Central Amazonian floodplain forests: tree adaptations in a pulsing system.

   I. Abstract/Resumo
  II. Introduction
 III. Effects of Flooding
      A. Seed Germination and Early Establishment
      B. Tree Growth and Periodicity
      C. Leaf Anatomy, Morphology, and Physiology
  IV. Adaptations of Trees from Amazonian Floodplains
      A. Roots
      B. Stem and Crown
      C. Release of Volatiles as a Reaction to Root Anoxia
      D. Reproductive Phenology and Seedling Establishment
   V. Variation in Flooding Tolerance and Zonation
  VI. Conclusions
 VII. Acknowledgments
VIII. Literature Cited

II. Introduction

The Amazon River and its large tributaries are accompanied by adjacent species-rich and highly adapted floodplain forests that are estimated to cover an area of more than 97,000 [km.sup.2] (Sippel et al., 1998; Hamilton et al., 2002). Seasonal variations in the river levels subject trees to periods of up to 210 days of continuous flooding per year, with changes of the water levels that can reach 10 cm per day (Junk, 1989). The flood pulse is very regular (Fig. 1), but irregularities in the maximum and minimum water levels in between years are common and may have a high relevance for the establishment phase (Scarano et al., 1997; Parolin, 2002a). 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 10-15 m high (Fig. 2A-D). At low water levels, drought may be a stress factor for some weeks (Junk, 1997).

[FIGURES 1-2 OMITTED]

The monomodal flood pulse poses a multitude of constraints for the trees that inhabit the floodplains by causing drastic changes in the bioavailability of nutrients, oxygen levels, and concentrations of phytotoxins. Inundated soils turn to hypoxic or anoxic conditions within a few hours as a result of oxygen consumption by respiring roots and microorganisms and of insufficient diffusion of oxygen through the water (Crawford, 1989, 1992; Armstrong et al., 1994; Visser et al., 2003). Oxygen depletion is accompanied by increased levels of C[O.sub.2], anaerobic decomposition of organic matter, increased solubility of mineral substances, and reduction of the soil redox potential (Ponnamperuma, 1972; Joly & Crawford, 1982; Kozlowski, 1984; Vartapetian et al., 2003). Depletion is followed by accumulation of many potentially toxic compounds, caused by alterations in the composition of the soil microflora (Ponnamperuma, 1984). In addition, high sedimentation rates in white-water floodplains (100 mg [l.sup.-1] suspended load in the Amazon River / Rio Sotimoes; Irion et al., 1997) increase the lack of oxygen in the root zone, and mud layers on the leaf surfaces may affect photosynthesis. The high productivity linked to the high nutrient availability in the varzea (white-water floodplains of the Amazon River and its affluents, sensu Prance, 1979) (Piedade et al., 1991) results in elevated decomposition rates, which further decrease the oxygen level. In the black-water floodplains of the Rio Negro and its affluents (seasonal igapo sensu Prance, 1979), additional stress is caused by the lack of available nutrients (Sioli, 1954; Furch, 1997).

In contrast to temperate zones, where flooding frequently occurs during winter and plants are in a dormant state while flooded or submerged, the aquatic phase in the Amazon region occurs during a period in which temperature and light conditions are optimal for plant growth. The mean annual temperature of 26.6[degrees]C with only small fluctuations, the average rainfall of 2100 mm per year (Ribeiro & Adis, 1984), and light intensities that reach values up to 3000 [micro]mol [m.sup.-2][s.sup.-] above the water surface at noon (Furch et al., 1985) represent favorable growth conditions for trees. This implies that adaptations are needed to allow survival despite prolonged flooding.

The diversity of species and life strategies is lower in Amazonian floodplains than in adjacent Amazonian terra firme forests (Gentry, 1982, 1992; Campbell et al., 1986; Balslev et al., 1987; Dumont et al., 1990; Nevo, 1993). On the other hand, diversity is still considerable, with an estimated 1000 species. This high species number stands in contrast to the adverse growth conditions for trees, a life form that evolved in terrestrial ecosystems and that, in general, dies more readily in response to flooding than to desiccation (Larcher, 1994).

Several studies contain descriptions of adaptations of single tree species in Amazonian floodplains that include quantitative aspects such as the flow of biomass and energy and anatomical, morphological, and physiological adaptations of organisms to the annual change between a terrestrial and an aquatic phase (e.g., Worbes, 1985; Meyer, 1991; Moreira et al., 1992, 1995; Schluter & Furch, 1992; Schluter et al., 1993; Nascimento et al., 1998; Scarano, 1998; Waldhoff & Furch, 1998; Graffmann, 2000; Parolin, 2000a; Rocas et al., 2001; Scarano et al., 2001; De Simone et al., 2002a, 2002b, 2003a; Gribel & Gibbs, 2002; Waldhoff & Furch, 2002; Waldhoff et al., 2002), but a review is lacking. This article describes the present state of knowledge about reactions to flooding and about adaptations of trees in Amazonian floodplains.

III. Effects of Flooding

In early studies, growth conditions in the aquatic phase of Amazonian floodplains were compared with temperate winters and therefore defined as "physiological winter" (Gessner, 1968). This implies reductions of growth and metabolic activity to complete dormancy, as observed for trees of temperate forests in the period of unfavorable growth conditions. However, although the terrestrial phase is the main growth period for tree species, this term implies growth restrictions that last for the whole or most of the unfavorable period. This is clearly not the case in Central Amazonia, where periods of limited growth last only few weeks and where new leaf flush, flowering, fruiting, and wood increment occur in most trees while flooded (Worbes, 1986, 1989, 1997; Parolin et al., 2002a; Schrogart et al., 2002).

A. SEED GERMINATION AND EARLY ESTABLISHMENT

After fruit maturation, which occurs at high water levels (Kubitzki & Ziburski, 1994), seeds fall into the water and may float and/or be submerged for several weeks. In many species (e.g., Aldina latifolia, Campsiandra comosa, Cecropia latiloba, Crateva benthami, Mora paraensis, Nectandra amazonum, Senna reticulata, Swartzia polyphylla, Vatairea guianensis, Vitex cymosa) seeds were shown to remain visually sound at least for more than two months when continuously submerged (Parolin & Junk, 2002). Other species (e.g., Crudia amazonica and Tabebuia barbata) had viable seeds at least for one month, but most seeds started to rot thereafter. This stands in contrast to the majority of land plants, whose seeds quickly lose viability if submerged for prolonged periods (Hook, 1984). On the contrary, seeds of floodplain species that were kept in air dried or decomposed within a few days (e.g., Tabebuia barbata, Nectandra amazonum--or weeks--e.g., Senna reticulata, Aldina latifolia) (Parolin, pers. obs.). Regardless of whether the seeds float or sink, seedling emergence starts only when the flood recedes and conditions are favorable for growth. Once established, the role of mycorrhizal symbiosis is assumed to be important for seedling survival during flooding, as was shown for Acosmium nitens in the Orinoco's floodplain (Rosales et al., 2002).

Mortality of waterlogged and submerged seedlings is generally low as compared with species from the adjacent terra firme. In Himatanthus sucuuba, a species that grows both in floodplains and in uplands, survival of submerged seedlings differed in the two ecosystems. Seed viability and germination rates after submergence were higher in seeds collected in the floodplains than in those collected in terra firme (Ferreira, 2002). Overall height growth and new leaf production are not severely affected by waterlogging in most species and may even be enhanced, as they are in Senna reticulata, where waterlogging caused accelerated seedling growth (Parolin, 2001c). In flooding experiments, seedlings of this species survived periods of up to two years with consecutive waterlogging in standing water (2/3 of the plant submerged).

Complete submergence is more crucial. Submerged seedlings of Senna reticulata die within a few days (Parolin, 200lb), but many other species tolerate several weeks of submergence in a state of rest. Soon after the water recedes, leaves resprout and--in an experiment under seminatural conditions--reach the height of the control plants 5 to 12 weeks after the end of submersion. This shows a high ability to compensate for the period of rest induced by submergence (Parolin, 200lc). In submerged Cecropia latiloba, new leaf buds were formed below the water surface several weeks before the water receded, which enabled the plant to have fully expanded leaves within few days after emergence (Parolin, 2002c).

B. TREE GROWTH AND PERIODICITY 

In adult trees, periodical growth reductions as a consequence of flooding are reflected by the formation of increment rings and by periodic shoot elongation (Worbes, 1986, 1989, 1997; Worbes & Junk, 1989; Dezzeo et al., 2003). Waterlogging causes reduced water conductance and consequently a water deficit in the crown, resulting in leaf shedding (Fig. 2D) and in a period of cambial dormancy (Worbes, 1989, 1996; Schongart et al., 2002). Leaf senescence increases with the onset of flooding, with chlorosis, epinasty, and abscission, and results in increased leaf fall during the aquatic period (Ferreira, 1991; Worbes, 1992; Wittmann & Parolin, 1999; Parolin et al., 2002a). New leaf production is reduced but not stopped, and most species resprout before the end of the aquatic phase, as a result of rehydration. The deciduous period lasts only for two months in most species (Schongart et al., 2002), whereas waterlogging may continue for several months. When leaves are submerged, they may be shed within days (Crudia amazonica, Senna reticulata) to weeks, or they may be kept below water for several months without apparent damage (Gustavia augusta, Pouteria glomerata, Rheedia brasiliensis, Symmeria paniculata, Tabernaemontanajuruana) (Waldhoff & Furch, 2002). The periodic behavior of vegetative phenology is determined by the tree's water status, which is a function of the interaction between the water potential of the environment and the structural and functional state of the tree (Reich & Borchert, 1984). In Amazonian floodplains, tree water status is directly linked to flooding. The flood pulse triggers vegetative phenology of the trees, except for stem-succulent species such as Pseudobombax munguba (Schongart et al., 2002). In this context, it is not yet clear whether leaf shedding is an adaptation to waterlogging or represents simply a consequence of the effect of flooding on the water status (Borchert, 1994; Muller & Junk, 2000). The assumption that flooding triggers leaf fall is supported by a study with two identical, but temporally distinct, experiments: different hydrological conditions (waterlogging, submergence, and drought) were directly responsible for the changes in growth and metabolism of some species (e.g., Cecropia latiloba, Crateva benthami, Nectandra amazonum, Senna reticulata, Tabebuia barbata, and Vitex cymosa)(Parolin, 2001b). The water deficit in the canopy of Central Amazonian floodplain forests during the inundation period appears to be similar to that found in trees on terra firme during the dry season (Worbes, 1986, 1997).

