Struggle in the flood: tree responses to flooding stress in four tropical floodplain systems

Pia Parolin; Florian Wittmann

doi:10.1093/aobpla/plq003

Struggle in the flood: tree responses to flooding stress in four tropical floodplain systems

Parolin, Pia; Wittmann, Florian 2010-02-22 00:00:00 Background In the context of the 200th anniversary of Charles Darwin’s birth in 1809, this study discusses and aims the variation in structure and adaptation associated with survival and reproductive success in the face of environmental stresses in the trees of tropical ﬂoodplains. Scope We provide a comparative review on the responses to ﬂooding stress in the trees of freshwater wetlands in tropical environments. The four large wetlands we evaluate are: (i) Central Amazonian ﬂoodplains in South America, (ii) the Okavango Delta in Africa, (iii) the Mekong ﬂoodplains of Asia and (iv) the ﬂoodplains of Northern Australia. They each have a predictable ‘ﬂood pulse’. Although ﬂooding height varies between the ecosystems, the annual pulse is a major driving force inﬂuencing all living organisms and a source of stress for which specialized adaptations for survival are required. Main points The need for trees to survive an annual ﬂood pulse has given rise to a large variety of adap- tations. However, phenological responses to the ﬂood are similar in the four ecosystems. Deciduous and evergreen species respond with leaf shedding, although sap ﬂow remains active for most of the year. Growth depends on adequate carbohydrate supply. Physiological adaptations (anaerobic metabolism, starch accumulation) are also required. Conclusions Data concerning the ecophysiology and adaptations of trees in ﬂoodplain forests worldwide are extremely scarce. For successful ﬂoodplain conservation, more information is needed, ideally through a globally co-ordinated study using reproducible comparative methods. In the light of climatic change, with increasing drought, decreased groundwater availability and ﬂooding periodicities, this knowledge is needed ever more urgently to facilitate fast and appropriate management responses to large-scale environmental change. ‘struggle for survival’ has been topical and controversial. Introduction Darwin’s theory of ‘survival of the ﬁttest’ is a synonym During the recent Darwin bicentennial year (2009) and for ‘natural selection’. Darwin asked ‘Can it be doubted, throughout the 151 years since the publication of ‘On from the struggle each individual has to obtain the Origin of Species’ (Darwin, 1859), discussion on the subsistence, that any minute variation in structure, * Corresponding author’s e-mail address: [email protected] AoB PLANTS Vol. 2010, plq003, doi:10.1093/aobpla/plq003, available online at www.aobplants.oxfordjournals.org & The Authors 2010. Published by Oxford University Press. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/2.5/uk/) which permits unrestricted non- commercial use, distribution, and reproduction in any medium, provided the original work is properly cited. AoB PLANTS Vol. 2010, plq003, doi:10.1093/aobpla/plq003 & The Authors 2010 1 Parolin and Wittmann — Adaptive responses of trees to ﬂooding in tropical ﬂoodplain systems habits or instincts, adapting that individual better to new The four large wetlands chosen for our analysis are conditions, would tell upon its vigour and health?’ the Central Amazonian ﬂoodplains of South America, (Darwin, 1842). Accordingly, the present study discusses the Okavango Delta region of Botswana, Africa, the the struggle for life in the forests of large ﬂood-pulsed Mekong ﬂoodplains of South-east Asia and the tropical wetlands in relation to what is known of variations in wetlands of Northern Australia (Fig. 1; Table 1). These structure, physiology and biochemistry that confer resili- ecosystems, each on a different continent, were ence. Contrary to the wisdom of Darwin, we cannot, chosen largely on the following pragmatic grounds. We unfortunately, deal with differences within populations looked for very large tropical freshwater ﬂoodplains because such data are very difﬁcult to obtain for these with forest patches (i.e. trees occurring there naturally) huge ecosystems. Instead, our aim is to bring together where ﬂooding occurs with regularity (the ‘ﬂood pulse’ data on responses of trees to ﬂooding in the freshwater of Junk et al., 1989), is characterized by high amplitudes wetlands of tropical environments, emphasizing the and where it is long-lasting (weeks or months). We were varying responses to different wetland structures and careful not to include areas merely prone to ﬂash ﬂoods ﬂooding conditions extant in tropical freshwater ﬂood- following heavy rain. Our assessments are based on plains of four continents. Although Gopal et al. (2000) many diverse publications and disparate data concern- have published a book on the biodiversity of wetlands ing the effects of ﬂooding on species richness, ecophy- and Junk (1997) produced a review of comparative biodi- siology and distribution of tropical trees. versity in ﬂoodplains around the world, there is no one While selecting our four ecosystems, it soon became publication which focuses on adaptation and survival evident that data are extremely scarce, despite their of trees in tropical wetlands. The present article aims importance for biodiversity and human resources to ﬁll this gap. (Wantzen and Junk, 2000). We were forced to exclude Fig. 1 Map indicating the approximate location of the four chosen ﬂoodplain forests. 2 AoB PLANTS Vol. 2010, plq003, doi:10.1093/aobpla/plq003 & The Authors 2010 Parolin and Wittmann — Adaptive responses of trees to ﬂooding in tropical ﬂoodplain systems Table 1 Characteristics of the four chosen ﬂoodplain ecosystems on four continents with a monomodal ﬂood pulse Central Okavango Delta Mekong Tonle Sap Kakadu Region in Amazonia Northern Australia ... ........... ........... ........... ........... ........... ........... ........... ........... ............ ........... ........... .. ......... ........... ........... ....... Continent South America Africa Asia Northern Australia ′ ′ ′ ′ ′ Geographical position 3815 S, 59858W18830 –208S, 228 –248E138N, 1048E1382 S, 133831 E Latitude 0 19 13 12 Age of ecosystem (Irion 2.4 million years 2.5 million years 7500 years 4000 years et al., 1997; Junk et al., 2006) Height asl (m) 0 – 50 1000 0 – 50 0 – 50 Connected rivers Major river Major river system Major river system Smaller rivers system Floodplain area (km ) 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 8 m Root level ,2m 1m height Flood duration where trees 7 months Several weeks? 6 – 8 months .6 months grow 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 Open savanna to 70 % of large trees and forest cover open areas Tree/canopy height 20 – 30 m 5 – 6 m 7 – 15 m 20 m Woody species (Junk et al., .1000 180 70 21 2006) Number of ﬂood-tolerant .1000 10 15 5 tree species Incidence of endemic tree High Very low Low Low? species Tree species diversity High Very low Few dominant species Low? Human pressure Low Low? Very high (wars; ﬁshing) Minimal Human impacts Timber Subsistence agriculture; Timber; ﬁshing; paddy Cattle grazing; tourism; extraction; ﬁsheries rice mining ﬁshing; cattle ranching Continued AoB PLANTS Vol. 2010, plq003, doi:10.1093/aobpla/plq003 & The Authors 2010 3 Parolin and Wittmann — Adaptive responses of trees to ﬂooding in tropical ﬂoodplain systems Table 1 Continued Central Okavango Delta Mekong Tonle Sap Kakadu Region in Amazonia Northern Australia ... ........... ........... ........... ........... ........... ........... ........... ........... ............ ........... ........... .. ......... ........... ........... ....... Changes Increasing Soil salinization due to tree Dramatic ﬂuctuations Invasion by alien plants incidence and felling; expansion of in water level of and animals; changed severity of agriculture; Mekong River; ﬁre regime; water drought agrarian-degradation; frequent ﬂoods and pollution from predicted degeneration of lower water levels in urban-tourism, mining major vegetation types dry season—an and salinization; sea from increased drying increasing problem level rise (Junk et al., (Ringrose et al., 2002) for farming (IUCN, 2006) 1991). many of the largest wetlands, e.g. the Congo basin in hydrology and climate. By comparing diversity and tree Africa or the Orinoco ﬂoodplains in Venezuela, because responses in four ﬂoodplain ecosystems on different only basic data on hydrology and climatology are avail- continents, we attempt to improve our understanding able, with almost no information on plant distribution, of the factors inﬂuencing the spatial distribution of tree adaptations and ecophysiology. It is important to plants, diversity of species and adaptations, and thus bring attention to such poorly researched wetlands, contribute to our knowledge of tropical wetland which are often inaccessible for social and political ecology. In this way, we hope to assist in the successful reasons but are threatened by the ever-increasing restoration of degraded ﬂoodplains and promote the human population and its need for water, waterways sustainable use and conservation of these highly valu- and hydroelectric power. The destruction is so fast that able ecosystems. we may never learn of the adaptations underpinning the success of the tree species in these areas. Flooding as a stress factor We are aware that differences between the four ecosys- tems are large, especially in respect of the inﬂuence of ﬁre Flooding with freshwater, although less harmful than and salinity. Those which are dominated by grasslands ﬂooding with saltwater, poses a multitude of constraints (Okavango and Northern Australian ﬂoodplains) are sub- on growth, survival and reproduction. Trees are basically jected to regular ﬁre (Heinl et al., 2004, 2006, 2007), terrestrial organisms and, in general, die more readily in whereas in the forest-dominated ﬂoodplains of Amazonia response to ﬂooding than to desiccation (Larcher, 1994). and Mekong, ﬁre plays no signiﬁcant role. In the Oka- Flooding involves inundation of part or all of vango, the high evapotranspiration causes salinity pro- the aboveground structures, whereas waterlogging is blems, which are negligible in the remaining three restricted mainly to inundation of the soil and rhizo- ecosystems. Also, ﬂooding amplitudes vary widely sphere (Colmer and Pedersen, 2008). Totally submerged between the ecosystems, with about 2 m in the Okavango plants have no direct contact with atmospheric oxygen and Northern Australian, 8 m in the Mekong and 15 m in and sunlight is weak or extinguished. Inundated soils the Amazon ﬂoodplains (Table 1). This implies that com- become hypoxic or anoxic within a few hours as the plete submergence of saplings and trees occurs only in combined result of oxygen consumption by respiring the Mekong and Amazon, posing different constraints roots plus micro-organisms and insufﬁciently fast diffu- for plant life than merely waterlogging of roots and sion of oxygen through water to replace the amounts stems (Parolin, 2009). However, our review is readily justi- consumed (Crawford, 1989, 1992; Armstrong et al., ﬁed because the regular ﬂood pulse is a major inﬂuence 1994; Visser et al., 2003). Oxygen depletion in soil is on all ﬂoodplain biology (Junk, 1989; Junk et al., 1989) accompanied by increased levels of entrapped CO , and a dominating stress which requires a suite of adap- anaerobic decomposition of organic matter, increased tations for its survival. solubility of mineral substances, notably iron and Throughout the world, wetland ecosystems are under manganese, and decreased redox potential (Joly and increasing pressure from agriculture, urbanization of Crawford, 1982; Kozlowski, 1984). The resulting chemi- catchment areas, tourism and recreational activities, cally reduced and potentially toxic compounds accumu- construction of impoundments and changes to late, their generation being the result of alterations in 4 AoB PLANTS Vol. 2010, plq003, doi:10.1093/aobpla/plq003 & The Authors 2010 Parolin and Wittmann — Adaptive responses of trees to ﬂooding in tropical ﬂoodplain systems the composition of the soil microﬂora as it responds to needed for survival. With all these constraints, imposed the changing conditions (Ponnamperuma, 1984). In by ﬂooding, this stress is clearly life-threatening for some ﬂoodplains, e.g. those of the Amazon River, sedi- higher plants. The struggle for survival of ﬂooding is mentation rates can be extremely high and the depo- therefore closely linked to the evolution of physiological, sition of sediment can decrease soil aeration and thus phenological, anatomical and morphological adap- favour oxygen shortage in the rhizosphere (Wittmann tations that confer tolerance and underpin successful et al., 2004; Wittmann and Parolin, 2005). Elevated and vigorous growth and fecundity despite the intense decomposition rates of highly productive ﬂoating stress. and non-ﬂoating macrophytes in ﬂoodplains further decrease oxygen concentrations in the ﬂoodwater Floodplain ecosystems (Armstrong et al., 1994). In temperate zones, ﬂooding frequently occurs during Here we characterize four extensive ﬂoodplain ecosys- winter when plants are dormant and light intensities tems present on four continents (Table 1). They include low. In contrast, the ﬂooding period in tropical ﬂood- the Central Amazon ﬂoodplains (where we have the plains occurs when temperatures and light intensities broadest and deepest knowledge of tree ecophysiology), are high and conditions overall are optimal for plant the Okavango Delta in Africa, the Mekong ﬂoodplains in growth. Therefore, the trees are not dormant and must South-east Asia (where relatively little is known about accommodate shortages of oxygen and, for submerged tree ecology) and the Northern Australian ﬂoodplains shoots, shortages of CO too at a time when conditions (where much is known about the herbaceous vegetation, favour fast respiration and depletion of reserves. This but much less about tree responses to freshwater implies that extraordinarily efﬁcient adaptations are 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 Mekong Tonle Kakadu Region in Delta Sap Northern Australia ... ........... ........... ........... ........... ........... ........... ........... ........... ............ ........... ........... .. ......... ........... ........... ....... Continent South America Africa Asia Northern Australia Tree distribution Zonation of trees along the Yes Yes Yes Yes ﬂooding gradient Degree of endemism Elevated Low/absent Low/absent Low/absent Leaf phenology Deciduous species: leaf shedding Yes No Yes ? at high waters Evergreen species Yes Yes Yes ? Reproductive phenology Linked to high water + ﬁsh ? Linked to high ? water + ﬁsh Physiological adaptations Reduction of metabolism and Yes No Yes? ? growth during high waters Morpho-anatomical adaptations Leaf xeromorphism; hypertrophic ?? ? lenticels; adventitious roots; aerenchyma Biochemical adaptations Increased activity of fermentative ?? ? enzymes; more VOC emission AoB PLANTS Vol. 2010, plq003, doi:10.1093/aobpla/plq003 & The Authors 2010 5 Parolin and Wittmann — Adaptive responses of trees to ﬂooding in tropical ﬂoodplain systems 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 ﬂood- plain forests that cover more than 300 000 km (Irion et al., 1997). The mean annual temperature of 26.6 8C changes little, average rainfall is 2100 mm year (Ribeiro and Adis, 1984) and noon light intensities can 22 21 reach 3000 mmol m s 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 (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 pre- dictable, 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 Fig. 2 Floodplain forests in Central Amazonia at high water. (Parolin et al., 2004; Parolin, 2009). At low water levels, (A) Nutrient-rich white-water va ´ rzea ﬂoodplain forest with drought may be a stress factor for several weeks (Junk, macrophytes in the foreground (Victoria amazonica; Rio 1997; Parolin et al., 2010). Natural ﬁres and salt are Solimo ˜ es near Manaus) and forest in the background. absent from this ecosystem. Although large terrestrial (B) Nutrient-poor black-water igapo ´ ﬂoodplain forest (Rio Negro near Manaus) (Photographs: Pia Parolin). mammals play important roles for tree establishment and distribution in the grasslands of other ﬂoodplains, they play no signiﬁcant role in the Amazonian ﬂoodplain ecotourism, however, provide sustainable management (Junk and da Silva, 1997). that partially limits the threats to this ecosystem. The differing origins of the various tributaries of the Tree vegetation Amazonian freshwater ﬂoodplains Amazonian River system can strongly inﬂuence water harbour the most species-rich ﬂoodplain forests in the chemistry, e.g. sources in the western Amazon Andes world (Wittmann et al., 2006). In the nutrient-rich or the Northern and Southern Amazonian Precambrian white-water va ´ rzea, there are more than 1000 shields. The resulting seasonally ﬂooded vegetation ﬂood-tolerant tree species (Fig. 3; Wittmann et al., can roughly be differentiated into the nutrient-rich and 2006). From igapo ´ , the comparatively low number of highly productive white-water ﬂoodplains (varzea) and inventories still does not allow reliable estimates of the nutrient-poor and less productive black-water or overall species richness. However, comparisons from clear-water ﬂoodplains (igapo ´ ) (Fig. 2; Sioli, 1954; both local and basin-wide scales indicate less species Prance, 1979). In Central Amazonia, both ﬂoodplain richness than in the va ´ rzea (Prance, 1979; Ferreira types undergo seasonal water-level changes of up to et al., 2005; Wittmann et al., 2010). Species-poor 10 m (Fig. 3). Trees establish at mean annual ﬂood levels ,7.5 m, corresponding to ﬂooded and/or water- low-lying forests (low va ´ rzea) are remarkably similar throughout the Amazon basin even when separated by logged periods of up to 300 days year (Wittmann et al., 2004, 2006). long distances. Species-rich high-va ´ rzea forests may be Human impact on Amazonian ﬂoodplains is increasing more ﬂoristically distinct, but share 30 % of their tree due to agriculture, cattle and buffalo farming, logging, species with the adjacent uplands (Wittmann et al., civil construction projects, mining and reservoirs for hydro- 2006). Tree species richness and alpha-diversity of electric power (Junk, 2000). Small-scale multiple uses and va ´ rzea forests are signiﬁcantly correlated to ﬂood 6 AoB PLANTS Vol. 2010, plq003, doi:10.1093/aobpla/plq003 & The Authors 2010 Parolin and Wittmann — Adaptive responses of trees to ﬂooding in tropical ﬂoodplain systems river catchment, the tree ﬂora of the va ´ rzea and igapo ´ differ substantially in species composition and diversity (Prance, 1979; Kubitzki, 1989). Comparisons at local and basin-wide scales suggest ﬂoristic similarities between both ecosystems to be ,20 % (Wittmann et al., 2010). The main reason for the diverging ﬂora is the contrasting nutrient level. This seems to act as a dis- tribution barrier for many white-water species migrating to the igapo ´ and vice versa. In addition, alluvial dyna- mism varies, with the white-water ﬂoodplains being highly dynamic systems where constant processes of sedimentation and erosion create a large variety of micro-habitats, thereby increasing biodiversity (Salo et al., 1986; Kalliola et al., 1991; Wittmann et al., 2004). Flooding tolerance and tree distribution There is a clear zonation of plant communities in the Amazonian va ´ rzea along the food-level gradient, which leads to characteristic species associations and forest types. Two main habitats are differentiated (Wittmann et al., 2002): (i) low-varzea forests, inﬂuenced by mean inundations with heights between 3.0 and 7.5 m (corresponding to a mean inundation period of 50 – 230 days year ) and (ii) high-va ´ rzea forests, inﬂuenced by mean inundations with heights of ,3.0 m (,50 days year ). However, the distribution of va ´ rzea tree families differs considerably between low- and high-varzea forests (Wittmann et al., 2006): Fabaceae, Malvaceae, Salicaceae, Urticaceae Fig. 3 Varzea ﬂoodplain forests in central Amazonia at low and Brassicaceae are more important in low-varzea water (Photographs: Florian Wittmann, Max-Planck-Institute forests, whereas Euphorbiaceae, Moraceae, Palmae, for Chemistry, Mainz, Germany). Annonaceae, Meliaceae and Myristicaceae are more important in high-va ´ rzea forests. The clear zonation of tree species along the ﬂood gra- height and length, and to the age of the forest stand ´ ´ dient in both Amazonian igapo and varzea indicates the (Wittmann et al., 2006). Maximum species richness different levels of acclimation and adaptation that these estimated from trees ≥10 cm in diameter at breast species have evolved in order to cope with the season- height (cm dbh) recorded in high-va ´ rzea forests of ally hypoxic/anoxic sites. Trees may disperse to higher Amazonia amounts to 84 species ha in the eastern ﬂooded sites than the parent trees and establish parts of the basin, 142 species ha in Central during the terrestrial phase, but they often prove to be Amazonia and 157 species ha in the southern part intolerant of the peculiar site conditions or quickly lose of western Amazonia (Wittmann et al., 2010). out competitively to better-adapted species (Wittmann Endemism is highest in highly ﬂooded low-lying forests et al., 2010). Many Amazonian ﬂoodplain tree species and was estimated to account for 39 % of the 186 that tolerate high and prolonged inundation show most common Central Amazonian varzea tree species adaptations against a wide range of potentially stressful (Wittmann et al., 2010). One hundred and twelve conditions. For example, they tolerate high sedimen- (60 %) of the most frequent Central Amazonian varzea tation rates when located near the river channels of tree species are generalists and are also to be found in white-water rivers and also tolerate poorly aerated other neotropical ecosystems. Where ﬂooding does not soils when located in backwater swamps. Furthermore, exceed 210 days year (Junk, 1989), trees are the they often tolerate full sunlight and drought during the dominating life form, whereas in longer-ﬂooded terrestrial phases when low river water levels coincide environments, grasses and macrophytes take over. with seasonally low precipitation. Trees that are success- As a result of the different chemical compositions and ful at highly ﬂooded sites are therefore light-demanding nutrient inputs of the ﬂooding water, depending on the pioneer species which also have a high resprouting AoB PLANTS Vol. 2010, plq003, doi:10.1093/aobpla/plq003 & The Authors 2010 7 Parolin and Wittmann — Adaptive responses of trees to ﬂooding in tropical ﬂoodplain systems capacity (Worbes et al., 1992; Wittmann and Parolin, before the end of the ﬂooded phase and remains high 2005). They also grow quickly and exhibit relatively throughout the terrestrial phase (Parolin, 2000). short life cycles as, for example, in the white-water pio- Morphological adaptations of the root system include neers Salix martiana and Cecropia latiloba (Worbes et al., hypertrophy of lenticels, formation of adventitious 1992; Parolin et al., 2002; Scho ¨ ngart, 2003). These suc- roots, development of aerenchyma, and the deposition cessful pioneer trees modify the local site conditions so of cell wall biopolymers such as suberin and lignin in per- much that new seedlings of the same species are no ipheral cell layers (Schlu ¨ ter and Furch, 1992; Schlu ¨ ter longer able to establish at the same site as the parent et al., 1993; De Simone et al., 2002a, b). Different types tree (Wittmann et al., 2010). of above-ground roots, e.g. plank-buttressing and adven- titious roots, are closely related to ﬂooding duration and Tree responses to ﬂooding The terrestrial phase is the habitat dynamics (Wittmann