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REVIEW

Submerged in darkness: adaptations to prolonged submergenceby woody species of the Amazonian floodplains

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

BackgroundIn Amazonian floodplain forests, .1000 tree species grow in an environment subject to extendedannual submergence which can last up to 9 months each year. Water depth can reach 10 m, fully submergingyoung and also adult trees, most of which reproduce during the flood season. Complete submergence occurs reg-ularly at the seedling or sapling stage for many species that colonize low-lying positions in the flooding gradient.Here hypoxic conditions prevail close to the water surface in moving water, while anaerobic conditions arecommon in stagnant pools. Light intensities in the floodwater are very low.Questions and Aims Despite a lack of both oxygen and light imposed by submergence for several months, mostleafed seedlings survive. Furthermore, underwater growth has also been observed in several species in the fieldand under experimental conditions. The present article assesses how these remarkable plants react to submerg-ence and discusses physiological mechanisms and anatomical adaptations that may explain their success.

Key words: Adaptation, Amazonian floodplains, darkness, environmental stress, flooding, hypoxia,submergence tolerance, trees, underwater photosynthesis, woody species.

I N TR O D U C TI O N

An excess of water is generally considered to be deleterious toplant health and growth (Schueler and Holland, 2000), andtotal submergence quickly kills most species. Not so inAmazonian floodplain forests where the seasonal regularityof the so-called flood-pulse (Junk et al., 1989) of theAmazon river has given rise to plants that survive regularlyrecurring long-term (weeks or months) total submergence.

More than 1000 tree species successfully survive and completetheir life cycles in this region (Wittmann et al., 2006).Submergence of terrestrial woody species is the main topicof the present review. The aim is to bring together much ofthe existing descriptive and experimental information on howtree species from Central Amazonian floodplains react to com-plete submergence. Numerous woody species thrive in thefloodplains. Many grow to large trees, often with commercialvalue, and show extreme submergence tolerance not seen inany other ecosystem. They are able to overcome severalweeks or months of complete submergence as foliated plantsdespite the stresses (see below) imposed by total inundationthat can last several weeks or months each year. The mechan-isms allowing these species to be so tolerant of submergenceremain largely obscure. The current state of our understandingis discussed in this review.

Trees have evolved to survive in a terrestrial environment.Flooding imposes various stresses on these life forms thatinclude oxygen deprivation of both roots and shoots, drasticchanges in the availability of carbon dioxide, mineral nutrientsand in the concentrations of phytotoxins, increased anaerobicdecomposition of organic matter, increased solubility of poten-tially toxic mineral substances such as ferrous ions, very lowsoil redox potentials, and light deprivation (Joly and

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 vul-nerable to submergence in warm conditions, which makestheir tolerance in tropical Amazonia all the more remarkablesince warm growing conditions last the whole year. This isin marked contrast to temperate zones where flooding fre-

quently occurs during winter when plants are in a quiescentstate while waterlogged or submerged. In the Amazonregion, submergence occurs when temperature and light con-ditions are optimal for plant growth and when many speciesmaintain their leaves below water for months.

The ecosystem of Amazonian floodplains

Amazonian floodplain 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, pre-dictable flood-pulse (Junket al., 1989). The following environ-mental characteristics pose constraints for plant growth.

Very long uninterrupted flooding. The areas where trees groware flooded for up to 210 d every year (Junk, 1989). Thepalm Astrocaryum jauari (Arecaceae) survives well eventhough it can be submerged for 300 d a year (Schluter et al.,1993). The annual flooding period can thus last longer thanthe dry terrestrial phase (which is the main growing period).

High flood amplitudes. In Central Amazonia, every year theriver levels rise and fall by up to 10 m, causing an annualflood-pulse (Junk et al., 1989, Fig. 2A and B). However,inter-annual variations occur (Fig. 2B) which can mean thatcertain trees can miss being waterlogged for one or two con-secutive years if the water is untypically low, as it was in* E-mail [email protected]

# The Author 2008. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved.

For Permissions, please email: [email protected]

Annals of Botany 103: 359376, 2009

doi:10.1093/aob/mcn216, available online at www.aob.oxfordjournals.org

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F IG . 1. Amazonian floodplain trees. (A) Forest with highly flood-tolerant tree species at high water; (B) varzea with high productivity as shown by macrophytegrowth; (C) exposed roots with receding water; (D) seedling establishment upon receding water in igapo ; (E) Crudia amazonica and (F) Vitex cymosa maintaintheir 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 pani-

culata maintains all leaves above and below water (pictures by Pia Parolin).

Parolin Prolonged flooding of woody species in Amazonian floodplains360
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1995 and 1997. In contrast, in some years, water levels areuntypically high and certain areas can remain waterloggedfor two or more consecutive years. This was the case in1993/94 (Fig. 2B).

