Introduction During the recent Darwin bicentennial year (2009) and throughout the 151 years since the publication of ‘On the Origin of Species’ (Darwin, 1859), discussion on the ‘struggle for survival’ has been topical and controversial. Darwin's theory of ‘survival of the fittest’ is a synonym for ‘natural selection’. Darwin asked ‘Can it be doubted, from the struggle each individual has to obtain subsistence, that any minute variation in structure, habits or instincts, adapting that individual better to new conditions, would tell upon its vigour and health?’ (Darwin, 1842). Accordingly, the present study discusses the struggle for life in the forests of large flood-pulsed wetlands in relation to what is known of variations in structure, physiology and biochemistry that confer resilience. Contrary to the wisdom of Darwin, we cannot, unfortunately, deal with differences within populations because such data are very difficult to obtain for these huge ecosystems. Instead, our aim is to bring together data on responses of trees to flooding in the freshwater wetlands of tropical environments, emphasizing the varying responses to different wetland structures and flooding conditions extant in tropical freshwater floodplains of four continents. Although Gopal et al. (2000) have published a book on the biodiversity of wetlands and Junk (1997) produced a review of comparative biodiversity in floodplains around the world, there is no one publication which focuses on adaptation and survival of trees in tropical wetlands. The present article aims to fill this gap. The four large wetlands chosen for our analysis are the Central Amazonian floodplains of South America, the Okavango Delta region of Botswana, Africa, the Mekong floodplains of South-east Asia and the tropical wetlands of Northern Australia (Fig. 1; Table 1). These ecosystems, each on a different continent, were chosen largely on the following pragmatic grounds. We looked for very large tropical freshwater floodplains with forest patches (i.e. trees occurring there naturally) where flooding occurs with regularity (the ‘flood pulse’ of Junk et al., 1989), is characterized by high amplitudes and where it is long-lasting (weeks or months). We were careful not to include areas merely prone to flash floods following heavy rain. Our assessments are based on many diverse publications and disparate data concerning the effects of flooding on species richness, ecophysiology and distribution of tropical trees. Fig. 1 Map indicating the approximate location of the four chosen floodplain forests. Table 1 Characteristics of the four chosen floodplain ecosystems on four continents with a monomodal flood pulse Central Amazonia Okavango Delta Mekong Tonle Sap Kakadu Region in Northern Australia Continent South America Africa Asia Northern Australia Geographical position 3°15′S, 59°58′W 18°30′–20°S, 22°–24°E 13°N, 104°E 13°2′S, 133°31′E Latitude 0 19 13 12 Age of ecosystem (Irion et al., 1997; Junk et al., 2006) 2.4 million years 2.5 million years 7500 years 4000 years Height asl (m) 0–50 1000 0–50 0–50 Connected rivers Major river system Major river system Major river system Smaller rivers Floodplain area (km2) 300 000 2500–8000; 28 000 15 000 99 000; 2900 Annual precipitation (mm) 2100 460–490 1600 1300–1450 Predictability of flooding High High High High Flood amplitude 15 m 1.85 m 8.2 m 2–5 m Mean/maximum flood height 8 m Root level 6 months Wetland main vegetation Forest Mainly grassland Forest/grassland Forest/grassland Trophic status Meso-eutrophic Mesotrophic Meso-eutrophic Oligo-mesotrophic Fire No Yes No? Yes Salt No Yes! No? No? Forest cover Closed forest Single trees 10 %, mosaic of stands of large trees and open areas Open savanna to 70 % forest cover Tree/canopy height 20–30 m 5–6 m 7–15 m 20 m Woody species (Junk et al., 2006) >1000 180 70 21 Number of flood-tolerant tree species >1000 10 15 5 Incidence of endemic tree species High Very low Low Low? Tree species diversity High Very low Few dominant species Low? Human pressure Low Low? Very high (wars; fishing) Minimal Human impacts Timber extraction; fishing; cattle ranching Subsistence agriculture; fisheries Timber; fishing; paddy rice Cattle grazing; tourism; mining Changes Increasing incidence and severity of drought Soil salinization due to tree felling; expansion of agriculture; agrarian-degradation; predicted degeneration of major vegetation types from increased drying (Ringrose et al., 2002) Dramatic fluctuations in water level of Mekong River; frequent floods and lower water levels in dry season—an increasing problem for farming (IUCN, 1991). Invasion by alien plants and animals; changed fire regime; water pollution from urban-tourism, mining and salinization; sea level rise (Junk et al., 2006) While selecting our four ecosystems, it soon became evident that data are extremely scarce, despite their importance for biodiversity and human resources (Wantzen and Junk, 2000). We were forced to exclude many of the largest wetlands, e.g. the Congo basin in Africa or the Orinoco floodplains in Venezuela, because only basic data on hydrology and climatology are available, with almost no information on plant distribution, tree adaptations and ecophysiology. It is important to bring attention to such poorly researched wetlands, which are often inaccessible for social and political reasons but are threatened by the ever-increasing human population and its need for water, waterways and hydroelectric power. The destruction is so fast that we may never learn of the adaptations underpinning the success of the tree species in these areas. We are aware that differences between the four ecosystems are large, especially in respect of the influence of fire and salinity. Those which are dominated by grasslands (Okavango and Northern Australian floodplains) are subjected to regular fire (Heinl et al., 2004, 2006, 2007), whereas in the forest-dominated floodplains