Adaptive strategies to tolerate prolonged flooding in seedlings of floodplain and upland populations of Himatanthus sucuuba, a Central Amazon tree

Long-term flooding imposes a strong selection pressure on plants for the development of protective mechanisms to alleviate the harmful effects of hypoxic and anoxic conditions. This is particularly critical in the Amazonian floodplains where plants withstand annual periods of flooding lasting 7 months and mean flooding amplitude reaching 10 m or more. Himatanthus sucuuba (Apocynaceae) is a tree that is found in the varzea (VZ) floodplains and non-flooded terra firme (TF) forests. It was examined whether individuals from these two contrasting habitats respond differently when subjected to extreme flooding conditions. TF and VZ seedlings were experimentally well-watered, waterlogged (roots and parts of the stems flooded), or submerged (whole plant flooded) during a 4-month period. Anaerobic respiration, evaluated by measuring alcohol dehydrogenase (ADH) activity, and root carbohydrate reserves were quantified, given that the availability of readily fermentable carbohydrates is essential to sustain an active fermentative metabolism. We also assessed changes in morphoanatomy, seedling survival, biomass accumulation and distribution. VZ seedlings had greater root concentrations of soluble sugars and starch, larger seedling mass and accumulated more biomass in roots and stems while TF seedlings allocated more towards stem and leaves. ADH activity was low in seedlings of both populations before exposure to flooding. Waterlogging induced an increase in ADH activity that reached a maximum value in 15 days. Thereafter activity decreased slowly, meanwhile a rapid formation of lenticels, adventitious roots and aerenchyma was observed. Submergence induced leaf shedding and the development of aerenchyma in the root cortex. While VZ seedlings maintained high levels of ADH activity throughout the whole 4-month period, ADH activity in TF seedlings peaked about 15 days after submersion followed by a continuous decrease and death of all the plants. Thus, VZ and TF seedlings differed considerably in terms of tolerating long-term exposure to flooding, especially under total submersion. These results suggest that the predictability and long-term duration of flooding in Central Amazon rivers can impose a selective pressure that is strong enough to result in large phenotypic differences between the two populations of H. sucuuba in the two habitat types.     

Which seed origin provides better tolerance to flooding and drought when restoring to face climate change?

Our goal was to establish the tolerance to flooding and drought of seedlings from a hydric gradient of different seed sources to provide recommendations for forest restoration in the face of climate change. We used Drimys winteri var. chilensis, a tree species that grows from extreme arid zones to wetlands along Chile, as the study subject. We expected that seedlings of xeric origin would perform better in drought conditions than populations from moist environments, and vice versa for flooding tolerance. We collected D. winteri seeds from xeric, mesic and wet environments. Seedlings at two development stages were submitted to an extreme flooding and drought treatment during 2 or 4 months in a common garden. After the flooding and drought assays finished, the number of surviving and damaged seedlings, lenticels and adventitious root presence, height, new leaves and specific leaf area, shoot/root ratio, water potential and/or chlorophyll fluorescence (Fv/Fm), were recorded. We found that flooding and drought affected almost all the parameters studied negatively. The xeric population seedlings, at both development stages studied, were the most tolerant to the drought and, unexpectedly, also to the flooding treatment. We recommend restoring with seedlings of xeric origin especially in arid areas where sudden flooding is frequent, as occurs in the Andes Mountains. In the face of climate change, we recommend carrying out common garden and field studies before advising which population origin should be used for restoration, since they do not always respond in accordance with expected patterns of local adaptation.     

EFFECTS OF FLOODING AND NUTRIENT ENRICHMENT ON BIOMASS ALLOCATION IN ACER RUBRUM SEEDLINGS

A greenhouse experiment was conducted on Acer rubrum seedlings to evaluate the effects of flood frequency on production and allocation of biomass and to test the effects of N and P fertilization on production and allocation. Seedlings from the Dismal Swamp were subjected to three flood treatments (no flooding, intermittent flooding, and continuous flooding) and four enrichment treatments (no enrichment, N additions, P additions, and N + P additions). More continuous flooding resulted in less biomass production. Biomass increased during the study in all treatments except for root mass in the continuously flooded treatment. However, production of abundant adventitious roots compensated for the lack of normal root growth. Root/shoot ratios exhibited the greatest decreases in the continuously flooded plants. Plants with N + P added had significantly more leaf, stem, and total mass than the nonenriched plants four months into the study. The N + P additions had apparently compensated for the effects of flood stress in the continuously flooded plants by the end of the study. The fertilized seedlings accumulated higher concentrations of N and P, but their nutrient use efficiency (biomass production per unit nutrient absorbed) was lower than in the nonenriched plants. Acer rubrum seedlings survive flooded conditions through several adaptations; however, theirgrowth is slowed by continuous flooding.     

