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International Journal of Phytoremediation, 16:1042–1057, 2014
Copyright CTaylor & Francis Group, LLC
ISSN: 1522-6514 print / 1549-7879 online
DOI: 10.1080/15226514.2013.810583
EFFECTS OF HIGH NUTRIENT SUPPLY ON THE
GROWTH OF SEVEN BAMBOO SPECIES
Julien Piouceau,1,2 Gr´
egory Bois,1Fr´
ed´
eric Panfili,1
Matthieu Anastase,1Laurent Dufoss´
e,2and V´
eronique Arfi1
1PHYTOREM S.A., site d’Areva, chemin de l’autodrome, Miramas, France
2Universit´
edeLaR
´
eunion, Laboratoire de Chimie des Substances Naturelles et des
Sciences des Aliments, site ESIROI-IDAI - D´
epartement Agroalimentaire,
Sainte-Clotilde, France
Over the last decade, bamboo has emerged as an interesting plant for the treatment of various
polluted waters using plant-based wastewater treatment systems. In these systems, nitrogen
and phosphorous concentrations in wastewater can exceed plant requirements and poten-
tially limit plant growth. The effects of two nutrient rates on the growth of seven bamboo
species were assessed in a one-year experiment: Dendrocalamus strictus, Thyrsostachys
siamensis, Bambusa tuldoides, Gigantochloa wrayi, Bambusa oldhamii, Bambusa multi-
plex and Bambusa vulgaris. Nutrient rates were applied with a 20:20:20 NPK fertilizer as 2.6
and 13.2 t.ha.yr−1NPK to three-year-old bamboo planted in 70 L containers. Morphological
characters, photosynthetic responses, and NPK content in bamboo tissues were investigated.
Under high-nutrient supply rate, the main trend observed was an increase of culm produc-
tion but the culms’ diameters were reduced. For the seven species, the aboveground biomass
yield tended to increase with high-nutrient rate. Increasing in nutrient rates also improved
the photosynthetic activity which is consistent with the increase of nitrogen and phospho-
rus contents measured in plant tissues. All the bamboo species tested appears suitable for
wastewater treatment purposes, but the species Bambusa oldhamii and Gigantochloa wrayi
showed the higher biomass yield and nutrient removal.
KEY WORDS: Bamboo species, specific leaf area, chlorophyll afluorescence, high nutrient rate, bamboo
biomass
INTRODUCTION
Over the last decades, wastewater treatment systems using phytoremediation princi-
ples have been developed (Adams et al. 2000; McCutcheon and Schnoor 2003). Most of
these systems are constructed wetlands which use aquatic plants (Vymazal 2011). Another
type of system uses terrestrial plants like poplar, willow and more recently bamboo species.
As a plant for treating wastewater, bamboo is interesting in many respects. For mature
bamboo plantations of giant species, the aboveground biomass yield can reach 25 and 47 t
DM.ha−1.yr−1under temperate and tropical climate respectively (Scurlock, Dayton, and
Address correspondence to Julien Piouceau; PHYTOREM S.A., site d’Areva, chemin de l’autodrome, 13140
Miramas, France. E-mail: julienpiouceau@phytorem.com
1042
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EFFECTS OF HIGH NUTRIENT SUPPLY 1043
Hames 2000). Mature bamboo plantations have also interesting evapotranspiration rates that
range from 9 to 13 mm.day−1under tropical climate (Kleinhenz and Midmore 2002). In
addition, the bamboo species’ dense root system favors the rhizodegradation (McCutcheon
and Schnoor 2003) of organic matter contained in wastewater.
In wastewater treatment system using bamboo species, the wastewater is directly
spread on the soil surface of the plantation (Perttu and Kowalik 1997; Rosenqvist and Ness
2004; Thawale, Juwarkar and Singh 2006; Singh et al. 2008; Arfi et al. 2009). Therefore
an over application of wastewater on the plantation can lead to a release of nutrients such
nitrate and phosphorus in the groundwater that contribute to the eutrophication of water
resources (Smith, Tilman, and Nekola 1999; Smith 2009). So it is important to determine
the amount of nutrients, especially the amount of N and P that can be stored in the plant
biomass. By selecting the species that are most adapted in terms of nutrient removal, growth
rate and biomass yield, it may be possible to optimize the treatment system. For wastewater
treatment systems using bamboo, young bamboos are planted on the existing soil (Arfi et al.
