Leaf traits of Cerrado trees vary according to season of leaf production

doi:10.21203/rs.3.rs-1551173/v1

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Leaf traits of Cerrado trees vary according to season of leaf production

https://doi.org/10.21203/rs.3.rs-1551173/v1

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A large number of studies on plant functional traits assume time-invariant species-level mean trait values. Studies examining how leaf functional traits vary according to the season in which leaves were produced are very rare. In this study, we selected four species of trees and evaluated how morphological traits, and mesophyll and stomatal dimensions of leaves produced in the dry season differed from those produced in the wet season in a highly seasonal woodland savanna (cerradão) in the Amazonia-Cerrado transition. We found substantial differences in leaf traits between cohorts of leaves produced in both seasons, with those produced during the wet season characterized by more acquisitive trait values (e.g., high stomatal density, large stomatal pore size and high specific leaf area) than leaves of the same species produced in the dry season which were characterized by water conservative leaf traits. The magnitude of the difference for selected traits was remarkable – e.g., stomatal density of leaves produced in the dry season was on average four times greater than those produced in the wet season. Our results cast strong doubts on the use of mean specific values for syntheses of leaf traits and demonstrate that species in the Amazonia-Cerrado transition exhibit very high intraseasonal variation. Whether this high level of plasticity observed seasonally also applies to response to future climate change remains an open question.

Leaf traits

Ecological strategies

Intraseasonal variation

Leaf economic spectrum

Seasonal drought

Functional traits are morpho-physio-phenological characteristics that directly or indirectly affect plant performance through their effects on growth, survival, and reproduction (Violle et al. 2007). These functional traits are also responsible for the demographic rates, environmental preferences and competitive capacity of plants (Wright et al. 2010; Aiba et al. 2020; Delhaye et al. 2020). Thus, understanding how functional traits vary between species and to what extent this variation can be considered adaptive is a central objective of plant functional ecology (Wright et al. 2004).

In recent years, there has been substantial interest in exploring patterns of plant functional trait covariation between species with climate, soils and nutrients on global scales (Ordoñez et al. 2009; Díaz et al. 2016) for predicting forest ecosystems responses to future climate change. Trait data revealed the existence of an “Leaf Economics Spectrum”, a strong covariation between maximum leaf photosynthesis and dark respiration rates with leaf nitrogen and phosphorus, and a trade-off between leaf longevity and maximum leaf photosynthesis rate (Wright et al. 2004). The spectrum has become an essential concept in the functional ecology of plants, where species are ordered in a continuum of acquisitive and conservative strategies (Wright et al. 2004; Reich 2014). However, most large-scale synthesis trait analyses (e.g., Díaz et al. 2016) use a single trait value per species, and do not incorporate intraspecific trait variation which could be the result of spatial variation in growth conditions like e.g., resource availability, or temporal variation, depending on the season or year of leaf production. Thus, these studies assume that intraspecific variation in traits has much less influence than differences between species. Although this assumption is sometimes appropriate, recent research suggests that intraspecific variation may be substantial (Hulshof and Swenson 2010; Violle et al. 2012; Bello et al. 2011), and may be especially significant at the local scale (Albert et al. 2010). Studies examining temporal variation in leaf functional traits are especially rare, given the substantial challenge of monitoring leaves over time. An understanding of the temporal patterns of these traits is also important for predicting the seasonality of carbon and water fluxes and thus contribute to our understanding of the functioning of terrestrial ecosystems (Schimel et al. 2015; Yang et al. 2016).