C. LEAF ANATOMY, MORPHOLOGY, AND PHYSIOLOGY

In species with leaves that do not possess a thick cuticle and thick outer epidermis walls, leaves rot fast when submerged and are shed after a few days (Waldhoff & Furch, 2002). Other species may keep their leaves below water for several months (e.g., Licania apetala, Nectandra amazonum, Symmeria paniculata). Whether deciduous or evergreen, and regardless of whether leaves are kept or shed trader water, the leaves of Amazonian floodplain trees exhibit traits that are generally considered xeromorph (Medina, 1983; Roth, 1984; Bolhar-Nordenkampf & Draxler, 1993; Waldhoff et al., 2002): large epidermal cells (Hevea spruceana, Eugenia inundata), thick outer epidermis walls (Rheedia brasiliensis, Himatanthus sucuuba), thick cuticle (Eschweilera tenuifolia, Simaba guianensis), compact spongy parenchyma with only few and small intercellular spaces (Senna reticulata, Licania apetala), sunken stomata (Vitex cymosa, Pouteria glomerata), and transcurrent vascular bundles with a strong sclerenchymatous bundle sheath (Nectandra amazonum, Eugenia inundata).

Specific leaf mass is higher in waterlogged months in several species (e.g., Cecropia latiloba, Nectandra amazonum, Senna reticulata, Tabebuia barbara, Vitex cymosa), but not in others (e.g., Crateva benthami) (Parolin, 2002b). Mean leaf size is significantly lower during the aquatic period in some cases, because of either increased leaf senescence and a subsequent loss of leaflets (Crateva benthami, Tabebuia barbata) or production of smaller leaves (Senna reticulata) (Parolin, 2002b). Leaf nitrogen content may drop significantly with waterlogging in many species (by 20-25% in Senna reticulata, Tabebuia barbata, Vitex cymosa) but may rise in others (+32% in Nectandra amazonum during the flooded season) (Parolin et al., 2002b). Cecropia latiloba, Tabebuia barbata, and Vitex cymosa show an additional peak of nitrogen in the first month after the end of waterlogging, indicating that flooding may disturb nitrogen uptake. Leaf water potential ranges between -8 and -20 bar (Scholander & Perez, 1968) but can be as low as -28 bar in waterlogged Nectandra amazonum (Parolin, 1997). With waterlogging, leaf water potential decreased by 5-30% in six analyzed species (Parolin, 1997).

The chlorophyll content of aerial leaves is lower in waterlogged than in nonflooded trees (Scholander & Perez, 1968; Furch, 1984; Schluter & Furch, 1992; Schluter et al., 1993; Parolin, 1997; Waldhoff et al., 1998). In submerged leaves, chlorophyll content is little affected, as shown for Symmeria paniculata, Tabernaemontana juruana, and Gustavia augusta (Waldhoff et al., 1998, 2002). Chlorophyll a fluorescence measurements on seedlings of Nectandra amazonum, Gustavia augusta, and Tabernaemontana juruana also showed that submerged seedlings maintain their photosynthetic apparatus at least so far undamaged that seedlings can start to photosynthesize shortly after emergence (Parolin, 1997; Waldhoff et al., 2000). In Tabernae-montana juruana, light saturation before submersion (800 [micro]mol [m.sup.-2][s.sup.-1]) did not differ much from the values after submersion (500 [micro]mol [m.sup.-2][s.sup.-1]) (Krack, 2000). Within three weeks of exposure, preflood values were achieved in most species. In Laetia corymbulosa and Tabernaemontana juruana, light harvesting was even higher after recovery than before submersion (Krack, 2000).

Under waterlogged conditions, most species show a reduction of mean C[O.sub.2] uptake in aerial leaves ranging from 10% (early successional Cecropia latiloba, Senna reticulata) to 20-50% (late successional Nectandra amazonum, Crateva benthami, Tabebuia barbata, Vitex cymosa) lower than in the terrestrial phase. C[O.sub.2] uptake rises again before the end of the flooded phase and remains high throughout the terrestrial phase (Parolin, 2000a). Single measurements--in contrast to average values of the complete aquatic period--show that photosynthetic activity during waterlogging could reach the same or even higher values than in the terrestrial phase in almost all analyzed species (Parolin, 2000a). Waterlogged adults or seedlings of Senna reticulata often showed higher assimilation rates than did nonflooded individuals: In a flooding experiment, waterlogged seedlings had an average assimilation rate that was 15% higher than that of the well-watered control (Parolin, 2001a). Senna reticulata, flooded by a water column of 4 m with only few leaves appearing above the water surface, showed assimilation rates of up to 25 [micro]mol C[O.sub.2] [m.sup.-2][s.sup.-1], which represent the highest photosynthetic activity measured in waterlogged Amazonian floodplain trees (Parolin, 2001 a). In several species the influence of drought appeared to be far more harmful than that of waterlogging or even submergence in terms of growth, photosynthetic performance, and vitality after the end of stress (Waldhoff et al., 1998). In fact, drought may represent more of an impairment than flooding to the survival of local vegetation (Keel & Prance, 1979; Scarano et al., 1994).

Chlorophyll fluorescence measurements on Symmeria paniculata showed that the current photochemical capacity (quantum yield Fv/Fm) of Photosynthetic System II (PSII) in nonsubmerged and submerged leaves at 0-1 m depth was not correlated with the changing water levels and remained above the lower limit of natural variation in healthy leaves ("threshold value of impairment") (Bolhar-Nordenkampf & Gotzl, 1992; Waldhoff et al., 2002). Submerged leaves maintained their vitality despite almost complete darkness below water: Even at water depths of 1-7 m, with a quantum flux of 1-10 [micro]mol [m.sup.-2][s.sup.-1] (PAR), Fv/Fm values lay below this threshold, showing a negative correlation with the duration of submergence (Waldhoff et al., 2002). When lighted, these submerged leaves began electron transport, which, however, appeared to be inhibited shortly after the start. Just which mechanisms maintain the photosynthetic apparatus almost undamaged during the submersion remains a question. Leaves of adult trees that were submerged in darkness (>1 m depth) recovered the Fv/Fm yield while still under water, during falling water levels, independently of how long the leaves were submerged prior to the measurements. There is a correlation between light intensity and the maintenance/recovery of the photosynthetic apparatus (PSII). In a greenhouse experiment, the light-harvesting complex of submerged seedlings of Tabernaemontana juruana. Pouteria glomerata, Laetia corymbulosa, Gustavia augusta, and Nectandra amazonum did not deteriorate, Rubisco was decomposed only to a low extent, and new proteins with unknown function were synthesized and accumulated during submergence (Krack, 2000). The same seedlings survived submergence only if they were well supplied with nutrients before flooding and if they were at least five months old (Krack, 2000), indicating that these processes imply high energy costs. Nevertheless, the energy balance in submerged seedlings is highly effective: In the palm Astrocaryum jauari the energy reserves in the roots were not exhausted after 300 days of submersion (Schluter et al., 1993).

Chloroplast shape and starch content may change with long-term submergence (Laetia corymbulosa, Pouteria glomerata) (Waldhoff et al., 2002), but transmission electron microscope (TEM) analyses of leaves from Symmeria paniculata at 1 m depth also showed that short-term submergence affected neither chloroplast shape nor the interior structures of chloroplasts with thylakoids, stacks, and starch grains.

IV. Adaptations of Trees from Amazonian Floodplains

Only adapted species--i.e., those that have characteristics enhancing their survival and reproduction and, thus, their fitness--are able to establish and survive under the extreme conditions of Amazonian floodplains. The regularity of the recurrence of flooding--i.e., the predictability of the flood pulse--enhances the evolution of specific adaptive traits and may have led to the large variety of species that are able to successfully colonize, establish, and dominate the floodplains. All trees inhabiting this area are plants whose growth is not inhibited by flooding (Gill, 1970). Morphological adaptations may be remnants of preadaptations from the nonflooded terra firme species in which floodplain trees originated (Kubitzki, 1989). The degree of flood tolerance may also depend on the time taken to colonize the floodplains. Some species have the potential for the development of adaptive traits--as revealed in waterlogging experiments--but do not show them in the field in average years. For example, under natural conditions in the floodplains, adventitious roots, lenticels, and stem hypertrophy were observed only in few individuals, probably due to the constant change in water level (Parolin, 2001b). Although not frequently encountered in the field, their function may be important in years with flooding anomalies.

