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Keywords:

  • Root architecture;
  • root branching;
  • root diameter distribution;
  • root topology;
  • topological index;
  • salt marsh

Summary

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  • 1
     We compared the root systems of seven halophytic species that occur at different elevations on a salt marsh, in order to (i) test the hypothesis that variations in root system architecture reflect adaptation to inundation frequency or nitrogen limitation, and (ii) verify the theoretically predicted relationships between root diameter, link magnitude and root topology. Diameters and lengths of individual laterals were determined along root axes, and branching patterns were quantified by calculating a topological index (TI).
  • 2
     Chenopodiaceae (annual dicots) showed that with increasing elevation, the branch density and length of individual first-order laterals tended to increase, so that the relative length of the main axes decreased. Root branching of the Chenopodiaceae at lower elevations was herringbone-like, whereas species from higher elevations had smaller TIs because their branching patterns were more complex.
  • 3
     The Gramineae, too, showed a tendency to increased length of individual laterals with increasing elevation. However, TI was not related to elevation, did not indicate a herringbone structure for all species, and was within the same range of that of the Chenopodiaceae.
  • 4
     As root topology of the Chenopodiaceae is related to elevation, but that of the grasses is not, topology is not necessarily an important adaptive trait in all plant families that inhabit the salt marsh. Short first- and second-order laterals may represent a more general architectural adaptation to frequent inundation, with longer first-order laterals being favourable to competition for nutrients.
  • 5
     Diameters at the root base tended to decrease if root branching was herringbone-like (TI close to 1). Roots of first-order laterals were approximately one-third of the diameter of the main axes; second-order laterals were approximately half the diameter of the first-order laterals. These ratios illustrate the value of using the developmental segment-ordering system in describing roots. The theoretically predicted relationship between root diameter and link magnitude was not present within individual orders of roots, whereas diameter did slowly increase with magnitude when combining different root orders.
  • 6
     In the absence of a clear relationship between root diameter and link magnitude, the predicted high carbon costs associated with herringbone root systems disappear, whereas the advantage of minimized inter-root competition remains. Consequently, herringbone root systems will be most efficient in terms of nutrients gained per carbon invested. However, dichotomous root systems offer a greater potential for exploring the soil, which contributes to the potential competitiveness of plants growing in nutrient limited habitats.

Introduction

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References

Coastal salt marshes have a unique vegetation tolerant of the multiple stresses and frequent disturbances related to tidal inundation. The plant community of a marsh is structured along the elevational gradient (De Leeuw 1992). The low part of the marsh is a stress-dominated environment, as frequent inundation results in anoxic soils with low redox potentials (Armstrong et al. 1985; Ewing et al. 1997). These conditions can reduce photosynthesis, growth and survival of plants (Pezeshki 1997; Pezeshki & Delaune 1996; Sanchez et al. 1997). Only species that facilitate aerobic metabolism and detoxification of the rhizosphere by oxygen transport through specialized root structures such as aerenchyma will survive in low parts of the marsh (Armstrong et al. 1991; Justin & Armstrong 1987). Alternative mechanisms of survival in flooded soils (Blom & Voesenek 1996) are generally insufficient in areas that are consistently flooded, such as the low marsh. Moving upwards along the elevational gradient, the severity of inundation-related stresses decreases, such that more species have the potential to survive. Competition for nitrogen then becomes more important in structuring the plant community, as nitrogen is the limiting nutrient in most salt marshes (Kiehl et al. 1997; Levine et al. 1998). Strategies that enable optimal foraging for nutrients in the high part of a salt marsh, however, are likely to conflict with traits required to survive in the low parts of the marsh. Hence our first objective was to test how plants from different elevations of the salt marsh have resolved this conflict in terms of their root architecture.

