No evidence for flooding stress memory in saplings of eight hardwood floodplain forest species

Alluvial floodplain forests became rare in many parts of Europe, due to anthropogenic changes. Therefore, restoration of floodplain forests is important, but a difficult task because of the complex environmental conditions. The zonation of woody species in floodplains is mainly determined by hydrological conditions, not only within one year but also during the previous years. Tolerance to flooding can be regarded as a key factor for the successful establishment. We examined whether a previous flooding showed an increased flooding tolerance of saplings from eight woody floodplain forest species after a recurrent flooding under controlled common garden conditions at the research station Gießen-Leihgestern (Germany). This would indicate a stress memory towards flooding stress. The individuals of the experiment already experienced a partial flooding of three different durations (three, six or nine weeks) or no flooding in the previous year. After nine months of recovery, these fourteen-month-old saplings were again either exposed to a partial flooding of nine weeks or no flooding. We assessed foliar injury and growth in terms of plant height, number of leaves and stem diameter three weeks (short-term recovery) and nine months (medium-term recovery) after flooding. The saplings showed no increased tolerance to a recurrent flooding irrespective of the previous experienced flooding duration. Therefore, no immediate stress memory towards flooding stress could be observed. To recover after flooding seems to be the better option compared to forming a stress memory, which explained that most species showed a decreased foliar injury after medium-term compared to short-term recovery period.

     

Flooding effects on plants recovering from defoliation in Paspalum dilatatum and Lotus tenuis

Background and Aims

Flooding and grazing are major disturbances that simultaneously affect plant performance in many humid grassland ecosystems. The effects of flooding on plant recovery from defoliation were studied in two species: the grass Paspalum dilatatum, regrowing primarily from current assimilation; and the legume, Lotus tenuis, which can use crown reserves during regrowth.

Methods

Plants of both species were subjected to intense defoliation in combination with 15 d of flooding at 6 cm water depth. Plant recovery was evaluated during a subsequent 30-d growth period under well-watered conditions. Plant responses in tissue porosity, height, tiller or shoot number and biomass of the different organs were assessed.

Key Results

Flooding increased porosity in both P. dilatatum and L. tenuis, as expected in flood-tolerant species. In P. dilatatum, defoliation of flooded plants induced a reduction in plant height, thus encouraging the prostrated-growth response typical of defoliated plants rather than the restoration of contact with atmospheric oxygen, and most tillers remained submerged until the end of the flooding period. In contrast, in L. tenuis, plant height was not reduced when defoliated and flooded, a high proportion of shoots being presented emerging above water (72 %). In consequence, flooding plus defoliation did not depress plant recovery from defoliation in the legume species, which showed high sprouting and use of crown biomass during regrowth, whereas in the grass species it negatively affected plant recovery, achieving 32 % lower biomass than plants subjected to flooding or defoliation as single treatments.

Conclusions

The interactive effect of flooding and defoliation determines a reduction in the regrowth of P. dilatatum that was not detected in L. tenuis. In the legume, the use of crown reserves seems to be a key factor in plant recovery from defoliation under flooding conditions.Key words: Allocation, defoliation, flooding, Lotus tenuis, Paspalum dilatatum, submergence     

How do Mycorrhizas Affect C and N Relationships in Flooded Aster tripolium Plants?

The mycorrhizal associations established between plants and fungi have multiple effects on plant growth, directly affecting stress tolerance. This work aimed to explore arbuscular mycorrhizal (AM) effects on carbon and nitrogen relationships of Aster tripolium L. and consequently on its flooding tolerance. Mycorrhizal and non-mycorrhizal juvenile plants were submitted to non-flooding and tidal flooding conditions for 56 d. Tidal flooding reduced biomass, but the presence of mycorrhiza had an ameliorating effect. The AM symbioses seem to have, like flooding, a stressful effect on A. tripolium at an early stage of plant development. However, once the plant was established, an improvement of growth performance of plants with mycorrhiza under flooding conditions was observed. The better tolerance of AM plants to flooding was mediated through an improvement of the osmotic adjustment of the plant tissues (higher concentrations of soluble sugars and proline) and through the increment of nitrogen acquisition in tidal-flooded plants.     

