Available online at www.sciencedirect.com
Environmental and Experimental Botany 63 (2008) 232–239
UV irradiance as a major influence on growth, development and
secondary products of commercial importance in Lollo Rosso
lettuce ‘Revolution’ grown under polyethylene films
E. Tsormpatsidis a,∗ , R.G.C. Henbest b , F.J. Davis c , N.H. Battey a , P. Hadley a , A. Wagstaffe a
a
Centre for Horticulture and Landscape, School of Biological Sciences, The University of Reading, Reading RG6 6AS, UK
b British Polythene Industries, Visqueen, Yarm Road, Stockton-on-Tees, Cleveland TS18 3GB, UK
c Department of Chemistry, School of Chemistry, Food Biosciences and Pharmacy, The University of Reading, Reading RG6 6AD, UK
Received 13 March 2007; received in revised form 20 November 2007; accepted 11 December 2007
Abstract
The growth and production of anthocyanin, flavonoid and phenolic compounds were evaluated in Lollo Rosso lettuce ‘Revolution’ grown
continuously under films varying in their ability to transmit UV radiation (completely transparent to UV, transparent above 320, 350, 370 and
380 nm and completely opaque to UV radiation). Plants were grown from seed under UV transparent and UV blocking films and destructively
harvested 3–4 weeks after transplanting. Plants under a complete UV blocking film (UV400) produced up to 2.2 times more total above ground
dry weight than plants under the UV transparent film. In contrast, anthocyanin content in plants under the UV blocking film was approximately
eight times lower than in plants under a UV transparent film. Furthermore, there was a curvilinear relationship between the anthocyanin content
and UV wavelength cutoff such that above 370 nm there was no further reduction in anthocyanin content. Fluorescence measurements indicated
that photosynthetic performance index was 15% higher under the presence of UVB and UVA (UV280) than under the presence of UVA (UV320)
and 53% higher than in the absence of UV radiation suggesting protection of the photosynthetic apparatus possibly by phenolic compounds. These
findings are of particular importance as the potential of UV transmitting films to increase secondary compounds may offer the opportunity to
produce plants commercially with increased health benefits compared to those grown under conventional films.
© 2007 Elsevier B.V. All rights reserved.
Keywords: Ultraviolet light; UV blocking films; UV transparent films; Red lettuce; Anthocyanins; Phenolics
1. Introduction
One of the most exciting developments in commercial protected cropping in recent years has been the introduction of
spectral filters incorporated into horticultural polythene films,
which block specific wavebands. Reduction in plant height has
been observed in a range of species under polyethylene films
with low transmission of FR light, offering an alternative method
of producing compact high quality plants without using chemical growth regulators (Haeringen et al., 1998; Rajapakse et al.,
1999; Runkle and Heins, 2001; Rajapakse and Li, 2004; Fletcher
et al., 2005). A new generation of UV transparent and UV blocking plastic films has also been developed which have a number
Abbreviations: PS II, photosystem II; UV, ultraviolet; UVA, ultraviolet-A;
UVB, ultraviolet-B; PI, performance index.
∗ Corresponding author. Tel.: +44 l183787960.
E-mail address: [email protected] (E. Tsormpatsidis).
0098-8472/$ – see front matter © 2007 Elsevier B.V. All rights reserved.
doi:10.1016/j.envexpbot.2007.12.002
of potential applications for protected cropping. Plastic films
which are opaque to UV offer an environmentally friendly way
of controlling pests and diseases (Doukas and Payne, 2007).
Recent research has shown that the incidence of whitefly was
significantly reduced under UV blocking films compared to standard films (Doukas, 2002; Doukas and Payne, 2007). Currently,
commercial production under plastic film structures is based on
standard horticultural films (or glass) that block some of the UV
radiation. In contrast, plastic films with high UV transmission
may offer a way of increasing secondary products and therefore
potential health benefits in response to increased UV radiation.
Little research has been carried out, however, to quantify the
effects of UV radiation on crop quality.