A. ROOTS

Morphological adaptations of the root system comprise hypertrophy of lenticels, formation of adventitious roots, plank buttressing and stilt rooting, development of aerenchyma, and the deposition of cell-wall biopolymers such as suberin and lignin in the root peripheral cell layers (Schluter & Furch, 1992; Schluter et al., 1993; Nascimento et al., 1998; Pimenta et al., 1998; Waldhoff et al., 1998; Parolin, 2001c; De Simone et al., 2002a, 2002b; Medri et al., 2002; Haase et al., 2003) (Fig. 2E-F). Different types of aboveground roots are closely related to flooding duration and habitat dynamics (Wittmann & Parolin, in press). Plank buttressing (tabular roots) is more common on sites subjected to lower sediment rates (e.g., in Aldina sp., Byrsonima amazonica, Cedrela odorata, and Pouteria spp.). Where sedimentation rates are high (e.g., on natural stands of Salix martiana), adventitious roots can replace the function of the ordinary root system, which often dies under several decimeters of sediment. In fact, the primary belowground root of Salix martiana reaches depths of up to 6 m, but the main root function is shifted to several well-defined layers of fine secondary roots stacked up along the main root with a space of 30-40 cm. The same was found in Alchornea castaneifolia, which also produced stilt roots up to 40 cm above the ground surface (Wittmann & Parolin, in press).

The development of adventitious roots in the oxygenated layer at the surface of the floodwater table and hypertrophy of lenticels at the stem above the water table improve the internal oxygen status by facilitating the entry of oxygen into the root and the stem by the shortest possible pathway. Several tree species (e.g., Salix martiana and Tabernaemontana juruana) respond to low oxygen concentrations by forming adventitious roots capable of longitudinal oxygen transport (Haase et al., 2003). On the other hand, pneumatophores as typical adaptations to enhance root aeration (Granville, 1974) are absent in varzea trees (Junk, 1984). They were described only for Pithecellobium latifolium occurring in "tidal varzea" near the mouth of the Amazon (Scarano et al., 1994), where tidal flooding with low water columns is common. According to Kubitzki (1989), their formation is impeded in Central Amazonia because of the high amplitudes of water-level fluctuations. On the other hand, aeration through respiratory apparatus like pneumatudes is potentially possible: Under experimental conditions several species produced these negatively geotropic aerial roots in a way similar to that described for the mangrove species Laguncularia racemosa (Geissler et al., 2002) or the palms Mauritia flexuosa and Euterpe oleracea (Granville, 1974).

Stem nodulation and nodulated adventitious roots were observed in various species and are understood as adaptations that allow legumes to fix [N.sub.2] in a flooded environment (James et al., 2001). In fact, the frequency of nodulation among genera was found to be higher in flooded than in nonflooded sites in both varzea and igapo, indicating that nodulation may even be favored in flooded areas (Moreira et al., 1992).

Root aerenchyma, promoting longitudinal oxygen transport, appear to be essential for improving the root's energy status for water and nutrient uptake (Jackson & Armstrong, 1999). Microelectrode investigations on 2-3-month-old cuttings from Salix martiana showed that their well-oxygenated aerenchymatous adventitious roots were able to build up an oxygenated layer several millimeters thick around the whole roots, suggesting a mechanism of detoxifying reduced phytotoxins by radial oxygen loss (ROL) (De Simone et al., 2002b; Haase et al., 2003). In older roots from adult trees that are submerged by a water table several meters high, the formation of aerenchyma may be less important for longitudinal oxygen transport, because the lacunae are destroyed by secondary root thickening and the long gas-diffusion distances. In this case an improvement of the root's energy status is achieved by reducing the number of oxygen-consuming cells in the root cortex (De Simone et al., 2002a). Deposition of suberin in radial (Casparian bands) and tangential cell walls of the exodermis equips the root with a hydrophobic barrier that contributes to the plant's overall resistance. It is supposed that a heavily suberized exodermis limits ROL from the root to the rhizosphere, conserving oxygen for root growth in oxygen-depleted soils (Colmer et al., 1998). The use of oxygen microelectrodes in combination with chemical analysis by GC/MS of enzymatically isolated rhizodermal cell walls revealed that cuttings of Tabernaemontana juruana avoid radial oxygen losses by developing strong suberin depositions in radial and tangential cell walls of the root hypodermis, starting immediately behind the root tip (De Simone et al., 2003b). In addition, suberin acts as a component of the wound- and pathogen-induced plant defense response, preventing infection by microbial pathogens (Mohan et al., 1993a, 1993b). Chemical analysis of enzymatically isolated rhizodermal cell walls from Laetia corymbulosa and Salix martiana revealed that the aromatic suberin moiety contains large amounts of para-hydroxybenzoic acid, suggesting a function of suberin in pathogen defense (De Simone et al., 2003a). A suberized exodermis appears to be well designed to prevent the entry of reduced phytotoxic compounds into the roots, but this is apparently not the case in Tabernaemontana juruana. Investigations of young cuttings subjected to supraoptimal [Fe.sup.2+] concentrations did not validate a function of suberin incrustations in excluding divalent iron from roots (De Simone et al., 2003a, 2003b). Suberization appears to prevent loss of water and stored solutes into the rhizosphere during drought periods, which may represent an important protective feature during the terrestrial phase (Zimmermann et al., 2000; Hose et al., 2001; Miyamoto et al., 2001).

In Central Amazonian species from varzea and igapo floodplains, induction of activity of fermentative enzymes such as alcohol dehydrogenase (ADH), lactate dehydrogenase (LDH), glutamate-pyruvate transaminoferase (GPT), and malate dehydrogenase (MDH) has been observed under anaerobic growth conditions in greenhouse experiments on young seedlings and trees (Schluter & Furch, 1992; Schluter et al., 1993; De Simone et al., 2002b) (Fig. 3). In waterlogged seedlings of Himatanthus sucuuba, ADH concentrations rose 15 days after the onset of hypoxic conditions and remained high throughout the 120 days of the experimental period (Ferreira, 2002). In seeds of the same species collected in nonflooded terra firme, ADH concentrations decreased after 30 days, and seedling mortality was 100% at the end of the experiment.

[FIGURE 3 OMITTED]

Not only hypoxia but, frequently, anoxia occurs in Amazonian floodplains. Anoxia in plant tissues reduces the rate of energy production (Gibbs & Greenway, 2003). Thus, adaptation to anoxia always includes coping with an energy crisis. Processes that receive energy from the limited supply available under anoxia include synthesis of anaerobic proteins and energy-dependent substrate transport. There is an urgent need to test whether--as is the case in other flood-tolerant plants (Greenway & Gibbs, 2003)--reductions in ion fluxes and protein turnover during anoxia achieve economies in energy consumption in Amazonian floodplain trees.

B. STEM AND CROWN

Water loss and gas exchange in the flooding period are effectively reduced by alterations in vegetative phenology and water storage. Leaf shedding during the aquatic phase has been documented to occur not only in deciduous species but also in evergreen trees, which tend to reduce new leaf production at high water levels (Parolin et al., 2002a). The xeromorphic leaf structure described for trees of tropical forests (Roth, 1984) and typical also for the floodplain species may represent a preadaptation that results from the dry habitats where most tree species originated (Kubitzki, 1989), which helps to cope both with insufficient water supply to the tree crowns during the aquatic phase and with periods of occasional drought in the terrestrial phase. Apparently, the leaves that are not shed and maintain their functions despite prolonged submergence (Fig. 2G) do not require different or additional morphological and/or anatomical traits. On the other hand, leaf anatomy is adjusted to the environmental conditions requiring high ecological plasticity (Rocas et al., 2001).

A reduction in the transpirational surface by decreasing leaf area is achieved in Senna reticulata, which produces new leaves almost constantly and thus is able to react to environmental conditions very quickly (Parolin, 2001a). Complete deciduousness may last for some months, as observed for Pseudobombax munguba, Ceiba pentandra, and other Bombacaceae (Gribel et al., 1999), but it may be as short as four weeks (e.g., Tabebuia barbata), despite waterlogging durations of seven months (Parolin, 1997). Tree water status is crucial for the production of new leaves and for the maintenance of maximum transpiration rates, despite prolonged unfavorable hydrological conditions in the environment (Borchert, 1994). Pseudobombax munguba improves its water status by storage in a succulent (Schongart et al., 2002), but this species appears to be the only stem-succulent tree in the floodplains. No other means of water storage have yet been found. High stem water potential enables trees to flush leaves, to flower, and to produce fruits (Fig. 2H) during the time of high water stress (Schongart et al., 2002). In this context, it is not clear whether leaf shedding is an adaptation to waterlogging or simply a consequence of the effect of flooding on the water status (Borchert, 1994). Recent measurements have shown that water uptake by roots is not reduced enough to explain leaf shedding (Muller & Junk, 2000). The assumption that flooding triggers leaf fall is supported by a study with two identical, but temporally distinct, experiments: Different hydrological conditions (waterlogging, submergence, and drought) were directly responsible for the changes in growth and metabolism of some species (e.g., Cecropia latiloba, Crateva benthami, Nectandra amazonum, Senna reticulata, Tabebuia barbata, and Vitex cymosa) (Parolin, 2001b). However, these experiments were performed with seedlings only. As shown by Ferreira (1991) for adult trees in the floodplains, precipitation may well play an important role as trigger for phenological events. Also, genetically fixed rhythms, related to the supposed origin of floodplain trees in savannas, may play a role, as seems to be the case in the genus Tabebuia and the family Bombacaceae.

