Variation in leaf functional trait and ecological strategies in two seedling species in disturbed forest fragments in Eastern Amazonia

ABSTRACT

The importance of understanding environmental changes has stimulated the study of plant functional traits, which reflect the species' ecological strategies and determine how they respond to environmental variations and climate change. We tested whether the functional traits and ecological strategies of the species Bactris hirta Mart. and Tetracera sp. in the seedling stage respond to water and soil nutrient availability and landscape variation. We evaluated leaf traits, (SLA, LDMC, Ψ_TLP, and ΨsFT) in thirteen fragments in Barcarena, Brazil. The SLA and LDMC were collected during periods of low and high water availability. We analyzed macronutrients, soil texture, and landscape metrics. Both species showed higher LDMC during periods of low water availability, despite no changes in SLA. The variation in leaf traits led to changes in CSR strategies; however, there was a prevalence of the stress-tolerance strategy. The Ψ_TLP and ΨsFT were more negative in palm species than in liana. The landscape and soil characteristics influenced resource allocation patterns and drought-related traits of the species, yet the species differed in the relationships among the variables. The ability of both species to show intraspecific variability may be an important mechanism contributing to the abundance and prevalence of palms and lianas in forest fragments.

Keywords:
CSR strategy; fragmentation; leaf traits; liana; palm; variation in water availability

Introduction

The Amazon comprises a complex system with diverse ecosystems, climatic and edaphic variations, and a high diversity of plants, exhibiting significant morphological, physiological, and phenological variations (Steege et al., 2015). At regional and local scales, soil gradients influence the diversity and productivity of Amazonian ecosystems (Quesada et al., 2012). The physical characteristics of the soil influence water retention capacity, and nutrient availability can drive species distribution and richness within a community (Quesada et al., 2012). The Amazon exhibits great soil heterogeneity due to different geological and geomorphological processes involved in its formation (Quesada et al., 2010a), resulting in significant variation in nutrient availability (Quesada et al., 2010a; Dalling et al., 2016; Cunha et al., 2022). Furthermore, there is a marked variation in precipitation and seasonality in the Amazon basin, influencing species distribution (Esquivel-Muelbert et al., 2019). The diversity and functioning of Amazonian ecosystems, which provide numerous ecosystem services, are threatened by anthropogenic actions that modify land use and natural landscapes (Gatti et al., 2014; Lapola et al., 2023).

Among anthropogenic actions, mining activities have caused various environmental impacts, ranging from deforestation for ore extraction to those associated with ore processing (Murguía et al., 2016). There is also increasing urbanization, leading to the conversion of forested areas for agricultural cultivation, urban expansion, and others, resulting in landscape fragmentation. Moreover, the remaining fragments are often subjected to selective tree logging and a pronounced edge effect (Lapola et al., 2023). These environmental disturbances can lead to changes in the remaining fragment microclimate, soil properties, and the isolation of plant populations (Silva & Tabarelli, 2000), resulting in intense forest degradation (Lapola et al., 2023).

The importance of understanding environmental changes has stimulated the study of plant functional traits, which reflect their ecological strategies and determine how they respond to environmental variations and ongoing climate change (Violle et al., 2007). Functional traits reflect resource acquisition and use strategies, as well as contributing to ecosystem functioning (Violle et al., 2007; Reich, 2014). Changes in environmental conditions can modify species traits, their resource allocation patterns, and trade-offs in resource utilization (Chesson, 2000; Westoby et al., 2002; Reich, 2014). Therefore, it is essential to evaluate how resource availability (water and nutrients) and environmental changes influence species traits.

Leaf morphological traits, such as specific leaf area (SLA) and leaf dry matter content (LDMC), are related to carbon investment for leaf production and are associated with leaf longevity, photosynthetic activity, and species growth rate (Wright et al., 2017). Global-scale studies highlight the role of nutrients and soil water availability in shaping resource allocation patterns for leaf tissue construction, thus establishing the leaf economics spectrum (Wright et al., 2017). Within this spectrum, species in environments with low soil nutrients (e.g. phosphorus) and water availability tend to exhibit leaves with more conservative traits, such as lower SLA, higher LDMC, and longer leaf longevity (Wright et al., 2017; Reich, 2014), in contrast to a more acquisitive strategy. However, increased anthropogenic activities have altered nutrient cycling and availability in the soil, increasing nutrient losses through leaching and erosive processes, thereby influencing these global relationships (Steffen et al., 2015).