Physiological integration enhanced the tolerance of Cynodon dactylon to flooding

Many flooding‐tolerant species are clonal plants; however, the effects of physiological integration on plant responses to flooding have received limited attention. We hypothesise that flooding can trigger changes in metabolism of carbohydrates and ROS (reactive oxygen species) in clonal plants, and that physiological integration can ameliorate the adverse effects of stress, subsequently restoring the growth of flooded ramets. In the present study, we conducted a factorial experiment combining flooding to apical ramets and stolon severing (preventing physiological integration) between apical and basal ramets of Cynodon dactylon, which is a stoloniferous perennial grass with considerable flooding tolerance. Flooding‐induced responses including decreased root biomass, accumulation of soluble sugar and starch, as well as increased activity of superoxide dismutase (SOD) and ascorbate peroxidase (APX) in apical ramets. Physiological integration relieved growth inhibition, carbohydrate accumulation and induction of antioxidant enzyme activity in stressed ramets, as expected, without any observable cost in unstressed ramets. We speculate that relief of flooding stress in clonal plants may rely on oxidising power and electron acceptors transferred between ramets through physiological integration.     

Interaction between depth and duration matters: flooding tolerance of 12 floodplain meadow species

In riparian landscapes, regular flooding plays a crucial role in the distribution and diversity of plant species. Particularly in floodplain grassland, the microrelief, which is often the result of riverine sedimentation through flooding, leads to differing flooding depths and durations on a microscale, with little-known impacts on plants. Here, we aim to reveal the effects of flooding duration and flooding depth, as well as their interaction, on seedlings of 12 floodplain meadow plant species. To this end, we performed flooding procedures for 2 and 4 weeks with no, partial, and complete submergence using seedlings of floodplain meadow species in six familial pairs with a preference for relatively wetter or drier microhabitats. We show that an increased flooding duration and flooding depth negatively affect the performance of seedlings. The interactive effect of these two factors appears to play an essential role in the flooding tolerance of plant species. In conclusion, our results suggest that the studied factors and their interaction have high importance in determining the flooding tolerance of floodplain meadow plant species. Despite its crucial function, the effect of the depth?×?duration interaction seems to be underestimated in experimental studies focusing on flooding effects in plants. Thus, this interaction, as well as its combination with other factors, should be studied in more detail to further understand plant responses to flooding events.     

Effect of Off-Season Flooding on Growth,Photosynthesis, Carbohydrate Partitioning,and Nutrient Uptake in Distylium chinense

Distylium chinense is an evergreen shrub used for the vegetation recovery of floodplain and riparian areas in Three Gorges Reservoir Region. To clarify the morphological and physiological responses and tolerance of Distylium chinense to off-season flooding, a simulation flooding experiment was conducted during autumn and winter. Results indicated that the survival rate of seedlings was 100%, and that plant height and stem diameter were not significantly affected by flooding. Adventitious roots and hypertrophic lenticels were observed in flooded seedlings after 30 days of flooding. Flooding significantly reduced the plant biomass of roots, net photosynthetic rate (P _n), stomatal conductance (g _s), transpiration rate (T _r), maximum photochemical efficiency (Fv/Fm), photochemical quenching (qP), and electron transport rate (ETR) in leaves, and also affected the allocation and transport of carbohydrate and nutrients. However, D. chinense was able to maintain stable levels of P _n, Fv/Fm, qP, ETR, and nutrient content (N and P) in leaves and to store a certain amount of carbohydrate in roots over prolonged durations of flooding. Based on these results, we conclude that there is a high flooding tolerance in D. chinense, and the high survival rate of D. chinense may be attributable to a combination of morphological and physiological responses to flooding.     