2009). Obviously, a good initial growth stage of young plantations is required to ensure
an optimal treatment. Domestic wastewater application provide high amount of nutrient,
especially nitrogen and phosphorus (Pescod 1992) for a young bamboo plantation. For
crops, an excess of nitrogen induces a rapid stem elongation and results in sensitive crops
to stem breakage; excess of nitrogen can also induces a decrease of biomass and grain yield
(Morishita 1988; Bennett 1993; Elia and Conversa 2012). High inputs of phosphorous
can induce zinc, iron and copper deficiencies (Forsee and Allison 1944; Bingham 1973)
and hence reduce the biomass yield. Few studies deal with the effect of high nutrient
application on the growth of bamboos (Li et al. 2000; Fernandez et al. 2003; Kleinhenz
et al. 2003). Li et al. (2000) showed that fertilization increase the shoot number but had no
effect on diameter and height for P. Pubescens. Conversely, Azmy et al. (2004) showed that
fertilization increase significantly the height and diameter and tend to increase the shoot
number for G. scortechinii. The mentioned studies suggest that fertilization induced various
morphological modifications which depend on the bamboo species. However, the nutrient
rates applied in these studies remain low as compared to the rates that can be reached in a
context of wastewater treatment. In addition, these studies report applications of fertilizer
on mature bamboo plantations and not on young bamboo.
Our study aims to provide new insights on the effect of high-nutrient supply rates, as
it occurs in wastewater treatment system, on the growth of young bamboos species and its
consequences on the biomass yield and on the potential storage of the major nutrients (i.e.,
NPK) in the biomass.
Bamboo represents over 70 genera and 1200 species in the Bambusoideae sub-family
and are present all over the world (Kleinhenz and Midmore 2001). Bamboo species use a
rhizomatous vegetative growth strategy. New shoots, or culms, arising from rhizomes and
grow rapidly achieving their final height within one to two months. Once the culms are fully
developed their external diameter did not increase anymore. Thus, the growth of bamboo is
defined by the number of new shoots that emerged each year, generally during the pluvial
season. Each year, culms increase in number and size forming a clump (set of culms).
In order to assess the growth of young bamboos under high-nutrient rates, a one-year
experiment was carried out using seven species of clumping bamboo (sympodial bamboo;
(Stapleton 1998)), selected for their high biomass yield at mature age. Three-years-old
bamboo seedlings were planted in containers receiving two nutrients rates: a “low” and a
“high” nutrient rate. A commercial fertilizer was used to mimic the concentration of nitrogen
and phosphorus contained in domestic wastewater. The response of bamboo species to high
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1044 J. PIOUCEAU ET AL.
nutrient rates was determined using the number of culms produced during the experiment
and their diameter. The final aboveground biomass yield was then quantified by allometric
equations. Chlorophyll afluorescence measurements were performed to determine the
photosynthetic activity of the bamboo species. Chlorophyll afluorescence measurements
are now widespread to examine photosynthetic performance and stress in plants and to
explain the growth variations that may occur between species (Baker 2008). In the same
way, the specific leaf area (SLA) was measured to explain variations in growth rate between
species. Indeed SLA is an indicator trait of resource-use strategies (Amanullah et al.
2007) and relative growth rate (Reich, Michael and Ellsworth 1997). Many studies have
demonstrated that the increase in NPK fertilization increased the nitrogen concentration
and are positively correlated with leaf photosynthetic activity (Jin et al. 2011). So, the total
nitrogen, phosphorous and potassium contents in leaves and culms were also measured to
explain growth patterns.
MATERIALS AND METHODS
Experimental Conditions
The experiment was conducted over one year, from March 25th, 2008 to March,
27th, 2009 (367 days), on Reunion Island, an overseas French department in the south-west
Indian Ocean. The experimental site was located at 21◦03S; 55◦19E, at an elevation of
1043 m. During the experiment, the site had a temperature range of 13.2 to 26.2 C◦, a total
rainfall of 1240 mm.yr−1and an average relative humidity of 81.2%.