and Parolin, 2005). The main growth period for trees in the Amazonian development of adventitious roots in the oxygenated ﬂoodplains. In contrast, in the ﬂooded period, growth layer at the surface of the ﬂoodwater table and hyper- decreases, metabolic activity slows and even complete trophy of lenticels on the surface of stems just above dormancy is induced in many species. However, none water level are thought to improve the internal oxygen of these responses lasts for the entire ﬂooding period. status by facilitating the entry of oxygen into the Limited growth lasts for only a few weeks and is often root and the stem by the shortest possible pathway followed by new leaf ﬂush, ﬂowering, fruiting and (Crawford, 1992). Pneumatophores are also familiar wood increment while the tree is still ﬂooded (Worbes, adaptations in mangroves but are absent in va ´ rzea 1997; Scho ¨ ngart et al., 2002). After fruit maturation, trees (Junk, 1984) except in palms found in headwater which usually occurs at high water levels (Kubitzki and regions and swamps (e.g. Mauritia, Mauritiella), where Ziburski, 1994), seeds fall into the water and may ﬂoat ﬂood amplitudes are small. Stem nodulation and nodu- and/or are submerged for several weeks without losing lated adventitious roots have been observed in various their viability. Seed germination starts only when the species, and are understood to be adaptations that ﬂood recedes, although some may protrude a radicle allow legumes to ﬁx nitrogen in a ﬂooded environment (Scarano et al., 2003) or even produce a complete (James et al., 2001). The frequency of such nodulation seedling while ﬂoating (Oliveira-Wittmann et al., 2007; among genera can be higher in ﬂooded than in non- Parolin, 2009). In most species, overall growth in height ﬂooded sites in both va ´ rzea and igapo ´ , indicating that and new leaf production are not severely inhibited nodulation may be favoured in ﬂooded areas (Moreira merely by waterlogging of the soil, and elongation may et al., 1992). even be enhanced, as in Senna reticulata. Here, Increased activity of fermentative enzymes such as waterlogging is reported to accelerate seedling shoot alcohol dehydrogenase (ADH), lactate dehydrogenase growth considerably (Parolin, 2001). (LDH), glutamate – pyruvate transaminase (GPT) and Submergence of part of or the entire shoot is a more malate dehydrogenase (MDH) has been observed under severe stress. Most tree species tolerate this in a state anaerobic soil conditions in the roots of several tree of rest and sprout new leaves soon after the water species (Schlu ¨ ter and Furch, 1992; Schlu ¨ ter et al., 1993; recedes. In species with leaves without a thick cuticle De Simone et al., 2002b). In addition, larger amounts or thick outer epidermis walls, leaves rot fast when sub- of volatile organic compounds are emitted to the merged and are shed after only a few days (Waldhoff atmosphere by terrestrial vegetation when ﬂooded and Furch, 2002). Other species may retain their leaves (Kesselmeier and Staudt, 1999). Acetaldehyde and in a healthy state below water for several months. Leaf ethanol may be emitted in larger amounts by ﬂooded shedding during the aquatic phase has been documen- trees and under other stress conditions such as sulphur ted not only in deciduous species but also in evergreen dioxide and ozone exposure, water deﬁcit, freezing and trees, which tend to produce new leaves only slowly at fast-changing light conditions (Kimmerer and Macdo- high water levels (Parolin et al., 2002). Whether decid- nald, 1987; Kesselmeier et al., 1997). Acetaldehyde (and formaldehyde) is exchanged bi-directionally uous or evergreen, and regardless of whether leaves are kept or shed under water, the leaves of Amazonian between the vegetation and the atmosphere, i.e. they ﬂoodplain trees exhibit traits that are generally con- are emitted or taken up, depending on environmental sidered as xeromorphic (Medina, 1983; Waldhoff, 2003). and atmospheric conditions (Kesselmeier et al., 1997). Physiological responses to waterlogging of the soil Recent measurements in the terra ﬁrme Amazonian include reductions of mean CO uptake in aerial leaves rain forest provide evidence that more short-chain alde- ranging from 10 to 50 % slower than in the terrestrial hydes and the corresponding organic acids were taken phase (Parolin et al., 2004). CO uptake rises again up from the air than produced, although release was 8 AoB PLANTS Vol. 2010, plq003, doi:10.1093/aobpla/plq003 & The Authors 2010 Parolin and Wittmann — Adaptive responses of trees to ﬂooding in tropical ﬂoodplain systems observed when ambient concentrations were below a speciﬁc level (Rottenberger et al., 2008). Africa: Okavango Delta The Okavango Delta (Fig. 4) is the world’s largest inland delta. It is located in northwestern Botswana and fed by the Okavango River, which originates in Angola’s western highlands. The ﬂoodwaters take 9 months to ﬂow from the source to the delta due to the extremely gentle gradient. The river discharges about 10 km of water onto the delta fan each year, augmented by 3 2 about 6 km of rainfall, which sustains about 2500 km of permanent wetland and up to 8000 km of seasonal wetland. Interaction between this surface water and the groundwater strongly inﬂuences the structure and function of the wetland ecosystem. The climate is semi- arid, and only 2 % of the water leaves as surface ﬂow and probably very little as groundwater ﬂow. The bulk of the water is lost to the atmosphere. The Okavango River also delivers about 170 000 tonnes of bedload sediment and about 360 000 tonnes of solutes to the delta each year, most of which is deposited on the fan. Local rainfall is low, averaging 490 mm year . This is greatly exceeded by the rate of evapotranspiration (1580 mm year ; Ellery et al., 1993). Temperatures range from maxima of 33.7 8C in summer to 28.7 8C in winter, with a mean relative humidity of 60 – 78 % in summer and 43 – 63 % in winter (Bonyongo et al., 2000). Precipitation data show ,10 mm of rainfall per month from May through October, whereas between January and March, it lies between 120 and 320 mm. The Okavango Delta experi- ences seasonal ﬂooding starting towards the north between October and April, and ending in May, June or July towards the southern part of the delta. Natural ﬂuc- tuations in water level result from variations in annual rainfall in the catchment area and rainfall within the delta itself (Bonyongo, 1999). The delta is almost perma- nently ﬂooded in the north, but only seasonally ﬂooded in the south. The rain falls during the summer and ﬁrst seeps into the parched ground before the rivers start ﬂowing. As it is the dry season, the ﬂoodwaters gradually evaporate Fig. 4 Forested savanna in the Okavango Delta with mopane over the subsequent months, leaving their valuable trees (C. mopane) at high and low water (Photographs: Michael Heinl, University of Innsbruck, Austria). salts and minerals in the ground. Fire plays a role in this ecosystem (Heinl et al.,2004, 2006, 2007). It is more frequent in the ﬂoodplains than adapted plants. As a consequence, locally high biological on the drylands because of greater biomass and fuel load. The incidence of ﬁre on the drylands correlates productivity occurs, which, in turn, supports many with annual rainfall events, while the frequency of grazing mammals (Heinl et al., 2004, 2006, 2007; ﬁres on ﬂoodplains is determined mostly by ﬂooding Tacheba et al., 2009). frequency. The greatest burn potential is found on ﬂood- Changes in the types of vegetation cover, due to both plains that become ﬂooded every second year. Temporal human and natural causes, have taken place since the variations in ﬂooding cause accumulation and sudden ﬁrst vegetation map was produced in 1971 (Ringrose et al., 2002). In the south-west, shifts to thorn trees mobilization of nutrients which are readily utilized by well- AoB PLANTS Vol. 2010, plq003, doi:10.1093/aobpla/plq003 & The Authors 2010 9 Parolin and Wittmann — Adaptive responses of trees to ﬂooding in tropical ﬂoodplain systems prevail, whereas in the eastern part of the country, wide- nutrient and sediment supply and sediment deposition, spread bush encroachment takes place. An increased and with the nature of the substratum, play a role human population density suggests that these are (Ellery and Tacheba, 2003). Trees, which are almost anthropogenic (agrarian-degradation) effects. Wherever exclusively conﬁned to islands, are particularly broadleaved evergreen trees are cleared, widespread important as they lower the water table beneath salinity occurs (Ellery et al., 2000). In the sparsely islands relative to the surrounding wetlands and settled central Kalahari region, changes from tree cause a net inward ﬂow of groundwater (McCarthy, savanna to shrubs may indicate the inﬂuence of 2006). Island fringes are generally characterized climate change with the associated effects of ﬁres and by a broadleaf evergreen riparian community of local adaptations. Projection of future vegetation Syzigium cordatum, Ficus verruculosa, F. natalensis, changes to about 2050 indicates degeneration of the F. sycamorus, Phoenix reclinata, Garcinia livingstonei major vegetation types due to expected drying of the and Diospyros mespiliformis. This gives way to local climate (Ringrose et al., 2002). interiors dominated by Acacia nigrescens, Croton megalobotrys and Hyphaene ventricosa.The most Tree vegetation The ﬂoodplains consist mostly of central regions are characterized either by short, grasslands with 1250 species (Ellery and Tacheba, 2003). sparse grassland dominated by Sporobolus spicatus or Woody plants are found in the riverine forests (e.g. are completely devoid of vegetation with sodium species of Ficus). On the higher, often salt-rich islands carbonate (trona)-encrusted soil surrounding a central which are ﬂooded less frequently, acacias, mopane pan of extremely high conductivity (Ellery et al., (Colophospermum mopane; Fig. 4) and the woody shrub 1993). Soil pH and mineral content (especially Pechuel-loeschea leubnitziae (a weed in many sodium) and groundwater chemistry (conductivity and ecosystems) predominate. Ellery and Tacheba (2003) pH) play a major role in the spatial distribution of reported 43 woody species in total in the dryland plant communities. However, Bonyongo et al. (2000) riverine woodland. None of these is endemic since most state that the timing and duration of the seasonal of them also occur in South Africa and Namibia ﬂooding are the most important factors determining (M. Heinl, University of Innsbruck, Austria, pers. comm.). the species composition of the vegetation. Despite an overall high plant species diversity in the delta, only 18 % of the vegetation is phanerophytes Tree responses to ﬂooding The riparian trees remain (trees), compared with 56 % hemicryptophytes and 8 % green all year and partly sustain their growth as a result true aquatic species (Ellery and Tacheba, 2003). of groundwater uptake in the dry periods. Riverine Although seldom ﬂooded, the riparian woodland trees forests in savanna areas depend on the river for their have their roots in the water table in permanent and water supply (Hughes, 1988). Flooding and lateral seasonal swamps (Ellery and Tacheba, 2003). Acacias groundwater ﬂow stimulate growth (Ringrose, 2003). and mopane are less ﬂood tolerant with pechuel Renewal of leaf growth, however, is primarily related to showing greater tolerance of ﬂooding, and also of ﬁre. rainfall, not to ﬂood events in the distal delta (Ringrose, Riparian woodlands are responsible for much of the 2003). Regenerative phenology has not yet been water lost from the ecosystem and deplete groundwater described for the trees of the Okavango Delta. In by transpiration (Ringrose, 2003). This leads to the general, however, riverine forests in African savannas uptake of toxic solutes by the transpiring trees, which show a high percentage of even-aged stands of trees, results in exceptionally good quality surface water. The indicating that hydrological factors are important for trees therefore ensure that islands of vegetation func- tree regeneration because they provide spasmodically tion as ‘kidneys’ within the landscape—a reason why favourable circumstances for establishment (Hughes, riparian woodlands are considered particularly impor- 1988). Although there are some data on the phenology, tant habitats in this ecosystem (Ellery and Tacheba, growth rhythms, physiological responses and 2003). morphological adaptations to ﬂooding in the non- Flooding tolerance and tree distribution Vegetation on woody vegetation (Ellery et al., 1992; Mantlana, 2008), islands in the perennial swamps of the Okavango Delta almost no published data were found for trees in the exhibits a marked zonation (Ellery et al., 1993). This is Okavango Delta. An exception is a recent study of leaf related primarily to aspects of the hydrological regime gas exchange of C. mopane in northwest Botswana such as depth, duration and timing of inundation, but (Veenendaal et al., 2008). Here, differences in mainly to soil and groundwater salinity (Ellery and physiological and morphological traits between tall and Tacheba, 2003). Also, processes associated with short forms of mopane [C. mopane (Kirk ex Benth.) Kirk 10 AoB PLANTS Vol. 2010, plq003, doi:10.1093/aobpla/plq003 & The Authors 2010 Parolin and Wittmann — Adaptive responses of trees to ﬂooding in tropical ﬂoodplain systems ex J. Le ´ onard] trees were compared. The tall form had a smaller leaf:ﬁne-root biomass ratio, higher leaf nitrogen concentrations and less negative leaf water potentials. These differences appeared to be attributable to differences in root depth and density between the physiognomic types, and thus to different ways that the two growth forms exploit available soil water, the tall form having a consistently more conservative water-use strategy as the dry season progressed than the short form (Veenendaal et al., 2008). Asia: Mekong ﬂoodplains The Mekong is the world’s eighth-longest river (Sarkkula et al., 2005). The lower Mekong basin in Cambodia and Vietnam includes ﬂoodplains (Fig. 5) which are among the few remaining global examples of relatively intact Fig. 5 Asia: Mekong ﬂoodplains in Giang Province at high and functioning ﬂoodplains in a large river basin. This water (Photographs: Manfred Niekisch, Zoological Garden is the case despite its high-density human population Frankfurt, Germany). of 54.8 million. It is widely accepted that this is one of the explanations for the highly productive ﬁsheries of the Mekong and its very high biological diversity. The ﬂoodplains cover 795 000 km (Sarkkula et al., 2005). large hydroelectric dams (Wikramanayake and Rundel, Since the only available data on tree ecophysiology 2002). An additional threat is the invasion of the come from Tonle Sap Lake, which is fed by the Mekong giant mimosa (Mimosa pigra). This aggressive shrubby River, we concentrate on the 15 000 km of ﬂoodplain species becomes established in fallow ﬁelds and dis- forest of this lake. turbed shrub land and swamp forest area after clear- At the peak of the wet season, the Tonle Sap can ance or burning. Once established, giant mimosa expand to 250 km long and up to 100 km wide in forms dense, impenetrable thickets of spiny growth places. The lake is shallow, measuring only 1 – 2 m at that choke out other native species and have little its deepest in the dry season, rising to more than 10 m value as wildlife habitat. in the wet season. As a result, when it ﬂoods, the total Tree vegetation The swamp shrub lands and forest of inundated area increases 4-fold. Mean annual rainfall the Tonle Sap Freshwater Swamp Forests eco-region is 1600 mm. Much of this eco-region is ﬂooded for at include two forest associations that have been least 6 months—from August to January or February described for the extensive ﬂoodplain area of Tonle (Wikramanayake and Rundel, 2002). Sap. This is a short-tree shrub land covering much of Most of the delta’s human inhabitants ﬁsh, farm and the area and comprises a stunted swamp forest live at subsistence levels. Although the annual ﬂood around the lake itself. Similar swamp forests are also cycle of the Mekong provides resources for these present along the ﬂoodplains of the Mekong and other people, it is a fragile balance. The ﬂoodplains of the major rivers in Cambodia (Wikramanayake and Rundel, Tonle Sap have been strongly affected by human 2002). Swamp forest originally dominated the activity and little of the original forest cover remains dry-season shoreline of Tonle Sap, covering about 10 % pristine. Throughout the dry season, burning is of the ﬂoodplain. It occurred in a mosaic of patch common, with ﬁres used to clear land before ploughing stands rather than as continuous forest stands or to facilitate access. Flooding has recently damaged (Wikramanayake and Rundel, 2002). Typically, these the infrastructure and caused extensive loss of property forests are ﬂooded for 6 – 8 months each year and and livelihood. At the same time, roads and their most species lose their leaves during this time. A associated developments have had a considerable continuous canopy 4 m high is formed by the impact on ﬂooding by fragmenting the wetlands and interrupting the natural ﬂow of water, sediments, dominant deciduous woody species. The most common species belong to the Euphorbiaceae, Fabaceae and nutrients and aquatic life. These impacts negate the beneﬁcial effects normally brought by the natural Combretaceae together with Barringtonia acutangula ﬂood cycle. The most signiﬁcant threat comes from and Diospyros cambodiana. Terminalia cambodiana is infrastructure development, particularly 149 planned an important local endemic. The forest vegetation is AoB PLANTS Vol. 2010, plq003, doi:10.1093/aobpla/plq003 & The Authors 2010 11 Parolin and Wittmann — Adaptive responses of trees to ﬂooding in tropical ﬂoodplain systems dominated by the ﬂood-tolerant tree Melaleuca cajuputi 2004). These ﬂoodplains are in an area broadly known as ssp. cumingiana (Safford et al., 2009). The swamp forest the ‘wet – dry tropics’. These have been deﬁned as areas is 7 – 15 m high. Although M. cajuputi may reach 40 m in with an annual rainfall of 600 – 1600 mm spread over Australasia, in the Mekong ﬂoodplain trees are no taller 4 – 7 months. The size of forested wetlands comprises 2900 km . There is a wet season characterized by thun- than 22 m even when 100 years old (Safford et al., derstorms, tropical cyclones and rain depressions. These 2009) and most commonly form bushes 3 – 6 m tall. commence late in the year (November – December) and Flooding tolerance and tree distribution Little last for 3 – 4 months (Taylor and Tulloch, 1985). The information is available on plant distribution and hydrological cycle has been identiﬁed as being impor- zonation along the Mekong River ﬂoodplains. In the tant in shaping the pattern of the vegetation in the Tonle Sap ﬂoodplain, the structure and composition of freshwater wetlands (Finlayson et al., 1989). Water woody vegetation appear to be largely a function of ﬂows on a seasonal basis, starting early in the wet the micro-heterogeneity of soil moisture and seasonal season and lasting until after the end of the rains. Flood- ﬂood dynamics. Tree height is related to soil moisture ing occurs once the catchment is saturated; heavy falls conditions, with the tallest trees growing closer to the of rain later in the season generate more widespread permanent lake basin and shorter ones at the ﬂooding. Freshwater ﬂow in the creeks and rivers periphery of the ﬂoodplain. Several species with ceases within a few months of the end of the rains, shrubby growth forms in this peripheral community and the creeks and ﬂoodplains dry out except for a few reach tree size in swamp forest habitats permanent swamps and billabongs (Finlayson et al., (Wikramanayake and Rundel, 2002). 1990). Some creeks or river reaches are fed by springs or groundwater seeps. Analyses of the water quality Tree responses to ﬂooding In the Mekong ﬂoodplains, within thick stands of submerged herbs and emergent the terrestrial phase is the main growth period for grasses late in the wet season reveal that, in addition trees. Most woody species of the ﬂoodplain of Tonle to variations in dissolved O and CO concentrations, 2 2 Sap are deciduous, a probable adaptation to the the water becomes alkaline in the late afternoon when periodic ﬂood pulse (Safford et al., 2009). Rather than CO concentrations are at their lowest. lose their leaves in the dry season, however, these Fire and invasive plants and animal species have a sig- species lose their leaves when submerged as the lake niﬁcant impact on the extent and distribution of plant deepens and the plants become partially or totally species and of the land cover (Finlayson et al., 1990). submerged. However, there are several woody species Damage to the natural levees that separate freshwater that remain evergreen (Lamberts and Koponen, 2008), and saline wetland communities caused by climate despite leaves being submerged for 6 – 8 months each change and by feral animals (especially water buffalo) year. With only a few exceptions, ﬂowering and fruit may also change the vegetation. Notable responses by production in the ﬂoodplain trees and shrubs are ﬂoodplain vegetation have already occurred following delayed for several months after the ﬂush of the removal of feral buffalo (Skeat et al., 1996). new leaves. Fruits reach maturity at the time of Tree vegetation Around 55 % of the terrestrial vegetation submergence, suggesting that ﬁsh may be important in the Kakadu Region is tropical tall grass savanna, dispersal agents (Safford et al., 2009). Unfortunately, composed of eucalypt-dominated open forest and no data on physiological responses to ﬂooding and woodland with a 1- to 2-m-tall grassy understorey morphological adaptations of the Mekong ﬂoodplain (Finlayson, 2005). A further 30 % of the region is covered tree species were found. There are some publications by heaths, and open woodlands with a sparse grass on the ecophysiology of non-ﬂooded environments, understorey. Closed-canopy monsoon rainforests are mainly dealing with drought-prone deciduous and dry restricted to ﬂoodplains, besides lowland springs, rock evergreen tropical forests (Tanaka et al., 2004; Ishida outcrops and beach levees. The seasonally inundated et al., 2006; Huete et al., 2008). Few, if any, studies ﬂoodplains include fringing woodland and forests, and describe the responses of trees typical of the Mekong billabongs (seasonally or permanently inundated lagoons ﬂoodplain. associated with the ﬂoodplain or river channels) Australia’s tropical ﬂoodplain wetlands (Finlayson, 2005). The forests are inundated by up to 1 m Floodplain wetlands are uncommon in the mostly arid of water during the wet season but are dry at other times. continent of Australia. However, an important partly Gallery and ﬂoodplain forests in monsoonal Northern forested wetland, the Kakadu National Park in Northern Australia are mostly sclerophyllous and dominated by Australia, extends over 99 000 km (Lowry and Finlayson, ﬁve closely related species of Melaleuca (Myrtaceae), 12 AoB PLANTS Vol. 2010, plq003, doi:10.1093/aobpla/plq003 & The Authors 2010 Parolin and Wittmann — Adaptive responses of trees to ﬂooding in tropical ﬂoodplain systems among which niche differentiation is unclear (Franklin environment. They noted that variability due to changes et al., 2007). The most important tree communities in the hydrological cycle has resulted in many speciﬁc (Finlayson, 2005) include Melaleuca open forest and adaptations that enable the plants to establish and grow woodland with a tree canopy cover of 10 – 70 %. These (Finlayson et al.,1989). The few details given include that are dominated by one or more Melaleuca species trees of the ﬂoodplains often have modiﬁed bark (M. viridiﬂora and M. cajaputi around the edges and at structures such as the corky bark of Sesbania formosa the northern end of the ﬂoodplain). The dominant and B. acutangula, and the distinctive papery bark of species in the backswamps that are inundated for 6 – 8 some melaleucas which possesses internal, longitudinal, months every year is M. leucadendra. There is also gas-ﬁlled passages. It is also said that the majority of open woodland providing canopy cover of ,10 % domi- seed-dispersal mechanisms involve water, even though nated by M. leucadendra. There are 12 terrestrial tree many parts of the ﬂoodplains are drier for a longer species, including Eucalyptus spp., Pandanus spiralis, period than they are wet. However, it is not clear if this Lophostemon lactiﬂuus and Syzygium suborbiculare. also applies to trees. Nothing seems to be known of the Paperbark swamp forest is dominated by trees including physiological and morphological adaptations of trees of M. viridiﬂora, M. cajaputi and M. leucadendra, and to a the Kakadu National Park. Responses to ﬂooding by lesser extent B. acutangula and Pandanus spp. melaleucas of North Queensland have, however, been The productivity of the ﬂoodplain vegetation changes documented and these may be relevant to the Kakadu with the annual cycle. This is indicated by periodic litter- since this is an environment with a median duration of fall from Melaleuca trees. In an intensively sampled inundation of 75 days (McJannet, 2008). Using a Melaleuca forest on the Magela ﬂoodplain, total litterfall heat-pulse method, McJannet found a strong 22 21 was 0.7 kg m year , whereas at a second site on relationship between tree size and tree water use, and the ﬂoodplain, less intensively investigated, a value of showed that transpiration by M. quinquenervia was 22 21 1.5 kg m year was recorded (Finlayson, 1988). unaffected by inundation. This ability to transpire during Comparative data for Melaleuca forests are limited to a ﬂooding may be due to physiological adaptations of this small number of studies of different species found in species, and to dynamic root systems that can quickly the wetlands in southern Australia. These deposit an respond to rising and falling water tables and dense 22 21 annual litterfall of 0.39 – 0.43 kg m year (Finlayson networks of ﬁne ageotropic roots, which grow on and et al., 1993). The distribution and density of trees on at within the papery bark. Waterlogged M. quinquenervia least part of the ﬂoodplain were seen to change con- also develops negatively gravitropic roots (Sena Gomes siderably between 1975 and 1990 (Finlayson, 2005), indi- and Kozlowski, 1980). cating the dynamic nature of the wetland environment. A study by O’Grady et al. (2006) of Corymbia bella and M. argentea in riparian zones of the Northern Territory, Flooding tolerance and tree distribution The duration of along the Daly River, showed that throughout the dry ﬂooding, depth of water and the velocity of water ﬂow are season predawn leaf water potentials were above major determinants of the vegetation composition of the 20.5 MPa, indicating that neither species suffered sig- ﬂoodplain (Finlayson et al., 1989). The changing pattern is niﬁcant unrelieved water-deﬁcit stress during the dry a function of both the ﬂooding and drying phases of the season. This was despite low soil matric potentials in hydrological cycle (Finlayson et al., 1989, 1990). The the top 1 m of soil. There were also no seasonal differ- vegetation of the ﬂoodplain billabongs is much ences in tree water use in either species. Xylem sap deu- inﬂuenced by adjacent plant communities on the terium concentrations indicated that M. argentea trees seasonally inundated ﬂoodplain (e.g. grass mats along the riverbank relied principally on river water or extending across the ﬂoodplain and into the billabongs). shallow groundwater, whereas C. bella growing along Franklin et al. (2007) propose that Melaleuca forests the levee was reliant on deep soil water reserves occur where disturbance by ﬁre and/or ﬂoodwater is too (O’Grady et al., 2006). This study demonstrates strong great for rain forest to persist, making them the wetland gradients of tree water use within tropical riparian com- analogue of the eucalypt species that dominate the munities in Northern Australia which probably can be better-drained parts of north Australia. extrapolated to the Kakadu Region. Tree responses to ﬂooding Little information is available on physiological responses and adaptations of trees in Discussion Australian ﬂoodplains. Cowie et al. (2000) have reviewed adaptations in wetlands by herbs and macrophytic We have demonstrated that in all tropical continents, vegetation, and summarized the nature of the ﬂoodplain highly adapted tree species populate the ﬂoodplain. AoB PLANTS Vol. 2010, plq003, doi:10.1093/aobpla/plq003 & The Authors 2010 13 Parolin and Wittmann — Adaptive responses of trees to ﬂooding in tropical ﬂoodplain systems There is little taxonomic overlap except for the Asian and an alternative, albeit inefﬁcient, alternative source of Australian ﬂoodplain where the genus Melaleuca domi- energy to Krebs cycle-based aerobic respiration nates, but Barringtonia also occurs in both ecosystems. (Crawford, 2003). Induction of the activity of fermenta- Forest types range from highly diverse dense forests tive enzymes such as ADH, LDH, GPT and MDH has (Amazonia, Mekong) to gallery forests or small tree been observed under anaerobic growth conditions in stands scattered in savanna-dominated environments Amazonian tree species (Schlu ¨ ter and Furch, 1992; (Okavango, Kakadu Region). In each ﬂoodplain, the Schlu ¨ ter et al., 1993; De Simone et al., 2002a; Ferreira, aquatic phase occurs when temperature and light con- 2002), and this probably also applies to species of the ditions are optimal for plant growth and development, Okavango, Mekong or Kakadu regions. implying the need for developmental and biochemical Underwater photosynthesis is common in temperate adaptations rather than relying on avoidance through herbs (Mommer and Visser, 2005) and postulated for dormancy (Parolin et al., 2004). Flooding patterns vary, some tree species in Amazonian ﬂoodplains (Schlu ¨ ter with durations ranging from more than half a year et al., 1993; Waldhoff et al., 2002; Parolin, 2009). It is (Amazonia, Mekong, partly Kakadu) to only a few weeks possible that underwater photosynthesis, which both (Okavango). The most important characteristic is the pre- increases internal oxygen concentrations and raises dictability of the time of the annual ﬂood (the ﬂood pulse energy supply, could partially alleviate the adverse concept of Junk et al., 1989). This predictability has effects of submersion. This may well be of adaptive sig- allowed the trees to form morphological and physiologi- niﬁcance in the trees of the Mekong ﬂoodplains where cal adaptations against ﬂooding. On the other hand, as ﬂood heights can exceed 2 m and might be associated a consequence of the differing ﬂood intensities and differ- with periods of complete submergence. ent ﬂooding tolerance of the plants along the ﬂooding In the four ﬂoodplains that we examined, the terres- gradient, tree distribution presents clear zonations in all trial non-ﬂooded phase is when tree growth is most vig- orous. However, many tree species retain actively four ecosystems. However, our wish to compare the underlying physiological and morphological reasons for ﬂowing phloem sap even during ﬂooding (Waldhoff this zonation was frustrated by a lack of relevant pub- et al., 2002; Visser et al., 2003), indicating that active lished data. A small number of species from the Asian, sources and sinks for respirable substrates operate African and Australian ﬂoodplains have been analysed under these conditions. A set of metabolic adaptations to date, and the dearth in our knowledge is alarming in is inevitably required to achieve this. We suggest that in the face of the speed at which the ﬂoodplains are being most tree species of the tropical ﬂoodplains, the damaged or destroyed and the pressing need for well- primary morphological strategies in response to ﬂood- informed recovery programmes. ing are similar to those of temperate species (Jackson Clearly, it is difﬁcult to be sure of the extent to which and Armstrong, 1999) or in the well-analysed tropical trees in the four ecosystems share similar underlying Amazonian ﬂoodplains (Parolin et al., 2004, 2010). In adaptations to ﬂooding stress. Phenological data indi- particular, there must be a development of gas-ﬁlled cate that this may be the case. For example, many spaces in the roots and stems to allow diffusion of deciduous species respond to ﬂooding with leaf shed- oxygen from the aerial portions of the plant into the ding, presumably as a means of reducing transpiration roots. Morphological adaptations that favour this are and water loss at a time when hypoxic or anaerobic hypertrophy of lenticels, formation of adventitious roots may offer large resistances to water uptake. roots, plank-buttressing and stilt rooting, development However, evergreen species are common in each of the of aerenchyma, and the deposition of cell wall biopoly- ﬂoodplains that we examined with the exception of mers such as suberin and lignin in the root peripheral the Australian wetlands. This indicates the possibility cell layers. The formation of aerial roots may compen- that other mechanisms exist to reduce transpirational sate for losses of respiration and function by roots losses, although here too a proportion of the leaves of affected by lack of oxygen in the soil. Under experimen- evergreen trees is also lost during ﬂooding. tal conditions with stable water levels, most species Physiological adaptations similar to those well known show the potential to produce adventitious roots. But, in temperate and Amazonian species can also be in the ﬁeld, they are seldom found, probably because expected in the tree species of the Mekong, Okavango their formation is hampered by a rapidly changing and Kakadu ﬂoodplains. Among the most important water level. Leaves of tropical forests in general, and will be root system adaptations to anoxia (Crawford, the Amazonian ﬂoodplain forests in particular, com- 2003; Gibbs and Greenway, 2003). These will include monly have xeromorphic structures (Waldhoff, 2003). the accumulation of adequate carbohydrate reserves This attribute contributes to suppressing water loss at and the ability to switch to alcoholic fermentation as times of low water supply. This can apply to tree 14 AoB PLANTS Vol. 2010, plq003, doi:10.1093/aobpla/plq003 & The Authors 2010 Parolin and Wittmann — Adaptive responses of trees to ﬂooding in tropical ﬂoodplain systems crowns during the aquatic phase and to periods of Conclusions and forward look drought in the terrestrial phase. Our comparative review on the adaptive responses of Strict comparability between the four ecosystems we trees to ﬂooding in four tropical freshwater ﬂoodplains studied is limited by region-speciﬁc constraints such as of different continents demonstrates that substantial the inﬂuence of groundwater quality and the incidence data about the ﬂoodplain tree ﬂora, its ecology of ﬁre and/or salt. These constraints might also be and functioning are lacking. Despite many physio- responsible for the large differences in tree diversity ecologically motivated studies on trees of the Central encountered in the four ecosystems. It is also true Amazonian ﬂoodplains, and a few studies on other tropi- that the two forested ﬂoodplains also exhibit striking cal freshwater ﬂoodplains, we are still only at the start of differences in their diversity. Tree species richness in our understanding of how terrestrial plants, especially the Amazonian white-water ﬂoodplains (va ´ rzea) is trees, cope with extended periods of ﬂooding. However, 10 times greater than that in the forests of Cambodia this knowledge is fundamental to understanding the (Tonle Sap; Campbell et al., 2006) and about three times evolution of ﬂooded landscapes and their organisms, above that in the Brazilian Pantanal, another extensive as well as their interaction with non-ﬂooded ecosystems. wetland dominated by savannah (Wittmann et al., The range of plant responses recorded in the different 2006). One reason for the comparatively high tree tropical ﬂoodplains leads us to the following conclusions: species richness in varzea forests of Amazonia is the coexistence of species well adapted to ﬂooding and generalist species that also occur in the uplands (Witt- (i) Regular ﬂooding is a severe stress to trees, resulting in reduced species richness compared with non- mann et al., 2006). Very little is known about the ﬂooded uplands. number of generalists vs. specialists among ﬂoodplain (ii) The regular ﬂood pulse has given rise to a large trees. In Amazonia, only a few tree species occur diversity of growth forms and adaptations by along the whole ﬂooding gradient, with most being trees. These seem to increase in variety with the restricted to very small topographic amplitudes (Witt- age of the respective ﬂoodplains and the climatic mann et al., 2002). Only 20 % of all va ´ rzea tree species occur in both low- and high-land habitats, stability to which they were exposed. (iii) Most ﬂoodplain tree species are restricted to small demonstrating the striking difference in ecophysiological topographic amplitudes along the ﬂooding gradi- constraints for tree survival and growth along the ﬂood- ing gradient. In the other ﬂoodplains of the world, gen- ents, leading to a distinct zonation of tree species. This implies different mechanisms or com- eralists may dominate, as in savanna ecosystems. binations of mechanisms conferring zone-speciﬁc However, we have too little information to speculate tolerance to ﬂood stress. This zonation is not about the ecological amplitude of trees in ﬂoodplains. dependent on the height of the ﬂooding amplitude. The degree of ﬂood tolerance depends, in large part, Most highly ﬂooded (.2 m) tree species react to on the time taken to colonize the ﬂoodplains. Morpho- high-water periods with leaf shedding, which is logical adaptations may be remnants of pre- adaptations from non-ﬂooded upland tree species associated with decreased metabolism and growth. (Kubitzki, 1989) which evolved further, leading over (iv) The occurrence of evergreen tree species does not time to highly adapted species. Thus, the phylogenetic development of adaptations depends on the age of depend on the height and magnitude of ﬂooding, since evergreen species are found in all three the ecosystem, and also on the dominating plant ﬂoodplains. families that colonized these ecosystems originally. In (v) Although the responses of trees to ﬂooding seem each of the four ecosystems, there are large differences in developmental age (Table 1). This implies different to be manifold, variability within an ecosystem is greater than that between ecosystems despite stages of adaptations among the organisms living widely differing species/genera/families dominat- there. Amazonian and African ﬂoodplains are extremely old, dating at least to the Pleistocene (.12 million ing the respective ﬂoodplains. (vi) Endemic tree species are rare, except in Amazonian years old), or even earlier. Such ancient landscapes ﬂoodplains. This may be the outcome of a mark- will have experienced several changes in climate and hydrology, i.e. during the glacial and interglacial edly stable climate over geological time. (vii) Future research must address the current paucity of periods. In contrast, the Mekong River basin and the published data on the ecophysiology and adap- Australian ﬂoodplains are much younger, and are tations and requirements of trees in the major thought to be no older than 7500 and 4000 years, ﬂoodplain forests. respectively (Junk et al., 2006). AoB PLANTS Vol. 2010, plq003, doi:10.1093/aobpla/plq003 & The Authors 2010 15 Parolin and Wittmann — Adaptive responses of trees to ﬂooding in tropical ﬂoodplain systems adaptation to adversity. Studies in Ecology 11. Oxford: Blackwell (viii) Attention also needs to be given to small wetlands Scientiﬁc Publications, 105 – 129. along small rivers or in remote places. These areas Crawford RMM. 1992. Oxygen availability as an ecological limit to have been almost totally neglected. plant distribution. Advances in Ecological Research 23: 93 – 185. Where possible, future studies should adopt methods Crawford RMM. 2003. Seasonal differences in plant responses to ﬂooding and anoxia. Canadian Journal of Botany 81: 1224 – 1246. which will allow comparisons to be made with conﬁdence. Darwin C. 1842 (published 1909). Pencil sketch of 1842. In: Darwin F, Climatic change, increasing prevalence of droughts, ed. The foundations of the origin of species: two essays written in alterations to groundwater availability and ﬂooding 1842 and 1844. Cambridge: Cambridge University Press. periodicities make such work increasingly urgent since Darwin C. 1859. On the origin of species by means of natural selec- freshwater ﬂoodplain forests are a vital human resource tion, or the preservation of favoured races in the struggle for life. that is under threat. They harbour many ﬁsh and London: John Murray [Facsimile of 1st edn.]: Cambridge, MA: mammal species, help moderate widespread ﬂooding of Harvard University Press, 1964. inhabited areas, regulate river levels, improve water De Simone O, Haase K, Mu¨ller E, Junk WJ, Schmidt W. 2002a. quality, act as substantial sinks for carbon and provide Adaptations of Central Amazon tree species to prolonged ﬂood- ing: root morphology and leaf longevity. Plant Biology 2: timber and non-timber forest products. Improving our 515 – 522. understanding of their workings will underpin their pres- De Simone O, Haase K, Mu¨ller E, Junk WJ, Gonsior GA, Schmidt W. ervation and effective future management. 2002b. Impact of root morphology on metabolism and oxygen distribution in roots and rhizosphere from two Central Amazon Contributions by the authors ﬂoodplain tree species. Functional Plant Biology 29: 1025 – 1035. Ellery WN, Tacheba B. 2003. Floristic diversity of the Okavango Both authors contributed to a similar extent in the prep- Delta, Botswana. In: Alonso LE, Nordin LA, eds. A rapid biological aration of this article. assessment of the aquatic ecosystems of the Okavango Delta, Botswana, Chapter 5. High Water Survey: RAP Bulletin of Biologi- Acknowledgements cal Assessment. We thank the Association of Tropical Biology and Conser- Ellery K, Ellery WN, Verhagen BT. 1992. The distribution of C3 and vation (ATBC) and the Society of Tropical Ecology (gto ¨ ) C4 plants in a successional sequence in the Okavango Delta. for support. We also thank Michael Heinl (University of South African Journal of Botany 58: 400 – 402. Innsbruck, Germany) for much information on the Ellery WN, Ellery K, McCarthy TS. 1993. Plant distribution in islands of the Okavango Delta, Botswana: determinants and feedback Okavango Delta. interactions. African Journal of Ecology 31: 118 – 134. Ellery WN, McCarthy TS, Dangerﬁeld JM. 2000. Floristic diversity in Conﬂict of interest statement the Okavango Delta, Botswana as an endogenous product of biological activity. In: Gopal B, Junk WJ, Davis JA, eds. Biodiver- None declared. sity in wetlands: assessment, function and conservation, Vol. I. Leiden: Backhuis. References Ferreira CS. 2002. Germinac¸a˜o e adaptac¸o˜es metabo´licas e morfo-anatoˆmicas em plaˆntulas de Himatanthus succuuba Armstrong W, Bra¨ndle R, Jackson MB. 1994. Mechanisms of ﬂood (Spruce) Wood., de ambientes de va´rzea e terra ﬁrme na Amazoˆ- tolerance in plants. Acta Botanica Neerlandica 43: 307 – 358. nia Central. MSc Thesis, Universidade do Amazonas (UA), Insti- Bonyongo MC. 1999. Vegetation ecology of the seasonal ﬂoodplains tuto Nacional de Pesquisas da Amazo ˆ nia (INPA), Manaus, 95. in the Okavango Delta, Botswana. Unpublished Thesis (MSc), Uni- Ferreira LV, Venticinque E, Almeida S. 2005. O desmatamento na versity of Pretoria. Amazo ˆ nia e a importa ˆ ncia das a ´ reas protegidas. Estudos Avan- Bonyongo MC, Veenendaal E, Bredenkamp G. 2000. Floodplain veg- c¸ados 19: 1 – 10. etation in the Nxaraga Lagoon area, Okavango Delta, Botswana. Finlayson CM. 1988. Productivity and nutrient dynamics of season- South African Journal of Botany 66: 15 – 21. ally inundated ﬂood plains in the Northern Territory. In: Campbell I, Poole C, Giesen W, Valbo-Jorgensen J. 2006. Species Wade-Marshall D, Loveday P, eds. North Australia: progress and diversity and ecology of Tonle Sap Great Lake, Cambodia. prospects, Vol. 2 ﬂoodplain research. Darwin: ANU Press, 58 – 83. Aquatic Sciences 68: 355 – 373. Finlayson CM. 2005. Plant ecology of Australia’s tropical ﬂoodplain Colmer TD, Pedersen O. 2008. Underwater photosynthesis and res- wetlands: a review. Annals of Botany 96: 541 – 555. piration in leaves of submerged wetland plants: gas ﬁlms Finlayson CM, Bailey BJ, Cowie ID. 1989. Macrophytic vegetation of improve CO and O exchange. New Phytologist 177: 918 – 926. 2 2 the Magela ﬂood plain, Northern Australia. Research report no. 5. Cowie ID, Armstrong MD, Woinarski JCZ, Brocklehurs PS, Short PS, Sydney: Ofﬁce of the Supervising Scientist. Dunlop CR. 2000. An overview of the ﬂoodplains. In: Cowie ID, Finlayson CM, Cowie ID, Bailey BJ. 1990. Characteristics of a sea- Short PS, Osterkamp P, Madsen M, eds. Floodplain ﬂora: a ﬂora sonally ﬂooded freshwater system in monsoonal Australia. of the coastal ﬂoodplains of the Northern Territory, Australia. In: Whigham DF, Good RE, Kvet J, eds. Wetland ecology and Canberra, Australia: ABRS, 1 – 33. management: case studies. Dordrecht: Kluwer Academic, Crawford RMM. 1989. The anaerobic retreat. In: Crawford R.M.M., 141 – 162. ed. Studies in plant survival. Ecological case histories of plant 16 AoB PLANTS Vol. 2010, plq003, doi:10.1093/aobpla/plq003 & The Authors 2010 Parolin and Wittmann — Adaptive responses of trees to ﬂooding in tropical ﬂoodplain systems Finlayson CM, Cowie ID, Bailey BJ. 1993. Litterfall in a Melaleuca landscape ecology of a mighty tropical river and its basin. Junk, forest on a seasonally inundated ﬂood plain in tropical 215 – 243. northern Australia. Wetlands Ecology and Management 2: Junk WJ. 1997. The central Amazonian ﬂoodplain: ecology of a 177 – 188. pulsing system. Ecological Studies 126. Heidelberg: Springer. Franklin DC, Brocklehurst PS, Lynch D, Bowman DMJS. 2007. Niche Junk WJ. 2000. Mechanisms for development and maintenance differentiation and regeneration in the seasonally ﬂooded Mel- of biodiversity in neotropical ﬂoodplains. In: Gopal B, aleuca forests of northern Australia. Journal of Tropical Ecology Junk WJ, Davis JA, eds. Biodiversity in wetlands: assessment, 23: 457 – 468. function and conservation,Vol.1.Leiden: Backhuis, Furch B, Correˆa AFF, Nunes JASM, Otto K-R. 1985. Lichtklimadaten 119 – 139. in drei aquatischen Okosystemen verschiedener physikalisch- Junk WJ, da Silva VMF. 1997. Mammals, reptiles and amphibians. chemischer Beschaffenheit. I. Abschwa ¨ chung, Ru ¨ ckstreuung In: Junk WJ, ed. The central Amazon ﬂoodplain: ecology of a und Vergleich zwischen Einstrahlung, Ru ¨ ckstrahlung und spha ¨ r- pulsing system. Ecological studies, 126. Berlin, Heidelberg: isch gemessener Quantenstromdichte (PAR). Amazoniana 9: Springer, 409 – 418. 