Variation in flooding-induced morphological traits in natural populations of white clover (Trifolium repens) and their effects on plant performance during soil flooding

Background and Aims

Soil flooding leads to low soil oxygen concentrations and thereby negatively affects plant growth. Differences in flooding tolerance have been explained by the variation among species in the extent to which traits related to acclimation were expressed. However, our knowledge of variation within natural species (i.e. among individual genotypes) in traits related to flooding tolerance is very limited. Such data could tell us on which traits selection might have taken place, and will take place in future. The aim of the present study was to show that variation in flooding-tolerance-related traits is present among genotypes of the same species, and that both the constitutive variation and the plastic variation in flooding-induced changes in trait expression affect the performance of genotypes during soil flooding.

Methods

Clones of Trifolium repens originating from a river foreland were subjected to either drained, control conditions or to soil flooding. Constitutive expression of morphological traits was recorded on control plants, and flooding-induced changes in expression were compared with these constitutive expression levels. Moreover, the effect of both constitutive and flooding-induced trait expression on plant performance was determined.

Key Results

Constitutive and plastic variation of several morphological traits significantly affected plant performance. Even relatively small increases in root porosity and petiole length contributed to better performance during soil flooding. High specific leaf area, by contrast, was negatively correlated with performance during flooding.

Conclusions

The data show that different genotypes responded differently to soil flooding, which could be linked to variation in morphological trait expression. As flooded and drained conditions exerted different selection pressures on trait expression, the optimal value for constitutive and plastic traits will depend on the frequency and duration of flooding. These data will help us understanding the mechanisms affecting short- and long-term dynamics in flooding-prone ecosystems.Key words: Secondary roots, aerenchyma, genotypic variation, petiole length, plant performance, root porosity, selection, soil flooding, specific leaf area (SLA), Trifolium repens, white clover     

Life cycle stage and water depth affect flooding-induced adventitious root formation in the terrestrial species Solanum dulcamara

Background and Aims Flooding can occur at any stage of the life cycle of a plant, but often adaptive responses of plants are only studied at a single developmental stage. It may be anticipated that juvenile plants may respond differently from mature plants, as the amount of stored resources may differ and morphological changes can be constrained. Moreover, different water depths may require different strategies to cope with the flooding stress, the expression of which may also depend on developmental stage. This study investigated whether flooding-induced adventitious root formation and plant growth were affected by flooding depth in Solanum dulcamara plants at different developmental stages.Methods Juvenile plants without pre-formed adventitious root primordia and mature plants with primordia were subjected to shallow flooding or deep flooding for 5 weeks. Plant growth and the timing of adventitious root formation were monitored during the flooding treatments.Key Results Adventitious root formation in response to shallow flooding was significantly constrained in juvenile S. dulcamara plants compared with mature plants, and was delayed by deep flooding compared with shallow flooding. Complete submergence suppressed adventitious root formation until up to 2 weeks after shoots restored contact with the atmosphere. Independent of developmental stage, a strong positive correlation was found between adventitious root formation and total biomass accumulation during shallow flooding.Conclusions The potential to deploy an escape strategy (i.e. adventitious root formation) may change throughout a plant’s life cycle, and is largely dependent on flooding depth. Adaptive responses at a given stage of the life cycle thus do not necessarily predict how the plant responds to flooding in another growth stage. As variation in adventitious root formation also correlates with finally attained biomass, this variation may form the basis for variation in resistance to shallow flooding among plants.     

Variable response of three Trifolium repens ecotypes to soil flooding by seawater

Background and Aims

Despite concerns about the impact of rising sea levels and storm surge events on coastal ecosystems, there is remarkably little information on the response of terrestrial coastal plant species to seawater inundation. The aim of this study was to elucidate responses of a glycophyte (white clover, Trifolium repens) to short-duration soil flooding by seawater and recovery following leaching of salts.

Methods

Using plants cultivated from parent ecotypes collected from a natural soil salinity gradient, the impact of short-duration seawater soil flooding (8 or 24 h) on short-term changes in leaf salt ion and organic solute concentrations was examined, together with longer term impacts on plant growth (stolon elongation) and flowering.

Key Results

There was substantial Cl^– and Na⁺ accumulation in leaves, especially for plants subjected to 24 h soil flooding with seawater, but no consistent variation linked to parent plant provenance. Proline and sucrose concentrations also increased in plants following seawater flooding of the soil. Plant growth and flowering were reduced by longer soil immersion times (seawater flooding followed by drainage and freshwater inputs), but plants originating from more saline soil responded less negatively than those from lower salinity soil.