UV radiation can be regarded as a stress factor which is capable of significantly affecting plant growth characteristics. Plant
height, leaf area, leaf length have been showed to decrease,
whereas leaf thickness was increased in response to UVB radiation (Teramura, 1983; Tevini and Teramura, 1989; Rozema et
E. Tsormpatsidis et al. / Environmental and Experimental Botany 63 (2008) 232–239
al., 1997). In addition, photosystem II can be adversely affected
by UVB radiation (Teramura, 1983; Caldwell et al., 1989; Tevini
et al., 1991; Rozema et al., 1997). Chlorophyll fluorescence has
been shown to be a simple and reliable technique for measuring the performance of photosystem II (Maxwell and Johnson,
2000) and the extent to which environmental stress can impair
photosynthetic efficiency (Maxwell and Johnson, 2000), e.g.
temperature (Lu and Zhang, 2000; Daymond and Hadley, 2004),
UV light (Kolb et al., 2001; Reddy et al., 2004), salinity (Chen
et al., 2004; Jiang et al., 2006) and water (Saccardy et al.,
1998).
Plants produce a wide range of flavonoids and related
phenolic compounds which tend to accumulate in leaves
of higher plants in response to UV radiation (Tevini and
Teramura, 1989; Rozema et al., 1997). It has been suggested
that plants have developed UV-absorbing compounds to protect them from damage to DNA or to physiological processes
caused by UV radiation (Stapleton, 1992). These UV-absorbing
compounds accumulate in the epidermis, preventing UV radiation from reaching the photosynthetic mesophyll (Stapleton,
1992; Braun and Tevini, 1993). In the red ‘Lollo Rosso’ lettuce, studied here, the main phenolic metabolites are phenolic
acids (cafeoyltartaric, chlorogenic, dicaffeoylquinic), flavonoids
(quercetin-3-glucuronide, quercetin-3-glucoside, quercetin 3-6malonyglucoside, quercetin-3-6-malonyglucoside 7-glucoside)
and the anthocyanin cyanidin 3-malonyglucoside (Ferreres et
al., 1997).
Plants may produce secondary products to protect them
against UV light damage, but these metabolites also play an
important role in human health. Phenolics, flavonoids and anthocyanins are responsible for antioxidant activity in fruits and
vegetables (Wang et al., 1996; Cao et al., 1997). Epidemiological studies have shown a positive relationship between fruit and
vegetable consumption and reduced incidence of chronic and
degenerative diseases (Heinonen et al., 1998; Prior et al., 1998).
These natural antioxidants have scavenging properties against
oxygen free radicals, offering protection to lipids, proteins and
nucleic acids (Heinonen et al., 1998).
Most published results on the effects of UV radiation on
plants are based on the effect of UV light added to either natural or artificial light (using UV lamps) (Rozema et al., 1997;
Krizek, 2004). Published studies based on UV exclusion from
natural radiation are limited (Krizek et al., 1997; Krizek et
al., 1998; Krause et al., 1999; Kolb et al., 2001; Kolb et al.,
2003). Krizek (2004) stated that results of experiments using
supplementary UV radiation are difficult to interpret due to unrealistically high UV radiation levels and inappropriate levels of
UVA (320–400 nm) irradiance. It seems that ambient levels of
PAR and UVA mitigate damage caused specifically by UVB
radiation. According to Caldwell et al. (1994), UVB radiation
caused biomass reduction only when PAR and UVA levels were
reduced to less than half that of sunlight levels. In addition, UVA
proved to be effective in ameliorating UVB damage when PAR
was low.
Here we describe the effect of UV radiation on quality and
on growth and development of ‘Lollo Rosso’ lettuce under
field conditions, using films that sequentially block specific
233
bands within UV region of the spectrum. The potential for
increasing secondary product levels by using a highly UV transparent film compared to standard horticultural UVI/EVA film is
assessed.
2. Materials and methods
2.1. Growth conditions and plant husbandry
Two experiments were conducted during the summers of
2005 and 2006 at the School of Biological Sciences Laboratories
Field Unit, Shinfield, Reading, UK. Each experiment was carried out in a suite of 10 tunnels, measuring 3 m × 2.7 m × 6.8 m
(W × H × L), specifically designed for studying experimental cladding materials. Six plastics that block progressively
at 20-nm intervals across the UV region were supplied by
British Polyethylene Industries Agri, Stockton-on-Tees, UK.
The spectral transmission of each film, measured using a
Benthams Spectroradiometer (M 300 EA monochromator, Benthams Instruments Ltd., Reading, Berkshire, UK) (Fig. 1).