Integrative leaf functioning traits, such as the water potential at the leaf turgor loss point (Ψ_TLP) are important traits related to soil water availability and drought resistance (Bartlett et al., 2012; 2014). The Ψ_TLP is a crucial indicator of plant water stress, indicating the threshold at which the plant ceases growth (Bartlett et al., 2012). Osmotic adjustment (ΨsFT) is a strategy used by plants to maintain cell turgor and may be associated with cellular ion concentration, serving as an important strategy for species to overcome periods of lower water availability in the environment (Bartlett et al., 2012; 2014).

It is possible to determine the species' competitive, stress-tolerant, and ruderal (CSR) strategies using leaf functional traits (Pierce et al., 2017). The CSR strategies indicate how ecological and evolutionary processes modulate plant species' strategies in response to stresses and disturbances (Grime, 1977; Pierce et al., 2017). Species can be classified according to their ability to compete for resources (competitors - C), tolerance to environmental stresses (stress-tolerators - S), and survival in environments exposed to frequent disturbances (ruderals - R) (Grime, 1977). Knowing that many plant species are plastic and can respond to environmental variations, Grime (2001) suggests that according to CSR theory groups, plant species have sets of common traits that confer similar responses to stresses and disturbances.

Species that can exhibit variations in their functional traits in response to environmental variations tend to have greater chances of survival in the face of anthropogenic and climatic changes (Mclean et al., 2014; Anderson & Gezon, 2015; Xie et al., 2015). Thus, plants could invest differently in their leaf structures as a result of environmental variations (Silva et al. 2019; Rebelo et al., 2024). This intraspecific variation can contribute to the stability of various species in areas where environmental filters are significant (Maracahipes et al., 2018). Moreover, plasticity can represent a strategy for tolerating resource limitations in the environment, influencing the survival and competitive ability of individuals and, therefore, their ecological strategies (Silva et al., 2019). In light of this, we evaluated a set of morphological and integrative leaf traits of two species, one being a liana and the other a palm tree in the seedling stage. We selected the seedling stage because, at this stage of development, plants are highly fragile and subject to structural variations related to environmental changes (James et al., 2011). We chose these species because the majority of studies are focused on trees and these two life forms show greater abundance and diversity in tropical forests, mainly in areas with high levels of disturbance and more exposition to sunlight, such as in forest fragments (Salm et al., 2011). The study was conducted in areas with low fertility due to its natural condition (Matos et al., 2023) and subject to anthropogenic actions, such as the proximity to areas with mining activities (bauxite refining and industrial activities) and urbanization, as well as in areas with less influence of these activities and with greater vegetative cover in Eastern Amazon at Barcarena, Pará State, Brazil (Cunha et al., 2022). These changes in land use have resulted in a highly fragmented landscape (Carmo & Costa, 2019; Cunha et al., 2022).

Therefore, we tested if the functional traits and CSR ecological strategies of the species Bactris hirta Mart. (Arecaceae) and Tetracera sp. (Dilleniaceae) vary between two sampling periods in response to the availability of water and soil nutrients, as well as landscape impacts. To do this, we formulated the following questions: i) How do functional traits vary in each species in relation to variation in water availability? We expect species adjustments in response to water availability, in which the species exhibit more conservative strategies during periods of lower water availability and more acquisitive strategies during periods of higher water availability; ii) What are the ecological CSR strategies shown by each seedling species in these fragments? Do CSR strategies change seasonally? We expect that seedlings in both species show a higher proportion of stress-tolerance strategy (S%) due to light limitation and variation in water availability and that the percentage of S% strategy is higher in periods of low water availability; and iii) What are the relationships between landscape components and soil characteristics on the variation in the functional traits for each species? We expect that variation in soil fertility influences the allocation to morphological and integrative leaf traits, with leaves exhibiting higher LDMC and SLA in soils with lower fertility and a more negative water potential at leaf turgor loss point (Ψ_TLP) in soils with higher sand content due to low water retention.