Rapid changes of water levels. The water level in the Amazonrises at an average of 50 mm d21. However, sometimes forseveral weeks in the periods of maximum change in levels, arise or fall of up to 100 150 mm d21 has been recorded(Junk and Piedade, 1997) between April and June. This fastrate of change negatively affects the effectiveness of morpho-logical adaptations to flooding such as adventitious roots

which are produced in the oxygen-rich surface layers of thewater.

Hypoxia. As soon as water covers the soil, partial oxygendeficiency (hypoxia) arises in the rhizosphere (Kozlowski,1984). Oxygen-consuming decomposition and fast sedimen-tation rates further decrease oxygen supply to the roots andmay lead to a complete absence of oxygen (anoxia) in the rhi-zosphere. Concentrations of dissolved oxygen in the flood-water in the range 056.0 mg L21 have been recordeddepending on the season and time of day (Furch and Junk,1997). There appear to be only modest inputs of oxygen into

the floodplain water from photosynthesis or stirred into thewater body by wind and currents. Oxygen concentrations atdepths below 300 mm are typically about 1 mg L21 due todepletions by decomposition of dead biomass. Clearly, verylittle oxygen is available from the floodwater itself tosupport plant respiration. Extremely low oxygen concen-trations were recorded by Furch and Junk (1997) at LagoCamaleao, where anoxia and the presence of H2S wereobserved periodically at a depth of 12 m. In extreme cases,up to 1 mg L21 of H2S have been measured at depths of0.5 m between June and September, the months when water

levels are highest.

High sedimentation. The sediment-rich white water floodplainsof the Amazon River and its tributaries called varzea(Prance, 1979) are subjected to high rates of sediment depo-sition which can amount to 3001000 mm each year (Junk,1989, Campbell et al., 1992). A concentration of about100 mg L2

1of suspended mineral solids has been reported

near Manaus. In deep water, 0.5 m from the bottom, suspendedsolids may reach 822 mg L21 (Furch and Junk, 1997). Thesefine coarse sediments increase the severity of hypoxia andprejudice leaf photosynthesis below water by imposing

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F IG . 2. Water level (height above sea level) of the Amazon River near Manaus showing the regular flood-pulse (Junket al., 1989): means of (A)12 months and

(B) monthly height between 1987 and 1999 showing interannual variations.

Parolin Prolonged flooding of woody species in Amazonian floodplains 361
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turbidity and depositing sediment on the leaf surfaces thatremains after the floodwater recedes (Ewing, 1996).

Water temperature. With average temperatures of 27 298C(Furch and Junk, 1997), the warm floodwater supports fastrates of oxygen-depleting respiration by plants and micro-organisms while itself carrying less dissolved oxygen than

would cooler water. For example, water at 108C contains11.26 g m23 when in full equilibrium with air but only7.36 g m23 at 308C, at 1 atmosphere pressure (1.013 10

5

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 quantumflux of 2 mmol m22 s21. In the turbid water of the varzea, nolight could be measured below 3 m (Furch et al., 1985), whileWaldhoff et al. (2002) measured a quantum flux of 1 10 mmolm22 s21 (PAR) at 17 m. In the varzea, 99% extinction occursbelow 1 5 m. In contrast, light intensities reach values of3000 mmol m2

2 s21 at noon above water level (Furch et al.,

1985). Different light penetration patterns among the differentwater types (white, black and clear) appear to influence plantestablishment on the forest borders in varzea and igapo (F.Wittmann, Max-Planck-Institute for Chemistry, Mainz,Germany, pers. comm.), but no quantitative data are currentlyavailable.

Mechanical strain. The dynamics, current and erosion power ofthe river system may mechanically damage trees and deterseedling establishment (Fig. 1C, D). However, mechanicalstrain of this kind may only be significant along the banks ofthe main river channels, which cover only a small part of theextensive floodplains. Its impact can probably be neglectedin the backwaters.

Drought. In the dry months of the terrestrial phase, when riverlevels and precipitation are low (between September andNovember; Fig. 2A), severe shortage of water may limitplant growth.

Despite the challenging conditions for plant growth in theAmazonian floodplains, the number of extant angiospermtree species is very high. With 50180 species ha21 withdiameter at breast height !10 cm (Pires and Koury, 1959;Balslev et al., 1987; Ayres, 1993; Worbes, 1997; Wittmannet al., 2002), species richness is greater than for others ofthe Earths forests. At least 918 flood-tolerant tree specieshave been identified in the nutrient-rich white water varzea(Wittmann et al., 2006) and many more in the nutrient-poorblack water floodplain forests of Amazonia. This makes

Amazonian floodplain forests the most species-rich floodplainforests, with many endemic species. In a recent review,Wittmann et al. (2008) classified 40% of 186 commoncentral Amazonian varzea tree species as endemics to theAmazonian varzea.