Seven species of clumping bamboo were selected for the experiment: Bambusa vul-
garis Schrad. (BVV), Bambusa oldhamii Munro (BO), Bambusa multiplex (Lour.) Raeusch.
ex Schult. (BMA), Bambusa tuldoides Munro (BV), Thyrsostachys siamensis Gamble (TS),
Dendrocalamus strictus (Roxb.) Nees (DS) and Gigantochloa wrayi Gamble (GW). These
species have been chosen for their high biomass yields and because these species are the
most studied in literature (Suwannapinunt and Thaiutsa 1988; Tripathi and Singh 1996;
Singh and Singh 1999; Kleinhenz and Midmore 2001; Castaneda-Mendoza et al. 2005;
Kibwage et al. 2008).
For each species, a cutting of mature culm from a mother clump was taken and planted
in soil to allow the sprouting of roots and rhizomes over a one-year period. Grown cuttings
were transplanted into 3 liter containers for one year, and then into 15 liter containers for
a further before being planted in 70 liter containers for the present experiment. At the
beginning of the experiment bamboo species were three years-old.
The growing media used was a 3:1:1 (v:v:v) mix of soil, scoria and sugar cane fibers.
Containers were then arranged in a fully randomized block design (7∗2) based on species
(seven levels) and nutrient rates (two levels), with 3 replicates per treatment. Each of the
three blocks contained each treatment combinations, giving a total of 42 containers of
bamboo.
Two stock solutions were prepared using a commercial fertilizer (20:20:20 NPK
Soluplant, Duclos International, France) diluted in tap water. The use of fertilizer solutions
allowed keeping steady the nutrient concentration of the solution all along the experiment,
that it would have not been the case if we had used domestic wastewater. Three kilograms
of the fertilizer were dissolved in 100 liters of tap water for the low-nutrient treatment,
and fifteen kilograms of fertilizer in 100 liters of tap water for the high-nutrient treatment.
One liter of a trace element solution (Oligo Drip 25 Fe, Duclos International, France) was
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EFFECTS OF HIGH NUTRIENT SUPPLY 1045
added to each of the two stock solutions. Plants were watered once a week with tap water
and twice a week with nutrient solutions using a drip irrigation system (Netafim TM, Israel).
The average height of water (with or without fertilizer) added at each watering session was
about 70 mm per container. Both stock solutions were diluted inline using a metering pump
(Dosatron, France) to provide the nutrient solution to the drip irrigation system via two
separate networks, one for each nutrient treatment. The dilution was 1% in the dry season
(May to November) and 1.6% in the wet season (December to April). The concentration
of the low-nutrient treatment corresponded approximately to the nitrogen concentration
found in domestic wastewater, which ranges between 20 and 85 mg.l−1(Pescod 1992);
the nitrogen concentration for the high-nutrient treatment was five times higher than in
domestic wastewater. The concentration range of phosphorous in domestic wastewater is
6to20mg.l
−1(Pescod 1992). In detail: during the dry season, the concentration of the
low-nutrient treatment was 60 mg.l−1of nitrogen (N), 60 mg.l−1of phosphorus (P) and
60 mg.l−1of potassium (K) (electric conductivity of 0.5 mS.cm−1) and the concentration
of the high-nutrient treatment was 300 mg.l−1of N, 300 mg.l−1of P and 300 mg.l−1of
K (electric conductivity of 1.3 mS.cm−1); during the wet season, the concentration of the
low-nutrient treatment was 96 mg.l−1of N, P, and K (0.7 mS.cm−1) and the concentration
of the high-nutrient treatment was 480 mg.l−1of N, P, and K (1.8 mS.cm−1). During the
experiment, a total of 45.6 g and 228 g N, P, and K per pot were added for the low and high
nutrient rate treatments respectively, that represents 2.6 and 13.2 t ha−1yr−1N, P and K
taking the pot area as the surface unit.
Bamboo Biomass Calculation
In order to determine the total number of culms produced during the experiment, all
culms initially present in each 70-liter container were counted and their diameter measured
with a digital caliper. The culms were then labeled with a paint spray. At the end of the
experiment, all unlabeled culms produced during the experiment were counted in each
container, their height measured with a tape measure, their basal diameters measured with
a digital caliper at the middle of the first internode and the number of internodes counted.