Fitter (1987) and Fitter et al. (1991) compared different patterns of root branching with respect to construction costs and intraroot competition for nutrients, using a link-based topological model (Fig. 1). Fitter & Stickland (1991) predicted that a ‘herringbone’ architecture, which is relatively expensive but minimizes inter-root competition, is favourable for slow-growing species from habitats where soil resources are scarce. The relatively cheap construction costs of ‘dichotomous’ root systems were predicted to be favourable for fast-growing species from nutrient-rich habitats. This scheme proved to be valuable in linking root-branching patterns to plant-growth strategies (Berntson & Woodward 1992; Fitter & Stickland 1991; Fitter et al. 1988; Taub & Goldberg 1996). Fitter et al. (1991) showed that the exploitation efficiency of contrasting root topologies is sensitive to the rate at which the root diameter increases with the link magnitude (the total number of root segments that are connected to the shoot through that specific link; Fig. 1). This sensitivity is caused by the greater effect of the root diameter on the construction cost function compared to its effect on nutrient uptake. Fitter (1987) assumed that root diameter increases with increasing magnitude of the individual link, because (i) high-magnitude links carry a relatively large percentage of the overall flow of the resources that are captured by the root system, and (ii) there is a good correlation between xylem cross-sectional area and root cross-sectional area, both within and between species. The relatively high costs of herringbone-like root systems is thus the result of the relatively large fraction of high-magnitude links in roots with a high topological index (TI; Fig. 1). However, the presumed increase of average root diameter with link magnitude and TI of the root system has not yet been validated, despite its importance. Observations on the increase of root radius with magnitude are limited to a few species (Table 2 of Fitter 1991). Taub & Goldberg (1996) speculated that the costs (diameter) of root systems may be less dependent on root topology in grasses than in dicots, but concluded that no data were available to test this.

image

Figure 1. Schematic representation of Fitter’s link-based parameters to describe root topology (Fitter 1987; Fitter 1991; after Werner & Smart 1973), and scans of root segments to illustrate the actual appearance of the roots that we studied. A link is defined as a piece of root between two branching points (interior link) or between a branch and a meristem (exterior link). The magnitude (M) of the overall root system represents the number of exterior links, which equals the number of meristems in a root. The magnitude of an individual link within the root system represents the total number of root segments connected to the shoot through that specific link. By definition, the magnitude of all exterior links is 1. The magnitude of interior links equals the sum of the magnitudes of the two links that are joined together (see numbers outside parentheses). The altitude of the overall root system (A) is the number of links in the longest path from an exterior link to the most basal link of the root system. The number within parentheses indicates the altitude of each possible path. The arrows on the root segment of Suaeda maritima indicate the main root and the first- and second-order laterals, respectively. The topological index of a root system may be defined as log altitude/log magnitude.

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Our objectives were twofold. The first objective was to test whether dicots from the low marsh have herringbone-like roots, and dicots from high elevations have dichotomously branched roots. That is, we hypothesize that the root-system topology of species from the low versus high marshes indicate growth strategies typical of slow-growing stress tolerators versus fast-growing competitors, respectively. Grasses are assumed to have a herringbone root topology, regardless of the elevational level of the habitat (cf. Taub & Goldberg 1996). The second objective was to test the assumptions with respect to root diameter and root topology (cf. Fitter 1987). That is, we hypothesize that root diameter increases with magnitude, and that this results in a stronger increase in diameter towards the base of herringbone-structured roots than to the base of more dichotomous roots. In addition, we also expect that the ratio of the diameter at the base of the main axis and the minimum root diameter (Dbase/Dmin) increase proportionally with the total number of links in a root system (cf. Van Noordwijk et al. 1994).

Materials and methods

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References

Plant material

Three species from the Gramineae and four from the Chenopodiaceae (annual dicots) were selected for the contrasting elevation of their habitats. The Gramineae were: Spartina anglica Hubbard from the low marsh; Puccinellia maritima (Hudson) Parl. from the low/middle marsh; and Elymus pycnanthus (Godron) Melderis from the high marsh. The Chenopodiaceae were: Salicornia europaea (L.) from the low marsh; Suaeda maritima (L.) Dumort from the middle marsh; Atriplex hastata (L.) from the middle/high marsh; and Atriplex litoralis (L.) from the supralittoral debris. Spartina can reach a cover up to 90% in the majority of the low marsh, whereas Salicornia dominates those areas that have not yet been occupied by Spartina. In the low/middle marsh Puccinellia will be dominant if management includes cattle grazing, or it will be dispersed and have a cover of about 15%. In most marshes Suaeda grows dispersed, and has a cover of only a few per cent. In the absence of cattle grazing, Elymus can reach a cover up to 90% in the high marsh. Atriplex hastata generally grows dispersed, and has a cover of a less than 10%. Large patches of Atriplex litoralis can be found in the flood line, adjacent to the dyke.