R EA C TI O N S A N D A D A P TA TI O N S TOC O M P L E TE S U B M E R G E N C E

Several studies over the last 10 years have described a largevariety of specific reactions to complete submergence oftrees and seedlings in Amazonian floodplains (e.g. Worbes,

1985; Meyer, 1991; Schluter and Furch, 1992; Schluteret 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; Parolinet 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; Hornaet al., 2008). Most of these studies were performed in thevicinity of Manaus. Unfortunately, in many of these reportsfew qualitative descriptions can be found on any onespecies, and no study focuses specifically on reactions to sub-mergence or analyses how the trees tolerate it over prolongedperiods.

Complete submergence is a very different constraint fromwaterlogging of the soil and root system or even partial sub-mergence where much of the shoot remains above the waterline (Colmer and Pedersen, 2008). Totally submerged plantshave no direct contact with atmospheric oxygen, and sunlightis weak or extinguished. Although abscisic acid (ABA)

accumulation leading to leaf stomatal closure has beendescribed in the literature as an almost immediate responseof plants to soil waterlogging (Voesenek et al., 2004), this isunlikely to occur in submerged Amazonian floodplain foresttrees, since in rice and Rumex palustris at least, ABA levelsdecrease 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 submergedplants as opposed to waterlogged plants seems a common yetpoorly understood feature (Schluter, 1989; Parolin et al., 2004)where different adaptations for growth and survival arerequired since they cannot escape by elongating to abovethe (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 theaerial atmosphere. In contrast, the term waterlogged is usedwhere at least a part of the plant (the stem and crown oreven only single branches or leaves) protrude above thewater surface. When the term flooding is used, as frequentlyfound in the literature, this is used to imply either waterloggedor submerged conditions.

Vegetative phenology under water

In Amazonian floodplains, different tree species exhibitdifferent leaf phenologies upon submergence (Table 1). Mostspecies shed their submerged leaves, but some maintain

them for months or even years despite prolonged submerg-ence, and without apparent damage (Fig. 1E, F, H andFig. 3; Waldhoff and Furch, 2002). Leaf life span variesbetween the species, ranging from a few months in Senna reti-culata to up to 5 years in Nectandra amazonum or even longerin Symmeria paniculata (Fig. 1H). Submerged seedlings ofseveral species sprout new leaf buds under water (Table 1;Fig. 3G) and expand the leaves as soon as the plantsemerge, or even before emergence (Parolin, 2001a).Unfortunately, there are no published studies of the character-istics of leaves that emerge under water. However, severalstudies analyse the responses of aerially produced leaves to

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TA B L E 1. Leaf phenology upon waterlogging and submergence in Amazonian floodplain trees

Species studied

No leafshedding uponwaterlogging

Shedding of allleaves upon

waterlogging

Shedding ofbelow-water leavesupon waterlogging

No leaf sheddingupon tree

submergence

Shedding of allleaves upon tree

submergence

New leabove

wa

Acosmium nitens (Vogel)

Yakovlev

? ?

Albizia multiflora 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 exBenth.

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 exBenth.

? ?

Licania apetala (E. Mey.) Fritsch Macrolobium acaciifolium(Benth.) Benth.

Nectandra amazonum Nees Pouteria elegans (DC.) Baehni Pouteria glomerata (Pohl exMiq.) 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 EXJ. F. MACBRIDE

Vitex cymosa Bert. ex Spreng.

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A

D

IH

E F

B C

G

F IG . 3. Submergence experiments (University of Kiel, Germany). (A) Nectandra amazonum maintains its leaves below water ( pictures under experimental con-ditions after submergence in darkness for 3 months). (B) Seedlings of Pterocarpus amazonum after 3 weeks of submergence in complete darkness and (C) 1month after emergence. (D) Psidium acutangulum submerged for 2 weeks in experimental conditions. (E) shoot increment in a submerged plant of Gustaviaaugusta and (F) Tabernaemontana juruana after 3 months in complete darkness. (G) after 4 d of complete submergence under experimental conditions, Salixmartiana 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).

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subsequent submergence (Schluter and Furch, 1992; Schluteret al., 1993; Waldhoff and Furch, 2002; Waldhoffet al., 2002).