Seeds of Lollo Rosso ‘Revolution’ (Elsoms Seeds Ltd., Lincolnshire, UK) were sown in plug trays containing peat-based
compost (Bulrush Horticulture Ltd., UK) and then immediately
transferred to each tunnel covered with one of the experimental films. After a period of 4 weeks they were transplanted into
either 1-m peat-filled grow bags (Bulrush Horticulture Ltd., UK)
(2005), or into 0.5-m peat-filled grow bags (2006) at a density
of 5 and 3 plants per bag, respectively. Six grow bags were
transferred into each tunnel.
Plants were irrigated with a standard commercial feed 3:1:1
(N, P, K) (Sinclair Horticultural, Lincoln, UK) applied through
a drip irrigation system (Field Ltd., Kent, UK) (four drippers
per peat bag) via a Dosatron (Dosatron International, Bordeaux,
France) set to provide an electrical conductivity of 1.4 ms.
Temperature in each tunnel was measured using T-type thermocouples inserted into aspirated screens. Tube solarimeters
(in-house construction, Szeicz et al., 1964), suspended 10 cm
below the film, were used for measuring total radiation in each
tunnel. Air temperature and radiation in each tunnel were measured every 30 s and half-hourly averages were recorded in a
data-logger (DT-500, Data Electronics, Cambridge, UK).
Fig. 1. Spectral transmission of UV blocking and UV transparent polyethylene
films.
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E. Tsormpatsidis et al. / Environmental and Experimental Botany 63 (2008) 232–239
2.2. Experimental design
The experiment was set out as two blocks in which treatments
(plastic films) were randomly allocated. In 2005, five films were
used and replicated twice (UV280, UV320, UV370, UV380 and
UV400) whereas six films were used in 2006 (UV280, UV320,
UV380 replicated twice and UV350, UV370 and UV400 replicated once). The experiment was repeated three times, twice in
2005 and once in 2006. Six grow bags were randomly allocated
to three plots within each tunnel. Two plants per grow bag were
used for growth measurements and one plant per grow bag for
secondary product analysis (n = 24 in 2005 and n = 12 in 2006).
Data were analyzed using the ANOVA procedure of the Genstat
statistical package (version 8) (VSN International Ltd., Oxford,
UK).
2.3. Growth and physiological measurements
Plants were harvested for analysis 26, 29 and 24 days after
transplanting in June 2005, July 2005 and July 2006, respectively. Leaf number and fresh and dry leaf weight were recorded.
Dry weight measurements were carried out after drying to
constant weight in a ventilated oven at 70 ◦ C. Chlorophyll fluorescence was measured on four different sunny days from
25 July 2006 to 29 July 2006 using a portable fluorometer
(Handy PEA, Hansatech Instruments Ltd., Kings Lynn, UK).
One leaf (same age) was chosen per plant from each of the
six grow bags in each tunnel. A total of 12 measurements per
treatment were made (UV280, UV320 and UV380). Fluorescence measurements included: maximum quantum yield of PS II
Fv /Fm was calculated as: Fv /Fm = (Fm − F0 )/Fm (Maxwell and
Johnson, 2000). Performance index of photosynthesis based on
the equal absorption (PIABS ) was calculated as PIABS = RC/ABS
[ϕP0 /(1 − ϕP0 )][ψ0 /(1 − ψ0 ]. Where RC/ABS is the density
of active PSII reaction centres per quantity of light absorbed
by the antenna, ϕP0 is maximum quantum yield for primary photochemistry and ψ0 expresses the probability that a
trapped photon enters the electron transport chain (Clark et al.,
2000).
2.4. Secondary product measurement
Sample preparation and extraction: Six lettuce plants from
each tunnel were chosen for analysis (one per peat bag). Each
sample was taken from one plant by removing the distal ends
(4 cm) of five to six leaves (Voipio and Autio, 1995). These
leaves were blended in a food processor and a 1-g sub-sample
was extracted with 10 ml of methanol:HCl (99:1) and placed
in a vial (Voipio and Autio, 1995). The mixture was stirred for
1–2 min with a hand held stirrer. The supernatant was then placed
in a screw-cap vial and placed in a cold room (2 ◦ C) overnight
to facilitate extraction. An aliquot of the filtered extract was
used the next day to determine total anthocyanins, flavonoids
and phenolics levels.