Seeds collected in 1997 from natural vegetation in the south-west of The Netherlands (51°27′ N, 3°39′ W) were stored at 5 °C and subsequently germinated at 20 °C. After germination, nine seedlings per species were each transplanted into a 1·25 l pot (80 mm diameter; 250 mm height; transparent plastic covered with black plastic). The pots were filled with a sandy sediment collected from a nearby marsh, to which slow-release fertilizer was added in the following amounts: 3·4 g 23 : 0 : 0 N : P : K + 1·6 g 10 : 48 : 0 N : P : K + 4 g 0 : 0 : 45 N : P : K (Osmocote, Scotts Europe BV, The Netherlands). Water was supplied in excess, as all pots could drain freely. We grew the plants under these optimal conditions (drained pots with regular irrigation and a surplus of nutrients) to minimize effects on root topology due to limited soil resources, which stimulates herringbone branching (Taub & Goldberg 1996). The transplanted seedlings were kept in a completely randomized design. After 26 days in a climate chamber (16 h of 21 °C, 400 µmol m−2 s−1 PAR; 8 h of 18 °C, darkness), plants were placed outdoors (June 1998). Plants were harvested when the roots reached the bottom of the (transparent) pots, but were still sufficiently uncrowded so that individual roots could be isolated (50–100 days after transplanting, depending on growth rates). The number of replicates per species is indicated in the legend to Fig. 2. At harvest, two ‘full-grown’ individual roots were isolated from each plant, full-grown being defined as branched roots with a maximum length of the main axes. That is, we picked basal roots and complete nodal axes for dicots and monocots, respectively. Full-grown roots were regarded as the most suitable for studying the topology, as branching had had most time to develop.

image

Figure 2. (a) The relative contribution of the main axes to the overall length of the root system (F6,40 = 3·83; P < 0·01). (b) Mean length of individual first-order (bars left; F6,40 = 1·54; P > 0·20) and second-order (bars right; F6,37 = 2·16; P = 0·07) lateral roots. (c) Branch density of first-order (bars left; F6,40 = 10·47; P < 0·01) and second-order (bars right; F6,37 = 6·03; P < 0·01) lateral roots. Species are sorted according to the elevation of their habitat: those from the low marsh are plotted towards the left side of the x-axes; those from the high marsh towards the right-hand side. Sal, Salicornia europaea (n = 5); Spa, Spartina anglica (n = 8); Puc, Puccinellia distans (n = 8); Sua, Suaeda maritima (n = 4); Ely, Elymus pycnanthus (n = 9); Ath, Atriplex hastata (n = 8); Atl, Atriplex litoralis (n = 5). The Gramineae are indicated by white bars (±SE); the Chenopodiaceae by grey bars (±SE). Significant differences are indicated by the letters on top of the bars: a–c for bars on the left; x–z for bars on the right.