The biomass yield was determined using allometric equations (Shanmughavel and
Francis 2001). For each bamboo species, the allometric equations were established using
the basal diameter. In each container, four culms were randomly sampled to measure basal
outer diameter, inner diameter (i.e. wall thickness), total fresh biomass, fresh leaf biomass
and fresh culm plus branch biomass. Weights were measured with a 0.1g-precision scale
(Kern & sohn GmbH, Germany). Sub-samples of leaves and culms (including branches)
were taken to determine the dry mass (DM) of each part and for chemical analysis once
dried.
Regression equations were established between the fresh mass (y), the dry mass (y)
and the basal diameter (x). Raw data was log-transformed to normalize the data distribution
and to linearize the regression functions according to the equation (1)
Log (y)=a+blog(x)(1)
Regression equations were computed with Minitab 15 software (Minitab Inc., USA). This
equation (1) was transformed to obtain the standard form of the allometric equation (2)
(Navar 2010):
y=bxa(2)
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1046 J. PIOUCEAU ET AL.
A correction factor was then applied to the final biomass result (y) to correct the bias
engendered by the logarithm transformation using the following equation (3) (Sprugel
1983)
CF =exp(SEEˆ2/2) (3)
where CF is the correction factor and SEE the standard error of the estimate of the regression.
The total aboveground biomass produced during the year of experimentation was
determined for each species thanks to the allometric equation obtained.
Plant Material, Water Content, and Chemical Analysis
To determine the dry mass, sub-samples of leaves, branches and culms were oven-
dried at 70 C◦for 48 hours in a drying oven (Memmert, GmbH & Co, Germany) to preserve
the nutrients for chemical analysis.
Nitrogen content was determined using the Dumas method by means of an element
analyzer (CN 2000, LECO Corporation, USA). For phosphorus and potassium analysis,
plant samples were turned into ash (500C◦for two hours). The ashes were cooled at ambient
air temperature and then digested in two milliliters of hydrochloric acid solution (HCL) at
50%, before being heated on a hot plate to total evaporation of HCL. Two milliliters of HCL
were added de novo and the ashes were allowed to stand in the HCL for ten minutes. The
solution was filtered and then diluted with distilled water in a 50 ml flask. The phosphorus
content was determined by a colorimetric method using the ammonium molybdate method
with a colorimeter (Proxima, Alliance Instruments Italy). Potassium content was determined
by atomic absorption spectrophotometry (220FS, Varian inc., USA).
Only the species B. oldhamii (BO), G. wrayi (GW), B. vulgaris (BVV), D. strictus
(DS) were analysed.
Chlorophyll aFluorescence Measurements
Fluorescence measurements were done using a pulse amplitude modulation portable
fluorometer (Mini-PAM, Walz GmbH, Germany). All measurements were made on mature
leaves from culms produced during the experiment. The maximum quantum yield of pho-
tosystem II (PSII) -noted Fv/Fmin the following- was obtained by dark-adapting leaves for
20 minutes, as recommended by Rascher et al. (2000), before applying a saturation pulse
of 8000 μmol m−2s−1for 800 milliseconds. The effective quantum yield of PSII (F/Fm)
-noted PSII in the following-,was obtained per the same protocol but on light-adapted
leaves.
Fluorescence measurements were done at the beginning and at the end of the exper-
iment, one block per day (in March 24, 25, 26, 2008 and in March 24, 25, 26, 2009) and
always in the morning to avoid the diurnal photoinhibition of midday (Fernandez-Baco
et al. 1998; Kumar, Pal and Teotia 2002). The measurements of Fv/Fmand PSII were
performed twice in the morning on three randomly selected leaves in each experimental
unit. As for the nutrient content analysis of tissues, we focused on the following species:
B. oldhamii (BO), G. wrayi (GW), B. vulgaris (BVV), D. strictus (DS) for the fluorescence
measurements.
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EFFECTS OF HIGH NUTRIENT SUPPLY 1047
Specific Leaf Area Measurements
Specific Leaf Area (SLA) is the ratio between the total leaf area divided by the total
dry mass of the leaves sampled. Leaf samples were taken randomly along the culms on the
following species: BO, GW, BVV, DS. Leaves were immediately scanned with a scanner
(Mustek Scanexpress, Mustek Systems Inc., Taiwan), weighted and then oven-dried at 105
C◦for 48 hours. The leaf area was calculated using scan images processed using Adobe
Illustrator CS4 software (Adobe Systems Inc., USA).
