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Sensitivity of seedlings from different oak species towaterlogging: effects on root growth and mineral

nutritionM Colin-Belgrand, E Dreyer, P Biron

To cite this version:M Colin-Belgrand, E Dreyer, P Biron. Sensitivity of seedlings from different oak species to water-logging: effects on root growth and mineral nutrition. Annales des sciences forestières, INRA/EDPSciences, 1991, 48 (2), pp.193-204. �hal-00882747�

Original article

Sensitivity of seedlings from different oakspecies to waterlogging: effects on root growth

and mineral nutrition

M Colin-Belgrand E Dreyer P Biron

1 Laboratoire d’Étude des Sols et de la Nutrition, INRA Nancy, Champenoux, 54280 Seichamps;2 Laboratoire de Bioclimatologie et d’Ecophysiologie Forestière, INRA Nancy,

Champenoux, 54280 Seichamps, France

(Received 16 August 1990; accepted 30 November 1990)

Summary — The tolerance of oak seedlings from 3 species (Quercus robur, Q rubra, Q palustris) toa 7-wk period of waterlogging was tested under greenhouse conditions. The seedlings had comple-ted their height growth when treatments were applied. A permanent water table was maintained at 6cm below the soil surface. Shoot growth, root growth and mineral content of xylem sap (P, K, Ca,Mg) and leaf tissues (N, P, K, Ca, Mg, S, Mn) were monitored weekly. Waterlogging had strongconsequences on root development; flooded roots decayed, while hypertrophied lenticels and sub-sequently adventitious roots appeared on the taproot. Although the mineral nutrient content in xylemsap displayed significant differences between species, no effect of waterlogging could be detected.But the combination of constant concentration and reduced transpiration in waterlogged seedlingsprobably resulted in a reduced nutrient flux to the leaves. Leaf nutrient contents decreased marked-ly, in particular for total N, and to a lesser extent for S and K; but in all cases they remained wellabove deficiency levels. No phytotoxic accumulation of Mn could be detected. Important interspecificdifferences appeared. The development of root adaptations was much greater for Q robur than forboth Q palustris and Q rubra, probably indicating a higher tolerance to flooding in the former spe-cies. Surprisingly, N and S concentrations decreased more in Q roburthan in both other species, butthis could be due to the fact that only Q robur continued leaf growth, leading to a dilution of N in leaftissues.

hypoxia / Quercus palustris / Quercus rubra / Quercus robur / xylem sap

Résumé — Sensibilité à l’ennoyage de semis de plusieurs espèces de chêne : effets sur lacroissance racinaire et le statut nutritionnel. La tolérance à l’hypoxie racinaire a été testée surdes semis de 3 espèces de chênes (Quercus robur, Q rubra, Q palustris) au cours d’une périoded’ennoyage contrôlé de 7 semaines. La nappe d’eau permanente était maintenue à 6 cm de la sur-face du sol, et ce traitement a été appliqué à la fin de la période de croissance active en hauteur. Lacroissance aérienne, racinaire, et les teneurs en éléments minéraux de la sève brute (P, K, Ca, Mg)et des tissus foliaires (N, P, K, Ca, Mg, S, Mn) ont été mesurées hebdomadairement. L’ennoyage aprovoqué de fortes perturbations de la croissance racinaire; les racines ennoyées ont rapidementdépéri, alors que des lenticelles hypertrophiées, puis des racines adventives sont progressivement

