Together, our findings support that the trees from distinct vegetation types exhibit strategies related to invest in water-saving (species open-canopy environments) and optimize carbon acquisition (species closed-canopy environments) (Rozendaal et al. 2006). The plant communities are under strong selective environmental pressure (Marimon et al. 2014) and, to survive in their habitat, these species developed distinct resource use adaptive strategies (Abrams et al. 1994; Araújo et al. 2021b).
The similarities in stomatal dimensions (i.e., stomatal density, the maximum area of the stomatal pore, and stomatal size) between leaves from closed-canopy and open-canopy trees can be explained by the strong effect of seasonal climate (Marimon et al. 2014), as Pearce et al. (2006) observed that stomatal dimensions are strongly associated with seasonal environments and reflect climate adaptations. In the rocky cerrado, where access to water and soil nutrients is more limited (Marimon and Haridasan 2005) we expected that the stomatal dimensions would be smaller than the values recorded in the semideciduous forest (Franco 2002; Pearce et al. 2006). However, in this case, it is possible that other morpho-anatomical strategies, such as the greater thickness leaves (Table 3) and the high occurrence of trichomes (~110/mm-2) in the rocky cerrado and the total absence of trichomes in the leaves of the trees of the semideciduous forest compensated for the stomatal dimensions and resulted in very similar values between both vegetations, as in general, smaller stomatal dimensions are linked to a smaller amount of water available (Franco 2002; Rossatto et al. 2009; Araújo et al. 2021b).
Overall, species growing in closed-canopy environments exhibited acquisitive strategies (i.e., higher leaf water content and higher specific leaf area). On the other hand, species from open-canopy environments have adopted conservative strategies (i.e., higher leaf thickness and higher trichomes density), validating the economic spectrum leaf and reflecting the environmental differences between these vegetation types (Wright et al. 2004; Marimon and Haridasan 2005; Araújo et al. 2021b).
Larger stomata are commonly found in leaves of closed-canopy environments owin help to increase CO2 assimilation capacity and evapotranspiration rates, which consequently promote greater growth rates (Galmés et al. 2007; Ogburn and Edwards 2010), as recorded for transition forest in previous studies (Marimon et al. 2014). On the other hand, for the open-canopy vegetations (i.e., rocky cerrado and typical cerrado), species able to have a faster response to stronger seasonal water stress and higher tolerance to dystrophic soils, may have been favoured by natural selection (Franco 2002; Marimon-Junior and Haridasan 2005). In fact, smaller stomata, as found for species in the rocky cerrado and typical cerrado minimize water deficit and promote water use efficiency (Golstein et al. 2008). Also, smaller stomata are associated with plants growing in high irradiance levels and low air humidity, conditions normally observed in open-canopy environments (Bedetti et al. 2011; Araújo et al. 2021b), providing faster responses to reduced leaf transpiration (Rossatto et al. 2009).
We also found that species in the semideciduous forest invest in higher specific leaf area at a given leaf N concentration probably to overcome light competition by increasing the leaf area, light interception, and photosynthetic rates (Grime 1983; Cornelissen et al. 2003; Casas et al. 2011). If the light is the main limiting factor for species in forest environment (Carswell et al. 2000; Felfili et al. 2001; Montgomery and Chazdon 2002), from an evolutionary point of view, the investment in leaf area may be more advantageous, even considering that thinner leaves are more susceptible to herbivores or prone to water loss (Westoby et al. 2002). Unexpectedly, in our study semideciduous forest species showed the lowest N and P leaf concentration on an area basis, which may reflect a strong nutrient limitation in these forest soils (Marimon et al. 2014). Furthermore, species from open-canopy environments invested in higher leaf thickness that helps reduce leaf damage caused by herbivores and increase leaf lifespan (Grime 1983; Cornelissen et al. 2003; Bündchen et al. 2015). Interestingly, species from the transitional forest showed markedly similar traits compared to species from rocky cerrado and typical cerrado, such as low SLA, high TRD and LET, which indicate mixed strategies responding to mixed environmental drivers. These findings reinforce the idea that transitional forest is typical contact areas between savannas and forests (Ratter 1993; Ivanauskas et al. 2008), especially in the Amazonia-Cerrado transition (Marimon et al. 2014; Marques et al. 2020). These different combinations of ecological strategies in transitional forest can be advantageous in dealing with different environmental pressures, an essential condition for the persistence of species over time.