Conclusions

The accumulation of proline and sucrose indicates a potential for solute accumulation as a response to the osmotic imbalance caused by salt ions, while variation in growth and flowering responses between ecotypes points to a natural adaptive capacity for tolerance of short-duration seawater soil flooding in T. repens. Consequently, it is suggested that selection for tolerant ecotypes is possible should the predicted increase in frequency of storm surge flooding events occur.     

Sensing and signalling during plant flooding.

Flooding is a major issue for plant survival in many regions of the world. Soil inundation induces multiple plant physiological dysfunctions, leading to a decline in plant growth and survival capacity. Some of the most important effects of flooding include a reduction in water and nutrient uptake and a decrease in metabolism. Prolonged soil flooding will also ultimately lead to anoxia conditions with profound effects on plant respiratory metabolism. However, it is still unclear which signals and which sensory mechanisms are responsible for triggering the plant response. In contrast, it is now established that flooding responses are typified by enhanced ethylene production, accompanied by a signalling cascade which includes a network of hormones and other common secondary signalling molecules. In recent years, there has been significant progress in the understanding of some of the signalling pathways involved during plant stress responses. Here, we present an overview of recent hypothesises on sensing and signalling during plant flooding.     

Is tolerance to summer flooding correlated with distribution patterns in river floodplains? A comparative study of 20 terrestrial grassland species

It is generally assumed that floods during the growing season have a strong impact on the distribution of grassland plant species in river floodplains but this proposition has never been tested. We examined the survival and growth responses of twenty species, originating from mid- and high-level floodplain grasslands along the River Rhine in the Netherlands, to total submergence for a maximum of two months in an outdoor flooding experiment. Plant survival and biomass reduction with flooding duration was determined as well as biomass recovery after de-submergence.
Our results indicate that species survival is the most prominent factor correlated with species distribution in floodplain areas. Relatively flood tolerant species occurred mainly at low elevations along the floodplain while more flood sensitive species were restricted to high parts of the floodplain gradient. Biomass reduction rates during submergence were only marginally significantly correlated with species lower distribution boundaries along the flooding gradient. Biomass recovery rate was significantly correlated with species distribution patterns in the field only after 2 weeks of complete submergence, but not after 4 and 8 weeks. Our results suggest that the more flood tolerant species can have various ways to survive and recover from flooding, ranging from low rates of biomass loss and low recovery to relatively high rates of biomass loss and quick recovery.
Our results are consistent with the notion that disturbance by floods during the growing season is an important determinant of species lower distribution boundaries in river floodplains. They also suggest that high survival under flooding may be achieved by different physiological mechanisms. Such mechanisms are discussed in this paper.     

Growth Control by Ethylene: Adjusting Phenotypes to the Environment

Plants phenotypically adjust to environmental challenges, and the gaseous plant hormone ethylene modulates many of these growth adjustments. Ethylene can be involved in environmentally induced growth inhibition as well as growth stimulation. Still, ethylene has long been considered a growth inhibitory hormone. There is, however, accumulating evidence indicating that growth promotion is a common feature in ethylene responses. This is evident in environmental challenges, such as flooding and competition, where the resulting avoidance responses can help plants avoid adversity. To show how ethylene-mediated growth enhancement can facilitate plant performance under adverse conditions, we explored a number of these examples. To escape adversity, plants can optimize growth and thereby tolerate abiotic stresses such as drought, and this response can also involve ethylene. In this article we indicate how opposing effects of ethylene on plant growth can be brought about, by discussing a unifying, biphasic ethylene response model. To understand the mechanistic basis for this multitude of ethylene-mediated growth responses, the involvement of ethylene in processes that control cell expansion is also reviewed.     

Does flood tolerance explain tree species distribution in tropical seasonally flooded habitats?

