Cristiane da Silva Ferreira

Plant reproduction in the Central Amazonian floodplains: challenges and adaptations

We review strategies of sexual and asexual reproduction and persistence in plants of flood-prone Central Amazonia. Adaptations in response to the strong instability of these environments are highlighted together with the importance of river connectivity for species dispersal and persistence.

Germinação de sementes e sobrevivência de plântulas de Himatanthus sucuuba (Spruce) Wood. em resposta ao alagamento, nas várzeas da Amazônia Central

Himatanthus sucuuba is a tree which colonizes the varzeas of Central Amazonia. The present work was carried out in order to analyze the adaptive strategies of the species to cope with the long periods of flooding common in the varzea. Seeds were accompanied from germination until the seedling stage, in experimental conditions simulating natural field conditions (terrestrial phase and flooding period). Germination was tested in two substrates: sand + sawdust (only irrigated), and in water (submergence). The seedlings produced were then subjected, for 120 days, to three treatments: control (daily irrigation), partial submersion (root system) and total submersion (whole seedling). Alterations in the morphology of seedlings and in root anatomy were examined, together with the activity of the enzyme alcohol dehydrogenase (ADH) 0, 15, 30, 60, 90, and 120 days after the start of the treatments. Irrespective of the flooding regime, germination rates and seedling formation were high, both above 80%. Under partial submersion, hypertrophic lenticels, adventitious roots and aerenchyma were formed in the roots while ADH activity remained high until the 60th day of flooding, declining afterwards. Seedlings under total submersion lost all leaves, did not form adventitious roots or lenticels, but developed aerenchyma. These seedlings showed the highest values of ADH, which remained high until the end of the experiment, indicating the diversion of the aerobic metabolism to the production of ethanol as the main pathway to maintain the energetic balance. Although some totally submersed seedlings died, 70% of them survived the 120 days of flooding. Seedlings of H. sucuuba modulate morpho-physiologically the tolerance to flooding according to the time of exposure to the stress and the height of the water column.

Biochemistry of Amazonian floodplain trees

Trees colonizing Central Amazonian floodplains are subjected to extended periods of waterlogging and submersion surviving up to seven months of flooding per year. Flood is a consequence of changes in water level of ca. 10 m in the largest rivers of the region, and leads to a fast depletion of oxygen in the soil modifying the metabolism of the plants. Flooding tolerance varies between species and ecotypes as well as the biochemical traits and processes allowing the survival and adaptation of plant species. This results in a typical substitution of plant communities in these environments according to the depth of inundation. Amongst the developed metabolic adjustments and growth strategies and adaptations plants may show wood-ring formation, indicating annual growth reduction related to the inundation phase. The reduction of growth is preceded by stomatal closing, degradation of leaf chlorophyll, decrease of photosynthetic rates, carbohydrate translocation, and alteration of the hormonal balance. Floodplain trees develop as well protection mechanisms which can diminish damages caused by the long lasting annual hypoxia or even anoxia. Although the majority of woody plants can support periods of anoxia varying between a few hours to some days, in non-adapted species, irreversible damages can be caused leading to the death of the roots, when longer periods of flooding are imposed. These damages are attributed to the accumulation of toxic end products of the anaerobic metabolism, the loss of metabolic energy or the lack of respiration substrate. All and all the adaptations described at the biochemical level for temperate tree species inhabiting wetland are found in Amazonian floodplain trees; however, they are not enough to explain plant survival. This indicates the existence of novel mechanisms still to be found which together with the fate of the tree species inhabiting Amazonian floodplains in a changing climate are the main challenges faced by wetland scientists in the near future.

Tolerância de Himatanthus sucuuba Wood. (Apocynaceae) ao alagamento na Amazônia Central

Himatanthus sucuuba is a tree species with known phytotherapic value which colonizes both white-water floodplains (varzea) and upland forests (terra firme) in Central Amazonian. The objective of this study was to compare germination and initial seedling development from seeds collected in both the ecosystems. There was no significant difference between dry seed mass, but in a four month period in a glasshouse in Manaus, Brazil, germination rate differed according to the substrate and origin of the seeds. In the substrate sand + sawdust (non-flooded) germination rate was high, independent of seed origin (varzea 94% and terra firme 91%). In the substrate constituted only by water (flooded), the seeds originating from varzea had a higher germination rate (96%) and seedling formation (84%) than those originating from terra firme which had a germination rate of 64% and none of the seeds formed seedlings. In this treatment, the radicles rot few days after their emission, indicating that the seeds originating from varzea present adaptive characteristics to the floodplain environment which are not present in seeds from terra firme.

Seed germination and seedling development in response to submergence in tree species of the Central Amazonian floodplains

This study shows that Central Amazonian floodplain trees can cope with long-term flooding during the early life-history stages. Seven of the eight studied species germinated and formed seedlings under water that endured submersion without any apparent injury for periods of 20 to 115 days, depending on the species. Only one of the seven did not survive re-exposure to air. The ability to germinate and form seedlings in water that subsequently are able to thrive in aerated soils would allow the most use of the short terrestrial phase available for seedling establishment in the lower portions of the flood-level gradient.

