Journal of Experimental Botany, Vol. 51, No. 349, pp. 1449-1457,
August 2000
© 2000 Oxford University Press
Original Papers |
Effect of nitrogen supply and defoliation on loss of organic compounds from roots of Festuca rubra
Plants Group, The Macaulay Land Use Research Institute, Craigiebuckler, Aberdeen AB15 8QH, Scotland, UK
Received 14 January 2000; Accepted 11 May 2000
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Abstract |
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The aim of this study was to determine the effects of N-supply and defoliation on rhizodeposition from Festuca rubra, in the context of whole-plant C- partitioning and root morphology. Plants were grown for 36 d in axenic sand microcosms continuously percolated with nutrient solutions of either high or low N concentration (2 mM or 0.01 mM NH4NO3, respectively). The effects of partial defoliation at weekly intervals were determined at high and low N. At low N, dry matter accumulation in roots and shoots was reduced significantly (P<0.001), with proportionately increased partitioning to roots, in comparison with the high N treatment. Root morphology was also affected by N-treatment; at low N, lower biomass production was offset by increased specific root length (P<0.001), reducing the magnitude of the significant (P=0.002) increase in total root length at high N. Cumulative release of organic C from roots of F. rubra over the experimental period was not altered significantly by N-treatment. However, as a proportion of net C-assimilation, rhizodeposition was significantly (P<0.001) greater at low N than at high N. Defoliation transiently (3–5 d) increased the release of soluble organic compounds from roots at each N-supply rate, and increased significantly (P<0.001) cumulative rhizodeposition over the experimental period. These effects of N-supply and defoliation on rhizodeposition are of importance in understanding interactions between plant and microbial productivity in grazed grasslands, and in interpretation of concurrent effects on microbially driven nutrient cycling processes in these systems.
Key words: Rhizodeposition, defoliation, N-supply, Festuca rubra.
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Introduction |
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In the absence of ferilizer additions, the productivity of temperate grasslands is commonly limited by the availability of mineral nutrients, predominantly N or P. The rate of cycling of these elements is therefore critical in determining fluxes to plant-available pools. These processes are driven by soil microbial communities, whose growth and activity is most commonly restricted by the availability of organic C-sources in soil. Since the major source of organic matter in soil is from plant primary production, entering soil as litter-fall, root turnover and rhizodeposition, there is a tight coupling between plant and microbial productivity. This coupling is manifested in there being a close relationship between plant and microbial biomass (Myrold et al., 1989
; Tracy and Frank, 1998), particularly where N limits plant growth (Frederick and Klein, 1994). Plant species is a strong determinant of the associated rhizosphere microbial community structure, with the quality of C-input from roots implicated as the greatest controlling factor (Westover et al., 1997; Grayston et al., 1998). Moreover, these relationships are apparent at the process level, with rates of mineral nutrient transformations closely linked to plant C-inputs to soil (Hungate et al., 1997; Hall et al., 1998).
Where water is not a limiting resource, antecedent nutrient availability and distribution are strong determinants of plant investment in root production, and of root topology (Fitter, 1994). In soils where availability of mineral N is low, relative investment to below-ground biomass is greater, and roots tend to be finer and less branched than those in more fertile soils (Fitter, 1985). This strategy is thought to facilitate construction-efficient soil exploration, with the trade-off that fine roots have a higher relative maintenance requirement (Fitter, 1987). This has implications for C-input to soil as rhizodeposition has been found to correlate more closely with root length than with root biomass (Xu and Juma, 1994). In grazed grasslands, plant C-partitioning is affected predominantly by interactions with the grazing animal. Soil nutrient distribution is temporally and spatially heterogeneous as a consequence of dung and urine returns, which in turn affect plant partitioning and root development. Removal of above-ground biomass during grazing is also a strong determinant of subsequent partitioning. Grasses tolerate defoliation through preferential allocation of assimilate, and remobilization of C and N storage compounds (from leaf blades, crowns and roots) to support recovery of photosynthetic capacity (Johansson, 1993). In addition, total root biomass and length have been reported to be less for heavily grazed swards, as a consequence of reduced rates of root extension and/or altered root demography (Arredondo and Johnson, 1999).
