The localised effect of granite on root proliferation and dauciform ...

The localised effect of granite on root proliferation and dauciform ...



ong>Theong> ong>localisedong> ong>effectong> ong>ofong> ong>graniteong> on root proliferation and dauciform root

production in Carex caryophyllea and its ong>effectong> on feldspar weathering.


1. Where phosphorus is limiting, some species ong>ofong> the family Cyperaceae have been found to

increase root proliferation and produce dauciform roots in response to ong>localisedong> nutrient


2. Carex caryophyllea plants were grown with different treatment bands to see if the P limitation

response could be initiated by a patch ong>ofong> feldspar-rich ong>graniteong> and if this response

would differ if soil was present in the treatment band.

3. C. caryophyllea produced the greatest root biomass and density ong>ofong> dauciform roots when

grown with a treatment band ong>ofong> mineral and sand. ong>Theong> highest amount ong>ofong> root biomass and

length was allocated to the depth ong>ofong> tube containing the treatment band in all P limited

plants not treated with 10ml P solution per tube once a week.

4. No dauciform roots were produced by plants that were treated with P solution, and there

was no increase in root proliferation in the treatment bands. ong>Theong>re was no significant ong>effectong>

ong>ofong> treatment on shoot dry weight.

5. Etch-pits weathered in the feldspar were detected in tubes containing plants grown with

ong>graniteong> and sand. ong>Theong>se plants produced a high density ong>ofong> dauciform roots and the weathering

is thought to be caused by the high concentration ong>ofong> organic acid exudation from

these roots.


Plants living on nutrient impoverished soils are ong>ofong>ten stress tolerators, well adapted to take up

the limited amount ong>ofong> nutrients available (Grime, 1986). In soils with low phosphorus (P)

concentrations most plants (~ 80%) have mycorrhizal associations to enable uptake ong>ofong> P from

the soil. Those that lack these have other means ong>ofong> increasing uptake, usually involving alterations

in the morphology ong>ofong> their root systems by increased carbon allocation to roots

(Vance et al., 2003), to increase their growth and proliferation. Some plants, e.g. Arabidopsis

thaliana, rely on increasing their root hair density and length in reduced P availability to increase

the surface area ong>ofong> roots available to take up the limited P (Ma et al., 2001). Plants can

also enhance P acquisition biochemically, by modifying the rhizosphere to overcome deficiency

in the soil. ong>Theong> release ong>ofong> hydrogen ions, organic acids and phosphatases increases

plant uptake ong>ofong> phosphorus (Jones, 1998). Organic acids chelate metal cations such as iron,

aluminium and calcium which bind P, causing its desorption by increasing its solubility and

therefore increasing its uptake into plants (Marschner, 1995). Phosphatases, such as phosphomonoesterase

and phosphodiesterase, are produced when P is limited in the soil (Leake &

Miles, 1996) and mineralize organic P converting it into an inorganic form available for plant

uptake (Tarafdar & Jungk, 1987). In P deficient soils, released phosphatases and organic acids

work together to increase the mobility ong>ofong> inorganic P (Neumann et al., 2000).


ong>Theong> development ong>ofong> specialized roots is another way ong>ofong> overcoming P deficiency. Cluster

roots are found in species ong>ofong> Proteaceae and in Lupinus albus, among others, their production

peaking at suboptimal levels ong>ofong> P (Neumann et al., 2000). Cluster roots increase the soil volume

covered by the roots by 300 times more than the same length ong>ofong> a normal root, thus increasing

the surface area ong>ofong> root for carboxylate exudation and subsequent solubilisation ong>ofong>

nutrients and uptake by the plant (Lamont, 2003).

Like Proteaceae species, some sedge species also produce modified roots, called dauciform

roots, in response to phosphorous deficiency. This adaptation is important as they are ong>ofong>ten

found in P limited calcareous soils. ong>Theong>se were first observed by Davies et al. (1973), who

described these roots as short, carrot-shaped branches ong>ofong>f the main roots, with very long and

dense root hairs. ong>Theong>y form mats in the surface layers ong>ofong> the soil, where P inputs are the

greatest from falling litter, and bind soil particles, so they become ensheathed in soil material.