Growth and biomass changes

The main period of biomass production is the terrestrial

non-flooded phase (Schluter, 1989; Worbes, 1997). With sub-mersion, growth in height stops after 1 3 weeks in mostspecies (Parolin, 2001a). However, some species show under-water shoot extension even in complete darkness. In an exper-iment in a greenhouse at the University of Kiel, shoots ofGustavia augusta were found to elongate by almost 400 mmunder such conditions (Fig. 3E), while Tabernaemontanajuruana elongated by about 30 mm (Fig. 3F). The portion ofthe stems that elongated below water had neither chlorophyllnor leaves. In the same greenhouse under experimental con-ditions, completely submerged Salix martiana producedadventitious roots on the stem (Fig. 3G; Waldhoff and Furch,2002; Waldhoff, 2003). Seedlings of N. amazonum developedlenticels after 13 d submergence (covering 10 20% of the

stem surface area); adventitious roots with negative geotropismemerged after 16 d of submergence, and more adventitiousroots appeared after 19 d (Fig. 3H). While waterloggedplants of these species induced very few adventitious roots(no more than 5% of the complete root mass), in completelysubmerged plants adventitious roots contributed up to 50%of the total root mass (Waldhoff et al., 2000b).

Dormancy, quiescence and periodic growth

Some non-woody species avoid flooding by completingtheir life cycle between two subsequent flood events, andflooding itself is survived by dormant life stages (e.g. seeds)(Bailey-Serres and Voesenek, 2008). In Amazonian floodplain

trees, dormant periods are found in the form of periodicalgrowth reductions as a consequence of flooding, which arereflected by the formation of increment rings and by periodicshoot elongation (Worbes, 1989, 1997; Worbes and Junk,1989). Entering a state of rest may help the trees minimizestress from flooding. However, this period of rest lasts for afew weeks only; trees then resprout and elongate their shootsin the remaining weeks or months of waterlogging or submerg-ence. No species is dormant for the whole flooded period.Waterlogged trees typically show high physiological activityduring most of the flooded period, while completely sub-merged trees show some growth at the beginning and end offlooding. This pattern is probably related to higher light inten-sities during early and late flooding 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 avoid-ance strategies that involve the development of certain anatom-ical and morphological traits, in particular fast underwaterelongation that returns shoot tips to the air if the water is nottoo deep. This amelioration response, called low oxygenescape syndrome (LOES; Bailey-Serres and Voesenek, 2008),facilitates the survival of submerged organs. However, LOESis costly and will only be selected for in environments wherethe cost is outweighed by benefits such as improved O2 andcarbohydrate status, both contributing to a higher fitness.

Since the benefits of LOES do not outweigh the costs whenflooding is too deep as in Amazonian floodplains a quies-cence strategy characterized by limited underwater growth andconservation of energy and carbohydrates is to be expected.

Waldhoff et al. (2002) observed that the photosyntheticsystem of submerged leaves becomes dormant. Evidence for

this adaptation in terms of very low photosystem II (PSII)chlorophyll fluorescence has been found in the field andunder more controlled experimental conditions forG. augusta, N. amazonum and T. juruana. After 5 months ofsubmergence in darkness, the relative potential quantumyield, Fv/Fm, decreased from 0.7 to 0.1 upon emergence, indi-cating a dormant photosynthetic apparatus. In temperateEuropean plants with which the method of chlorophyll fluor-escence measurement was originally developed, an Fv/Fmratio 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 analysedhere the leaves were merely quiescent since, upon de submerg-ence, the Fv/Fm ratio returned to normal values after 6 d, indi-

cating no irreversible damage.

Mortality

Considerable seedling mortality is brought about by flood-ing in the Amazonian floodplains. However, Ziburski (1990)found that most tree species fatalities are higher fromdrought than from flooding. However, few quantitative dataare available. Table 2 summarizes what is known. Extremelylow mortality was recorded in seedlings of the palmA. jauari, with only 10% mortality recorded after 300 d sub-mergence in the field at 288C (Schluter, 1989). In Himatanthus sucuuba, mortality ,30% was found in varzeapopulations in one flooded period. In contrast, in upland popu-

lations of the same species, 100% mortality has been reported(Ferreira, 2002).

Germination underwater

The seeds of many tree species remain visually sound whencontinuously submerged or floating for .2 months (Table 3;Parolin and Junk, 2002; Parolin et al., 2004). This is in markedcontrast to the majority of land plants, whose seeds quickly loseviability if submerged for prolonged periods (Hook, 1984).Seeds of Amazonian floodplain species which are kept in air,dry or decompose within a few days (e.g. Tabebuia barbata andN. amazonum) or weeks (e.g. Senna reticulata and Aldina latifo-lia; Parolin et al., 2008a). In species that reproduce during the

aquatic phase and regardless of whether the seeds float or sink,germination starts after the flood recedes (Parolin et al., 2004).However, many seeds can float for very long periods and germi-nate already while floating (Table 3). While some speciesproduce only a radicle, others form fully developed seedlings,emitting radicles, cotyledons and primary leaves from buoyantseeds, as observed in the field (Ziburski, 1990) and underexperimental conditions in Manaus (Oliveira, 1998;Oliveira-Wittmann et al., 2007). This behaviour may enhancefast seedling establishment, because plants are growing whilethe water is still receding. However, seedlings that develop inwater are often morphologically different from those that