Phenotypic plasticity and precipitation response in Sonoran Desert winter annuals

Temporal environmental variation has profound influences on population dynamics and community structure. Examination of functional traits that influence resource uptake and allocation can illuminate how co-occurring species translate environmental variation into different demographic outcomes, yet few studies have considered interspecific differences in trait plasticity. We experimentally manipulated soil moisture to test the hypothesis that differences in morphological plasticity contribute to species differences in demographic response to unpredictable precipitation in Sonoran Desert winter annual plants. We compared plasticity of leaf traits and biomass allocation between Pectocarya recurvata (Boraginaceae) and Stylocline micropoides (Asteraceae), co-occurring species that differ in long-term demographic patterns. The species with highly variable population dynamics, Stylocline, had striking increases in leaf area and root biomass in response to an experimental increase in soil moisture. In contrast, the species with buffered long-term population dynamics, Pectocarya, did not differ in leaf morphology or biomass allocation between soil moisture treatments. Regardless of water treatment, Pectocarya had earlier reproductive phenology and greater fecundity than Stylocline, suggesting that differences in the timing of the phenological transitions from vegetative to reproductive growth may affect species' responses to precipitation pulses. Combining long-term observations with experimental manipulations provides a window into the functional underpinnings and demographic consequences of trait plasticity.     

Relationship of light intensity to leaf resin composition and yield in the tropical leguminous genera Hymenaea and Copaifera

Hymenaea and Copaifera are closely related morphologically distinct tree genera whose leaf resins appear to be composed of the same sesquiterpene hydrocarbons which occur in similar quantitative compositional patterns. The seedlings of both genera grow in varying light intensities in the understories of different lowland tropical ecosystems from desert thorn forests to equatorial evergreen rain forests; all eventually grow into high light intensity. Previous controlled environment studies of the effects of photoperiod, temperature and moisture status have shown little phenotypic plasticity in the leaf resin composition of Hymenaea seedlings. In this study, focusing on light intensity, both control chamber experiments comparing seedlings of H. courbaril var. courbaril, H. courbaril var. subsessilis, C. officinalis and C. pubiflora, grown under low and high light treatments, and field data from saplings of C. multijuga, growing under shaded and unshaded conditions, also show lack of phenotypic plasticity in resin composition. The yield of resin (mg/g leaf tissue), however, varied considerably among individuals, and increased significantly from low to high light conditions in both control chamber and field conditions. The relationship of increased synthesis is discussed with regard to photosynthetic capacity, allocation of carbon and herbivory.     

Evolutionary reduction of developmental plasticity in desert spadefoot toads

Organisms vary their rates of growth and development in response to environmental inputs. Such developmental plasticity may be adaptive and positively correlate with environmental heterogeneity. However, the evolution of developmental plasticity among closely related taxa is not well understood. To determine the evolutionary pattern of plasticity, we compared plasticity in time to and size at metamorphosis in response to water desiccation in tadpoles among spadefoot species that differ in breeding pond and larval period durations. Like most tadpoles, spadefoot tadpoles possess the remarkable ability to accelerate development in response to pond drying to avoid desiccation. Here, we hypothesize that desert spadefoot tadpoles have evolved reduced plasticity to avoid desiccation in ephemeral desert pools compared to their nondesert relatives that breed in long-duration ponds. We recorded time to and size at metamorphosis following experimental manipulation of water levels and found that desert-adapted species had much less plasticity in larval period and size at metamorphosis than nondesert species, which retain the hypothetical ancestral state of plasticity. Furthermore, we observed a correlation between degree of plasticity and fat body content that may provide mechanistic insights into the evolution of developmental plasticity in amphibians.     