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Analysis of the root system

Intact roots were spread out on a transparent tray (500 mm long × 300 mm wide) in a thin layer of water. A millimetre grid was placed underneath the tray. The system used to describe the roots conformed with the developmental (centrifugal) segment-ordering system (Berntson 1997). To characterize the main axis and its first- and second-order laterals (third-order laterals were rare for all species), the main axis was divided into a sequence of segments (generally 50 mm long). The following parameters were then determined on the central subsegments (generally 20 mm long): (i) the diameter of the main axis; (ii) the total number of first-order lateral roots; (iii) the average length and diameter of four individual first-order lateral roots; (iv) the total number of second-order lateral roots on a representative first-order lateral; and (v) the average length and diameter of four second-order lateral roots. These measurements on root diameters were made (to ± 20 µm) using a stereomicroscope with a graticuled eyepiece. Individual intact roots were also scanned (for protocol see Bouma et al. 2000a) using a flat-bed scanner (HP ScanJet 4c, Hewlett-Packard, USA) with a transparency adapter (HP Transparency Adapter, Hewlett-Packard). The scanned images were used to obtain root diameters on segments of the first-order laterals with a known link magnitude (Fig. 1), using winrhizo software (Regent Instrument Inc., Quebec, Canada).

The measurements on the segments (generally 50 mm long) with their central subsegments (generally 20 mm long) were then used to derive the overall lengths of the main axis and of the first- and second-order laterals, both per segment and for the total root, and to calculate link-based parameters to describe the root topology. The TI of the root was calculated as the ratio of log altitude over log magnitude (details in Fig. 1). Although not necessarily the best index to describe topology (Berntson 1995), it is the most commonly used index in the sparse recent literature on root topology (e.g. Taub & Goldberg 1996; Arrendondo & Johnson 1999), and comparison between different TIs is risky (Berntson 1995).

Statistical analysis

The plants were grown in a complete randomized design. Statistically relevant information, such as the number of replicates, F values, P levels, and regression equations with r2 values, are indicated in the legends to the figures. Differences between species were tested for significance by anova using the Tukey honest significance test for unequal sample sizes (5% significance level). If the homogeneity of variance was found to be significant by the univariate test of Cochran, Hartley and Bartlett, we applied a square root (Fig. 2b,c) or a log (Figs 2a, 3) transformation before performing the anova. anovas were performed using statistica software (StatSoft Inc., Tulsa, OK, USA), and regression analyses were performed in excel (Microsoft Inc.).

image

Figure 3. Topological index (log altitude/log magnitude) for seven halophyte species with habitats of contrasting elevation. Species are sorted and abbreviated as explained in Fig. 2. Significant differences are indicated by letters on top of the bars (F6,40 = 5·12; P < 0·01).

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Results

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References

Root architecture and elevation

In all species, lateral roots contributed more to total root length than the main axes (main axes <15% overall root length; Fig. 2a). The relative importance of the lateral roots increased with increasing elevation for the Chenopodiaceae, but not for the grasses. Species from habitats with relatively infrequent inundation (high elevations) tended to grow longer laterals than those from more frequently inundated elevations (low elevations; Fig. 2b). Although the mean length of the laterals tended to be longer in Elymus than in Spartina (Fig. 2b), the relative contribution of the main axis to total root length was the same for both (Fig. 2a), because of significantly greater branch density in Spartina than in Elymus (Fig. 2c; F6,40 = 10·47; P < 0·01). The branch density of the grasses did not show a relationship with elevation, whereas for the Chenopodiaceae the branch density of the first-order laterals tended to increase with increasing elevation (Fig. 2c).

The TI of the Chenopodiaceae decreased with increasing elevation (Fig. 3; F6,40 = 5·12; P < 0·01). To some extent, this supports our first hypothesis. For the grasses, however, we found no relation between TI and elevation (Fig. 3). In contrast to our first hypothesis, their TI was within the same range as that of the Chenopodiaceae, indicating that these grasses have more second-order laterals than expected.