Genetic Variability, Divergence and Speciation in Trees of Periodically Flooded Forests of the Amazon: A Case Study of Himatanthus sucuuba (Spruce) Woodson

Contrary to the theory that geographic isolation is the main trigger for speciation, recent studies emphasize the continuous adaptation to different habitats as the driving force initiating diversification. In this way, adaptive divergence in response to contrasting selective pressures of populations of the same species in geographically or ecologically continuous environments may occur if long-lasting barriers are induced by biotic or abiotic events. Plants of the Amazon floodplains withstand annual periods of flooding which can last seven months. To verify if the regularity of the “flood pulse” of the Amazon River can induce speciation, we investigated populations of Himatanthus sucuuba (Apocynaceae) colonizing whitewater floodplains (varzea) and non-flooded uplands (terra-firme) in the region. In independent experiments, we simulated flooding conditions, to evaluate the germination and growth of seedlings from both environments. The two populations showed significant differences for most parameters evaluated. Thus, flooding is apparently a feature strong enough to promote phenotypic differentiation among varzea and terra firme populations. Indeed, molecular analysis showed genetic difference between populations, revealing that different ecological pressures may promote adaptive changes in Amazonian plants to insure establishment in different environments.

Anatomia da lâmina foliar de onze espécies lenhosas dominantes nas savanas de Roraima

Knowledge of the anatomical characteristics of the leaf blade is crucial to the understanding of plant adaptation to the environment. The objective of this study was to describe the leaf anatomy of 11 woody species of common occurrence in the open savannas of the northern edge of the Amazon. The focus of the study was on the identification of leaf adaptive features to cope with high irradiances and seasonal water deficits. Leaf samples were fixed and processed by the usual methods for anatomical and histochemical studies. Bowdichia virgilioides, Byrsonima coccolobifolia, By. crassifolia, By. verbascifolia, Casearia sylvestris, Curatella americana, Erythroxylum suberosum, Himatanthus articulatus, Miconia albicans, Roupala montana and Xylopia aromatica showed leaf anatomical traits typical of heliophilous and xerophilous plants such as thick cuticle, stomata prevailing on the abaxial surface, strong investment in photosynthetic tissue. In eight of the eleven species the palisade parenchyma (PP) occupied 50% or more of the mesophyll. Curatella americana, with isobilateral mesophyll, and Bo. virgilioides, with homogeneous mesophyll were the species with the highest investment in PP (~80% and 100%, respectively). Leaves were also characterized by the presence of hypodermis (Bo. virgilioides and X. aromatica) or stratified epidermis, dense indumenta, crystalliferous idioblasts and bundle sheath extensions. This distinctive assortment of anatomical traits helps protecting the leaf blade against excessive irradiances, increases mechanical strength, minimize transpiration and contribute to the maintenance of leaf water balance. Overall they favor the establishment of these species in the seasonal savannas of northern Amazon.

Flood tolerance in two tree species that inhabit both the Amazonian floodplain and the dry Cerrado savanna of Brazil

Abstract Comparing plants of the same species thriving in flooded and non-flooded ecosystems helps to clarify the interplay between natural selection, phenotypic plasticity and stress adaptation. We focussed on responses of seeds and seedlings of Genipa americana and Guazuma ulmifolia to substrate waterlogging or total submergence. Both species are commonly found in floodplain forests of Central Amazonia and in seasonally dry savannas of Central Brazil (Cerrado). Although seeds of Amazonian and Cerrado G. americana were similar in size, the germination percentage of Cerrado seeds was decreased by submergence (3 cm water) and increased in Amazonian seeds. The seeds of Amazonian G. ulmifolia were heavier than Cerrado seeds, but germination of both types was unaffected by submergence. Three-month-old Amazonian and Cerrado seedlings of both species survived 30 days of waterlogging or submersion despite suffering significant inhibition in biomass especially if submerged. Shoot elongation was also arrested. Submersion triggered chlorosis and leaf abscission in Amazonian and Cerrado G. ulmifolia while waterlogging did so only in Cerrado seedlings. During 30 days of re-exposure to non-flooded conditions, G. ulmifolia plants that lost their leaves produced a replacement flush. However, they attained only half the plant dry mass of non-flooded plants. Both submerged and waterlogged G. americana retained their leaves. Consequently, plant dry mass after 30 days recovery was less depressed by these stresses than in G. ulmifolia. Small amounts of cortical aerenchyma were found in roots 2 cm from the tip of well-drained plants. The amount was increased by flooding. Waterlogging but not submergence promoted hypertrophy of lenticels at the stem base of both species and adventitious rooting in G. ulmifolia. Despite some loss of performance in dryland plants, flood tolerance traits were present in wetland and dryland populations of both species. They are part of an overall stress-response potential that permits flexible acclimation to locally flooded conditions.