*

Correspondence and reprints

apparues au collet du pivot racinaire. Les teneurs en éléments minéraux de la sève ont présenté desdifférences interspécifiques significatives, mais aucune modification induite par la contrainte n’a puêtre détectée. Étant donnée la réduction observée de la transpiration, cette constance des concentra-tions s’est cependant probablement traduite par une forte réduction du flux total d’éléments minérauxvers les feuilles. Les teneurs foliaires en éléments minéraux ont sensiblement diminué au cours de

l’ennoyage, en particulier en ce qui concerne N, et dans une moindre mesure S; mais dans tous lescas, les concentrations foliaires sont restées largement au-dessus des seuils de carence décrits pourles chênes. L’ennoyage ne s’est pas traduit par une accumulation toxique de Mn. D’importantes diffé-rences interspécifiques dans les réactions à la contrainte sont apparues. La néoformation racinaire aété beaucoup plus importante chez Q robur que chez Q palustris et Q rubra, ce qui semble indiquerune meilleure tolérance à l’ennoyage chez la première espèce. Les concentrations foliaires de N et Sont plus fortement diminué chez Q robur que dans les 2 autres espèces, mais cette différence estprobablement due au maintien d’une certaine croissance chez Q robur, entraînant une dilution del’azote initialement présent et non renouvelé du fait de l’ennoyage.

hypoxie racinaire / Quercus palustris / Quercus robur / Quercus rubra / sève sylémique

INTRODUCTION

Forest trees display a broad spectrum oftolerances to waterlogging. Their degreeof tolerance is often estimated from eitherduration of survival or measured growthand productivity in forest stands or youngplantations submitted to root hypoxia dueto flooding under natural conditions. Survi-val time may vary from a few wk for themost sensitive species, to several (2-3) yrfor the most tolerant ones (Kozlowski,1982). Large differences in tolerancesometimes appear in closely related spe-cies, and the underlying physiologicalmechanisms are seldom clearly analysed.

Oak species vary greatly in their sensi-tivity to waterlogging. Some oak speciesare common in bottomlands and flood-

plains and seem very flood-tolerant. For in-stance, survival under inundation was 2-3

yr for Quercus nigra, Q nuttali and Q phel-lis (Hall et al, 1946; in Kozlowski, 1982).Q palustris did not show altered water rela-tions after 2 yr of continuous flooding in

the central Mississipi valley, although it

displayed premature leaf yellowing and ab-scission (Black, 1984). Q robur is thoughtto tolerate up to 97 d of flooding everyyear (Dister, 1983). Q robur and Q petraea

exhibit different behaviours when plantedin temporarily waterlogged soils in North-

eastern France. The former species seemsto present a better tolerance to soil hypox-ia at the seedling stage, as shown bygrowth experiments with different depths ofwater tables (Lévy et al, 1986). But the lat-ter displays a better productivity on tempo-rary flooded soils in forest stands andshows much larger increases of growth fol-lowing mechanical soil drainage (Beckerand Lévy, 1986). At the seedling stage, arating of decreasing flood tolerance

showed that Q robur behaved better thanQ petraea, and Q rubra had the poorestgrowth (Belgrand, 1983).

Differences in waterlogging tolerance

between Q rubra, Q petraea and Q roburappeared strongly correlated with a differ-entiated ability to develop root adaptations(Belgrand, 1983). In fact, the most fre-

quently reported reaction of trees to soil

hypoxia is the induction of morphologicaland anatomical changes in the root sys-tems of flood-tolerant species (Justin andArmstrong, 1987). Formation of hypertro-phied lenticels followed by the differentia-tion of adventitious and flood-adaptedroots has been commonly described for abroad range of species (Coutts and Arm-

strong, 1976; Coutts, 1982; Harrington,1987; McKevlin et al, 1987).

Flooding induces important perturba-tions in mineral nutrient assimilation. LeafN content of Picea abies was strongly re-duced by flooding (Lévy, 1981). For mostelements (N, K, Fe, Mn and to a lesser ex-tent Mg and Ca) leaf content was reducedin different Pinus species after 30 d of roothypoxia in nutrient solutions (Topa andMcLeod, 1986). But these effects were

mainly observed with trees still growingduring the waterlogging period. No infor-mation on mineral nutrients circulating inthe xylem sap of waterlogged seedlings iscurrently available.