Root diameters and topology

In contrast to our second hypothesis, the diameter of the main axes and the diameter of the first-order laterals did not increase with increasing magnitude (Fig. 4). This was the case regardless of the TI of the root system, despite our hypothesis that the herringbone-structured roots, in particular, would increase in diameter towards the root base. Within the seven species that we studied, the only exception was Atriplex hastata, where a few thick basal root segments with an exceptionally high magnitude resulted in a negligible increase of the diameter with magnitude (DAth = 0·10MAth + 647; P < 0·01; r2 = 0·48; n = 36). We observed no strong relationship between diameters at the base of the main axis (Dbase), or the ratio between the diameter at the base of the main axis and the minimum root diameter (Dbase/Dmin) with the total number of links within the root system (Fig. 5). The regression between Dbase/Dmin and the total number of links (TNL) could only explain one-fifth of the variation (Dbase/Dmin = 0·29 TNL; P < 0·01; r2 = 0·20; n = 45). If an individual root of a given branching order was relatively coarse or thin compared to the species average, it remained coarse or thin over its whole length, regardless of the number of laterals. A slight increase in diameter (D;µm) with magnitude (M) was found when combining main axes, first- and second-order laterals: DSal = 1·03MSal + 285 (P < 0·01; r2 = 0·10; n = 76); DSpa = 0·69MSpa + 376 (P < 0·01; r2 = 0·40; n = 135); DPuc = 0·66MPuc + 255 (P < 0·01; r2 = 0·19; n = 144); DSua = 0·56MSua + 305 (P < 0·01; r2 = 0·25; n = 146); DEly = 0·43MEly + 400 (P = 0·01; r2 = 0·04; n = 164); DAth = 0·16MAth + 379 (P < 0·01; r2 = 0·48; n = 155); DAtl = 0·60MAtl + 372 (P < 0·01; r2 = 0·29; n = 132); subscripts indicate species. This may be explained by the inherently higher magnitude of segments of the main axes than those of the first- and second-order laterals (Fig. 6), combined with the strong correlation between root order and root diameter (Fig. 7). The diameter of the second-order laterals was approximately half that of the first-order lateral (DI2 = 0·51DI1; P < 0·01; r2 = 0·51; n = 44), whereas the diameter of the first-order laterals was approximately one-third of that of the main axis (DI1 = 0·32DI0; P < 0·01; r2 = 0·46; n = 47). Furthermore, if the main axis of an individual intact root was relatively coarse or thin compared to the species average, the first- and second-order laterals of that individual intact root were generally also coarser or thinner than the average (Fig. 7). Despite the clear correlations that underlie the trend between diameter and magnitude observed when all branching orders were combined, the increase of diameter with magnitude remained relatively small. The latter is because root segments of a specific branching order have quite constant diameters, even though they may differ widely in magnitude.

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Figure 4. Relationship between magnitude and average diameter of segments of the main axis (a) and first-order laterals (b). No such relationship could be plotted for the second-order laterals as their magnitude is always 1 due to the absence of third-order laterals. To enhance clarity of (b), we only indicated the average diameter per species for segments of equal magnitude. Species abbreviations as in Fig. 2.

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image

Figure 5. The relationship between (a) diameter at the base of the main axis and (b) the ratio between that basal diameter and the minimum root diameter, with the total number of links. Species are abbreviated as explained in Fig. 2. The regression between Dbase/Dmin and the total number of links (TNL) could only explain one-fifth of the variation (log [Dbase/Dmin] = 0·29 log TNL; P < 0·01; r2 = 0·20; n = 45). By definition, the line originates from point 1,1, as Dbase/Dmin = 1 where a root consists of one link only. Based on the relationship between root diameters of different orders (Fig. 7), the expected value for Dbase/Dmin would be ≈6.

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image

Figure 6. The (auto-)correlation between the mean (±SE) magnitude of a segment of the main axes, and that of a segment of a first-order lateral. By definition, the magnitudes of segments of the main axes exceed those of segments of the first-order laterals. Species abbreviations as in Fig. 2.

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image

Figure 7. Relationship between root diameter of (a) the main axis and first-order laterals (DI1 = 0·32DI0; P < 0·01; r2 = 0·46; n = 47) and (b) the first- and second-order laterals (DI2 = 0·51DI1; P < 0·01; r2 = 0·51; n = 44). Species abbreviations as in Fig. 2. Solid lines indicate regression equations.

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The TI was well correlated with relative root length in the different orders of laterals (Fig. 8a; P < 0·01; r2 > 0·7; n = 47), which illustrates the relevance of describing root branching in this manner. There was a weak but significant tendency for the diameter at the base of the main axis to decrease in both Chenopodiaceae and Gramineae, with increasing TI (Droot base = −1585TI + 2044; P < 0·01; r2 = 0·23; n = 47; Fig. 8b). Our observations thus refute the hypothesis that root diameter increases with increasing magnitude and increasing TI.

