Oxygen dynamics and plant-sediment interactions in isoetid ...

NewPaper 2Phytologist Research 329oligotrophic habitat. Lobelia’s special structure can insteadbe interpreted as an adaptation to use CO 2 in the sedimentpore water as a much richer carbon source for photosynthesisthan the surrounding water. Pore water in natural sandysediments contained 0.60 mM CO 2 (Table 1), which is 40times higher than CO 2 concentrations in air-saturated lakewater (c. 0.015 mM). Lobelia can only use CO 2 for photosynthesisand air-saturated concentrations are too low tosupport positive net photosynthesis (Winkel & Borum,2009). To ensure high CO 2 supply from the sediment toleaf photosynthesis, root surfaces must be large and highlypermeable and air lacunae must be wide and short throughroots and leaves. Moreover, to maintain high CO 2 concentrationsin plants growing on sediments of low decompositionrates, plants must prevent CO 2 loss to the water via theintraplant gas transport route and this requires a lid (adiffusion barrier) on leaf surfaces.The diffusion barrier on Lobelia’s leaves also reducesevaporation and ensures survival when plants regularlybecome exposed to the air following drawdown of the watertable during summer (Pedersen & Sand-Jensen, 1992).Most submerged aquatic plants dry out upon exposure toair and several species, including the common isoetidLittorella uniflora (Nielsen et al., 1991), survive by producingnew aerial leaves with stomata. Lobelia does not investin a new set of leaves, which would be costly and perhapsimpossible considering its low intrinsic growth rate andnutrient-poor habitat. Thus, special structural and physiologicaladaptations serve several purposes and need to beviewed in regard to the entire plant life.Environmental changes and plant stressSediment chemistry was very susceptible to addition ofmodest amounts of easily degradable organic matter. O 2disappeared from most of the sediment in the light withaddition of only 0.1 or 0.2% organic matter and it took100 d for O 2 to resume penetration deeper than 40 mm atthe lowest dose. Even after 194 d, pore-water concentrationsof DIC, CO 2 , NH + 4 and Fe 2+ were elevated relative tocontrol values, reaching the substantial 200 lM NH + 4 and510 lM Fe 2+ at 0.2% organic addition (Table 1). Theselow organic treatments did not reduce leaf nutrients,+chlorophyll and photosynthesis, although such high NH 4concentrations stress other macrophytes when leaves aredirectly exposed (Smolders et al., 1996).Higher additions of organic matter (0.4–1.6%) clearlyimpeded photosynthesis and incorporation of TP and TNin the leaves. The most parsimonious explanation for thestress is prolonged anoxia in leaves and roots in the darkreducing ATP production by oxidative phosphorylation tosustain uptake, transport and incorporation of mineral ionsand organic solutes in cell products (Aguilar et al., 2003;van Dongen et al., 2003). A crucial role of TP and TN inleaf tissue for forming the photosynthetic apparatus issupported by significant positive correlations between TP,TN, chlorophyll and photosynthesis. According to highNH + 4 concentrations in all organic amendments and highortho-P concentration in the 1.6% treatment, it is not alack of N and P in the sediment that restricts leaf nutrients,but insufficient uptake from the sediment and transfer toleaf tissue.Anoxia initiates the accumulation of NH +4 and theformation of Fe 2+ and other reduced compounds in thesediment (e.g. Mn 2+ , sulphides and small fatty acids), whichmay contribute to plant stress (Gibbs & Greenway, 2003).These compounds accumulate as a consequence of anoxiaand do not have the same fundamental physiological influenceas many hours of anoxia in the plant tissue. Also,insufficient ATP formation and gradual depletion of carbohydratereserves can account for the inability to incorporateN and P in leaf tissue despite high sediment availability.Moreover, high concentrations of NH + 4 and Fe 2+ withoutany apparent stress on photosynthesis developed in sedimentwith 0.2% organic addition, i.e., concentrations onlytwo to five times lower than observed at greater organicamendments. This result supports the notion that O 2 deprivationis the overriding stress factor.Phosphorus in leaf tissue declined below the general minimumthreshold to support photosynthesis and growth ofsubmerged macrophytes at organic amendments of 0.4–1.6% (legend to Fig. 7). Although the critical threshold isan average for many macrophytes and Lobelia may havelower requirements than most other species (Moeller, 1978;Demars & Edwards, 2007), leaf P, chlorophyll and photosynthesisare so low in the 1.6% organic treatment thatLobelia can just barely survive. These results imply that Plimitation in Lobelia represents a strong additional stress oforganic enrichment and O 2 deprivation as a result of one ormore mechanisms. First, inorganic P remains adsorbed tosoil particles or gradually thicker Fe-coatings formed onroot surfaces in reduced sediments (Christensen & Sand-Jensen, 1998). Second, and probably most significantly,reduced root uptake, translocation and leaf incorporation ofP are the result of O 2 stress and insufficient ATP production(Gibbs & Greenway, 2003). Thirdly, widespreadanoxia is proposed to reduce uptake and translocation of Pby mycorrhiza fungi (Wigand et al., 1998). TN depletionin leaf tissue is less severe, perhaps because of continued diffusiveuptake of NH + 4 from high pore-water concentrations(Marschner, 1995), which does not require active rootmembrane uptake or transfer by fungi.In summary, anoxia in sediments and leaf lacunae late atnight was a surprising recurring summer phenomenon inpristine Lobelia populations on nutrient-poor sandy sediments.Small additions of labile organic matter drasticallyreduced O 2 depth penetration and prolonged leaf anoxiabecause impermeable leaf surfaces prevented O 2 supplyÓ 2010 The AuthorsNew Phytologist Ó 2010 New Phytologist Trust50New Phytologist (2011) 190: 320–331www.newphytologist.com