Determination of total phenolics, flavonoids and anthocyanin: Total soluble phenolics in the extract were determined
spectrophotometrically (CECIL 1000 series Cecil Instruments
Ltd., Cambridge, UK) using a modified Folin-Ciocalteu colorimetric method (Singleton et al., 1999; Wang and Lin, 2000;
Meyers et al., 2003). Results were expressed as mg of gallic acid
equivalent (GAE) per 100 g of fresh weight. Total flavonoid content of the extracts was determined spectrophotometrically using
a modified colorimetric method described by Jia et al. (1999),
modified by Meyers et al. (2003). Results were expressed as
mg of catechin equivalents per 100 g fresh weight. Total anthocyanin content was determined using the pH differential method.
Anthocyanin content was estimated in a spectrophotometer at
510 and 700 nm buffers at pH 1.0 and 4.5 (Wrolstad, 1976;
Giusti and Wrolstad, 2001; Meyers et al., 2003). All values
were estimated as cyanidin-3glucoside using a molar extinction
coefficient of 26,900 (Wrolstad, 1976; Giusti et al., 1999).
2.5. Spectral transmission and experimental conditions
The UV400 film was opaque to radiation of the UV waveband, whilst, the UV280 film showed the highest transmission
to UV spectrum (Fig. 1). The UV280 and UV320 films had 81%
and 39% transmission, respectively in the UV region, whilst,
UV350, UV370, UV380 and UV400 had 22%, 10%, 3.5% and
0% transmission, respectively (Table 1). All the films used in
this study exhibited the same PAR (400–700 nm) transmission
except for the UV370 film which had a slightly reduced transmission (between 4% and 7% lower than the other films). There was
no significant effect of the film on temperature or light measured
within the tunnels. Therefore, observed effects over the experimental period were most likely to be due to differences in UV
light spectrum rather than to differences in other environmental
variables (Table 1).
Table 1
PAR transmission, average daily temperature and average light levels during the experimental period for each treatment
Treatment
UV280
UV320
UV350
UV370
UV380
UV400
PAR (400–700 nm)
% transmission
86
86
86
79
85
84
*Only used in 2006 season.
UV (280–400 nm)
% transmission
81
39
22
10
3.5
0
Average temperature (◦ C)
Average total daily radiation (Mj m−2 d−1 )
June 2005
July 2005
2006
June 2005
July 2005
2006
15.9
15.6
*
15.6
15.8
15.6
18.8
18.7
*
18.5
18.8
18.5
21.1
21.1
21.2
21.2
21
21
15.2
15.2
*
14.1
15.0
14.8
16.7
16.7
*
15
16.4
16.1
12.6
12.5
12.5
11.4
12.4
12.1
E. Tsormpatsidis et al. / Environmental and Experimental Botany 63 (2008) 232–239
235
Fig. 2. Total above ground dry weight (A and B) and leaf number (C and D) of lettuce plants under UV280, UV320, UV350, UV380 and UV400 film treatments
in 2005 (A and C) and 2006 (B and D). The vertical bars (A and C) show treatment LSD at 5% level. The vertical bars (B and D) show average LSD at 5% level
(unbalanced structure).
3. Results
3.2. Effect of UV on phenolic compounds
3.1. Effect of UV on growth
Total anthocyanin content of lettuce was higher in plants
grown under the UV280 and UV320 films than in plants under
the UV350, UV370, UV380 and UV400 films (P < 0.001)
(Fig. 5A and B). In 2006, anthocyanin content was 50%
higher under a UV transparent film (UV280) compared to
plants under the standard horticultural UVI/EVA film (UV320)
(Fig. 5B). The lowest anthocyanin content was observed in
plants under the UV400 film which was up to eight times lower
than plants under the UV transparent film UV280 film (2006)
(Fig. 5B).