Material and methods

Area of study and sampled species

The study was carried out in 13 fragments of riparian vegetation in the Conde and Cabanos district, in the municipality of Barcarena, Pará, Brazil (Fig. 1 A-B ). The region's climate is classified as tropical rain, type "Af" according to the Köppen classification (Alvares et al., 2013), the months with high rainfall vary from December to May and the months with lower precipitation vary from June to November (Fig. 2), the year average temperature is 26.9 °C (Piratoba et al., 2017). The vegetation type is Dense Ombrophilous Forest, with the presence of floodplain forest bordered by the Pará and Acará rivers (Souza & Lisboa, 2005).

Figure 1.
Sampling points for collecting functional traits in the municipality of Barcarena, Pará, Brazil. (A) Landsat 8 image with RGB composition (Bands 6, 5, and 4) and (B) Land use and cover classification based on MapBiomas.

Figure 2.
Monthly rainfall over two years of functional data collection at Barcarena, Pará State, Brazil.

The data were collected in three different field campaigns that varied in precipitation (Fig. 2): November 2018, representing the end of the dry season, which represented a month with low water availability during our study, March 2019, representing the peak of the wet season, and May 2019, also in the wet season. From here, we will call November as a month with low water availability, March, and May with high water availability, in the wet season.

The leaf traits were collected in November 2018 and May 2019, while the integrative leaf traits were collected in March 2019 and May 2019. Seedlings of two species were selected for the study: a palm, Bactris hirta Mart. (Arecaceae), and liana, belonging to the genus Tetracera sp. (Dilleniaceae). The species were deposited in the herbarium HF, Herbário Profa. Normélia Vasconcelos (acronym according to Thiers, 2024 continuously updated), under the following vouchers: Bactris hirta (6683) and Tetracera sp (6684). The studied species belong to important functional groups (palms and lianas), which are significant in Amazonian (Flora e Funga do Brasil, 2024). These species were chosen because they were found in most of the forest fragments during preliminary visits, meeting the minimum quantity criteria (3-5 individuals per fragment). Additionally, they are easy to identify in the field in the seedling stage, which helps avoid mistakes in collecting individuals.

Traits measurements

In each forest fragment, three individuals per species were selected, choosing individuals with similar size, ranging from 35 to 40 cm in height. Due to limitations in the number of individuals available, the seasonal data collection, and the focus on seedlings rather than adults, we adapted our sampling approach from the protocol developed by Pérez-Hanguindeguy et al. (2013). Thus, from the three individuals/species, five leaves were collected per individual, three for leaf trait measurements and two for integrative leaf traits assessments. For most individuals, this number of leaves corresponds to all the leaves present on the plant, accurately representing each species at this developmental stage. The data were collected from 13 fragments, so if the differences between periods of water availability are marked, the results regarding the species' responses should be reliable.

The leaves were labeled in the field and packed in dark plastic bags to minimize dehydration. In the laboratory the following traits were measured: 1) morphological-specific leaf area (SLA) and leaf dry matter content (LDMC); 2) integrative traits - water potential at turgor loss point (Ψ_TLP) and osmotic potential at maximum turgor (ΨsFT). In the laboratory, the leaves were placed in a container filled with water for 4 h to rehydrate. After rehydration, the leaves were photographed with a digital camera, and the images were analyzed using the ImageJ software (Abrámoff et al., 2004) to determine leaf area. The leaves were weighed on a precision analytical balance (0.001g) to measure the saturated fresh mass, then placed in an oven at 65ºC for 72 h to determine the dry mass. The specific leaf area (SLA) (mm² g^-1) was calculated based on the ratio between leaf area and leaf dry mass; leaf dry matter content (LDMC) (g g^-1) was measured by dividing the leaf dry mass by its saturated fresh mass.

The integrative leaf traits were analyzed using the pressure-volume curve (P-V curves). The curves were constructed from two leaves/individual of each species. In the laboratory, the petioles of the leaves were cut under water to avoid cavitation in the vessels and placed in beakers of water for 24 h to hydrate them. For the measurements, the leaves were weighed on a precision scale to determine the saturated leaf mass; they were then placed in a Scholander chamber to measure the corresponding water potential (MPa) (Bartlett et al., 2012). The leaves were left on the bench to dehydrate, and the same procedure was repeated until the leaf mass stopped oscillating. At the end of the process, the leaves were placed in an oven at 65ºC for 72 h and weighed on a digital scale to determine the relative water content. The water potential at the turgor loss point (Ψ_TLP) and osmotic potential at maximum turgor (ΨsFT) were calculated from the curves.