C. RELEASE OF VOLATILES AS A REACTION TO ROOT ANOXIA

Large amounts of volatile organic compounds (VOC) are emitted to the atmosphere by terrestrial vegetation (Kesselmeier & Staudt, 1999). Therefore, the Amazonian ecosystem, with its large terra firme and floodplain areas, is of great interest for atmospheric chemistry. VOC species such as short-chain aldehydes play an important role in atmospheric chemistry. They influence the oxidizing capacity of the atmosphere, generate free radicals, and are involved in the production of organic nitrates (Singh & Hanst, 1981; Carlier et al., 1986; Thompson, 1992; Singh et al., 1995, 2000). In addition, they contribute significantly to the formation of organic aerosols (Li et al., 2001) and, by oxidation to formic and acetic acid, to the acidity of the atmosphere (Talbot et al., 1990; Kotzias et al., 1997). The emission quantity and quality of VOC is under environmental and ecophysiological control. Recent work on non-Amazonian tree species demonstrated the effects of root anoxia on physiological processes and the release of oxygenated volatiles to the atmosphere (Kreuzwieser et al., 1999, 2000). The authors demonstrated that roots of vascular plants affected by anoxia produce high amounts of ethanol, which is transported into the leaves, where it can be remetabolized by oxidation, thereby generating acetaldehyde and acetic acid as an intermediate; however, a fraction of these compounds may be lost to the atmosphere. This fermentation reaction and VOC release is also found in lichen species (Wilske et al., 2001), demonstrating the general significance. Furthermore, acetaldehyde and ethanol may be also emitted under stress conditions such as S[O.sub.2] and [O.sub.3] exposure, water deficit, freezing, or fast-changing light conditions (Kimmerer & Kozlowski, 1982; Kimmerer & McDonald, 1987; Kesselmeier et al., 1997; Holzinger et al., 2000). Acetaldehyde (and formaldehyde) are exchanged bidirectionally between the vegetation and the atmosphere; that is, they are both emitted and taken up, depending on environmental and atmospheric conditions (Kesselmeier, 2001). Recent measurements in the terra firme Amazonian rain forest provided evidence that both short-chain aldehydes and the corresponding organic acids were mainly taken up by the tree species investigated, although a release was observed when ambient concentrations were below a specific compensation point (Kuhn et al., 2002; Rottenberger et al., in press).

With this background, regions such as the Amazon Basin, with long-term episodes of flooding over large areas, are of special interest because of the potential change of emission caused by root anoxia (see above). It is therefore of considerable importance to investigate the emission behavior of Amazonian floodplain tree species. First results were achieved by Rottenberger (2003) and will be summarized here. Branch enclosure measurements performed in a greenhouse experiment on four different floodplain species exposed to several days of inundation showed that emission of ethanol and acetaldehyde is inducible in response to flooding in all species (Fig. 4). A pronounced diurnal pattern in acetaldehyde and ethanol emissions was observed, with zero exchange at night, a strong emission burst in the morning, and a decrease in the afternoon. This pattern is interpreted to result from an ethanol accumulation in the roots at night, when stomata are closed and transport is restricted by a lack of transpiration, followed by transport to the leaves driven by the light-induced transpiration stream as soon as stomata open. This general diurnal emission pattern was observed in all tree species investigated, although emission rates were substantially different among species (Fig. 5). Maximal emission of acetaldehyde and ethanol (numbers given in parentheses) differed by up to two orders of magnitude, ranging between 3 (5) nmol [m.sup.-2][min.sup.-1] in Salix martiana and 200 (500) nmol [m.sup.-2][min.sup.-1] in Laetia corymbulosa. Furthermore, the tree species behaved differently as far as the ratio of acetaldehyde to ethanol is concerned. Obviously, there are large interspecific differences not only in the ethanol production in the roots but also in the subsequent metabolic conversion inside the leaves. Whereas Tabernaemontana juruana emits predominately ethanol, suggesting a limitation of leaf ADH, Laetia corymbulosa is a strong acetaldehyde emitter, indicative of a high ADH activity. Hence, the differences in emission rates can be related to species-specific metabolic adaptations, reflected in increased ADH activity and/or morphological adaptations of the plant to improve the oxygen availability in the roots, such as formation of adventitious roots and development of aerenchyma (De Simone et al., 2002a, 2002b). Species with an insufficient oxygen supply need to switch over to fermentation, resulting in subsequent transport of ethanol to the leaves and emission of ethanol and its oxidation products. To a certain extent, ethanol might also be directly released from the roots into the surrounding water (Kreuzwieser et al., 1999), as shown for European tree species. Species (e.g., Salix martiana) with improved oxygen supply to the roots will produce no or rather low amounts of ethanol (Fig. 5).

[FIGURES 4-5 OMITTED]

The different adaptive strategies are also reflected by species-specific differences in the temporal trend of the maximal emission rates over the flooding period of several days (Fig. 5). Emission rates of Salix martiana did not show a significant variation and remained constantly low, In contrast, all other species investigated showed an increase of the maximal emission rates at first stage, indicative of increasing oxygen deficit and ethanol production in the roots, followed by a decline in emission after three to seven days. For Laetia corymbulosa the decline in emission rates was associated with a progressive and pronounced reduction in leaf physiological activities (data not shown), indicating a poor acclimation to the unfavorable conditions. For Tabernaemontana juruana the decline in emission rates is assumed to reflect an acclimation response, because leaf physiological activities (assimilation, transpiration, and stomatal conductance) were significantly less affected during the whole flooding period. In this context it is also remarkable that the emission rates of fermentation products from Amazonian floodplain species were generally lower than were those reported for European species (Kreuzwieser et al., 1999; Holzinger et al., 2000). This difference may indicate preconditioning of floodplain species toward long-lasting flooding periods.

D. REPRODUCTIVE PHENOLOGY AND SEEDLING ESTABLISHMENT

The main means of dispersal in Amazonian floodplain trees are hydro- and ichthyochory (Fig. 21-J), emphasized by a close correlation between the timing of flooding and fruit maturation (Ziburski, 1991; Parolin et al., 2002a). For several tree species it has been shown that seed production coincides with the flood pulse for dispersal by water flow and fish (Gottsberger, 1978; Goulding, 1980; Moegenburg, 2002; Mannheimer et al., 2003). The diaspores show morphological adaptations that enhance floatation, such as spongy tissues or large, air-filled spaces (Kubitzld & Ziburski, 1994; Williamson et al., 1999; Williamson & Costa, 2000). Germination starts immediately after the retreat of the flood, but it is not clear whether submergence is directly responsible for the inhibition of seed germination. Seeds may germinate while floating, as shown for Carapa guianensis (Scarano et al., 2003). In an experiment with 12 tree species (Parolin & Junk, 2002) to test whether seed germination occurs only in nonflooded seeds, four species (Crateva benthami, Mora paraensis, Nectandra amazonum, and Vatairea guianensis) showed radicle growth while submerged, but none of the species under investigation was able to produce a shoot as long as it was submerged (Oliveira, 1998; Oliveira & Piedade, 2002; Parolin & Junk, 2002).

Adaptations related to seedling establishment also include high seed masses in nutrientpoor igapo (mean seed mass = 7.1 g) that, even when considering taxonomic relatedness, were significantly higher than in nutrient-rich varzea (mean seed mass = 1.2 g) (Parolin, 2000b). At high elevations in the flooding gradient the larger seeds enabled rapid height growth, allowing escape from submergence. Because of the short duration of the nonflooded period and strong competition with highly productive macrophytes and grasses, fast germination and growth may be crucial for survival of tree species, especially those that do not tolerate submersion and must grow tall quickly in order to maintain some leaves above the water surface when the flood comes. In the case of Senna reticulata, which succumbs to submersion, seedlings grow to a height of 4 m in the first terrestrial period of less than eight months (Parolin, 2001a). In the same period several species (e.g., the early successional species Cecropia latiloba and Salix martiana) grow up to 1 m and others (e.g., species with large seeds, such as Aldina latifolia. Mora paraensis, and Vatairea guianensis) up to 2 m (Parolin, 2002a, 2002c).

A high reiteration capacity and vigorous resprouting after damage through rotting or mechanical injury may be considered as further adaptations to effective establishment, which is found not only in early successional species such as Senna reticulata or Cecropia latiloba but also in species of later successional stages, as, for example, Platymiscium ulei, Piranhea trifoliata, and Tabebuia barbara (Worbes, 1997; Parolin, 2001a, 2002c). Salix martiana shows intensive vegetative propagation through parts of broken stems, and the lower branches of Eugenia inundata become rooted (Worbes, 1997), thus contributing to fast and effective establishment in the short terrestrial period.

V. Variation in Flooding Tolerance and Zonation 

Plant survival in Amazonian floodplains, as in other flood-prone forests, seems to be the result of more than one adaptive mechanism (Scarano et al., 1994, 1998). Species that grow and photosynthesize well when waterlogged do not necessarily do well when submerged. These two types of flooding events require different adaptations for growth and survival (Parolin, 2001c). Species that tolerate submergence and prolonged waterlogging (e.g., Symmeria paniculata or Eschweilera tenuifolia) establish on the lower sites, which may be flooded for up to 210 days per year. Less-tolerant species (e.g., Mora paraensis or Pentaclethra macroloba) are restricted to the upper parts, close to the terra firme, which are flooded for shorter periods (Junk, 1989; Ferreira, 2000). In the temperate regions, habitats flooded for more than 40% of the year cannot be colonized by woody species, although once established they may survive (Gill, 1970). Only few species (e.g., Malouetia furfuracea) are generalists and are able to colonize both high and low sites (Worbes, 1997). Trees seem to persist on lower sites longer in the igapo than in the varzea (Worbes, 1997), which may be attributed to higher photon flux in black water than in white water and, thus, to the better conditions for leaf survival below water and to better oxygen conditions (Schluter & Furch, 1992; Schluter et al., 1993; Worbes, 1997).