Although effects of N-supply and defoliation on plant C-partitioning and physiological processes are becoming increasing well understood (Richards, 1993), quantification of C-inputs to soil, and interactions with the microbial biomass and nutrient cycling limit our understanding of the coupling between plant and microbial productivity. In this context, rhizodeposition is of central importance, as it supplies readily utilizable substrate to microbial communities in the rhizosphere, supporting elevated growth, activity and nutrient cycling around roots. However, the necessary understanding of how release of organic C from roots is affected by factors prevalent in grazed ecosystems is lacking (Bardgett et al., 1998).
The importance of defoliation in increasing C-flow from roots to soil has been inferred from studies in grasslands which found strong correlations between grazing intensity and the growth and activity of soil microbial communities (Bardgett and Leemans, 1995; Bardgett et al., 1997). However, it is uncertain to what extent these effects are a consequence of shifts in quantity and/or quality of rhizodeposition, altered root demography or secondary effects of the grazing animal. However, Bardgett et al. have also demonstrated shifts from fungally dominated to bacterially dominated microbial communities under grassland subjected to increasing grazing intensity, which is interpreted to be a consequence of increased release of readily utilizable C-compounds (Bardgett et al., 1996). This interpretation is supported by the few studies which have investigated effects of clipping or insect grazing on exudation of soluble organic compounds from roots(Hamlen et al., 1972; Bokhari and Singh, 1974; Holland et al., 1996). The mechanism by which increased exudation in response to defoliation occurs is uncertain, although it has been suggested that it is associated with increased partitioning of carbohydrates to roots, as a means of grazing tolerance (Holland et al., 1996; Bardgett et al., 1998). For grasses, this hypothesis seems unlikely as it has been demonstrated that defoliation results in reduced carbohydrate content in roots (Prud'homme et al., 1992; Morvan-Bertrand et al., 1999), as a consequence of reduced allocation of assimilate below ground and utilization of reserves to support root maintenance (Donaghy and Fulkerson, 1997). Consequently, it is timely to consider efflux of organic C from grasses, in the context of whole-plant responses to defoliation, to improve the understanding of factors mediating C-flux into grazed grassland systems.
A previous work (Paterson and Sim, 1999), demonstrated increased rhizodeposition from roots of Lolium perenne in response to defoliation and low N-supply. However, the generality of these responses is uncertain. Assimilate allocation and root morphological responses to defoliation and N-supply vary considerably between grass species (Arredondo and Johnson, 1999), and it is probable that effects on rhizodeposition will also be species-specific. In particular, faster growing species differ from slower growers (e.g. Lolium species cf. Festuca species) in relation to the rate of recovery of root function following defoliation (Thornton and Millard, 1996), and this may be important in mediating the response of rhizodeposition to defoliation.
The aim of this study was to test the hypothesis that defoliation increases rhizodeposition from Festuca rubra, and to assess the influence of N-supply on this process, in the context of whole-plant C-partitioning and root growth responses.
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Materials and methods |
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Seed sterilization and germination
Seeds of F. rubra were surface-sterilized in 0.5% (v/v) peracetic acid for 15 min, as described previously (Paterson and Sim, 1999
). The sterilized seeds were transferred aseptically to glass Petri dishes containing sterile moist sand and germinated in the dark at 20 °C. After 4 d (sufficient for root emergence) the seeds were transferred to a light-bench (16 h daylength with a PAR of 450 µmol m-2 s-1, 20 °C) for 4 d prior to planting in the microcosms. A subsample of the sterilized seed was placed onto Petri dishes containing plate count agar (PCA), and incubated at 20 °C for 8 d to confirm sterility of the seed.
Microcosms and growth conditions
The design of the axenic microcosm system has been described previously (Hodge et al., 1996). The modifications adopted to eliminate extraneous C sources from the microcosm assembly and supply tubing (described by Paterson and Sim, 1999) were applied in this study. However, in this case organic C was removed from the sand by muffle furnace (700 °C for 8 h), following an initial wash to remove particulate material.