Statistical Analyses
Regression trend lines and the coefficient of determination (R2) were calculated using
Minitab 15 software (Minitab inc., USA). A two-way ANOVA was performed with SPSS
software (SPSS inc., IBM, USA) to test the effect of the “species” factor and the effects
of “nutrient rates” factor on the mean number of culms (produced during the experiment),
their diameters, total aboveground biomass, nutrient concentration in leaves and culms,
fluorescence parameters and SLA. The LSD test was used to compare nutrient rate effects
across bamboo species on the mean number of shoots, their diameters, total aboveground
biomass, nutrient concentration in leaves and culms, fluorescence parameters and SLA.
RESULTS
Effect of the Nutrient Rate on the Number of Culms and
on Culms Morphology
On the whole, the mean number of new culms per species increased significantly
with the increase in nutrient rate (Figure 1a; p <0.01). This increase in culm number is
significant for BMA (p <0.01), from 35 to 52 new culms and for DS (p <0.001) from
14 to 33 new culms produced, for the low and high-nutrient treatments respectively. On
the contrary, high-nutrient treatment tended to reduce the number of culms of GW from 35
culms with the low-nutrient treatment to 27 culms with the high-nutrient treatment.
On the whole, the mean diameter of culms tended to decrease with the increase in
nutrient rate (Figure 1b). This decrease is significant for DS (p <0.001) from 16 to 10.5
millimeters. Conversely the mean diameter of culms significantly increased for GW (p <
0.05) and BV (p <0.001) from 8.2 to 10.2 and 11.3 to 16.1 millimeters respectively with
the high-nutrient treatment. For the high nutrient rate, no significant effect was noticed on
the height of culms and their wall thickness (data not shown).
The aboveground biomass yield was determined with allometric equations listed
in Table 3. The increase in nutrient rate significantly increased total aboveground fresh
biomass (Figure 2; p <0.001). A significant increase of the biomass (p <0.05) by 25,
48, 51, and 63% was observed for GW, BV, BMA, and BO respectively. The species GW
produced 5.9 to 7.5 kg, and the species BO produced 9.6 to 11.2 kg more aboveground
fresh biomass with the high-nutrient treatment than the other species.
Photosynthetic Activity and SLA
All bamboo species showed Fv/Fmratios above 0.700 (Table 1). The Fv/Fmratio
tended to be higher for the high-nutrient treatment. This trend was even significant for the
BVV species (p <0.001). The values of PSII tended to be higher for GW, BVV, and
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Figure 1 Mean number (a) and diameter (b) of new bamboo culms produced during the experiment for the low and the high-nutrient treatment for the species. B. vulgaris (BVV),
T. siamensis (TS), B. tuldoides (BV), B. oldhamii (BO), G. wrayi (GW), D. strictus (DS), and B. multiplex (BMA). Letters indicate significant differences among the two nutrient
treatments (LSD, p <0.05).
1048
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EFFECTS OF HIGH NUTRIENT SUPPLY 1049
Figure 2 Total aboveground fresh mass (kg) produced over the one-year experiment for low and high-nutrient
treatments for T. siamensis (TS); B. tuldoides (BV); D. strictus (DS); B. vulgaris (BVV); B. multiplex (BMA); G.
wrayi (GW); B. oldhamii (BO). Letters indicate significant differences between the two nutrient treatments (LSD,
p<0.05).
DS under the high-nutrient treatment. In decreasing order, the PSII is higher with the
high-nutrient treatment for DS, BVV, BO, and GW.
The SLA increased significantly (p <0.05) with the high nutrient treatment. The
SLA increased significantly for DS (p <0.05) from 231.4 to 279.3 g.cm−1for the low
and high-nutrient treatments respectively (Table 1). The SLA tended to increase with the
Tab l e 1 Chorophyll afluorescence measurements and specific leaf area (SLA) for the low and high-nutrient
treatment
Species Nutrient rate Fv/FmaYield (PSII)bSLA (g.cm−1)c
D. strictus Low 0,758 ±0,014bc 0,744 ±0,065b 231,40 ±18,10a
High 0,757 ±0,008bc 0,770 ±0,022b 279,30 ±32,70b
B. vulgaris Low 0,700 ±0,016a 0,650 ±0,043ab 192,60 ±23,20a
High 0,787 ±0,009c 0,705 ±0,048ab 215,00 ±16,70a
G. wrayi Low 0,714 ±0,019ab 0,561 ±0,050a 206,75 ±5,46a
High 0,720 ±0,023ab 0,649 ±0,087ab 209,98 ±7,30a
B. Oldhamii Low 0,723 ±0,027ab 0,751 ±0,034b 187,67 ±6,85a
High 0,742 ±0,010abc 0,672 ±0,080ab 203,15 ±7,15a
a Fv/Fm maximum quantum yield of photosystem II; b Yield effective quantum yield of photosystem II; cSLA
specific leaf area.