of Amazonia and Mekong, fire plays no significant role. In the Okavango, the high evapotranspiration causes salinity problems, which are negligible in the remaining three ecosystems. Also, flooding amplitudes vary widely between the ecosystems, with about 2 m in the Okavango and Northern Australian, 8 m in the Mekong and 15 m in the Amazon floodplains (Table 1). This implies that complete submergence of saplings and trees occurs only in the Mekong and Amazon, posing different constraints for plant life than merely waterlogging of roots and stems (Parolin, 2009). However, our review is readily justified because the regular flood pulse is a major influence on all floodplain biology (Junk, 1989; Junk et al., 1989) and a dominating stress which requires a suite of adaptations for its survival. Throughout the world, wetland ecosystems are under increasing pressure from agriculture, urbanization of catchment areas, tourism and recreational activities, construction of impoundments and changes to hydrology and climate. By comparing diversity and tree responses in four floodplain ecosystems on different continents, we attempt to improve our understanding of the factors influencing the spatial distribution of plants, diversity of species and adaptations, and thus contribute to our knowledge of tropical wetland ecology. In this way, we hope to assist in the successful restoration of degraded floodplains and promote the sustainable use and conservation of these highly valuable ecosystems. Flooding as a stress factor Flooding with freshwater, although less harmful than flooding with saltwater, poses a multitude of constraints on growth, survival and reproduction. Trees are basically terrestrial organisms and, in general, die more readily in response to flooding than to desiccation (Larcher, 1994). Flooding involves inundation of part or all of the aboveground structures, whereas waterlogging is restricted mainly to inundation of the soil and rhizosphere (Colmer and Pedersen, 2008). Totally submerged plants have no direct contact with atmospheric oxygen and sunlight is weak or extinguished. Inundated soils become hypoxic or anoxic within a few hours as the combined result of oxygen consumption by respiring roots plus micro-organisms and insufficiently fast diffusion of oxygen through water to replace the amounts consumed (Crawford, 1989, 1992; Armstrong et al., 1994; Visser et al., 2003). Oxygen depletion in soil is accompanied by increased levels of entrapped CO2, anaerobic decomposition of organic matter, increased solubility of mineral substances, notably iron and manganese, and decreased redox potential (Joly and Crawford, 1982; Kozlowski, 1984). The resulting chemically reduced and potentially toxic compounds accumulate, their generation being the result of alterations in the composition of the soil microflora as it responds to the changing conditions (Ponnamperuma, 1984). In some floodplains, e.g. those of the Amazon River, sedimentation rates can be extremely high and the deposition of sediment can decrease soil aeration and thus favour oxygen shortage in the rhizosphere (Wittmann et al., 2004; Wittmann and Parolin, 2005). Elevated decomposition rates of highly productive floating and non-floating macrophytes in floodplains further decrease oxygen concentrations in the floodwater (Armstrong et al., 1994). In temperate zones, flooding frequently occurs during winter when plants are dormant and light intensities low. In contrast, the flooding period in tropical floodplains occurs when temperatures and light intensities are high and conditions overall are optimal for plant growth. Therefore, the trees are not dormant and must accommodate shortages of oxygen and, for submerged shoots, shortages of CO2 too at a time when conditions favour fast respiration and depletion of reserves. This implies that extraordinarily efficient adaptations are needed for survival. With all these constraints, imposed by flooding, this stress is clearly life-threatening for higher plants. The struggle for survival of flooding is therefore closely linked to the evolution of physiological, phenological, anatomical and morphological adaptations that confer tolerance and underpin successful and vigorous growth and fecundity despite the intense stress. Floodplain ecosystems Here we characterize four extensive floodplain ecosystems present on four continents (Table 1). They include the Central Amazon floodplains (where we have the broadest and deepest knowledge of tree ecophysiology), the Okavango Delta in Africa, the Mekong floodplains in South-east Asia (where relatively little is known about tree ecology) and the Northern Australian floodplains (where much is known about the herbaceous vegetation, but much less about tree responses to freshwater flooding; Table 2). Table 2 Characteristics of the forest vegetation (distribution, phenology, physiological adaptations) in the four chosen floodplain ecosystems on four continents Central Amazonia Okavango Delta Mekong Tonle Sap Kakadu Region in Northern Australia Continent South America Africa Asia Northern Australia Tree distribution Zonation of trees along the flooding gradient Yes Yes Yes Yes Degree of endemism Elevated Low/absent Low/absent Low/absent Leaf phenology Deciduous species: leaf shedding at high waters Yes No Yes ? Evergreen species Yes Yes Yes ? Reproductive phenology Linked to high water + fish ? Linked to high water + fish ? Physiological adaptations Reduction of metabolism and growth during high waters Yes No Yes? ? Morpho-anatomical adaptations Leaf xeromorphism; hypertrophic lenticels; adventitious roots; aerenchyma ? ? ? Biochemical adaptations Increased activity of fermentative enzymes; more VOC emission ? ? ? South America: Central Amazonian floodplains There are extensive floodplains along the Amazon River and its large tributaries throughout the Amazon basin. These contain large species-rich and highly