In the tropics, seasonally flooded forests (SFF) harbor fewer tree species than terra firme (i.e. non-flooded) forests. The low species diversity of tropical flooded forests has been ascribed to the paucity of species with adaptations to tolerate flooding. To test the hypothesis that flooding is the only factor restricting most species from SFF, we compared plant morphological and physiological responses to flooding in 2-month old seedlings of 6 species common to SFF and 12 species common to terra firme forests. Although flooding impaired growth, total biomass, maximum root length and stomatal conductance in most species, responses varied greatly and were species-specific. For example, after 90 days, flooding reduced leaf area growth by 10-50% in all species, except in Tabebuia, a common species from non-flooded habitats. Similarly, flooding had a 5-45% negative effect on total biomass for all species, except in 1 SFF and 1 terra firme species both of which had more biomass under flooding. A principal component analysis, using the above responses to flooding, provided no evidence that SFF and terra firme species differed in their responses to flooding. Flooding also caused reductions in root growth for most species. Rooting depth and root: shoot ratios were significantly less affected by flooding in SFF than in terra firme species. Although flood tolerance is critical for survival in flooded habitats, we hypothesize that responses to post-flooding events such as drought might be equally important in seasonal habitats. Therefore, we suggest that the ability to grow roots under anoxia might be critical in predicting success in inundated habitats that also experience a strong dry season.     

Sapling growth and survivorship as affected by light and flooding in a river floodplain forest of southeast Texas

We investigated the effects of light and flooding on growth and survivorship of saplings in a river floodplain forest of southeast Texas. Growth responses to light were consistent with the expectation that shade-intolerant species grow faster than shade-tolerant species in high light, and vice versa. Mortality risk was not associated with shade tolerance level unless high mortality risks associated with a period of high flooding were removed. These results support the hypothesis that shade-tolerant species in floodplains may be limited by flooding as previous studies suggested. Also, compared to their performance at a nearby mesic site, common species showed little intraspecific difference in shade tolerance, especially for shade-intolerant species. Finally, the positive correlation between low-light growth and survivorship suggests that carbon allocation to continued growth may be favored as a sapling strategy in floodplains.     

Drought responses of flood-tolerant trees in Amazonian floodplains

Background

Flood-tolerant tree species of the Amazonian floodplain forests are subjected to an annual dry period of variable severity imposed when low river-water levels coincide with minimal precipitation. Although the responses of these species to flooding have been examined extensively, their responses to drought, in terms of phenology, growth and physiology, have been neglected hitherto, although some information is found in publications that focus on flooding.

Scope

The present review examines the dry phase of the annual flooding cycle. It consolidates existing knowledge regarding responses to drought among adult trees and seedlings of many Amazonian floodplain species.

Main Findings

Flood-tolerant species display variable physiological responses to dry periods and drought that indicate desiccation avoidance, such as reduced photosynthetic activity and reduced root respiration. However, tolerance and avoidance strategies for drought vary markedly among species. Drought can substantially decrease growth, biomass and photosynthetic activity among seedlings in field and laboratory studies. When compared with the responses to flooding, drought can impose higher seedling mortality and slower growth rates, especially among evergreen species. Results indicate that tolerance and avoidance strategies for drought vary markedly between species. Both seedling recruitment and photosynthetic activity are affected by drought,

Conclusions

For many species, the effects of drought can be as important as flooding for survival and growth, particularly at the seedling phase of establishment, ultimately influencing species composition. In the context of climate change and predicted decreases in precipitation in the Amazon Basin, the effects of drought on plant physiology and species distribution in tropical floodplain forest ecosystems should not be overlooked.Key words: Drought responses, Amazonia, floodplain forests, tree ecology, várzea     

Effect of the <Emphasis Type="Italic">ipt</Emphasis> gene expression on wheat tolerance to root flooding

The effect of enhanced cytokinin synthesis due to expression of the ipt gene from Agrobacterium tumefaciens on plant tolerance to root flooding was studied. Transgenic wheat (Triticum aestivum L.) plants carrying the ipt gene were more tolerant to flooding than wild-type plants. The effect of transformation was manifested in the higher yield and less growth inhibition during flooding. The measurements of activities of antioxidant enzymes, superoxide dismutase and catalase, as well as MDA content during flooding revealed differences between wild-type and transgenic plants that correlated with their tolerance. These results point to the protective role of cytokinins during wheat root flooding.     

