Trees (2005) 19: 374–384 DOI 10.1007/s00468-004-0396-x
ORIGINAL ARTICLE
Elisabetta Tamasi · Alexia Stokes · Bruno Lasserre · Fr´ederic Danjon · St´ephane Berthier · Thierry Fourcaud · Donato Chiatante
Influence of wind loading on root system development and architecture in oak (Quercus robur L.) seedlings. Received: 18 November 2003 / Accepted: 7 October 2004 / Published online: 18 January 2005 C Springer-Verlag 2005
Abstract The effect of wind loading on seedlings of English oak (Quercus robur L.) was investigated. Instead of using a traditional wind tunnel, an innovative ventilation system was designed. This device was set up in the field and composed of a rotating arm supporting an electrical fan, which emitted an air current similar to that of wind loading. Oaks were sown from seed in a circle around the device. A block of control plants was situated nearby, and was not subjected to artificial wind loading. After 7 months, 16 E. Tamasi · B. Lasserre () · D. Chiatante Dipartimento di Scienze e Tecnologie per l Ambiente ed il Territorio, Universit`a degli Studi del Molise, Via Mazzini 8, 86170 Isernia, Italy e-mail:
[email protected] Tel.: +39-0865-478905 Fax: +39-0865-411283 E. Tamasi · A. Stokes · B. Lasserre · S. Berthier Laboratoire de Rh´eologie du Bois de Bordeaux, Unit: CNRS/INRA/Universit´e Bordeaux I, Domaine de l Hermitage, 69, Route d’Arcachon, 33612 Cestas Cedex, France T. Fourcaud CIRAD Unit´e de Mod´elisation des Plantes, Laboratoire de Rh´eologie du Bois de Bordeaux, Domaine de l Hermitage, 69, Route d’Arcachon, 33612 Cestas Cedex, France F. Danjon INRA Ephyse, Recherches Foresti`eres, 69, route d’Arcachon, 33612 Cestas Cedex, France D. Chiatante Dipartimento di Scienze Chimiche ed Ambientali, Universit`a degli Studi dell’Insubria, Via Valleggio 11, 22100 Como, Italy S. Berthier Forest Research, Northern Research Station Roslin, Midlothian, EH25, 9SY, UK
plants from each treatment were excavated, and root architecture and morphological characteristics measured using a 3D digitiser. The resulting geometrical and topological data were then analysed using AMAPmod software. Results showed that total lateral root number and length in wind stressed plants were over two times greater than that in control trees. However, total lateral root volume did not differ significantly between treatments. In comparing lateral root characters between the two populations, it was found that mean root length, diameter and volume were similar between the two treatments. In trees subjected to wind loading, an accentuated asymmetry of root distribution and mean root length was found between the windward and leeward sides of the root system, with windward roots being significantly more numerous and longer than leeward roots. However, no differences were found when the two sectors perpendicular to the wind direction were compared. Mean tap root length was significantly higher in control samples compared to wind stressed plants, whilst mean diameter was greater in the latter. Wind loading appears to result in increased growth of lateral roots at the expense of the tap root. Development of the lateral root system may therefore ensure better anchorage of young trees subjected to wind loading under certain conditions. Keywords Quercus robur L. . Wind . Tree root architecture . Anchorage . AMAPmod Introduction Plant root system development is a complex process involving several internal and environmental factors and their mutual interaction. As a result of the numerous storms and landslides which have affected northern Europe for the last 50 years, researchers are dedicating more resources to the problems of tree stability and to the fundamental role of the root system in ensuring anchorage (Coutts 1983, 1986; Ennos et al. 1993; Ennos 1994; Stokes et al. 1995, 1997; Nicoll and Ray 1996; Chiatante et al. 2003).
