This study investigated the intraspecific variation in wood features and tree growth of B. riedelianum trees originating from three populations and grown in two common garden experiments in São Paulo State, Brazil. The results show that tree growth, determined by stem height and diameter, was mostly influenced by the environment at the trial sites, specifically precipitation and SPEI, being promoted by wet conditions. Wood features vary among populations and are strongly influenced by the temperature of trial sites.
4.1. Genetic Difference between Populations
We raised the hypothesis that intraspecific variation in the wood features of B. riedelianum
trees would be related to the climatic of populations origin site. We expected that populations from drier and warmer sites, with lower precipitation, would have wood characterized by higher water transport safety than trees from cooler sites with higher precipitation. Indeed, trees from Bauru, the site with lower annual precipitation and higher temperature, had narrower vessels and thinner walls, more clustered and denser, and occupying a larger fraction of wood than trees from other populations. Together, these anatomical features provide greater safety for water transport under higher negative tensions in drier environments [16
]. However, unlike our expectation, trees from Alvorada do Sul, the site with higher annual precipitation than other provenances showed wood with water safety similar to that in trees from Bauru. We observed wood anatomical features with greater efficiency in water transport in trees from Gália, the site with intermediate precipitation between provenances.
We found a lower potential hydraulic conductivity, narrow vessels, with thin walls, in higher density and more clustered, with smaller intervessel pits and narrow openings, rays in higher density and higher parenchyma fraction (axial parenchyma + rays), features that together indicate greater water transport safety in trees from Alvorada do Sul. This region is characterized by high rainfall, fertile soils, low winter temperatures, and being prone to frost [28
]. In general, narrow vessels are advantageous in sites with low temperatures to avoid freeze-induced cavitation, as well as to minimize the impacts of drought-induced cavitation [46
]. According to Fisher et al. [5
] and Schreiber et al. [6
], the selection of narrow vessels may be an adaptation in populations that experience freezing periods that minimize the effects caused by frost induced cavitation, thus maintaining the xylem functional for the next growing season. Our findings, therefore, suggest that the formation of wood with high hydraulic safety in trees from Alvorada do Sul could reflect the low temperatures experienced at the origin site. However, experimental studies are necessary to confirm this statement.
4.2. Phenotypic Plasticity of Tree Growth and Wood Formation
In general, our trees responded to the increase in water availability through the formation of wood with a higher water transport efficiency. Regardless of origin, trees grown in a wetter environment (Luís Antônio) had wider vessels, with thicker walls, less clustered, with larger intervessel pits and wider openings, longer vessel elements, fibers with narrower lumen and thicker walls, less frequent rays and smaller fraction of parenchyma (axial parenchyma + rays). The increase in vessel diameter also had a positive effect on potential hydraulic conductivity. Our results showed that the vessels are the cells with the highest degree of plasticity in B. riedelianum
, with variations in diameter, wall thickness, grouping, and size of intervessel pits. Vessels are responsible for long-distance water conduction in plants, performing a central role in hydraulic efficiency and safety [16
]. Variations in vessel dimensions could represent a key trait for the adaptation or acclimation to changes in environmental conditions, such as increasing of temperatures and drought events, thus ensuring growth and survival of this species within its natural distribution range.
The plastic responses observed in wood of mature B. riedelianum
trees in the wetter trial site reflect greater efficiency in conducting water and mechanical support on vessel walls. In this trial site, the formation of larger vessels provides low resistance to water flow and increases water transport ability [16
]. The thickening of vessel walls makes larger vessels less prone to mechanical damage, such as micro-fractures and implosion of their walls [16
]. Micro-fractures in the vessel wall may trigger the heterogeneous nucleation of gas particles between the cell walls or intercellular spaces, initiating the embolism process [38
]. Large, thick-walled vessels also have larger intervessel pits with wider openings. These latter are potentially more efficient in conducting water but decrease the mechanical reinforcement of vessel cell walls [11
]. In addition, intervessel pits with large openings could decrease support to the pit membrane during stretching [49
]. Thus, the formation of fibers with narrower lumen and thicker walls found in B. riedelianum
trees grown in the wetter trial site could compensate for potential cell wall weakening. Therefore, wide thicker-walled vessels immersed in a denser fiber matrix may confer greater mechanical strength to support larger intervessel pits and with wider openings in the wood.
We found plasticity in the size of vessel elements. In vessels, the length is determined by the size of initial fusiforms of the vascular cambium [50
], and the diameter is linked to cell expansion. Variation in water availability to vascular cambium has an effect on the elongation of the initial fusiforms [51
] and cellular expansion [52
]. Therefore, the higher water availability in Luís Antônio may have favored the formation of longer and wider vessels. Similarly, the lower precipitation in Pederneiras may have been a limiting factor to elongation of the initial fusiform of the vascular cambium and cell expansion, thus resulting in the formation of shorter vessel elements and narrower vessels.
When testing the responses of the wood of B. reidelianum
to variations in temperature, precipitation and SPEI among trial sites using transfer functions, we found that temperature had a greater effect on the anatomical features of vessels, fibers and rays. In general, the wood showed a greater capacity to water transport and vulnerability to mechanical damage, with larger vessels, less clustered and with thicker walls and longer fibers, wider and thinner walls in warmer environments. In the context of ongoing global changes, plants will experience warmer temperatures, often associated with less precipitation. The formation of wider vessels makes the wood more prone to drought-induced embolism, leading to hydraulic failure and even tree death [53
]. Our results also indicate that taller rays and higher density occur in warmer environments. From the functional perspective, taller rays and higher density associated with larger vessels would be an important requirement to maintain hydraulic conductance in the stem, as well as hydraulic recovery through vessel refilling mechanisms [20
Our results also indicate that wood density responds to an increase in temperature, with less dense wood occurring in warmer environments. The lower density may result from the combination of wider elements, vessels, and fibers, with thinner walls. Less dense wood leads to a decrease in the mechanical strength of the stem [55
], making it more fragile and prone to breakage caused by animals or falling debris [56
]. The decrease in wood density makes plants less resistant to damage caused by herbivores and pathogen attack, which can decrease their growth, life-span, and biomass allocation [57
]. Therefore, our results suggest that an increase in temperature may stimulate B. riedelianum
to form wood more prone to embolism, with lower mechanical resistance and higher susceptibility to pathogen attack.
The growth in stem height and diameter was sensitive to changes in the environmental conditions of the trial sites. Regardless of provenance, all trees responded similarly in both common garden experiments, with increased growth in stem height and diameter in the wetter trial site. In addition, the result of the transfer function on stem height and diameter growth demonstrates that tree growth benefits from an increase in precipitation and responds negatively to higher SPEI. Considering the climate predictions indicating 25% increases in precipitation across the natural range of B. riedelianum
, a region that mainly covers southern and south-eastern Brazil [24
], we may expect a positive impact on tree growth in a future scenario. However, the possible benefits of an increase in precipitation should be carefully examined. Firstly, possible changes in rainfall intensity, duration, and distribution throughout the year should be taken into account. Secondly, south and south-eastern Brazil is already exploited for crop production, and potential new areas are awaiting future agricultural expansion and development in the next decades, which will make the natural range of the studied species more prone to deforestation. At the same time, an important warming is predicted in South America [24
], making it difficult to predict the growth responses of trees under complex climate change scenarios. Under these conditions, plastic responses in the growth of B. riedelianum
could be essential to guarantee persistence of the species in the drier sites.