Physiological and morphological responses of red alder and sitka alder to flooding

Red alder (Alnus rubra Bong.) and sitka alder (A. viridis ssp. sinuata [Regel] Löve & Löve) are nitrogen-fixing woody species that grow sympatrically along the Pacific coast of North America. Red alder is found in poorly drained lowlands, as well as in soils of moist upland slopes, whereas sitka alder generally colonizes well-drained soils. To identify factors that contribute to flood tolerance, we conducted greenhouse experiments subjecting both species to a 20-day flood and 10-day recovery and red alder to a 50-day flood and 20-day recovery. We determined the effect of this stress on nitrogenase activity, root and nodule alcohol dehydrogenase (ADH) activity, lenticel and adventitious root development, relative growth rate (RGR), and leaf gas exchange. After 24 h of flooding, nitrogenase activity could not be detected in either species. Limited nitrogenase activity did return in red alder at the end of a 10-day recovery following the 20-day flood, but sitka alder showed no recovery of nitrogenase activity. After 50 days of continuous flooding, red alder nitrogenase activity returned to pretreatment levels. Red alder root and nodule ADH activity was more than twice that of sitka alder under flooded conditions. Sitka alder showed extensive root mortality and leaf abscission over the same 20-day flooding period. Flooded red alder exhibited an initial decline in root RGR, but recovered between days 10 and 20 with the formation of adventitious roots. Furthermore, initiation of adventitious roots in red alder coincided with an increase in stomatal conductance without a similar recovery of carbon dioxide exchange rate. Sitka alder formed few adventitious roots, lost much of its root and leaf biomass, and showed no restoration of growth during flooding or recovery. Different responses of red and sitka alder to flooding serve as a partial explanation for the different patterns of distribution of these species and suggest some adaptations of red alder that permit flood tolerance.     

Survival and growth responses of eight Everglades tree species along an experimental hydrological gradient on two tree island types

Questions: How are the early survival and growth of seedlings of Everglades tree species planted in an experimental setting on artificial tree islands affected by hydrology and substrate type? What are the implications of these responses for broader tree island restoration efforts? Location: Loxahatchee Impoundment Landscape Assessment (LILA), Boynton Beach, Florida, USA. Methods: An experiment was designed to test hydrological and substrate effects on seedling growth and survivorship. Two islands – a peat and a limestone‐core island representing two major types found in the Everglades – were constructed in four macrocosms. A mixture of eight tree species was planted on each island in March of 2006 and 2007. Survival and height growth of seedlings planted in 2006 were assessed periodically during the next two and a half years. Results: Survival and growth improved with increasing elevation on both tree island substrate types. Seedlings' survival and growth responses along a moisture gradient matched species distributions along natural hydrological gradients in the Everglades. The effect of substrate on seedling performance showed higher survival of most species on the limestone tree islands, and faster growth on their peat‐based counterparts. Conclusions: The present results could have profound implications for restoration of forests on existing landforms and artificial creation of tree islands. Knowledge of species tolerance to flooding and responses to different edaphic conditions present in wetlands is important in selecting suitable species to plant on restored tree islands     

Response and adaptation by plants to flooding stress

Stress on plants imposed by flooding of the soil and deeper submergence constitutes one of the major abiotic constraints on growth, species' distribution and agricultural productivity. Flooding stress is also a strong driver of adaptive evolution. This has resulted in a wide range of biochemical, molecular and morphological adaptations that sanction growth and reproductive success under episodic or permanently flooded conditions that are highly damaging to the majority of plant species. However, even seemingly poorly adapted species possess some short-term resilience that is important for overall success of these plants in various habitats. The papers contained in this Special Issue address these topics and emphasize molecular, biochemical and developmental processes that impact on flooding tolerance. Most of the articles are based on lectures given to the 8th Conference of the International Society for Plant Anaerobiosis (ISPA), held at the University of Western Australia, Perth, 20-24 September, 2004. Reviews and research papers are presented from the leading laboratories currently working on plant responses to flooding stress.