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Much research has been carried out on the influence of mechanical stress on the above-ground parts of herbaceous (Jaffe 1973; Jaffe and Telewski 1984) and woody plants (Telewski 1990, 1995). However, fewer studies have examined responses in the root systems of mechanically perturbed plants. It is known that morphological changes may occur in the shape of individual roots when trees are subjected to certain mechanical stresses, but less is known about the root system as a whole (Cannell and Coutts 1988; Stokes et al. 1997). Root systems of adult Sitka spruce (Picea sitchensis) trees exposed to a natural prevailing wind were found to possess more structural root mass on the leeward side compared to the windward side (Nicoll and Ray 1996). The cross-sections of the structural roots of these trees, measured at different distances from the tree centre, were larger on the leeward side of the tree with a shape analogous to a T-beam, i.e. there was more secondary growth on the upper side of the root, which helps resist against failure in compression. Experiments carried out on woody and herbaceous plants subjected to mechanical stresses have shown that whereas stem growth responses are variable, root system growth and topology may be altered considerably (Stokes et al. 1995, 1997; Goodman and Ennos 1998, 1999). Stokes et al. (1995, 1997) demonstrated that mechanical perturbation of young Sitka spruce (P. sitchensis), results in increased root diameter growth and a greater number of windward and leeward roots. In wind-stressed trees of the same species, it was found that windward roots were more highly branched with longer root tips. Goodman and Ennos (1998) showed that root systems of herbaceous plants, Helianthus annuus L. and Zea mays L., grown in a glasshouse and subjected to regular, unidirectional stem flexure, responded locally to the mechanical stimulation. Considerable differences were found between lateral roots along the axis of stimulation compared with lateral roots in zones perpendicular to the bending axis: firstorder lateral roots were also thicker, more rigid and more numerous. Previous experiments on trees have usually focused on the responses of coniferous species to wind loading, and it is not known if a similar growth response occurs in hardwood species. Therefore the aim of the present study was
Fig. 1 Representation of the electrical wind device set up in the field. An electrical fan is situated at one end of a 4 m long rotating metallic arm. This arm is attached to a motor at the centre of the circle, and a counter weight steadies the arm at the other side of the motor. Seedlings were sown in a circle around the device, and the arm rotated in the anti-clockwise direction, subjecting each plant to a wind speed of 5.5 ms−1 every 30 s
to determine if similar traits could be found in young English oak (Quercus robur L.) trees subjected to wind action. Instead of using traditional techniques, whereby plants are grown in pots in a wind tunnel and submitted to glasshouse climatic conditions, it was decided to carry out the experiment under more natural conditions in the field. A new device was designed, made up of a fan supported by a metallic arm which rotated in an anti-clockwise direction (Fig. 1). A large number of plants could then be exposed to the same wind-speed and without the effect of unidirectional light, which influences both shoot and root growth (Stokes et al. 1995; Berthier and Stokes 2004). Tree growth and root system architecture were then measured using a 3D digitiser (Danjon et al. 1999a, b) and results interpreted with regards to tree anchorage characteristics. Materials and methods The experimental site and artificial wind device The experiment took place in the INRA nursery, Pierroton, 25 km from Bordeaux and 45 km from the Atlantic Ocean, in south-west France. Mean annual wind speed in this area is 3.3 ms−1 (M´et´eo-France), and the prevailing wind direction is north-west. In order to aid germination, 100 oak seeds (Quercus robur L., provenance Pierroton, France) were sown in compost in plastic pots in July 1999, and carefully planted out in August 1999. Q. robur is a forest species native to the south-west of France. When the seedlings were transplanted, lateral roots had not yet developed, only a short radical (1–2 cm long) was present. Seedlings were planted in a flat, sandy podzolic soil, characteristic of the region, along the perimeter of a circle with a 5 m radius (Fig. 1). At the centre of this circle, a motor with a rotating arm 8 m long and an electrical fan fixed to one end of the arm was installed (Fig. 1). The arm and the fan turned non-stop in an anti-clockwise direction and took 20 min to turn one circle producing a wind-speed of 8.0 ms−1 at the fan exit and of 5.5 ms−1 at a distance of 1 m from the fan. Each oak seedling was thus subjected to wind loading for 30 s every hour. On the same site, an equal number of seeds were planted nearby in a