Like cluster roots, the development ong>ofong> dauciform roots shows a lot ong>ofong> plasticity depending on

the availability ong>ofong> phosphorus (Shane et al., 2006). Dauciform root production is caused by

limiting P concentrations (Ballard, 2001). If the availability ong>ofong> phosphorous is increased, it

will be sensed by an increase in the concentration ong>ofong> P in the leaf and the production ong>ofong> dauciform

roots will be suppressed (Shane et al., 2005). This minimizes energy expenditure; the

synthesis ong>ofong> modified roots is not initiated when it is unnecessary. Similarly, the addition ong>ofong> P

causes a decrease in the concentration ong>ofong> phosphatase on the surface the root (Hedley et al,

1983). However in P starvation, phosphatase activity is increased, both by an increase in root

density and by the production ong>ofong> dauciform roots, which have higher levels ong>ofong> phosphatase

activity than the same area ong>ofong> an unmodified root (Ballard, 2001).

ong>Theong> abundance ong>ofong> root hairs and highly branched morphology ong>ofong> dauciform roots enables

them to extract more P from the soil than normal roots, giving an overlap in the areas ong>ofong> soil

each root hair is able to deplete P from, thus allowing a concentrated release ong>ofong> carboxylates

(mainly citric acid) and phosphatases into a particular area. ong>Theong>se are released in a single

pulse at the point ong>ofong> dauciform root maturity (Shane et al., 2006), this may be to overwhelm

microorganisms which can use root exudates as an energy source and allow for increased hydrolysis

ong>ofong> organic P esters to allow P uptake (Playstead et al., 2006).

Johnson (2007) found that certain species ong>ofong> sedge (e.g. Carex caryophyllea and Carex

flacca) are spatially precise in their foraging. When grown in a tube ong>ofong> sand with a band ong>ofong>

soil making up 3% ong>ofong> the total volume ong>ofong> the growth medium, they show a ong>localisedong> increase

in root proliferation and turn on the expression ong>ofong> dauciform roots in the soil patch. He found

that 90% ong>ofong> the total dauciform roots produced were allocated to this small area as was 40%

ong>ofong> the total root biomass. This is a response to the P present in small quantities in the soil but

absent in the sand. ong>Theong>y are able to sense the environment before producing dauciform roots

and releasing exudates.

ong>Theong> aim ong>ofong> this study is to find out if C. caryophyllea would produce dauciform roots and

increase their root proliferation in a ong>localisedong> response to a band ong>ofong> ong>graniteong>, which would

suggest they are able to uptake P from the mineral. This will be compared to the number ong>ofong>

dauciform roots produced and increase in root proliferation in a band ong>ofong> soil and a band ong>ofong>

mineral and soil together. Rock is P limiting (Hong>ofong>fland et al., 2004) so it is hypothesised that



C. caryophyllea will locally increase root proliferation and dauciform root production in response

to a band ong>ofong> mineral as it does to a band ong>ofong> soil, as shown by Johnson (2007). It is hypothesized

that the plants grown with a mineral and sand band will produce the highest number

ong>ofong> dauciform roots and the greatest amount ong>ofong> root biomass overall. ong>Theong>y are also likely

to increase ong>localisedong> root proliferation and dauciform root production in the treatment band

the most as they are probably more P limited than plants grown with the other treatment

bands. In all P limited plants, it is predicted that root biomass and dauciform root production

will be lower in all areas ong>ofong> the tube that do not contain the treatment band.

Plants grown with mineral and soil bands and soil and sand bands were hypothesized to show

a ong>localisedong> increase in root proliferation and modified root production in response to their

treatment bands also, but to a lesser extent, as they are less P limited due to the presence ong>ofong>

soil in their treatment band.

Two controls with added P fertilizer will be used as a comparison to see the difference in root

proliferation down the sections ong>ofong> the tube. P limitation is ameliorated by the addition ong>ofong> P

fertilizer, thus inhibiting P limitation responses from the plant such as dauciform root production

and ong>localisedong> root proliferation to a P source. It is predicted that the tubes treated with P

fertilizer will produce no dauciform roots and have a relatively uniform distribution ong>ofong> root

biomass, decreasing towards the bottom ong>ofong> the tube, with no ong>localisedong> increase in root proliferation

where the treatment band is located. ong>Theong>y are predicted to have a lower root biomass

and length overall, as fewer resources need to be allocated to root growth as P is not in limiting

supply. It is also predicted that the plants treated with P fertilizer will produce the highest

shoot weights as less resources are being allocated to the root system and released in exudates

in order to uptake P.

