Ann Bot-2009-Parolin-359-76

Annals of Botany 103: 359 376, 2009 doi:10.1093/aob/mcn216, available online at www.aob.oxfordjournals.
org
REVIEW
Submerged in darkness: adaptations to prolonged submergence by woody species of the Amazonian oodplains
Pia Parolin*
Max-Planck-Institute for Evolutionary Biology, Tropical Ecology, PO Box 165, D-24302 Plon, Germany
Received: 21 April 2008 Returned for revision: 2 June 2008 Accepted: 1 September 2008 Published electronically: 10 November 2008
Background In Amazonian oodplain forests, .1000 tree species grow in an environment subject to extended annual submergence which can last up to 9 months each year. Water depth can reach 10 m, fully submerging young and also adult trees, most of which reproduce during the ood season. Complete submergence occurs regularly at the seedling or sapling stage for many species that colonize low-lying positions in the ooding gradient. Here hypoxic conditions prevail close to the water surface in moving water, while anaerobic conditions are common in stagnant pools. Light intensities in the oodwater are very low. Questions and Aims Despite a lack of both oxygen and light imposed by submergence for several months, most leafed seedlings survive. Furthermore, underwater growth has also been observed in several species in the eld and under experimental conditions. The present article assesses how these remarkable plants react to submergence and discusses physiological mechanisms and anatomical adaptations that may explain their success. Key words: Adaptation, Amazonian oodplains, darkness, environmental stress, ooding, hypoxia, submergence tolerance, trees, underwater photosynthesis, woody species.
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IN T RO DU C T IO N An excess of water is generally considered to be deleterious to plant health and growth (Schueler and Holland, 2000), and total submergence quickly kills most species. Not so in Amazonian oodplain forests where the seasonal regularity of the so-called ood-pulse (Junk et al., 1989) of the Amazon river has given rise to plants that survive regularly recurring long-term (weeks or months) total submergence. More than 1000 tree species successfully survive and complete their life cycles in this region (Wittmann et al., 2006). Submergence of terrestrial woody species is the main topic of the present review. The aim is to bring together much of the existing descriptive and experimental information on how tree species from Central Amazonian oodplains react to complete submergence. Numerous woody species thrive in the oodplains. Many grow to large trees, often with commercial value, and show extreme submergence tolerance not seen in any other ecosystem. They are able to overcome several weeks or months of complete submergence as foliated plants despite the stresses (see below) imposed by total inundation that can last several weeks or months each year. The mechanisms allowing these species to be so tolerant of submergence remain largely obscure. The current state of our understanding is discussed in this review. Trees have evolved to survive in a terrestrial environment. Flooding imposes various stresses on these life forms that include oxygen deprivation of both roots and shoots, drastic changes in the availability of carbon dioxide, mineral nutrients and in the concentrations of phytotoxins, increased anaerobic decomposition of organic matter, increased solubility of potentially toxic mineral substances such as ferrous ions, very low soil redox potentials, and light deprivation (Joly and
* E-mail pparolin@botanik.uni-hamburg.de
Crawford, 1982; Kozlowski, 1984; Crawford, 1989, 1992; Armstrong et al., 1994; Vartapetian and Jackson, 1997; Schluter and Crawford, 2001, Visser et al., 2003; Bailey-Serres and Voesenek, 2008). Trees are especially vulnerable to submergence in warm conditions, which makes their tolerance in tropical Amazonia all the more remarkable since warm growing conditions last the whole year. This is in marked contrast to temperate zones where ooding frequently occurs during winter when plants are in a quiescent state while waterlogged or submerged. In the Amazon region, submergence occurs when temperature and light conditions are optimal for plant growth and when many species maintain their leaves below water for months.
The ecosystem of Amazonian oodplains
Amazonian oodplain forests cover approx. 300 000 km2 along and between the main rivers in the Amazon basin (Fig. 1A and B). They are characterized by a monomodal, predictable ood-pulse (Junk et al., 1989). The following environmental characteristics pose constraints for plant growth.
Very long uninterrupted ooding. The areas where trees grow are ooded for up to 210 d every year (Junk, 1989). The palm Astrocaryum jauari (Arecaceae) survives well even though it can be submerged for 300 d a year (Schluter et al., 1993). The annual ooding period can thus last longer than the dry terrestrial phase (which is the main growing period). High ood amplitudes. In Central Amazonia, every year the river levels rise and fall by up to 10 m, causing an annual ood-pulse (Junk et al., 1989, Fig. 2A and B). However, inter-annual variations occur (Fig. 2B) which can mean that certain trees can miss being waterlogged for one or two consecutive years if the water is untypically low, as it was in
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Parolin Prolonged ooding of woody species in Amazonian oodplains
F I G . 1. Amazonian oodplain trees. (A) Forest with highly ood-tolerant tree species at high water; (B) varzea with high productivity as shown by macrophyte growth; (C) exposed roots with receding water; (D) seedling establishment upon receding water in igapo; (E) Crudia amazonica and (F) Vitex cymosa maintain their leaves above the water surface whereas the leaves below water rot within a few days; (G) leaf covered by freshwater sponge in igapo; (H) Symmeria paniculata maintains all leaves above and below water ( pictures by Pia Parolin).

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F I G . 2. Water level (height above sea level) of the Amazon River near Manaus showing the regular ood-pulse (Junk et al., 1989): means of (A)12 months and (B) monthly height between 1987 and 1999 showing interannual variations.
1995 and 1997. In contrast, in some years, water levels are untypically high and certain areas can remain waterlogged for two or more consecutive years. This was the case in 1993/94 (Fig. 2B).
Rapid changes of water levels. The water level in the Amazon rises at an average of 50 mm d21. However, sometimes for several weeks in the periods of maximum change in levels, a rise or fall of up to 100 150 mm d21 has been recorded (Junk and Piedade, 1997) between April and June. This fast rate of change negatively affects the effectiveness of morphological adaptations to ooding such as adventitious roots which are produced in the oxygen-rich surface layers of the water. Hypoxia. As soon as water covers the soil, partial oxygen
the oodplain water from photosynthesis or stirred into the water body by wind and currents. Oxygen concentrations at depths below 300 mm are typically about 1 mg L21 due to depletions by decomposition of dead biomass. Clearly, very little oxygen is available from the oodwater itself to support plant respiration. Extremely low oxygen concentrations were recorded by Furch and Junk (1997) at Lago Camaleao, where anoxia and the presence of H2S were observed periodically at a depth of 1 2 m. In extreme cases, up to 1 mg L21 of H2S have been measured at depths of 0.5 m between June and September, the months when water levels are highest.