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Figure 8. Relationship between (a) topological index and relative contribution of different branching orders to total root length; and (b) topological index and diameter at the base of the main axis. (a) Circles and triangles indicate Chenopodiaceae and Gramineae, respectively. Black, grey and white symbols represent the main root, first- and second-order laterals. All relations were highly significant (P < 0·0001): RLmain root = −23TI + 37 (r2 = 0·74; n = 47), RLfirst-order root= 84/{1 + e[−(TI − 0·71) / 0·076]} (r2 = 0·79; n = 47) and RLsecond-order root = 1·03 + 814TI − 1598TI2 + 784TI3 (r2 = 0·87; n = 47). (b) Species abbreviations as in Fig. 2. A regression could explain about a quarter of the total variation (Droot base =−1585TI + 2044; P < 0·01; r2 = 0·23; n = 47).

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Discussion

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References

Root topology and elevation

Species from the high, nutrient-limited marsh benefit in theory from root systems that allow for rapid acquisition of nutrients that become available throughout the soil. Dichotomously and randomly branched root systems (TI < 1) have theoretically greater capacity to acquire nutrients than do herringbone-like root systems (TI = 1). Hence, the relatively small TIs of Chenopodiaceae from high elevations (Fig. 3) contribute to their potential competitiveness in that nutrient-limited habitat. These TIs (Fig. 3) fitted well within the range observed on other dicots with a fast relative growth rate (Taub & Goldberg 1996). The smaller TIs observed by Fitter & Stickland (1991) on 13 dicot species may be explained by methodological differences. Fitter & Stickland (1991) calculated the TI based on the whole root system of relatively small plants, whereas both the study of Taub & Goldberg (1996) and ours analysed one axis for each of the larger plants. Herringbone roots may aid survival in anoxic sediments of the low marsh, by minimizing oxygen leakage and exposure to phytotoxins, while remaining advantageous in environments where nutrient mobility is high, as is probably the case at the lowest (wettest) parts of the marsh. The herringbone-like root topology of Chenopodiaceae from low elevations (high TI; Fig. 3) thus contributes to their potential competitiveness at low elevations.

Based on the general trends in root topology (Fitter & Stickland 1991; Taub & Goldberg 1996), we expected a high TI for all grasses, regardless of elevation. For two of the three grass species we studied, the TI was similar to that of the Chenopodiaceae from high elevations (Fig. 3). Although these indices are still comparable to that observed for other grass species (Fitter & Stickland 1991; Taub & Goldberg 1996), they are more an exception than the rule. The somewhat smaller values that we observed could be due to the ‘larger’ roots that we examined (magnitudes of up to 2500 versus magnitudes of less than 60). Fitter (1987) indicated that TI decreases from high to low values at magnitudes around 20–50. We chose, however, to study roots of a ‘normal’ length, as it is only for a brief period that roots with a magnitude <60 are relevant to the competitive interactions of the species we studied. For example, ignoring all second-order laterals, a magnitude of 60 represents a main axis of <10 cm for Spartina (branch density first-order laterals = 6·5 cm−1; Fig. 2a) and a main axis of <20 cm for Elymus (branch density first-order laterals = 3·5 cm−1; Fig. 2a). In general, more data on ‘large’ root systems and size effects are needed regarding the size effect on the trade-off between efficiency and the potential of exploitation (Berntson 1994).