Values are means ±SE. The values with different letters indicate significant differences between the species
and the nutrient rates (LSD, p <0.05).
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1050 J. PIOUCEAU ET AL.
high-nutrient treatment for BO, GW, and BVV. In decreasing order, the SLA was higher
with the high-nutrient treatment for DS, BVV, GW, and BO.
Nitrogen and Phosphorus Contents
Applying a higher nutrient rate induced a significant increase of nitrogen in leaves
and culms (p <0.001). The nitrogen content in culms increased for all species by a factor
of 2 to 4 with the high-nutrient treatment compared to the low-nutrient treatment. For the
high-nutrient treatment the nitrogen content ranged from 29.4 to 36 g.kg−1for the leaves
and from 14.1 to 18.8 g.kg−1DM for the culms. DS was the species which store the higher
amount of nitrogen in leaves and culms (Table 2) and the species BO showed the best
response to the high-nutrient treatment with an increase in the leaves’ nitrogen content of
38% and 349% for the culms.
The phosphorus content was significantly increased in leaves and culms with the
high-nutrient treatment (p <0.001). The phosphorus contents between leaves and culm
was close and ranged from 1.8 to 4.3 g.kg−1for the leaves and from 1.9 to 3.5 g.kg−1DM
for the culms. BO was the species which store the higher amount of phosphorus in leaves
and culms (Table 2) and GW showed the best response to a high nutrient treatment with an
increase in the leaves and culms’ phosphorus content of 81%.
Depending on the species and the plant part, the potassium contents increased or
decreased with the high-nutrient treatment. For the DS species, the potassium content in
culms increased significantly from 7.7 to 14.6 g.kg−1DM (p <0.01) and tended to increase
in leaves from 16.5 to 17.3 g.kg−1DM. For the GW species, the potassium content tended
to increase in leaves from 12.6 to 14 g.kg−1DM and in culms from 5.5 to 6.9 g.kg−1DM.
Conversely, for the BVV and BO species, potassium decreased in leaves and culms.
Tab l e 2 Average nitrogen, phosphorus and potassium contents in leaves and culms in five bamboo species, for
the low and the high-nutrient treatment.
Species Plant part Nutrient rate Nitrogen (g/kg DM) Phosphorus (g/kg DM) Potassium (g/kg DM)
D. strictus Leaf Low 30,7±1,3c 1,8±0,1a 16,5±1,8cd
High 36 ±1,5d 2,5±0,3b 17,3±1,6d
Culm Low 6,2±0,9ab 1,3±0,3a 7,7±2ab
High 18,8±2,4e 1,9±0,4abc 14,6±3,6c
B. vulgaris Leaf Low 28,4±0,9c 1,7±0,0a 16,5±1,1cd
High 30,7±1,3c 1,8±0,1a 15,4±0,5cd
Culm Low 8,8±0,9b 1,5±0,2a 10,6±1,7bc
High 17,8±0,3de 2,3±0,2bc 9,5±1,8ab
G. wrayi Leaf Low 25,4±1,1b 1,8±0,1a 12,6±0,7ab
High 29,4±0,9c 3,2±0,1c 14 ±1bc
Culm Low 6,6±0,6ab 1,9±0,2ab 5,5±0,6a
High 14,1±1,1c 3,3±0,3d 6,9±1,5ab
B. oldhamii Leaf Low 22,2±1,7a 2,6±0,0b 9,8±1,4a
High 30,6±1,0c 4,3±0,2d 10,8±1a
Culm Low 3,4±0,2a 2,6±0,3c 8,9±2,2ab
High 14,9±1,9cd 3,5±0,3d 7,6±1,7ab
Values are means ±SE. The values with different letters indicate significant differences between the species
and the nutrient rates (LSD, p <0.05)
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EFFECTS OF HIGH NUTRIENT SUPPLY 1051
Tab l e 3 Allometric equations for fresh biomass determination by species
Species ´
Equation∗R2(%)
T. siamensis y=1,015 1,052 ∗x2,32091,6
B. tuldoides y=1,113 3,604 ∗x1,89784,4
D. strictus y=1,080 0.441 ∗x2,46989,5
B. vulgaris y=1,025 0,900 ∗x2,32398,3
B. multiplex y=1,008 0,034 ∗x3,33297,3
G. wrayi y=1,062 1,083 ∗x2,34794,5
B. oldhamii y=1,012 6,359 ∗x1,68895,3
∗y=Total above ground fresh biomass (g); x =Basal diameter (mm).