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20 KV X236 100U 000 01094 BKI

20 KV X2480 10U 018 21596 BKI

20 KV X2280 10U 001 07896 BKI

20 KV X40 1000U 000 01995 BKI20 KV X73 1000U 008 41095 BKI

20 KV X2440 10U 019 21596 BKI

20 KV X692 100U 000 01995 BKI

20 KV X208 100U 000 01094 BKI

Emerged leaf Submerged leafA B

E F

G H

C D

F IG . 4. Anatomical characteristics: cross-section of (A) emerged and (B) submerged leaf ofTabernaemontana juruana; (C) Eugenia inundata cross-section withlarge epidermal cells; (D) Garcinia brasiliensis thick outer-epidermis walls; (E) stomata on the upper leaf side in Garcinia brasiliensis; (F) sunken stomata on thelower side of the leaf in Cassia leiandra, with wax crystals; (G) Psidium acutangulum cross-section of adventitious root with schizogenous aerenchyma and somelarger intercellular spaces of lysigenous origin; (H) Cecropia latiloba: cross section of young adventitious root with aerenchyma ( pictures by Danielle Waldhoff ).

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with respect to the ambient environment called photomorpho-genesis in light apparently are not optimized or changed withrespect to the long period of darkness under water (Fig. 4A, B).Since many leaves do not rot or detach from the plant during sub-mergence, some type of morpho-anatomical adjustment pre-sumably must exist to explain this, but research into this

aspect is needed. Only two morphological characteristics of sub-merged leaves a thick cuticle and thick outer epidermis walls are clearly different from non-submerged leaves (Waldhoffand Furch, 2002). In species that do not possess these character-istics, leaves rot quickly when submerged and are shed within afew days (Table 1). Damage to the mesophyll of submergedleaves by microbial decomposition processes has never beenobserved (Fernandes-Correa and Furch, 1992). The leaves thatsurvive submergence can be just as functional as those sproutinglater (Fernandes-Correa and Furch, 1992), while chlorophyllcontent may lie within the range of that of non-submergedleaves or can even become elevated (Furch, 1984). Submergedleaves usually appear darker than leaves that subsequentlysprout 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 beenfound to be infiltrated with water (Schluter, 1989; Waldhoffand Parolin, 2008), in contrast to the earlier proposal ofScholander and Perez (1968). Thick cuticles (Fig. 4C, D) andepicuticular waxes, and an associated gas-filled outer layer(Schluter, 1989) may well prevent influx of water into sub-merged leaves and also improve their capacity to withstandmechanical impact during inundation (Schluter et al., 1993).If submerged leaves normally became infiltrated, gas exchangeand mineral supply would be prevented (Fernandes-Correa andFurch, 1992). It is probable that the waxy leaf surfaces that areabundant in some species (Fig. 4F) favour the retention of agas layer over the leaf surface (Fernandes-Correa and Furch,

1992). These gas films enable the stomata to remain openwhen submerged (Colmer and Pedersen, 2008) and allow asmall amount of photosynthesis. This would be enhanced bythe high partial pressures of dissolved CO2 that often prevailin the water (K. Furch, Max-Planck-Institute for Limnology/Plon, Germany, pers. comm.) that create a diffusion gradientdriving CO2 into the stomatal cavities.

From the observations described, it can be concluded thatleaves not shed at the beginning of the inundation mostlyremain functional when submerged, at least to depths wheresome light is available (Furch, 1984; Schluter and Furch,1992).

Roots. Root activity is restricted by total submergence

(Worbes, 1997). Under natural conditions in the floodplains,adventitious roots, lenticels or stem hypertrophy wereseldom observed, probably due to the constant change inwater level (Parolin et al., 2004). The potential capacity ofAmazonian floodplain trees to form these adaptationsbecomes more evident in flooding experiments under morecontrolled conditions. Thus, although not frequently encoun-tered in the field, their function may be important in yearswith flooding anomalies.

As mentioned above, submerged N. amazonum can produceadventitious roots (Fig. 3H), and lengths up to 105 mm (com-pared with 370 mm in waterlogged individuals) have been

measured by Parolin (2001a). Oliveira-Wittmann (2006) sub-merged seedlings of Laetia corymbulosa in a greenhouse andobserved adventitious roots protruding directly from theveins of leaves which were still attached to the plant, andalso in detached leaves.