The different mechanisms for tolerating waterlogging and submergence and the various combinations of adaptations lead to different growth and establishment strategies, which may be related to the zonation found along the flooding gradient (Junk, 1989; Ferreira, 2000; Wittmann & Junk, 2003). Scarano et al. (1994) showed that plants from low areas had roots with increased starch and reduced glucose compared with those from high areas in the flooding gradient. Physiological measurements at the root level are still very scarce for tree species from Amazonian floodplains, and more studies are urgently needed to better understand the occurrence and photosynthetic performance of a given species. Such physiological adaptations appear to account for their success in surviving long periods of flooding. Other adaptive mechanisms to flooding are growth habits in the establishment phase. Fast-growing seedlings may evade submersion as long as they are established on high levels in the flooding gradient, which facilitates the protrusion of leaves above the water surface, allowing oxygen transport from the leaves via the shoots to the roots. On lower levels, escape from submersion is impossible, and the strategy for tolerating prolonged submersion is more effective. In fact, seedlings on these sites grow far less in height than do species from the higher levels (Parolin, 2002a). This leads to the assumption that the typical zonation found in Amazonian floodplains is closely linked to the submersion tolerance of the seedlings, perhaps less than to the flood tolerance of adult trees. Flooding tolerance of seedlings and old trees is often far lower than is that of adult trees (Kozlowski, 1982). Parkia pendula, a species from terra firme, may survive in the floodplains as adult trees, but seedlings die if they are flooded for more than a month, whereas the closely related species Parkia discolor tolerates prolonged flooding in every ontogenetic stadium (Scarano & Crawford, 1992). This also shows the importance of years with anomalous water levels. While the regular flooding periodicity may allow only the establishment of highly tolerant species, unusually low river levels may favor the establishment of several species. This is clearly the case for Eugenia inundata, which formed monospecific stands at the lowest floodplain levels near Manaus (Brazil) in a period that was drier than average (Junk, 1997). The adult trees grew well until an atypical, incessant flooding period killed them. The species has not yet regenerated at these sites because another period of unusually low water did not occur. Also, Eschweilera tenuifolia, Symmeria paniculata, and Macrolobium acaciifolium form monospecific stands of equal age on long-flooded levels that probably result from colonizations in anomalous years. This supports the hypothesis of Davis and Richards (1934) that average environmental conditions do not influence plant distribution as much as do extreme years.

One important factor related to the establishment and growth strategies is the availability of nutrients. In the nutrient-poor igapo, seedlings invest in high leafage and higher leaf xeromorphy, and they tend to remain in a state of rest during the waterlogged and submerged period, with low photosynthetic activity. In the nutrient-rich varzea, on the other hand, the formation of morphological adaptations requires high energy input, which is provided by almost uninterrupted photosynthetic activity and high nutrient availability from the environment (Parolin, 2001b). These differences are reflected in different species composition in varzea and igapo (Kubitzki, 1989; Ferreira, 1997).

VI. Conclusions

The Central Amazonian inundation forests are composed of species that are highly tolerant of waterlogging and submergence. Given the role that Amazonian floodplain trees play in the ecology of the whole ecosystem, their potential for exploitation, and the strong anthropogenic impact to which the forests are already subjected, understanding the functioning of the trees and their life histories appears to be of fundamantal importance. Although data on reproduction and adaptations are still scarce, findings to date indicate that the species possess a multitude of survival strategies. Further elucidation of the great diversity of strategies requires maintenance of the multidisciplinary approach, with in situ studies and laboratory investigations at the molecular, morphological, and physiological levels. Most features were measured under experimental conditions with constant water levels. Detailed field studies, especially on adult trees, are lacking. Very little is also known about phenotypic plasticity and genetic variation in the trees that inhabit Amazonian floodplains (Paiva et al., 1985; Hall et al., 1994; Silvera et al., 2003). It may be expected, though, that new adaptations--especially at the physiological level--will be discovered to explain the capacity of the trees to maintain their vitality despite extreme flooding.

VII. Acknowledgments

We wish to thank the technicians of the Instituto Nacional de Pesquisas da Amazonia (INPA) for their help in the field. This work was supported by the INPA / Max Planck project. Jennifer Henry and two anonymous referees gave valuable comments on the manuscript.

VIII. Literature Cited

Armstrong, W., R. Brandle & M. B. Jackson. 1994. Mechanisms of flood tolerance in plants. Acta Botanica Neerlandica 43: 307-358.

Balslev, H., J. Luteya, B. Oellgaard & L. B. Holm-Nielsen. 1987. Composition and structure of adjacent unflooded and floodplain forest in Amazonian Ecuador. Opera Botanica 92: 37-57.

Bolhar-Nordenkampf, H. R. & G. Draxler. 1993. Functional leaf anatomy. Pp. 91-112 in D. O. Hall, J. J. O. Scurlock, H. R. Bolhar-Nordankampf, R. C. Leegood & S. P. Long (eds.), Photosynthesis and production in a changing environment. Chapman and Hall, London.

-- & M. Gotzl. 1992. Chlorophyllfluoreszenz als Indikator der mit der Seehohe zunehmender Stressbelastung yon Fichtennadeln. FBVA Berichte (Schriflenreihe der Forstlicher Bundesveranstalter) 67: 119-131.

Borchert, R. 1994. Soil and stem water storage determine phenology and distribution of tropical dry forest trees. Ecology 75: 1437-1449.

Campbell, D. G., D. C. Daly, G. T. Prance & U. N. Maciel. 1986. Quantitative ecological inventory of terra firme and varzea tropical forest on the Rio Xingu, Brazilian Amazon. Brittonia 38: 369-393.

Carlier, P., H. Hannachi & G. Mouvier. 1986. The chemistry of carbonyl compounds in the atmosphere: A review. Atmospheric Environment 20: 2079-2099.

Colmer, T. D., M. R. Gibberd, A. Wiengweera & T. K. Tinh. 1998. The barrier to radial oxygen loss from roots of rice (Oryza sativa L.) is induced by growth in stagnant solution. Journal of Experimental Botany 49: 1431-1436.

Crawford, R. M. M. 1989. The anaerobic retreat. Pp. 105-129 in R. M. M. Crawford (ed.), Studies in plant survival: Ecological case histories of plant adaptation to adversity. Studies in Ecology, 11. Blackwell Scientific Publications, Oxford.

--. 1992. Oxygen availability as an ecological limit to plant distribution. Advances in Ecological Research 23: 93-185.

Davis, T. A. W. & P. W. Richards. 1934. The vegetation of Moraballi Creek, British Guiana: An ecological study of a limited area of tropical rain forest. Journal of Ecology 22: 106-155.

De Simone, O., E. Muller, W. J. Junk & W. Schmidt. 2002a. Adaptations of Central Amazon tree species to prolonged flooding: Root morphology and leaf longevity. Functional Plant Biology 29: 1025-1035.

--, K. Haase, E. Muller, W. J. Junk, G. A. Gonsior & W. Schmidt. 2002b. Impact of root morphology on metabolism and oxygen distribution in roots and rhizosphere from two Central Amazon floodplain tree species. Functional Plant Biology 29: 1025-1035.

--, E. Muller, W. J. Junk, K. Richau & W. Schmidt. 2003a. Iron distribution in three Central Amazon tree species from whitewater inundation areas (varzea) subjected to different iron regimes. Trees 17: 535-541.

--, K. Hasse, E. Muller, W. J. Junk, K. Hartmann, L. Schreiber & W. Schmidt. 2003b. Apoplasmic barriers and oxygen transport properties of hypodermal cell walls in roots from four Amazonian tree species. Plant Physiology 132(1): 206-217.

Dezzeo, N., M. Worbes, I. Ishii & R. Herrera. 2003. Annual tree rings revealed by radiocarbon dating in seasonally flooded forest of the Mapire River, a tributary of the lower Orinoco River, Venezuela. Plant Ecology 168: 165-175.

Dumont, J. F., S. Lamotte & F. Kahn. 1990. Wetland and upland forest ecosystems in Peruvian Amazonia: Plant species diversity in the light of some geological and botanical evidence. Forest Ecology and Management 33/34: 125-139.

Ferreira, C. S. 2002. Germinacao e adaptacoes metabolicas e morfo-anatomicas em plantulas de Himatanthus succuuba (Spruce) Wood., de ambientes de varzea e terra firme na Amazonia Central. Master's thesis, Univ. do Amazonas, Instituto National de Pesquisas da Amazonia, Manaus.

Ferreira, L. V. 1991. O efeito do periodo de inundacao na zonacao de comunidades, fenologia e regeneracao em uma floresta de igapo na Amazonia Central. Master's thesis, Istituto Nacional de Pesquisas da Amazonia, Manaus.

--. 1997. is there a difference between the white water floodplain Forests (varzea) and black water floodplain forests (igapo) in relation to number of species and density? Revista Brasileira de Ecologia 2: 60-62.

--. 2000. Effects of flooding duration on species richness, floristic composition and forest structure in river margin habitat in Amazonian blackwater floodplain forests: Implications for future design of protected areas. Biodiversity and Conservation 9: 1-14.

Furch, B. 1984. Untersuchungen zur Uberschwemmungstoleranz yon Baumen der Varzea and des Igapo: Blattpigmente. Biogeographica 19: 77-83.

--, A. F. F. Correa, J. A. S. M. Nunes & K. R. Otto. 1985. Lichtklimadaten in drei aquatischen Okosysteman verschiedener physikalisch-chemischer Beschaffenheit, I. Abschwachung, Ruckstreuung und Vergleich zwischen Einstrahlung, Ruckstrahlung and spharisch gemessaner Quantenstromdichte (PAR). Amazoniana 9: 411-430.

