Tamarix

4.1 | Anatomical-Hydraulic Traits of the Tamarix View in CoL Species Compared to Phylogeny and Distribution

Despite their shared morphology and commonality in their occurrence at dry and salt-influenced sites, the investigated Tamarix species exhibited striking differences in their anatomical and hydraulic features. However, the phylogenetically most distant species T. aphylla and T. hispida did not differ in these traits from most of the other species and the phylogenetic distances among the species were not correlated with their distances among traits. This prompts us to reject our first general hypothesis as well as Subhypothesis 1.1. Under the assumption that the T. hispida specimens investigated in our study are representative of the species, T. hispida 's intermediate position in most of the studied features can be explained by its wide distributional range, which reaches from N China across entire Central Asia to Iran, covering approximately 90° of geographical longitude, and, thus, requires adaptation to a relatively broad range of habitat and climatic conditions. In principle, plant functional traits can adopt similar values across a wide range of environmental conditions (Anderegg 2023). Accordingly, 19 species of western North-American oaks exhibited a relatively high embolism resistance along an aridity gradient from mesic to xeric sites (Skelton et al. 2021). In a comparison of deciduous ring-porous oak species, Quercus robur L., which has the widest distribution of the Eurasian oaks extending from north-western Spain to the Ural (Meusel, Jaeger, and Weinert 1965) with a strong climatic gradient, exhibits a P 50 value of −2.7 MPa that is between that of the North-American Q. rubra L. (−2.3 MPa), which has been successfully cultivated in Central Europe, and the indigenous Q. petraea ([Matt.] Liebl.) and Q. pubescens Willd. (both −3.3 MPa; Tyree and Cochard 1996). Likewise, T. hispida 's anatomical-hydraulic traits took a position between the other Tamarix species along the regressions with climatic variables except for wood density, which was the lowest of all the Tamarix species studied here. However, its low wood density of 0.62 ± 0.02 g cm−3 is in the range of 0.51—0.65 g cm−3 that, across a broad range of angiosperm and gymnosperm families from all continents, has been assessed to be most efficient in water transport ( Kallarackal et al. 2013). This may enhance the species' capability to conquer additional habitats. Wood density also was the only anatomical-hydraulic trait, in which T. hispida differed significantly from T. aphylla that also has a wide distribution (across approximately 90° of longitude) but is more confined to warmer climates ( Table 1 View TABLE 1 ).

In conformity with our Subhypothesis 1.2, the traits of T. boveana and T. gallica , which are proximate in phylogeny, geographic distribution and exposure to site and climate conditions, are similar to each other. This is in parallel to the findings by Skelton et al. (2021) of closely related North-American oak species varying only little in their resistance to xylem embolism. It seems that in all these species, genetic relatedness, distribution range and adaptation to similar environmental conditions have resulted in similar trait expression. In the case of the Spanish Tamarix species investigated here, this similarity in trait expression may have evolved during the genus' spread from the east to the west of the Mediterranean region and adjacent areas. In that direction, the species number of Tamarix decreases (Terrones and Juan 2023) and this trend may have been accompanied by a specialisation during the evolution of these two taxa that are the youngest in our species set (≤ 1 million years [Myr] old) (Terrones and Juan 2023). This specialisation may have been a response to the transition from a temperate to a cooler and drier climate, especially during the glacials, at the end of the Early Pleistocene (Middle–Late Calabrian), which was also accompanied by a spread of steppe taxa at lower elevations of the Mediterranean region ( Combourieu-Nebout et al. 2015). On the other hand, larger phylogenetic distances among co-occurring woody species of the same genus with convergent traits have also been found and related to competition avoidance or niche partitioning within the same habitat in oak communities of Florida ( Cavender-Bares et al. 2004) . At the habitat scale, such niche partitioning between the two Spanish Tamarix species of our study may have been effective at sites with severe drought ( T. gallica ) or salt stress ( T. boveana ; cf. Table 1 View TABLE 1 ) but could not be explored within the scope of the present investigation.