Aboveground Biomass and Nutrient Uptake
From the biomass results obtained using allometric equations (Table 3), and from the
number of culms counted after one year of growth, the annual aboveground biomass yield
and the density of culms per hectare was estimated, assuming a plantation density of 400
clumps/ha (Table 4). From the tissue’s nutrient content (Table 2) and the total aboveground
dry biomass, the nitrogen and phosphorus stored in the bamboo biomass was estimated
using a density of 400 clumps/ha (Table 4). This table shows that four years old bamboo
in containers produced between 1.1 and 2.6 t DM ha−1yr−1for the low-nutrient treatment,
and between 1.4 and 3.4 t DM ha−1yr−1for the high-nutrient treatment. The species TS,
BV, and DS produced the lowest amount of biomass with 1.4 t DM ha−1yr−1, and GW and
BO produced the highest amount of biomass with 3.1 and 3.4 t DM ha−1yr−1respectively.
The density of culms per hectare varied between species. The species TS showed the
lowest culm density with the high-nutrient treatment, with a yield of 6268 culms.ha−1, and
the species BMA showed the highest culm density with a yield of 38,520 culms.ha−1.In
Table 4, the lowest amount of nitrogen stored in the aboveground biomass with the high-
nutrient treatment was for the species DS (30 kg.ha−1), followed by BVV (32 kg.ha−1),
GW (55 kg.ha−1), and BO (73 kg.ha−1). The species which stored the lowest amount
of phosphorus was DS (3 kg.ha−1), followed by BVV (4 kg.ha−1), GW (10 kg.ha−1),
BO (15 kg.ha−1). The species which stored the lowest amount of potassium was BVV
(17 kg.ha−1), followed by DS (22 kg.ha−1), GW (27 kg.ha−1), and BO (33 kg.ha−1).
DISCUSSION
Growth of Clumping Bamboo Species under High Nutrient Rates
The high-nutrient treatment had an effect on both the number of culms produced and
the culm diameter. We did not observe any effect on culm height and culm wall thickness,
contrary to Shunshan (1994), who observed that culm wall thickness decreased with the
application of mineral fertilizer with Phyllostachys pubescens J. Houz. As shown in Figures
1a and 1b, the morphological responses mainly depended on the bamboo species. For the
species BVV, TS, BO and DS, we observed an increase in the number of culms produced
as previously described in other studies (Kleinhenz and Midmore 2002; Kleinhenz et al.
2003; Razak and Isma¨
ıl 2006). Our results showed that culms diameter was also decreased
for these species, a response that has never been observed to our knowledge. Conversely,
for the species GW high nutrient rates decreased the number of culms produced, but culm
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Tab l e 4 Estimate of biomass yield, density of culms and nutrient uptake during the year of experimentation for a plantation of 400 clumps/ha
Nutrient Fresh aboveground Dry aboveground Initial culm Final culm Nitrogen Phosphorus Potassium
Species rate biomass (t/ha/yr) biomass (t/ha/yr) density (culm/ha) density (culm/ha) (kg/ha) (kg/ha) (kg/ha)
T. siamensis Low 2,7±0,51,6±0,3 4000 6000 — — —
High 2,8±0,51,4±0,3 2800 6268 — — —
B. tuldoides Low 2,1±0,21,1±0,1 8132 13200 — — —
High 3,1±0,41,4±0,2 5732 11068 — — —
D. strictus Low 3,2±0,51,6±0,3 4932 10800 14 ±42±113±4
High 3,1±0,71,4±0,3 10280 23720 30 ±93±122±7
B. vulgaris Low 2,7±0,21
,4±0,1 6268 9068 17 ±12±116±2
High 3,2±0,81,5±0,4 3732 6932 32 ±84±117±3
B. multiplex Low 2,3±0,21,2±0,1 16132 30132 — — —
High 3,5±0,11,7±0,1 17468 38520 — — —
Gigantochloa wrayi Low 4,7±0,32,6±0,2 13868 27880 29 ±15±118±2
High 5,8±0,43,1±0,2 12268 23068 55 ±610±127±6
B. oldhamii Low 4,5±0,52,2±0,3 8800 12532 18 ±36±220±1
High 7,3±0,73,4±0,3 10400 16932 73 ±915±233±5
Values are means ±Standard Error.