In this study, we compared 3 speciesknown to differ in their waterlogging toler-ance (Q robur, Q rubra and Q palustris)and tested their ability to produce adventi-tious roots in response to a 7-wk flooding.We tried to assess the consequences ofthese differences on the transport of miner-al nutrients to shoots, and on the leaf min-eral content. In a forthcoming paper(Dreyer et al, 1991) the consequences ofthe observed perturbation in root growthon shoot physiology will be assessed.

MATERIALS AND METHODS

Plant material

Acorns were collected during autumn 1987, un-der individuals of Q robur L (Amance Forest,near Nancy, France), Q rubra L (FénétrangeForest, Moselle, France) and Q palustrisMuenchh (Pujo Forest, Tarbes, Hautes Pyré-nées, France). Acorns were stored at -1 °C andsown during the following February in special in-dividual 5-I, 25-cm deep pots, containing a 50/50 v/v mixture of peat/sandy loam. The mainfeatures of this substrate are shown in table I.An external transparent vertical tubing was con-nected to the bottom of these pots, allowing a

precise control of water table level. Seedlingswere grown in a glasshouse near Nancy; daytemperatures were maintained between 20-30 °C, with a night temperature of 16 °C main-tained through heating, and humidity ≈ 60%. Noadditional light was supplied. Height growth wasmonitored weekly from germination on.

Waterlogging

Plants were flooded with tap water on June15th. The upper level of the water table was ad-

justed daily to 6 cm below the soil surface, andmaintained for 7 wk. Pots were then drained and

seedlings allowed to grow for 2 more wk. Sixtyplants were used for each species, with 30 ran-domly selected as controls and 30 treated. Theexperimental design consisted of 3 blocks (1 perspecies), in which treatments were randomlydistributed. Destructive measurements (bio-mass, water status, nutrient content and xylemsap composition) were made weekly on 2 ran-domly selected waterlogged and 2 control

plants. Roots were rinsed with tap water. Thestructure of the root system was observed; in

particular, the presence of lenticels and the de-gree of root senescence were assessed visual-

ly. Root systems were divided thereafter into oldroots, white tips and neoformed roots, and wereoven-dried (65 °C for 24 h). Leaves and stemswere used for mineral content analysis.

Water status and xylem sap extraction

Shoots of selected plants (2 control and 2 treat-ed saplings per species) were cut off once

weekly after being submitted to at least 12 h darkness, and predawn leaf water potential(ψwb) was measured with a pressure chamber.After attaining the balancing pressure, the barkwas removed from the cut end, the pressurewas slowly increased to 2.5 MPa, and main-tained for 5 min. Extruding sap was collectedwith a micropipette and frozen immediately in

liquid nitrogen before being stored at -18 °C.Roots were rinsed with tap water and xylem sapwas extracted by the same technique as for theshoots.

Mineral analyses

Concentrations of P, K, Mg and Ca in the xylemsap were measured directly with an inductivelycoupled plasma spectrometer (ICP, Jobin

Yvon). Nutrient concentrations were measuredtogether on the leaves of 2 seedlings, and theresults were therefore mean concentrations ofboth seedlings. Total leaf nitrogen was deter-mined by Kjeldahl mineralization and a colori-metric procedure (Technicon Autoanalyser),while leaf P, Ca, Mg, K, S and Mn concentra-tions were determined after wet mineralization

(HClO4 + H2O2) and ICP quantitation.

Statistical analysis

Results were analysed using an ANOVA andtesting for differences between collection dates,species and treatments. As soon as no signifi-cant change could be detected over a longerperiod of time, data were gathered for the mainwaterlogging period (ie, from wk 1-7) and com-pared directly with corresponding controls usinga Student t-test; n = 14 for root and shoot xylemsap, and n = 7 for leaf mineral content.