The assembled microcosms and tubing were autoclaved (121 °C for 20 min) in sealed bags, after first wetting the sand matrix to optimize sterilization. Prior to planting, the sand matrices were percolated (60 cm3 d-1) for 14 d with 0.25 strength Hoagland's nutrient solution (Hoagland and Arnon, 1950), modified to contain either 2 mM or 0.01 mM NH4NO3, designated ‘high N’ and ‘low N’, respectively. Twelve replicate microcosms for each N-treatment were used. The leaching period allowed complete wetting of the sand matrix and testing of microcosm sterility (dilution plating of leachate samples onto PCA).
Experimental period
Seedlings (three per microcosm) were transferred aseptically through the lower port in the top chamber of the microcosms, and planted into the sand. The microcosms were then transferred to a controlled environment room (Conviron®, Winnipeg, Canada), that was set for a 14 h daylength with a PAR of 700 µmol m-2 s-1 at plant level and a constant relative humidity of 50%. Plant growth temperature was maintained at 20 °C for both light and dark periods. Radiative heat generated in the glass microcosms necessitated that the environment room temperature be set to 6 °C during the light period. The delivery rate of the nutrient solutions was reduced to 45 cm3 d-1 after planting, and maintained at this lower rate for the 36 d duration of the experiment. Three days after planting and continuously thereafter, air from within the growth room was pumped through the top chamber of each microcosm after passing through a 0.2 µm filter to maintain sterility, flow rate was adjusted to 60–80 cm3 min-1. Nutrient solution which had percolated through the sand matrices was collected every 2–3 d by generating negative pressures in acid-washed sterile glass collection vessels connected to the bottom chamber of the microcosms. Sterility of the microcosms during sampling was maintained by use of a 3-way Leur-lock, which was closed to isolate the microcosm except during sample collection. Sample volume was determined gravimetrically and an aliquot dispensed for pH determination. The remainder was stored at -18 °C prior to total organic carbon (TOC) and mineral N determinations.
For application of defoliation treatments, six of the microcosms from each of the N treatments were transferred to a laminar air-flow cabinet, without disconnecting the nutrient supply lines. The top chamber was connected to an air pump to maintain positive pressure within the chamber and the lower port removed to allow access to the plants. Scissors were flamed with ethanol and used to defoliate to an even height of 4 cm, shoot fragments were removed with flamed forceps. Plants were defoliated 14, 21, 28, and 35 d after planting (DAP). At harvest, defoliation to a constant height of 4 cm resulted in removal of approximately 30% and 20% of leaf blade area, for the high and low N treatments, respectively.
Re-uptake assay
At the mid-point of the light period 33 DAP (3 d prior to harvest), 250 kBq of 14C-glucose (0.14 µmol C), in 1 cm3 sterile deionized water, was injected into the nutrient supply line of each microcosm. A soda lime trap was connected to the air-outflow line of each microcosm to collect respired 14CO2. The 14C content of subsequent percolated nutrient solution collections was determined by liquid scintillation counting. Following harvest (see below), the 14C-content of the sand, roots, shoot and soda lime trap were determined by dry combustion (Harvey Biological Oxidiser OX400, RJ Harvey, New Jersey) and trapping in 20 cm3 of scintillation cocktail (5 g l-1 Permablend (Packard, Canberra) in a solution of toluene/ Carbosorb (Packard, Canberra) (4 : 1, v/v).
