Do karst woody plants control xylem tension to avoid substantial xylem cavitation in the wet season?

Cavitation-induced decrease in the hydraulic conductance of plant stems, roots, and leaves has long been suggested to lead to stomatal closure, thereby preventing the increase in xylem tension that can induce run-away xylem cavitation (Jones and Sutherland 1991; Nardini and Salleo 2000; Domec et al. 2006; Guyot et al. 2012; Daniela et al. 2016; Xiong et al. 2018). Because embolized xylem cells can reduce hydraulic conductivity and greatly retard photosynthesis and growth, plants would be expected to have strong control over xylem tension and typically operate at a water potential above or near the critical potential at which cavitation commences (Sperry 2000). This hypothesis has been evidenced by tight associations between minimum water potential and hydraulic resistance in various ecosystems (e.g., Pockman and Sperry 2000; Markesteijn et al. 2011b; Gadow et al. 2016). For instance, Nardini and Salleo (2000) demonstrated that 11 tree species in a Mediterranean ecosystem suffered an average of 10% cavitation before stomata began to close. A survey of the hydraulic architecture of 13 tropical dry forest species in Bolivia showed that the average loss of hydraulic conductivity corresponding to minimum leaf water potential was about 20% in the wet season (Markesteijn et al. 2011b).

However, the functional association between minimum water potential and hydraulic safety does not prove that plants can control embolisms, because the loss of hydraulic conductivity is not a linear function of water potential. In fact, a detailed analysis of published data has shown that there exists a large variation among species at the same site in native embolism rates during a day (Pockman and Sperry 2000; Markesteijn et al. 2011a, 2011b). For example, re-analysis of data from Markesteijn et al. (2011a, 2011b) revealed that daily conductivity loss ranged from 5%–63% of maximum conductivity. The embolism rate varied widely, from 11%–95% in the dry season and from 11%–93% in the wet season, across 12 Sonoran desert species (Pockman and Sperry 2000).

Johnson et al. (2009) hypothesized that there may exist two different strategies for the daily maintenance of hydraulic conductivity: 1) a “radical” strategy of substantial loss and subsequent recovery and 2) a more conservative strategy of loss avoidance. Such a hypothesis, we believe, should be assessed broadly in different global ecosystems for a more comprehensive understanding of the role of cavitation in plant water balance. Furthermore, the two strategies might have different impacts on photosynthesis. The conservative strategy requires that plants close their stomata before catastrophic hydraulic failure occurs. As soon as stomata close, photosynthesis would suffer from a shortage of CO₂ and absorbed light would exceed photosynthetic requirements; consequently, photosystem II (PSII) would be temporarily or chronically photo-inactivated, which could be reflected by a decrease in maximum quantum efficiency of PSII photochemistry (F_v/F_m) (Baker 2008). On the other hand, the radical strategy, which allows massive temporary cavitation with stomata open, would not affect PSII photochemistry, because ambient CO₂ could diffuse into leaf intercellular spaces, particularly if such massive cavitation temporarily relieved water stress (Holtta et al. 2012); therefore its F_v/F_m should be higher than that in the conservative strategy. This expectation, to our knowledge, has not yet been tested.

The karst topography is characterized by shallow soils with low water-retention capacity and high porosity of the underlying limestone rock. Compared to other karst areas at similar latitudes, the karst area in southwestern China is unique because of its abundant precipitation, with rainfall concentrated in the growing season (from May to September) (Wu et al. 2003), mainly due to the rise in elevation of the Qinghai–Tibet Plateau. Previous studies have shown that the water potential at which a 50% loss in hydraulic conductivity occurs (Ψ₅₀) in 31 woody species in this area was only − 1.27 MPa (Fan et al. 2011), compared with high resistance in Mediterranean (Tognetti et al. 1998) and Central American karst regions (McElrone et al. 2004). Xylem tension measurements in the wet season have shown that woody plants experienced average midday leaf water potentials (Ψ_min) of about − 1.5 MPa (Yu et al. 2002; Liu et al. 2012), suggesting that, on average, more than 50% embolism will occur in the field. Unfortunately, the Ψ₅₀ and Ψ_min measurements were made either separately or across different species; therefore, whether karst woody plants in southwestern China can control xylem tension above a critical threshold remains unknown. This knowledge is also crucial to better evaluate the suitability of plant species to site-specific reforestation programs in the karst area in southwestern China, which has suffered serious degradation due to intensive human disturbances.