Biomass allocation, shade tolerance and seedling survival of the invasive species

Berberis darwinii (Berberidaceae) is a serious environmental weed in New Zealand, capable of invading a range of different light environments from grazed pasture to intact forest. According to optimal partitioning models, some plants optimise growth under different environmental conditions by shifting biomass allocation among tissue types (e.g. roots, shoots) to maximise the capture of limiting resources (e.g. water, light). We examined patterns of growth, biomass allocation, and seedling survival in Berberis darwinii to determine whether any of these factors might be contributing to invasion success. Growth and biomass allocation parameters were measured on seedlings grown for 7 months in five natural light environments in the field. Survival was high in the sunniest sites, and low in the shadiest sites. Seedlings grown in full sun were an order of magnitude taller and heavier, had five times as many leaves, and proportionally more biomass allocated to leaves than seedlings grown in other light environments. In the shade, leaves were bigger and thinner, and leaf area as a proportion of total plant biomass increased, but the proportion of above- to below-ground biomass was similar across all light and soil moisture environments. In summary, although leaf traits were plastic, patterns of biomass allocation did not vary according to optimal partitioning models, and were not correlated with patterns of seedling survival. Implications for the management of this invasive species are discussed.     

Root Plasticity of Populus euphratica Seedlings in Response to Different Water Table Depths and Contrasting Sediment Types

Riparian plants in arid regions face a highly variable water environment controlled by hydrological processes. To understand whether riparian plants adapt to such environments through plastic responses, we compared the root traits, biomass allocation and growth of Populus euphratica Oliv. Seedlings grown in lysimeters filled with clay or clay/river sand sediments under inundation and varying water table conditions. We hypothesized that adaptive phenotypic plasticity is likely to develop or be advantageous in seedlings of this species to allow them to adapt desert floodplain environments. Growth was significantly reduced by inundation. However, rather than following relatively fixed trait and allocation patterns, the seedlings displayed adaptive mechanisms involving the development of adventitious roots to enhance plant stability and obtain oxygen, together with a lower proportion of root biomass. At the whole-plant level, at deeper water table depths, seedlings allocated more biomass to the roots, and total root length increased with decreasing water table depths, regardless of the sediment, consistent with optimal partitioning theory. The sediment type had a significant effect on seedling root traits. P. euphratica displayed very different root traits in different sediment types under the same hydrological conditions, showing a greater first-order root number in clay sediment under shallower water table conditions, whereas rooting depth was greater in clay/river sand sediment under deep water table conditions. In clay sediment, seedlings responded to lower water availability via greater root elongation, while the root surface area was increased through increasing the total root length in clay/river sand sediment, suggesting that seedlings facing deeper water tables are not always likely to increase their root surface area to obtain more water. Our results indicate that P. euphratica seedlings are able to adapt to a range of water table conditions through plastic responses in root traits and biomass allocation.     

Responses of Pinus clausa, Pinus serotina and Pinus taeda seedlings to anaerobic solution culture. I. Changes in growth and root morphology

Seedlings of pond pine ( Pinus serotina Michx.), sand pine [ P. clausa (Engelm.) Sarg.] and two edaphic seed sources of loblolly pine ( P. taeda L., dry- and wet-site seed sources) were grown in non-circulating, continuously flowing solution culture under aerobic (250 μ M O₂) and anaerobic (≤ 23 μ M O₂) conditions. Survival was 100% for all seedlings at 11 weeks. Although shoot height, biomass and leaf emergence of loblolly and pond pine seedlings were not significantly affected by 15 or 30 days of anaerobic growth conditions, root biomass was significantly reduced. Sand pine suffered the largest reduction in biomass, showing extensive root dieback and shoot chlorosis with retarded leaf development. These anaerobically induced symptoms of flooding injury were less severe in dry-site loblolly pine, and absent in wet-site loblolly and pond pine seedlings. Adventitious or new, secondary roots, and stem or taproot lenticels were particularly abundant under the 30-day anaerobic treatment in wet-site loblolly and pond pine seedlings, present to a lesser degree in dry-site loblolly pine, and nearly absent in sand pine seedlings. These results indicate that much of the immediate damage from flooding is due to the anoxic condition of the root rather than to the build-up of phytotoxins or soil nutrient imbalances. On the basis of overall seedling vigor, root plasticity and growth, we suggest the following flooding-tolerance/intolerance species (seed source) gradient: pond pine ≥ wet-site loblolly pine > dry-site loblolly pine > sand pine.     

