Adaptive strategies in young Inga vera subsp. affinis plants under floodingAbstract
Inga vera subsp. affinis (DC.) T.D.Penn. is a common species in riparian vegetation of the Atlantic Forest within the Upper Paraná River Floodplain (UPRF) and of great ecological importance in the restoration of native forests. Since UPRF environments are subject to periodic flooding, this study aimed to analyze the adaptive strategies of I. vera subsp. affinis under flooding. I. vera fruits were collected from riparian mother trees to obtain seedlings, which were subjected to flooding for 44 days. After the experiment, 10 individuals from each treatment were selected, and their height, root length, leaf area, number of leaves, and the fresh and dry mass of leaves, stems, and roots were measured. Physiological traits were evaluated from the extraction and quantification of soluble sugars in leaves and roots, as well as the quantification of photosynthetic pigments in the leaves of seedlings. Results were subjected to analysis of variance according to their respective assumptions. I. vera plants showed reduced growth under flooding, lower levels of photosynthetic pigments, and increased production of soluble sugars, which were relocated to the roots. These findings indicate the species’ capacity for physiological adjustment to floods, which can support conservation strategies for riparian tree species in relation to climate change and adaptations of the species itself over time.
Keywords:
rainforest; Fabaceae; soluble carbohydrates; water stress; ecophysiology
Resumo
Inga vera subsp. affinis (DC.) T.D.Penn.é uma espécie frequente na vegetação ripária da Mata Atlântica da Planície de Inundação do Alto Rio Paraná (PIAP) e de grande importância ecológica, relacionada à recuperação de florestas nativas. Considerando que os ambientes do PIAP estão sujeitos a ciclos de inundação, o estudo teve por objetivo analisar as estratégias adaptativas de I. vera subsp. affinis em condições de alagamento. Foram coletados frutos de I. vera em matrizes ribeirinhas para obtenção de plântulas que foram submetidas ao alagamento por um período de 44 dias. Após a experimentação, utilizou-se 10 indivíduos de cada tratamento e mensurados a altura, o comprimento da raiz, a área foliar, o número de folhas, a massa fresca e massa seca das folhas, do caule e da raiz. Os atributos fisiológicos foram avaliados a partir da extração e quantificação de açúcares solúveis das folhas e raízes e da quantificação foliar dos pigmentos fotossintéticos das mudas de ingá. Os resultados obtidos foram submetidos à análise de variância conforme seus respectivos pressupostos. I. vera apresentou diminuição do crescimento em alagamento, menor teor dos pigmentos fotossintéticos e maior produção de açúcares solúveis realocados para as raízes, indicando capacidade de modulação fisiológica da espécie às condições de alagamento, podendo subsidiar estratégias de conservação para espécies arbóreas ripárias em relação à mudanças climáticas e a adaptações da própria espécie ao longo do tempo.
Palavras-chave:
floresta tropical; Fabaceae; carboidratos solúveis; estresse hídrico; ecofisiologia
1. Introduction
The Upper Paraná River Floodplain (UPRF) is an area included in the Atlantic Forest biome and subject to flooding and seasonal high-water events, which strongly select for phenotypic traits in vegetation due to highly hydromorphic soils (Campos et al., 2000).
Inga vera subsp. affinis (DC.) T.D. Penn., Fabaceae, popularly known as “ingazeiro”, “ingá”, “ingá-do-brejo”, “ingá-banana”, among others is a native tree species found across all Brazilian biomes and is considered one of the most frequent and ecologically important species in the riparian forest of the UPRF (Campos et al., 2000; Souza and Kita, 2003). I. vera is predominantly a riparian species in this area, contributing to the ecological functions of local habitats (hydrological and food chain) by providing structural habitat diversity, food for wildlife (fruits), and resources for the regional human population (Rodrigues and Leitão Filho, 2001). This species has achieved greater stability in these environments due to its high capacity for morphological and physiological adaptation to fluctuations in hydromorphic gradients (Campos and Souza, 2002; Budke et al., 2010; Artusi et al., 2020; Vitali et al., 2025). These strategies confer both resistance and resilience—qualities inherent to ecological dominance in terms of species representativeness and population abundance in the vegetation (Barbosa et al., 2022; Feitosa et al., 2023; Guerreiro et al., 2025).