Many studies have shown that microclimate, differential light conditions, edaphic characteristics, and phenology trigger differences in leaf traits (Mckown et al. 2013; Wu et al. 2017; Delhaye et al. 2020; Araújo et al. 2021b). In this context, the variation in soil water availability may be particularly important, as it plays an important role in the distribution of species and can affect the structure and dynamics of forests (Engelbrecht et al. 2007; Phillips et al. 2009; Da Costa et al. 2010). Precipitation variability affects the ecological strategies of plants (Rossatto and Kolb 2009). For example, a study using perennials in Australia found that specific leaf area and leaf thickness decrease as precipitation decreases (Cunningham et al. 1999). On the other hand, stomatal density increases as the climate becomes drier and warmer for a South African genus (Carlson et al. 2016). Precipitation seasonality is a particulary important control on vegetation function in the Amazonia-Cerrado transition (Marimon et al. 2014), which is subject to a long dry season (approximately six months). Although it is well known that seasonality causes changes in phenology and productivity, the relation between seasonality on leaf traits have not yet been studied, except for a single study for an evergreen neotropical savanna tree (Rossatto and Kolb 2009). Plants can reduce leaf area to increase water transport efficiency (Scholz et al. 2008) or invest in higher stomatal density and smaller stomata to increase their water use efficiency (Pearce et al. 2006; Galmés et al. 2007) in the dry season. On the other hand, during the rainy season, plants can invest in greater petiole length and specific leaf area that help in greater light interception and capture, while larger stomata permit larger carbon flux to the carboxylation site in the chloroplast and thus promote higher carbon capture and growth (Takenaka 1994; Westoby 1998; Beaulieu et al. 2008; Rossatto et al. 2009).

In this study, we evaluate whether and how leaves of four important woodland savanna (cerradão) tree species in the Amazonia-Cerrado transition exhibit different leaf trait values depending on whether they were produced in the dry season or wet season. In this region, plants may already be close important physiological thermal thresholds and may therefore be vulnerable to climate change (Tiwari et al. 2020; Araújo et al. 2021a). The ability to adjust leaf characteristics from one season to the next may confer an advantage and help to ensure the survival of these species under future climate change (Via 1993). In this context, we address the following questions: 1) Do traits of leaves in woodland savanna (cerradão) in the Amazonia-Cerrado transition formed during wet versus dry season differ? We hypothesise that acquisitive traits like greater specific leaf area, greater petiole length, higher stomata number density and higher maximum stomatal pore opening will be larger for leaves formed during the wet season, while conservative trait values like smaller stomata, thicker cuticular and adaxial epidermis, and higher trichome density will be more strongly expressed in leaves formed during the dry season; 2) How important are seasonality and taxonomic identity as controls of variation in leaf traits? We hypothesise that seasonality (dry and wet season) is more important to explain most of the variability of traits in this savanna system than taxonomic differences (species).

Study area and selected species

We carried out the study at Bacaba Municipal Park (14°41'09” S and 52°20'09” W), a conservation unit of approximately 500 ha, in Nova Xavantina, Mato Grosso state, Brazil (Fig. 1). Bacaba Municipal Park is located in the most extensive and diverse vegetation transition zone in South America, between the Amazonia and Cerrado biomes. It is an area of ecological tension composed of a mosaic of savanna and forest formations (Ratter et al. 1973; Marimon et al. 2006, 2014; Marques et al. 2020), whose maintenance is important for biodiversity conservation (Morandi et al. 2016). The region's climate has a marked seasonality with two well-defined periods, one rainy (October to March) and the other very dry (April to September), being Aw type, according to Köppen’s classification (Alvares et al. 2013). Annual average precipitation is 1.500 mm and average annual temperature 25°C (Marimon et al. 2010).

We carried out the study in a woodland savanna (cerradão), with trees up to 15 m height, a dense litter layer and a deep, acidic, alic and dystrophic soil (Marimon-Junior and Haridasan 2005; Reis et al. 2015). It has a continuous canopy, with tree cover ranging from 50 to 90%, and the microclimate is characterized by higher air humidity and lower temperature and solar radiation compared to nearby savanna environments (Araújo et al. 2021b). We selected four evergreen tree species positioned among those with the highest importance value index, which considers the highest relative density, frequency and dominance in the studied vegetation (Reis et al. 2015): Qualea parviflora Mart. (Vochysiaceae), Pseudobombax longiflorum (Mart.) A. Robyns (Malvaceae), Hymenaea stigonocarpa Mart. ex Hayne and Vatairea macrocarpa (Benth.) Ducke, both Fabaceae. These species have a wide geographic distribution and occur locally in a range of vegetation types (open savanna, woody savanna, and closed-canopy forests) (Ratter et al. 2006).