Many roots are characterized by the formation of suberized

and lignified barriers in the exodermis that can be expected toregulate radial transport of solutes and gases (De Simone et al.,2003b). In four species from Amazonian floodplains, DeSimone et al. (2003b) found that radial loss of oxygen waseffectively restricted by the formation of suberized barriersbut not by lignification of exodermal cell walls. Specieswhich form new roots below water also form suberized bar-riers (De Simone, 2003b). Suberin polymers also play a deter-mining role in pathogen defence, either by a breakdown ofpolymers by enzymes of microbial origin (e.g. in L. corymbulosa and S. martiana) and subsequent release oftoxic phenols, or by acting as a mechanical barrier (DeSimone et al., 2003b).

Aerenchyma. Aerenchyma facilitates gas transfer through theshoot to the root system by lowering the resistance thathampers gas diffusion and mass flow within organs (Couttsand Armstrong, 1976; Bailey-Serres and Voesenek, 2008).The presence of aerenchyma can provide a system of intercon-nected channels from leaf to root tip. However, analyses byWorbes (1986) of the xylem from approx. 100 dicotyledonoustree species did not reveal significant amounts of aerenchyma.Worbes (1997) states that even if aerenchyma were present, thelong length of tree roots (up to 30 m in adult trees) precludesthe possibility of gas exchange processes between stem androot tips by means of gas diffusion. An alternative mechanism,that of mass flow driving long-distance root aeration in treesvia aerenchyma, is controversial (Armstrong and Armstrong,

2005). Usually, trees of inundation forests cannot support theO2 demand for the respiration of their roots during theaquatic phase via lenticels in the stems and air conductingsystems or via pneumatophores. Exceptions include mangroveand Taxodium distichum (Worbes, 1997). Also Nunez-Eliseaet al. (1999) found that in some water lilies (Annonaspecies), waterlogging did not increase intercellular gasspaces in pre-existing xylem near the pith or in xylem tissueformed during flooding, and concluded that flood tolerancedid not involve a promotion of aerenchyma formation in thestem. Botelho et al. (1998) describe a similar situation in Inga vera and Virola surinamensis from eastern Amazonianfloodplains: anatomical cuttings of experimentally raised sap-lings did not show any aerenchyma formation or other struc-

tural adaptation to flooding.Despite the foregoing, some observations do point to mor-

phological and anatomical stress-avoiding systems. Forexample, aerenchyma tissues were found in the roots of2-year-old seedlings of the palm A. jauari (Schluter, 1989), aswould be expected since aerenchyma is commonly found inpalms (Scarano et al., 1994). Microelectrode investigations on2- to 3-month-old cuttings from S. martiana showed that theirwell-oxygenated aerenchymatous adventitious roots were ableto build up a several millimetres thick oxygenated layeraround the whole roots, suggesting a mechanism of detoxifyingreduced phytotoxins by radial oxygen loss (ROL; De Simone

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et al., 2002b; Haase et al., 2003). In older roots from adult treessubmerged by several metres of water, the formation of aerench-yma may be of little importance for longitudinal oxygen trans-port not only because of the long diffusion pathway that exceedsthe approx. 300 mm down which aeration by diffusion is effec-tive (Armstrong, 1979), but because the lacunae are destroyed

by secondary root thickening. Overall, gas transport via aerench-yma appears to play only a minor role at best in sustaining sub-merged Amazonian tree species.

Physiological reactions

Leaf water potential. In combination with other observations,leaf water potential provides a basis for judging the functionalcapability of the leaves. The water potentials of several broad-leaf, woody plants that frequently occur in inundation forestsfall within the range between 0.2 and 2.4 MPa(Fernandes-Correa and Furch, 1992). One-year-old leaveswhich had been submerged in several metres depth for somemonths always gave lower water potentials than newly

emerged, non-submerged leaves of the same species thatwere only a few weeks old (Fernandes-Correa and Furch,1992).

Leaf chlorophyll. In most species analysed, total chlorophyllcontent decreases during submergence (Parolin, 1997). InS. paniculata, chlorophyll concentrations were higher in sub-merged than in aerial leaves, but changes in chlorophyllcontent were associated with leaf age rather than with depthand 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 weresubmerged in complete darkness for 5 months, chlorophyllconcentrations 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 ofsoluble proteins indicate high metabolic rates. In her fieldstudy on A. jauari, Schluter (1989) found lower concentrationsof soluble proteins [250500 mg g21 fresh weight (f. wt)] in theroots during submergence compared with those of non-submerged roots (up to 1200 mg g21 f. wt). Differences areeven more dramatic in the leaves of the plants (drained, up to3600 mg g2