Physiological adaptations directly influence photosynthesis and metabolism, which in turn affect morphological adaptations and plant responses in interaction with the biotic environment and abiotic fluctuations, by characteristics of plant anatomy—such as leaves, roots, and stems. Plant organs and abiotic factors, such as water, are traits and resources that enable the analysis of growth parameters, including height, number of leaves, leaf area, biomass, and the synthesis of pigments and carbohydrates, indicating how tree species respond to abiotic variations in water availability (Fajardo and Siefert, 2018; Dovrat et al., 2019).
The energy stored by the plant is largely explained by photosynthetic efficiency, deposited as non-structural carbohydrates (Carmo-Silva and Salvucci, 2013; Saeki and Iwasaki, 2020; Baião et al., 2024). Reductions in chlorophyll concentration can decrease carboxylation efficiency in flooded plants, as radiation absorption depends on the concentration of photosynthetic pigments, affecting quantum efficiency and, consequently, the carboxylation process (Rengifo et al., 2005; Bertolde et al., 2012). Thus, plant growth and the allocation of soluble carbohydrates can be modulated according to environmental saturation.
The study of the ecological niche of riparian forests contributes to a broader understanding of biodiversity conservation in subtropical forests, highlighting important functions such as potential carbon storage (Castaño et al., 2024) and the physiological plasticity of riparian tree species across different soil moisture gradients (Nash and Graves, 1993; Pérez-Jiménez, et al.. 2015). Furthermore, knowledge of a given species’ adaptive strategies, especially in the initial growth of native species, which ensure its establishment under habitat-imposed stresses, can inform decision-making regarding its use in restoration and biodiversity conservation efforts. Plants in the early stages of growth can serve as models for the responses of tree seedlings to climate change and for the species' adaptations over time. Recent studies have shown that species with low flood tolerance are favored by tolerant species, indicating inter-species interactions and benefits in flood-prone environments (Silva et al., 2023). In this way, studies like this contribute to the ecological understanding of tropical riparian trees subject to large abiotic variations. Therefore, this study aimed to analyze the growth of young Inga vera subsp. affinis plants and its adaptive response under flooding conditions.
2. Methodology
2.1. Study area and material collection
To collect Inga vera fruits, mother trees with ripe fruits were selected from the riparian vegetation of the UPRF, located approximately from 22° 40’ to 22° 58’ S and 53° 10’ to 53° 39’ W, in Porto Rico’s district.
The regional climate is classified as humid subtropical (Cfa) according to the Köppen system, with an average annual temperature of 24 °C and average annual precipitation of 1,500mm, with the highest rainfall occurring from November to March (IDR, 2019). UPRF soils originate from alluvial sediments and are generally hydromorphic, influencing vegetation patterns and creating forest patches with distinct characteristics (Souza Filho and Stevaux, 1997). Vegetation domain in the region is dominated by the Atlantic Forest and falls within the phytogeographical domain of the Semi-deciduous Seasonal Forest (IBGE, 1982).
2.2. Seedling production and experimental design
The collected I. vera fruits were transported to the Limnology, Ichthyology and Aquaculture Research Group (Nupélia) Riparian Vegetation laboratory at the State University of Maringá (UEM), Paraná State. Seeds were manually extracted from the fruits and subsequently sown in trays in a greenhouse, containing a mixture of medium-grain sand and commercial organic substrate in a 2:1 ratio, respectively, until germination. Irrigation was applied as needed.
After emergence, seedlings were transplanted into adequate plastic bags, measuring 10×20 cm, using the same type of substrate, for a 15-day acclimation period. After acclimatization, plants were subjected to water stress by flooding, in which 50 randomly selected individuals were placed in small individual plastic buckets, filled with water to approximately 3 cm above the substrate surface (Maurenza et al., 2009). Simultaneously, another 50 young control plants were maintained at field capacity (control). Thus, the experiment was conducted with two treatments: control and flooding. Both conditions were maintained for 44 days.