High sedimentation. The sediment-rich white water oodplains of the Amazon River and its tributaries called varzea (Prance, 1979) are subjected to high rates of sediment deposition which can amount to 300 1000 mm each year (Junk, 1989, Campbell et al., 1992). A concentration of about 100 mg L21 of suspended mineral solids has been reported near Manaus. In deep water, 0.5 m from the bottom, suspended solids may reach 822 mg L21 (Furch and Junk, 1997). These ne coarse sediments increase the severity of hypoxia and prejudice leaf photosynthesis below water by imposing
deciency (hypoxia) arises in the rhizosphere (Kozlowski, 1984). Oxygen-consuming decomposition and fast sedimentation rates further decrease oxygen supply to the roots and may lead to a complete absence of oxygen (anoxia) in the rhizosphere. Concentrations of dissolved oxygen in the oodwater in the range 05 6.0 mg L21 have been recorded depending on the season and time of day (Furch and Junk, 1997). There appear to be only modest inputs of oxygen into
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Parolin Prolonged ooding of woody species in Amazonian oodplains 1985; Meyer, 1991; Schluter and Furch, 1992; Schluter et al., 1993; Scarano et al., 1994; Botelho, 1996; Nascimento et al., 1998; Waldhoff and Furch, 1998, 2002; Graffmann, 2000; De Simone et al., 2002a, b, 2003a, b, c; Gribel and Gibbs, 2002; Waldhoff et al., 2002; Parolin et al., 2004, 2006, 2008a, b, c; Ferreira et al., 2005, 2007; Maia et al., 2005; Oliveira-Wittmann, 2006; Piedade et al., 2006; Wittmann et al., 2006; Graffmann et al., 2008; Horna et al., 2008). Most of these studies were performed in the vicinity of Manaus. Unfortunately, in many of these reports few qualitative descriptions can be found on any one species, and no study focuses specically on reactions to submergence or analyses how the trees tolerate it over prolonged periods. Complete submergence is a very different constraint from waterlogging of the soil and root system or even partial submergence where much of the shoot remains above the water line (Colmer and Pedersen, 2008). Totally submerged plants have no direct contact with atmospheric oxygen, and sunlight is weak or extinguished. Although abscisic acid (ABA) accumulation leading to leaf stomatal closure has been described in the literature as an almost immediate response of plants to soil waterlogging (Voesenek et al., 2004), this is unlikely to occur in submerged Amazonian oodplain forest trees, since in rice and Rumex palustris at least, ABA levels decrease sharply with a few hours of total submergence (Hoffmann-Benning and Kende, 1992; Benschop et al., 2005). Gas exchange taking place in the leaves of submerged plants as opposed to waterlogged plants seems a common yet poorly understood feature (Schluter, 1989; Parolin et al., 2004) where different adaptations for growth and survival are required since they cannot escape by elongating to above the (rising) water. In this article the term submerged is used in the sense that there is no direct contact between any part of the shoot and the aerial atmosphere. In contrast, the term waterlogged is used where at least a part of the plant (the stem and crown or even only single branches or leaves) protrude above the water surface. When the term ooding is used, as frequently found in the literature, this is used to imply either waterlogged or submerged conditions.
turbidity and depositing sediment on the leaf surfaces that remains after the oodwater recedes (Ewing, 1996).
Water temperature. With average temperatures of 27 298C (Furch and Junk, 1997), the warm oodwater supports fast rates of oxygen-depleting respiration by plants and microorganisms while itself carrying less dissolved oxygen than would cooler water. For example, water at 108C contains 11.26 g m23 when in full equilibrium with air but only 7.36 g m23 at 308C, at 1 atmosphere pressure (1.013 105 N m22 or 101.3 kPa) (http://openlearn.open.ac.uk/mod/ resource/view.php?id=185880).
Light penetration through water. In the clear water of the igapo (sensu Prance, 1979) at a depth of 8 m there is still a quantum ux of 2 mmol m22 s21. In the turbid water of the varzea, no light could be measured below 3 m (Furch et al., 1985), while Waldhoff et al. (2002) measured a quantum ux of 1 10 mmol m22 s21 (PAR) at 1 7 m. In the varzea, 99% extinction occurs below 1 5 m. In contrast, light intensities reach values of 3000 mmol m22 s21 at noon above water level (Furch et al., 1985). Different light penetration patterns among the different water types (white, black and clear) appear to inuence plant establishment on the forest borders in varzea and igapo (F. Wittmann, Max-Planck-Institute for Chemistry, Mainz, Germany, pers. comm.), but no quantitative data are currently available.
Mechanical strain. The dynamics, current and erosion power of the river system may mechanically damage trees and deter seedling establishment (Fig. 1C, D). However, mechanical strain of this kind may only be signicant along the banks of the main river channels, which cover only a small part of the extensive oodplains. Its impact can probably be neglected in the backwaters. Drought. In the dry months of the terrestrial phase, when river
levels and precipitation are low (between September and November; Fig. 2A), severe shortage of water may limit plant growth. Despite the challenging conditions for plant growth in the Amazonian oodplains, the number of extant angiosperm tree species is very high. With 50 180 species ha21 with diameter at breast height !10 cm (Pires and Koury, 1959; Balslev et al., 1987; Ayres, 1993; Worbes, 1997; Wittmann et al., 2002), species richness is greater than for others of the Earths forests. At least 918 ood-tolerant tree species have been identied in the nutrient-rich white water varzea (Wittmann et al., 2006) and many more in the nutrient-poor black water oodplain forests of Amazonia. This makes Amazonian oodplain forests the most species-rich oodplain forests, with many endemic species. In a recent review, Wittmann et al. (2008) classied 40% of 186 common central Amazonian varzea tree species as endemics to the Amazonian varzea. R E ACT I ON S AN D AD A P TAT I ON S TO CO MPLETE S UBME RGE NCE Several studies over the last 10 years have described a large variety of specic reactions to complete submergence of trees and seedlings in Amazonian oodplains (e.g. Worbes,
Vegetative phenology under water
In Amazonian oodplains, different tree species exhibit different leaf phenologies upon submergence (Table 1). Most species shed their submerged leaves, but some maintain them for months or even years despite prolonged submergence, and without apparent damage (Fig. 1E, F, H and Fig. 3; Waldhoff and Furch, 2002). Leaf life span varies between the species, ranging from a few months in Senna reticulata to up to 5 years in Nectandra amazonum or even longer in Symmeria paniculata (Fig. 1H). Submerged seedlings of several species sprout new leaf buds under water (Table 1; Fig. 3G) and expand the leaves as soon as the plants emerge, or even before emergence (Parolin, 2001a). Unfortunately, there are no published studies of the characteristics of leaves that emerge under water. However, several studies analyse the responses of aerially produced leaves to
TA B L E 1. Leaf phenology upon waterlogging and submergence in Amazonian oodplain trees

No leaf shedding upon waterlogging Shedding of all leaves upon waterlogging ? ? ? 2 ? 2 ? ? ? 2 2 ? ? Shedding of below-water leaves upon waterlogging No leaf shedding upon tree submergence ? Shedding of all leaves upon tree submergence ? New leaf production above water during waterlogging ? ? ? ? ? ? ? ? New leaf/shoot production below water during submergence ? ? ? ? ? ? ? ? ? ? ? ? ?
Species studied Acosmium nitens (Vogel) Yakovlev Albizia multiora Kunth. (Barneby & Grimes) Alchornea castaneifolia (Hum. & Bonpl. ex Willd.) A. Juss. Astrocaryum jauari Mart. Cecropia latiloba Miq. Ceiba pentandra (L.) Gaertn. Crataeva benthamii Eichler Crudia amazonica Spruce ex Benth. Eschweilera tenuifolia (BERG.) MIERS Eugenia inundata DC. Garcinia brasiliensis Mart. Gustavia augusta L. Genipa spruceana Steyerm. Hevea spruceana (Benth.) Mull. Arg. Himatanthus sucuuba (Spruce) Wood. Ilex inundata Poepp. ex Reissek Laetia corymbulosa Spruce ex Benth. Licania apetala (E. Mey.) Fritsch Macrolobium acaciifolium (Benth.) Benth. Nectandra amazonum Nees Pouteria elegans (DC.) Baehni Pouteria glomerata (Pohl ex Miq.) Radlk. Pseudobombax munguba (Mart. & Zucc.) Dugand Psidium acutangulum DC. Salix martiana Willd. Senna reticulata (Willd.) H.S. Irwin & Barneby Simaba guianensis Aubl. Swartzia laevicarpa Amshoff Symmeria paniculata Benth. Tabebuia barbata (E. Mey.) Sandwith Tabernaemontana juruana (MARKGR.) SCHUMANN EX J. F. MACBRIDE Vitex cymosa Bert. ex Spreng.