Developing a mathematical model for variation of physiological responses of Jatropha curcas leaves depending on leaf positions under soil flooding

The effect of soil flooding on photosynthesis, transpiration and stomatal conductance of Jatropha curcas seedlings were studied under natural environmental variables. Soil flooding reduced photosynthesis (P _N), transpiration (E) and stomatal conductance (gs) in response to leaf positions of Jatropha curcas plants. Based on the results, we conclude that decrease in stomatal opening and stomatal limitation of photosynthesis, followed by decrease in individual leaf area are the main causes of reductions in carbon uptake of flooded seedlings. A mathematical relationship was successfully developed to describe photosynthesis, transpiration and stomatal response of Jatropha under soil flooding stress.     

The role of carbohydrates in seed germination and seedling establishment of Himatanthus sucuuba, an Amazonian tree with populations adapted to flooded and non-flooded conditions

Background and Aims

In the Amazonian floodplains plants withstand annual periods of flooding which can last 7 months. Under these conditions seedlings remain submerged in the dark for long periods since light penetration in the water is limited. Himatanthus sucuuba is a tree species found in the ‘várzea’ (VZ) floodplains and adjacent non-flooded ‘terra-firme’ (TF) forests. Biochemical traits which enhance flood tolerance and colonization success of H. sucuuba in periodically flooded environments were investigated.

Methods

Storage carbohydrates of seeds of VZ and TF populations were extracted and analysed by HPAEC/PAD. Starch was analysed by enzyme (glucoamylase) degradation followed by quantification of glucose oxidase. Carbohydrate composition of roots of VZ and TF seedlings was studied after experimental exposure to a 15-d period of submersion in light versus darkness.

Key Results

The endosperm contains a large proportion of the seed reserves, raffinose being the main non-structural carbohydrate. Around 93 % of the cell wall storage polysaccharides (percentage dry weight basis) in the endosperm of VZ seeds was composed of mannose, while soluble sugars accounted for 2·5%. In contrast, 74 % of the endosperm in TF seeds was composed of galactomannans, while 22 % of the endosperm was soluble sugars. This suggested a larger carbohydrate allocation to germination in TF populations whereas VZ populations allocate comparatively more to carbohydrates mobilized during seedling development. The concentration of root non-structural carbohydrates in non-flooded seedlings strongly decreased after a 15-d period of darkness, whereas flooded seedlings were less affected. These effects were more pronounced in TF seedlings, which showed significantly lower root non-structural carbohydrate concentrations.

Conclusions

There seem to be metabolic adjustments in VZ but not TF seedlings that lead to adaptation to the combined stresses of darkness and flooding. This seems to be important for the survival of the species in these contrasting environments, leading these populations to different directions during evolution.     

Development and plasticity of endangered shrub Lindera melissifolia (Lauraceae) seedlings under contrasting light regimes

Lindera melissifolia (Walt.) Blume seedlings were raised in a growth chamber to determine the effects of light availability on shoot growth pattern, and basic leaf and stem growth. Lindera melissifolia seedlings exhibited a sympodial shoot growth pattern for 3 months following emergence from the soil medium, but this pattern was characterized by a reduction in leaf blade area approximately 30 days after emergence, followed by increases in leaf blade area. Seedlings receiving low light were 76% taller than seedlings receiving high light. Seedlings receiving low light also had larger leaf blade dimensions, blade area, seedling leaf area, and greater mass. Seedlings raised in high light had a greater proportional distribution of biomass in the roots, suggesting possible water stress from greater vapor pressure deficits. Furthermore, these seedlings displayed sharp angles of blade inclination and blade folding – acclimation that reduces exposure to light and subsequent higher leaf temperatures in open environments. These differences in morphological response to light resulted in high phenotypic variability in L. melissifolia seedlings. Lindera melissifolia seedling development showed a brief period of phenotypic plasticity, followed by ontogenetic plasticity. The short period of phenotypic plasticity may, however, have profound ecological implications for the conservation and recovery of this federally endangered shrub. Further experimentation should take into account the development of ontogenetic standards for comparisons of plant traits in addition to temporal standards.     