Ecological strategies (CSR)

The relative proportions of CSR strategies were calculated for each species in each collection campaign using the values of leaf area (LA), specific leaf area (SLA), and leaf dry matter content (LDMC) using the StrateFy tool (Pierce et al., 2017).

Physico-chemical soil variables

Soil properties were assessed in each fragment by taking five soil samples at a depth of 0-10 cm. The following soil characteristics were measured: phosphorus (P), potassium (K), total nitrogen (N), pH, calcium (Ca), aluminum (Al), organic matter (OM), sum of bases (BS), potential acidity (H+Al), total sand, silt, and clay. The analyses were carried out by the laboratory LABRAS, located in Monte Carmelo, Minas Gerais, Brazil. The methods used by the laboratory are following the protocol established by Silva (2009).

Landscape analysis

The landscape variables in the 13 fragments sampled were based on land use and land cover categories obtained from the MapBiomas platform for the two years of the study (2018 and 2019) (Fig 1 B ). Satellite images from the Planet constellation with a spatial resolution of 4.7 m in true image composition (RGB) were also used to delimit the fragments. Using ArcMap 10.2 software, an extension of the ArcGIS software package, the land use and land cover rasters were converted into vectors and attached to each fragment polygon. Finally, the percentage area of each land use class was estimated. The land use and land cover categories identified in this study were: urban area; wetland; floodable forest; grassland; forest formation; mining; pasture; river and lake.

Data analysis

To answer the first question, how the functional traits (SLA, LDMC, Ψ_TLP, and ΨsFT) vary between Bactris hirta and Tetracera sp. in relation to variation in water availability (May, wet season and November, dry season), the Student's t-test was used with separate variance when the data set met the assumptions of normality and homoscedasticity, and the Mann-Whitney (U) test when the assumptions were not met.

To answer question two, i.e. what ecological CSR strategies are used by Bactris hirta and Tetracera sp. in Amazonian Forest fragments in wet and dry season (May and November, respectively), the StrateFy tool proposed by Pierce et al. (2017) were used. To check whether there was a difference between the proportions of C, S, and R between periods with high and low water availability, we used Student's t-test with separate variances when the data set met the assumptions of normality and homoscedasticity, and the Mann-Whitney (U) test when the assumptions were not met.

To answer question three about the relationships between landscape components and soil characteristics on the variation in the functional traits (SLA, LDMC, ΨTLP, and ΨsFT), the predictor variables (landscape and soil) were selected through a Pearson correlation matrix to avoid multicollinearity (Figure S1). The selected variables were: forest formation, pH, P, H+Al, OM, BS, and total sand. After selecting these variables, generalized linear models (GLMs) were fitted using the lme4 package (Bates et al., 2022). The models were executed as follows: four global models were run, one for each functional trait (SLA, LDMC, Ψ_TLP, and ΨsFT). Next, we selected the best model for each functional trait using the stepwise selection method (forward selection) through the stepAIC function from the MASS package (Venables & Ripley 2002). To better visualize the relationships of the final models, the significant estimates of each model were plotted using the ggplot2 package (Wickham, 2016). Assumptions of residual normality and homoscedasticity were assessed using the Shapiro-Wilk and Levene tests, respectively.

All statistical and graphical analyses were carried out using the R software, with a significance level of 0.05 (R Core Team, 2023).

Results

Variation in leaf traits and CSR strategies due to variations in water availability

Both species differed in LDMC between periods of low and high precipitation (Bactris hirta: T=2.784, DF= 9.502, p=0.020; Tetracera sp.: W=56, p=0.008), in which the LDMC was higher in the period with low water availability (November 2018) (Fig. 3 A-B ). There were no differences in SLA between periods of low and high precipitation for both species; Bactris hirta (SLA: T=-1.327, DF= 10.982, p=0.211) (Figure S2-C) and Tetracera sp. (SLA: T=-1.673, DF= 13.415, p=0.117) (Figure S3-C).

Figure 3.
Student's t-test and Mann-Whitney test (U) for the LDMC morphological trait in the species studied. Bactris hirta (A), Tetracera sp. (B). Different letters (a, b) indicate statistically significant differences between the months.