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F I G . 3. Submergence experiments (University of Kiel, Germany). (A) Nectandra amazonum maintains its leaves below water (pictures under experimental conditions after submergence in darkness for 3 months). (B) Seedlings of Pterocarpus amazonum after 3 weeks of submergence in complete darkness and (C) 1 month after emergence. (D) Psidium acutangulum submerged for 2 weeks in experimental conditions. (E) shoot increment in a submerged plant of Gustavia augusta and (F) Tabernaemontana juruana after 3 months in complete darkness. (G) after 4 d of complete submergence under experimental conditions, Salix martiana produced adventitious roots on the stem below water (arrows), and so did Nectandra amazonum (H) after 19 d. (I) New leaves emerging below water in Cecropia latiloba (pictures by Danielle Waldhoff).
Parolin Prolonged ooding of woody species in Amazonian oodplains subsequent submergence (Schluter and Furch, 1992; Schluter et al., 1993; Waldhoff and Furch, 2002; Waldhoff et al., 2002).
Growth and biomass changes
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The main period of biomass production is the terrestrial non-ooded phase (Schluter, 1989; Worbes, 1997). With submersion, growth in height stops after 1 3 weeks in most species (Parolin, 2001a). However, some species show underwater shoot extension even in complete darkness. In an experiment in a greenhouse at the University of Kiel, shoots of Gustavia augusta were found to elongate by almost 400 mm under such conditions (Fig. 3E), while Tabernaemontana juruana elongated by about 30 mm (Fig. 3F). The portion of the stems that elongated below water had neither chlorophyll nor leaves. In the same greenhouse under experimental conditions, completely submerged Salix martiana produced adventitious roots on the stem (Fig. 3G; Waldhoff and Furch, 2002; Waldhoff, 2003). Seedlings of N. amazonum developed lenticels after 13 d submergence (covering 10 20% of the stem surface area); adventitious roots with negative geotropism emerged after 16 d of submergence, and more adventitious roots appeared after 19 d (Fig. 3H). While waterlogged plants of these species induced very few adventitious roots (no more than 5% of the complete root mass), in completely submerged plants adventitious roots contributed up to 50% of the total root mass (Waldhoff et al., 2000b).
Dormancy, quiescence and periodic growth
Since the benets of LOES do not outweigh the costs when ooding is too deep as in Amazonian oodplains a quiescence strategy characterized by limited underwater growth and conservation of energy and carbohydrates is to be expected. Waldhoff et al. (2002) observed that the photosynthetic system of submerged leaves becomes dormant. Evidence for this adaptation in terms of very low photosystem II (PSII) chlorophyll uorescence has been found in the eld and under more controlled experimental conditions for G. augusta, N. amazonum and T. juruana. After 5 months of submergence in darkness, the relative potential quantum yield, Fv/Fm, decreased from 0.7 to 0.1 upon emergence, indicating a dormant photosynthetic apparatus. In temperate European plants with which the method of chlorophyll uorescence measurement was originally developed, an Fv/Fm ratio below 0.2 0.3 is taken to indicate senescence or irrevers` ible damage (Bolhar-Nordenkampf and Goetzl, 1992). However, in the three species of Amazonian plants analysed here the leaves were merely quiescent since, upon de submergence, the Fv/Fm ratio returned to normal values after 6 d, indicating no irreversible damage.
Mortality
Some non-woody species avoid ooding by completing their life cycle between two subsequent ood events, and ooding itself is survived by dormant life stages (e.g. seeds) (Bailey-Serres and Voesenek, 2008). In Amazonian oodplain trees, dormant periods are found in the form of periodical growth reductions as a consequence of ooding, which are reected by the formation of increment rings and by periodic shoot elongation (Worbes, 1989, 1997; Worbes and Junk, 1989). Entering a state of rest may help the trees minimize stress from ooding. However, this period of rest lasts for a few weeks only; trees then resprout and elongate their shoots in the remaining weeks or months of waterlogging or submergence. No species is dormant for the whole ooded period. Waterlogged trees typically show high physiological activity during most of the ooded period, while completely submerged trees show some growth at the beginning and end of ooding. This pattern is probably related to higher light intensities during early and late ooding when the water column is ,1 m deep. It is widely recognized that some submergence-tolerant plants such as R. palustris or the majority of rice cultivars use avoidance strategies that involve the development of certain anatomical and morphological traits, in particular fast underwater elongation that returns shoot tips to the air if the water is not too deep. This amelioration response, called low oxygen escape syndrome (LOES; Bailey-Serres and Voesenek, 2008), facilitates the survival of submerged organs. However, LOES is costly and will only be selected for in environments where the cost is outweighed by benets such as improved O2 and carbohydrate status, both contributing to a higher tness.
Considerable seedling mortality is brought about by ooding in the Amazonian oodplains. However, Ziburski (1990) found that most tree species fatalities are higher from drought than from ooding. However, few quantitative data are available. Table 2 summarizes what is known. Extremely low mortality was recorded in seedlings of the palm A. jauari, with only 10% mortality recorded after 300 d sub mergence in the eld at 288C (Schluter, 1989). In Himatanthus sucuuba, mortality ,30% was found in varzea populations in one ooded period. In contrast, in upland populations of the same species, 100% mortality has been reported (Ferreira, 2002).
Germination underwater
The seeds of many tree species remain visually sound when continuously submerged or oating for .2 months (Table 3; Parolin and Junk, 2002; Parolin et al., 2004). This is in marked contrast to the majority of land plants, whose seeds quickly lose viability if submerged for prolonged periods (Hook, 1984). Seeds of Amazonian oodplain species which are kept in air, dry or decompose within a few days (e.g. Tabebuia barbata and N. amazonum) or weeks (e.g. Senna reticulata and Aldina latifolia; Parolin et al., 2008a). In species that reproduce during the aquatic phase and regardless of whether the seeds oat or sink, germination starts after the ood recedes (Parolin et al., 2004). However, many seeds can oat for very long periods and germinate already while oating (Table 3). While some species produce only a radicle, others form fully developed seedlings, emitting radicles, cotyledons and primary leaves from buoyant seeds, as observed in the eld (Ziburski, 1990) and under experimental conditions in Manaus (Oliveira, 1998; Oliveira-Wittmann et al., 2007). This behaviour may enhance fast seedling establishment, because plants are growing while the water is still receding. However, seedlings that develop in water are often morphologically different from those that
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Anatomical characteristics and changes induced by submergence Leaves. Deciduous or evergreen, and regardless of whether
TA B L E 2. Seedling mortality in Amazonian varzea on emersed and submerged forest oor

Seedling mortality (%) on submerged forest oor 0 ? ? 4 9 10 10 11 18 24 30 42 49 50 78 92 100 100 Seedling mortality (%) on emersed forest oor 0 10 9 ? 0 ? ? ? 97 ? 0 100 70 ? 40 ? 15 70
Species Genipa spruceana 1 Salix martiana 2 Cecropia latiloba 4 Buchenavia oxycarpa 2 Vitex cymosa 6 Astrocaryum jauari 7 Eschweilera ovalifolia 2 Eschweilera ovalifolia 7 Crataeva benthamii 2 Neolabatia cuprea 2 Himatanthus sucuuba 5 Vitex cymosa 2 Psidium acutangulum 2 Macrolobium acaciifolium 7 Macrolobium acaciifolium 2 Pterocarpus amazonum 2 Senna reticulata 4 Senna reticulata 3
Data from 1Gurgel (2008) (under experimental conditions, after 90 d), Ziburski (1990), 3Parolin (2001b), 4Parolin et al. (2002b) (under eld conditions), 5Ferreira (2002) (under experimental conditions), 6 Oliveira-Wittmann et al. (2008), 7Schluter (1989).