RESULTS

Effects of flooding on shootand root growth

Flooding was imposed after completeshoot growth cessation in Q rubra and Qpalustris as shown by growth dynamics (fig1). Two growth flushes had been complet-ed on Q rubra and Q palustris; while a 3rdflush was beginning on Q robur. In this lat-ter case, flooding slightly reduced heightgrowth, while in the former 2 species, it

had no effect no shoot growth; an apparentdecrease in height for Q rubra was onlydue to recurrent sampling and consequentreduction of plant number. No resumptionof growth occurred after drainage. Leaf

characteristics were very different between

species but were not dramatically affectedby waterlogging (table II). Q rubra had thelargest leaf area per plant despite limitedheight, and the largest leaf specific weight,while Q robur showed only 2/3 of this area,and Q palustris had lower area and specif-ic leaf weights. Flooding had no significanteffect on these parameters; specific leaf

weight increased slightly but this increasewas only significant for Q robur. No leafnecrosis was detected during the entire pe-riod.

Root growth dynamics were much moreaffected by flooding. Some morphologicalfeatures were common to all species:flooding induced a rapid decay of preexist-ing roots, with senescence and disappear-ance of white tips, and necrosis of tap rootand flooded lateral roots.

Hypertrophied lenticels appeared by theend of the 3rd week at the root collar andon non flooded roots and developed mark-edly. Finally, adventitious roots were

formed from the 4th week on, in the soil

above the water table. These new rootswere poorly ramified, had a larger diame-ter, and were not suberized even after 4wk (fig 4).

These reactions occurred in all species,but with very different intensities. Q roburseedlings developed abundant hypertro-phied lenticels by the end of the 3rd wk,and numerous adventitious roots ap-peared after 4 wk of waterlogging. Q rubraseedlings showed a remarkable hypertro-phy of stem and lenticels but only very fewadventitious roots, which appeared only af-ter 6 wk of flooding. Q palustris displayedonly few adventitious roots, and almost nolenticels or stem hypertrophy.

As shown in fig 3a, total root biomass(including senescing roots) was slightly de-creased in flooded Q rubra and Q palustrisafter 4 wk of waterlogging but increased inQ robur as compared to the control. A

strong decrease in the biomass of white

tips, eg growing root apices, appeared atthe same time (fig 3b) in response to flood-ing in all species. The total weight of ad-ventitious roots was very variable: Q robur

developed the largest amount, while Q ru-bra and Q palustris formed only very fewsuch roots. In Q robur, they achieved asubstantial biomass (fig 3b).

Effects of flooding on nutrient transportin the xylem sap and on shoot nutrientstatus

Table III shows the measured concentra-tions of mineral nutrients in the xylem sapextracted from roots and shoots. As no sig-nificant change could be detected in con-trol or in flooded plants after wk 1, we com-pared all the data collected till the end ofthe waterlogging period directly. As a gen-eral rule, nutrient concentrations were

about twice as high in the sap extractedfrom roots than in the sap from shoots.

Significant differences related to specieswere found for all the tested elements, withthe exception of Ca. Q robur showed thehighest concentrations of Mg and K, whileQ rubra had the highest concentrations ofP. Only seldom were the effects of floodingstatistically significant. Significant reduc-tions only appeared for K and Ca in Q pa-lustris and in Q rubra. Large variations be-tween individual plants did not allow closercomparisons.

Leaf nutrient contents showed large dif-ferences between species. Total N was

significantly higher in Q robur, while Cawas more concentrated in Q rubra (tableIV). The total mass of nutrients present inthe leaves was much higher in Q rubra dueto a larger leaf area than in Q robur and Qpalustris (table IV). Flooding induced a

highly significant reduction in total leaf N,and significant reductions in S contents.The reduction in leaf nitrogen appearedvery rapidly in Q robur, for which it was

highly significant; it was less marked andslower but still significant in Q rubra and Qpalustris (fig 4). Reductions in S and Kalso appeared in Q robur, and were nonsignificant for both the other species. Nophytotoxic increase in Mn could be ob-served.