Furch, K. 1997. Chemistry of varzea and igapo soils and nutrient inventory in their floodplain forests. Pp. 47-68 in W. J. Junk (ed.), The Central Amazon floodplain: Ecology of a pulsing system. Ecological Studies, 126. Springer Verlag, Heidelberg.

Geissler, N., R. Schnetter & M.-L. Schnetter. 2002. The pneumatodes of Laguncularia racemosa: Little known rootlets of surprising structure, and notes on a new fluorescent dye for lipophilic substances. Plant Biology 6: 729-739.

Gentry, A. H. 1982. Patterns of neotropical plant species diversity. Evolutionary Biology 15: 1-83.

--. 1992. Tropical forest biodiversity distributional patterns and their conservational significance. Oikos 6: 19-28.

Gessner, F. 1968. Zur okologischen Problematik der Uberschwemmungswalder des Amazonas. Internationale Revue der Gesamten Hydrobiologie 53: 525-547.

Gibbs, J. & H. Greenway. 2003. Mechanisms of anoxia tolerance in plants, I. Growth, survival and anaerobic catabolism. Functional Plant Biology 30: 1-47.

Gill, C. J. 1970. The flooding tolerance of woody species: A review. Forestry Abstracts 31: 671-688.

Gottsberger, G. 1978. Seed dispersal by fish in the inundated regions of Humaita, Amazonia. Biotropica 10: 170-183.

Goulding, M. 1980. Interactions of fishes with fruits and seeds. Pp. 217-232 in M. Goulding (ed.), The fishes and the forest: Explorations in Amazonian natural history. Univ. of California Press, Berkeley.

Graffmann, K. C. 2000. Die Bedeutung der Druckventilation fur die Sanarstoffversorgung des Wurzelsystems bei Baumen der amazonischen Uberschwemmungswalder. Ph.D. diss., Univ. Koln.

Granville, J. J. 1974. Apecu sur In structure des pneumatophores de deux especes des sols hydromorphes en Guyane, Mauritia flexuosa L. et Euterpe oleracea Mart. (Palmae): Generalisation au systeme respiratoire racinare d'autres palmiers. Cahier Orstom Serie Biologie 23: 3-22.

Greenway, H. & J. Gibbs. 2003. Mechanisms of anoxia tolerance in plants, II. Energy requirements for maintenance and energy distribution to essential processes. Functional Plant Biology 30: 999-1036.

Gribel, R. & P. E. Gibbs. 2002. High outbreeding as a consequence of selfed ovule mortality and single vector bat pollination in the Amazonian tree Pseudobombax munguba (Bombacaceae). International Journal of Plant Sciences 163:1035-1043.

--, -- & A. L. Queioz. 1999. Flowering phenology and pollination biology of Ceiba pentandra (Bombacaceae) in Central Amazonia. Journal of Tropical Ecology 15: 247-263.

Haase K., O. De Simone, W. & J. Junk & W. Schmidt. 2003. Internal oxygen transport in cuttings from flood-adapted varzea tree species. Tree Physiology 23(15): 1069-1076.

Hall, P., L. C. Orrell & K. S. Bawa. 1994. Genetic diversity and mating system in a tropical tree, Carapa guianensis (Meliaceae). American Journal of Botany 81: 1104-1111.

Hamilton, S. K., S. J. Sippel & J. M. Melack. 2002. Comparison of inundation patterns among major South American floodplains. Journal of Geophysical Research--Atmospheres 107: 8038.

Holzinger, R., L. Sandoval-Soto, S. Rottenberger, P. J. Crutzen & J. Kesselmeier. 2000. Emissions of volatile organic compounds from Quercus ilex L. measured by Proton Transfer Reaction Mass Spectrometry under different environmental conditions. Journal of Geophysical Research--Atmospheres 105: 20573-20579.

Hook, D. D. 1984. Adaptations to flooding with fresh water. Pp. 265-294 in T. T. Kozlowski (ed.), Flooding and plant growth. Academic Press, Orlando, FL.

Hose, E., L. Schreiber, D. Clarskon, E. Steudle & W. Hartung. 2001. The exodermis: A variable apoplastic barrier in roots. Journal of Experimental Botany 52: 2245-2264.

Irion, G., W. J. Junk & J. A. S. N. Mello. 1997. The large Central Amazonian river floodplains near Manaus: Geological, climatological, hydrological and geomorphological aspects. Pp. 23-46 in W. J. Junk (ed.), The Central Amazon floodplain: Ecology of a pulsing system. Ecological Studies, 126. Springer Verlag, Heidelberg.

Jackson, M. B. & W. Armstrong. 1999. Formation of aerenchyma and the processes of plant ventilation in relation to soil flooding and submergence. Plant Biology 1: 274-287.

James, E. K., M. D. Loureiro, A. Pott, V. J. Pott, C. M. Martins, A. A. Franco & J. I. Sprent. 2001. Flooding-tolerant legume symbioses from the Brazilian pantanal. New Phytologist 150: 723-738.

Joly, C. A. & R. M. M. Crawford. 1982. Variation in tolerance and metabolic responses to flooding in some tropical trees. Journal of Experimental Botany 33: 799-809.

Junk, W. J. 1984. Ecology of the varzea, floodplain of Amazonian whitewater rivers. Pp. 215-243 in H. Sioli (ed.), The Amazon: Limnology and landscape ecology of a mighty tropical river and its basin. W. Junk, Dordrecht.

--. 1989. Flood tolerance and tree distribution in Central Amazonian floodplains. Pp. 47-64 in L. B. Nielsen, I. C. Nielsen & H. Balslev (eds.), Tropical forests: Botanical dynamics, speciation and diversity. Academic Press, London.

-- (ed.). 1997. The Central Amazon floodplain: Ecology of a pulsing system. Ecological Studies, 126. Springer Verlag, Heidelberg.

--, P. B. Bayley, & R. E. Sparks. 1989. The flood pulse concept in river-floodplain systems. Pp. 110-127 in D. P. Dodge (ed.), Proceedings of the International Large River Symposium. Fisheries and Oceans, Communications Directorate, Ottawa.

Keel, S. H. K. & G. T. Prance. 1979. Studies of the vegetation of a white-sand black-water igapo (Rio Negro, Brazil). Acta Amazonica 9: 645-655.

Kesselmeier, J. 2001. Exchange of short-chain oxygenated volatile organic compounds (VOCs) between plants and the atmosphere: A compilation of field and laboratory studies. Journal of Atmospheric Chemistry 39(3): 219-233.

-- & M. Staudt. 1999. Biogenic volatile organic compounds (VOC): An overview on emission, physiology and ecology. Journal of Atmospheric Chemistry 33: 23-88.

--, K. Bode, U. Hofmann, H. Muller, L. Schafer, A. Wolf, P. Ciccioli E. Brancaleoni A. Cecinato, M. Frattoni, P. Foster, C. Ferrari, V. Jacob, J. L. 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: 119-133.

Kimmerer, T. W. & T. T. Kozlowski. 1982. Ethylene, ethane, acetaldehyde, and ethanol-production by plants under stress. Plant Physiology 69: 840-847.

-- & R. C. McDonald. 1987. Acetaldehyde and ethanol biosynthesis in leaves of plants. Plant Physiology 84: 1204--1209.

Kotzias, D., C. Konidara & C. Sparta. 1997. Volatile carbonyl compounds of biogenic origin: Emission and concentration in the atmosphere. Pp. 67-87 in G. Helas, J. Slanina & R. Steinhrecher (eds.), Biogenic volatile organic compounds in the atmosphere. SPB Academic Publishers, Amsterdam.

Kozlowski, T. T. 1982. Water supply and tree growth, II. Flooding. Forest Abstracts, Commonwealth Forestry Bureau 43: 145-161.

--. 1984. Plant responses to flooding of soil. BioScience 34:162-166.

Krack, S. 2000. Untersuchungen zur Uberflutungstoleranz yon Baumen (Jungpflanzen) der zentralamazonischen Weisswasser-Uberschwemmungswalder (Varzea) bei Manaus/Amazonas. Master's thesis, Univ. Wurzburg.

Kreuzwieser, J., U. Scheerer & H. Rennenberg. 1999. Metabolic origin of acetaldehyde emitted by poplar (Populus tremula x P. alba) trees. Journal of Experimental Botany 50: 757-765.

--, F. Kuhnemann, A. Martis, H. Rennenberg & W. Urban. 2000. Diurnal pattern of acetaldehyde emission by flooded poplar trees. Physiologia Plantarum 108: 79-86.

Kubitzki, K. 1989. Die Flora der amazonischen Uberschwemmungswalder and ihre okologischen Beziehungen. Pp. 215-226 in G. Hartmann (ed.), Amazonien im Umbruch. Dietrich Reimer Verlag, Berlin.

-- & A. Ziburski. 1994. Seed dispersal in flood plain forests of Amazonia. Biotropica 26: 30-43. Kuhn, U., S. Rottenberger, T. Biesenthal, C. Ammann, A. Wolf, G. Schebeske, S. T. Oliva, T. M. Tavares & J. Kesselmeier. 2002. Exchange of short-chain monocarboxyclic acids by vegetation at a remote tropical forest site in Amazonia. Journal of Geophysical Research--Atmospheres 107(D20): 8069; doi:l0.1029/2000JD000303.