The positive relationship between N leaf tissue concentrations and stomata density for rocky cerrado and for transitional forest species may suggest a stronger pressure to optimize resources in these vegetations, particularly water and nitrogen, probably to maximize photosynthesis (Wright et al. 2003). Moreover, P and stomata size scaled positively, but only for forests formations, where plants should invest in primary growth to reach the canopy and successfully compete for light. Whereas P limitation is associated with lower wood density and greater hydraulic conductivity (Resco de Dios 2003), the coordination between P availability and stomata size (reflecting the anatomical adjustment to stomata opening control) in low-P soil and light-limited vegetation might be a key adaptation. Thus, the interaction between nutrients and water availability may have critical implications for the future distribution of plants and their responses to increasing drought severity and length (Cramer et al. 2009).
In addition, the relatively high trichomes density observed in rocky cerrado and typical cerrado species, may also reflect adaptation to control water deficit due increase water vapour concentration around the leaf boundary layer (Fahn and Cutler 1992; Larcher 2000). It is noteworthy that the combination of high temperature, high light incidence and low humidity of the air are determining factors influencing open-canopy environments species (Franco 2002; Araújo et al. 2021b). Trichomes are important adaptive strategies that help decrease light incidence and leaf temperature (Klich et al. 1997), which also promote water saving and concurrently avoid photoinhibition damage.
There was an overlap in leaf traits between all vegetation types analysed, which may be expected in a transition zone characterized by ecological tensions (Furley and Ratter 1988; Ratter 1993; Marimon et al. 2006, 2014). Notably, the similar leaf nutrient concentration at a mass basis and similar stomata density between trees of all vegetation types suggest some common environmental drivers, such as likely similar nutrient limitation and climate seasonality. However, morphological and anatomical adjustments are associated with a strong connection between plant structures and functioning and we could find two major clusters with different ecological strategies, where trees from closed-canopy habitats optimize carbon acquisition, while trees in open-canopy environments invest in water-saving strategies (Bedetti et al. 2011). In this context, our hypothesis was partially supported.
Our findings suggest that trees from closed-canopy environments may be more vulnerable to drought events as they present a combination of functional traits that are less safe to deal with prolonged droughts, especially semideciduous forest species that share no traits to manage larger water balance during droughts and may suffer more from water stress. Even with similar STS and AMAX values to the rocky cerrado, this may not guarantee greater water security for semideciduous forest species, because they have low hydraulic safety margins and, therefore, are more susceptible to the risk of hydraulic failure compared to open-canopy environments species (Aasamaa et al. 2001; Hetherington and Woodward 2003; Jancoski 2019). On the other hand, species from open-canopy environments are frequently exposed to water deficit and high temperatures and have developed a set of functional traits that are more resistant to drier and hotter conditions (Jancoski 2019; Araújo et al. 2021a; b).
In this region, where deforestation is accelerated, and the climate becomes increasingly drier and hotter (Jiménez‐Muñoz et al. 2013; Haghtalab et al. 2020). Trees are vulnerable to global warming, which has negatively impacted physiological mechanisms and caused irreversible damage to photosystem II, exposing species beyond their physiological limits that are adapted (Araújo et al. 2020a) and may have severe consequences, such as changes in plant communities composition, structure and functioning. Therefore, processes such as water use efficiency will be critical for the survival of species that inhabit hot and dry regions (Hulme 2005). Thus, tree species that invest in resource storage and water-saving strategies can better cope with expected future climate change, especially in the Amazonia-Cerrado transition, where some of the warmest temperatures and fastest warming in the tropics have been recorded and trees are more likely to be affected by ongoing and future climate change (Tiwari et al. 2020; Araújo et al. 2020a; b). Thus, we suggest that key traits linked to water savings contribute to the functional stability of species that occur in this important Amazonia-Cerrado ecological tension zone and can potentially contribute to the persistence of plant communities over time.