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rectangular block, but were not subjected to artificial wind loading, and thus represented the controls (Tamasi 2002). Although all plants were exposed to natural wind loading, the site was sheltered by 6 m high hedges at a distance of 20 m from the experimental plots. Plants were automatically watered once a day, by a sprinkler type irrigation system during the period August– October 1999. Seedlings in both blocks were assumed to be subjected to the same growth conditions, as these blocks were only 10 m apart. In order to verify this hypothesis, the pH and quantity of N, P, K, Ca and Mg in the top 10 cm of soil were measured in 24 samples taken randomly from the blocks (Berthier and Stokes 2004). No significant differences or restrictive values for oak growth were noticed (P>0.05 with pH =6.0±0.3, N=0.80±0.14 g kg−1 , P205 =0.131±0.003 g kg−1 , Ca=1.16±0.11 Cmol kg−1 , Mg=0.09±0.02 Cmol kg−1 and K=0.03±0.01 Cmol kg−1 ). Anemometers (034A, Met One Instruments, Ore., USA) and thermometers (Unilog, Czech Republic) were installed in each block, above the seedlings, to register ambient air properties. Sensors measuring soil humidity and temperature at a depth of 20 cm were added (ML2×, DeltaT Devices, Cambridge, UK). All instruments were connected to a datalogger (Minicube VX, EMS Brno, Czech Republic) programmed to record the specified data every 5 min throughout the growing season. The sensors were moved around inside the blocks to reveal possible withinblock differences and microclimates. No durable significant differences i.e. over 1 day, were revealed between or within blocks (P>0.05). Natural winds at a height of 1.5 m within the overall experimental site were found to originate from an azimuth of 294±26◦ , with a mean speed of 0.52±0.23 ms−1 during June–September. Photosynthetically Active Radiation (PAR) data were also available from a weather station located 3 km from the site (Berbigier et al. 2001). PAR was measured at a height of 38 m, i.e. 13 m above a forest canopy. PAR ranged from roughly 500 mol m−2 per day in June, to 380 mol m−2 per day in September.
Fig. 2 The low magnetic-field 3D digitising system consists of an electronic unit, a transmitter and a receiver. For each digitised point, the system’s electronic unit records the coordinates [x, y, z] of the point, producing, at the same time, a topological code which describes the structural relationships between the points. Subsequently, all this architectural information is collected in specific files, and treated with AMAPmod software
In order to analyse plant response to wind, 32 7-monthold root system samples were chosen at random, 16 from the wind stressed plants and 16 from the controls. Before harvesting the young trees, each wind stressed plant was marked with a felt-tip pen on the windward side of the stem and control plants on the northern side. Care was taken not to break roots during the excavation process. Root systems were then washed and immediately analysed. Three dimensional (3D) digitising of root systems A topological and geometrical description of the root system was carried out using a low-magnetic field 3D digitiser (3SPACE Fastrak, Polhemus, Long ranger option, http://www.polhemus.com) driven by the software Diplami (Sinoquet and Rivet 1997; Danjon et al. 1999a, b). This device is composed of an electronic unit, a transmitter and a receiver (Fig. 2). For each digitised point, [x, y, z] coordinates and diameter (measured manually) were assessed jointly with the topology i.e. how individual roots are connected to each other through branching. Once a plant had been excavated, it was immediately tied to a stake for digitising. In order to reproduce the orientation that each plant had in the field, it was considered that in those plants subjected to wind loading, the wind direction coincided with a defined axis of the sphere’s reference system. In control plants, due north was considered as coinciding with the same axis of the sphere’s reference system. Data were saved in files and exported to the software AMAPmod (Godin et al. 1997a). In AMAPmod software, root systems are represented by “Multiscale Tree Graphs” (MTG) (Godin and Caraglio 1998). A MTG is a topological structure in which root data are organised hierarchically in scales. This organisation previews that each individual root can be considered as an axis and each axis as a sequence of root segments, a root segment being the part of