Feldspar crystals contain apatite inclusions, the weathering ong>ofong> which is known to release P

(Hong>ofong>fland et al., 2004). Feldspars will be placed within bands containing ong>graniteong> to see if

there is any ong>effectong> ong>ofong> weathering from the dauciform roots. This will be compared with the

ong>effectong> ong>ofong> unmodified roots on the surface ong>ofong> the feldspar crystals and 2 other controls where

no plants were grown in the tubes. It has been found that certain plant species can take up

phosphate from rocks. Hong>ofong>fland et al., (1989) documented the mobilisation ong>ofong> P from phosphate

in the rock by rape (Brassica napus), probably due to its production ong>ofong> long fine root

hairs in P deficiency. Weathering ong>ofong> rocks releases the phosphate bound in them (Griffith et

al., 1977). Organic acids released by plants have a small role in mineral weathering, which is

thought to increase nutrient availability to the plant, and increase feldspar dissolution rates

below a certain acidity. ong>Theong>y may play a greater role in the areas closer to the plant roots

where there is more ong>localisedong> exudation (Drever & Stillings, 1997). However, plants themselves

probably contribute much more to weathering, through binding soil particles and

breaking down the parent material (Drever, 1994). It is predicted that where there is a ong>localisedong>

increase ong>ofong> dauciform roots and root proliferation in the treatment band there will be a

greater extent ong>ofong> weathering as there is a higher surface area ong>ofong> roots to release organic acids

and bind the rock. Treatments with added P fertilizer were used as controls, as they it would

produce no dauciform roots nor increase their root proliferation in the treatment band as they

would not be limited in P. Unmodified roots are predicted to have less ong>ofong> a weathering ong>effectong>



and where no plant was grown it is predicted that the surface ong>ofong> the feldspar will have barely

changed at all.

Materials and Methods

Carex caryophyllea is a sedge ong>ofong> the family Cyperaceae. It is found in grasslands in most areas

ong>ofong> the UK, mainly on calcareous soils. (Jermy & Tutin, 1968). ong>Theong>y are short plants and

have keeled leaves which curve outwards. ong>Theong> C.caryophyllea plants and the soil used in this

experiment were obtained from Redmire Moor in the Yorkshire Dales, from a roadside quarry

in carboniferous limestone.

Tubes were made for the plants to be grown in, 2 halves ong>ofong> the tube were taped together at the

sides and a mesh was glued to the bottom ong>ofong> the tube to prevent the sand and treatments from

falling out. ong>Theong> tubes were put in an oven overnight at 40ºC, to get rid ong>ofong> the glue fumes so as

not to cause damage to the plants. ong>Theong>re was a hole on one side ong>ofong> the tube, approximately

1cm from the top. In this was inserted a plastic plug, to keep a standard volume ong>ofong> 1.91cm³

free for the input ong>ofong> the treatment bands. ong>Theong> tubes were filled with sand and in some, C.

caryophyllea was planted. As they were grown in sand, there were no areas ong>ofong> increased nutrients

like in the field, so the production ong>ofong> modified roots in response to surface horizons

was eradicated. All modified roots, and the majority ong>ofong> the root system was removed before


Granite was obtained from Shap quarry in Cumbria. Pink feldspar crystals which had flat

shiny surfaces were picked out ong>ofong> the 2-4mm ong>graniteong> and the rest was ground down to 0.5-

1mm pieces using a ball mill and 2 sieves. Treatment bands were made up, according to volume

ong>ofong> material to be put in them. ong>Theong> treatment bands with ong>graniteong> in also had three feldspar

crystals in which came to the weight ong>ofong> 0.16998 ± 0.01 g.

ong>Theong> treatment bands were inserted into the tubes on the 28/10/08. Combinations ong>ofong> treatments

are shown in figure 1. Sedges planted with a band ong>ofong> soil and sand were used as comparisons

to ones with mineral in their treatment band, in terms ong>ofong> root proliferation and dauciform root

production. Treatments with added P fertilizer were used as controls to see the distribution ong>ofong>

roots and ong>effectong>s ong>ofong> unmodified roots on feldspar weathering. Treatments with no plants were

used as controls to see the ong>effectong> ong>ofong> feldspar weathering where no roots are present.