411 – 430. Junk WJ, Bayley PB, Sparks RE. 1989. The ﬂood pulse concept in Gibbs J, Greenway H. 2003. Mechanisms of anoxia tolerance in river-ﬂoodplain systems. In: Dodge DP, ed. Proceedings of the plants. I. Growth, survival and anaerobic catabolism. Functional International Large River Symposium. Canadian Special Publi- Plant Biology 30: 1 – 47. cation of Fisheries and Aquatic Sciences 106: 110 – 127. Gopal B, Junk WJ, Davis JA. 2000. Biodiversity in wetlands: assess- Junk WJ, Brown M, Campbell IC, Finlayson M, Gopal B, Ramberg L, ment, function and conservation, Vol. 1. Leiden: Backhuis. Warner BG. 2006. The comparative biodiversity of seven Heinl M, Sliva J, Tacheba B. 2004. Vegetation changes after single globally important wetlands: a synthesis. Aquatic Sciences 68: ﬁre-events in the Okavango Delta wetland, Botswana. South 400 – 414. African Journal of Botany 70: 695 – 704. Kalliola R, Salo J, Puhakka M, Rajasilta M. 1991. New site for- Heinl M, Neuenschwander A, Sliva J, Vanderpost C. 2006. Inter- mation and colonizing vegetation in primary succession on actions between ﬁre and ﬂooding in the Okavango Delta ﬂood- the Western Amazon ﬂoodplains. Journal of Ecology 79: plains, Botswana. Landscape Ecology 21: 699 – 709. 877 – 901. Heinl M, Frost P, Vanderpost C, Sliva J. 2007. Fire activity on dry- Kesselmeier J, Staudt M. 1999. Biogenic volatile organic com- lands and ﬂoodplains in the southern Okavango Delta, Bots- pounds (VOC): an overview on emission, physiology and wana. Journal of Arid Environments 68: 77 – 87. ecology. Journal Atmospheric Chemistry 33: 23 – 88. Huete AR, Restrepo-Coupe N, Ratana P, Didan K, Saleska SR, Kesselmeier J, Bode K, Hofmann U, Mu¨ller H, Scha¨fer L, Wolf A, Ichii K, Panuthai S, Gamo M. 2008. Multiple site tower ﬂux Ciccioli P, Brancaleoni E, Cecinato A, Frattoni M, Foster P, and remote sensing comparisons of tropical forest dynamics Ferrari C, Jacob V, Fugit JL, Dutaur L, Simon V, Torres L. in monsoon Asia. Agricultural and Forest Meteorology 148: 1997. Emission of short chained organic acids, aldehydes and 748 – 760. monoterpenes from Quercus ilex L., Pinus pinea L. in relation to physiological activities, carbon budget and emission algor- Hughes FMR. 1988. The ecology of African ﬂoodplain forests in ithms. Atmospheric Environment 31: 119 – 133. semi-arid and arid zones: a review. Journal of Biogeography 15: 127 – 140. Kimmerer TW, Macdonald RC. 1987. Acetaldehyde and ethanol biosynthesis in leaves of plants. Plant Physiology 84: Irion G, Junk WJ, Mello JASN. 1997. The large central Amazonian 1204 – 1209. river ﬂoodplains near Manaus: geological, climatological, hydro- logical and geomorphological aspects. In: Junk WJ, ed. The Kozlowski TT. 1984. Responses of woody plants to ﬂooding. In: Central Amazon ﬂoodplain: ecology of a pulsing system. Ecologi- Kozlowski TT, ed. Flooding and plant growth. Orlando: Academic cal Studies 126. Heidelberg: Springer, 23 – 46. Press, 129 – 163. Ishida A, Diloksumpun S, Ladpala P, Staporn D, Panuthai S, Kubitzki K. 1989. The ecogeographical differentiation of Amazo- Gamo M, Yazaki K, Ishizuka M, Puangchit L. 2006. Contrasting nian inundation forests. Plant Systematics and Evolution 162: seasonal leaf habits of canopy trees between tropical dry- 285 – 304. deciduous and evergreen forests in Thailand. Tree Physiology Kubitzki K, Ziburski A. 1994. Seed dispersal in ﬂood plain forests of 26: 643 – 656. Amazonia. Biotropica 26: 30 – 43. IUCN. 1991. http://cmsdata.iucn.org/downloads/mrwd_nwg_ Lamberts D, Koponen J. 2008. Flood pulse alterations and pro- regional_meeting_december_2009_ﬁnal_2.pdf. ductivity of the Tonle Sap ecosystem: a model for impact Jackson MB, Armstrong W. 1999. Formation of aerenchyma and assessment. Ambio 37: 178 – 184. the processes of plant ventilation in relation to soil ﬂooding ¨ Larcher W. 1994.Okophysiologie der Pﬂanzen: Leben, Leistung und and submergence. Plant Biology 1: 274 – 287. Streßbewa ¨ ltigung der Pﬂanzen in ihrer Umwelt. 5th Edn. Ulmer James EK, Loureiro MD, Pott A, Pott VJ, Martins CM, Franco AA, Stuttgart, UTB fu ¨ r Wissenschaft. Sprent JI. 2001. Flooding-tolerant legume symbioses from the Lowry J, Finlayson CM. 2004. A review of spatial data sets for Brazilian Pantanal. New Phytologist 150: 723 – 738. wetland inventory in northern Australia. In: Supervising scientist Joly CA, Crawford RMM. 1982. Variation in tolerance and metabolic report 178. Darwin. responses to ﬂooding in some tropical trees. Journal of Exper- Mantlana KB. 2008. Seasonal and inter-annual variations of imental Botany 33: 799 – 809. leaf-level photosynthesis and soil respiration in the representa- Junk WJ. 1984. Ecology of the va ´ rzea, ﬂoodplain of Amazonian tive ecosystems of the Okavango Delta, Botswana. PhD Thesis, whitewater rivers. In: Sioli H, ed. The Amazon. Limnology and Wageningen University, The Netherlands. AoB PLANTS Vol. 2010, plq003, doi:10.1093/aobpla/plq003 & The Authors 2010 17 Parolin and Wittmann — Adaptive responses of trees to ﬂooding in tropical ﬂoodplain systems McCarthy TS. 2006. Groundwater in the wetlands of the Okavango of the volatile C -compounds ethanol, acetaldehyde and Delta, Botswana, and its contribution to the structure and func- acetic acid between leaves of Amazonian ﬂoodplain tree tion of the ecosystem. Journal of Hydrology 320: 264 – 282. species and the atmosphere. Biogeosciences 5: 1085 – 1100. McJannet D. 2008. Water table and transpiration dynamics in a Safford RJ, Maltby E, Duong Van Ni , Branch NP. 2009. Melaleuca seasonally inundated Melaleuca quinquenervia forest, north wetlands and sustainable development in the Mekong Delta, Queensland, Australia. Hydrological Processes 22: 3079 – 3090. Vietnam. In: Maltby E, Barker T, eds. The wetlands handbook. Oxford: Blackwells, 829 – 849. Medina E. 1983. Adaptations of tropical trees to moisture stress. In: Golley FB, ed. Ecosystems of the world: tropical rain forest eco- Salo J, Kalliola R, Ha¨kkinen I, Ma¨kinen Y, Niemela¨ P, Puhakka M, systems. Amsterdam: Elsevier, 225 – 237. Coley PD. 1986. River dynamics and the diversity of Amazon lowland forest. Nature 322: 254 – 258. Mommer L, Visser EJW. 2005. Underwater photosynthesis in ﬂooded terrestrial plants: a matter of leaf plasticity. Annals of Sarkkula J, Koponen J, Kummu M. 2005. Tools for integrated basin Botany 96: 581 – 589. ﬂow management at Lower Mekong basin ﬂoodplains. In: Zerger A, Argent RM, eds. MODSIM 2005 International Congress Moreira FMDS, Silva MFD, Faria SMD. 1992. Occurrence of nodula- on Modelling and Simulation. Canberra: Modelling and Simu- tion in legume species in the Amazon region of Brazil. New Phy- lation Society of Australia and New Zealand, 2153 – 2159. tologist 121: 563 – 570. Scarano FR, Ribeiro KT, Moraes LFD, Lima HC. 1997. Plant estab- O’Grady AP, Eamus D, Cook PG, Lamontagne S. 2006. Comparative lishment on ﬂooded and unﬂooded patches of a freshwater water use by the riparian trees Melaleuca argentea and Corym- swamp forest in southeastern Brazil. Journal of Tropical bia bella in the wet – dry tropics of northern Australia. Tree Physi- Ecology 14: 793 – 803. ology 26: 219 – 228. Scarano FR, Pereira TS, Rocas G. 2003. Seed germination during Oliveira-Wittmann A, Piedade MTF, Wittmann F, Parolin P. 2007. ﬂoatation and seedling growth of Carapa guianensis, a tree Germination in four low-va ´ rzea tree species of Central Amazo- from ﬂood-prone forests of the Amazon. Plant Ecology 168: nia. Aquatic Botany 86: 197 – 203. 291 – 296. Parolin P. 2000. Phenology and CO -assimilation of trees in Schlu¨ter U-B, Furch B. 1992. Morphologische, anatomische und Central Amazonian ﬂoodplains. Journal of Tropical Ecology 16: physiologische Untersuchungen zur Uberﬂutungstoleranz des 465 – 473. Baumes Macrolobium acaciaefolium, charakteristisch fu ¨ r die Parolin P. 2001. Senna reticulata, a pioneer tree from Amazonian Weiß- und Schwarzwasseru ¨ berschwemmungswa ¨ lder bei va ´ rzea ﬂoodplains. The Botanical Review 67: 239 – 254. Manaus, Amazonas. Amazoniana 12: 51 – 69. Parolin P. 2009. Submerged in darkness: adaptations to prolonged Schlu¨ter U-B, Furch B, Joly CA. 1993. Physiological and anatomical submergence by woody species of the Amazonian Floodplains. adaptations by young Astrocaryum jauari Mart. (Arecaceae) in Annals of Botany 103: 359 – 376. periodically inundated biotopes of Central Amazonia. Biotropica Parolin P, Armbru¨ster N, Wittmann F, Ferreira LV, Piedade MTF, 25: 384 – 396. Junk WJ. 2002. A review of tree phenology in central Amazo- Scho¨ngart J. 2003. Dendrochronological and dendroclimatic studies nian ﬂoodplains. Pesquisas, Botaˆnica 52: 195 – 222. in Central Amazonian Forests. Research Program May 2003 – April Parolin P, De Simone O, Haase K, Waldhoff D, Rottenberger S, 2005, 1 – 13. Kuhn U, Kesselmeier J, Schmidt W, Piedade MTF, Junk WJ. Scho¨ngart J, Piedade MFT, Ludwigshausen S, Horna V, Worbes M. 2004. Central Amazon ﬂoodplain forests: tree survival in a 2002. Phenology and stem-growth periodicity of tree species in pulsing system. The Botanical Review 70: 357 – 380. Amazonian ﬂoodplain forests. Journal of Tropical Ecology 18: Parolin P, Lucas C, Piedade MTF, Wittmann F. 2010. Drought 581 – 597. responses of ﬂood-tolerant trees in Amazonian ﬂoodplains. Sena Gomes AR, Kozlowski TT. 1980. Responses of Melaleuca quin- Annals of Botany 105: 129 – 139. quenervia seedlings to ﬂooding. Physiologia Plantarum 49: Ponnamperuma FN. 1984. Effects of ﬂooding on soils. In: 373 – 377. Kozlowski TT, ed. Flooding and plant growth. Orlando: Academic Sioli H. 1954. Betrachtungen u ¨ ber den Begriff ‘Fruchtbarkeit’ eines Press, 9 – 45. Gebiets anhand der Verha ¨ ltnisse in Bo ¨ den und Gewa ¨ ssern Ama- Prance GT. 1979. Notes on the vegetation of Amazonia. III. Termi- zoniens. Forschung Fortschritt 28: 65 – 72. nology of Amazonian forest types subjected to inundation. Brit- Skeat AJ, East TJ, Corbett LK. 1996. Impact of feral water buffalo. tonia 31: 26 – 38. In: Finlayson CM, von Oertzen I, eds. Landscape and vegetation Ribeiro MNG, Adis J. 1984. Local rainfall variability—a potential ecology of the Kakadu Region, Northern Australia. Dordrecht: bias for bioecological studies in the Central Amazon. Acta Ama- Kluwer Academic, 155 – 177. zonica 14: 159 – 174. Tacheba B, Segosebe E, Vanderpost C, Sebego R. 2009. Assessing Ringrose S. 2003. Characterisation of riparian woodlands and their the impacts of ﬁre on the vegetation resources that are potential water loss in the distal Okavango Delta, Botswana. available to the local communities of the seasonal wetlands Applied Geography 23: 281 – 302. of the Okavango, Botswana, in the context of different land Ringrose S, Chipanshi AC, Matheson W, Chanda R, Motoma L, uses and key government policies. African Journal of Ecology Magole I, Jellema A. 2002. Climate- and human-induced 47: 71 – 77. woody vegetation changes in Botswana and their Tanaka K, Takizawa H, Kume T, Xu J, Tantasirin C, Suzuki M. 2004. implications for human adaptation. Environmental Management Impact of rooting depth and soil hydraulic properties on 30: 98 – 109. the transpiration peak of an evergreen forest in northern Rottenberger S, Kleiss B, Kuhn U, Wolf A, Piedade MTF, Junk W, Thailand in the late dry season. Journal of Geophysical Research Kesselmeier J. 2008. The effect of ﬂooding on the exchange 18 AoB PLANTS Vol. 2010, plq003, doi:10.1093/aobpla/plq003 & The Authors 2010 Parolin and Wittmann — Adaptive responses of trees to ﬂooding in tropical ﬂoodplain systems Taylor JA, Tulloch D. 1985. Rainfall in the wet – dry tropics: extreme Wittmann F, Parolin P. 2005. Aboveground roots in Amazonian events at Darwin and similarities between years during the ﬂoodplain trees. Biotropica 37: 609 – 619. period 1870 – 1983. Australian Journal of Ecology 10: 281 – 295. Wittmann F, Anhuf D, Junk WJ. 2002. Tree species distribution and Veenendaal EM, Mantlana KB, Pammenter NW, Weber P, community structure of Central Amazonian va ´ rzea forests by Huntsman-Mapila P, Lloyd J. 2008. Growth form and seasonal remote sensing techniques. Journal of Tropical Ecology 18: variation in leaf gas exchange of Colophospermum mopane 805 – 820. savanna trees in northwest Botswana. Tree Physiology 28: Wittmann F, Junk WJ, Piedade MTF. 2004. The va ´ rzea forests in 417 – 424. Amazonia: ﬂooding and the highly dynamic geomorphology Visser EJW, Voesenek LACJ, Vartapetian BB, Jackson MB. 2003. interact with natural forest succession. Forest Ecology and Man- Flooding and plant growth. Annals of Botany 91: 107 – 109. agement 196: 199 – 212. Waldhoff D. 2003. Leaf structure in trees of Central Amazonian Wittmann F, Scho¨ngart J, Montero JC, Motzer T, Junk WJ, ﬂoodplain forests (Brazil). Amazoniana 17: 451 – 469. Piedade MTF, Queiroz HL, Worbes M. 2006. Tree species compo- sition and diversity gradients in white-water forests across the Waldhoff D, Furch B. 2002. Leaf morphology and anatomy in Amazon Basin. Journal of Biogeography 33: 1334 – 1347. eleven tree species from Central Amazonian ﬂoodplains (Brazil). Amazoniana 17: 79 – 94. Wittmann F, Junk WJ, Scho¨ngart J. 2010. Phytogeography, species diversity, community structure and dynamics of central Amazo- Waldhoff D, Junk WJ, Furch B. 2002. Fluorescence parameters, nian ﬂoodplain forests. In: Junk WJ, Piedade MTF, Parolin P, chlorophyll concentration, and anatomical features as indi- Wittmann F, Scho ¨ ngart J, eds. Central Amazonian Floodplain cators for ﬂood adaptation of an abundant tree species in forests: ecophysiology, biodiversity and sustainable manage- Central Amazonia: Symmeria paniculata. Environmental and ment. Ecological Studies. Heidelberg: Springer. Experimental Botany 48: 225 – 235. Worbes M. 1997. The forest ecosystem of the ﬂoodplains. In: Wantzen KM, Junk WJ. 2000. The importance of Junk WJ, ed. The Central Amazon ﬂoodplain: ecology of a stream-wetland-systems for biodiversity: a tropical perspective. pulsing system. Ecological Studies 126. Heidelberg: Springer, In: Gopal B, Junk WJ, Davis JA, eds. Biodiversity in wetlands: assess- 223 – 266. ment, function and conservation, Vol. 1. Leiden: Backhuys, 11 – 34. Worbes M, Klinge H, Revilla JD, Martius C. 1992. On the dynamics, Wikramanayake E, Rundel P. 2002. Tonle sap freshwater swamp ﬂoristic subdivision and geographical distribution of va ´ rzea forests. In: Wikramanayake E, Dinerstein E, Loucks C, eds. Terres- forests in Central Amazonia. Journal of Vegetation Science 3: trial ecoregions of the Indo-Paciﬁc: a conservation assessment. 553 – 564. Washington, DC: Island Press, 824 pp. AoB PLANTS Vol. 2010, plq003, doi:10.1093/aobpla/plq003 & The Authors 2010 19 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png AoB Plants Pubmed Central http://www.deepdyve.com/lp/pubmed-central/struggle-in-the-flood-tree-responses-to-flooding-stress-in-four-30G4iKb4kE

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References (130)

C. Finlayson, I. Oertzen (1996)
Landscape and Vegetation Ecology of the Kakadu Region, Northern Australia
A. Bennett (1872)
The Origin of Species by means of Natural Selection; or the Preservation of Favoured Races in the Struggle for Life
Nature, 5
E. Medina (1983)
Adaptations of tropical trees to moisture stress
Ecosystems of the world
W. Ellery, K. Ellery, T. McCarthy (1993)
Plant distribution in islands of the Okavango Delta, Botswana: determinants and feedback interactions
African Journal of Ecology, 31
A. Wittmann, M. Piedade, P. Parolin, F. Wittmann (2007)
Germination in four low-várzea tree species of Central Amazonia
Aquatic Botany, 86
T. McCarthy (2006)
Groundwater in the wetlands of the Okavango Delta, Botswana, and its contribution to the structure and function of the ecosystem
Journal of Hydrology, 320
P. Parolin, O. Simone, K. Haase, D. Waldhoff, S. Rottenberger, U. Kuhn, J. Kesselmeier, B. Kleiss, Wolfgang Schmidt, M. Piedade, W. Junk (2004)
Central Amazonian floodplain forests: Tree adaptations in a pulsing system
The Botanical Review, 70
J. Salo, R. Kalliola, Ilmari Häkkinen, Y. Mäkinen, P. Niemelä, M. Puhakka, P. Coley (1986)
River dynamics and the diversity of Amazon lowland forest
Nature, 322
F. Wittmann, W. Junk, M. Piedade (2004)
The várzea forests in Amazonia: flooding and the highly dynamic geomorphology interact with natural forest succession
Forest Ecology and Management, 196
B. Furch, Ana Corrêa, José Mello (1985)
Lichtklimadaten in drei aquatischen Ökosystemen verschiedener physikalisch-chemischer Beschaffenheit. I. Abschwächung, Rückstreuung und Vergleich zwischen Einstrahlung, Rückstrahlung und sphärisch gemessener Quantenstromdichte (PAR)
, 9
W. Junk (1984)
Ecology of the várzea, floodplain of Amazonian whitewater rivers
WN Ellery, B Tacheba, LE Alonso, LA Nordin (2003)
Floristic diversity of the Okavango Delta, Botswana
A rapid biological assessment of the aquatic ecosystems of the Okavango Delta, Botswana
D. Lamberts, J. Koponen (2008)
Flood Pulse Alterations and Productivity of the Tonle Sap Ecosystem: A Model for Impact Assessment
, 37
WJ Junk, PB Bayley, RE Sparks (1989)
The flood pulse concept in river-floodplain systems. In: Dodge DP
Proceedings of the International Large River Symposium. Canadian Special Publication of Fisheries and Aquatic Sciences, 106
F. Wittmann, D. Anhuf, W. Junk (2002)
Tree species distribution and community structure of central Amazonian várzea forests by remote-sensing techniques
Journal of Tropical Ecology, 18
M. Jackson, W. Armstrong (1999)
Formation of Aerenchyma and the Processes of Plant Ventilation in Relation to Soil Flooding and Submergence
Plant Biology, 1
K. Wantzen, W. Junk (2000)
THE IMPORTANCE OF STREAM-WETLAND-SYSTEMS FOR BIODIVERSITY - A TROPICAL PERSPECTIVE
J. Gibbs, H. Greenway (2003)
Review: Mechanisms of anoxia tolerance in plants. I. Growth, survival and anaerobic catabolism.
Functional plant biology : FPB, 30 3
(1989)
Macrophytic vegetation of the Magela flood plain
M Heinl, A Neuenschwander, J Sliva, C Vanderpost (2006)
Interactions between fire and flooding in the Okavango Delta floodplains, Botswana
Landscape Ecology, 21
C. Darwin, F. Darwin (1987)
The Foundations of the Origin of Species: Two Essays Written in 1842 and 1844
(1985)
Lichtklimadaten in drei aquatischen Ökosystemen verschiedener physikalischchemischer Beschaffenheit
Cristiane Ferreira (2002)
Germinação e adaptações metabólicas e morfo-anatômicas em plântulas de Himatanthus sucuuba (Spruce) Wood, de ambientes de várzea e terra firme na Amazônia Central
Anthony O'Grady, D. Eamus, Peter Cook, S. Lamontagne (2006)
Comparative water use by the riparian trees Melaleuca argentea and Corymbia bella in the wet-dry tropics of northern Australia.
Tree physiology, 26 2
E. Maltby, T. Barker (2009)
The wetlands handbook
RMM Crawford, R.M.M. Crawford (1989)
The anaerobic retreat
Studies in plant survival. Ecological case histories of plant adaptation to adversity. Studies in Ecology 11
M. Heinl, P. Frost, C. VanderPost, J. Slíva (2007)
Fire activity on drylands and floodplains in the southern Okavango Delta, Botswana
Journal of Arid Environments, 68
J. Schöngart, M. Piedade, Sabine Ludwigshausen, V. Horna, M. Worbes (2002)
Phenology and stem-growth periodicity of tree species in Amazonian floodplain forests
Journal of Tropical Ecology, 18
M. Worbes, H. Klinge, J. Revilla, C. Martius (1992)
On the dynamics, floristic subdivision and geographical distribution of varzea forests in Central Amazonia
Journal of Vegetation Science, 3
(1994)
O ¨ kophysiologie der Pflanzen: Leben, Leistung und Streßbewä ltigung der Pflanzen in ihrer Umwelt
P Parolin, Simone De, K Haase, D Waldhoff, S Rottenberger, U Kuhn, J Kesselmeier, W Schmidt, MTF Piedade, WJ Junk (2004)
Central Amazon floodplain forests: tree survival in a pulsing system
The Botanical Review, 70
FN Ponnamperuma, TT Kozlowski (1984)
Effects of flooding on soils
Flooding and plant growth
T. Kozlowski (1985)
Flooding and Plant Growth
Agriculture, Ecosystems & Environment, 18
A. Skeat, T. East, L. Corbett (1996)
Impact of feral water buffalo
L. Mommer, E. Visser (2005)
Underwater photosynthesis in flooded terrestrial plants: a matter of leaf plasticity.
Annals of botany, 96 4
F. Scarano, T. Pereira, Giselle Rôças (2003)
Seed germination during floatation and seedling growth of Carapa guianensis, a tree from flood-prone forests of the Amazon
Plant Ecology, 168
U. Schlüter, B. Furch, C. Joly (1993)
Physiological and anatomical adaptations by young Astrocaryum jauari Mart. (Arecaceae) in periodically inundated biotopes of central Amazonia.
Biotropica, 25
B. Tacheba, E. Segosebe, C. VanderPost, R. Sebego (2009)
Assessing the impacts of fire on the vegetation resources that are available to the local communities of the seasonal wetlands of the Okavango, Botswana, in the context of different land uses and key government policies.
African Journal of Ecology, 47
J. Heinen (2003)
Terrestrial Ecoregions of the Indo-Pacific: A Conservation Assessment. E. Wikramanayake, E. Dinerstein, C. J. Loucks, D. M. Olson, J. Morrison, J. Lamoreux, M. McKnight, and P. Hedao. 2002. Island Press, Washington, DC. 643 pp. $85 paperback.
Environmental Practice, 5
W. Junk (1989)
The flood pulse concept in river-floodplain systems
, 106
F. Wittmann, J. Schöngart, W. Junk (2010)
Phytogeography, Species Diversity, Community Structure and Dynamics of Central Amazonian Floodplain Forests
(2003)
Floristic diversity of the Okavango Delta, Botswana A rapid biological assessment of the aquatic ecosystems of the Okavango Delta, Botswana, Chapter 5
(2002)
Tonle sap freshwater swamp forests
C. Finlayson, I. Cowie, B. Bailey (1990)
Characteristics of a Seasonally Flooded Freshwater System in Monsoonal Australia
(2004)
A review of spatial data sets for wetland inventory in northern Australia
B. Gopal, W. Junk, Jenny Davis (2000)
Biodiversity in wetlands: assessment, function and conservation. Vol. 2
I. Campbell, C. Poole, W. Giesen, J. Valbo‐Jørgensen (2006)
Species diversity and ecology of Tonle Sap Great Lake, Cambodia
Aquatic Sciences, 68
P. Parolin (2001)
Senna reticulata, a pioneer tree from Amazonian várzea floodplains
The Botanical Review, 67
H. Sioli (1984)
The Amazon : limnology and landscape ecology of a mighty tropical river and its basin
E. Veenendaal, K. Mantlana, N. Pammenter, Piet Weber, P. Huntsman-Mapila, J. Lloyd (2008)
Growth form and seasonal variation in leaf gas exchange of Colophospermum mopane savanna trees in northwest Botswana.
Tree physiology, 28 3
(2010)
AoB PLANTS
D. Whigham, R. Good, J. Květ (1990)
Wetland Ecology and Management: Case Studies
M. Kummu, J. Koponen, J. Sarkkula (2005)
Tools for Integrated Basin Flow Management at Lower Mekong Basin Floodplains
W. Junk, Mark Brown, I. Campbell, M. Finlayson, B. Gopal, L. Ramberg, B. Warner (2006)
The comparative biodiversity of seven globally important wetlands: a synthesis
Aquatic Sciences, 68
M. Ribeiro, J. Adis (1984)
Local Rainfall Variability - A Potential Bias for Bioecological Studies in the Central Amazon
Acta Amazonica, 14
D. McJannet (2008)
Water table and transpiration dynamics in a seasonally inundated Melaleuca quinquenervia forest, north Queensland, Australia
Hydrological Processes, 22
G. Prance (2008)
Notes on the vegetation of amazonia III. The terminology of amazonian forest types subject to inundation
Brittonia, 31
W. Armstrong, R. Brändle, M. Jackson (1994)
Mechanisms of flood tolerance in plants
Plant Biology, 43
(1988)
Productivity and nutrient dynamics of seasonally inundated flood plains in the Northern Territory
D. Waldhoff (2003)
Leaf structure in trees of Central Amazonian floodplain forests (Brazil)
Amazoniana-limnologia Et Oecologia Regionalis Systemae Fluminis Amazonas, 17
F. Wittmann, J. Schöngart, J. Montero, Thomas Motzer, W. Junk, M. Piedade, H. Queiroz, M. Worbes (2006)
Tree species composition and diversity gradients in white‐water forests across the Amazon Basin
Journal of Biogeography, 33
W. Junk (1997)
The Central Amazon Floodplain
C Darwin, F Darwin (1842)
Pencil sketch of 1842
The foundations of the origin of species: two essays written in 1842 and 1844
F. Scarano, K. Ribeiro, L. Moraes, H. Lima (1997)
Plant establishment on flooded and unflooded patches of a freshwater swamp forest in southeastern Brazil
Journal of Tropical Ecology, 13
K. Ellery, W. Ellery, B. Verhagen (1992)
The distribution of C3 and C4 plants in a successional sequence in the Okavango Delta
South African Journal of Botany, 58
A. Ishida, S. Diloksumpun, P. Ladpala, D. Staporn, S. Panuthai, M. Gamo, K. Yazaki, M. Ishizuka, L. Puangchit (2006)
Contrasting seasonal leaf habits of canopy trees between tropical dry-deciduous and evergreen forests in Thailand.