Harvest and analysis
All of the microcosms were harvested 36 DAP. The top chamber was removed in a fume hood and allowed to vent for 1 min to remove any 14CO2 present, the plants were then excised at the sand surface. The shoot material was transferred to an oven at 70 °C where it was stored until it attained a constant weight (minimum 4 d). The root material with closely adhering sand was removed, and the adhering sand was washed off in a measured volume of deionized water (25–50 cm3 dependent on the size of the root system). The washing solution was then passed through glass wool to remove particulate material, a 5 cm3 aliquot dispensed and 14C content determined by liquid scintillation counting. The remaining solution was stored at -18 °C prior to TOC analysis. Total root length of the washed material was determined on a root scanner (Comair–Commonwealth Aircraft Corporation Ltd., Port Melbourne, Australia) after first cutting the root system into 2 cm lengths and spreading these fragments out. The root material was then dried at 70 °C until it reached a constant weight. The remaining ‘bulk sand’ was washed with 100 cm3 of deionized water, and the washing solution passed through glass wool. A 5 cm3 aliquot was dispensed for liquid scintillation counting and the remainder stored at -18 °C prior to TOC analysis. The sand, both that which had been adhering to the root and ‘bulk sand’, was dried at 70 °C.
The dried plant material was weighed and then ground finely using a ball mill. A 5 g fraction of each sand sample was also ground. The dried and ground samples were then used to determine: (1) 14C contents by dry combustion and (2) C and N content (CHN analyser, Carlo Erba Strumentazione, Milan, Italy). All washings and percolated nutrient solutions were analysed using a Total Organic Carbon Analyser (model 700, Corporation College Station, Texas) for TOC.
Mean daily plant 
and 
depletions of the percolated nutrient solution were determined on single samples (those also used for TOC determinations) throughout the experimental period. Colorometric assays of and concentrations were determined with an autoanalyser (Technicon Traaks 800). Nitrate in solution was reduced to nitrite with hydrazine and reacted with sulphanilamide, adsorbance was measured at 520 nm. Ammonium in solution was reacted with salicylate using nitroprusside as a catalyst, adsorbance was measured at 660 nm.
Statistics
Two-way analysis of variance (ANOVA) was used to determine the statistical significance of treatment effects, and to establish whether there were significant interactions between nitrogen and defoliation treatments. Prior to ANOVA, mean plant weights were transformed to their natural logarithms to account for standard deviations proportional to the means. Means for 14C partitioning between pools were transformed using arcsine as a function prior to analysis, to account for percentage distributions. The significance of differences between individual means was determined at the 5% level by applying a Tukey test.
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Results |
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Pre-planting tests indicated that percolated nutrient solution contained no culturable microbial contaminants and that the total organic carbon (TOC) was less than 1 mg l-1 (results not shown), providing a suitably low background against which to detect root-derived C.
Plant growth and partitioning
N-treatment strongly affected dry matter accumulation and partitioning in F. rubra. Shoot and root weights were increased significantly (P<0.001) at ‘high N’ (Table 1), concurrent with a shift in root weight ratio (RWR), from 0.15 at high N to 0.57 at low N, for non-defoliated plants. Therefore, although low N reduced root production, allocation to roots increased as a proportion of the whole-plant C-budget. High N also increased (P<0.002) total root length, although this was offset by a significant increase in specific root length (SRL) at low N (Table 1). Tissue N concentrations were reduced significantly (P<0.001) at low N, for both shoots and roots.
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Defoliation was found to affect root weight and total root length, reducing significantly (P<0.05) these parameters with both N-treatments (Table 1
). Defoliation did not significantly affect SRL in this study. Over the period of the experiment, at high N, defoliation was found to reduce significantly (P=0.011) root nitrate uptake (per microcosm) from the percolated solution (Fig. 1). No significant effects of defoliation on mineral N uptake were observed with low N supply.
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Release of organic C from roots
Cumulative release of organic C from roots of F. rubra over the whole experimental period was increased significantly (P<0.001) in defoliated treatments (Table 2). This increase in net loss of organic C from roots was a consequence of large increases in rhizodeposition (3–5 d duration) following defoliation events, at both high and low N-supply (Figs 2, 3). Despite greater root biomass at high N, release of organic C from roots was not increased significantly. Indeed, when root-released C is expressed as a percentage of plant net assimilate (Table 2), rhizodeposition constitutes a significantly (P<0.001) increased proportion of the plant C-budget at low N.
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N-treatment and defoliation (Table 2
) affected the fate of 14C supplied as 14C-glucose in the nutrient solution (to assess re-uptake processes). Total uptake of 14C by F. rubra was reduced at low N (P<0.001). The fate of assimilated 14C was affected by both N-treatment and defoliation, with greatly reduced (P<0.001) allocation to shoots at low N, allocation to shoots was reduced further (P<0.02) with imposition of defoliation (Table 2).