adapted floodplain forests that cover more than 300 000 km2 (Irion et al., 1997). The mean annual temperature of 26.6 °C changes little, average rainfall is ∼2100 mm year−1 (Ribeiro and Adis, 1984) and noon light intensities can reach 3000 µmol m−2 s−1 at the water surface (Furch et al., 1985). Seasonal variations in river levels subject trees to periods of up to 210 days of continuous flooding each year. The rate of change in the water level can be fast and reach 10 cm day−1 (Junk, 1989), leading to a total rise of up to 16 m in western Amazonia, 10 m in Central Amazonia and 6 m in eastern Amazonia (Junk, 1989). The ‘flood pulse’ (Junk et al., 1989) is monomodal and the timing is predictable, resulting in well-defined high-water (aquatic phase) and low-water (terrestrial phase) periods each year. The timing of the pulse is predictable, but irregularities occur in the maximum and minimum water levels. This can be of great relevance for seedling establishment (Scarano et al., 1997). At high water levels, tree roots and stems are waterlogged, and small trees and seedlings may be completely submerged for several months by a water column of up to 8 m (Parolin et al., 2004; Parolin, 2009). At low water levels, drought may be a stress factor for several weeks (Junk, 1997; Parolin et al., 2010). Natural fires and salt are absent from this ecosystem. Although large terrestrial mammals play important roles for tree establishment and distribution in the grasslands of other floodplains, they play no significant role in the Amazonian floodplain (Junk and da Silva, 1997). The differing origins of the various tributaries of the Amazonian River system can strongly influence water chemistry, e.g. sources in the western Amazon Andes or the Northern and Southern Amazonian Precambrian shields. The resulting seasonally flooded vegetation can roughly be differentiated into the nutrient-rich and highly productive white-water floodplains (várzea) and the nutrient-poor and less productive black-water or clear-water floodplains (igapó) (Fig. 2; Sioli, 1954; Prance, 1979). In Central Amazonia, both floodplain types undergo seasonal water-level changes of up to 10 m (Fig. 3). Trees establish at mean annual flood levels 12 million years old), or even earlier. Such ancient landscapes will have experienced several changes in climate and hydrology, i.e. during the glacial and interglacial periods. In contrast, the Mekong River basin and the Australian floodplains are much younger, and are thought to be no older than 7500 and 4000 years, respectively (Junk et al., 2006). Conclusions and forward look Our comparative review on the adaptive responses of trees to flooding in four tropical freshwater floodplains of different continents demonstrates that substantial data about the floodplain tree flora, its ecology and functioning are lacking. Despite many physio-ecologically motivated studies on trees of the Central Amazonian floodplains, and a few studies on other tropical freshwater floodplains, we are still only at the start of our understanding of how terrestrial plants, especially trees, cope with extended periods of flooding. However, this knowledge is fundamental to understanding the evolution of flooded landscapes and their organisms, as well as their interaction with non-flooded ecosystems. The range of plant responses recorded in the different tropical floodplains leads us to the following conclusions: Regular flooding is a severe stress to trees, resulting in reduced species richness compared with non-flooded uplands. The regular flood pulse has given rise to a large diversity of growth forms and adaptations by trees. These seem to increase in variety with the age of the respective floodplains and the climatic stability to which they were exposed. Most floodplain tree species are restricted to small topographic amplitudes along the flooding gradients, leading to a distinct zonation of tree species. This implies different mechanisms or combinations of mechanisms conferring zone-specific tolerance to flood stress. This zonation is not dependent on the height of the flooding amplitude. Most highly flooded (>2 m) tree species react to high-water periods with leaf shedding, which is associated with decreased metabolism and growth. The occurrence of evergreen tree species does not depend on the height and magnitude of flooding, since evergreen species are found in all three floodplains. Although the responses of trees to flooding seem to be manifold, variability within an ecosystem is greater than that between ecosystems despite widely differing species/genera/families dominating the respective floodplains. Endemic tree species are rare, except in Amazonian floodplains. This may be the outcome of a markedly stable climate over geological time. Future research must address the current paucity of published data on the ecophysiology and adaptations and requirements of trees in the major floodplain forests. Attention also needs to be given to small wetlands along small rivers or in remote places. These areas have been almost totally neglected. Where possible, future studies should adopt methods which will allow comparisons to be made with confidence. Climatic change, increasing prevalence of droughts, alterations to groundwater availability and flooding periodicities make such work increasingly urgent since freshwater floodplain forests are a vital human resource that is under threat. They harbour many fish and mammal species, help moderate widespread flooding of inhabited areas, regulate river levels, improve water quality, act as substantial sinks for carbon and provide timber and non-timber forest products. Improving our understanding of their workings will underpin their preservation and effective future management. Contributions by the authors Both authors contributed to a similar extent in the preparation of this article. Conflict of interest statement None declared.