1 f. wt; submerged: 500 700 mg g21 f. wt). In

Macrolobium acaciifolium, Schluter (1989) measured unchan-ging concentrations of soluble proteins in leaves and rootsfrom up to 60 d of submergence. Thereafter, concentrations

decreased, but increased again before the end of the submergedperiod, which indicates a stimulation of this aspect of anabolicmetabolism. Krack (2000) analysed the accumulation anddegradation of proteins as reactions to submergence in darknessand found that many species show changes in protein patterns.Proteins with different molecular weights degraded partly orcompletely while others were newly synthesized. After sub-mergence for .5 months there was a tendency for protein syn-thesis to exceed degradation. This might be interpreted as apositive stress reaction to submergence and light depletion.After 6 months underwater T. juruana leaf protein degradationprevailed, e.g. that of heat shock protein 70. In

L. corymbulosa and P. glomerata, light-harvesting chlorophyll-binding proteins (LHCPs) a protective component of PSII become degraded, indicating that PSII must be protected byother proteins since photosynthetic capacity is retained.Rubisco as a component of the Calvin cycle also degradedonly partly in several species analysed under experimental sub-

mergence (pers. obs.).Antioxidant compounds and vitamins in plant leaves canminimize plant damage by alleviating oxidative challengeand organ damage under submersion. Fruits of Amazonianfloodplain trees contain some of the highest known concen-trations of vitamin C in plants (e.g. Myrciaria).Concentrations of another antioxidant, vitamin E, are alsohigh in the latex and the leaves of various Amazonianspecies (Oliveira-Wittmann, 2006): the latex ofG. brasiliensis contains seven of the eight known forms ofvitamin E, and its leaves contain the second highest recordedconcentration of d-tochochromanol. Further research isneeded to determine if these proteins and vitamins help toprotect PSII from degradation or have other roles as anti-stress

agents.

ANAEROBIC PATHWAYS

The only available data on anaerobic pathways is forM. acaciifolium (Fabaceae) and the palm A. jauari (Schluter,1989) as adult trees in the field or as seedlings grown in con-trolled conditions. Oxygen consumption of the root tissue inair was reduced after periods of submergence, but even after.300 d underwater, aerobic respiration resumed after a shortperiod of re-adjustment (Schluter, 1989; Schluter and Furch,1992; Schluter et al., 1993). Thus it can be assumed that a func-tional respirational capability is continuously maintained forlong periods of submergence in these trees. Schluter also

measured increasing levels of malate as submergence pro-ceeded and a strong increase in ethanol in roots of M. acaciifolium after 200 d underwater. This is a commonphenomenon upon submergence (Turner, 1960). Like ethanol,lactate is produced by a short pathway following glycolysis.However, in contrast to ethanol, Schluter (1989) found con-stantly low concentrations of lactate (,0.5 mM g2

1 f. wt) inroots of submerged A. jauari. A decrease of respiration after50 d of inundation measured by Schluter indicates that theanaerobic pathway of energy gain is only a provisional solution

Alanine is a third compound that can be formed by a shortpathway leading from glycolysis and one that my help reducepotentially damaging cytoplasmic acidosis by consuming redu-cing power. However, alanine in the roots of A. jauari showed

no apparent relationship to hypoxic or anoxic conditions, itsconcentration varying between 1.0 and 3.0 mM g21 f. wt regard-less of aeration status (Schluter, 1989). However, alanine con-centrations of M. acaciifolium rose 10-fold after 200 d ofsubmergence before decreasing (Schluter, 1989).

U N D ER WA TER P H O TO S Y N TH ES I S

At the whole-plant level, complete submergence leads to a dra-matic shift in the carbon budget and energy status, potentiallyresulting in death (Bailey-Serres and Voesenek, 2008). Somerelief of this problem, with the leaves still submerged, can

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be underwater photosynthesis (Mommer and Visser, 2005).Improved survival of submergence in the light is sometimespositively correlated with a higher carbohydrate status andinternal oxygen concentrations that underwater photosynthesiscan bring about (reviewed by Bailey-Serres and Voesenek,2008). However, the whole aspect of underwater photosyn-

thesis is poorly understood. A few data are available for asmall number of Amazonian tree species, and most of thispublished material is hypothetical or speculative.Fernandes-Correa and Furch (1992) postulated a gas exchangemechanism through the stomata under water, and proposed twoprovisional names for this process, reverse plastron respir-ation and plastron photosynthesis, based on the concept ofplastron breathing developed by animal physiologists (plas-tron ; respiratory bubble). In support of this idea, openstomata have been observed in submerged M. acaciifoliumand A. jauari, suggesting the possibility of gas exchange atthe interface between the water and air (Schluter, 1989).Influx of CO2 could be promoted by the high partial pressureof dissolved CO2 that is usually encountered in the

Amazonian floodwater. Schluter (1989) calculated that therewould be an influx of up to several hundred mL cm22 h21

CO2. Calculations based on leaf structure and the density ofthe stomata suggest that an influx of about 200 mL CO2 m