The Ψ_TLP and ΨsFT were analyzed in two months during the wet season, with high water availability. As we expected, the values of these traits were similar between these two months for both species, Bactris hirta (Ψ_TLP: W=12, p=0.394; ΨsFT: W=22, p=0.589) (Figure S2-AB) and Tetracera sp. (Ψ_TLP: W=25, p=0.321; ΨsFT: W=43, p=0.541) (Figure S3-AB).

Both species showed a higher proportion of stress tolerance strategy (S) regardless of the precipitation. However, they also exhibited an S/CS and CS strategy, indicating a combination of stress-tolerant and competitive traits (Fig. 4 and Table S1).

Figure 4.
Relative proportion of CSR strategies - competition (C%), stress tolerance (S%), and ruderalism (R%) for two seedlings species from forest fragments in the Eastern Amazon.

Comparing the periods of variation in water availability, Bactris hirta showed a significant difference between the low and high precipitation periods, especially in competition and stress tolerance strategies. During the low precipitation period (November), individuals showed a higher proportion of competition strategy compared to individuals in the period with higher water availability (C%: T=4.187, DF=31.078, p<0.001) (Fig. 5 A ). On the other hand, the proportion of stress tolerance was higher during high precipitation (S%: T=-3.806, DF=30.342, p<0.001) (Fig. 5 B ). No significant differences were observed in the proportion of ruderalism between the periods (R%: W=105, p=0.154) (Fig. 5 C ). For Tetracera sp, significant differences were also identified between the periods with variation in water availability for the three ecological strategies (C%: T=-3.806, DF=30.342, p<0.001; S%: T=-2.685, DF=39.836, p=0.012; R%: T=-4.621, DF=38.283, p<0.001) (Fig. 5 D -F). The proportion of competition strategy was higher during the low precipitation period, while the proportions of ruderalism and stress tolerance were higher in the period with higher precipitation.

Figure 5.
Student's t-test and Mann-Whitney test (U) for the relative proportions of the CSR strategies - competition (C%), stress tolerance (S%), and ruderalism (R%), of the two seedlings species in forest fragments in the eastern Amazon. Bactris hirta (A, B and C), Tetracera sp. (D, E and F). Different letters (a, b) indicate statistically significant differences between the months.

Edaphic variables and landscape metrics influence the species' functional traits

For the species Bactris hirta, the best model to explain the variation in LDMC included the variables forest formation and total sand. The forest formation variable had a significant and negative effect (p=0.028), while the total sand had a significant and positive effect (p=0.017). The best model to explain the variation of SLA included the variables sum of bases (BS) and H+Al, however, these variables did not have a significant effect on this trait (BS: p=0.098; H+Al: p=0.087) (Fig. 6 and Table S2).

Figure 6.
Generalized linear models (GLMs) of the relationships between landscape components and soil characteristics in the variation of morphological functional traits for two species in the seedling stage in forest fragments in the Eastern Amazon.

For Tetracera sp., the best model to explain the variation of LDMC included the variables total sand, P, and forest formation. Only the variable P had a significant negative effect (p=0.045); the others were not significant (total sand: p=0.123; Forest formation: p=0.105). For SLA, the best model to explain the variation included the variables: total sand, BS, pH, P, OM, and H+Al. The BS variable had a positive and significant effect (p=0.023) and pH had a significant negative effect (p=0.039). The other variables were not significant (Total sand: p=0.059; P: p=0.183; OM: p=0.145; H+Al: p=0.165) (Fig. 6 and Table S2).

For Bactris hirta, the best model to explain the variation of osmotic potential at full turgor (ΨsFT) included the variables total sand, BS, pH, P, H+Al, and forest formation. The total sand variable had a significant and positive effect (p=0.049), and the forest formation had a significant and negative effect (p=0.042), while the other variables were not significant (BS: p=0.076; Ph: p=0.168; P: p=0.144; H+Al: p=0.123). The best model to explain the variation of water potential at the turgor loss point (Ψ_TLP) included the variables BS, P, and OM. The variables BS and P had significant and positive effects (BS: p=0.003; P: p=0.002). The OM variable did not have a significant effect on this trait (p=0.094) (Fig. 7 and Table S2).

Figure 7.
Generalized linear models (GLMs) of the relationships between landscape components and soil characteristics in the variation of integrative leaf traits for two species in the seedling stage in forest fragments in the Eastern Amazon.

