4.1 Hydathode-mediated foliar water uptake is probably a widespread phenomenon among Crassula species
After decades of speculation, our results reaffirm hydathode-mediated FWU as a common phenomenon in both subgenera of Crassula (i.e.Disporocarpa and Crassula ), regardless of growth form, habitat preference and phylogenetic relationship. Our results unequivocally prove that FWU through hydathodes is possible in all but one of the Crassula species examined. The fact that LYCH fluorescence was present throughout the uptake path demonstrates that this is an entirely, or at least predominantly, apoplastic process (Fig. 8 ). The foliar distribution of hydathodes, occurring on the most exposed leaf surfaces (Table 2 ; Voronin et al. 1976; Martin and von Willert 2000), and the highly developed 3D venation that interconnects them (Rost 1969; Melo-de-Pinna et al. 2016; Fradera-Soler et al. 2021) are anatomical features that further imply that FWU and subsequent redistribution of absorbed water provide an ecophysiological advantage to Crassula species. Since succulents experience very little water loss, even small amounts of water from fog and dew can considerably improve their water balance (von Willert et al. 1992). Furthermore, Martin and von Willert (2000) reported that CO2 uptake rates in Crassula increase in response to FWU and that absorbed water can be transferred from wetted older leaves to younger ones, which highlights the far-reaching physiological consequences of this phenomenon.
Other genera in the Crassulaceae, such as Kalanchoe ,Aichryson and Sedum , have only marginal hydathodes or a single (sub)apical one (Caballero and Jiménez 1977; ‘t Hart and Bleij 2003; Thiede and Eggli 2007; Moreira et al. 2012), and even though there are reports of laminar hydathodes in some Cotyledon species (Weingart 1935), further anatomical investigations are needed to confirm this. This makes Crassula one of the few, if not the only, plant group in which laminar hydathodes and leaf succulence converge. Succulent organs are characterized by high values of hydraulic capacitance (C ) (i.e. the change in water content relative to the change in Ψ), which reflects their ability to maintain relatively high Ψ values even during periods of net water loss (Ogburn and Edwards 2010; Fradera-Soler et al. 2022; Leverett et al. 2023). As hypothesized by Berry et al. (2019), high values of C should result in lower overall FWU rates that are sustained for longer: an increase in Ψ resulting from FWU will be slower and will take longer to reach equilibrium, so that the Ψ gradients that underlie FWU can persist for longer. Indeed, a trade-off between C and FWU has been postulated, with species with high C exhibiting lower FWU rates and/or capacity (Gotsch et al. 2015; Boanares et al. 2018). Moreover, higher C means that succulents capable of FWU such asCrassula will be able to absorb greater amounts of atmospheric water, thus buffering declines in Ψ during drought. This suggests that the ecophysiological implications of hydathode-mediated FWU have likely played an important role in the diversification of Crassula , particularly in (semi-)arid habitats with periodically high air humidity in western southern Africa, such as the Succulent Karoo.
However, not all Crassula species seem to be capable of hydathode-mediated FWU. In this study FWU could not be induced inC. perforata (Fig. 8 ), which agrees with the observations by Martin and von Willert (2000). Tölken (1974, 1977) did not observe signs of FWU in C. rupestris , C. macowanianaor C. brevifolia either. In contrast with most Crassulaspecies, these four species share some commonalities: belonging to subgenus Crassula , a mostly glabrous leaf surface with a hydrophobic waxy bloom, a relatively large shrubby growth form, and the ability to dominate in exposed zonal habitats under considerable aridity (Jürgens 1995; Bruyns et al. 2019; Lu et al. 2022). It has been hypothesized that, since these larger species have more extensive root systems, high leaf hydrophobicity may increase water throughfall during precipitation events and provide more water to the roots (Rosado and Holder 2013; Fradera-Soler et al. 2021), which may render FWU less essential for their survival. This may also explain the loss of hydathodes in C. brevifolia (von Willert et al. 1992; Martin and von Willert 2000).