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develop on substrate, and exhibit strongly warped shoots. Ziburski (1990) found that seedlings of Hevea brasiliensis and Pseudobombax munguba, formed while oating, rotted within a few days, or that radicles were already too well developed (A. latifolia) for seedlings to survive once deposited on dry ground. Similarly, radicles of water-germinated seedlings moved to a substrate were found by Oliveira-Wittmann et al. (2007) to be incapable of penetrating the soil, resulting in seedling death. However, it cannot be excluded that seedlings emerging from oating seeds may successfully establish when they get trapped by oating debris and associated organic material.
they are retained or lost under water, the leaves of Amazonian oodplain trees exhibit traits which are generally considered as xeromorph (Fig. 4A, B; Bolhar-Nordenkampf and Draxler, 1993; Waldhoff et al., 2002; Waldhoff and Parolin, 2008. Typical xeromorphic features are large epidermal cells (Hevea spruceana and Eugenia inundata), thick outer epidermal walls (Garcinia brasiliensis and H. sucuuba), thick cuticle (Eschweilera tenuifolia and Simaba guianensis), compact spongy parenchyma with few small intercellular spaces (S. reticulata and Licania apetala), sunken stomata (Vitex cymosa and Pouteria glomerata) and transcurrent vascular bundles with a strong sclerenchymatous bundle sheath (N. amazonum and E. inundata). As leathery and/or xeromorphic leaves are typical of tropical trees (Roth, 1984), such characteristics of oodplain trees are unlikely to represent adaptations to ooding. They may, instead, be preadaptations to the dry upland habitats where these species originated (Kubitzki, 1989; Wittmann et al., 2006). The leaves which are retained when submerged maintain their structure and functional capability long after the oods recede and dry conditions return. Other studies mainly in temperate wetlands have shown that leaf plasticity allows different types of leaf anatomy to form under different environmental conditions (Mommer et al., 2005, 2006). The development of new, acclimated leaves may be crucial for survival under water, especially in ameliorating the problem of impeded gas exchange. True aquatic plant species often have thin, highly dissected leaves, a morphology which is believed to be directed to the optimization of gas exchange underwater (Sculthorpe, 1967). These aquatic leaves do not possess stomata. Instead, cuticles of these leaves are minimized or even lacking, and, therefore, underwater gas exchange most probably occurs via the epidermal cells and cuticle layer (Mommer and Visser, 2005). Fernandes-Correa and Furch (1992) state that, surprisingly, most plants in Amazonian oodplains do not display scotomorphogenesis induced by the lack of light during the ood periods. Their outer form, inner structure, metabolism and movements
TA B L E 3. Generative adaptations against submergence in Amazonian oodplain trees

Adaptation Dispersal linked to water and sh Seeds remain viable while submerged/oating for several months Function of adaptation Large distance dispersal Dispersal linked to water, wait until terrestrial period allows establishment Most species Aldina latifolia, Campsiandra comosa, Cecropia latiloba, Crataeva benthamii, Crudia amazonica, Mora paraensis, Nectandra amazonum, Senna reticulata, Swartzia polyphylla, Tabebuia barbata, Vatairea guianensis, Vitex cymosa Aldina latifolia, Carapa guianensis, Cecropia latiloba, Crataeva benthamii, Hevea brasiliensis, Laetia corymbulosa, Mora paraensis, Nectandra amazonum, Pachira aquatica, Pithecellobium inaequale, Vatairea guianensis Hevea brasiliensis, Pseudobombax munguba, Salix martiana Species (examples) References Goulding (1983); Kubitzki and Ziburski (1994) Parolin and Junk (2002); Parolin et al. (2004)
Germination in water (radicle emission)
fast germination upon emergence
Kubitzki (1985); Ziburski (1990); Parolin and Junk (2002); Scarano et al. (2003); Koshikene (2005); Oliveira-Wittmann et al. (2007) Ziburski (1990); Oliveira (1998); Oliveira-Wittmann et al. (2007)
Germination in water (fully developed seedling)
Fast germination upon emergence?
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Emerged leaf
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F I G . 4. Anatomical characteristics: cross-section of (A) emerged and (B) submerged leaf of Tabernaemontana juruana; (C) Eugenia inundata cross-section with large epidermal cells; (D) Garcinia brasiliensis thick outer-epidermis walls; (E) stomata on the upper leaf side in Garcinia brasiliensis; (F) sunken stomata on the lower side of the leaf in Cassia leiandra, with wax crystals; (G) Psidium acutangulum cross-section of adventitious root with schizogenous aerenchyma and some larger intercellular spaces of lysigenous origin; (H) Cecropia latiloba: cross section of young adventitious root with aerenchyma ( pictures by Danielle Waldhoff).
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Parolin Prolonged ooding of woody species in Amazonian oodplains measured by Parolin (2001a). Oliveira-Wittmann (2006) submerged seedlings of Laetia corymbulosa in a greenhouse and observed adventitious roots protruding directly from the veins of leaves which were still attached to the plant, and also in detached leaves. Many roots are characterized by the formation of suberized and lignied barriers in the exodermis that can be expected to regulate radial transport of solutes and gases (De Simone et al., 2003b). In four species from Amazonian oodplains, De Simone et al. (2003b) found that radial loss of oxygen was effectively restricted by the formation of suberized barriers but not by lignication of exodermal cell walls. Species which form new roots below water also form suberized barriers (De Simone, 2003b). Suberin polymers also play a determining role in pathogen defence, either by a breakdown of polymers by enzymes of microbial origin (e.g. in L. corymbulosa and S. martiana) and subsequent release of toxic phenols, or by acting as a mechanical barrier (De Simone et al., 2003b).