For Tetracera sp., the best model to explain the variation of osmotic potential at full turgor (ΨsFT) included the variables total sand and H+Al. Both variables had significant and negative effects (total sand: p=0.022; H+Al: p=0.029). The best model to explain the variation of water potential at the turgor loss point (Ψ_TLP) included the variables total sand, BS, and H+Al. Both variables also had significant and negative effects (BS: p=0.004; H+Al: p=0.006) (Fig. 7 and Table S2).

Discussion

Our results show clear evidence of intraspecific trait variation for liana and palm seedlings under variation in water availability. The variation in leaf traits reflects changes in the species' CSR ecological strategies, contributing to the ability of both species to successfully occupy the forest fragments in the Eastern Amazon. The landscape and soil characteristics influenced resource allocation patterns and drought-related traits of both species. However, each species showed a relationship with different variables, reinforcing that different life forms respond differently to soil fertility and physical traits according to their biology, adopting strategies to maximize the uptake and use of resources.

Intraspecific variation in traits and CSR ecological strategies

Species exhibited variation in some traits between periods of difference in water availability, that reflected in the species' ecological strategies. The morphological traits were collected in periods with marked differences in precipitation (Fig. 2), and both species showed higher LDMC for the leaves collected during periods of lower precipitation, indicating a higher investment in carbon to build their leaves during the months that comprise the dry season. On small spatial scales, Jung et al. (2014) observed intraspecific shifts in LDMC due to variation in microclimatic conditions. Changes in carbon investments to build the leaves reflect a shift in plant strategies to conserve and use available resources, in which leaves built during low precipitation tend to present more conservative traits (Wright et al., 2017). Higher LDMC in plants indicates the presence of litter intercellular space and high mesophyll resistance to gas diffusion that may decrease leaf transpiration (Bussotti & Pollastrini, 2015), limiting water losses during periods with low water availability. The SLA was similar between periods of low and high precipitation, even with the changes in LDMC. The environmental conditions can affect the plant’s SLA and LDMC in different ways, leading to a decoupling of these two traits (Anderegg et al., 2018; Messier et al., 2017). Messier et al. (2017) showed that LDMC is sensitive to variations in small-scale environmental gradients, and it is the best-suited trait to detect the plastic response to micro-environmental gradients, corroborating our results for palm and liana seedlings in tropical fragments, which showed leaves with higher LDMC in periods of low water availability, without changes in SLA.

The leaf turgor loss points and osmotic potential did not differ within the species, as the two plant collection periods did not show differences in precipitation patterns. However, the leaves in the wet season showed more negative leaf turgor loss point and osmotic potential in the palm species B. hirta (Ψ_TLP=1.72 + 0.23) than in the liana Tetracera sp. (Ψ_TLP=1.12 + 0.18). The Ψ_TLP is strongly related to plant drought tolerance and associated with species distributions along water supply gradients (Bartlett et al., 2012; 2014). It is also a predictor of seedlings survival in drought conditions (Álvarez-Cansino et al., 2022). Thus, the ΨTLP values we found for palm and liana seedlings fall within the range observed in tropical forests (Bartlett et al. 2012; 2014; Maréchaux et al., 2015). Regarding the lianas, Maréchaux et al. (2017) showed a higher plasticity in Ψ_TLP for lianas in tropical forests compared to trees, in which the Ψ_TLP adjusts under drier conditions, contributing to improved leaf drought tolerance through osmotic adjustments. Besides that, lianas show higher Ψ_TLP than trees in the wet season that is compensated by their high plasticity, adjusting their tolerance during the dry season (Maréchaux et al. 2015; 2017).The palm showed a more negative Ψ_TLP in the wet season than the liana. In a subtropical forest, the palm Euterpe edulis showed a similar Ψ_TLP to our study (-1.65 MPa) (Gatti et al., 2014). Palm trees are adapted to warm and humid tropical environments, tend to have large vessels, and show a high water demand (Aparecido et al., 2015; Brum et al., 2019). Thus, they are considered drought-vulnerable and have declined in abundance in many long-term Amazon Forest plots (Esquivel-Muelbert et al., 2019). However, in Amazon forests with shallow water tables, palms are considered resistant to drought, and the belowground hydrological environment can buffer the climatological water deficit (Sousa et al., 2020). In the leaf level, Carr (2011) showed that in moisture stress, the leaves did not show signs of wilting due to the high fibrous tissue, thick hypodermis, and well-developed cuticle characteristic of palm tree leaves. Thus, the sensibility of palms to drought is still controversial and can be variable among species and environments. The Ψ_TLP that we observed for the palm is like the average for trees in tropical forests (Bartlett et al., 2012). However, we still do not know about the plasticity in Ψ_TLP and osmotic potential traits that may contribute to species resistance to drought.