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Discussion |
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The response of the growth of F. rubra to low N-supply is consistent with plasticity of biomass allocation to optimize the balance between C-assimilation and N-acquisition (Marschner et al., 1996
). This attribute is considered to be advantageous, particularly in soils with relatively low and heterogeneous nutrient supply. The reduced biomass accumulation and markedly lower tissue N concentrations at low N (Table 1) are consistent with strong N-limitation, also evident from the high depletion (c. 75% of that applied) of and from the nutrient solution (Fig. 1). The increase in SRL to low N has also been observed for roots in low nutrient environments, and is considered to maximize the efficiency of root foraging for scarce nutrients (Fitter, 1985).
Defoliation was found to reduce root biomass accumulation and also total root length, at both high and low N (Table 1). This response has been found previously for grasses, and is a consequence of priority allocation of assimilate and reserves to support regrowth of photosynthetic tissues (Richards, 1993; Donaghy and Fulkerson, 1998). Defoliation has been found to reduce rates of root extension, and with increasing severity also results in elevated rates of root death (Jarvis and Macduff, 1989). However, these responses are species-dependent (Arredondo and Johnson, 1999). Indeed, in a previous study under directly comparable conditions with Lolium perenne, root biomass and total root length were found to be insensitive to defoliation (Paterson and Sim, 1999). Effects of defoliation on root growth are thought to be mediated by whole-plant C-status (Donaghy and Fulkerson, 1997, 1998) with restoration of root extension only occurring on re-establishment of a positive daily C-balance (Clement et al., 1978). In turn, above-ground compensatory responses to restore photosynthetic capacity following defoliation in a short-grass species, have been found to be dependent on tissue N concentrations (Hamilton et al., 1998). At high tissue N concentrations (reflecting high soil mineral N concentrations), compensatory responses of short-grass species increased the rapidity of recovery from defoliation (Hamilton et al., 1998). However, in this study there was no evidence for increased shoot production at high N following defoliation (Table 1). Indeed, although there was an apparent significant (P=0.035) interaction between N-supply and defoliation on shoot biomass production, this was for reduced growth depression at low N as a consequence of defoliation. In this instance, it is likely that this effect was a consequence of the lower percentage shoot removal at low N, due to the lower growth at low N and defoliation to a constant height in each N-treatment. Interactive effects of N-supply and defoliation were not found with respect to release of organic C from roots, or for measured plant growth parameters (Tables 1, 2).
Nitrogen supply did not affect the total cumulative release of organic C from roots of F. rubra, despite greatly increased plant biomass accumulation at high N (Table 2). However, when expressed as a proportion of net plant C-assimilation, rhizodeposition was significantly greater (c. x10) from non-defoliated plants at low N than at high N. This finding is consistent with previous studies reporting effects of N-supply on organic C release from roots (Bowen, 1969; Hodge et al., 1996). Paterson and Sim suggested that proportionately increased rhizodeposition from L. perenne at low N was correlated with production of a finer root network, quantified by increased SRL (Paterson and Sim, 1999). In the present study, proportionately increased rhizodeposition from F. rubra at low N was again coincident with increases in SRL. However, more work is required to factor confounding effects of N-supply on plant physiological processes and on morphological adaptations, in relation to understanding impacts on C-flow from roots.
Defoliation of F. rubra consistently resulted in increased release of organic C from roots at each N-supply following each defoliation event. Increased rhizodeposition was transient, returning to baseline levels within 3–5 d (Figs 2, 3). On the basis that microbial communities under grazed swards are more active and bacterially dominated than those under ungrazed swards, it has been hypothesized that rhizodeposition increases in response to defoliation (Bardgett et al., 1998). The results of this study and a previous one with L. perenne (Paterson and Sim, 1999) support this hypothesis, indicating that (under axenic conditions) two perennial grass species’ consistently increase soluble rhizodeposition following defoliation. The soluble component of rhizodeposition is derived primarily from diffusive release of root metabolites (in greatest part; sugars, organic acids and amino acids), that are readily utilized as substrates by microorganisms (Mühling et al., 1993; Jones and Darrah, 1994). Increased rates of release of such substrates, would favour relatively copiotrophic organisms, consistent with the shift to more active, bacterially dominated communities reported from field experiments (Bardgett and Leemans, 1995; Bardgett et al., 1996).