As the root topology of the Chenopodiaceae is related to elevation, but that of the grasses is not, we conclude that topology is not necessarily an important adaptive trait in all plant families that inhabit the salt marsh. This conclusion is further supported by the finding that the length of the second-order laterals was short in all species (Fig. 2b). By definition, herringbone-like roots lack second-order laterals (Fig. 1). The appearance of root systems will thus resemble that of a herringbone-like root if second-order laterals are very short. Nevertheless, those very short second-order laterals will lower the TI significantly (Fig. 3). Short lateral roots may be an adaptation to aid aeration of the root tips under inundated conditions, but may as well be the result of limited oxygen supply preventing the roots from growing longer. In addition to water, nutrient and assimilate transport, species from low areas of the marsh also require oxygen transport towards root tips, a requirement that may limit root length (Sorrell 1994). Apart from morphological adaptations such as aerenchyma formation (Blom & Voesenek 1996; Justin & Armstrong 1987), a trend towards relatively short lateral roots at low elevations seems a valuable architectural adaptation to anoxic and hypoxic soils. In rice (Ota 1970) and Rumex species (Visser et al. 1996), water-logging reduces the development of lateral roots. Within Spartina anglica, Puccinellia maritima and Elymus pycnanthus, however, we observed only a limited plasticity in lateral length upon flooding (Bouma et al. 2000b). Among the species that we studied, those from the lower elevations tended to have shorter first-order laterals (Fig. 2b), and the relative contribution of the main axis to the total root length was greater for Chenopodiaceae from lower elevations (Fig. 2a). The second-order laterals were short in all species (Fig. 2b).

Root diameter and elevation

Theoretically, a maximum specific root length [SRL; m root (g root)−1] will maximize the water and nutrient acquisition per unit carbon invested. However, the minimum root diameter may be limited by demands for maximum root length of the main axes or attached laterals, soil impedance, defence against grazing and pathogens, and root aeration (Eissenstat 1992; Eissenstat 1997; Fitter 1987; Spek & Van Noordwijk 1994; Van Noordwijk et al. 1994). The average root diameters of the highest order of laterals from Spartina, Puccinellia and Elymus (Fig. 7b) matched those for other soil-grown Graminoids (100–250 µm; Eissenstat 1992). The requirement for oxygen transport through the roots of species from the low part of the marsh (e.g. Spartina) has not resulted in particularly large fine-root diameters. An earlier study showed no effect of flooding on root diameters of Spartina anglica, Puccinellia maritima or Elymus pycnanthus (Bouma et al. 2000b); this has not yet been studied for the Chenopodiaceae included in the present study. This is in contrast to findings for Rumex, where the most flood-resistant species had roots with the largest diameter, and produced the thickest adventitious root in response to flooding (Visser et al. 1996).

Root diameter relations

The pipestem model or constant squared diameter rule states that the cross-sectional area of a main stem is equal to the sum of the cross-sectional area of all tree branches (Leonardo da Vinci, as cited by Mandelbrot 1983). Combining this rule with the theory on root topology, Van Noordwijk et al. (1994) predicted a linear relation between the total number of links and the ratio between the diameter at the base of the main axis and the minimum root diameter (Dbase/Dmin). This relationship is also expected for complex branching patterns, such as allotomous proportionate branching with unequal branches (Spek & van Noordwijk 1994). Our observations showed the expected relationship to be just insignificant (Fig. 5). Instead, we found much stronger relationships indicating that, on average, the diameter of the first-order root is approximately one-third that of the main axes, and the diameter of the second-order laterals is approximately half that of the first-order roots (Fig. 7). We expect these relationships to be relevant for the capacity of root systems to supply water and nutrients towards other plant tissues.

According to the Hagen–Poiseuille equation, total flow is proportional to the fourth power of the diameter of a cylinder (Vogel 1989). By approximation, one main axis would have a similar flow capacity to 95 ([1/0·32]4) first-order laterals with 0·32 times the diameter of that main axis, defining flow capacity as the maximum flow that may be expected based on root diameter only. Similarly, one first-order lateral would have a similar flow capacity to 15 second-order laterals. In long roots, the overall flow capacity of all first-order laterals can thus exceed that of the main axis, and that of all second-order laterals can exceed that of the first-order laterals. This indicates that there is a need for over capacity in laterals to explore the soil. For example, water uptake is generally limited to the roots in the highest soil layers where water can be obtained. This need not be the same place where nutrient uptake occurs, or where water will be available later on. It is, however, also clear that the root systems studied follow, to some extent, a pipestem model for flow capacity, as the root diameters of the main axes have a weak but significant tendency to increase with decreasing TI (most branched; Fig. 8). We expect the pipestem model to work best for large plants with woody roots.