DISCUSSION

Shoot growth

The experiment was designed to assessthe waterlogging effects on well developedseedlings which had already completedtheir annual growth. Effects on shoot

growth were therefore only detected in Qrobur which was the only species still dis-playing growth. The limited increases in

specific leaf weight and the lack of necro-sis showed that waterlogging had no dele-terious effects on the leaves. However, thisresult cannot be generalised, as growingleaves probably would have reacted differ-ently.

Root adaptations

Root reactions were very strong in all 3

species. Decay of the flooded fraction ofthe root systems occurred during the firstfew weeks, with apparently the same inten-sity for all seedlings. The appearance ofhypertrophied lenticels and adventitiousroots in the soil layers above the water ta-ble was also noted in all seedlings, al-

though with different intensities. These rootreactions are a common feature of water-

logging effects on tree seedlings; theyhave been observed on a wide range of

species including Quercus macrocarpa(Tang and Kozlowski, 1982), Fraxinus

pennsylvanica (Gomes and Kozlowski,1980), Alnus rubra and Populus trichocar-

pa (Harrington, 1987), Actinidia chinensis(Savé and Serrano, 1986), Gmelina arbor-ea (Osonubi and Osundina, 1987), Crypto-meria japonica (Yamamoto and Kozlowski,1987), Picea sitchensis (Coutts, 1981), Pi-nus contorta (Coutts and Philipson, 1978)and many others.

Flood-induced roots are white, thick,more succulent and poorly ramified, andlack root hairs; they display both largercells and aerenchyma (Keeley, 1979; An-geles et al, 1986; Justin and Armstrong,1987). These modifications are supposed

to improve oxygen diffusion through hyper-trophied lenticels and gas transport to nonaerated roots (Hook et al, 1971; Keeley,1979; Drew, 1983). They may also be as-sociated with resistance to iron or manga-nese toxicity (Green and Etherington,1977).

Mineral nutrition

The reliability of our xylem sap extractiontechnique with relatively high pressure (2.5

MPa) may be questioned. The fact thatconcentrations were about twice as high insap extracted from roots than from shoots

may be partly explained by the differencesin ion mobilisation in pressurized roots vsshoots. Concentrations of K, Mg and Cameasured by Scuiller (1990) in seedlingsof different Quercus species growing onthe same substrate were very similar toours. Despite a large interindividual vari-

ability, significant differences appeared be-tween species independently from water-

logging, particularly for P, Mg and K. Couldthese differences be related to different

growth habits ? Q robur, displaying thehighest K and Mg, had the greatest heightgrowth, while Q rubra, with higher P, builtup the largest leaf area. But concentrationsare not necessarily correlated with the totalnutrient fluxes from roots to shoots. In fact,transpiration was lower in Q rubra despiteits larger leaves (Dreyer et al, 1991) andtotal nutrient fluxes therefore lower. Q pa-lustris had the lowest concentrations and

transpiration rates among the 3 species,and therefore probably the lowest nutrienttransport to the leaves.

Waterlogging had only very limited ef-

fects on the xylem sap concentrations; sig-nificant reductions only appeared for K.We do not know of any other attempt toanalyse flooding effects on xylem sap con-tents. Effects of water stress on xylem sapcomposition have sometimes been as-

sessed; Scuiller (1990) observed only limit-ed increases in osmotic potential and ionconcentrations with decreasing predawnleaf water potential. It may be concludedthat the stability of xylem sap concentra-tions, associated with a reduced transpira-tion flux (Dreyer et al, 1991), probably re-sulted in a reduction of the total flux ofmineral nutrients to shoots in waterloggedseedlings.