Latcher, W. 1994. Okophysiologie der Pflanzen: Leben, Leistung and Stressbewaltigung der Pflanzen in ihrer Umwelt, 5. Aufl. Ulmer Stuttgart, UTB fur Wissenschaft.

Li, P., K. A. Perreau, E. Covington, C. H. Song, G. R. Carmichael & V. H. Grassian. 2001. Heterogeneous reactions of volatile organic compounds on oxide particles of the most abundant crustal elements: Surface reactions of acetaldehyde, acetone, and propinnaldehyde on Si[O.sub.2], [A1.sub.2][O.sub.3,][Fe.sub.2][O.sub.3], Ti[O.sub.2], and CaO. Journal of Geophysical Research--Atmospheres 106: 5517-5529.

Mannheimer, S., G. Bevilacqua, E. P. Caramaschi & F. R. Scarano. 2003. Evidence for seed dispersal by the catfish Auchenipterichthys longimanus in an Amazonian lake. Journal of Tropical Ecology 19: 215-218.

Medina, E. 1983. Adaptations of tropical trees to moisture stress. Pp. 225-237 in F. B. Golley (ed.), Ecosystems of the world: Tropical rain forest ecosystems. Elsevier Scientific Publishing, Amsterdam.

Medri, M. E., E. Bianchini, J. A. Pimenta, S. Colli & C. Muller. 2002. Estudos sohre a tolerancia ao alagamento em especies arboreas nativas da bacia do rio Tibagi. Pp. 133-172 in M. E. Medri, E. Bianchini, O. A. Shibatta & J. A. Pimenta (eds.), A bacia do Rio Tibagi. Published by the editors, Londrina.

Meyer, U. 1991. Feinwurzelsysteme and Mykorrhizatypen als Anpassungsmechanismen in Zentralamazonischen Uberschwemmungswaldern: Igapo and Varzea. Ph.D. diss., Univ. Hohenheim.

Miyamoto, N., E. Steudle, T. Hirasawa & R. Lafitte. 2001. Hydraulic conductivity of rice roots. Journal of Experimental Botany 52: 1835-1846.

Moegenburg, S. M. 2002. Spatial and temporal variation in hydrochory in Amazonian floodplain forest. Biotropica 34: 606-612.

Mohan, R., M. A. Bajar & P. E. Kolattukudy. 1993a. Induction of a tomato anionic peroxidase gene (tap1) by wounding in transgenic tobacco and activation of tap1/GUS and tap2/GUS chimeric gone fusions in transgenic tobacco by wounding and pathogen attack. Plant Molecular Biology 21: 341-354.

--, P. Vijayan & P. E. Kolattukudy. 1993b. Developmental and tissue-specific expression of a tomato anionic peroxidase (tap1) gene by a minimal promoter with wound and pathogen induction by an additional 5' flanking region. Plant Molecular Biology 22: 475-490.

Moreira, F. M. d. S., M. F. d. Silva & S. M. D. Faria. 1992. Occurrence of nodulation in legume species in the Amazon region of Brazil. New Phytologist 121: 563-370.

Moreira, F. W, F. M. d. S. Moreira & M. F. d. Silva. 1995. Germinacao, crescimento inicial e nodulacao am viveiro de saboarana (Swartzia laevicarpa AMSHOFF). Acta Amazonica 25: 149-160.

Muller, E. & W. J. Junk. 2000. The influence of waterlogging on root water uptake and transpiration of trees of the Central Amazonian varzea. Verhandlungen des Internationalen Vereins fur Limnologie 27: 1725-1729.

Nascimento, B. M., O. L. E. Mota, O. M. Lousade & C. D. J. Reis. 1998. The morphological-anatomical adaptation of young plants of Inga vera Willd. and Virola surinamensis (Rolland. ex Rottb.) to submersion. Boletim do Museu Paraense Emilio Goeldi Serie Botanica 14: 93-107.

Nevo, E. 1993. Adaptive speciation at the molecular and organismal levels and its bearing on Amazonian biodiversity. Evolucion Biologica 7: 207-249.

Oliveira, A. C. 1998. Aspectos da dinamica populacional de Salix martiana Leyb. (Salicaceae) em areas de varzea da Amazonia Central. Master's thesis, INPA/FUA.

-- & M. T. F. Piedade. 2002. Implicacoes ecologicas da fenologia reprodutiva de Salix martiana Leyb. (Salicaceae) em Areas de varzea da Amazonia Central. Acta Amazonica 32: 377-385.

Paiva, J. R. d., P. D. S. Goncalves & L. Gasparotto. 1985. Genetic variation among Hevea provenances. Pesquisa Agropecuana Brasileira 20: 97-108.

Parolin, P. 1997. Auswirkungen periodischer Vernassung and Uberflutung auf Phanologie, Photosynthese and Blattphysiologie von Baumarten unterschiedlicher Wachstumsstrategie in zentralamazonischen Uberschwemmungsgebieten. Herbert Utz Verlag Wissenschaft, Munich.

--. 2000a. Phenology and C[O.sub.2] assimilation of trees in Central Amazonian floodplains. Journal of Tropical Ecology 16: 465-473.

--. 2000b. Seed mass in Amazonian floodplain forests with contrasting nutrient supplies. Journal of Tropical Ecology 16: 417-428.

--. 2001a. Senna reticulata, a pioneer tree from Amazonian varzea floodplains. Botanical Review 67: 239-254.

--. 2001b. Seed germination and early establishment in 12 tree species from nutrient-rich and nutrient-poor Central Amazonian floodplains. Aquatic Botany 70: 89-103.

--. 2001c. Morphological and physiological adjustments to waterlogging and drought in seedlings of Amazonian floodplain trees. Oecologia 128: 326-335.

--. 2002a. Submergence tolerance vs. escape from submergence: Two strategies of seedling establishment in Amazonian floodplains. Environmental and Experimental Botany 48: 177-186.

--. 2002b. Seasonal changes of specific leaf mass and leaf size in trees of Amazonian floodplains. Phyton 42: 169-186.

--. 2002c. Life history and environment of Cecropia latiloba in Amazonian floodplains. Revista de Biologia Tropical 50: 531-545.

-- & W. J. Junk. 2002. The effect of submergence on seed germination in trees from Amazonian floodplains. Boletim Museu Goeldi 18: 321-329.

--, N. Armbruster, F. Wittmann, L. V. Ferreira, M. T. F. Piedade & W. J. Junk. 2002a. Phenology of trees in Central Amazonian floodplains. Pesquisas Botanicas 52: 195-222.

--, -- & W. J. Junk. 2002b. Seasonal changes of leaf nitrogen content in trees of Amazonian floodplains. Acta Amazonica 32: 231-240.

Piedade, M. T. F., W. J. Junk & S. P. Long. 1991. The productivity of the [C.sub.4] grass Echinochloa polystachya on the Amazon floodplain. Ecology 72: 1456-1463.

Pimenta, J. A., E. Bianchini & M. F. Medri. 1998. Adaptations to flooding by tropical trees: morphological and anatomical modifications. Pp. 157-176 in F. R. Scarano & A. C. Franco (eds.) Ecophysiological strategies of xerophytic and amphibious plants in the Neotropies. Serie Oecologia Brasiliensis, 4. PPGE-UFRJ, Rio de Janeiro.

Ponnamperuma, F. N. 1972. The chemistry of submerged soils. Advances in Agronomy 24: 29-95.

--. 1984. Effects of flooding on soils. Pp. 9-45 in T. T. Kozlowski (ed.), Flooding and plant growth. Academic Press, Orlando, FL.

Prance, G. T. 1979. Notes on the vegetation of Amazonia, III. Terminology of Amazonian forest types subjected to inundation. Brittonia 31: 26-38.

Reich, P. B. & P. Borchert. 1984. Water stress and tree phenology in a tropical dry forest in the lowlands of Costa Rica. Journal of Ecology 72:61-74.

Ribeiro, M. N. G. & J. Adis. 1984. Local rainfall variability: A potential bias for bioecological studies in the Central Amazon. Acta Amazonica 14: 159-174.

Rocas, G., F. R. Scarano & C. F. Barros. 2001. Variation in leaf anatomy of Alchornea triplinervia (Spreng.) Mull. Arg. (Euphorbiaceae) under different light and soil-water regimes. Botanical Journal of the Linnean Society 136: 231-238.

Rosales, J. G., C. Vispo, N. Dezzeo, L. Blanco-Belmonte, C. Kaab-Vispo, N. Gonzalez, F. Daza, C. Bradley, D. Gilvear, G. Escalante, N. Chacon & G. Petts. 2002. Ecohydrology of riparian forests in the Orinoco River Basin. Pp. 93-110 in M. McClain (ed.), The ecohydrology of South American rivers and wetlands. Special Publication 6. International Association of Hydrological Sciences, Wallingford.

Roth, I. 1984. Stratification of tropical forests as seen in leaf structure. Junk, The Hague.

Rottenberger, S. 2003. Exchange of oxygenated volatile organic compounds between Amazonian and European vegetation and the atmosphere. Ph.D. diss., Univ. of Mainz.

--, U. Kuhn, A. Wolf, C, Schebeske, S. T. Oliva, T. Tavares & J. Kesselmeier. In press. Exchange of short-chain aldehydes between Amazonian vegetation and the atmosphere. Ecological Applications.

Scarano, F. R. 1998. A comparison of dispersal, germination and establishment of woody plants subjected to distinct flooding regimes in Brazilian flood-prone forests and estuarine vegetation. Pp. 176-193 in F. R. Scarano & A. C. Franco (eds.), Ecophysiological strategies of xerophytic and amphibious plants in the Neotropics. Serie Oecologia Brasiliensis, 4. PPGE-UFRJ, Rio de Janeiro.