Plasticity in seedling morphology,biomass allocation and physiology among ten temperate tree species in response to shade is related to shade tolerance and not leaf habit

• Mechanisms of shade tolerance in tree seedlings, and thus growth in shade, may differ by leaf habit and vary with ontogeny following seed germination. To examine early responses of seedlings to shade in relation to morphological, physiological and biomass allocation traits, we compared seedlings of 10 temperate species, varying in their leaf habit (broadleaved versus needle‐leaved) and observed tolerance to shade, when growing in two contrasting light treatments – open (about 20% of full sunlight) and shade (about 5% of full sunlight).
• We analyzed biomass allocation and its response to shade using allometric relationships. We also measured leaf gas exchange rates and leaf N in the two light treatments.
• Compared to the open treatment, shading significantly increased traits typically associated with high relative growth rate (RGR) – leaf area ratio (LAR), specific leaf area (SLA), and allocation of biomass into leaves, and reduced seedling mass and allocation to roots, and net assimilation rate (NAR). Interestingly, RGR was not affected by light treatment, likely because of morphological and physiological adjustments in shaded plants that offset reductions of in situ net assimilation of carbon in shade. Leaf area‐based rates of light‐saturated leaf gas exchange differed among species groups, but not between light treatments, as leaf N concentration increased in concert with increased SLA in shade.
• We found little evidence to support the hypothesis of a increased plasticity of broadleaved species compared to needle‐leaved conifers in response to shade. However, an expectation of higher plasticity in shade‐intolerant species than in shade‐tolerant ones, and in leaf and plant morphology than in biomass allocation was supported across species of contrasting leaf habit.

     

Differentiation in populations of Hordeum spontaneum Koch along a gradient of environmental productivity and predictability: plasticity in response to water and nutrient stress

Plants from four populations of Hordeum spontaneum originating in distinct environments of Israel were compared for stress induced phenotypic plasticity. The environments ranged along a gradient of increasing rainfall amount and predictability from low (desert) to moderate (semisteppe batha) to high (Mediterranean grassland and mountain, the latter also experiencing frost stress). The plants were exposed to a set of four treatments: no stress (optimum water and nutrients), water, nutrient and both water and nutrient stress. Plants from the four populations (or ecotypes) exhibited different patterns of plasticity in response to the different stresses (water and nutrients) and in different trait categories (reproductive, fitness and resource allocation). The importance of plasticity in response to water stress appears to decrease, and to nutrient stress appears to increase along the increasing rainfall gradient. The mountain ecotype, growing in an area with high potential productivity (amount of rainfall) but experiencing periodic frosts, was the most plastic among ecotypes in resource allocation under both water and nutrient stress, but exhibited low plasticity in other trait categories. In contrast, the desert ecotype had low plasticity in resource allocation under water stress and the lowest plasticity among the four ecotypes in all trait categories in response to nutrient stress. The ecotype originating in Mediterranean grassland, a predictable and most favourable environment, was highly plastic in fitness and allocation traits in response to low nutrient levels which is likely to occur due to competition in productive environment. We discuss the observed differences in ecotype plasticity as part of their environmentally induced adaptive ‘strategies’. We found no support for the hypothesis that plants originating in environments with greater variation and unpredictability are more plastic. © 2002 The Linnean Society of London, Biological Journal of the Linnean Society 2002, 75 , 301–312.     

水分因素对沙地柏实生苗水分和生长特征的影响

为探讨未来降雨变化对半干旱气候区毛乌素沙地常绿优势灌木沙地柏(Sabina vulgaris)实生苗水分和生长特征的可能影响，在鄂尔多斯沙地草地生态站开展了模拟降雨变化的实验。水分饱和亏缺和组织密度随土壤水分含量提高而降低，失水系数却相反，这表明沙地柏实生苗的保水抗旱性随模拟降雨量增加而降低。水分梯度对枝茎面积比无显著影响，叶质量茎面积比和叶质量枝面积比随土壤水分含量增大而降低，这意味着实生苗分枝的供水潜力随水分可利用性提高而降低。水分变化显著影响生物量分配，而对形态和植冠生产力指数均无显著影响；生物量、株高和基茎增量的变化反映了沙地柏生长的缓慢性。根系对水分变化的敏感性高于叶和茎，地下部分生物量投资随水分可利用性提高而增大，这暗示沙地柏实生苗可能通过节约利用水分方式适应自然生境中的水分胁迫。     