+P fertilizer



Figure 1. C.caryophyllea grown in sand with different treatment bands and controls: 1. Grown

with a band ong>ofong> soil and sand. 2. Grown with a band ong>ofong> mineral and soil. 3.Grown with a band ong>ofong>

mineral and sand. 4.Grown awith same treatment band as 2 but with added P fertilizer. 5 Grown

with same treatment band as 3 but with added P fertilizer. 6. No plant grown, band ong>ofong> mineral

and soil. 7. No plant grown, band ong>ofong> mineral and sand.


+P fertilizer



= Band ong>ofong> soil and sand

= Band ong>ofong> mineral and soil

= Band ong>ofong> mineral and sand

= Sand



ong>Theong> tubes were left for around a month to grow in a growth chamber with a propagator over

them to reduce water loss from the plants by evapo-transpiration so they would not dry out.

ong>Theong>y were watered every day except for weekends and when they were fertilized. 10ml ong>ofong>

nutrient solution made up ong>ofong> 1ml ong>ofong> N, K, Mg, Ca diluted in a litre ong>ofong> distilled water was

added to each tube for 3 days in a row in the first week, and from then on once a week until

harvesting. 10ml P solution made up ong>ofong> 50ml P added to 950ml distilled water was added to

treatments 4 and 5 (Figure 1.) once every week.

Plants were harvested from 28/11/08 - 5/12/08. ong>Theong> two sides ong>ofong> the tubes were split apart

and the sand containing roots was cut into sections for analysis (Figure 2.). ong>Theong> roots in each

section were extracted, cut up and spread around a square dish with a 0.5 x 0.5cm grid on the

bottom. This was put under a microscope and the number ong>ofong> times a root crossed a grid line

and the number ong>ofong> dauciform roots produced was recorded for each section. Number ong>ofong> grid

intersects crossed was used to estimate the length ong>ofong> the roots (Tennant, 1975). ong>Theong> shoots

and roots from each section were dried in an oven at 80ºC, put in a desiccator overnight and


Pieces ong>ofong> feldspar were extracted from the treatment bands and scanned using vertical scanning

inferometry VSI (Veeco Instruments) to map the surface topography ong>ofong> crystals at

nanometric scale. 3D images were compared to see if there were any noticeable ong>effectong>s ong>ofong> the

different treatments on the feldspar surface.


Dauciform roots could be seen to bind the soil and mineral particles ensheathing themselves

in the material in order to access P (Figure 3).



1 2 3 4

1.5cm 1.5cm 1.5cm 10.4cm

Figure 2. Lengths ong>ofong> sections cut in the growth medium for root extraction


Dauciform roots were produced by C.caryophyllea in all tubes except those treated with P

fertilizer (Figure 4.). Where this was added, no dauciform roots were seen in any ong>ofong> the sections,

and these were therefore not included in the statistical analysis as they were obviously

statistically different.

ong>Theong> production ong>ofong> dauciform roots per cm 3 growth substrate varied significantly between

depths ong>ofong> substrate (Figure 4) (Two-way ANOVA, F=25.48, d.f.=3, p


Number ong>ofong> dauciform roots produced/cm 3

Mean no. dauciform roots/cm 3
















section 2

section 3

section 4

1 2 3 4 5

Figure>Theong> ong>effectong> ong>ofong> treatment on the number ong>ofong>

dauciform roots/cm 3 Treatment

produced in each section





Mean no.dauciform roots/cm 3







1 2 3 4


Figure 5. Tukey comparison ong>ofong> ong>effectong>s. Means with different letter codes do not differ significantly

(tukey test p>0.05).(A) ong>Theong> ong>effectong> ong>ofong> treatment on the number ong>ofong> dauciform roots

produced/cm3. (B) ong>Theong> ong>effectong> ong>ofong> section on mean number ong>ofong> dauciform roots produced/cm3



Treatments: 1)Soil and sand band.

2)Mineral and soil band. 3) mineral and sand

band. 4) mineral and soil band + P fertilizer.

5) Mineral and sand band + P fertilizer.

