the Karoo that the capability to reversibly store large amounts of water, i.e., succulence itself, is the most important life strategy of perennials to survive under arid conditions. While it is generally accepted that rain during the mild winter in the Karoo benefits the entire vegetation (von Willert et al., 1992; Esler and Rundel, 1999), few investigations on the potentially distinct responses of C3- and CAM-succulents are available (von Willert et al., 1985; Eller and Ferrari, 1997). The few reported data, however, propose some advantages of CAM as it may facilitate rapid water uptake and use (von Willert et al., 1992; Eller and Ferrari, 1997; Matmati et al., 2012). Comparative evaluations of the potential effects of this feature on the distribution of C3- and CAM-succulents in this specific natural habitat are lacking.
While several comparative field studies on the ecophysiology of co-occurring tropical C3- and CAM-epiphytes have been reported (Griffith et al., 1986; Lüttge et al., 1986; Zotz and Winter, 1994), similar comprehensive studies on C3- and CAM-succulents naturally co-occurring in the same desert habitat are rare (Rundel et al., 1980; von Willert et al., 1992; Eller and Ferrari, 1997) and their results equivocal. Thus, the question still remains to answer whether CAM provides a better adaptation to long-term drought than the C3 mode of photosynthesis in morphologically similar succulents in the same arid environment.
Augea capensis Thunb. (Zygophyllaceae) and Malephora purpureo-crocea (Haw.) Schwantes (Mesembryanthemaceae) are both low shrubby plants of similar habit with highly succulent leaves of similar size and shape (Fig. 1). Both species are native to southern Africa. Only in few regions of the Knersvlakte, a part of the Little Namaqualand, particularly in the northern Knersvlakte, the Central Knersvlakte Vygieveld and the Quartz Vygieveld these species grow co-occurring (Mucina et al., 2006). The dwarf shrub A. capensis utilises typical C3 photosynthesis (Rossa and von Willert, 1999; van Heerden et al., 2007; Swanepoel et al., 2007); M. purpureo-crocea is known as a weak-CAM performing species (von Willert et al., 1977). Thus, to answer the above question in a multi-year study, relevant ecophysiological parameters of both species were repeatedly monitored and, in addition, their ability to metabolically utilize artificially improved soil water availability analysed in their natural habitat on an area in the Knersvlakte, which is predominantly covered with a mixed population of the above species.
Section snippets
Study site
Both during summer (February 1987, 1991) and winter months (August 1990), investigations were carried out on the farm Kalkgat (31° 7ʹ 0.78″ S, 18° 55ʹ 15.20″ E) located in the Knersvlakte at the foot of the Bokkeveld Mountain, Western Cape Province, South Africa (Fig. 1A). Mucina et al. (2006) assigned the Kalkgat region to the Knersvlakte Shale Vygieveld vegetation unit with typical winter-rainfall between May and August (mean annual precipitation: 126 mm) and a mean annual temperature of
Diurnal variations of gas exchange parameters and leaf water potential
In both summer and winter months, CO2 gain of A. capensis leaves was restricted to the light period only, while at night, respiratory CO2 was released (Fig. 2E and F) with mean exchange rates ranging between −0.07 and −0.46 µmol m−2 s−1. Carbon dioxide uptake (Fig. 2E and F) but also transpiration was maximal during the morning (Fig. 2G and H), particularly in winter, and was greatly restricted during the driest (Fig. 2A and B) and hottest hours of the day (Fig. 2C and D), when also xylem water
Evaluation of the growth success of M. purpureo-crocea and A. capensis
From the presented results, it seems simple to answer the basic question of this study. The ability to perform CAM obviously does not per se provide any pronounced advantages to better “survive” (von Willert et al., 1992) in the same drought-prone arid environment than the C3 mode of photosynthesis. In morphologically similar succulents, and only then it is meaningful to compare (Eller and Ferrari, 1997), both photosynthetic pathways resulted in equivalent plant cover under the edaphic and
Conclusion
The presented results highlighted that the adaptation strategy succulence is of higher importance than the respective photosynthetic pathway. Under identical conditions in the same natural habitat, carbon gain of the C3 species was always higher than that of the CAM plant and its overall WUE of the latter was similar. At (artificial) high soil water availability, stomata of the CAM-species Malephora rapidly opened during the day and light period-CO2 uptake increased drastically, while that at
Author contributions
Conceptualization, M.V. & W.B.H; Data curation, M.V. & W.B.H; Formal analysis, M.V. & W.B.H; Investigation, M.V.; Methodology, M.V. & W.B.H; Resources, M.V. & W.B.H; Validation, M.V. & W.B.H; Visualization, W.B.H & M.V.; Roles/Writing - original draft, W.B.H & M.V.; Writing - review & editing, W.B.H.
Declaration of Competing Interest
None.
Acknowledgements
We thank Willem van Wyk, Niewouldtville, for the permission and his support to work at Kalkgat. The investigations were supported by the Deutsche Forschungsgemeinschaft (DFG) and Deutsche Akademische Austausch Dienst (DAAD). We thank the Volkswagen of South Africa for providing 4WD minibuses.
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Dedicated to Prof. Dr. Dieter Joachim von Willert on the occasion of his 80th birthday.