Leaf mineral contents of our seedlingswere for all species and treatments wellabove the deficiency levels for oaks (Bon-neau, 1986). Large interspecies differenc-es were observed for N and Ca. Despitethe fact that Q rubra is a well known calci-

fuge species, it concentrated ≈ 2/3 more

Ca in its leaves than the other 2 species.But Q robur displayed much higher N con-tents, which may be correlated with the

higher rates of photosynthesis observed inthis species (Dreyer et al, 1991). Q rubramobilized the largest total amount of nutri-ents due to its high leaf area. The effects

of waterlogging on leaf nutrient contentswere limited and showed a great variabilitybetween species and measured elements.Observed decreases in total N, which ap-peared in Q robur seedlings and to a less-er extent in the other species, were in ac-cordance with earlier observations by Lévy(1981) with Picea abies, or Meyer et al(1986) with Gossypium hirsutum. In fact,decreases in N contents are often the ear-liest response to flooding (Drew and Sis-woro, 1979; Meyer et al, 1986; Harrington,1987). These decreases may either bedue to nitrate reduction and accelerateddenitrification (Lévy, 1981), or to the inabil-ity of the roots to take up enough N evenbefore the onset of strong denitrification

(Drew and Sisworo, 1979; Meyer et al,1987). Decreases in other elements in Qrobur were not statistically significant. Inboth the other species, apart from de-creases in N, no difference could be de-tected. In this respect, our results differfrom earlier reports, which showed signifi-cant decreases in almost all the tested ele-ments (N, P, K in 3 different Pinus spe-cies; Topa and McLeod, 1986; K, Mg inAlnus rubra and Populus trichocarpa; Har-rington, 1987). In fact, improving soil fertili-ty often limits the effects of waterloggingon tree growth (De Bell et al, 1984), but inthese cases, flooding was imposed on ac-tively growing plants, while our seedlingshad almost stopped shoot and leaf growth.

Only Q robur maintained to some extentgrowth and also displayed the most signifi-cant reductions in leaf mineral contents.Further data are needed to clarify mineralbudgets of saplings submitted to waterlog-ging and flooding.

Mn toxicity, which has been associatedwith waterlogging by some authors

(Sonneveld and Voogt, 1975) was not de-tected here; Mn contents decreased or re-mained at the same levels as in controls,as was also observed by Topa and McLe-od (1986) and Harrington (1987).

Comparison of waterlogging toleranceamong species

The 3 oak species tested are thought todisplay wide differences in waterloggingtolerance. Q robur is supposed to tolerateroot hypoxia (Lévy et al, 1986), Q rubra iswell known for its marked intolerance,while Q palustris is supposed to be moretolerant (Abbott and Dawson, 1983). Theintensity of the root reactions observedwas in agreement with these observationsfor Q robur and Q rubra and confirmed ear-lier findings (Belgrand, 1983). The weakreactions of Q palustris roots were surpris-ing and may have been caused by our par-ticular growth conditions. Root reactions ofactively growing seedlings may be very dif-ferent from those observed here.

Differences in root reaction were not fol-lowed by strong differences in mineral nu-trition. The greatest reductions appeared inQ robur, which showed the largest root ad-aptations. This could be explained by a di-lution of elements, particularly N, in the stillgrowing tissues of Q robur associated witha decrease in absorption. In both the other

species, the cessation of growth, whichwas not related to waterlogging, allowed arelative stability of nutrient contents. In

fact, the mineral richness of the culturemedium which resulted in mean leaf con-tents largely above deficiency levels andeven above optimal levels (Bonneau,1986) probably explained this stability.

The most important difference in water-logging tolerance that we observed was re-lated to the ability of Q robur to developroot adaptations in flooded plants. It is still

difficult to develop an analysis of floodingtolerance between species in the absenceof a general model of hypoxic stress ef-

fects at the whole sapling level. There isstill need for further research to improveour knowledge in this area.

ACKNOWLEDGMENTS

The authors wish to thank JM Gioria for growingthe seedlings, C Bréchet for help in mineralanalysis and 2 anonymous reviewers for helpfulcriticism on the first draft of this manuscript.

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