Aerenchyma. Aerenchyma facilitates gas transfer through the
with respect to the ambient environment called photomorphogenesis in light apparently are not optimized or changed with respect to the long period of darkness under water (Fig. 4A, B). Since many leaves do not rot or detach from the plant during submergence, some type of morpho-anatomical adjustment presumably must exist to explain this, but research into this aspect is needed. Only two morphological characteristics of submerged leaves a thick cuticle and thick outer epidermis walls are clearly different from non-submerged leaves (Waldhoff and Furch, 2002). In species that do not possess these characteristics, leaves rot quickly when submerged and are shed within a few days (Table 1). Damage to the mesophyll of submerged leaves by microbial decomposition processes has never been observed (Fernandes-Correa and Furch, 1992). The leaves that survive submergence can be just as functional as those sprouting later (Fernandes-Correa and Furch, 1992), while chlorophyll content may lie within the range of that of non-submerged leaves or can even become elevated (Furch, 1984). Submerged leaves usually appear darker than leaves that subsequently sprout following de-submergence, a consequence of greater chlorophyll content (Furch, 1984) and a smaller amount of inter cellular space (Schluter, 1989). In no cases have leaves been found to be inltrated with water (Schluter, 1989; Waldhoff and Parolin, 2008), in contrast to the earlier proposal of Scholander and Perez (1968). Thick cuticles (Fig. 4C, D) and epicuticular waxes, and an associated gas-lled outer layer (Schluter, 1989) may well prevent inux of water into submerged leaves and also improve their capacity to withstand mechanical impact during inundation (Schluter et al., 1993). If submerged leaves normally became inltrated, gas exchange and mineral supply would be prevented (Fernandes-Correa and Furch, 1992). It is probable that the waxy leaf surfaces that are abundant in some species (Fig. 4F) favour the retention of a gas layer over the leaf surface (Fernandes-Correa and Furch, 1992). These gas lms enable the stomata to remain open when submerged (Colmer and Pedersen, 2008) and allow a small amount of photosynthesis. This would be enhanced by the high partial pressures of dissolved CO2 that often prevail in the water (K. Furch, Max-Planck-Institute for Limnology/ Plon, Germany, pers. comm.) that create a diffusion gradient driving CO2 into the stomatal cavities. From the observations described, it can be concluded that leaves not shed at the beginning of the inundation mostly remain functional when submerged, at least to depths where some light is available (Furch, 1984; Schluter and Furch, 1992).
Roots. Root activity is restricted by total submergence
(Worbes, 1997). Under natural conditions in the oodplains, adventitious roots, lenticels or stem hypertrophy were seldom observed, probably due to the constant change in water level (Parolin et al., 2004). The potential capacity of Amazonian oodplain trees to form these adaptations becomes more evident in ooding experiments under more controlled conditions. Thus, although not frequently encountered in the eld, their function may be important in years with ooding anomalies. As mentioned above, submerged N. amazonum can produce adventitious roots (Fig. 3H), and lengths up to 105 mm (compared with 370 mm in waterlogged individuals) have been
shoot to the root system by lowering the resistance that hampers gas diffusion and mass ow within organs (Coutts and Armstrong, 1976; Bailey-Serres and Voesenek, 2008). The presence of aerenchyma can provide a system of interconnected channels from leaf to root tip. However, analyses by Worbes (1986) of the xylem from approx. 100 dicotyledonous tree species did not reveal signicant amounts of aerenchyma. Worbes (1997) states that even if aerenchyma were present, the long length of tree roots (up to 30 m in adult trees) precludes the possibility of gas exchange processes between stem and root tips by means of gas diffusion. An alternative mechanism, that of mass ow driving long-distance root aeration in trees via aerenchyma, is controversial (Armstrong and Armstrong, 2005). Usually, trees of inundation forests cannot support the O2 demand for the respiration of their roots during the aquatic phase via lenticels in the stems and air conducting systems or via pneumatophores. Exceptions include mangrove and Taxodium distichum (Worbes, 1997). Also Nunez-Elisea et al. (1999) found that in some water lilies (Annona species), waterlogging did not increase intercellular gas spaces in pre-existing xylem near the pith or in xylem tissue formed during ooding, and concluded that ood tolerance did not involve a promotion of aerenchyma formation in the stem. Botelho et al. (1998) describe a similar situation in Inga vera and Virola surinamensis from eastern Amazonian oodplains: anatomical cuttings of experimentally raised saplings did not show any aerenchyma formation or other structural adaptation to ooding. Despite the foregoing, some observations do point to morphological and anatomical stress-avoiding systems. For example, aerenchyma tissues were found in the roots of 2-year-old seedlings of the palm A. jauari (Schluter, 1989), as would be expected since aerenchyma is commonly found in palms (Scarano et al., 1994). Microelectrode investigations on 2- to 3-month-old cuttings from S. martiana showed that their well-oxygenated aerenchymatous adventitious roots were able to build up a several millimetres thick oxygenated layer around the whole roots, suggesting a mechanism of detoxifying reduced phytotoxins by radial oxygen loss (ROL; De Simone
Parolin Prolonged ooding of woody species in Amazonian oodplains et al., 2002b; Haase et al., 2003). In older roots from adult trees submerged by several metres of water, the formation of aerenchyma may be of little importance for longitudinal oxygen transport not only because of the long diffusion pathway that exceeds the approx. 300 mm down which aeration by diffusion is effective (Armstrong, 1979), but because the lacunae are destroyed by secondary root thickening. Overall, gas transport via aerenchyma appears to play only a minor role at best in sustaining submerged Amazonian tree species.
Physiological reactions Leaf water potential. In combination with other observations,
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leaf water potential provides a basis for judging the functional capability of the leaves. The water potentials of several broadleaf, woody plants that frequently occur in inundation forests fall within the range between 0.2 and 2.4 MPa (Fernandes-Correa and Furch, 1992). One-year-old leaves which had been submerged in several metres depth for some months always gave lower water potentials than newly emerged, non-submerged leaves of the same species that were only a few weeks old (Fernandes-Correa and Furch, 1992).
Leaf chlorophyll. In most species analysed, total chlorophyll
L. corymbulosa and P. glomerata, light-harvesting chlorophyllbinding proteins (LHCPs) a protective component of PSII become degraded, indicating that PSII must be protected by other proteins since photosynthetic capacity is retained. Rubisco as a component of the Calvin cycle also degraded only partly in several species analysed under experimental submergence (pers. obs.). Antioxidant compounds and vitamins in plant leaves can minimize plant damage by alleviating oxidative challenge and organ damage under submersion. Fruits of Amazonian oodplain trees contain some of the highest known concentrations of vitamin C in plants (e.g. Myrciaria). Concentrations of another antioxidant, vitamin E, are also high in the latex and the leaves of various Amazonian species (Oliveira-Wittmann, 2006): the latex of G. brasiliensis contains seven of the eight known forms of vitamin E, and its leaves contain the second highest recorded concentration of d-tochochromanol. Further research is needed to determine if these proteins and vitamins help to protect PSII from degradation or have other roles as anti-stress agents. A N A E RO B I C PAT H WAY S The only available data on anaerobic pathways is for M. acaciifolium (Fabaceae) and the palm A. jauari (Schluter, 1989) as adult trees in the eld or as seedlings grown in controlled conditions. Oxygen consumption of the root tissue in air was reduced after periods of submergence, but even after .300 d underwater, aerobic respiration resumed after a short period of re-adjustment (Schluter, 1989; Schluter and Furch, 1992; Schluter et al., 1993). Thus it can be assumed that a functional respirational capability is continuously maintained for long periods of submergence in these trees. Schluter also measured increasing levels of malate as submergence proceeded and a strong increase in ethanol in roots of M. acaciifolium after 200 d underwater. This is a common phenomenon upon submergence (Turner, 1960). Like ethanol, lactate is produced by a short pathway following glycolysis. However, in contrast to ethanol, Schluter (1989) found constantly low concentrations of lactate (,0.5 mM g21 f. wt) in roots of submerged A. jauari. A decrease of respiration after 50 d of inundation measured by Schluter indicates that the anaerobic pathway of energy gain is only a provisional solution. Alanine is a third compound that can be formed by a short pathway leading from glycolysis and one that my help reduce potentially damaging cytoplasmic acidosis by consuming reducing power. However, alanine in the roots of A. jauari showed no apparent relationship to hypoxic or anoxic conditions, its concentration varying between 1.0 and 3.0 mM g21 f. wt regard less of aeration status (Schluter, 1989). However, alanine concentrations of M. acaciifolium rose 10-fold after 200 d of submergence before decreasing (Schluter, 1989). U N D E R WAT E R P H OTO S Y N T H E S I S At the whole-plant level, complete submergence leads to a dramatic shift in the carbon budget and energy status, potentially resulting in death (Bailey-Serres and Voesenek, 2008). Some relief of this problem, with the leaves still submerged, can
content decreases during submergence (Parolin, 1997). In S. paniculata, chlorophyll concentrations were higher in submerged than in aerial leaves, but changes in chlorophyll content were associated with leaf age rather than with depth and length of submergence (Parolin, 1997; Waldhoff et al., 1998, 2002; Fernandez et al., 1999; Rengifo et al., 2005). On the other hand, when T. juruana and P. glomerata were submerged in complete darkness for 5 months, chlorophyll concentrations were unchanged (Krack, 2000). The leaves of A. jauari showed diminishing chlorophyll upon submergence, but after 150 d under water a slight increase was measured (Schluter, 1989).