At present, the physiological basis for increased rhizodeposition following defoliation is unproven. It has been suggested that it is coincident with increased assimilate allocation to roots, as a means of tolerating further defoliation (Bardgett et al., 1998). However, as discussed, this is not a strategy applicable to the grass species used in this study. Indeed, for most perennial grasses, root soluble carbohydrate concentration declines rapidly following defoliation, as a consequence of reduced assimilate supply and utilization of stored reserves for root maintenance (Prud’homme et al., 1992; Richards, 1993). This reduced carbohydrate status is reflected in suppression of root activity in relation to energy dependent uptake processes. In this study, root uptake of was reduced significantly (P<0.05) following defoliation for F. rubra grown at high N, when defoliation effects were considered across sampling dates (Fig. 1). This is relevant to the release of organic compounds from roots, as the release of sugars and amino acids is known to be balanced by active re-uptake processes (Jones and Darrah, 1993; Mühling et al., 1993). Perturbation of re-uptake, as a consequence of reduced root energy status, would be expected to increase net efflux of root metabolites, consistent with the effects of defoliation reported here.
Plant uptake of applied 14C-glucose was reduced at low N-supply, but unaffected by defoliation (Table 2). This result indicates that defoliation did not reduce uptake of the labelled organic compound, as would have been predicted on the basis of expected effects on root energy status. However, the result should be treated cautiously, as the assay was carried out at the end of the experimental period with a single model rhizodeposit, only. The discrete nature of increased rhizodeposition, and reduced mineral N uptake, following defoliation make it essential in future work to consider C efflux with greater temporal resolution.
The partitioning of 14C taken up by F. rubra from the nutrient solutions was dependent on the treatment imposed on the plant. At high N, a much greater proportion (6–7 times greater) of 14C taken up by the roots was translocated to the shoots (Table 2). This is in accordance with observed effects on whole-plant C-partitioning, where the shoot tissue is the dominant sink for assimilated C. Defoliation also had a significant effect on translocation of root assimilated 14C. However, it was found that defoliation reduced translocation to the shoots (Table 2), which is contrary to the effects of defoliation on whole-plant C-partitioning (i.e. reduced root biomass and length). It is likely that this is a consequence of the route of 14C-uptake, in that 14C in the root will initially be available to support the local energy requirement. This is consistent with utilization of root storage compounds following defoliation, which have been found to be used primarily for root maintenance, with the root remaining a sink for photosynthetically assimilated C (Briske, 1996). It could be argued, therefore, that the reduced translocation of 14C to shoots in the defoliated treatments is supportive evidence for reduced root energy status following defoliation.
In conclusion, these results support the supposition that defoliation of grasses increases C-flux from roots to soil. Nitrogen supply was found to affect gross biomass accumulation and partitioning, with low N-supply also increasing SRL. As a proportion of net plant C-assimilation, rhizodeposition was increased at low N. It is suggested, that as for L. perenne (Paterson and Sim, 1999), production of finer root systems in F. rubra at low N increases the release of organic C. In an ecological context, such increased rhizodeposition at low N may stimulate ‘fast-cycles’ of nutrients through active components of the microbial biomass facilitating increased plant nutrient acquisition.
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Acknowledgments |
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We would like to thank Yvonne Cook who provided
and analyses, and Dr Barry Thornton for helpful comments during preparation of this manuscript. This work was funded by The Scottish Executive Rural Affairs Department. |
Notes |
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1 To whom correspondence should be addressed. Fax: +44 1224 311 556. E\|[hyphen]\|mail\|[colon ]\| eric.paterson{at}mluri.sari.ac.uk
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