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the root included between two subsequent digitised points. The root length and volume are thus obtained as the sum of each root segment length and volume. The computer language in AMAPmod is AML (Godin et al. 1997b) which supplies pre-existing functions. Additional functions were written by the first author in order to carry out the analysis. A detailed description of the measurement and analysis techniques is given in Danjon et al. (1999a, b). Data analysis A system for classifying roots was established: the taproot was considered as a zero order root, the laterals originating from the taproot as first order roots, and their daughter roots as second order roots. Root length and volume were considered as the sum of each root segment length and volume. Tap root diameter was defined as the mean of the basal diameters of the root segments of which it was composed. However, lateral root diameter was taken as the basal diameter of the first segment of the root. This differentiation was adopted due to the dissimilarity in root dimensions between the tap and lateral roots. In all root systems, the tap root was significantly thicker than the lateral roots, and was usually highly tapered. Lateral roots tapered only slightly, if at all. In order to determine if wind loading has an effect on root system architecture two kinds of analyses were carried out: (1) a longitudinal analysis, splitting the tap root into three equal lengths, in order to differentiate between the lateral roots borne along the first third of the taproot and their daughter branches (proximal lateral roots), from the laterals borne along the final two thirds of the taproot length and their branches (distal lateral
Fig. 3 Longitudinal and radial analysis of root system growth and form. In the longitudinal analysis, the root system was split into two sections around the central axis: the upper third (proximal roots) of the length of the taproot, and the lower two-thirds (distal roots). The radial analysis carried out on root system, allowed us to group 1◦ L roots depending on their azimuth, into four quadrants. For the root
roots) (Fig. 3). This kind of differentiation was made assuming the fundamental factor, already shown in conifers, that the superficial first order lateral roots are the most important in terms of anchorage (Stokes et al. 1995, 1997; Dupuy et al. 2003; Cucchi et al. 2004). A relative depth analysis was adopted, i.e. the length of the tap root was not taken into account in this analysis. This type of analysis was chosen because of the high variability in size observed between seedlings. If the tap root had been split into set lengths, the bias would be towards small plants having significantly shorter tap roots than larger plants. (2) a radial analysis was also carried out, which grouped the first order lateral roots, depending on their azimuth, into four quadrants. In plants subjected to wind loading, the wind direction was considered as 0◦ , therefore windward (315◦ –45◦ ) and leeward quadrants (135◦ –225◦ ) were defined, as well as two quadrants perpendicular to the wind direction (45◦ –135◦ , 225◦ –315◦ ) (Fig. 3). For root systems of control plants, similar quadrants were defined: north-west (270◦ –360◦ , also the prevailing natural wind direction) and south-east (90◦ –180◦ ), and north-east (0◦ –90◦ ) and south-west (180◦ –270◦ ) in the direction perpendicular to the natural wind. In order to obtain the biomass of roots in each quadrant, the number of lateral roots for each sample was manually counted and their spatial position noted. The roots were then classified according to their branching status, depth and the quadrant into which they had been classed. Each lateral root was then cut at the point of insertion with its mother root and the lateral root total fresh weight measured. The fresh weight of each taproot was also measured. All the shoot and root system components were then dried in an oven at a temperature of 100◦ C for 3 days and their biomass measured.