The prevalent strategy exhibited by the two species in the seedling stage was stress tolerance. The stress-tolerators survive in resource-poor or abiotically variable environments investing their biomass in persistent tissues and mechanisms favoring resource conservation (Grime, 2001; Pierce et al., 2017; Dayrell et al., 2018). The understory environmental conditions present in the forest fragments, with low light incidence, may have acted as an important environmental filter, resulting in the predominance of the stress tolerance strategy for both species. Furthermore, water availability contributes to intraspecific variation in the percentage of each strategy between the wet and dry seasons in both species. The percentage of C was higher during periods of low water availability, while S was higher during the wet period. Thus, the intraspecific changes in C, S, and R strategies reinforce the role of environmental filters and the variation in conditions, reflecting in the plants' ecological strategies related to their growth, and this can change with plant development and ontogeny (May et al., 2017; Dayrell et al., 2018; Wen et al., 2023).

The response of different life forms may be very different to seasonality and global climate change according to their biology and ecological strategies (Sousa et al., 2020). The ability of the two studied species to change their traits in the seedling stage can be an important strategy to increase the survival rates of lianas and palms in variable ecosystems. Lianas are shown to increase in abundance in perturbed areas and seasonal and dry ecosystems (Phillips et al., 2002; de Azevedo Amorim et al., 2018). For palms, global change also has the potential to alter their distributions and individual physiological functioning, but probably they will continue to be an important element in tropical ecosystems (Renninger & Phillips, 2016).

Soil and landscape variables influence the traits in palm and liana

The landscape and soil characteristics influenced resource allocation patterns and drought-related traits of the species, yet the species differed in the relationships among the variables. Forest formation and total sand directly influenced the morphological and integrative traits of the palm species Bactris hirta. Forest formation is directly linked to canopy cover, which represents the upper stratum (dossel) of a forest. The species showed a negative relationship with forest formation and a positive relationship with total sand, indicating that lower canopy cover, increased exposure to direct sunlight, and reduced soil water retention led to higher LDMC and a more negative osmotic potential (ΨsFT), indicating a more conservative strategy in resource use. Areas with lower canopy cover and drier soils may experience higher evapotranspiration. Thus, these plants tend to maintain more negative potentials and resistance to water deficits in their tissues (Bartlett et al., 2012; 2014).

Base sum (BS) and phosphorus (P) were the best predictors of Ψ_TLP for palm Bactris hirta. A more negative Ψ_TLP occurs in species more affiliated with drought (Bartlett et al., 2012; Lenz et al., 2006; Májeková et al., 2016; Kram et al., 2022). To our knowledge, this is the first study showing a correlation between plant species' Ψ_TLP and soil nutrient availability. However, Oliveira et al. (2018) showed a positive correlation between the water potential at which the plant loses 50% of hydraulic conductivity (P50) with soil P concentration, indicating a relationship between drought tolerance and soil P availability, suggesting the evolution of a stress tolerance syndrome to both, nutritional and hydraulic limitation. Thus, our result with Ψ_TLP agrees with the observed pattern in Oliveira et al. (2018).

Phosphorus was shown to be the best predictor for LDMC in the liana Tetracera sp., correlating negatively. Phosphorus is an essential nutrient for plants, involved in many metabolic functions such as photosynthesis and cellular respiration (Rao & Terry, 1989; Crous et al., 2017). Under conditions of soil with low P availability, plants generally invest more in the production of cellular structures, with long-lived and dense leaves (Wright & Westoby, 2004). Therefore, the negative correlation between soil P content and LDMC of the species reflects the plants' ability to adjust their morphology and resource allocation in response to environmental conditions. Specific leaf area (SLA) was related to base sum and pH. The species showed a positive relationship with base sum and a negative relationship with pH, suggesting that nutrient-rich soils and lower pH promote more acquisitive strategies, with high SLA.