Data collection

To assess the effect of dry versus wet season leaf formation on leaf traits, we sampled five individuals per species. For each individual we selected three terminal branches completely exposed to the sun, and collected all the leaves present at the end of the dry season (10-Sep-2019). In 10-Feb-2020, during the peak of the rainy reason, we returned to the same branches and collected again all the leaves. For all individuals, we selected leaves fully expanded from the edge of the tree crown at an average height of 12.45 ± 2.62 m and with a diameter at breast height > 10 cm in individuals located near the edge of the studied area and in the centre, in natural gaps. We analysed 11 anatomical and morphological leaf traits (Table S1).

For determining morphological traits, we randomly selected 25 leaves for each species (five leaves per individual) that were: 1) fully expanded, 2) in full sun and 3) free from damages such as caused by pathogens and/or herbivores. At the peak of the dry and rainy seasons, we determined the wet weight of the leaves with a precision balance (± 0.001 g), then placed them in paper bags in an oven at 60°C, and after 72 h determined the dry weight. The specific leaf area was calculated as the ratio between leaf area (determined using the ImageJ software) and leaf dry mass. We measured leaf thickness using an electronic digital micrometre (± 0.001 mm) and petiole length using a digital caliper (± 0.001 mm), following the protocol proposed by Pérez-Harguindeguy et al. (2016).

For the anatomical traits, we selected 15 leaves per species (three leaves per individual) and employed the method of leaf surface impression with condensing silicone of high moulding technology (Speedex), as proposed by Weyers and Johansen (1985) to measure stomatal density and size. Later, we used colourless enamel to make the impression of the mould on slides for examination under an optical microscope (Zeiss Primo Star), with an attached camera, to visualize the stomata and trichomes. We recorded stomatal measurements under 100x microscopic magnification and selected 10 fields randomly per leaf; then we processed the images with the ImageJ software (Abràmoff et al. 2004).

For each individual, we calculated the stomatal density as the average of the number of stomata counted in the same fields of view previously recorded, and subsequently estimated the average stomatal densities, lengths and widths per species, measuring 25 stomatal complexes per individual. We measured the guard cell length (“L” in µm), the guard cell pair width (“W” in µm), the stomatal size (“S”, estimated as S = L*W, according to Franks et al. (2009, 2012) and the maximum area of the stomatal pore (“AMAX”, in µm²). We calculated the maximum area of the stomatal pore as AMAX = α*S, where α = 0.12 (Franks and Beerling 2009) and measured the trichomes density (when present) as the average of the number of trichomes counted in the same fields of view recorded previously and then estimate the densities.

For the leaf structure traits, we took a sample of 2 x 2 cm² from the median portion of the leaf blade and used a free-hand cross-section. We fixed the leaf fragment in a half-open petiole of Cecropia sp. and cut with the free hand and a razor blade. Afterwards, we stored the samples in Petri dishes and added 3 ml of sodium hypochlorite, until the samples became translucent. We rinsed three times with distilled water and stained the samples with a proportion of 50% methylene blue and 50% safranin. We photographed the slides with a camera coupled to an optical microscope, we randomly selected 10 fields of each leaf with a magnification objective of 100x to assess the thickness of the adaxial cuticle, adaxial epidermis and palisade and spongy parenchyma (Roeser 1962).