The total flavonoids followed a similar pattern to anthocyanins across the different film treatments. In general, the
higher the UV radiation transmitted through the film, the higher
the flavonoid content. Plants under the UV transparent film
(UV280) had 63% and 92% higher flavonoid contents than plants
Lettuce showed a strong response to UV radiation. In reduced
UV radiation vegetative growth was increased compared to
plants in high UV radiation levels (Fig. 2). No significant
interaction between vegetative growth and planting month was
observed in 2005 and in both years total above ground dry
weight in lettuce plants under UV350, UV370, UV380 and
UV400 was higher than in plants under the UV280 and UV320
(P < 0.001). Plants under a complete UV blocking film (UV400)
produced 40% and 122% more total above ground dry weight
in 2005 and 2006, respectively, than plants under the UV transparent treatment (UV280) (Fig. 2A and B). Plants under the
UV320 (standard horticultural UVI/EVA film) produced 10%
and 34% higher total above ground dry weight than in plants
under the UV280 film in 2005 and 2006, respectively (Fig. 2A
and B). Leaf number was also proportionally increased in plants
grown under treatment films that blocked UV radiation. Plants
under the UV400 film produced 28% and 66% more leaves in
2005 and 2006, respectively, than plants in the UV280 treatment (Fig. 2C and D). Total above ground dry weight was
linearly related to UV wavelength cutoff of individual films
(Fig. 3).
No significant differences were observed in the ratio of variable and maximum photochemical efficiency of PSII (Fv /Fm )
of plants grown under UV380 compared to those plants grown
under the UV280 and UV320 films (Fig. 4A). Significant, differences were, however observed, in photosynthetic performance
index (PIABS ). Plants under a UV transparent film (UV280) had
15% and 53% higher performance index than plants under a less
UV transparent film (UV320) and a UV blocking film (UV380),
respectively (Fig. 4B).
Fig. 3. Linear relationship between total above ground dry weight and wavelength cutoff (nm) of individual treatment films. R2 values are shown in the
graphs. Standard error bars are shown.
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E. Tsormpatsidis et al. / Environmental and Experimental Botany 63 (2008) 232–239
Fig. 4. Effect of solar UV light transmission through UV blocking and UV transparent films on leaf fluorescence (A) Fv /Fm and (B) PIABS . The vertical bars show
treatment LSD at 5% level.
under the UV blocking film (UV400) in June and July plantings
(2005), respectively (Fig. 5C). Plants under the UV transparent (UV280) film had 20% higher flavonoid content than plants
under the commercial film (UV320) (Fig. 5D).
The total phenolic content was also highest in plants from
the UV280 and UV320 films and declined progressively in
plants grown under the UV350, UV370, UV380 and UV400
films (P < 0.001) (Fig. 5F). Complete blocking of UV radiation (UV400) reduced phenolic content in lettuce plants by
50% compared to commercial film (UV320 treatment) and by
60% compared to UV transparent film (UV280) in the July
2005 planting (Fig. 5E). In 2006 the highly UV transparent film
(UV280) increased total phenolic content by 20% compared to
the UV320 film (standard horticultural UVI/EVA film) (Fig. 5F).
The month of planting (2005) had a significant effect on secondary product content (P < 0.001) (Fig. 5A, C and E). In general
secondary product content was lower during June and higher
during July, probably due to lower radiation levels in June.
Secondary products were highly correlated with the degree
of UV radiation cutoff. A curvilinear relationship could be fit-
Fig. 5. Anthocyanin content (A and B), flavonoid content (C and D) and phenolic content (E and F) of lettuce plants under UV280, UV320, UV350, UV380 and
UV400 film treatments in 2005 (A, C and E) and 2006 (B, D and F). The vertical bars (A, C and E) show the LSD between treatment and month at 5% level. The
vertical bars (B, D and F) show treatment LSD at 5% level.
E. Tsormpatsidis et al. / Environmental and Experimental Botany 63 (2008) 232–239
237
Fig. 6. (A) The curvilinear relationship between anthocyanin content and wavelength cutoff of individual treatment films. (B) The curvilinear relationship between
phenolic content and wavelength cutoff (nm) of individual treatment films. R2 values and standard error bars are shown.
ted between anthocyanin content and level of UV radiation
(P < 0.001) (Fig. 6A). Similarly, total phenolic content was
curvilinear related to degree of UV radiation cutoff (Fig. 6B).
4. Discussion
The Lolo Rosso lettuce ‘Revolution’ used in this study
showed a clear response to an increase in the proportion of UV
light by increasing secondary metabolites and reducing growth.