Total sand and H+Al were the best predictors of osmotic potential (ΨsFT) for the liana species, correlating negatively. Likewise, base sum and H+Al were the best predictors of Ψ_TLP, correlating negatively. H+Al refers to the concentration of hydrogen and aluminum ions in the soil, which are important indicators of soil acidity, a specific problem in tropical regions characterized by high weathering rates and decomposability rates (Quesada et al., 2011 b ). In the study region, the soil shows a high acidity, and the organic matter is classified as low (Matos et al., 2023). Acidity directly impacts soil nutrient availability (Taiz et al., 2017), as reflected in the base sum. In the continuous weathering process, where clay and essential nutrients are leached over time, soils have a predominantly sandy composition (Lambers et al., 2008). This negative correlation between integrative traits (ΨsFT and Ψ_TLP) and soil variables aligns with the results observed in the palm species Bactris hirta, highlighting the role of soil acidity in nutrient availability and consequently in the hydraulic parameters of these species.

In conclusion, the two studied species showed intraspecific trait variation in the seedlings stage, wherein leaves collected during periods of low water availability had a higher leaf dry mass content, indicating changes in patterns of resource allocation and the CSR ecological strategies. Despite variations among periods in the proportion of each CSR component, both species predominantly exhibited a stress-tolerance strategy. The forest formation and soil variables related to fertility and water retention (e.g., sand) influenced resource allocation patterns for leaf construction and drought-related traits (Ψ_TLP) in both species. Thus, the ability of both species, belonging to different functional groups, to respond with plasticity during the seedling and juvenile stages may be an important mechanism, likely contributing to the abundance and prevalence of palms and lianas in forest fragments in the Eastern Amazon.

Acknowledgements

We are thankful to Hydro Alunorte for the project financial support “Avaliação de Biota Aquática e Vegetação ciliar da hidrografia que influencia a bacia do Murucupi e arredores da Hydro Alunorte” and to scholarship to JP, RDP and TSS. Our gratitude also goes to Dr. Leandro Juen, the project general coordinator. Many thanks to Ana Carolina Enríquez Espinosa, Josiney Araújo, Luane G. Botelho Rebelo, and Raimundo Luis Souza for their invaluable help with fieldwork and elemental analyses. We also thank Roberta Cerqueira Macedo, the curator of the Herbarium HF, for her support in the deposition of the exsiccates. JP, VN-R, and RDP were supported by a scholarship from Coordenação de Aperfeiçoamento de Pessoal de Nıvel Superior (CAPES/Brazil - financial code 001) and CNPq. GST (Process 304591/2022-0) and TSM (Process 311835/2023-6) acknowledge CNPq for a productivity scholarship and the L’OREAL-UNESCO-ABC “Para Mulheres na Ciência/For Women in Science” grant.

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Supplementary Material

The following online material is available for this article:

Table S1.

Relative proportion of CSR strategies - competition (C%), stress tolerance (S%) and ruderalism (R%), for two species from forest fragments in the Eastern Amazon.

Table S2.

Linear fit of the best model according to the AIC criterion for the two species between functional traits and soil and landscape variables of forest fragments in the Eastern Amazon.

Figure S1.

Pearson's correlation matrix (p<0.05) between soil and landscape characteristics of forest fragments in the Eastern Amazon. Squares with "X" indicate non-significant correlations.

Figure S2.

Student's t-test and Mann-Whitney (U) test for the morphological traits and physiological/integrative characteristics for the palm species Bactris hirta. Water potential at the turgor loss point (Ψ_TLP) (A); Osmotic potential at maximum turgor (ΨsFT) (B); Specific leaf area (SLA) (C). Different letters (a, b) indicate statistically significant differences between the months.

Figure S3.

Student's t-test and Mann-Whitney (U) test for the morphological traits and physiological/integrative characteristics for the liana species Tetracera sp. Water potential at the turgor loss point (Ψ_TLP) (A); Osmotic potential at maximum turgor (ΨsFT) (B); Specific leaf area (SLA) (C). Different letters (a, b) indicate statistically significant differences between the months.

Edited by

• Editor Chef:
  Thais Almeida

• Associate Editor:
  Ana Silva Moreira

Publication Dates

• Publication in this collection
  30 May 2025
• Date of issue
  2025

History

• Received
  22 May 2024
• Accepted
  11 Dec 2024