Root diameters and magnitude

In contrast to our hypothesis and the assumptions underlying the efficiency calculations of Fitter (1987) and Fitter et al. (1991), we did not find a strong relationship between root diameter and link magnitude (Fig. 4). For example, the large differences in magnitude that occur over small distances along the main axis of a large root system were not reflected in differences in diameter. Only by combining all diameters of the main axis and the first- and second-order laterals, we found that the diameter increased between 0·16 and 1·03 µm per magnitude. This is, however, much less than the 1–8 µm per magnitude suggested by Fitter (1991). Root order (Fig. 7) was more important for the diameter than the magnitude of a link (Fig. 4). Our findings illustrate the value of using the developmental segment-ordering system.

Herringbone root systems were predicted to be relatively costly because of their relatively large mean root diameters (Fitter 1987; Fitter et al. 1991). In species where there is no relationship between root diameter and link magnitude, the predicted high costs associated with herringbone root systems disappear. In such species, herringbone architecture may be assumed to have an advantage over dichotomous branching, as the former minimizes inter-root competition. So, Taub & Goldberg (1996) hypothesized that the diameter (i.e. costs) of grass roots was relatively independent of link magnitude, because they found herringbone root systems in all the grasses they studied. This contention is supported by our findings on the three Gramineae that we studied. The question remains, however, why the Chenopodiaceae (dicots) that we studied, did not have a perfect herringbone-like root system in the absence of a relationship between root diameter and link magnitude. There are two important factors in answering this question. First, the appearance of the root systems of most of the species that we studied resembles that of a herringbone-like root, owing to the short length of the second-order laterals (Fig. 2b). Secondly, there is a trade-off between efficiency and potential of exploitation (Berntson 1994). As discussed in relation to the pipestem model and the Hagen–Poiseuille equation, there are other indications (cf. Berntson 1994) that suggest need for some over-capacity in laterals, to allow a plant to explore the soil.

Root diameter may not always be affected by the magnitude of individual links. This is an important observation regarding the sensitivity of simulating the exploitation efficiency of contrasting root topologies for the rate at which the root diameter changes with magnitude (Fitter 1987; Fitter et al. 1991). However, we studied only a few nonwoody dicots and monocots from one ecosystem. A broader survey is needed to establish how common the (lack of a) relationship between magnitude and diameter is. The theoretically predicted relationship may hold better for large plants of perennials and woody species.

Conclusions

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References

Our study clarifies the relationship between (i) the architectural traits of root systems of seven halophytic species and habitat elevation, and between (ii) root topology, link magnitude and root diameter. Our results illustrate that the previously assumed relationship between root diameter and link magnitude is incorrect for these species. We observed a clear relation between the diameter of the main axis and the first- and second-order laterals for all species. The Chenopodiaceae showed a clear relationship between TI and elevation. Dichotomous branching at high elevations allows for rapid acquisition of nutrients which contribute to their potential competitiveness in that nutrient-limited habitat. Herringbone roots may aid survival at low elevations, as a minimal root length helps in minimizing oxygen leakage and exposure to phytotoxins. In contrast, the Gramineae showed no such relationship. Thus root topology is not necessarily an important adaptive trait in all plant families that inhabit the salt marsh; other traits may compensate for a root topology that deviates from what may theoretically be expected. In the species we studied, the length of individual first-order laterals tended to increase for those with habitats at relatively high elevations. The length of the second-order laterals was short in all species, regardless of their habitat.

Acknowledgements

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References

We thank G.M. Berntson, A.H. Fitter, A.H.L. Huiskes and P. Kamermans for their valuable and constructive comments on previous drafts of this paper. Scotts Europe BV is gratefully acknowledged for supplying Osmocote slow-release fertilizer.

References

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
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Received 9 May 2000; accepted 11 December 2000