Statistical analysis

We performed all analyzes using the R software version 4.0.4 (R Core Team 2021), checked normality and homogeneity of variance using Shapiro-Wilk and Levene tests, respectively (Levene 1961; Shapiro-Wilk 1965), and when necessary, we log10-transformed variables for normality assumptions. To test our hypotheses, we compared the leaf traits of the species between the rainy and dry seasons, using a two-way ANOVA (with species and seasonality as predictors). Subsequently, we adopted Tukey's post-hoc tests to test the differences in leaf traits of each species between seasonal variation in precipitation, with individuals as our statistical unit. We also performed a principal component analysis (correlation PCA) to further explore leaf trait associations in both seasons.

To assess the variability in our trait data, we computed the coefficient of variation (CV) for each functional trait, within each species and between the dry and rainy seasons, (Albert et al. 2010; Zhang and Yu 2018). To further understand the importance of taxonomic vs. seasonal controls on trait variation, we constructed multilevel linear mixed models for each functional trait measured with seasonality and species as nested random factors, following the approach used in Rosas et al. (2019).

Dry versus wet season leaf traits

Seasonal patterns within species revealed that leaves produced in the rainy season generally show more acquisitive traits than those produced in the dry season, which are more conservative in nature. For the leaf morphological traits, all species showed higher values of specific leaf area in the rainy season compared to the dry season, and only Hymenaea stigonocarpa had higher petiole length values in the rainy season (Fig. 2).

Leaf mesophyll traits exhibited less clear-cut seasonal variation than specific leaf area. For example, Pseudobombax longiflorum leaves produced in the dry season had markedly lower palisade parenchyma thickness than those produced in the wet season, but this was not true for other species (Fig. 2). In the dry season, Qualea parviflora produced leaves with thicker adaxial cuticle and spongy parenchyma while H. stigonocarpa produced leaves with thicker epidermis. However, for Vatairea macrocarpa none of the leaf mesophyll traits differed statistically between seasons (Fig. 2).

We recorded greater stomatal density in the dry season for H. stigonocarpa and P. longiflorum than in the wet season (Fig. 2; Fig. S1). On the other hand, leaves produced in the wet season of these same species had larger stomata and larger maximum opening of the stomatal pore in the rainy season (Fig. 2). In contrast, stomatal density and size, and maximum stomatal pore opening did not differ statistically between seasons for Q. parviflora and V. macrocarpa (Fig. 2). Furthermore, Q. parviflora, H. stigonocarpa and V. macrocarpa presented higher values of trichomes density in the dry season (Fig. 2).

In general, for all leaf traits, the coefficient of variation (CV) was widely variable both between species and between seasons (Fig. S2). In the rainy season, we recorded higher CV values for H. stigonocarpa and P. longiflorum, while in the dry season the highest values were for Q. parviflora and V. macrocarpa (Fig. S2). For all species, the anatomical and leaf mesophyll traits were the most variable between the seasons (Fig. S2). Both species and season were significant predictors of most of the leaf traits here evaluated, except for the palisade parenchyma thickness where species was a significant predictor (Table S2). The interactions between the two effects were also generally significant, except for specific leaf area (Table S2).

Acquisitive-conservative leaf traits variation

To identify major trait axes of variation and how traits of leaves formed during dry versus wet season align along these axis we performed a PCA analysis. The PCA explained 69.1% of the total variation in the first two axes (Fig. 3). The first axis (explaining 40.8% of the variance) was associated with the traits that are associated with photosynthesis and gas exchange such as specific leaf area (SLA) and stomata size (STS) (acquisitive traits), (Table S3). The second axis (explaining 28.3% of the variance) was more closely associated with traits linked to resilience under dry conditions like cuticle thickness, spongy parenchyma thickness and palisade parenchyma thickness (conservative traits), (Fig. 3, Table S3). Trait value coordinates with regards to the first two axis for leaves formed during dry versus wet season reveal a marked shift between seasons. There is nearly no overlap between traits of leaves produced in the dry season and those produced in the wet season, with the former being much more associated with acquisitive trait values (Fig. 3).