After the experimental period, 10 individuals from each treatment—flooded and control (44 days old)—were removed from the bags by vertical sectioning, and the substrate was washed off. These plants were then used to evaluate the parameters that will be further discussed.
2.3. Biometrics
Biometric parameters were evaluated in 10 plants (n = 10): shoot height (SH) and root length (RL) were measured using a ruler (cm); number of leaves (NL) by direct counting, and collar diameter (CD) with a digital caliper (mm). Fresh mass of leaves (LFM), stems (SFM), and roots (RFM) was determined using an analytical balance (g). After drying in an oven at 60 °C for 72 h dry mass of leaves (LDM), stems (SDM) and roots (RDM) were estimated using a MARK/M214Ai precision analytical scale.
Shoot dry mass (ShDM) values and the ratios RDM/ShDM, RDM/TDM (total dry mass), LDM/TDM, SDM/TDM, ShDM/TDM, SH/ShDM, and SH/CD were calculated using values previously obtained.
Fully expanded leaves from the third node of seedlings were scanned and subsequently measured to calculate leaf area using the Image-Pro® plus 4.5 software.
2.4. Quantification of photosynthetic pigments
The procedures for analyzing the content of photosynthetic pigments were carried out at the Seed and Seedling Physiology Laboratory (LAFISP), UEM.
Chlorophyll a, chlorophyll b, and carotenoids contents were quantified according to Lichtenthaler (1987) by macerating fresh plant material in 80% acetone. A total of 100mg of fresh leaves from the second or third node of five seedlings (n = 5) was macerated with 80% acetone using a mortar and pestle and then filtered through qualitative filter paper. The extract was collected in a graduated cylinder to a final volume of 25 mL. Absorbance was measured using a Shimadzu UV-VIS-1201 spectrophotometer at 470nm, 645nm, 647nm, and 663nm wavelengths. Total chlorophyll content was calculated by summing the values of chlorophyll a and chlorophyll b. Results were expressed as sample means and standard error (mean±SE) in mg of chlorophyll and carotenoids per gram of fresh mass (mg.g−1 FM).
2.5. Quantification and determination of soluble sugars
The procedures for analyzing the content of soluble sugars were carried out at the Seed and Seedling Physiology Laboratory (LAFISP), UEM.
Soluble sugar biomass (µg.g) was quantified in leaf and root samples from 10 individuals per treatment. Plant material was macerated and centrifuged to obtain an alcoholic extract, which was evaporated before the addition of distilled water to obtain the aqueous extract, from which soluble compounds were quantified. Total soluble sugar content was determined at 620 nm absorbance (Clegg, 1956) using a Shimadzu UV-VIS-1201 spectrophotometer .
2.6. Data analysis
Data analysis was conducted to compare the mean of quantitative traits between treatments using parametric analysis of variance (ANOVA) in GraphPadPrism 8, followed by a Student’s t-test. Homogeneity of variance (Levene’s test) and normality (Shapiro–Wilk) were assessed, with p-values ≤ 0.05 considered statistically significant.
3. Results
The analysis of the biometric parameters is presented in Table 1, while the coefficient of variation and significance are in Table 2.
Biometric parameters of Inga vera subsp. affinis under field capacity (control) and water stress (flooding).
Coefficient of variation and significance of the analyses performed for each parameter of Inga vera subsp. Affinis plants, according to the t-test.
After seedling assessment, I. vera individuals exhibited greater leaf and root growth in field-capacity soil (control) compared to flooded soil (Figure 1). However, no formation of lenticels or adventitious roots was observed.
Under flooding, plants showed a significant 27% reduction in height growth compared to control plants (Table 1). Plant roots showed an average reduction of 69% in RL than control plants. The number of leaves was also lower under flooded soil, with three leaves in flooded plants and five in controls. CD showed no significant differences between treatments.