Sections: 1) 0 - 1.5cm deep. 2) 1.5 – 3.0cm

deep. 3) 3.0 – 4.5cm deep. 4) 4.5 10.4cm





Mean no. dauciform roots produced per cm root length


Mean no. dauciform roots per cm root length















1 2 3 4 5


Figure 6. ong>Theong> ong>effectong> ong>ofong> treatment on the mean number ong>ofong>

dauciform roots produced per unit root length in each section.



1 2 3


Figure7. Effect ong>ofong> treatment on the mean number ong>ofong>

dauciform roots produced per cm root length. Means

having the same letter code do not differ significantly

(Tukey test p>0.05)


section 1

section 2

section 3

section 4

ong>Theong> treatment band had a very significant

ong>effectong> on the number ong>ofong> dauciform roots

produced per cm root length (Two-way

ANOVA, F=9.05, d.f.= 2, p

Mean root dry weight (g/cm 3 )

Mean root length per volume growth substrate (cm/cm 3 )



= 12, p = 0.716).

In treatments 1, 2 and 3 the highest amount

ong>ofong> root biomass was allocated to the section

containing the treatment band, as hypothesized.

ong>Theong> amount ong>ofong> root biomass produced

was lower above and much lower below this

section. In P fertilized treatments, the

amount ong>ofong> biomass produced decreased with

depth, and there was no increase in root

biomass at depths 1.5 – 3.0cm, where the

treatment band was contained, as expected

(Figure 9). ong>Theong>re was a highly significant

ong>effectong> ong>ofong> section on the amount ong>ofong> root biomass

produced (two-way ANOVA, F= 62.78,

d.f.=3, p


would reduce shoot biomass.

Observations from the VSI scanning suggest that the sedges grown with the treatment band ong>ofong>

mineral and sand weathered the feldspar to a much greater extent than any ong>ofong> the other treatments.

At 50x and 100x magnification, etch pits ong>ofong> an approximate depth ong>ofong> 0.3μm and diameter

ong>ofong> 0.5μm are clearly visible, and in some areas, lateral lines ong>ofong> these pits have formed.

Etch pits were not observed on the feldspar surfaces in any other treatment, and their surfaces

appeared much smoother (Figure 11.).











Line ong>ofong>

etch pits






etch pit

Line ong>ofong>

etch pits




This experiment has shown that C.caryophyllea will produce a ong>localisedong> response in its root

system to low concentrations ong>ofong> phosphorus in its growth medium, supporting the work ong>ofong>

Johnson (2007). ong>Theong> production ong>ofong> dauciform roots and increased root growth in tubes containing

the mineral and sand band suggest that C.caryophyllea can directly uptake P from the

mineral, supporting the initial predictions. ong>Theong> direct uptake ong>ofong> P from rock has also been

seen in other plant species. Wallander et al.’s (1997) experiment on Pinus sylvestris seedlings

showed that they could weather apatite, by which they were able to increase their nutrient

supply. This challenges the general conceptions ong>ofong> P acquisition, suggesting that

C.caryophyllea may be able to take up organic P, bypassing the mineralization process to

PO4, which could have important implications for their fitness in the field.

Plants which produced modified roots increased root hair proliferation in zones ong>ofong> nutrient

availability in order to compensate for the rest ong>ofong> the root system which subjected to infertile


Figure 11. VSI images ong>ofong> surface layers ong>ofong> feldspars from different treatments. (A) Non

reacted feldspar. 100x. (B) mineral and soil band, no plant grown. 100x. (C)Mineral and

sand, no plant grown. 50x. (D) Mineral and soil band, plant grown.100x. (E) mineral and

sand and plant (i) 100x (ii) 50x. (F) Mineral and soil and P fertilizer. 50x. (G) Mineral

and sand and P fertilizer. 100x.


conditions. Net absorption in these ong>localisedong> patches is increased in order to maintain their

relative growth rate (Drew & Saker, 1978). Plants grown with the treatment band ong>ofong> ong>graniteong>

and sand showed the greatest extent ong>ofong> dauciform root production, suggesting that

C.caryophyllea finds the phosphorous in the mineral more inaccessible than in the soil. However

the production ong>ofong> dauciform roots is not as ong>localisedong> to the resource patch as it is with

the other two treatments. Dauciform roots are produced at high levels all down the root prong>ofong>ile.