-- & R. M. M. Crawford. 1992. Ontogeny and the concept of anoxia-tolerance: The case of the Amazonian leguminous tree Parkia pendula. Journal of Tropical Ecology 8: 349-352.

--, J. H. Cattanio & R. M. M. Crawford. 1994. Root carbohydrate storage in young saplings of an Amazonian tidal varzea forest before the onset of the wet season. Acta Botanica Brasilica 8:129-139.

--, K. T. Ribeiro, L. F. D. Moraes & H. C. Lima. 1997. Plant establishment on flooded and unflooded patches of a freshwater swamp forest in southeastern Brazil. Journal of Tropical Ecology 14: 793-803.

--, R. I. Rios & F. A. Esteves. 1998. Tree species richness, diversity and flooding regime: Case studies of recuperation after anthropic impact in Brazilian flood-prone forests. International Journal of Ecology and Environmental Sciences 24: 223-235.

--, H. M. Duarte, K. T. Ribeiro, P. J. F. P. Rodrigues, E. M. B. Barcellos, A. C. Franco, J. Brulfert, E. Deleens & U. Luttge. 2001. Four sites with contrasting environmental stress in southeastern Brazil: Relations of species, life form diversity, and geographical distribution to ecophysiologieal parameters. Botanical Journal of the Linnean Society 136: 345-364.

--, T. S. Pereira & G. Rocas. 2003. Seed germination during flotation and seedling growth of Carapa guianensis, a tree from flood-prone forests of the Amazon. Plant Ecology 168: 291-296.

Schluter, U. B. & B. Furch. 1992. Morphologische, anatomische und physiologische Untersuchungen zur Uberflutungstoleranz des Baumes Macrolobium acaciaefolium, charakteristisch fur die Weigand Schwarzwasseruberschwemmungswalder bei Manaus, Amazonas. Amazoniana 12: 51-69.

--, -- & C. A. Joly. 1993. Physiological and anatomical adaptations by young Astrocaryum jauari Mart. (Arecaceae) in periodically inundated biotopes of Central Amazonia. Biotropica 25: 384-396.

Scholander, P. F. & M. O. Perez. 1968. Sap tension in flooded trees and bushes of the Amazon. Plant Physiology 43: 1870-1873.

Schongart, J., M. T. F. Piedade, S. Ludwigshausen, V. Horna & M. Worbes. 2002. Phenology and stem-growth periodicity of tree species in Amazonian floodplain forests. Journal of Tropical Ecology 18: 581-597.

Silvera K., J. B. Skillman & J. W. Dalling. 2003. Seed germination, seedling growth and habitat partitioning in two morphotypes of the tropical pioneer tree Trema micrantha in a seasonal forest in Panama. Journal of Tropical Ecology 19: 27-34.

Singh, H. B. & P. L. Hanst. 1981. Peroxyacetyl Nitrate (PAN) in the unpolluted atmosphere: An important reservoir for nitrogen oxides. Geophysical Research Letters 8: 941-944.

--, M. Kanakidou, P. J. Crutzen & D. J. Jacob. 1995. High concentrations and photochemical fate of oxygenated hydrocarbons in the global troposphere. Nature 378: 50-54.

--, A. Tabazadeh, Y. Fukui, I. Bey, R. Yantosca, D. Jacob, F. Arnold, K. Wohlfrom, E. Atlas, F. Flocke, D. Blake, N. Blake, B. Heikes, J. Snow, R. Talbot, G. Gregory, G. Sachse, S. Vay & Y. Kondo. 2000. Distribution and fate of selected oxygenated organic species in the troposphere and stratosphere over the Atlantic. Journal of Geophysical Research-Atmospheres 105: 3795-3805.

Sioli, H. 1954. Betrachtungen uber den Begriff "Fruchtbarkeit" eines Gebiets anhand der Verhaltnisse in Boden und Gewassern Amazoniens. Forschung Fortschritt 28: 65-72.

Sippel, S. J., S. K. Hamilton, J. M. Melack & E. M. M. Novo. 1998. Passive microwave observations of inundation area and the area/stage relation in the Amazon river floodplain. International Journal of Remote Sensing 19: 3055-3074.

Talbot, R. W., M. O. Andreae, H. Berresheim, D. J. Jacob & K. M. Beecher. 1990. Sources and sinks of formic, acetic, and pyruvic acids over Central Amazonia, 2. Wet Season. Journal of Geophysical Research--Atmospheres 95: 16799-16811.

Thompson, A. M. 1992. The oxidizing capacity of the earths atmosphere: Probable past and future changes. Science 256: 1157-1165.

Vartapetian, B. B., I. N. Andreeva, I. P. Generazova, L. I. Polyakova, I. P. Maslova, Y. I. Dolgikh & A. Y. Stepanova. 2003. Functional electron microscopy in studies of plant response and adaptation to anaerobic stress. Annals of Botany 91 (Special Issue SI): 155-172.

Visser, E. J. W., L. A. C. J. Voesenek, B. B. Vartapetian & M. B. Jackson. 2003. Flooding and plant growth. Annals of Botany 91 (Special Issue SI): 107-109.

Waldhoff, D. & B. Furch. 1998. Effect of waterlogging and flooding on some abundant tree species of Central Amazonia examined under defined conditions in climatic chambers. Proceedings / International Association of Theoretical and Applied Limnology 26: 1886-1887.

-- & --. 2002. Leaf morphology and anatomy in eleven tree species from Central Amazonian floodplains (Brazil). Amazoniana 17: 79-94.

--, W. J. Junk & B. Furch. 1998. Responses of three Central Amazonian tree species to drought and flooding under controlled conditions. International Journal of Ecology and Environmental Sciences 24: 237-252.

-- ,-- & --. 2000. Comparative measurements of chlorophyll a fluorescence parameters of Nectandra amazonum under different environmental conditions in climate controlled chambers. Proceedings / International Association of Theoretical and Applied Limnology 27: 2052-2056.

--, B. Furch & W. J. 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: 225-235.

Williamson, G. B. & F. Costa. 2000. Dispersal of amazonian trees: Hydrochory in Pentaclethra macroloba. Biotropica 32: 548-552.

--, -- & C. V. Minte Vera. 1999. Dispersal of Amazonian trees: Hydrochory in Swartzia polyphylla. Biotropica 31 : 460-465.

Wilske, B., R. Holzinger & J. Kesselmeier. 2001. Evidence for ethanolic fermentation in lichens during periods of high thallus water content. Symbiosis 31: 95-111.

Wittmann, F. & W. J. Junk. 2003. Sapling communities in Amazonian white-water forests. Journal of Biogeography 30(10): 1533-1544.

-- & P. Parolin. 1999. Phenology of six tree species from Central Amazonian varzea. Ecotropica 5: 51-57.

-- & --. In press. Above-ground roots in Amazonian floodplain trees. Biotropica.

Worbes, M. 1985. Structural and other adaptations to lung-term flooding by trees in Central Amazonia. Amazoniana 9: 459-484.

--. 1986. Lebensbedingungen und Holzwachstum in zentralamazonischen Uberschwemmungswaldern. Scripta Geobotanica. Erich Goltze, Gottingen.

--. 1989. Growth rings, increment and age of trees in inundation forests, savannas and a mountain forest in the Neotropics. IAWA Bulletin, n.s., 10: 109-122.

--. 1992. Occurrence of seasonal climate and tree-ring research in the Tropics. Lundqua Report 34: 338-342.

--. 1996. Rhythmisches Wachstum und anatomisch-morphologische Anpassungen an Lebensstrategien von Baumen in zentralamazonischen Uberschwemmungswadern. Mitteilungen der Deutschen Dendrologischen Gesellschaft 82:155-172.

--. 1997. The forest ecosystem of the floodplains. Pp. 223-366 in W. J. Junk (ed.), The Central Amazon floodplain: Ecology of a pulsing system. Ecological Studies, 126. Springer Verlag, Heidelberg.

-- & W. J. Junk. 1989. Dating tropical trees by means of [C.sub.14] from bomb tests. Ecology 70: 503-507.

Ziburski, A. 1991. Dissemination, Keimung und Etablierung einiger Baumarten der Uberschwemmungswalder Amazoniens. Pp. 1-96 in W. Rauh (ed.), Tropische und subtropische Pflanzenwelt, 77. Akademie der Wissenschaften und der Literatur, Mainz.

Zimmermann, H. M., K. Hartmann, L. Schreiber & E. Steudle. 2000. Chemical composition of apoplastic barriers in relation to radial hydraulic conductivity of corn roots (Zea mays L.). Planta 210: 302-311.

P. PAROLIN, (1) O. DE SIMONE, (1) K. HAASE, (1) D. WALDHOFF, (2) S. ROTTENBERGER, (3) U. KUHN, (3) J. KESSELMEIER, (3) B. KLEISS, (4) W. SCHMIDT, (5) M. T. F. PIEDADE, (6) AND W. J. JUNK (1)

(1) Tropical Ecology Working Group Max Planck Institute for Limnology 24302 Ploen, Germany

(2) Center for Biology Botanical Institute and Botanical Garden Christian-Albrechts-University Kiel 24098 Kiel, Germany

(3) Biogeochemistry Department Max Planck Institute for Chemistry 55020 Mainz, Germany

(4) Atmospheric Chemistry Department Max Planck Institute for Chemistry 55020 Mainz, Germany

(5) Department of Biology Carl von Ossietzky-University Oldenburg 26111 Oldenburg, Germany

(6) INPA/Max Planck 69011 Manaus, Amazonas, Brazil