Regarding plant biomass, the LFM and LDM in the flooded treatment were 50% and 55% lower, respectively, compared to control plants. For stem mass, significant differences were observed in SFM, with flooded plants showing an average reduction of 63% compared to controls. RFM was significantly lower under flooding (83%); however, no statistical differences were found for SDM and RDM compared to control plants. TFM and TDM showed significant reductions of 62% and 70%, respectively, while shoot fresh mass (ShFM) and ShDM of flooded plants decreased on average 55% and 29% compared to control plants (Table 1).
The RDM/ShDM ratio showed a significant 55% reduction under flooding. RDM/TDM and LDM/TDM also decreased significantly under stress, 53% and 7%, respectively. SDM/TDM and ShDM/TDM showed significantly higher values under flooding, increasing 84% and 25%, respectively. SH/ShDM decreased significantly by 8% and SH/CD by 7% under the same conditions. Leaf area showed a significant reduction of 19% under flooded soil.
Regarding soluble sugars, roots showed higher concentrations in plants subjected to flooding compared to controls (Figure 2A), but no significant differences were observed in leaf sugar concentrations between treatments (Figure 2B).
Root (A) and leaf (B) soluble carbohydrates of Inga vera subsp. affinis plants under control and flood conditions. Means were compared non-parametric t-test (P ≤ 0.05), ns = not significant.
For photosynthetic pigments, both treatments showed differences in chlorophyll a, chlorophyll b, and carotenoid contents, with values approximately 50% statistically lower in flooded plants (Figures 33B). The chlorophyll a/b ratio in flooded plants was 13% significantly lower, and total chlorophyll was 48% lower under flooding. No significant differences were observed for the total chlorophyll/carotenoid ratio (Figure 3F).
Photosynthetic pigment content of Inga vera subsp. affinis under field-capacity (control) and flooding conditions. Differences in chlorophyll a (A), chlorophyll b (B), total chlorophyll (C), chlorophyll a/b (D), carotenoids (E), and total chlorophyll/carotenoid ratio (F) in I. vera leaves under control and flooding conditions are represented by an asterisk (*), with P ≤ 0.05; ns = indicates non-significant differences between treatments.
4. Discussion
In riparian areas subject to cyclic flooding from river overflows, vegetation is highly selective due to the need for adaptation to hydromorphic soils (Vazzoler, 1997). I. vera occurs within the Semi-deciduous Seasonal Forest domain, mainly in hydromorphic forest patches of the Alluvial Semi-deciduous Seasonal Forest or riparian forest (Kawakita et al., 2024). In response to flooding cycles, this and other native subtropical riparian species develop morphophysiological adaptations, such as higher sugar concentrations in leaves and translocation to the roots (storage), as well as the growth of adventitious roots, which facilitate oxygen diffusion. These adjustments alter shoot growth, increasing survival in hydromorphic environments (Samojeden et al., 2018; Dovrat et al., 2019; Marcílio et al., 2019; Bispo and Vieira, 2022; Barbeiro et al., 2023).
As observed in I. vera, studies with young Lonchocarpus cultratus and Handroanthus chrysotrichus plants have reported reduced growth under flooding, with shorter heights, lower number of leaves, and leaf and root dry mass in L. cultratus, along with declines in chlorophyll content and increases in root soluble carbohydrates (Marcílio et al., 2019; Bispo and Vieira, 2022). Similarly, analysis of young Inga marginata and Inga vera plants under flooding also indicates that changes in growth and morphophysiological responses are important variables for the survival of riparian species in flooded environments (Bender et al., 2017; Feitosa et al., 2023; Lopez et al., 2025). Thus, an intrinsic relationship can be observed between growth-related morphological traits and the levels of sugar production and photosynthetic pigments—especially chlorophyll—which are essential to interpret the developmental dynamics and survival of riparian tree species.