Tree physiology, 26 5
D. Batzer (2001)
Biodiversity in wetlands: assessment, function and conservation, edited by B. Gopal, W.J. Junk and J.A. Davis. Backhuys Publishers, Leiden, Netherlands, 2000, 353 pp. Price: US$98. ISBN 90 5782 059 5.
Aquatic Conservation-marine and Freshwater Ecosystems, 11
C. Gill (1970)
The flooding tolerance of woody species - a review.
, 31
D. Franklin, P. Brocklehurst, D. Lynch, D. Bowman (2007)
Niche differentiation and regeneration in the seasonally flooded Melaleuca forests of northern Australia
Journal of Tropical Ecology, 23
C. Joly, R. Crawford (1982)
Variation in Tolerance and Metabolic Responses to Flooding in some Tropical Trees
Journal of Experimental Botany, 33
F. Hughes (1988)
The ecology of African floodplain forests in semi-arid and arid zones: a review
Journal of Biogeography, 15
W. Junk (2000)
Mechanisms for development and maintenance of biodiversity in neotropical floodplains.
(1984)
Ecology of the vá rzea, floodplain of Amazonian whitewater rivers In: Sioli H, ed. The Amazon. Limnology and landscape ecology of a mighty tropical river and its basin. Junk
K. Mantlana (2008)
Seasonal and inter-annual variations of leaf-level photosynthesis and soil respiration in the representative ecosystems of the Okavango Delta, Botswana
S. Rottenberger, B. Kleiss, U. Kuhn, A. Wolf, M. Piedade, W. Junk, J. Kesselmeier (2008)
The effect of flooding on the exchange of the volatile C2-compounds ethanol, acetaldehyde and acetic acid between leaves of Amazonian floodplain tree species and the atmosphere
Biogeosciences, 5
C. Finlayson (2005)
Plant ecology of Australia's tropical floodplain wetlands: a review.
Annals of botany, 96 4
Katsunori Tanaka, Hideki Takizawa, T. Kume, Jianqing Xu, C. Tantasirin, Masakazu Suzuki (2004)
Impact of rooting depth and soil hydraulic properties on the transpiration peak of an evergreen forest in northern Thailand in the late dry season
Journal of Geophysical Research, 109
M. Heinl, A. Neuenschwander, J. Slíva, C. VanderPost (2006)
Interactions between fire and flooding in a southern African floodplain system (Okavango Delta, Botswana)
Landscape Ecology, 21
L. Ferreira, Eduardo Venticinque, S. Almeida (2005)
O desmatamento na Amazônia e a importância das áreas protegidas
, 19
F. Wittmann, P. Parolin (2005)
Aboveground Roots in Amazonian Floodplain Trees 1
Biotropica, 37
M. Austin, R. Crawford (1989)
Studies in Plant Survival.
Journal of Ecology, 77
J. Lock, I. Cowie, P. Short, M. Madsen (2000)
Floodplain Flora: A Flora Of The Coastal Floodplains Of The Northern Territory, Australia
D. Waldhoff, B. Furch (2002)
Leaf morphology and anatomy in eleven tree species from Central Amazonian floodplains (Brazil)
Amazoniana-limnologia Et Oecologia Regionalis Systemae Fluminis Amazonas, 17
C. Finlayson, I. Cowie, B. Bailey (1993)
Biomass and litter dynamics in a Melaleuca forest on a seasonally inundated floodplain in tropical, northern Australia
Wetlands Ecology and Management, 2
M. Bonyongo (2007)
Vegetation ecology of the seasonal floodplains in the Okavango Delta, Botswana
(2003)
Dendrochronological and dendroclimatic studies in Central Amazonian Forests. Research Program
P. Parolin, N. Armbruester, F. Wittmann, L. Ferreira, M. Piedade, W. Junk (2002)
A review of tree phenology in Central Amazonian floodplains
, 52
R. Safford, E. Maltby, D. Ni, N. Branch (2009)
Melaleuca Wetlands and Sustainable Development in the Mekong Delta, Vietnam
E. James, M. Loureiro, A. Pott, V. Pott, Claudia Martins, Avilio Franco, J. Sprent (2001)
Flooding‐tolerant legume symbioses from the Brazilian Pantanal
New Phytologist, 150
J. Kesselmeier, M. Staudt (1999)
Biogenic Volatile Organic Compounds (VOC): An Overview on Emission, Physiology and Ecology
Journal of Atmospheric Chemistry, 33
(2000)
Floristic diversity in the Okavango Delta, Botswana as an endogenous product of biological activity
W. Junk, V. Silva (1997)
Mammals, Reptiles and Amphibians
T. Colmer, O. Pedersen (2008)
Underwater photosynthesis and respiration in leaves of submerged wetland plants: gas films improve CO2 and O2 exchange.
The New phytologist, 177 4
S. Ringrose (2003)
Characterisation of riparian woodlands and their potential water loss in the distal Okavango Delta, Botswana
Applied Geography, 23
E. Visser, L. Voesenek, B. Vartapetian, M. Jackson (2003)
Flooding and Plant Growth
Annals of Botany, 91
W. Junk (2010)
The Central Amazon Floodplain: Ecology of a Pulsing System
Thomas Kimmerer, Robert MacDonald (1987)
Acetaldehyde and ethanol biosynthesis in leaves of plants.
Plant physiology, 84 4
D. Waldhoff, B. Furch, W. Junk (2002)
Fluorescence parameters, chlorophyll concentration, and anatomical features as indicators for flood adaptation of an abundant tree species in Central Amazonia: Symmeria paniculata
Environmental and Experimental Botany, 48
O. Simone, E. Müller, W. Junk, W. Schmidt (2002)
Adaptations of Central Amazon Tree Species to Prolonged Flooding: Root Morphology and Leaf Longevity
Plant Biology, 4
ID Cowie, MD Armstrong, JCZ Woinarski, PS Brocklehurs, PS Short, CR Dunlop, ID Cowie, PS Short, P Osterkamp, M Madsen (2000)
An overview of the floodplains
Floodplain flora: a flora of the coastal floodplains of the Northern Territory, Australia
G. Irion, W. Junk, J. Mello (1997)
The Large Central Amazonian River Floodplains Near Manaus: Geological, Climatological, Hydrological and Geomorphological Aspects
John Taylor, D. Tulloch (1985)
Rainfall in the wet‐dry tropics: Extreme events at Darwin and similarities between years during the period 1870–1983 inclusive
Austral Ecology, 10
O. Simone, K. Haase, E. Müller, W. Junk, G. Gonsior, W. Schmidt (2002)
Impact of root morphology on metabolism and oxygen distribution in roots and rhizosphere from two Central Amazon floodplain tree species.
Functional plant biology : FPB, 29 9
A. Gomes, T. Kozlowski (1980)
Responses of Melaleuca quinquenervia seedlings to flooding
Physiologia Plantarum, 49
C. Darwin (2019)
On the origin of species by means of natural selection: Or the preservation of the favoured races in the struggle for life.
A. Cutini (2002)
Pinus pinea L.
P. Parolin (2009)
Submerged in darkness: adaptations to prolonged submergence by woody species of the Amazonian floodplains.
Annals of botany, 103 2
F. Ponnamperuma (1984)
CHAPTER 2 – Effects of Flooding on Soils
T. Kozlowski (1984)
CHAPTER 4 – Responses of Woody Plants to Flooding
J. Kesselmeier, K. Bode, U. Hofmann, H. Müller, L. Schäfer, A. Wolf, P. Ciccioli, E. Brancaleoni, A. Cecinato, M. Frattoni, P. Foster, C. Ferrari, V. Jacob, J. Fugit, L. Dutaur, V. Simon, L. Torres (1997)
Emission of short chained organic acids, aldehydes and monoterpenes from Quercus ilex L. and Pinus pinea L. in relation to physiological activities, carbon budget and emission algorithms
Atmospheric Environment, 31
TT Kozlowski, TT Kozlowski (1984)
Responses of woody plants to flooding
Flooding and plant growth
M. Bonyongou, G. Bredenkamp, E. Veenendaal (2000)
Foodplain vegetation in the Nxaraga Lagoon area, Okavango Delta, Botswana
South African Journal of Botany, 66
R. Crawford (2003)
Seasonal differences in plant responses to flooding and anoxia
Botany, 81
Ursula-Brigitte Schlüter, B. Furch (1992)
Morphologische, anatomische und physiologische Untersuchungen zur Überflutungstoleranz des Baumes Macrolobium acaciaefolium, charakteristisch für die Weiß- und Schwarzwasser-Überschwemmungswälder bei Manaus, Amazonas
, 12
M. Worbes (1997)
The Forest Ecosystem of the Floodplains
A. Huete, N. Restrepo-Coupe, Piyachat Ratana, K. Didan, S. Saleska, K. Ichii, S. Panuthai, M. Gamo (2008)
Multiple site tower flux and remote sensing comparisons of tropical forest dynamics in Monsoon Asia
Agricultural and Forest Meteorology, 148
P. Parolin (2000)
Phenology and CO2-assimilation of trees in Central Amazonian floodplains
Journal of Tropical Ecology, 16
R. Crawford (1992)
Oxygen availability as an ecological limit to plant distribution
Advances in Ecological Research, 23
M. Heinl, J. Slíva, B. Tacheba, G. Bredenkamp (2004)
Vegetation changes after single fire-events in the Okavango Delta wetland, Botswana
South African Journal of Botany, 70
R. Crawford (1989)
Studies in plant survival: Ecological case histories of plant adaptation to adversity
K. Kubitzki, Albrecht Ziburski (1994)
Seed dispersal in flood plain forests of Amazonia
Biotropica, 26
CM Finlayson, ID Cowie, BJ Bailey (1993)
Litterfall in a Melaleuca forest on a seasonally inundated flood plain in tropical northern Australia
Wetlands Ecology and Management, 2
P. Parolin (2002)
Submergence tolerance vs. escape from submergence: two strategies of seedling establishment in Amazonian floodplains
Environmental and Experimental Botany, 48
K. Kubitzki (1989)
The ecogeographical differentiation of Amazonian inundation forests
Plant Systematics and Evolution, 162
F. Moreira, M. Silva, Faria Miana (1992)
Occurrence of nodulation in legume species in the Amazon region of Brazil
New Phytologist, 121
R. Kalliola, Jukka Salo, M. Puhakka, M. Rajasilta (1991)
New site formation and colonizing vegetation in primary succession on the western Amazon floodplains.
Journal of Ecology, 79
W. Junk, M. Piedade, F. Wittmann, J. Schöngart, P. Parolin (2010)
Amazonian Floodplain Forests. Ecophysiology, Biodiversity and Sustainable Management
P. Parolin, C. Lucas, M. Piedade, F. Wittmann (2010)
Drought responses of flood-tolerant trees in Amazonian floodplains.
Annals of botany, 105 1
(1954)
Betrachtungen über den Begriff ‘Fruchtbarkeit’ eines Gebiets anhand der Verhältnisse in Böden und Gewässern Amazoniens
S. Ringrose, A. Chipanshi, W. Matheson, R. Chanda, L. Motoma, I. Magole, A. Jellema (2002)
Climate- and Human-Induced Woody Vegetation Changes in Botswana and Their Implications for Human Adaptation
Environmental Management, 30

Publisher: Pubmed Central
Copyright: © The Author 2010. Published by Oxford University Press.
eISSN: 2041-2851
DOI: 10.1093/aobpla/plq003
Publisher site: See Article on Publisher Site

Abstract

Background In the context of the 200th anniversary of Charles Darwin’s birth in 1809, this study discusses and aims the variation in structure and adaptation associated with survival and reproductive success in the face of environmental stresses in the trees of tropical ﬂoodplains. Scope We provide a comparative review on the responses to ﬂooding stress in the trees of freshwater wetlands in tropical environments. The four large wetlands we evaluate are: (i) Central Amazonian ﬂoodplains in South America, (ii) the Okavango Delta in Africa, (iii) the Mekong ﬂoodplains of Asia and (iv) the ﬂoodplains of Northern Australia. They each have a predictable ‘ﬂood pulse’. Although ﬂooding height varies between the ecosystems, the annual pulse is a major driving force inﬂuencing all living organisms and a source of stress for which specialized adaptations for survival are required. Main points The need for trees to survive an annual ﬂood pulse has given rise to a large variety of adap- tations. However, phenological responses to the ﬂood are similar in the four ecosystems. Deciduous and evergreen species respond with leaf shedding, although sap ﬂow remains active for most of the year. Growth depends on adequate carbohydrate supply. Physiological adaptations (anaerobic metabolism, starch accumulation) are also required. Conclusions Data concerning the ecophysiology and adaptations of trees in ﬂoodplain forests worldwide are extremely scarce. For successful ﬂoodplain conservation, more information is needed, ideally through a globally co-ordinated study using reproducible comparative methods. In the light of climatic change, with increasing drought, decreased groundwater availability and ﬂooding periodicities, this knowledge is needed ever more urgently to facilitate fast and appropriate management responses to large-scale environmental change. ‘struggle for survival’ has been topical and controversial. Introduction Darwin’s theory of ‘survival of the ﬁttest’ is a synonym During the recent Darwin bicentennial year (2009) and for ‘natural selection’. Darwin asked ‘Can it be doubted, throughout the 151 years since the publication of ‘On from the struggle each individual has to obtain the Origin of Species’ (Darwin, 1859), discussion on the subsistence, that any minute variation in structure, * Corresponding author’s e-mail address: [email protected] AoB PLANTS Vol. 2010, plq003, doi:10.1093/aobpla/plq003, available online at www.aobplants.oxfordjournals.org & The Authors 2010. Published by Oxford University Press. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/2.5/uk/) which permits unrestricted non- commercial use, distribution, and reproduction in any medium, provided the original work is properly cited. AoB PLANTS Vol. 2010, plq003, doi:10.1093/aobpla/plq003 & The Authors 2010 1 Parolin and Wittmann — Adaptive responses of trees to ﬂooding in tropical ﬂoodplain systems habits or instincts, adapting that individual better to new The four large wetlands chosen for our analysis are conditions, would tell upon its vigour and health?’ the Central Amazonian ﬂoodplains of South America, (Darwin, 1842). Accordingly, the present study discusses the Okavango Delta region of Botswana, Africa, the the struggle for life in the forests of large ﬂood-pulsed Mekong ﬂoodplains of South-east Asia and the tropical wetlands in relation to what is known of variations in wetlands of Northern Australia (Fig. 1; Table 1). These structure, physiology and biochemistry that confer resili- ecosystems, each on a different continent, were ence. Contrary to the wisdom of Darwin, we cannot, chosen largely on the following pragmatic grounds. We unfortunately, deal with differences within populations looked for very large tropical freshwater ﬂoodplains because such data are very difﬁcult to obtain for these with forest patches (i.e. trees occurring there naturally) huge ecosystems. Instead, our aim is to bring together where ﬂooding occurs with regularity (the ‘ﬂood pulse’ data on responses of trees to ﬂooding in the freshwater of Junk et al., 1989), is characterized by high amplitudes wetlands of tropical environments, emphasizing the and where it is long-lasting (weeks or months). We were varying responses to different wetland structures and careful not to include areas merely prone to ﬂash ﬂoods ﬂooding conditions extant in tropical freshwater ﬂood- following heavy rain. Our assessments are based on plains of four continents. Although Gopal et al. (2000) many diverse publications and disparate data concern- have published a book on the biodiversity of wetlands ing the effects of ﬂooding on species richness, ecophy- and Junk (1997) produced a review of comparative biodi- siology and distribution of tropical trees. versity in ﬂoodplains around the world, there is no one While selecting our four ecosystems, it soon became publication which focuses on adaptation and survival evident that data are extremely scarce, despite their of trees in tropical wetlands. The present article aims importance for biodiversity and human resources to ﬁll this gap. (Wantzen and Junk, 2000). We were forced to exclude Fig. 1 Map indicating the approximate location of the four chosen ﬂoodplain forests. 2 AoB PLANTS Vol. 2010, plq003, doi:10.1093/aobpla/plq003 & The Authors 2010 Parolin and Wittmann — Adaptive responses of trees to ﬂooding in tropical ﬂoodplain systems Table 1 Characteristics of the four chosen ﬂoodplain ecosystems on four continents with a monomodal ﬂood pulse Central Okavango Delta Mekong Tonle Sap Kakadu Region in Amazonia Northern Australia ... ........... ........... ........... ........... ........... ........... ........... ........... ............ ........... ........... .. ......... ........... ........... ....... Continent South America Africa Asia Northern Australia ′ ′ ′ ′ ′ Geographical position 3815 S, 59858W18830 –208S, 228 –248E138N, 1048E1382 S, 133831 E Latitude 0 19 13 12 Age of ecosystem (Irion 2.4 million years 2.5 million years 7500 years 4000 years et al., 1997; Junk et al., 2006) Height asl (m) 0 – 50 1000 0 – 50 0 – 50 Connected rivers Major river Major river system Major river system Smaller rivers system Floodplain area (km ) 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 8 m Root level ,2m 1m height Flood duration where trees 7 months Several weeks? 6 – 8 months .6 months grow 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 Open savanna to 70 % of large trees and forest cover open areas Tree/canopy height 20 – 30 m 5 – 6 m 7 – 15 m 20 m Woody species (Junk et al., .1000 180 70 21 2006) Number of ﬂood-tolerant .1000 10 15 5 tree species Incidence of endemic tree High Very low Low Low? species Tree species diversity High Very low Few dominant species Low? Human pressure Low Low? Very high (wars; ﬁshing) Minimal Human impacts Timber Subsistence agriculture; Timber; ﬁshing; paddy Cattle grazing; tourism; extraction; ﬁsheries rice mining ﬁshing; cattle ranching Continued AoB PLANTS Vol. 2010, plq003, doi:10.1093/aobpla/plq003 & The Authors 2010 3 Parolin and Wittmann — Adaptive responses of trees to ﬂooding in tropical ﬂoodplain systems Table 1 Continued Central Okavango Delta Mekong Tonle Sap Kakadu Region in Amazonia Northern Australia ... ........... ........... ........... ........... ........... ........... ........... ........... ............ ........... ........... .. ......... ........... ........... ....... Changes Increasing Soil salinization due to tree Dramatic ﬂuctuations Invasion by alien plants incidence and felling; expansion of in water level of and animals; changed severity of agriculture; Mekong River; ﬁre regime; water drought agrarian-degradation; frequent ﬂoods and pollution from predicted degeneration of lower water levels in urban-tourism, mining major vegetation types dry season—an and salinization; sea from increased drying increasing problem level rise (Junk et al., (Ringrose et al., 2002) for farming (IUCN, 2006) 1991). many of the largest wetlands, e.g. the Congo basin in hydrology and climate. By comparing diversity and tree Africa or the Orinoco ﬂoodplains in Venezuela, because responses in four ﬂoodplain ecosystems on different only basic data on hydrology and climatology are avail- continents, we attempt to improve our understanding able, with almost no information on plant distribution, of the factors inﬂuencing the spatial distribution of tree adaptations and ecophysiology. It is important to plants, diversity of species and adaptations, and thus bring attention to such poorly researched wetlands, contribute to our knowledge of tropical wetland which are often inaccessible for social and political ecology. In this way, we hope to assist in the successful reasons but are threatened by the ever-increasing restoration of degraded ﬂoodplains and promote the human population and its need for water, waterways sustainable use and conservation of these highly valu- and hydroelectric power. The destruction is so fast that able ecosystems. we may never learn of the adaptations underpinning the success of the tree species in these areas. Flooding as a stress factor We are aware that differences between the four ecosys- tems are large, especially in respect of the inﬂuence of ﬁre Flooding with freshwater, although less harmful than and salinity. Those which are dominated by grasslands ﬂooding with saltwater, poses a multitude of constraints (Okavango and Northern Australian ﬂoodplains) are sub- on growth, survival and reproduction. Trees are basically jected to regular ﬁre (Heinl et al., 2004, 2006, 2007), terrestrial organisms and, in general, die more readily in whereas in the forest-dominated ﬂoodplains of Amazonia response to ﬂooding than to desiccation (Larcher, 1994). and Mekong, ﬁre plays no signiﬁcant role. In the Oka- Flooding involves inundation of part or all of vango, the high evapotranspiration causes salinity pro- the aboveground structures, whereas waterlogging is blems, which are negligible in the remaining three restricted mainly to inundation of the soil and rhizo- ecosystems. Also, ﬂooding amplitudes vary widely sphere (Colmer and Pedersen, 2008). Totally submerged between the ecosystems, with about 2 m in the Okavango plants have no direct contact with atmospheric oxygen and Northern Australian, 8 m in the Mekong and 15 m in and sunlight is weak or extinguished. Inundated soils the Amazon ﬂoodplains (Table 1). This implies that com- become hypoxic or anoxic within a few hours as the plete submergence of saplings and trees occurs only in combined result of oxygen consumption by respiring the Mekong and Amazon, posing different constraints roots plus micro-organisms and insufﬁciently fast diffu- for plant life than merely waterlogging of roots and sion of oxygen through water to replace the amounts stems (Parolin, 2009). However, our review is readily justi- consumed (Crawford, 1989, 1992; Armstrong et al., ﬁed because the regular ﬂood pulse is a major inﬂuence 1994; Visser et al., 2003). Oxygen depletion in soil is on all ﬂoodplain biology (Junk, 1989; Junk et al., 1989) accompanied by increased levels of entrapped CO , and a dominating stress which requires a suite of adap- anaerobic decomposition of organic matter, increased tations for its survival. solubility of mineral substances, notably iron and Throughout the world, wetland ecosystems are under manganese, and decreased redox potential (Joly and increasing pressure from agriculture, urbanization of Crawford, 1982; Kozlowski, 1984). The resulting chemi- catchment areas, tourism and recreational activities, cally reduced and potentially toxic compounds accumu- construction of impoundments and changes to late, their generation being the result of alterations in 4 AoB PLANTS Vol. 2010, plq003, doi:10.1093/aobpla/plq003 & The Authors 2010 Parolin and Wittmann — Adaptive responses of trees to ﬂooding in tropical ﬂoodplain systems the composition of the soil microﬂora as it responds to needed for survival. With all these constraints, imposed the changing conditions (Ponnamperuma, 1984). In by ﬂooding, this stress is clearly life-threatening for some ﬂoodplains, e.g. those of the Amazon River, sedi- higher plants. The struggle for survival of ﬂooding is mentation rates can be extremely high and the depo- therefore closely linked to the evolution of physiological, sition of sediment can decrease soil aeration and thus phenological, anatomical and morphological adap- favour oxygen shortage in the rhizosphere (Wittmann tations that confer tolerance and underpin successful et al., 2004; Wittmann and Parolin, 2005). Elevated and vigorous growth and fecundity despite the intense decomposition rates of highly productive ﬂoating stress. and non-ﬂoating macrophytes in ﬂoodplains further decrease oxygen concentrations in the ﬂoodwater Floodplain ecosystems (Armstrong et al., 1994). In temperate zones, ﬂooding frequently occurs during Here we characterize four extensive ﬂoodplain ecosys- winter when plants are dormant and light intensities tems present on four continents (Table 1). They include low. In contrast, the ﬂooding period in tropical ﬂood- the Central Amazon ﬂoodplains (where we have the plains occurs when temperatures and light intensities broadest and deepest knowledge of tree ecophysiology), are high and conditions overall are optimal for plant the Okavango Delta in Africa, the Mekong ﬂoodplains in growth. Therefore, the trees are not dormant and must South-east Asia (where relatively little is known about accommodate shortages of oxygen and, for submerged tree ecology) and the Northern Australian ﬂoodplains shoots, shortages of CO too at a time when conditions (where much is known about the herbaceous vegetation, favour fast respiration and depletion of reserves. This but much less about tree responses to freshwater implies that extraordinarily efﬁcient adaptations are 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 Mekong Tonle Kakadu Region in Delta Sap Northern Australia ... ........... ........... ........... ........... ........... ........... ........... ........... ............ ........... ........... .. ......... ........... ........... ....... Continent South America Africa Asia Northern Australia Tree distribution Zonation of trees along the Yes Yes Yes Yes ﬂooding gradient Degree of endemism Elevated Low/absent Low/absent Low/absent Leaf phenology Deciduous species: leaf shedding Yes No Yes ? at high waters Evergreen species Yes Yes Yes ? Reproductive phenology Linked to high water + ﬁsh ? Linked to high ? water + ﬁsh Physiological adaptations Reduction of metabolism and Yes No Yes? ? growth during high waters Morpho-anatomical adaptations Leaf xeromorphism; hypertrophic ?? ? lenticels; adventitious roots; aerenchyma Biochemical adaptations Increased activity of fermentative ?? ? enzymes; more VOC emission AoB PLANTS Vol. 2010, plq003, doi:10.1093/aobpla/plq003 & The Authors 2010 5 Parolin and Wittmann — Adaptive responses of trees to ﬂooding in tropical ﬂoodplain systems 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 ﬂood- plain forests that cover more than 300 000 km (Irion et al., 1997). The mean annual temperature of 26.6 8C changes little, average rainfall is 2100 mm year (Ribeiro and Adis, 1984) and noon light intensities can 22 21 reach 3000 mmol m s 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 (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 pre- dictable, 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 Fig. 2 Floodplain forests in Central Amazonia at high water. (Parolin et al., 2004; Parolin, 2009). At low water levels, (A) Nutrient-rich white-water va ´ rzea ﬂoodplain forest with drought may be a stress factor for several weeks (Junk, macrophytes in the foreground (Victoria amazonica; Rio 1997; Parolin et al., 2010). Natural ﬁres and salt are Solimo ˜ es near Manaus) and forest in the background. absent from this ecosystem. Although large terrestrial (B) Nutrient-poor black-water igapo ´ ﬂoodplain forest (Rio Negro near Manaus) (Photographs: Pia Parolin). mammals play important roles for tree establishment and distribution in the grasslands of other ﬂoodplains, they play no signiﬁcant role in the Amazonian ﬂoodplain ecotourism, however, provide sustainable management (Junk and da Silva, 1997). that partially limits the threats to this ecosystem. The differing origins of the various tributaries of the Tree vegetation Amazonian freshwater ﬂoodplains Amazonian River system can strongly inﬂuence water harbour the most species-rich ﬂoodplain forests in the chemistry, e.g. sources in the western Amazon Andes world (Wittmann et al., 2006). In the nutrient-rich or the Northern and Southern Amazonian Precambrian white-water va ´ rzea, there are more than 1000 shields. The resulting seasonally ﬂooded vegetation ﬂood-tolerant tree species (Fig. 3; Wittmann et al., can roughly be differentiated into the nutrient-rich and 2006). From igapo ´ , the comparatively low number of highly productive white-water ﬂoodplains (varzea) and inventories still does not allow reliable estimates of the nutrient-poor and less productive black-water or overall species richness. However, comparisons from clear-water ﬂoodplains (igapo ´ ) (Fig. 2; Sioli, 1954; both local and basin-wide scales indicate less species Prance, 1979). In Central Amazonia, both ﬂoodplain richness than in the va ´ rzea (Prance, 1979; Ferreira types undergo seasonal water-level changes of up to et al., 2005; Wittmann et al., 2010). Species-poor 10 m (Fig. 3). Trees establish at mean annual ﬂood levels ,7.5 m, corresponding to ﬂooded and/or water- low-lying forests (low va ´ rzea) are remarkably similar throughout the Amazon basin even when separated by logged periods of up to 300 days year (Wittmann et al., 2004, 2006). long distances. Species-rich high-va ´ rzea forests may be Human impact on Amazonian ﬂoodplains is increasing more ﬂoristically distinct, but share 30 % of their tree due to agriculture, cattle and buffalo farming, logging, species with the adjacent uplands (Wittmann et al., civil construction projects, mining and reservoirs for hydro- 2006). Tree species richness and alpha-diversity of electric power (Junk, 2000). Small-scale multiple uses and va ´ rzea forests are signiﬁcantly correlated to ﬂood 6 AoB PLANTS Vol. 2010, plq003, doi:10.1093/aobpla/plq003 & The Authors 2010 Parolin and Wittmann — Adaptive responses of trees to ﬂooding in tropical ﬂoodplain systems river catchment, the tree ﬂora of the va ´ rzea and igapo ´ differ substantially in species composition and diversity (Prance, 1979; Kubitzki, 1989). Comparisons at local and basin-wide scales suggest ﬂoristic similarities between both ecosystems to be ,20 % (Wittmann et al., 2010). The main reason for the diverging ﬂora is the contrasting nutrient level. This seems to act as a dis- tribution barrier for many white-water species migrating to the igapo ´ and vice versa. In addition, alluvial dyna- mism varies, with the white-water ﬂoodplains being highly dynamic systems where constant processes of sedimentation and erosion create a large variety of micro-habitats, thereby increasing biodiversity (Salo et al., 1986; Kalliola et al., 1991; Wittmann et al., 2004). Flooding tolerance and tree distribution There is a clear zonation of plant communities in the Amazonian va ´ rzea along the food-level gradient, which leads to characteristic species associations and forest types. Two main habitats are differentiated (Wittmann et al., 2002): (i) low-varzea forests, inﬂuenced by mean inundations with heights between 3.0 and 7.5 m (corresponding to a mean inundation period of 50 – 230 days year ) and (ii) high-va ´ rzea forests, inﬂuenced by mean inundations with heights of ,3.0 m (,50 days year ). However, the distribution of va ´ rzea tree families differs considerably between low- and high-varzea forests (Wittmann et al., 2006): Fabaceae, Malvaceae, Salicaceae, Urticaceae Fig. 3 Varzea ﬂoodplain forests in central Amazonia at low and Brassicaceae are more important in low-varzea water (Photographs: Florian Wittmann, Max-Planck-Institute forests, whereas Euphorbiaceae, Moraceae, Palmae, for Chemistry, Mainz, Germany). Annonaceae, Meliaceae and Myristicaceae are more important in high-va ´ rzea forests. The clear zonation of tree species along the ﬂood gra- height and length, and to the age of the forest stand ´ ´ dient in both Amazonian igapo and varzea indicates the (Wittmann et al., 2006). Maximum species richness different levels of acclimation and adaptation that these estimated from trees ≥10 cm in diameter at breast species have evolved in order to cope with the season- height (cm dbh) recorded in high-va ´ rzea forests of ally hypoxic/anoxic sites. Trees may disperse to higher Amazonia amounts to 84 species ha in the eastern ﬂooded sites than the parent trees and establish parts of the basin, 142 species ha in Central during the terrestrial phase, but they often prove to be Amazonia and 157 species ha in the southern part intolerant of the peculiar site conditions or quickly lose of western Amazonia (Wittmann et al., 2010). out competitively to better-adapted species (Wittmann Endemism is highest in highly ﬂooded low-lying forests et al., 2010). Many Amazonian ﬂoodplain tree species and was estimated to account for 39 % of the 186 that tolerate high and prolonged inundation show most common Central Amazonian varzea tree species adaptations against a wide range of potentially stressful (Wittmann et al., 2010). One hundred and twelve conditions. For example, they tolerate high sedimen- (60 %) of the most frequent Central Amazonian varzea tation rates when located near the river channels of tree species are generalists and are also to be found in white-water rivers and also tolerate poorly aerated other neotropical ecosystems. Where ﬂooding does not soils when located in backwater swamps. Furthermore, exceed 210 days year (Junk, 1989), trees are the they often tolerate full sunlight and drought during the dominating life form, whereas in longer-ﬂooded terrestrial phases when low river water levels coincide environments, grasses and macrophytes take over. with seasonally low precipitation. Trees that are success- As a result of the different chemical compositions and ful at highly ﬂooded sites are therefore light-demanding nutrient inputs of the ﬂooding water, depending on the pioneer species which also have a high resprouting AoB PLANTS Vol. 2010, plq003, doi:10.1093/aobpla/plq003 & The Authors 2010 7 Parolin and Wittmann — Adaptive responses of trees to ﬂooding in tropical ﬂoodplain systems capacity (Worbes et al., 1992; Wittmann and Parolin, before the end of the ﬂooded phase and remains high 2005). They also grow quickly and exhibit relatively throughout the terrestrial phase (Parolin, 2000). short life cycles as, for example, in the white-water pio- Morphological adaptations of the root system include neers Salix martiana and Cecropia latiloba (Worbes et al., hypertrophy of lenticels, formation of adventitious 1992; Parolin et al., 2002; Scho ¨ ngart, 2003). These suc- roots, development of aerenchyma, and the deposition cessful pioneer trees modify the local site conditions so of cell wall biopolymers such as suberin and lignin in per- much that new seedlings of the same species are no ipheral cell layers (Schlu ¨ ter and Furch, 1992; Schlu ¨ ter longer able to establish at the same site as the parent et al., 1993; De Simone et al., 2002a, b). Different types tree (Wittmann et al., 2010). of above-ground roots, e.g. plank-buttressing and adven- titious roots, are closely related to ﬂooding duration and Tree responses to ﬂooding The terrestrial phase is the habitat dynamics (Wittmann and Parolin, 2005). The main growth period for trees in the Amazonian development of adventitious roots in the oxygenated ﬂoodplains. In contrast, in the ﬂooded period, growth layer at the surface of the ﬂoodwater table and hyper- decreases, metabolic activity slows and even complete trophy of lenticels on the surface of stems just above dormancy is induced in many species. However, none water level are thought to improve the internal oxygen of these responses lasts for the entire ﬂooding period. status by facilitating the entry of oxygen into the Limited growth lasts for only a few weeks and is often root and the stem by the shortest possible pathway followed by new leaf ﬂush, ﬂowering, fruiting and (Crawford, 1992). Pneumatophores are also familiar wood increment while the tree is still ﬂooded (Worbes, adaptations in mangroves but are absent in va ´ rzea 1997; Scho ¨ ngart et al., 2002). After fruit maturation, trees (Junk, 1984) except in palms found in headwater which usually occurs at high water levels (Kubitzki and regions and swamps (e.g. Mauritia, Mauritiella), where Ziburski, 1994), seeds fall into the water and may ﬂoat ﬂood amplitudes are small. Stem nodulation and nodu- and/or are submerged for several weeks without losing lated adventitious roots have been observed in various their viability. Seed germination starts only when the species, and are understood to be adaptations that ﬂood recedes, although some may protrude a radicle allow legumes to ﬁx nitrogen in a ﬂooded environment (Scarano et al., 2003) or even produce a complete (James et al., 2001). The frequency of such nodulation seedling while ﬂoating (Oliveira-Wittmann et al., 2007; among genera can be higher in ﬂooded than in non- Parolin, 2009). In most species, overall growth in height ﬂooded sites in both va ´ rzea and igapo ´ , indicating that and new leaf production are not severely inhibited nodulation may be favoured in ﬂooded areas (Moreira merely by waterlogging of the soil, and elongation may et al., 1992). even be enhanced, as in Senna reticulata. Here, Increased activity of fermentative enzymes such as waterlogging is reported to accelerate seedling shoot alcohol dehydrogenase (ADH), lactate dehydrogenase growth considerably (Parolin, 2001). (LDH), glutamate – pyruvate transaminase (GPT) and Submergence of part of or the entire shoot is a more malate dehydrogenase (MDH) has been observed under severe stress. Most tree species tolerate this in a state anaerobic soil conditions in the roots of several tree of rest and sprout new leaves soon after the water species (Schlu ¨ ter and Furch, 1992; Schlu ¨ ter et al., 1993; recedes. In species with leaves without a thick cuticle De Simone et al., 2002b). In addition, larger amounts or thick outer epidermis walls, leaves rot fast when sub- of volatile organic compounds are emitted to the merged and are shed after only a few days (Waldhoff atmosphere by terrestrial vegetation when ﬂooded and Furch, 2002). Other species may retain their leaves (Kesselmeier and Staudt, 1999). Acetaldehyde and in a healthy state below water for several months. Leaf ethanol may be emitted in larger amounts by ﬂooded shedding during the aquatic phase has been documen- trees and under other stress conditions such as sulphur ted not only in deciduous species but also in evergreen dioxide and ozone exposure, water deﬁcit, freezing and trees, which tend to produce new leaves only slowly at fast-changing light conditions (Kimmerer and Macdo- high water levels (Parolin et al., 2002). Whether decid- nald, 1987; Kesselmeier et al., 1997). Acetaldehyde (and formaldehyde) is exchanged bi-directionally uous or evergreen, and regardless of whether leaves are kept or shed under water, the leaves of Amazonian between the vegetation and the atmosphere, i.e. they ﬂoodplain trees exhibit traits that are generally con- are emitted or taken up, depending on environmental sidered as xeromorphic (Medina, 1983; Waldhoff, 2003). and atmospheric conditions (Kesselmeier et al., 1997). Physiological responses to waterlogging of the soil Recent measurements in the terra ﬁrme Amazonian include reductions of mean CO uptake in aerial leaves rain forest provide evidence that more short-chain alde- ranging from 10 to 50 % slower than in the terrestrial hydes and the corresponding organic acids were taken phase (Parolin et al., 2004). CO uptake rises again up from the air than produced, although release was 8 AoB PLANTS Vol. 2010, plq003, doi:10.1093/aobpla/plq003 & The Authors 2010 Parolin and Wittmann — Adaptive responses of trees to ﬂooding in tropical ﬂoodplain systems observed when ambient concentrations were below a speciﬁc level (Rottenberger et al., 2008). Africa: Okavango Delta The Okavango Delta (Fig. 4) is the world’s largest inland delta. It is located in northwestern Botswana and fed by the Okavango River, which originates in Angola’s western highlands. The ﬂoodwaters take 9 months to ﬂow from the source to the delta due to the extremely gentle gradient. The river discharges about 10 km of water onto the delta fan each year, augmented by 3 2 about 6 km of rainfall, which sustains about 2500 km of permanent wetland and up to 8000 km of seasonal wetland. Interaction between this surface water and the groundwater strongly inﬂuences the structure and function of the wetland ecosystem. The climate is semi- arid, and only 2 % of the water leaves as surface ﬂow and probably very little as groundwater ﬂow. The bulk of the water is lost to the atmosphere. The Okavango River also delivers about 170 000 tonnes of bedload sediment and about 360 000 tonnes of solutes to the delta each year, most of which is deposited on the fan. Local rainfall is low, averaging 490 mm year . This is greatly exceeded by the rate of evapotranspiration (1580 mm year ; Ellery et al., 1993). Temperatures range from maxima of 33.7 8C in summer to 28.7 8C in winter, with a mean relative humidity of 60 – 78 % in summer and 43 – 63 % in winter (Bonyongo et al., 2000). Precipitation data show ,10 mm of rainfall per month from May through October, whereas between January and March, it lies between 120 and 320 mm. The Okavango Delta experi- ences seasonal ﬂooding starting towards the north between October and April, and ending in May, June or July towards the southern part of the delta. Natural ﬂuc- tuations in water level result from variations in annual rainfall in the catchment area and rainfall within the delta itself (Bonyongo, 1999). The delta is almost perma- nently ﬂooded in the north, but only seasonally ﬂooded in the south. The rain falls during the summer and ﬁrst seeps into the parched ground before the rivers start ﬂowing. As it is the dry season, the ﬂoodwaters gradually evaporate Fig. 4 Forested savanna in the Okavango Delta with mopane over the subsequent months, leaving their valuable trees (C. mopane) at high and low water (Photographs: Michael Heinl, University of Innsbruck, Austria). salts and minerals in the ground. Fire plays a role in this ecosystem (Heinl et al.,2004, 2006, 2007). It is more frequent in the ﬂoodplains than adapted plants. As a consequence, locally high biological on the drylands because of greater biomass and fuel load. The incidence of ﬁre on the drylands correlates productivity occurs, which, in turn, supports many with annual rainfall events, while the frequency of grazing mammals (Heinl et al., 2004, 2006, 2007; ﬁres on ﬂoodplains is determined mostly by ﬂooding Tacheba et al., 2009). frequency. The greatest burn potential is found on ﬂood- Changes in the types of vegetation cover, due to both plains that become ﬂooded every second year. Temporal human and natural causes, have taken place since the variations in ﬂooding cause accumulation and sudden ﬁrst vegetation map was produced in 1971 (Ringrose et al., 2002). In the south-west, shifts to thorn trees mobilization of nutrients which are readily utilized by well- AoB PLANTS Vol. 2010, plq003, doi:10.1093/aobpla/plq003 & The Authors 2010 9 Parolin and Wittmann — Adaptive responses of trees to ﬂooding in tropical ﬂoodplain systems prevail, whereas in the eastern part of the country, wide- nutrient and sediment supply and sediment deposition, spread bush encroachment takes place. An increased and with the nature of the substratum, play a role human population density suggests that these are (Ellery and Tacheba, 2003). Trees, which are almost anthropogenic (agrarian-degradation) effects. Wherever exclusively conﬁned to islands, are particularly broadleaved evergreen trees are cleared, widespread important as they lower the water table beneath salinity occurs (Ellery et al., 2000). In the sparsely islands relative to the surrounding wetlands and settled central Kalahari region, changes from tree cause a net inward ﬂow of groundwater (McCarthy, savanna to shrubs may indicate the inﬂuence of 2006). Island fringes are generally characterized climate change with the associated effects of ﬁres and by a broadleaf evergreen riparian community of local adaptations. Projection of future vegetation Syzigium cordatum, Ficus verruculosa, F. natalensis, changes to about 2050 indicates degeneration of the F. sycamorus, Phoenix reclinata, Garcinia livingstonei major vegetation types due to expected drying of the and Diospyros mespiliformis. This gives way to local climate (Ringrose et al., 2002). interiors dominated by Acacia nigrescens, Croton megalobotrys and Hyphaene ventricosa.The most Tree vegetation The ﬂoodplains consist mostly of central regions are characterized either by short, grasslands with 1250 species (Ellery and Tacheba, 2003). sparse grassland dominated by Sporobolus spicatus or Woody plants are found in the riverine forests (e.g. are completely devoid of vegetation with sodium species of Ficus). On the higher, often salt-rich islands carbonate (trona)-encrusted soil surrounding a central which are ﬂooded less frequently, acacias, mopane pan of extremely high conductivity (Ellery et al., (Colophospermum mopane; Fig. 4) and the woody shrub 1993). Soil pH and mineral content (especially Pechuel-loeschea leubnitziae (a weed in many sodium) and groundwater chemistry (conductivity and ecosystems) predominate. Ellery and Tacheba (2003) pH) play a major role in the spatial distribution of reported 43 woody species in total in the dryland plant communities. However, Bonyongo et al. (2000) riverine woodland. None of these is endemic since most state that the timing and duration of the seasonal of them also occur in South Africa and Namibia ﬂooding are the most important factors determining (M. Heinl, University of Innsbruck, Austria, pers. comm.). the species composition of the vegetation. Despite an overall high plant species diversity in the delta, only 18 % of the vegetation is phanerophytes Tree responses to ﬂooding The riparian trees remain (trees), compared with 56 % hemicryptophytes and 8 % green all year and partly sustain their growth as a result true aquatic species (Ellery and Tacheba, 2003). of groundwater uptake in the dry periods. Riverine Although seldom ﬂooded, the riparian woodland trees forests in savanna areas depend on the river for their have their roots in the water table in permanent and water supply (Hughes, 1988). Flooding and lateral seasonal swamps (Ellery and Tacheba, 2003). Acacias groundwater ﬂow stimulate growth (Ringrose, 2003). and mopane are less ﬂood tolerant with pechuel Renewal of leaf growth, however, is primarily related to showing greater tolerance of ﬂooding, and also of ﬁre. rainfall, not to ﬂood events in the distal delta (Ringrose, Riparian woodlands are responsible for much of the 2003). Regenerative phenology has not yet been water lost from the ecosystem and deplete groundwater described for the trees of the Okavango Delta. In by transpiration (Ringrose, 2003). This leads to the general, however, riverine forests in African savannas uptake of toxic solutes by the transpiring trees, which show a high percentage of even-aged stands of trees, results in exceptionally good quality surface water. The indicating that hydrological factors are important for trees therefore ensure that islands of vegetation func- tree regeneration because they provide spasmodically tion as ‘kidneys’ within the landscape—a reason why favourable circumstances for establishment (Hughes, riparian woodlands are considered particularly impor- 1988). Although there are some data on the phenology, tant habitats in this ecosystem (Ellery and Tacheba, growth rhythms, physiological responses and 2003). morphological adaptations to ﬂooding in the non- Flooding tolerance and tree distribution Vegetation on woody vegetation (Ellery et al., 1992; Mantlana, 2008), islands in the perennial swamps of the Okavango Delta almost no published data were found for trees in the exhibits a marked zonation (Ellery et al., 1993). This is Okavango Delta. An exception is a recent study of leaf related primarily to aspects of the hydrological regime gas exchange of C. mopane in northwest Botswana such as depth, duration and timing of inundation, but (Veenendaal et al., 2008). Here, differences in mainly to soil and groundwater salinity (Ellery and physiological and morphological traits between tall and Tacheba, 2003). Also, processes associated with short forms of mopane [C. mopane (Kirk ex Benth.) Kirk 10 AoB PLANTS Vol. 2010, plq003, doi:10.1093/aobpla/plq003 & The Authors 2010 Parolin and Wittmann — Adaptive responses of trees to ﬂooding in tropical ﬂoodplain systems ex J. Le ´ onard] trees were compared. The tall form had a smaller leaf:ﬁne-root biomass ratio, higher leaf nitrogen concentrations and less negative leaf water potentials. These differences appeared to be attributable to differences in root depth and density between the physiognomic types, and thus to different ways that the two growth forms exploit available soil water, the tall form having a consistently more conservative water-use strategy as the dry season progressed than the short form (Veenendaal et al., 2008). Asia: Mekong ﬂoodplains The Mekong is the world’s eighth-longest river (Sarkkula et al., 2005). The lower Mekong basin in Cambodia and Vietnam includes ﬂoodplains (Fig. 5) which are among the few remaining global examples of relatively intact Fig. 5 Asia: Mekong ﬂoodplains in Giang Province at high and functioning ﬂoodplains in a large river basin. This water (Photographs: Manfred Niekisch, Zoological Garden is the case despite its high-density human population Frankfurt, Germany). of 54.8 million. It is widely accepted that this is one of the explanations for the highly productive ﬁsheries of the Mekong and its very high biological diversity. The ﬂoodplains cover 795 000 km (Sarkkula et al., 2005). large hydroelectric dams (Wikramanayake and Rundel, Since the only available data on tree ecophysiology 2002). An additional threat is the invasion of the come from Tonle Sap Lake, which is fed by the Mekong giant mimosa (Mimosa pigra). This aggressive shrubby River, we concentrate on the 15 000 km of ﬂoodplain species becomes established in fallow ﬁelds and dis- forest of this lake. turbed shrub land and swamp forest area after clear- At the peak of the wet season, the Tonle Sap can ance or burning. Once established, giant mimosa expand to 250 km long and up to 100 km wide in forms dense, impenetrable thickets of spiny growth places. The lake is shallow, measuring only 1 – 2 m at that choke out other native species and have little its deepest in the dry season, rising to more than 10 m value as wildlife habitat. in the wet season. As a result, when it ﬂoods, the total Tree vegetation The swamp shrub lands and forest of inundated area increases 4-fold. Mean annual rainfall the Tonle Sap Freshwater Swamp Forests eco-region is 1600 mm. Much of this eco-region is ﬂooded for at include two forest associations that have been least 6 months—from August to January or February described for the extensive ﬂoodplain area of Tonle (Wikramanayake and Rundel, 2002). Sap. This is a short-tree shrub land covering much of Most of the delta’s human inhabitants ﬁsh, farm and the area and comprises a stunted swamp forest live at subsistence levels. Although the annual ﬂood around the lake itself. Similar swamp forests are also cycle of the Mekong provides resources for these present along the ﬂoodplains of the Mekong and other people, it is a fragile balance. The ﬂoodplains of the major rivers in Cambodia (Wikramanayake and Rundel, Tonle Sap have been strongly affected by human 2002). Swamp forest originally dominated the activity and little of the original forest cover remains dry-season shoreline of Tonle Sap, covering about 10 % pristine. Throughout the dry season, burning is of the ﬂoodplain. It occurred in a mosaic of patch common, with ﬁres used to clear land before ploughing stands rather than as continuous forest stands or to facilitate access. Flooding has recently damaged (Wikramanayake and Rundel, 2002). Typically, these the infrastructure and caused extensive loss of property forests are ﬂooded for 6 – 8 months each year and and livelihood. At the same time, roads and their most species lose their leaves during this time. A associated developments have had a considerable continuous canopy 4 m high is formed by the impact on ﬂooding by fragmenting the wetlands and interrupting the natural ﬂow of water, sediments, dominant deciduous woody species. The most common species belong to the Euphorbiaceae, Fabaceae and nutrients and aquatic life. These impacts negate the beneﬁcial effects normally brought by the natural Combretaceae together with Barringtonia acutangula ﬂood cycle. The most signiﬁcant threat comes from and Diospyros cambodiana. Terminalia cambodiana is infrastructure development, particularly 149 planned an important local endemic. The forest vegetation is AoB PLANTS Vol. 2010, plq003, doi:10.1093/aobpla/plq003 & The Authors 2010 11 Parolin and Wittmann — Adaptive responses of trees to ﬂooding in tropical ﬂoodplain systems dominated by the ﬂood-tolerant tree Melaleuca cajuputi 2004). These ﬂoodplains are in an area broadly known as ssp. cumingiana (Safford et al., 2009). The swamp forest the ‘wet – dry tropics’. These have been deﬁned as areas is 7 – 15 m high. Although M. cajuputi may reach 40 m in with an annual rainfall of 600 – 1600 mm spread over Australasia, in the Mekong ﬂoodplain trees are no taller 4 – 7 months. The size of forested wetlands comprises 2900 km . There is a wet season characterized by thun- than 22 m even when 100 years old (Safford et al., derstorms, tropical cyclones and rain depressions. These 2009) and most commonly form bushes 3 – 6 m tall. commence late in the year (November – December) and Flooding tolerance and tree distribution Little last for 3 – 4 months (Taylor and Tulloch, 1985). The information is available on plant distribution and hydrological cycle has been identiﬁed as being impor- zonation along the Mekong River ﬂoodplains. In the tant in shaping the pattern of the vegetation in the Tonle Sap ﬂoodplain, the structure and composition of freshwater wetlands (Finlayson et al., 1989). Water woody vegetation appear to be largely a function of ﬂows on a seasonal basis, starting early in the wet the micro-heterogeneity of soil moisture and seasonal season and lasting until after the end of the rains. Flood- ﬂood dynamics. Tree height is related to soil moisture ing occurs once the catchment is saturated; heavy falls conditions, with the tallest trees growing closer to the of rain later in the season generate more widespread permanent lake basin and shorter ones at the ﬂooding. Freshwater ﬂow in the creeks and rivers periphery of the ﬂoodplain. Several species with ceases within a few months of the end of the rains, shrubby growth forms in this peripheral community and the creeks and ﬂoodplains dry out except for a few reach tree size in swamp forest habitats permanent swamps and billabongs (Finlayson et al., (Wikramanayake and Rundel, 2002). 1990). Some creeks or river reaches are fed by springs or groundwater seeps. Analyses of the water quality Tree responses to ﬂooding In the Mekong ﬂoodplains, within thick stands of submerged herbs and emergent the terrestrial phase is the main growth period for grasses late in the wet season reveal that, in addition trees. Most woody species of the ﬂoodplain of Tonle to variations in dissolved O and CO concentrations, 2 2 Sap are deciduous, a probable adaptation to the the water becomes alkaline in the late afternoon when periodic ﬂood pulse (Safford et al., 2009). Rather than CO concentrations are at their lowest. lose their leaves in the dry season, however, these Fire and invasive plants and animal species have a sig- species lose their leaves when submerged as the lake niﬁcant impact on the extent and distribution of plant deepens and the plants become partially or totally species and of the land cover (Finlayson et al., 1990). submerged. However, there are several woody species Damage to the natural levees that separate freshwater that remain evergreen (Lamberts and Koponen, 2008), and saline wetland communities caused by climate despite leaves being submerged for 6 – 8 months each change and by feral animals (especially water buffalo) year. With only a few exceptions, ﬂowering and fruit may also change the vegetation. Notable responses by production in the ﬂoodplain trees and shrubs are ﬂoodplain vegetation have already occurred following delayed for several months after the ﬂush of the removal of feral buffalo (Skeat et al., 1996). new leaves. Fruits reach maturity at the time of Tree vegetation Around 55 % of the terrestrial vegetation submergence, suggesting that ﬁsh may be important in the Kakadu Region is tropical tall grass savanna, dispersal agents (Safford et al., 2009). Unfortunately, composed of eucalypt-dominated open forest and no data on physiological responses to ﬂooding and woodland with a 1- to 2-m-tall grassy understorey morphological adaptations of the Mekong ﬂoodplain (Finlayson, 2005). A further 30 % of the region is covered tree species were found. There are some publications by heaths, and open woodlands with a sparse grass on the ecophysiology of non-ﬂooded environments, understorey. Closed-canopy monsoon rainforests are mainly dealing with drought-prone deciduous and dry restricted to ﬂoodplains, besides lowland springs, rock evergreen tropical forests (Tanaka et al., 2004; Ishida outcrops and beach levees. The seasonally inundated et al., 2006; Huete et al., 2008). Few, if any, studies ﬂoodplains include fringing woodland and forests, and describe the responses of trees typical of the Mekong billabongs (seasonally or permanently inundated lagoons ﬂoodplain. associated with the ﬂoodplain or river channels) Australia’s tropical ﬂoodplain wetlands (Finlayson, 2005). The forests are inundated by up to 1 m Floodplain wetlands are uncommon in the mostly arid of water during the wet season but are dry at other times. continent of Australia. However, an important partly Gallery and ﬂoodplain forests in monsoonal Northern forested wetland, the Kakadu National Park in Northern Australia are mostly sclerophyllous and dominated by Australia, extends over 99 000 km (Lowry and Finlayson, ﬁve closely related species of Melaleuca (Myrtaceae), 12 AoB PLANTS Vol. 2010, plq003, doi:10.1093/aobpla/plq003 & The Authors 2010 Parolin and Wittmann — Adaptive responses of trees to ﬂooding in tropical ﬂoodplain systems among which niche differentiation is unclear (Franklin environment. They noted that variability due to changes et al., 2007). The most important tree communities in the hydrological cycle has resulted in many speciﬁc (Finlayson, 2005) include Melaleuca open forest and adaptations that enable the plants to establish and grow woodland with a tree canopy cover of 10 – 70 %. These (Finlayson et al.,1989). The few details given include that are dominated by one or more Melaleuca species trees of the ﬂoodplains often have modiﬁed bark (M. viridiﬂora and M. cajaputi around the edges and at structures such as the corky bark of Sesbania formosa the northern end of the ﬂoodplain). The dominant and B. acutangula, and the distinctive papery bark of species in the backswamps that are inundated for 6 – 8 some melaleucas which possesses internal, longitudinal, months every year is M. leucadendra. There is also gas-ﬁlled passages. It is also said that the majority of open woodland providing canopy cover of ,10 % domi- seed-dispersal mechanisms involve water, even though nated by M. leucadendra. There are 12 terrestrial tree many parts of the ﬂoodplains are drier for a longer species, including Eucalyptus spp., Pandanus spiralis, period than they are wet. However, it is not clear if this Lophostemon lactiﬂuus and Syzygium suborbiculare. also applies to trees. Nothing seems to be known of the Paperbark swamp forest is dominated by trees including physiological and morphological adaptations of trees of M. viridiﬂora, M. cajaputi and M. leucadendra, and to a the Kakadu National Park. Responses to ﬂooding by lesser extent B. acutangula and Pandanus spp. melaleucas of North Queensland have, however, been The productivity of the ﬂoodplain vegetation changes documented and these may be relevant to the Kakadu with the annual cycle. This is indicated by periodic litter- since this is an environment with a median duration of fall from Melaleuca trees. In an intensively sampled inundation of 75 days (McJannet, 2008). Using a Melaleuca forest on the Magela ﬂoodplain, total litterfall heat-pulse method, McJannet found a strong 22 21 was 0.7 kg m year , whereas at a second site on relationship between tree size and tree water use, and the ﬂoodplain, less intensively investigated, a value of showed that transpiration by M. quinquenervia was 22 21 1.5 kg m year was recorded (Finlayson, 1988). unaffected by inundation. This ability to transpire during Comparative data for Melaleuca forests are limited to a ﬂooding may be due to physiological adaptations of this small number of studies of different species found in species, and to dynamic root systems that can quickly the wetlands in southern Australia. These deposit an respond to rising and falling water tables and dense 22 21 annual litterfall of 0.39 – 0.43 kg m year (Finlayson networks of ﬁne ageotropic roots, which grow on and et al., 1993). The distribution and density of trees on at within the papery bark. Waterlogged M. quinquenervia least part of the ﬂoodplain were seen to change con- also develops negatively gravitropic roots (Sena Gomes siderably between 1975 and 1990 (Finlayson, 2005), indi- and Kozlowski, 1980). cating the dynamic nature of the wetland environment. A study by O’Grady et al. (2006) of Corymbia bella and M. argentea in riparian zones of the Northern Territory, Flooding tolerance and tree distribution The duration of along the Daly River, showed that throughout the dry ﬂooding, depth of water and the velocity of water ﬂow are season predawn leaf water potentials were above major determinants of the vegetation composition of the 20.5 MPa, indicating that neither species suffered sig- ﬂoodplain (Finlayson et al., 1989). The changing pattern is niﬁcant unrelieved water-deﬁcit stress during the dry a function of both the ﬂooding and drying phases of the season. This was despite low soil matric potentials in hydrological cycle (Finlayson et al., 1989, 1990). The the top 1 m of soil. There were also no seasonal differ- vegetation of the ﬂoodplain billabongs is much ences in tree water use in either species. Xylem sap deu- inﬂuenced by adjacent plant communities on the terium concentrations indicated that M. argentea trees seasonally inundated ﬂoodplain (e.g. grass mats along the riverbank relied principally on river water or extending across the ﬂoodplain and into the billabongs). shallow groundwater, whereas C. bella growing along Franklin et al. (2007) propose that Melaleuca forests the levee was reliant on deep soil water reserves occur where disturbance by ﬁre and/or ﬂoodwater is too (O’Grady et al., 2006). This study demonstrates strong great for rain forest to persist, making them the wetland gradients of tree water use within tropical riparian com- analogue of the eucalypt species that dominate the munities in Northern Australia which probably can be better-drained parts of north Australia. extrapolated to the Kakadu Region. Tree responses to ﬂooding Little information is available on physiological responses and adaptations of trees in Discussion Australian ﬂoodplains. Cowie et al. (2000) have reviewed adaptations in wetlands by herbs and macrophytic We have demonstrated that in all tropical continents, vegetation, and summarized the nature of the ﬂoodplain highly adapted tree species populate the ﬂoodplain. AoB PLANTS Vol. 2010, plq003, doi:10.1093/aobpla/plq003 & The Authors 2010 13 Parolin and Wittmann — Adaptive responses of trees to ﬂooding in tropical ﬂoodplain systems There is little taxonomic overlap except for the Asian and an alternative, albeit inefﬁcient, alternative source of Australian ﬂoodplain where the genus Melaleuca domi- energy to Krebs cycle-based aerobic respiration nates, but Barringtonia also occurs in both ecosystems. (Crawford, 2003). Induction of the activity of fermenta- Forest types range from highly diverse dense forests tive enzymes such as ADH, LDH, GPT and MDH has (Amazonia, Mekong) to gallery forests or small tree been observed under anaerobic growth conditions in stands scattered in savanna-dominated environments Amazonian tree species (Schlu ¨ ter and Furch, 1992; (Okavango, Kakadu Region). In each ﬂoodplain, the Schlu ¨ ter et al., 1993; De Simone et al., 2002a; Ferreira, aquatic phase occurs when temperature and light con- 2002), and this probably also applies to species of the ditions are optimal for plant growth and development, Okavango, Mekong or Kakadu regions. implying the need for developmental and biochemical Underwater photosynthesis is common in temperate adaptations rather than relying on avoidance through herbs (Mommer and Visser, 2005) and postulated for dormancy (Parolin et al., 2004). Flooding patterns vary, some tree species in Amazonian ﬂoodplains (Schlu ¨ ter with durations ranging from more than half a year et al., 1993; Waldhoff et al., 2002; Parolin, 2009). It is (Amazonia, Mekong, partly Kakadu) to only a few weeks possible that underwater photosynthesis, which both (Okavango). The most important characteristic is the pre- increases internal oxygen concentrations and raises dictability of the time of the annual ﬂood (the ﬂood pulse energy supply, could partially alleviate the adverse concept of Junk et al., 1989). This predictability has effects of submersion. This may well be of adaptive sig- allowed the trees to form morphological and physiologi- niﬁcance in the trees of the Mekong ﬂoodplains where cal adaptations against ﬂooding. On the other hand, as ﬂood heights can exceed 2 m and might be associated a consequence of the differing ﬂood intensities and differ- with periods of complete submergence. ent ﬂooding tolerance of the plants along the ﬂooding In the four ﬂoodplains that we examined, the terres- gradient, tree distribution presents clear zonations in all trial non-ﬂooded phase is when tree growth is most vig- orous. However, many tree species retain actively four ecosystems. However, our wish to compare the underlying physiological and morphological reasons for ﬂowing phloem sap even during ﬂooding (Waldhoff this zonation was frustrated by a lack of relevant pub- et al., 2002; Visser et al., 2003), indicating that active lished data. A small number of species from the Asian, sources and sinks for respirable substrates operate African and Australian ﬂoodplains have been analysed under these conditions. A set of metabolic adaptations to date, and the dearth in our knowledge is alarming in is inevitably required to achieve this. We suggest that in the face of the speed at which the ﬂoodplains are being most tree species of the tropical ﬂoodplains, the damaged or destroyed and the pressing need for well- primary morphological strategies in response to ﬂood- informed recovery programmes. ing are similar to those of temperate species (Jackson Clearly, it is difﬁcult to be sure of the extent to which and Armstrong, 1999) or in the well-analysed tropical trees in the four ecosystems share similar underlying Amazonian ﬂoodplains (Parolin et al., 2004, 2010). In adaptations to ﬂooding stress. Phenological data indi- particular, there must be a development of gas-ﬁlled cate that this may be the case. For example, many spaces in the roots and stems to allow diffusion of deciduous species respond to ﬂooding with leaf shed- oxygen from the aerial portions of the plant into the ding, presumably as a means of reducing transpiration roots. Morphological adaptations that favour this are and water loss at a time when hypoxic or anaerobic hypertrophy of lenticels, formation of adventitious roots may offer large resistances to water uptake. roots, plank-buttressing and stilt rooting, development However, evergreen species are common in each of the of aerenchyma, and the deposition of cell wall biopoly- ﬂoodplains that we examined with the exception of mers such as suberin and lignin in the root peripheral the Australian wetlands. This indicates the possibility cell layers. The formation of aerial roots may compen- that other mechanisms exist to reduce transpirational sate for losses of respiration and function by roots losses, although here too a proportion of the leaves of affected by lack of oxygen in the soil. Under experimen- evergreen trees is also lost during ﬂooding. tal conditions with stable water levels, most species Physiological adaptations similar to those well known show the potential to produce adventitious roots. But, in temperate and Amazonian species can also be in the ﬁeld, they are seldom found, probably because expected in the tree species of the Mekong, Okavango their formation is hampered by a rapidly changing and Kakadu ﬂoodplains. Among the most important water level. Leaves of tropical forests in general, and will be root system adaptations to anoxia (Crawford, the Amazonian ﬂoodplain forests in particular, com- 2003; Gibbs and Greenway, 2003). These will include monly have xeromorphic structures (Waldhoff, 2003). the accumulation of adequate carbohydrate reserves This attribute contributes to suppressing water loss at and the ability to switch to alcoholic fermentation as times of low water supply. This can apply to tree 14 AoB PLANTS Vol. 2010, plq003, doi:10.1093/aobpla/plq003 & The Authors 2010 Parolin and Wittmann — Adaptive responses of trees to ﬂooding in tropical ﬂoodplain systems crowns during the aquatic phase and to periods of Conclusions and forward look drought in the terrestrial phase. Our comparative review on the adaptive responses of Strict comparability between the four ecosystems we trees to ﬂooding in four tropical freshwater ﬂoodplains studied is limited by region-speciﬁc constraints such as of different continents demonstrates that substantial the inﬂuence of groundwater quality and the incidence data about the ﬂoodplain tree ﬂora, its ecology of ﬁre and/or salt. These constraints might also be and functioning are lacking. Despite many physio- responsible for the large differences in tree diversity ecologically motivated studies on trees of the Central encountered in the four ecosystems. It is also true Amazonian ﬂoodplains, and a few studies on other tropi- that the two forested ﬂoodplains also exhibit striking cal freshwater ﬂoodplains, we are still only at the start of differences in their diversity. Tree species richness in our understanding of how terrestrial plants, especially the Amazonian white-water ﬂoodplains (va ´ rzea) is trees, cope with extended periods of ﬂooding. However, 10 times greater than that in the forests of Cambodia this knowledge is fundamental to understanding the (Tonle Sap; Campbell et al., 2006) and about three times evolution of ﬂooded landscapes and their organisms, above that in the Brazilian Pantanal, another extensive as well as their interaction with non-ﬂooded ecosystems. wetland dominated by savannah (Wittmann et al., The range of plant responses recorded in the different 2006). One reason for the comparatively high tree tropical ﬂoodplains leads us to the following conclusions: species richness in varzea forests of Amazonia is the coexistence of species well adapted to ﬂooding and generalist species that also occur in the uplands (Witt- (i) Regular ﬂooding is a severe stress to trees, resulting in reduced species richness compared with non- mann et al., 2006). Very little is known about the ﬂooded uplands. number of generalists vs. specialists among ﬂoodplain (ii) The regular ﬂood pulse has given rise to a large trees. In Amazonia, only a few tree species occur diversity of growth forms and adaptations by along the whole ﬂooding gradient, with most being trees. These seem to increase in variety with the restricted to very small topographic amplitudes (Witt- age of the respective ﬂoodplains and the climatic mann et al., 2002). Only 20 % of all va ´ rzea tree species occur in both low- and high-land habitats, stability to which they were exposed. (iii) Most ﬂoodplain tree species are restricted to small demonstrating the striking difference in ecophysiological topographic amplitudes along the ﬂooding gradi- constraints for tree survival and growth along the ﬂood- ing gradient. In the other ﬂoodplains of the world, gen- ents, leading to a distinct zonation of tree species. This implies different mechanisms or com- eralists may dominate, as in savanna ecosystems. binations of mechanisms conferring zone-speciﬁc However, we have too little information to speculate tolerance to ﬂood stress. This zonation is not about the ecological amplitude of trees in ﬂoodplains. dependent on the height of the ﬂooding amplitude. The degree of ﬂood tolerance depends, in large part, Most highly ﬂooded (.2 m) tree species react to on the time taken to colonize the ﬂoodplains. Morpho- high-water periods with leaf shedding, which is logical adaptations may be remnants of pre- adaptations from non-ﬂooded upland tree species associated with decreased metabolism and growth. (Kubitzki, 1989) which evolved further, leading over (iv) The occurrence of evergreen tree species does not time to highly adapted species. Thus, the phylogenetic development of adaptations depends on the age of depend on the height and magnitude of ﬂooding, since evergreen species are found in all three the ecosystem, and also on the dominating plant ﬂoodplains. families that colonized these ecosystems originally. In (v) Although the responses of trees to ﬂooding seem each of the four ecosystems, there are large differences in developmental age (Table 1). This implies different to be manifold, variability within an ecosystem is greater than that between ecosystems despite stages of adaptations among the organisms living widely differing species/genera/families dominat- there. Amazonian and African ﬂoodplains are extremely old, dating at least to the Pleistocene (.12 million ing the respective ﬂoodplains. (vi) Endemic tree species are rare, except in Amazonian years old), or even earlier. Such ancient landscapes ﬂoodplains. This may be the outcome of a mark- will have experienced several changes in climate and hydrology, i.e. during the glacial and interglacial edly stable climate over geological time. (vii) Future research must address the current paucity of periods. In contrast, the Mekong River basin and the published data on the ecophysiology and adap- Australian ﬂoodplains are much younger, and are tations and requirements of trees in the major thought to be no older than 7500 and 4000 years, ﬂoodplain forests. respectively (Junk et al., 2006). AoB PLANTS Vol. 2010, plq003, doi:10.1093/aobpla/plq003 & The Authors 2010 15 Parolin and Wittmann — Adaptive responses of trees to ﬂooding in tropical ﬂoodplain systems adaptation to adversity. Studies in Ecology 11. Oxford: Blackwell (viii) Attention also needs to be given to small wetlands Scientiﬁc Publications, 105 – 129. along small rivers or in remote places. These areas Crawford RMM. 1992. Oxygen availability as an ecological limit to have been almost totally neglected. plant distribution. Advances in Ecological Research 23: 93 – 185. Where possible, future studies should adopt methods Crawford RMM. 2003. Seasonal differences in plant responses to ﬂooding and anoxia. Canadian Journal of Botany 81: 1224 – 1246. which will allow comparisons to be made with conﬁdence. Darwin C. 1842 (published 1909). Pencil sketch of 1842. In: Darwin F, Climatic change, increasing prevalence of droughts, ed. The foundations of the origin of species: two essays written in alterations to groundwater availability and ﬂooding 1842 and 1844. Cambridge: Cambridge University Press. periodicities make such work increasingly urgent since Darwin C. 1859. On the origin of species by means of natural selec- freshwater ﬂoodplain forests are a vital human resource tion, or the preservation of favoured races in the struggle for life. that is under threat. They harbour many ﬁsh and London: John Murray [Facsimile of 1st edn.]: Cambridge, MA: mammal species, help moderate widespread ﬂooding of Harvard University Press, 1964. inhabited areas, regulate river levels, improve water De Simone O, Haase K, Mu¨ller E, Junk WJ, Schmidt W. 2002a. quality, act as substantial sinks for carbon and provide Adaptations of Central Amazon tree species to prolonged ﬂood- ing: root morphology and leaf longevity. Plant Biology 2: timber and non-timber forest products. Improving our 515 – 522. understanding of their workings will underpin their pres- De Simone O, Haase K, Mu¨ller E, Junk WJ, Gonsior GA, Schmidt W. ervation and effective future management. 