Tamarix ramosissima View in CoL displays a similarly wide or even wider longitudinal distribution than T. hispida View in CoL (from N Korea to SE Turkey). Maybe even more importantly, it can grow under very harsh environmental conditions in an extremely continental climate, characterised by very cold winters and hot-dry summers with extremely low amounts of annual precipitation (down to approximately 33 mm; Thomas et al. 2000). In such regions, T. ramosissima View in CoL can penetrate far into the desert ( Bruelheide et al. 2010) by forming cone-shaped dunes (Qong, Takamura, and Hudaberdi 2002), provided that the plants have access to groundwater (Thomas et al. 2006). Under conditions of regular severe winter frost and high transpirational demand in summer, a high resistance against xylem dysfunction due to embolism of the conduits is necessary. In accordance with our Hypothesis 2.1, this is accomplished in T. ramosissima View in CoL by the most negative P 50 values found in our study. Likewise, in a comparison of Nothofagus species in South-Central Chile, N. antarctica (G.Forst.) Oerst. View in CoL , whose distribution centre is located at the highest elevations (> 1500 m a.s.l.), exhibited the smallest conduit areas and the most negative P 50 values ( Dettmann, Pérez, and Thomas 2013). Nevertheless, T. ramosissima View in CoL also disposes of a certain fraction of large conduits and exhibits the largest maximum conduit area, which facilitates high rates of water transport from the roots to the leaves (i.e., high k t values) during the period of rapid growth after the onset of continental spring (Thomas et al. 2008). Thus, the possession of large fractions of both small and wide conduits—'vessel dimorphism’ (cf. Dickison 2000)—facilitates the expansion of T. ramosissima View in CoL and T. hispida View in CoL into regions characterised by hot-dry as well as cold seasons.

As they display (semi-)ring porous wood with its broad vessels as well as simple perforation plates, Tamarix species are already at the pinnacle of water-conducting efficiency (cf. Sperry 2003). Nevertheless, the differences in anatomical and hydraulic traits among the species investigated in the present study might to some extent be related to their evolutionary history, although we found no significant correlations between the distances in phylogeny and the investigated traits. Tamarix aphylla View in CoL , which has a broad longitudinal distribution from north-western India to Morocco (approx. 83°), is similar to most other Tamarix species of the present study in its anatomical-hydraulic traits and belongs to the basal group of the genus, which has a crown age of 16.65 Myr (Terrones and Juan 2023) that extends to the climatic optimum of the Miocene. Speciation then progressed to T. hispida View in CoL with an age of 4.47 Myr (Terrones and Juan 2023) and a similarly wide distribution, also requiring adaption of the wood's anatomical-hydraulic traits to a broad range of environmental conditions (see above). Tamarix nilotica View in CoL with an age of less than 3 Myr (Terrones and Juan 2023) and a distribution range restricted to the Levant and north-eastern Africa is more specialised, exhibiting anatomical traits that facilitate an efficient water transport at times of ample water supply. Its evolution may be related to the onset of the Mediterranean climate (3.2—2.8 Myr B.P.; Terrones and Juan 2023). At the other end of the spectrum, the Spanish species T. gallica View in CoL and T. boveana View in CoL , the youngest taxa of our study (≤ 1 Myr; Terrones and Juan 2023), exhibit traits related to high embolism resistance, which is typical of species that need not only tolerate drought but also salt stress. Unfortunately, no robust data are available on the ages of T. ramosissima View in CoL and T. negevensis View in CoL .

Wood hydraulic properties, and hydraulic conductance and embolism resistance in particular, are also influenced by other anatomical traits, whose examination was beyond the scope of the present study. For instance, conduit conductivity scales with conduit length ( Choat, Cobb, and Jansen 2008) and is positively related to the extent of conduit aggregation ( Martínez-Vilalta et al. 2012). Embolism resistance is not only positively correlated with (t b −1) h 2 (see Section 2.4), but also with the proportion of the xylem's libriform fibre walls close to the conduits and negatively, with the fibres' lumen areas ( Jacobsen et al. 2005; Lachenbruch and McCulloh 2014). Regarding the conduits' ultrastructure, embolism resistance proved to be negatively related to the pit membrane area per conduit and the occurrence of large pores ( Hacke et al. 2006; Wheeler et al. 2005). However, as the conduit's pit membrane area is connected to the conduit diameter, which, together with (t b −1) h 2, has also been determined in the present study, we are confident that our anatomical investigations have captured the most relevant traits related to the hydraulic properties of the wood. Nevertheless, other anatomical traits that have not been investigated here might exhibit a stronger linkage to the species' phylogeny.