Proteins and antioxidant compounds. High concentrations of soluble proteins indicate high metabolic rates. In her eld study on A. jauari, Schluter (1989) found lower concentrations of soluble proteins [250500 mg g21 fresh weight (f. wt)] in the roots during submergence compared with those of nonsubmerged roots (up to 1200 mg g21 f. wt). Differences are even more dramatic in the leaves of the plants (drained, up to 3600 mg g21 f. wt; submerged: 500700 mg g21 f. wt). In Macrolobium acaciifolium, Schluter (1989) measured unchanging concentrations of soluble proteins in leaves and roots from up to 60 d of submergence. Thereafter, concentrations decreased, but increased again before the end of the submerged period, which indicates a stimulation of this aspect of anabolic metabolism. Krack (2000) analysed the accumulation and degradation of proteins as reactions to submergence in darkness and found that many species show changes in protein patterns. Proteins with different molecular weights degraded partly or completely while others were newly synthesized. After submergence for .5 months there was a tendency for protein synthesis to exceed degradation. This might be interpreted as a positive stress reaction to submergence and light depletion. After 6 months underwater T. juruana leaf protein degradation prevailed, e.g. that of heat shock protein 70. In
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Parolin Prolonged ooding of woody species in Amazonian oodplains found between the potential quantum yield of leaves above or below the water line (Waldhoff et al., 2000a). Completely submerged seedlings of N. amazonum in the laboratory survived submergence in complete darkness for at least 4 months, grew a little in height (approx. 3%) and lost about 80% of the leaves. The lowest values of Fv/Fm measured on leaves under water (around 0.1) are far below the so-called irreversible damage value (IDV) of 0.23 mentioned earlier ` (Bolhar-Nordenkampf and Goetzl, 1992). However, in these species, the damage is not irreversible. When deeply submerged leaves were raised to within 1 m of the water surface and thus moved from darkness into light, Fv/Fm values quickly recovered to 0.7 0.8. Such values are generally considered to indicate a healthy state of a leaf. Waldhoff et al. (2002) concluded that the photosynthetic apparatus remains mostly intact during 4 months submersion in these species. Similar ndings were reported by Fernandez et al. (1999) for S. paniculata, Acosmium nitens and E. tenuifolia, which occur both in Amazonia and in the oodplains of the Venezuelan Mapire River. In this work, de-submerged leaves that had been under water for a little over 4 months displayed photosynthetic rates and leaf conductances similar to those of leaves that were never submerged, indicating the maintenance of photosynthetic capacity under water.
The key role of starch
be underwater photosynthesis (Mommer and Visser, 2005). Improved survival of submergence in the light is sometimes positively correlated with a higher carbohydrate status and internal oxygen concentrations that underwater photosynthesis can bring about (reviewed by Bailey-Serres and Voesenek, 2008). However, the whole aspect of underwater photosynthesis is poorly understood. A few data are available for a small number of Amazonian tree species, and most of this published material is hypothetical or speculative. Fernandes-Correa and Furch (1992) postulated a gas exchange mechanism through the stomata under water, and proposed two provisional names for this process, reverse plastron respiration and plastron photosynthesis, based on the concept of plastron breathing developed by animal physiologists (plastron ; respiratory bubble). In support of this idea, open stomata have been observed in submerged M. acaciifolium and A. jauari, suggesting the possibility of gas exchange at the interface between the water and air (Schluter, 1989). Inux of CO2 could be promoted by the high partial pressure of dissolved CO2 that is usually encountered in the Amazonian oodwater. Schluter (1989) calculated that there would be an inux of up to several hundred mL cm22 h21 CO2. Calculations based on leaf structure and the density of the stomata suggest that an inux of about 200 mL CO2 m22 h21 would be possible for S. paniculata and Tabernaemontana muricata, thereby acieving a small but possibly signicant rate of underwater photosynthetic xation of externally sourced CO2. A pre-requisite for this would be a sufcient light intensity. According to Furch et al. (1985), this pre-requisite is met at depths of down to 3 m in the varzea. The quantum density recorded with an underwater sensor was 10 mmol m22 s21 at a depth of 3 m. Such underwater CO2 assimilation would be in addition to photosynthetic xation of internally generated respiratory CO2 that can generate metabolically signicant amounts of O2, as shown for rice by Boamfa et al. (2003). Schluter et al. (1993) postulate that there is xation of external CO2. It is also possible that respiratory CO2 from roots may nd its way to leaves via aerenchyma and be assimilated by photosynthesis (Jackson, 2006). Another observation by Fernandes-Correa and Furch (1992) also led to the conclusion that underwater photosynthesis would be possible in some Amazonian oodplain tree species. Fernandes-Correa and Furch submerged branches of T. muricata in 200 mm of water for about 5 months before transferring them to the laboratory in plastic bags lled with river water. After removing the water, CO2 assimilation was assessed by infrared gas analysis. Photosynthetic activity was detected, indicating that the photosynthetic apparatus remained intact and functional. Direct measurements of underwater photosynthesis and respiration are lacking, however, both for trees of Amazonian oodplains and for other wetland species (Mommer and Visser, 2005). Data on underwater chlorophyll uorescence (Waldhoff et al., 2002) give further indications of the resilience of the photosynthetic apparatus to long-term submergence. These authors used a diving pulse amplitude modulation (PAM) chlorophyll uorometer in the eld at depths up to 8 m below the water surface and during laboratory-based submergence. The results indicate a surprising absence of damage. In individual plants in the eld (e.g. A. jauari, P. glomerata and S. paniculata), no difference was
Starch is limiting for survival in submerged plants. The ability to store carbohydrates in underground organs before the wet season is one of the strategies favouring survival during ooding (Crawford, 1992; Scarano et al., 1994) since anaerobic metabolism is costly in terms of carbohydrate consumption as compared with normal aerobic respiration. In Amazonian oodplain trees, carbohydrates are transferred into the roots in the dry season and utilized during ooding (Worbes, 1997). Sucrose is the main sugar reserve in the roots of H. sucuuba (Ferreira, 2006). In different populations of this species near Manaus, signicantly higher amounts were measured in the roots of oodplain populations (167.3 mg g21 dry matter) as compared with upland populations (101.3 mg g21 dry matter; Ferreira et al., 2008). The high reserves accumulated in the roots during the non-ooded period underpin respiratory metabolism in the subsequent waterlogged and submerged period (Ferreira et al., 2008). A considerable concentration of soluble carbohydrates in the roots at the end of the inundation period was found in A. jauari and M. acaciifolium, even after 312 d of waterlog ging and submergence (Schluter, 1989). This points to a slowing of metabolic rate during submergence. The content of non-soluble carbohydrates does not seem to be the limiting factor for survival. Reserves remaining at the end of submergence are used for fast regeneration of leaves and roots and upon de-submergence and the re-entry of aerial O2 (Schluter, 1989). The species with the highest reported concentrations of total soluble sugars and starch are V. cymosa, Crataeva benthamii and P. munguba; species with lower contents of carbohydrates are Crescentia amazonica, S. martiana and Cecropia latiloba (Koshikene, 2005). Species of later successional stages have higher concentrations of carbohydrates than early successional species (Koshikene, 2005). Late