The objectives of present study were to 1) investigate variation in native embolism in branches and its relationship to leaf traits in 13 woody species (six evergreen and seven deciduous) at two sites in the karst area of southwestern China; 2) examine whether there are associations between Loss and PSII’s photochemistry among woody species; and 3) investigate the relationship between native embolism and leaf phenology. Because many studies have demonstrated that evergreen species have larger safety margins (the difference between Ψ_min and the water potential at which cavitation occurs), higher cavitation resistance, and lower daily minimum water potential (Choat et al. 2005; Chen et al. 2009; Markesteijn et al. 2011b; O’Brien et al. 2017) than co-occurring deciduous species, we expected that evergreen species would lose less conductivity than deciduous species on sunny days.

The loss of leaf conductivity in the field, most likely due to leaf or stem xylem embolism (Domec et al. 2006; Woodruff et al. 2007; Johnson et al. 2009; Blackman et al. 2017), can be accurately predicted from field measurements of leaf water potentials and laboratory-generated vulnerability curves (Brodribb and Holbrook 2004; Johnson et al. 2009). The 13 species in this study varied substantially in Loss in the field, from 1.39% in the evergreen I. chinensis to 90.07% in the deciduous S. sebiferum in the field. The large variation in Loss in the karst area in China argued against the hypothesis that plants control xylem tension above threshold for cavitation. Interestingly, Loss in the current study did not significantly depress the efficiency of PSII and/or the photosynthetic rate, suggesting that photosynthetic capacity was not affected by xylem cavitation, even in the extreme case of S. sebiferum, which lost 90% hydraulic conductivity at noon.

Loss values for a total 75 species was bimodally-distributed, further supporting the idea that plants can adopt two strategies to deal with xylem cavitation: 1) maintain the water potential above the cavitation threshold, or 2) tolerate massive xylem cavitation and subsequent recovery (Jones and Sutherland 1991; Johnson et al. 2009). Some plants can operate well beyond the point of xylem failure via stomata closure, but they sacrifice carbon fixation, because ambient CO₂ cannot diffuse into leaf intercellular spaces. Other plants can tolerate massive cavitation over the short term, allowing photosynthesis to continue. In fact, massive cavitation was experimentally demonstrated to help relieve water stress temporarily by releasing water from embolizing conduits to the transpiration stream (Logullo and Salleo 1992; Holtta et al. 2012) and to lower the risk of xylem wall implosion (Pratt et al. 2008).

There were no sign of physiological stress in the 13 species at noon and no significant differences in F_v/F_m between plants with less than 40% and more than 60% Loss. The relationship between Loss and F_v/F_m was also not significant. Thus, plants adopting both strategies could maintain PSII efficiency at noon in the karst region of China, possibly via different hydraulic solutions. For example, the radical strategy allowing massive xylem cavitation could temporarily relieve water stress and therefore might maintain photosynthesis for hours before leaf water reserves are exhausted (Logullo and Salleo 1992; Holtta et al. 2012). Such massive embolized conduits could be expected to be fully refilled before the following dawn. In fact, Ψ_predawn values of two fig species in the karst region of southwestern China were close to zero (Liu et al. 2012b), suggesting they had fully refilled embolized conduits. However, another survey of 50 karst woody species at forest site demonstrated that Ψ_predawn values were about − 1.0 MPa (Liu et al. 2012a), suggesting that embolisms persisted. Such a large discrepancy between two studies at similar sites deserves further investigation. For the conservative strategy, these plants might develop a stronger ability to dissipate excessive absorbed light energy as nonphotochemical quenching (NPQ) to alleviate excitation pressure at PSII reaction centres and consequently maintain PSII maximum quantum efficiency (Baker 2008). Interestingly, it is noteworthy that g_s had no association with Loss (Table 4); possibly whole-plant hydraulic adjustment participates in the regulation of Loss, which merit further investigation.