4.2 | Anatomical-Hydraulic Traits of Tamarix Species in Relation to Climate

Our results agree with former studies showing high correlation between the variation in anatomical-hydraulic traits and site climate. Across the Oleaceae family with its cosmopolitan distribution from the tropics to cool-temperate latitudes, including 29 genera and more than 600 species, the vessel diameter decreases and the vessel frequency increases with increasing seasonality or lower cold-season temperatures, which can be interpreted as a strategy of higher safety from freeze-induced embolism in cold periods (Baas et al. 1988; Niu, Meinzer, and Hao 2017; Sperry and Sullivan 1992). Likewise, out of five endemic Rhamnus species ( Rhamnaceae ) growing in the Mediterranean region of southern Turkey, the species occurring close to the sea level in a milder climate exhibited a larger vessel area (calculated from the averaged radial and tangential vessel diameters) than the other species, which grew at elevations of 700 m a.s.l or above (Akkemik et al. 2007). The P 50 values of the Asian Juniper species J . drupacea Labill., J. pseudosabina Fisch. & C.A.Mey. and J. seravschanica Kom. were negatively related to the mean annual temperature and positively, to the precipitation sum of the driest quarter at their sites of growth ( Larter et al. 2024). For Prunus ( Rosaceae ), evidence was provided for a co-evolution of wood anatomy-based embolism resistance in closely related species, driven by adaptation to environmental conditions (Scholz et al. 2013). Overall, these results suggest that not only forms of growth, life and leaves but also anatomical-hydraulic traits of the wood have been differentiated along phylogenetic paths during evolution, whereas their extant configuration is organised as a specific adaptation to the respective sites of growth, resulting in clear differences among related species. At the species level, the results of our comparison of Tamarix species across a wide geographic gradient is in line with these implications.

At least five out of the seven Tamarix species studied here can certainly be considered phreatophytes, that is, plants with a temporary or permanent access to the groundwater ( Table 1 View TABLE 1 ; Thomas 2014). Probably, this is also true for T. negevensis and T. nilotica (Zohary 1982) . Accordingly, rooting depths of up to 30 m have been reported for Israeli species of this genus (Zohary 1982). This means that such plants are less dependent on precipitation and that the vapour pressure deficit of the air has a much larger effect on the plants' water relations than rainfall (Thomas et al. 2008). Correspondingly, conduits with a low density per unit shoot cross-section but with a large hydraulic diameter and maximum cross-sectional area—traits that lead to an increase in hydraulic conductivity—were found in species growing at sites with only minute amounts of precipitation in the year's driest quarter ( Figure 3 View FIGURE 3 ), where the plants most strongly depend on access to groundwater. Nevertheless, precipitation events can result in an increased water uptake by Tamarix due to a rise in the local groundwater level (Nippert et al. 2010).

Contrary to our Hypothesis 2.2, however, T. boveana and T. gallica , which were sampled from regions with relatively mild temperatures throughout the year (and, accordingly, small annual temperature amplitudes) and moderate values of average SPEI, did not exhibit anatomical-hydraulic traits indicative of a low resistance to xylem embolism. Instead, their wood features, characterised by high wood density, numerous but small conduits, low k t and strongly negative P 50 values, were typical of species growing under arid conditions. Although the sampling sites of T. boveana and T. gallica in our study are not the climatically most extreme ones across the range of our species, the species' capabilities of tolerating not only dry conditions but also high salt concentrations ( Table 1 View TABLE 1 ) require the investigated traits of drought tolerance. Accordingly, their P 50 values were even lower than the medians of measured P 50 values from desert or Mediterranean biomes but within the range of measured P 50 values across taxa occurring in regions with low annual precipitation ( Maherali, Pockman, and Jackson 2004). To our knowledge, the gymnosperm Juniperus drupacea , which occurs from southern Greece to Syria, currently holds the record of the most negative P 50 value determined so far in Eurasian woody species (−11.8 MPa; Larter et al. 2024). The anatomical-hydraulic features of T. boveana and T. gallica may have also facilitated their spread into more continental regions of the Iberian Peninsula. Overall, over evolutionary timescales, climate and phylogeny interact to determine physiological traits like embolism resistance within a genus ( Larter et al. 2017) but spatially, climate is the major driver of tree species distribution ranges at the global scale ( Lerner et al. 2023). It needs to be kept in mind, however, that it remains problematic to predict traits from the environment because in a given habitat, several plant species can coexist with quite different expressions of individual traits (Anderegg 2023).