Total anthocyanins were greatest when both UVA and UVB
were present (UV280 film). Where UVB was excluded and
UVA was transmitted, as in the UV320 film, anthocyanin content was reduced. This means that a highly UV transparent film
(UV280) is capable of increasing anthocyanin content compared
to a standard horticultural UVI/EVA film (UV320). Excluding
both UVA and UVB by the use of the UV400 film further reduced
anthocyanin content by up to eight times. Voipio and Autio
(1995), reported increases in anthocyanin content of lettuce
plants under supplementary UVA radiation. The present study
indicates that both UVB and UVA are involved in anthocyanin
photo-induction. These observations agree with the previously
reported studies of Krizek et al. (1998), who found that excluding UVA and UVB significantly reduced anthocyanin content of
lettuce compared to plants grown in the presence of UVA and
UVB radiation. In this study, however, 370 nm appeared to be
the critical wavelength beyond which further UV blocking did
not significantly decrease anthocyanin content.
Total flavonoids and phenolics showed similar responses to
UV radiation to anthocyanins with the highest content under UV
transparent films. The greater accumulation of flavonoids in the
presence of UVB and UVA suggest a protective role against UV
damage. It has been reported that these compounds accumulate
in leaves of higher plants to screen out harmful UV radiation
(Tevini and Teramura, 1989; Stapleton, 1992; Rozema et al.,
1997; Mazza et al., 2000). Increases in flavonoids after exposure to UVB light have also been reported in Brassica napus by
Olsson et al. (1998). Ryan et al. (1998) reported greater accumulation of flavonoids in response to UVB radiation. The present
study is in agreement with Krizek et al. (1998), who found high
rates of accumulation of UV-absorbing compounds in lettuce
grown in the presence of UVA and UVB radiation.
We have shown in this study that total above ground dry
weight is positively correlated with the degree of UV radiation
cutoff transmitted by the films. This finding indicates that the
presence of ambient levels of UVB and UVA decreased growth
of lettuce and agree with previously reported studies of Krizek
et al. (1997, 1998) who found increases in cucumber and lettuce fresh weight when UVA and UVB were absent. Diaz et al.
(2006) also reported a reduction in fresh weight of lettuce under
films that transmit UV radiation. Krizek et al. (1998) suggested
that the growth reduction in an UV environment could be due
to damage to the photosynthetic apparatus. UV radiation can
cause damage to photosynthetic apparatus by damaging photosystem II (Stapleton, 1992; Rozema et al., 1997), and high
levels of UVB radiation have been shown to reduce photosynthesis in pea (Nogués et al., 1999). In this study, however, we
have shown that lettuce plants under ambient levels of UV are
not subject to stress compared to plants under a non-UV environment, as no suppression on the Fv /Fm ratio was observed.
Photosynthetic performance index (PIABS ), however, indicated
an increased photosynthetic efficiency in plants exposed to UVB
and UVA. This could be as a result of the increased anthocyanin
levels protecting plants against photoinhibition.
Since growth reduction under UV environment was accompanied by accumulation of anthocyanins, flavonoids and phenolics,
it may be that the plant diverts energy produced by photosynthesis to synthesize these compounds to protect itself from UV
damage. Further studies, however, are needed in which photosynthetic rate will be measured directly to test whether growth
inhibition is due to a high cost of photo-protection. In addition,
accumulation of anthocyanins in the leaf epidermis may have
caused internal shading which can lead to a reduction of light
available to chlorophyll (Steyn et al., 2002; Neill and Gould,
2003). This possible light reduction may have also contributed
to growth reduction.
5. Conclusion
The key findings of this study are the high levels of secondary
products under UV transparent films. Plants in the presence of
UVB and UVA (UV280) appeared not to be stressed and this may
be because they accumulate secondary products which effec-
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E. Tsormpatsidis et al. / Environmental and Experimental Botany 63 (2008) 232–239
tively protect the photosynthetic apparatus. Our results indicate
that the quality of Lollo Rosso (in terms of phenolic compounds)
can be enhanced under a highly UV transparent film (UV280)
compared to the standard horticultural UVI/EVA film (UV320).
These findings are of particular importance for growers as these
films are commercially available.
Acknowledgements
The authors wish to thank the RETF (Research Endowment Trust Fund) of The University of Reading and British
Polyethylene Industries for co-funding this study and Mr.
David McLay for his technical support during the experimental
period.
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