Control I. vera specimens showed higher RDM/ShDM values, indicating greater mass allocation to the roots (values closer to 1), whereas flooded plants invested more in the stem (higher SDM/TDM) (Table 1). Additionally, plants under flooding exhibited lower leaf and root mass (LDM/TDM, RDM/TDM). This suggests greater mass allocation to the stem in relation to leaves and roots, contributing to the greater height observed in control plants (Table 1). Plants under flooding may exhibit greater stem elongation, which may be influenced by the phytohormone ethylene (Wang and Komatsu, 2022). Furthermore, flooded environments may reduce aeration in the root system, thereby reducing root energy metabolism and inducing less growth (Leeggangers et al., 2023), as observed in I. vera plants.
The higher content of soluble carbohydrates in the roots of I. vera plants under flooding conditions suggests the allocation of sugars from leaves to roots, as well as the mobilization of stored carbohydrates, promoting the increase in soluble sugars in the roots. The accumulation of sugars in tree species under flooding, as a consequence of phloem translocation to the root system, has been reported by Kreuzwieser et al. (2004). Moreover, the increase in root soluble carbohydrates indicates a flooding tolerance mechanism (Rengifo et al., 2005), given their protective role against hypoxia and anoxia during flooding stress (Bispo and Vieira, 2022).
Recent studies have also shown an increase in total sugars and sucrose in the roots of Zygia cataractae under flooding conditions (Barbeiro et al., 2023). Lonchocarpus cultratus also exhibited reduced root and total dry mass, as well as a greater accumulation of soluble sugars in the roots after flooding treatment (Marcílio et al., 2019). Inga marginata demonstrated higher acclimation in waterlogged soil, which appears to be associated with increased accumulation of soluble sugars (Bender et al., 2017; Samojeden et al., 2018).
Soluble sugars play not only an energetic role but also function as part of the plant’s defense system together with the cellular antioxidant system, participating in catabolic and anabolic reactions that limit and eliminate the harmful effects of reactive oxygen species (ROS), such as superoxide radicals (O2–) and hydroxyl radicals (OH–). These radicals interact with proteins, lipids, and DNA, causing cellular damage and even cell death, thereby impairing normal functioning (Bittencourt and Silva, 2018), as observed in the protection of the cell membrane (Hu et al., 2012) and the photosynthetic apparatus. Thus, the accumulation of soluble sugars is an important acclimation strategy for seedlings under environmental stress (Roitsch, 1999; Hasanuzzaman et al., 2020).
Among structures affected by stress is the chlorophyll molecule, whose content was also lower in Inga vera under water stress. This reduction may be one of the main factors contributing to the decreased growth of plants in waterlogged soil. Gonçalves et al. (2012) suggest that the reduced flux of light energy in the photosynthetic system results from the lower concentration of pigments than from functional alterations in the photosynthetic apparatus.
Plants kept in flooded soil showed reduced growth—as evidenced by lower height, root length, and fresh and dry mass of leaves and roots. No leaf abscission, lenticel formation, or adventitious roots were observed, all of which are typically associated with plants in water-saturated soils. The absence of adventitious roots and lenticels during the flooding period may be due to the energy-saving strategy of younger I. vera plants as observed in the greater amount of soluble sugars in the flooded root, despite the low production of chlorophyll and carotenoids., which favors survival maintenance and growth under flooding conditions with the allocation of carbohydrates as osmoprotective molecules.
5. Conclusion
It was concluded that flooding treatment altered the physiological responses of young I. vera plants, negatively affecting their growth. These adjustments may enable riparian species to survive during flooding cycles in flood-prone areas. In this context, ecophysiology studies of native trees are relevant to investigate the role of morphophysiological mechanisms in the dynamics of tropical and subtropical riparian forests under ongoing climate fluctuations.
Acknowledgements
We thank CAPES for the scholarship awarded to the first author, to the support of the Araucaria Foundation for the research development with the funding of the NAPI Project: RESTORE and NAPI Genetic Resources and Biotechnology, to the Graduate Program of Compared Biology, to the State University of Maringá, and to our laboratory colleagues who helped us with data collection.
Data Availability Statement
The research data analyzed in this study are not publicly available by any means.
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Editor:
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