Parolin Prolonged ooding of woody species in Amazonian oodplains successional T. barbata has more sugars in the stem bark during the aquatic phase than earlier successional C. benthamii; T. barbata can apparently take advantage of a greater sugar supply already stored (Parolin et al., 2008b). Anatomical comparisons of submerged and non-submerged leaves at the cellular level showed changes in two species which apparently are related to inundation. Chloroplasts in leaves of L. corymbulosa submerged for 5 months contained almost no starch in their leaves. However, 3 d after de-submergence, the starch content started to increase and, by 8 d, concentrations had grown by 50%. Starch appears to be used as an energy source for physiological processes during submergence. In leaves of P. glomerata a few days after the end of inundation chloroplast numbers were seen to increase with a presumed benet to light harvesting and photosynthetic activity (Waldhoff et al., 2002). In rice, the amount of stored carbohydrates in plant organs is positively correlated with the level of submergence tolerance (Jackson and Ram, 2003). Scarano et al. (1994) also showed that trees from low areas in the ooding gradient had roots with increased starch and reduced glucose compared with those from high areas in the ooding gradient. In S. paniculata, A. nitens and E. tenuifolia submerged leaves do not represent a sink for carbohydrates synthesized by aerial leaves. Instead they are able to sustain themselves and even contribute to the carbon budget of the plant (Fernandez et al., 1999). However, the study of Horna (2002) indicates high carbon loss in seasonally ooded varzea forests due to maintenance respiration. The contribution of growth respiration is relatively small. A close relationship exists between apparent CO2 release in branches and tree leaf phenology. A quantitatively important source of additional CO2 release in lower stem sections of varzea trees during early ooding most probably caused by ascending transport of dissolved CO2 with the xylem sap was found and described for the rst time by Horna (2002).
The key role of light
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leaves. If this is the case, photoinhibition might explain the observation. A longer and deeper submergence caused photoinhibition in S. paniculata (Waldhoff et al., 2002) and in Pouteria orinocensis (Fernandez, 2006).
RECOV E RY UPON DE- S UB MERG EN CE For a whole plant to be considered anoxia tolerant it is not necessary that every organ or tissue must survive oxygen deprivation (Schluter and Crawford, 2001). Ecologically, all that is required is the survival of those organs that are essential for subsequent regeneration on return to air. In Amazonian oodplains, the whole plant normally survives long periods of submergence even if the leaves have died. At the end of the ooding, roots recommence growth and new leaf development starts. In deciduous species, new crowns are fully developed within 1 month of de-submergence (Fig. 3C). A marked ability to compensate for the period of dormancy imposed by submergence is shown by fast growth in height of seedlings after ooding. In an experiment under semi-natural conditions, formerly submerged Crataeva benthamii and Cecropia latiloba seedlings recovered to the height of non-submerged wellwatered control plants 5 12 weeks after the end of submergence (Fig. 5; Parolin, 2001a). Most importantly for fast recovery and maximum exploitation of the shorter periods underwater, submerged seedlings maintain their photosynthetic apparatus at least to the extent that seedlings can
22 21 Mean height (cm) 20 19 18 17 30 25 Mean height (cm) 20 15 10 5 0 5 10 15 Time (weeks)
F I G . 5. Seedling growth under semi-natural conditions: seedlings reached the height of the control plants 5 12 weeks after the end of submergence (from Parolin, 2001a).
Flood end
Crataeva benthamii
Control Waterlogged Submerged Flood end
Even under water, light plays a key role. Schluter (1989) concluded that the limiting factor for photosynthesis under complete submergence in Amazonian oodplains is light rather than CO2. She therefore proposed that most species which fail to shed their leaves under water are well adapted to extreme low light. On the other hand, submergence does not lead to shade-like adaptation since quantum yield can be similar in aerial and submerged leaves. For seedlings submerged in darkness, the potential quantum yield (Fv/Fm) ` dropped below the IDV (Bolhar-Nordenkampf and Goetzl, 1992; Waldhoff et al., 2000a), but recovered again in the same leaves within 2 4 weeks. For plants that were submerged in light, Fv/Fm remained well above the IDV at approx. 0.66. ` According to Bolhar-Nordenkampf and Goetzl (1992) and Waldhoff et al. (2000a), the lower limit of natural variation in Fv/Fm for healthy leaves is approx. 0.55. This might suggest that submerged seedlings are not negatively affected by ooding, but by oxidative damage from re-exposure to light ( photoinhibition). The lack of light accompanying longterm submergence might increase the vulnerability of the light-harvesting complex to excess light energy in submerged
Cecropia latiloba
20
25
30
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Parolin Prolonged ooding of woody species in Amazonian oodplains ecosystems (Wilson and Keddy, 1985). The clear species zonation shows that most Amazonian oodplain species do not possess high ecological amplitudes and thus exhibit low tolerance of different ecological constraints and are therefore not widely distributed. An exception is Ceiba pentandra which grows both in Amazonian oodplains and in uplands of the neotropics and in Africa (Dick et al., 2007), but most species have a relatively small ecological amplitude (Wittmann et al., 2006). Species such as S. paniculata or E. tenuifolia that tolerate submergence and prolonged waterlogging establish on lower sites which may be ooded up to 210 d per year. Less tolerant species (e.g. Mora paraensis and Pentaclethra macroloba) are restricted to the upper parts close to the terra rme, which are ooded for shorter periods (Junk, 1989). On lower levels, escape from submergence is impossible and the strategy of tolerance to prolonged submersion is more efcient. Seedlings on these sites are shorter than species from the higher levels, leading to the assumption that the typical zonation found in Amazonian oodplains is more closely linked to the submersion tolerance of the seedlings than of adult trees (Parolin, 2002a). F I NA L RE M A R K S The reactions and adaptations to submergence described herein give only a supercial picture of the reactions and adaptations among the .1000 highly waterlogging- and submergencetolerant tree species of Amazonian oodplains. Very few of these species have been analysed so far. Furthermore, only a few features of any one species have been investigated. There is obviously still much to learn. There is a pressing need to study more species since this is likely to reveal novel adaptations. All the species cited in this review belong to highly ooded low varzea or low igapo tree communities. The lack of ecophysiological studies is especially marked for low varzea tree species or in tree species that occur at the transitional zone oodplains/uplands. These transitional areas contain .70% of the 900 tree species recorded in varzea oodplains (Wittmann et al., 2006). More generally, submergence tolerance has been analysed mostly in species inhabiting temperate grassland oodplains. The ndings from such work promote an understanding of whole ecosystems which in turn assists in their management and conservation. For example, Voesenek et al. (2004) proposes (a) life cycle timing, (b) avoidance and (c) tolerance as the three main solutions that different species appear to adopt for survival of submergence in the Rhine oodplain of The Netherlands. Perhaps in the Amazonian oodplains we too will come to similar conclusions, but the mechanisms and adaptations which underpin these strategies are, as yet, not understood. The survival strategy of life cycle timing (Voesenek et al., 2004) holds true only in part in Amazonian oodplains. Trees on the lowest levels in the ooding gradient the subject of this review have adapted their life cycle timing to the conditions in situ, i.e. their reproductive phenology is linked to high water (Goulding, 1983; Kubitzki and Ziburski, 1994) and growth is linked to ooding periodicity and restricted to the dry season. However, due to the very long ooded period and the tropical warm conditions all year round, underwater dormancy does not appear to be the