systems of wind stressed plants windward (315◦ –45◦ ) and leeward quadrants (135◦ –225◦ ) were defined, as well as two quadrants perpendicular to the wind direction (45◦ –135◦ , 225◦ –315◦ ). The root system image is a typical reconstruction from real data using the software AMAPmod
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The data was checked using AMAPmod to reconstruct 3D images of the root systems which can then be displayed from any angle, any magnification and coloured according to their branching order (Fig. 3). Statistical methods The distribution of each population was tested using the Kolmogorov-Smirnov normality test (Dagnelie 1973, 1975). If the result of the normality test was positive, parametric comparison methods were adopted. If the contrary was found, non-parametric comparison tests were assumed (Dagnelie 1973, 1975; Sprent 1992). Two-sample T-tests and non-parametric Mann-Whitney tests were used on independent samples, in order to compare wind stressed and control populations (inter population tests). A two-factors unbalanced variance analysis and a non-parametric Friedman test were carried out on paired samples, in order to determine if differences existed between the four quadrants, in the two axial directions (artificial/natural wind direction and perpendicular to artificial/natural wind direction), and between longitudinal (proximal and distal) areas in both wind loaded and control root systems (intra population tests). Subsequently, PVA and PT indicate probabilities of the null hypothesis for the variance analyses and T-tests respectively, and PF and PMW designate probabilities of the null hypothesis for the Friedman and Mann-Whitney tests, respectively. The two-factors unbalanced variance analysis corresponded to the following theoretical model:
Fig. 4 Box-plot representation of distributions, indicative of the number of 1◦ L roots, in wind stressed and control plants. In the box plot, the upper and lower limits correspond, respectively, to the value of the first (Q1 ) and the third (Q3 ) quartile of the distribution; the black circle is the median symbol and the vertical lines connect two extreme values, obtained as a linear combination of Q1 and Q3 values. Therefore it can be seen that although there is much variability in wind-stressed plants, significantly more 1◦ L roots were present (PMW =0.02) compared to control seedlings of Quercus robur L.
X i j = µ + Si + P j + εi j where Xij is the observed value, µ the general mean, Si either the quadrant factor (3 df) or the longitudinal sector factor (1 df), Pj the root system factor (15 df) and εij the random error term. All factors were considered to be fixed. In the Friedman test, the root systems were counted as blocks and the quadrants or longitudinal regions as treatments. In the variance analysis, the two quadrants along the axis perpendicular to artificial or natural wind loading were considered as two repetitions of the same level. In the Friedman test, means of data from the two quadrants along the axis perpendicular to artificial or natural wind stimulation were used.
Fig. 5 A significantly higher number of distal 1◦ L roots were present (PT =0.02) in wind stressed seedlings of Q. robur, compared to control plants. Values are median ±Q1 and Q3 , with vertical lines connecting extreme values
Results
the oak seedlings. Thus, first order lateral roots (1◦ L) represented 92% of total lateral root number in the wind stressed block and 96% of total lateral root number in the control block; no third order lateral roots were found in any plants. In wind loaded trees, the median of the distribution of 1◦ L roots was significantly greater compared to control plants (PMW =0.02, Fig. 4, Table 3) and a significantly higher number of distal 1◦ L roots was also present, compared to control plants (PT =0.02, Fig. 5, Table 3). However, the total number of proximal 1◦ L roots between the two treatments was not significantly different.
Number of lateral roots
Intra populations analysis
Inter populations analysis
In root systems of both wind stressed and control plants, no differences were found between the median values of proximal 1◦ L and distal 1◦ L root distributions.
A low number of second order lateral roots (2◦ L) was found in both populations, probably due to the very young age of
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In wind loaded plants, the spatial distribution of 1◦ L roots was highly asymmetric between the two quadrants in the direction of artificial wind loading. The median of the windward 1◦ L root distribution was significantly greater than that of the leeward 1◦ L roots (PF =0.01, Fig. 6, Table 1). Windward 1◦ L roots represented 75% of the total number of 1◦ L roots existing in the two quadrants in the wind direction in all wind stressed trees. The mean number of leeward 1◦ L roots was significantly lower than the mean number of 1◦ L roots growing perpendicular to the wind direction (PVA