22

h21 would be possible for S. paniculata andTabernaemontana muricata, thereby acieving a small but poss-ibly significant rate of underwater photosynthetic fixation ofexternally sourced CO2. A pre-requisite for this would be asufficient light intensity. According to Furch et al. (1985),this pre-requisite is met at depths of down to 3 m in thevarzea. The quantum density recorded with an underwatersensor was 10 mmol m2

2 s21 at a depth of 3 m. Such under-water CO2 assimilation would be in addition to photosyntheticfixation of internally generated respiratory CO2 that can gener-

ate metabolically significant amounts of O2, as shown for riceby Boamfa et al. (2003). Schluter et al. (1993) postulate thatthere is fixation of external CO2. It is also possible that respir-atory CO2 from roots may find its way to leaves via aerench-yma and be assimilated by photosynthesis (Jackson, 2006).Another observation by Fernandes-Correa and Furch (1992)also led to the conclusion that underwater photosynthesiswould be possible in some Amazonian floodplain treespecies. Fernandes-Correa and Furch submerged branches ofT. muricata in 200 mm of water for about 5 months beforetransferring them to the laboratory in plastic bags filled withriver water. After removing the water, CO2 assimilation wasassessed by infrared gas analysis. Photosynthetic activity wasdetected, indicating that the photosynthetic apparatus remained

intact and functional. Direct measurements of underwaterphotosynthesis and respiration are lacking, however, both fortrees of Amazonian floodplains and for other wetland species(Mommer and Visser, 2005). Data on underwater chlorophyllfluorescence (Waldhoff et al., 2002) give further indicationsof the resilience of the photosynthetic apparatus to long-termsubmergence. These authors used a diving pulse amplitudemodulation (PAM) chlorophyll fluorometer in the field atdepths up to 8 m below the water surface and duringlaboratory-based submergence. The results indicate a surpris-ing absence of damage. In individual plants in the field (e.g.A. jauari, P. glomerata and S. paniculata), no difference was

found between the potential quantum yield of leaves aboveor below the water line (Waldhoff et al., 2000a). Completelysubmerged seedlings of N. amazonum in the laboratory sur-vived submergence in complete darkness for at least 4months, grew a little in height (approx. 3%) and lost about80% of the leaves. The lowest values of Fv/Fm measured on

leaves under water (around 0.1) are far below the so-calledirreversible damage value (IDV) of 0.23 mentioned earlier

(Bolhar-Nordenkampf and Goetzl, 1992). However, in thesespecies, the damage is not irreversible. When deeply sub-merged leaves were raised to within 1 m of the water surfaceand thus moved from darkness into light, Fv/Fm valuesquickly recovered to 0.7 0.8. Such values are generally con-sidered to indicate a healthy state of a leaf. Waldhoff et al.(2002) concluded that the photosynthetic apparatus remainsmostly intact during 4 months submersion in these species.Similar findings were reported by Fernandez et al. (1999) forS. paniculata, Acosmium nitens and E. tenuifolia, whichoccur both in Amazonia and in the floodplains of theVenezuelan Mapire River. In this work, de-submerged leaves

that had been under water for a little over 4 months displayedphotosynthetic rates and leaf conductances similar to those ofleaves that were never submerged, indicating the maintenanceof photosynthetic capacity under water.

The key role of starch

Starch is limiting for survival in submerged plants. Theability to store carbohydrates in underground organs beforethe wet season is one of the strategies favouring survivalduring flooding (Crawford, 1992; Scarano et al., 1994) sinceanaerobic metabolism is costly in terms of carbohydrate con-sumption as compared with normal aerobic respiration. InAmazonian floodplain trees, carbohydrates are transferred

into the roots in the dry season and utilized during flooding(Worbes, 1997). Sucrose is the main sugar reserve in theroots of H. sucuuba (Ferreira, 2006). In different populationsof this species near Manaus, significantly higher amountswere measured in the roots of floodplain populations(167.3 mg g21 dry matter) as compared with upland popu-lations (101.3 mg g21 dry matter; Ferreira et al., 2008). Thehigh reserves accumulated in the roots during the non-floodedperiod underpin respiratory metabolism in the subsequentwaterlogged and submerged period (Ferreira et al., 2008). Aconsiderable concentration of soluble carbohydrates in theroots at the end of the inundation period was found inA. 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 contentof non-soluble carbohydrates does not seem to be the limitingfactor for survival. Reserves remaining at the end of submerg-ence are used for fast regeneration of leaves and roots andupon de-submergence and the re-entry of aerial O2 (Schluter,1989). The species with the highest reported concentrationsof total soluble sugars and starch are V. cymosa, Crataevabenthamii and P. munguba; species with lower contents ofcarbohydrates are Crescentia amazonica, S. martiana andCecropia latiloba (Koshikene, 2005). Species of later succes-sional stages have higher concentrations of carbohydratesthan early successional species (Koshikene, 2005). Late

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