Variability of leaf morphoanatomical traits

To separate the effects of season versus species on leaf traits we perforned a variance partition analysis. The proportion of the overall variance accounted for by species vs. season varied according to the specific trait considered (Table S4). 'Species' explained a high percentage of the variance (33–93%) for leaf traits including specific leaf area, leaf thickness, petiole length and trichomes density (Fig. 4). Variables related to stomata (e.g., stomata density) and leaf mesophyll traits (e.g., cuticle thickness and epidermis thickness) were associated to a high degree with seasonality (> 60% of variance explained) (Fig. 4; Table S4).

Seasonal vs. taxonomic controls on leaf traits variation

Seasonal and intraspecific variation of traits indicate how species adapt to environmental variation (Hoffmann and Franco 2003; Laureto and Cianciaruso 2015) and establish themselves in environments with contrasting environmental filters (e.g., savanna- forest, Maracahipes et al. 2018; Araújo et al. 2021b; Jancoski et al. 2022). However, there are very few studies that investigate leaf traits in more than one season (e.g., Rossatto and Kolb 2009).

Our results show that trees in a woodland savanna in the Amazonia-Cerrado transition region produce different types of leaves in the dry versus rainy season. This suggests that the season of production is an important control for many foliar traits, including specific leaf area, leaf mesophyll characteristics and stomatal traits. For some traits, the magnitude of these differences is remarkable. For example, specific leaf area of leaves produced in the dry season was approximately half of that produced in the wet season for each species considered. Across most traits evaluated, season of leaf production explained more of the variance than taxonomic identity. This may reflect 1) a long-term adaptation to seasonality or 2) a short-term response to in situ water stress during the period of leaf production. As water availability is an important control on carbon capture, it can exert strong selective pressure on plant functional traits and modulate ecological strategies (Franco et al. 2005; Damascos et al. 2005; Souza et al. 2015).

Our results of seasonal variation in leaf traits are consistent with work along spatial environmental gradients (Olsen et al. 2013; Carlson et al. 2016; Araújo et al. 2021b) and with seasonal studies (e.g., Rossatto and Kolb 2009). For example, trichome density increases as sites become drier aiding in greater transpirational cooling capacity and stomatal size decreases, and smaller stomata can close more rapidly in response to desiccation (Franks and Beerling 2009; Franks et al. 2009).

The dominant species evaluated in this study occur in various environments (savannas and forests) and may have particularly high plasticity in relation to others that are more restricted in habitat preference. This high plasticity in leaf traits of our dominant species may be an important mechanism for allowing trees to persist within savannas and forests throughout the Amazonia-Cerrado transition potentially being a necessary condition for species persistence over time in a highly seasonal environment (Gvozdevaite et al. 2018). It may possibly also offer these species a degree of resistance to environmental changes in the Amazonia-Cerrado transition in the future (Araújo et al. 2021b). Thus it raises the question of whether species without this plasticity may be lost from these communities under future climate change (higher temperatures and possible decreases in precipitation). This study did not evaluate whether species restricted to single habitats have the same capacity for seasonal adjustment of foliar properties and future studies are required to ascertain this.

Seasonal shifts in acquisitive vs. conservative leaf trait values

We found clear differences in leaf structural attributes, leaf mesophyll characteristics and stomatal traits of woodland savanna leaves produced in the dry season and those produced in the rainy season, shifting their position along the acquisitive-conservative spectrum. The trees in our study were found to produce more acquisitive leaves (e.g., larger stomatal dimensions and higher specific leaf area) during the rainy season, allowing for higher rates of carbon assimilation and plant growth during the season where water availability is high (Wright et al. 2004; Aiba et al. 2020). On the other hand, in the dry season, our focal trees tended to produce more conservative leaves (e.g., higher trichome density, thicker epidermis and cuticle, and lower specific leaf area) that allow for better regulation of water loss and nutrient use during a period where water availability is low (Franco et al. 2005; Souza et al. 2015; Heilmeier 2019).