CO2浓度倍增和土壤干旱对两种幼龄沙生灌木碳分配的影响

利用大型环境生长箱研究了两种幼龄沙地优势灌木柠条 (Caraganaintermedia) 和羊柴 (Hedysarummon golicum) 对CO2 浓度倍增和土壤干旱交互作用的响应。CO2 浓度倍增并没有改善两种沙生灌木叶片的水分状况, 而土壤干旱使叶片的相对含水量 (RWC) 显著降低。在土壤水分充足条件下, CO2 浓度倍增促进两种沙生灌木植株生长, 在干旱条件下则主要促进根的生长, 提高根冠比。土壤干旱显著减少了植株生物量, 但相对促进了根的生长, 特别是显著提高了羊柴的根冠比。CO2 倍增使稳定性碳同位素组分 (δ13 C) 降低, 但土壤干旱使之增加。两种沙生灌木叶片与根部的δ13 C值呈极显著线性关系, 羊柴的斜率大于柠条的, 表明前者叶片与根部在光合产物分配上具有较高的生态可塑性, 这和干旱条件下羊柴的根冠比增加相关联。羊柴的“源库”调节特性反映了对土壤水分胁迫具有较高的耐性。     

Nutrient levels within leaves,stems, and roots of the xeric species Reaumuria soongorica in relation to geographical,climatic, and soil conditions

Besides water relations, nutrient allocation, and stoichiometric traits are fundamental feature of shrubs. Knowledge concerning the nutrient stoichiometry of xerophytes is essential to predicting the biogeochemical cycling in desert ecosystems as well as to understanding the homoeostasis and variability of nutrient traits in desert plants. Here, we focused on the temperate desert species Reaumuria soongorica and collected samples from plant organs and soil over 28 different locations that covered a wide distributional gradient of this species. Carbon (C), nitrogen (N), and phosphorus (P) concentrations and their stoichiometry were determined and subsequently compared with geographic, climatic, and edaphic factors. The mean leaf C, N, and P concentrations and C/N, C/P, and N/P ratios were 371.6 mg g⁻¹, 10.6 mg g⁻¹, 0.73 mg g⁻¹, and 59.7, 837.9, 15.7, respectively. Stem and root C concentrations were higher than leaf C, while leaf N was higher than stem and root N. Phosphorus concentration and N/P did not differ among plant organs. Significant differences were found between root C/N and leaf C/N as well as between root C/P and leaf C/P. Leaf nutrient traits respond to geographic and climatic factors, while nutrient concentrations of stems and roots are mostly affected by soil P and pH. We show that stoichiometric patterns in different plant organs had different responses to environmental variables. Studies of species-specific nutrient stoichiometry can help clarify plant–environment relationships and nutrient cycling patterns in desert ecosystems.     

Variability in amount and frequency of water supply affects roots but not growth of arid shrubs

Rainfall and soil moisture variability have a strong effect on plant survival and seed germination in arid environments, yet very little is known about the effects on roots and growth of woody seedlings. Here we focused on the effects of variability in both amount and frequency of water supply on juvenile root and leaf functional traits and growth of seven Mediterranean shrub species occurring in arid SE Spain, Anthyllis cytisoides, Atriplex halimus, Ephedra fragilis, Genista umbellata, Lycium intricatum, Retama sphaerocarpa, and Salsola oppositifolia. In a 14-month greenhouse experiment we manipulated water supply expecting that reduced water amount and pulses of watering of different magnitude affected functional traits and seedling growth, even if the amount of water provided was the same. Different watering patterns altered soil drying dynamics, with reduced supply of water amount and frequent watering becoming the driest treatment. We found that roots of all species responded to alterations in water supply by changing biomass allocation patterns (i.e., higher root-to-shoot mass [R:S] ratio in droughted plants), and by altering fine roots diameter, measured in terms of specific root length. Indeed, differences in growth rate among species were significantly linked to fine roots diameter and biomass allocation, which relates to uptake capacity of roots. However, relative growth rate and leaf traits such as specific leaf area were insensitive, likely because prolonged droughts over longer periods of time seem necessary to constraint growth in all these arid shrubs.