re-start to photosynthesize shortly after re-emergence (Parolin, 1997; Waldhoff et al., 2000a). Five minutes after de-submergence, seedlings of N. amazonum achieve rates of CO2 assimilation of up to 80% of non-submerged controls (Parolin, 2001a). In summary, in most species which maintain their leaves below water (e.g. N. amazonum, T. juruana and G. augusta) the photochemical capacity after months of submergence in darkness recovers within 10 d to values in the range of healthy and well-functioning leaves (Waldhoff et al., 2002). A hypothesis to explain this capacity is that the energy needed for the recovery of leaves submerged in the dark is so low that for the seedlings it is more advantageous to keep the leaves rather than to shed them all. The main challenge to survival by the leaves after submergence is lightinduced photoinhibition of photosynthesis. Comparisons of development of leaves submerged in light and darkness reveals that those in light apparently suffer no impairment of the photosynthetic apparatus, based on Fv/Fm analyses. Recovery in Amazonian oodplain species takes about 30 min, which is presumably the time it takes for a rearrangement of PSII reaction centres. Recovery by less well-adapted species takes 6 8 h and probably corresponds to the time needed to repair PSII reaction centres. Total recovery of the leaves of N. amazonum, T. juruana and G. augusta after submergence may take 3 weeks (Waldhoff et al., 2002). However, recovery from values close to 0 has not been reported. P L A S T I C I T Y, IN T R A S P E C I F I C DI F F E R E N C E S AN D E COTYPE S Plants have evolved a number of mechanisms thought to reduce the negative effects of submergence. These include both metabolic and morphological plasticity (Armstrong et al., 1994). Very little is known about the developmental plasticity and genetic variation in the trees inhabiting Amazonian oodplains. One of the few examples is a study by Ferreira (2002) on H. sucuuba. This species grows both in oodplains and in uplands, and shows a clear ecophysiological and genetic differentiation along the ooding gradient. Seed viability, germination rates and overall survival of submerged seedlings originating from populations of oodplain and upland environments differ signicantly (Ferreira, 2002, 2006; Ferreira et al., 2007, 2008). Submerged seedlings originating from uplands were seen to die after about 100 d, whereas 70% those originating from the oodplain populations survived. Morphological and physiological differences were also found, e.g. in the amount and pattern of aerenchyma formation (Ferreira, 2002). The differences in ooding tolerance within this species strongly indicate ecotypic differentiation between the two habitat types, which may be enforced by a strong selective pressure due to the regular ood pulse. Genetic analyses have conrmed that the populations are closely related, although it is not clear to what extent gene ow exists between them. Thus, H. sucuuba is an example of a species seemingly en route to separate into different species with differing waterlogging and submergence tolerance along the ooding gradient. A similar pattern can be seen in the distinct distribution limits of plant species along the vertical elevation gradient of river oodplains in other
Parolin Prolonged ooding of woody species in Amazonian oodplains strategy adopted to survive long-term submergence, although it can be successful in tropical rice (Jackson and Ram, 2003), but only when submergence is relatively short. The second strategy, that of avoidance, is not an option on the lowlying sites in Amazonian oodplains. Here, trees are unable to avoid and escape waterlogging or submergence by fast elongation of their shoots due to the immense ooding depth. Submergence-induced shoot elongation, a typical feature of the escape strategy, cannot accommodate low-lying sites with a water column of 10 m. Consequently, the third strategy, that of tolerance, must be pre-eminent in enabling trees to survive and grow vigorously under the given circumstances. This strategy encompasses a whole range of physiological and structural adaptations, e.g. tight regulation of ATP production and consumption, or the amelioration of reactive oxygen species, but we do not know the extent to which they actually apply to Amazonian oodplain forest species. There is no comparable ecosystem elsewhere on Earth: plants from other terrestrial ecosystems do not show this remarkable degree of tolerance to submergence. As research into Amazonian oodplain forest species expands, we will surely nd many new adaptations at the physiological, biochemical and molecular levels. CON C L U S IO NS Present knowledge of the mechanisms and adaptations of the trees of Amazonian oodplain forests which allow them to survive the extreme conditions of waterlogging and especially of complete submergence in darkness is still fragmentary. The present review describes some adaptive reactions of trees and their seedlings in the eld and in more controlled experimental conditions, but few answers can yet be given to questions of how these reactions are brought about. Little is known concerning the organs such as roots or leaves that are formed under water, although from what we know from temperate species the morphology and anatomy of these may be signicantly different from those developed in air (Mommer et al., 2006, 2007). A major challenge is to explain how the plants maintain seemingly healthy leaves below water for weeks or months and retain a functional photosynthetic apparatus. Nothing is presently known about hormonal regulation of development during and after submergence and its role in adaptive responses. Similarly very little is known about the role of antioxidants in submerged and de-submerged tissues (Voesenek et al., 2004; Oliveira-Wittmann, 2006), although recent work with rice may point a way forward (Santosa et al., 2007). Tolerance-conferring mechanisms known for temperate trees have not been much studied in Amazonian tree species, but in view of the high diversity of species we may expect many different kinds of adaptations and perhaps some that are new to science. Joly and Crawford (1982) supposed that ooding tolerance mechanisms in tropical trees are much more complex than those described for temperate species. The physiological, anatomical and phenological adaptations known for temperate species are all found in Amazonian oodplain trees as well, but they are not sufcient to explain plant survival of submergence under tropical temperatures for many months when light is excluded and prolonged oxygen shortage
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is an inevitability. Thus, novel adaptations remain to be discovered. This understanding may gain increasing importance in the light of climatic changes which already affect Amazonian oodplain forests, where changing ooding regimes and more and longer oods and droughts are being experienced (Junk et al., 2008). With increasing logging and ecosystem destruction, the need for reforestation and forest management becomes more pressing. This is a major challenge for the future. To measure up to this challenge, we will need to improve very signicantly our knowledge of seedling ecology, basic physiology and adaptive strategies of the trees in this highly productive and uniquely diverse ecosystem. ACK NOW L E D G ME NT S I thank Danielle Waldhoff and Florian Wittmann for discussions on the draft of this paper, and Michael B. Jackson for very helpful comments and corrections of the manuscript. I also thank Eric Visser for the analysis of old SEM pictures for the morphoanatomical description of root aerenchyma. This article is dedicated to Professor Dr Joachim Adis. L I T E R AT U R E CI T E D
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Annals of Botany 103: 359 376, 2009 doi:10.1093/aob/mcn216, available online at www.aob.oxfordjournals.

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