This was not predicted, it was thought that the mineral band would cause just a ong>localisedong>

production ong>ofong> dauciform roots in a similar way to a band ong>ofong> soil. In the field, the high exudation

ong>ofong> organic acids by these highly modified roots can cause mineral weathering and the

release ong>ofong> P into the bulk soil (van Breemen et al., 2000). A similar process may have occurred

in the tubes, allowing P to be released into the sand, so it is not just concentrated in the

treatment band, accounting for the high number ong>ofong> dauciform roots per unit root length in all


As predicted, the sedges treated with P fertilizer did not produce dauciform roots anywhere in

the growth medium, nor did they increase their root proliferation in response to any treatment

band. Root biomass and proliferation was greatest at the nearest to the plant, and decreased

with depth. ong>Theong>se were not limited by P and so it would be a waste ong>ofong> energy for them to produce

structures to facilitate P uptake, and excess P may cause toxicity.

ong>Theong> roots ong>ofong> plants deficient in P become a dominant sink ong>ofong> photosynthates from the shoots

(Marschner, 1995). Sedges that were P limited allocated a higher amount ong>ofong> their dry weight

to their root system than those supplied with sufficient P, the highest allocation being to the

section containing the treatment band, as predicted. ong>Theong> production ong>ofong> shoot biomass did not

appear to be altered by different treatments; therefore it appears that changes in the root systems

were produced without any significant ong>effectong> on above ground biomass. This result has

also been seen in barley where plants treated with extra phosphates produced similar shoot

weights to those that were untreated (Drew, 1975). This was not predicted; it was thought that

the sedges treated with P solution, which were therefore not P limited, would have a greater

shoot dry weight as fewer resources would be allocated to the root system in order to take up

P. Perhaps this is a limitation ong>ofong> the low growing mechanism ong>ofong> C.caryophyllea. Plants growing

on low nutrient soils, such as the calcareous soils low in plant-available P where

C.caryophyllea are ong>ofong>ten found, generally produce dry matter at low rates. ong>Theong>y also tend to

accumulate mineral nutrients when they are more readily available as their demands for the

use ong>ofong> the nutrient in growth have been exceeded (Grime, 1986). High amounts ong>ofong> P supplied

to plants which typically grow on infertile soils have also been seen to accumulate to toxic

amounts, to the detriment ong>ofong> the plants growth (Jones, 1974).

Dauciform roots exude a burst ong>ofong> organic acids to mobilize P bound in the soil. This causes

the local rhizosphere to be subjected to intense chemical extraction (Marschner, 1995). Organic

acids have been documented to cause weathering to some extent (Drever, 1994) and

observations from the VSI scanning suggested that where the highest density ong>ofong> dauciform

roots are produced, the weathering ong>effectong>s are the strongest, as etch pits were only seen in

feldspars that had been in the mineral and sand treatment band. This confirms the initial predictions

as the higher the density ong>ofong> dauciform roots, the greater the concentration ong>ofong> organic



acid exudation.

In this experiment the weathering ong>effectong> observed on the feldspar was only very small compared

to ong>effectong>s shown by Smith et al. (1999), as unfortunately the time constraints meant that

the plants had to be harvested after 1 month. If plants had been left to grow for longer they

may have had a more prominent ong>effectong> on feldspar weathering. In future work it may be useful

to scan the feldspar before input into treatment bands, and then again after plant harvest

and statistically compare the two to see the ong>effectong> ong>ofong> the plant on the feldspar surface.

In future, aseptic culture ong>ofong> the sedges may be useful, to determine whether the weathering is

in fact due entirely to the plant or if microorganisms in the growth medium also play a role.

As microorganisms deplete organic acids, feldspars in treatment bands containing soil and

therefore potentially soil bacteria, may not have been as intensely weathered, as the bacteria

may have got rid ong>ofong> the acids before they could do much damage to the feldspar surface. In

addition, microorganisms may also have played a part in the weathering ong>ofong> the feldspars from

the mineral bands, as they may also use the feldspar as a P source.


Jonathan Leake obtained all materials needed and assisted throughout the experiment and

write-up. Megan Andrews, Ben Palmer, Irene Johnson and Adele Duran helped with technical

aspects ong>ofong> the experiment including the VSI scanning, sieving and grinding the ong>graniteong>, assembling

the tubes, and photographing the dauciform roots.


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change. PHD ong>Theong>sis, University ong>ofong> Sheffield, UK. P45-70

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