2002b. Impact of root morphology on metabolism and oxygen distribution in roots and rhizosphere from two Central Amazon Contributions by the authors ﬂoodplain tree species. Functional Plant Biology 29: 1025 – 1035. Ellery WN, Tacheba B. 2003. Floristic diversity of the Okavango Both authors contributed to a similar extent in the prep- Delta, Botswana. In: Alonso LE, Nordin LA, eds. A rapid biological aration of this article. assessment of the aquatic ecosystems of the Okavango Delta, Botswana, Chapter 5. High Water Survey: RAP Bulletin of Biologi- Acknowledgements cal Assessment. We thank the Association of Tropical Biology and Conser- Ellery K, Ellery WN, Verhagen BT. 1992. The distribution of C3 and vation (ATBC) and the Society of Tropical Ecology (gto ¨ ) C4 plants in a successional sequence in the Okavango Delta. for support. We also thank Michael Heinl (University of South African Journal of Botany 58: 400 – 402. Innsbruck, Germany) for much information on the Ellery WN, Ellery K, McCarthy TS. 1993. Plant distribution in islands of the Okavango Delta, Botswana: determinants and feedback Okavango Delta. interactions. African Journal of Ecology 31: 118 – 134. Ellery WN, McCarthy TS, Dangerﬁeld JM. 2000. Floristic diversity in Conﬂict of interest statement the Okavango Delta, Botswana as an endogenous product of biological activity. In: Gopal B, Junk WJ, Davis JA, eds. Biodiver- None declared. sity in wetlands: assessment, function and conservation, Vol. I. Leiden: Backhuis. References Ferreira CS. 2002. Germinac¸a˜o e adaptac¸o˜es metabo´licas e morfo-anatoˆmicas em plaˆntulas de Himatanthus succuuba Armstrong W, Bra¨ndle R, Jackson MB. 1994. Mechanisms of ﬂood (Spruce) Wood., de ambientes de va´rzea e terra ﬁrme na Amazoˆ- tolerance in plants. Acta Botanica Neerlandica 43: 307 – 358. nia Central. MSc Thesis, Universidade do Amazonas (UA), Insti- Bonyongo MC. 1999. Vegetation ecology of the seasonal ﬂoodplains tuto Nacional de Pesquisas da Amazo ˆ nia (INPA), Manaus, 95. in the Okavango Delta, Botswana. Unpublished Thesis (MSc), Uni- Ferreira LV, Venticinque E, Almeida S. 2005. O desmatamento na versity of Pretoria. Amazo ˆ nia e a importa ˆ ncia das a ´ reas protegidas. Estudos Avan- Bonyongo MC, Veenendaal E, Bredenkamp G. 2000. Floodplain veg- c¸ados 19: 1 – 10. etation in the Nxaraga Lagoon area, Okavango Delta, Botswana. Finlayson CM. 1988. Productivity and nutrient dynamics of season- South African Journal of Botany 66: 15 – 21. ally inundated ﬂood plains in the Northern Territory. In: Campbell I, Poole C, Giesen W, Valbo-Jorgensen J. 2006. Species Wade-Marshall D, Loveday P, eds. North Australia: progress and diversity and ecology of Tonle Sap Great Lake, Cambodia. prospects, Vol. 2 ﬂoodplain research. Darwin: ANU Press, 58 – 83. Aquatic Sciences 68: 355 – 373. Finlayson CM. 2005. Plant ecology of Australia’s tropical ﬂoodplain Colmer TD, Pedersen O. 2008. Underwater photosynthesis and res- wetlands: a review. Annals of Botany 96: 541 – 555. piration in leaves of submerged wetland plants: gas ﬁlms Finlayson CM, Bailey BJ, Cowie ID. 1989. Macrophytic vegetation of improve CO and O exchange. New Phytologist 177: 918 – 926. 2 2 the Magela ﬂood plain, Northern Australia. Research report no. 5. Cowie ID, Armstrong MD, Woinarski JCZ, Brocklehurs PS, Short PS, Sydney: Ofﬁce of the Supervising Scientist. Dunlop CR. 2000. An overview of the ﬂoodplains. In: Cowie ID, Finlayson CM, Cowie ID, Bailey BJ. 1990. Characteristics of a sea- Short PS, Osterkamp P, Madsen M, eds. Floodplain ﬂora: a ﬂora sonally ﬂooded freshwater system in monsoonal Australia. of the coastal ﬂoodplains of the Northern Territory, Australia. In: Whigham DF, Good RE, Kvet J, eds. Wetland ecology and Canberra, Australia: ABRS, 1 – 33. management: case studies. Dordrecht: Kluwer Academic, Crawford RMM. 1989. The anaerobic retreat. In: Crawford R.M.M., 141 – 162. ed. Studies in plant survival. Ecological case histories of plant 16 AoB PLANTS Vol. 2010, plq003, doi:10.1093/aobpla/plq003 & The Authors 2010 Parolin and Wittmann — Adaptive responses of trees to ﬂooding in tropical ﬂoodplain systems Finlayson CM, Cowie ID, Bailey BJ. 1993. Litterfall in a Melaleuca landscape ecology of a mighty tropical river and its basin. Junk, forest on a seasonally inundated ﬂood plain in tropical 215 – 243. northern Australia. Wetlands Ecology and Management 2: Junk WJ. 1997. The central Amazonian ﬂoodplain: ecology of a 177 – 188. pulsing system. Ecological Studies 126. Heidelberg: Springer. Franklin DC, Brocklehurst PS, Lynch D, Bowman DMJS. 2007. Niche Junk WJ. 2000. Mechanisms for development and maintenance differentiation and regeneration in the seasonally ﬂooded Mel- of biodiversity in neotropical ﬂoodplains. In: Gopal B, aleuca forests of northern Australia. Journal of Tropical Ecology Junk WJ, Davis JA, eds. Biodiversity in wetlands: assessment, 23: 457 – 468. function and conservation,Vol.1.Leiden: Backhuis, Furch B, Correˆa AFF, Nunes JASM, Otto K-R. 1985. Lichtklimadaten 119 – 139. in drei aquatischen Okosystemen verschiedener physikalisch- Junk WJ, da Silva VMF. 1997. Mammals, reptiles and amphibians. chemischer Beschaffenheit. I. Abschwa ¨ chung, Ru ¨ ckstreuung In: Junk WJ, ed. The central Amazon ﬂoodplain: ecology of a und Vergleich zwischen Einstrahlung, Ru ¨ ckstrahlung und spha ¨ r- pulsing system. Ecological studies, 126. Berlin, Heidelberg: isch gemessener Quantenstromdichte (PAR). Amazoniana 9: Springer, 409 – 418. 411 – 430. Junk WJ, Bayley PB, Sparks RE. 1989. The ﬂood pulse concept in Gibbs J, Greenway H. 2003. Mechanisms of anoxia tolerance in river-ﬂoodplain systems. In: Dodge DP, ed. Proceedings of the plants. I. Growth, survival and anaerobic catabolism. Functional International Large River Symposium. Canadian Special Publi- Plant Biology 30: 1 – 47. cation of Fisheries and Aquatic Sciences 106: 110 – 127. Gopal B, Junk WJ, Davis JA. 2000. Biodiversity in wetlands: assess- Junk WJ, Brown M, Campbell IC, Finlayson M, Gopal B, Ramberg L, ment, function and conservation, Vol. 1. Leiden: Backhuis. Warner BG. 2006. The comparative biodiversity of seven Heinl M, Sliva J, Tacheba B. 2004. Vegetation changes after single globally important wetlands: a synthesis. Aquatic Sciences 68: ﬁre-events in the Okavango Delta wetland, Botswana. South 400 – 414. African Journal of Botany 70: 695 – 704. Kalliola R, Salo J, Puhakka M, Rajasilta M. 1991. New site for- Heinl M, Neuenschwander A, Sliva J, Vanderpost C. 2006. Inter- mation and colonizing vegetation in primary succession on actions between ﬁre and ﬂooding in the Okavango Delta ﬂood- the Western Amazon ﬂoodplains. Journal of Ecology 79: plains, Botswana. Landscape Ecology 21: 699 – 709. 877 – 901. Heinl M, Frost P, Vanderpost C, Sliva J. 2007. Fire activity on dry- Kesselmeier J, Staudt M. 1999. Biogenic volatile organic com- lands and ﬂoodplains in the southern Okavango Delta, Bots- pounds (VOC): an overview on emission, physiology and wana. Journal of Arid Environments 68: 77 – 87. ecology. Journal Atmospheric Chemistry 33: 23 – 88. Huete AR, Restrepo-Coupe N, Ratana P, Didan K, Saleska SR, Kesselmeier J, Bode K, Hofmann U, Mu¨ller H, Scha¨fer L, Wolf A, Ichii K, Panuthai S, Gamo M. 2008. Multiple site tower ﬂux Ciccioli P, Brancaleoni E, Cecinato A, Frattoni M, Foster P, and remote sensing comparisons of tropical forest dynamics Ferrari C, Jacob V, Fugit JL, Dutaur L, Simon V, Torres L. in monsoon Asia. Agricultural and Forest Meteorology 148: 1997. Emission of short chained organic acids, aldehydes and 748 – 760. monoterpenes from Quercus ilex L., Pinus pinea L. in relation to physiological activities, carbon budget and emission algor- Hughes FMR. 1988. The ecology of African ﬂoodplain forests in ithms. Atmospheric Environment 31: 119 – 133. semi-arid and arid zones: a review. Journal of Biogeography 15: 127 – 140. Kimmerer TW, Macdonald RC. 1987. Acetaldehyde and ethanol biosynthesis in leaves of plants. Plant Physiology 84: Irion G, Junk WJ, Mello JASN. 1997. The large central Amazonian 1204 – 1209. river ﬂoodplains near Manaus: geological, climatological, hydro- logical and geomorphological aspects. In: Junk WJ, ed. The Kozlowski TT. 1984. Responses of woody plants to ﬂooding. In: Central Amazon ﬂoodplain: ecology of a pulsing system. Ecologi- Kozlowski TT, ed. Flooding and plant growth. Orlando: Academic cal Studies 126. Heidelberg: Springer, 23 – 46. Press, 129 – 163. Ishida A, Diloksumpun S, Ladpala P, Staporn D, Panuthai S, Kubitzki K. 1989. The ecogeographical differentiation of Amazo- Gamo M, Yazaki K, Ishizuka M, Puangchit L. 2006. Contrasting nian inundation forests. Plant Systematics and Evolution 162: seasonal leaf habits of canopy trees between tropical dry- 285 – 304. deciduous and evergreen forests in Thailand. Tree Physiology Kubitzki K, Ziburski A. 1994. Seed dispersal in ﬂood plain forests of 26: 643 – 656. Amazonia. Biotropica 26: 30 – 43. IUCN. 1991. http://cmsdata.iucn.org/downloads/mrwd_nwg_ Lamberts D, Koponen J. 2008. Flood pulse alterations and pro- regional_meeting_december_2009_ﬁnal_2.pdf. ductivity of the Tonle Sap ecosystem: a model for impact Jackson MB, Armstrong W. 1999. Formation of aerenchyma and assessment. Ambio 37: 178 – 184. the processes of plant ventilation in relation to soil ﬂooding ¨ Larcher W. 1994.Okophysiologie der Pﬂanzen: Leben, Leistung und and submergence. Plant Biology 1: 274 – 287. Streßbewa ¨ ltigung der Pﬂanzen in ihrer Umwelt. 5th Edn. Ulmer James EK, Loureiro MD, Pott A, Pott VJ, Martins CM, Franco AA, Stuttgart, UTB fu ¨ r Wissenschaft. Sprent JI. 2001. Flooding-tolerant legume symbioses from the Lowry J, Finlayson CM. 2004. A review of spatial data sets for Brazilian Pantanal. New Phytologist 150: 723 – 738. wetland inventory in northern Australia. In: Supervising scientist Joly CA, Crawford RMM. 1982. Variation in tolerance and metabolic report 178. Darwin. responses to ﬂooding in some tropical trees. Journal of Exper- Mantlana KB. 2008. Seasonal and inter-annual variations of imental Botany 33: 799 – 809. leaf-level photosynthesis and soil respiration in the representa- Junk WJ. 1984. Ecology of the va ´ rzea, ﬂoodplain of Amazonian tive ecosystems of the Okavango Delta, Botswana. PhD Thesis, whitewater rivers. In: Sioli H, ed. The Amazon. Limnology and Wageningen University, The Netherlands. AoB PLANTS Vol. 2010, plq003, doi:10.1093/aobpla/plq003 & The Authors 2010 17 Parolin and Wittmann — Adaptive responses of trees to ﬂooding in tropical ﬂoodplain systems McCarthy TS. 2006. Groundwater in the wetlands of the Okavango of the volatile C -compounds ethanol, acetaldehyde and Delta, Botswana, and its contribution to the structure and func- acetic acid between leaves of Amazonian ﬂoodplain tree tion of the ecosystem. Journal of Hydrology 320: 264 – 282. species and the atmosphere. Biogeosciences 5: 1085 – 1100. McJannet D. 2008. Water table and transpiration dynamics in a Safford RJ, Maltby E, Duong Van Ni , Branch NP. 2009. Melaleuca seasonally inundated Melaleuca quinquenervia forest, north wetlands and sustainable development in the Mekong Delta, Queensland, Australia. Hydrological Processes 22: 3079 – 3090. Vietnam. In: Maltby E, Barker T, eds. The wetlands handbook. Oxford: Blackwells, 829 – 849. Medina E. 1983. Adaptations of tropical trees to moisture stress. In: Golley FB, ed. Ecosystems of the world: tropical rain forest eco- Salo J, Kalliola R, Ha¨kkinen I, Ma¨kinen Y, Niemela¨ P, Puhakka M, systems. Amsterdam: Elsevier, 225 – 237. Coley PD. 1986. River dynamics and the diversity of Amazon lowland forest. Nature 322: 254 – 258. Mommer L, Visser EJW. 2005. Underwater photosynthesis in ﬂooded terrestrial plants: a matter of leaf plasticity. Annals of Sarkkula J, Koponen J, Kummu M. 2005. Tools for integrated basin Botany 96: 581 – 589. ﬂow management at Lower Mekong basin ﬂoodplains. In: Zerger A, Argent RM, eds. MODSIM 2005 International Congress Moreira FMDS, Silva MFD, Faria SMD. 1992. Occurrence of nodula- on Modelling and Simulation. Canberra: Modelling and Simu- tion in legume species in the Amazon region of Brazil. New Phy- lation Society of Australia and New Zealand, 2153 – 2159. tologist 121: 563 – 570. Scarano FR, Ribeiro KT, Moraes LFD, Lima HC. 1997. Plant estab- O’Grady AP, Eamus D, Cook PG, Lamontagne S. 2006. Comparative lishment on ﬂooded and unﬂooded patches of a freshwater water use by the riparian trees Melaleuca argentea and Corym- swamp forest in southeastern Brazil. Journal of Tropical bia bella in the wet – dry tropics of northern Australia. Tree Physi- Ecology 14: 793 – 803. ology 26: 219 – 228. Scarano FR, Pereira TS, Rocas G. 2003. Seed germination during Oliveira-Wittmann A, Piedade MTF, Wittmann F, Parolin P. 2007. ﬂoatation and seedling growth of Carapa guianensis, a tree Germination in four low-va ´ rzea tree species of Central Amazo- from ﬂood-prone forests of the Amazon. Plant Ecology 168: nia. Aquatic Botany 86: 197 – 203. 291 – 296. Parolin P. 2000. Phenology and CO -assimilation of trees in Schlu¨ter U-B, Furch B. 1992. Morphologische, anatomische und Central Amazonian ﬂoodplains. Journal of Tropical Ecology 16: physiologische Untersuchungen zur Uberﬂutungstoleranz des 465 – 473. Baumes Macrolobium acaciaefolium, charakteristisch fu ¨ r die Parolin P. 2001. Senna reticulata, a pioneer tree from Amazonian Weiß- und Schwarzwasseru ¨ berschwemmungswa ¨ lder bei va ´ rzea ﬂoodplains. The Botanical Review 67: 239 – 254. Manaus, Amazonas. Amazoniana 12: 51 – 69. Parolin P. 2009. Submerged in darkness: adaptations to prolonged Schlu¨ter U-B, Furch B, Joly CA. 1993. Physiological and anatomical submergence by woody species of the Amazonian Floodplains. adaptations by young Astrocaryum jauari Mart. (Arecaceae) in Annals of Botany 103: 359 – 376. periodically inundated biotopes of Central Amazonia. Biotropica Parolin P, Armbru¨ster N, Wittmann F, Ferreira LV, Piedade MTF, 25: 384 – 396. Junk WJ. 2002. A review of tree phenology in central Amazo- Scho¨ngart J. 2003. Dendrochronological and dendroclimatic studies nian ﬂoodplains. Pesquisas, Botaˆnica 52: 195 – 222. in Central Amazonian Forests. Research Program May 2003 – April Parolin P, De Simone O, Haase K, Waldhoff D, Rottenberger S, 2005, 1 – 13. Kuhn U, Kesselmeier J, Schmidt W, Piedade MTF, Junk WJ. Scho¨ngart J, Piedade MFT, Ludwigshausen S, Horna V, Worbes M. 2004. Central Amazon ﬂoodplain forests: tree survival in a 2002. Phenology and stem-growth periodicity of tree species in pulsing system. The Botanical Review 70: 357 – 380. Amazonian ﬂoodplain forests. Journal of Tropical Ecology 18: Parolin P, Lucas C, Piedade MTF, Wittmann F. 2010. Drought 581 – 597. responses of ﬂood-tolerant trees in Amazonian ﬂoodplains. Sena Gomes AR, Kozlowski TT. 1980. Responses of Melaleuca quin- Annals of Botany 105: 129 – 139. quenervia seedlings to ﬂooding. Physiologia Plantarum 49: Ponnamperuma FN. 1984. Effects of ﬂooding on soils. In: 373 – 377. Kozlowski TT, ed. Flooding and plant growth. Orlando: Academic Sioli H. 1954. Betrachtungen u ¨ ber den Begriff ‘Fruchtbarkeit’ eines Press, 9 – 45. Gebiets anhand der Verha ¨ ltnisse in Bo ¨ den und Gewa ¨ ssern Ama- Prance GT. 1979. Notes on the vegetation of Amazonia. III. Termi- zoniens. Forschung Fortschritt 28: 65 – 72. nology of Amazonian forest types subjected to inundation. Brit- Skeat AJ, East TJ, Corbett LK. 1996. Impact of feral water buffalo. tonia 31: 26 – 38. In: Finlayson CM, von Oertzen I, eds. Landscape and vegetation Ribeiro MNG, Adis J. 1984. Local rainfall variability—a potential ecology of the Kakadu Region, Northern Australia. Dordrecht: bias for bioecological studies in the Central Amazon. Acta Ama- Kluwer Academic, 155 – 177. zonica 14: 159 – 174. Tacheba B, Segosebe E, Vanderpost C, Sebego R. 2009. Assessing Ringrose S. 2003. Characterisation of riparian woodlands and their the impacts of ﬁre on the vegetation resources that are potential water loss in the distal Okavango Delta, Botswana. available to the local communities of the seasonal wetlands Applied Geography 23: 281 – 302. of the Okavango, Botswana, in the context of different land Ringrose S, Chipanshi AC, Matheson W, Chanda R, Motoma L, uses and key government policies. African Journal of Ecology Magole I, Jellema A. 2002. Climate- and human-induced 47: 71 – 77. woody vegetation changes in Botswana and their Tanaka K, Takizawa H, Kume T, Xu J, Tantasirin C, Suzuki M. 2004. implications for human adaptation. Environmental Management Impact of rooting depth and soil hydraulic properties on 30: 98 – 109. the transpiration peak of an evergreen forest in northern Rottenberger S, Kleiss B, Kuhn U, Wolf A, Piedade MTF, Junk W, Thailand in the late dry season. Journal of Geophysical Research Kesselmeier J. 2008. The effect of ﬂooding on the exchange 18 AoB PLANTS Vol. 2010, plq003, doi:10.1093/aobpla/plq003 & The Authors 2010 Parolin and Wittmann — Adaptive responses of trees to ﬂooding in tropical ﬂoodplain systems Taylor JA, Tulloch D. 1985. Rainfall in the wet – dry tropics: extreme Wittmann F, Parolin P. 2005. Aboveground roots in Amazonian events at Darwin and similarities between years during the ﬂoodplain trees. Biotropica 37: 609 – 619. period 1870 – 1983. Australian Journal of Ecology 10: 281 – 295. Wittmann F, Anhuf D, Junk WJ. 2002. Tree species distribution and Veenendaal EM, Mantlana KB, Pammenter NW, Weber P, community structure of Central Amazonian va ´ rzea forests by Huntsman-Mapila P, Lloyd J. 2008. Growth form and seasonal remote sensing techniques. Journal of Tropical Ecology 18: variation in leaf gas exchange of Colophospermum mopane 805 – 820. savanna trees in northwest Botswana. Tree Physiology 28: Wittmann F, Junk WJ, Piedade MTF. 2004. The va ´ rzea forests in 417 – 424. Amazonia: ﬂooding and the highly dynamic geomorphology Visser EJW, Voesenek LACJ, Vartapetian BB, Jackson MB. 2003. interact with natural forest succession. Forest Ecology and Man- Flooding and plant growth. Annals of Botany 91: 107 – 109. agement 196: 199 – 212. Waldhoff D. 2003. Leaf structure in trees of Central Amazonian Wittmann F, Scho¨ngart J, Montero JC, Motzer T, Junk WJ, ﬂoodplain forests (Brazil). Amazoniana 17: 451 – 469. Piedade MTF, Queiroz HL, Worbes M. 2006. Tree species compo- sition and diversity gradients in white-water forests across the Waldhoff D, Furch B. 2002. Leaf morphology and anatomy in Amazon Basin. Journal of Biogeography 33: 1334 – 1347. eleven tree species from Central Amazonian ﬂoodplains (Brazil). Amazoniana 17: 79 – 94. Wittmann F, Junk WJ, Scho¨ngart J. 2010. Phytogeography, species diversity, community structure and dynamics of central Amazo- Waldhoff D, Junk WJ, Furch B. 2002. Fluorescence parameters, nian ﬂoodplain forests. In: Junk WJ, Piedade MTF, Parolin P, chlorophyll concentration, and anatomical features as indi- Wittmann F, Scho ¨ ngart J, eds. Central Amazonian Floodplain cators for ﬂood adaptation of an abundant tree species in forests: ecophysiology, biodiversity and sustainable manage- Central Amazonia: Symmeria paniculata. Environmental and ment. Ecological Studies. Heidelberg: Springer. Experimental Botany 48: 225 – 235. Worbes M. 1997. The forest ecosystem of the ﬂoodplains. In: Wantzen KM, Junk WJ. 2000. The importance of Junk WJ, ed. The Central Amazon ﬂoodplain: ecology of a stream-wetland-systems for biodiversity: a tropical perspective. pulsing system. Ecological Studies 126. Heidelberg: Springer, In: Gopal B, Junk WJ, Davis JA, eds. Biodiversity in wetlands: assess- 223 – 266. ment, function and conservation, Vol. 1. Leiden: Backhuys, 11 – 34. Worbes M, Klinge H, Revilla JD, Martius C. 1992. On the dynamics, Wikramanayake E, Rundel P. 2002. Tonle sap freshwater swamp ﬂoristic subdivision and geographical distribution of va ´ rzea forests. In: Wikramanayake E, Dinerstein E, Loucks C, eds. Terres- forests in Central Amazonia. Journal of Vegetation Science 3: trial ecoregions of the Indo-Paciﬁc: a conservation assessment. 553 – 564. Washington, DC: Island Press, 824 pp. AoB PLANTS Vol. 2010, plq003, doi:10.1093/aobpla/plq003 & The Authors 2010 19

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Struggle in the flood: tree responses to flooding stress in four tropical floodplain systems

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Struggle in the flood: tree responses to flooding stress in four tropical floodplain systems

Struggle in the flood: tree responses to flooding stress in four tropical floodplain systems

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