Our results demonstrate a very large seasonal adaptive capacity for some leaf traits (e.g., anatomical traits, Fig. S1) but not others (e.g., petiole length and trichomes density). The most plastic leaf traits included stomatal density, stomatal size and maximum stomatal pore opening, traits that are related to carbon absorption and water control and are therefore more important for species capacity to cope with seasonal drought (Franks et al. 2009). The plasticity observed in these characteristics can be driven by the imposition of additional stress as the drought progresses, resulting in a decline in gas exchange, especially under greater evaporative demands from the atmosphere, as there is a tendency to produce more conservative leaves in the dry season (e.g., Rossatto and Kolb 2009).

Implications for future work

The variability of plant functional traits over space and time allows trees to live in different environmental conditions (Neyret et al. 2016; Rosas et al. 2019; Araújo et al. 2022). However, we know little about how this variability is distributed and coordinated at different organizational levels; knowledge is even more limited in relation to seasonal leaf traits. We show that traits of leaves produced in wet versus dry season of the same individuals differ markedly, suggesting that seasonality should be considered in future ecophysiological studies. This seasonal component of intraspecific variation may be more significant than generally assumed but has been largely ignored thus far. Analyses that neglect this source of variation can generate inaccurate or biased estimates of plant leaf traits, which can significantly affect predictions and conclusions drawn from such research.

It may be that species in markedly seasonal regions such as Amazonia-Cerrado transition and the focal species in our study are outliers in their capacity for seasonal plasticitiy, given that they are found across a range of different ecosystem types (Marimon-Junior and Haridasan 2005). Describing and integrating savanna-forest dynamics and predicting their responses to environmental change from measurements of functional traits at the individual level remains a challenge (Cianciaruso et al. 2012; Neyret et al. 2016; Cássia-Silva et al. 2017; Maracahipes et al. 2018). The extent to which leaf trait plasticity affects community composition and function has been little investigated and is a key area for further study.

Our study reveals the importance of repeated sampling of plant functional traits. The number of studies to have evaluated changes in leaf traits over time is very small and more studies are needed to assess the generality of our findings. Based on our findings, we recommend that ecologists to be more cautious when making predictions based on foliar traits, especially in seasonal environments. We hope that this research will stimulate further studies aiming to include the seasonal factor and intraspecific variation to better estimate leaf traits in other biological systems, in order to improve predictive frameworks that address the potential of plant species to adapt to climate change.

Our findings demonstrate that trees in the Amazonia-Cerrado transition exhibit very high intraseasonal variation, produce leaves with more acquisitive characteristics in the rainy season and more conservative characteristics in the dry season. Whether this high level of plasticity observed seasonally also applies to response to future climate change remains an open question.

Funding: Not applicable.

Conflicts of interest/Competing interests: The authors declare that they have no conflict of interest.

Ethics approval: Not applicable.

Consent to participate: All patients included in this study gave written informed consent to participate in this research.

Consent for publication: All patients provided written informed consent to publish the data contained within this paper.

Availability of data and material: The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request.

Code availability: Not applicable.

Acknowledgements: We thank CAPES (Coordination for the Improvement of Higher Education Personnel)-Finance Code 001 for granting the author’s scholarship and PELD/CNPq Proc. 441244/2016-5 for financial support. Fieldwork for this project was funded by two Natural Environment Research Council (NERC) grants: BIO-RED (NE/N012542/1) and ARBOLES (NE/S011811/1).

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Leaf traits of Cerrado trees vary according to season of leaf production

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Version 1

Abstract

Figures

Introduction

Materials And Methods

Study area and selected species

Data collection

Statistical analysis

Results

Dry versus wet season leaf traits

Acquisitive-conservative leaf traits variation

Variability of leaf morphoanatomical traits

Discussion

Seasonal vs. taxonomic controls on leaf traits variation

Seasonal shifts in acquisitive vs. conservative leaf trait values

Implications for future work

Conclusion

Declarations

References

Supplementary Files

Status:

Version 1