The previously reported strong association between Ψ₅₀ and Ψ_min across species in some ecosystems (e.g., Pockman and Sperry 2000; Markesteijn et al. 2011b; Choat et al. 2012) was not observed by using our data in the current study, suggesting that xylem resistance is not necessarily related to the tensions experienced in the karst area. In fact, the absence of such an association could be explained by the fact that karst plants maintained a very narrow range of Ψ_min (from − 0.96 MPa in S. obovatus to − 1.61 MPa in M. japonicus) in the present study. Such “isohydric” regulation behaviour may also have been seen in other studies in this area (Yu et al. 2002; Liu et al. 2012a). For example, Liu et al. (2012a) reported a Ψ_min range from about − 1 to − 1.8 MPa in the wet season and − 1 to − 2.6 MPa in the dry season (50 tree species), and Yu et al. (2002) reported a Ψ_min range from − 0.79 to − 2.2 MPa in the wet season (25 tree species). In other words, plants with isohydric regulation might have larger variations in loss of hydraulic conductivity than “anisohydric” one. For example, a relatively isohydric piñon pine experienced loss of root hydraulic conductivity ranging from 0 to 100% PLC during a seven-year observation period, compared with the constant and very small PLC of a co-occurring anisohydric juniper (McDowell 2011).

Theoretical assessments of the role of stomatal regulation on hydraulic conductance revealed a positive, linear relationship between g_s and K_l if the whole-plant water pressure gradient and D between the leaf and air remain similar (Sperry et al. 1993; Oren et al. 1999). Given that the species studied here had similar Ψ_min and D, the close relationship between K_l and g_s found was consistent with previous studies in other ecosystems (Hubbard et al. 2001; Santiago et al. 2004). Interestingly, the K_lnoon was not significantly correlated with g_s; similarly, Santiago et al. (2004) reported that the correlation coefficient between K_init and g_s was lower than that between K_lmax and g_s. The absence of correlation between K_lnoon and g_s could have many explanations. For example, leaf capacity may decouple the relationship between K_lnoon and g_s.

Evergreen species, with 42.7% Loss at midday, tended to maintain xylem conductivity better than deciduous species (with 64.7%) in the current study, although the difference between groups was not significant (P = 0.221). This tendency was also seen in the more even distribution of Loss frequencies in deciduous than in evergreen species; 18 deciduous species had less than 50% and 18 had more than 50% Loss, while more evergreen species (25 of 39) had less than 50% Loss. These results were consistent with our expectation that evergreens could avoid massive cavitation at midday better than co-occurring deciduous species.

A MANOVA revealed a non-significant contrast between deciduous and evergreen species in hydraulic and associated leaf traits, which means these two life-history adaptations are likely part of a continuum of strategies (Borchert 1994; Brodribb et al. 2002; Williams et al. 2008; Ishida et al. 2010). On the other hand, deciduous species were geared towards higher hydraulic conductance, photosynthetic rate, stomatal conductance, lower hydraulic safety margin and lower cavitation-resistance and minimum water potential than co-occurring evergreen species, in agreement with previous reports (Gartner et al. 1990; Sobrado 1993; Choat et al. 2005; Chen et al. 2009; Markesteijn et al. 2011b; Fu et al. 2012; O’Brien et al. 2017). The strategy of higher tolerance of hydraulic loss seen in deciduous species might guarantee sufficient carbon gain when water is abundant, or water stress could be relieved temporarily by releasing water from embolizing conduits to the transpiration stream, which might favour fast growth closely associated with a higher photosynthetic rate during the growing season (Santiago et al. 2004; Chen et al. 2009). During droughts or winter, deciduous species minimize transpiration by shedding their leaves, thereby greatly reducing the risk of long-term hydraulic failure (Maherali et al. 2004).

In conclusion, we found no evidence that karst woody species in southwestern China could control xylem tension to avoid substantial xylem cavitation. The variation in loss of leaf conductivity in this study did not significantly depress the efficiency of PSII. Ψ₅₀ was not related to Ψ_min. The frequency distribution of the loss of leaf hydraulic conductivity due to xylem cavitation at noon in a total of 75 species from this study and the literature supported the idea presented by Johnson et al. (2009) that there may exist two different strategies for the daily maintenance of hydraulic conductivity. The co-occurring evergreen and deciduous woody species of karst in southwestern China differed significantly in some stem hydraulic and associated leaf traits. Under the high variable daily moisture conditions in karst areas in China, the interactions between isohydric regulation behaviour, low cavitation resistance (Fan et al. 2011), and other hydraulic traits (particularly root systems) for maintaining homeostatic water balance in whole plants are worthy of further study. A more sophisticated design of field investigation on a single species in different seasons, to explore the relationship between PLC, F_v/F_m, water storage capacity and NPQ, is necessary for future study.