1052
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EFFECTS OF HIGH NUTRIENT SUPPLY 1053
diameter was significantly larger. Azmy et al. (2004) reported a similar increase of G.
scortechinii culm diameter in response to fertilization.
The growth of bamboo mainly depends on the rhizome. Li et al. (2000) suggest
that the increase in nutrient rate releases more buds from dormancy from the rhizome,
increasing the number of shoots. However, in this study the shoots developing from these
buds ultimately had the same size despite fertilization. In our study, the diameter of shoots
was also affected suggesting a change in the ontogeny of culms on the contrary to Li et al.
(2000). The change in the ontogeny is probably a characteristic of the sympodial bamboo
(pachymorph rhizome) that cannot colonize their environment by the rhizome elongation
as well as the monopodial bamboo (leptomorph rhizome) studied by Li et al. (2000).
Our results suggest that an increase in culm number implies a decrease of the diameter
of shoots and vice-versa. These results may reveal two separate growth strategies in response
to a nutrient-rich environment for bamboo species to colonize their environment. In the first,
the bamboo species produce more culms to rapidly colonize their environment and in the
second, the bamboo produce culms with larger diameters, and therefore taller culms (Yen,
Ji, and Lee 2010) that can reach the light more easily in a dense forest. These speculations
are consistent when the different Asian origins with different ecological constraints are
factored in.
Despite changes in growth strategies the high-nutrient treatment tended to increase
the biomass yield of the species BV, BVV, BMA, GW, and BO, especially for BMA and
BO which showed a 50–60% increase in biomass. Conversely, the high-nutrient treatment
had little or no effect on the biomass yield of the TS and DS species. The final biomass
yield depended not only on the combination of each type of morphological pattern (i.e.,
number of new culms, diameter), but also on their magnitude. Indeed, the number of culms
in DS clumps significantly increased with nutrient rates, while culm diameter was strongly
reduced. However, the result of these two morphological responses in terms of biomass
yield was balanced, since the aboveground biomass remained similar for both the low
and high nutrient rate treatments (Fig. 2). Moreover, despite the high increase in biomass
(51%) and high density of culms (38520 culms; Table 4) of BMA, this species does not
produce the highest biomass yield among the seven species studied. These results indicate
that, whatever the species, the intrinsic morphological characteristics of the species, which
actually conditions the mass of culm, are an important factor in the global biomass yield.
All the species showed Fv/Fm values higher than 0.700 (Table 1), that is close to the
maximum value for a plant’s quantum yield (i.e., 0.83; (Bj ¨
orkman and Demmig 1987)).
These results reveal that all the bamboos were in a growth state during the experiment
and were not limited by any stress caused by the high nutrient rate. Indeed, the yield
parameter (PSII) of bamboo tended to increase between the beginning and the end of
the experiment (data not shown), and between the low and high-nutrient treatment for all
bamboo species (Table 1). These results are in compliance with the SLA increase for the
high-nutrient treatment. Several studies demonstrated that SLA is positively correlated to
the leaves’ photosynthetic activity and to the increase of their nitrogen content (Reich,
Michael and Ellsworth 1997; Wright et al. 2004; Jin et al. 2011). Indeed, applying the
high-nutrient treatment increased the leaves’ nitrogen content significantly (Table 2), as
observed by several authors (Li et al. 1998; Kleinhenz and Midmore 2001; Kleinhenz et al.
2003).
The nitrogen content in leaves range from 29.4 and 36 g.kg−1DM with the high
nutrient rate, that is close to the value of 3.0% recommended by Kleinhenz et al. (2003)
for optimal yields. For the culms, the nitrogen content was two to four times higher for
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1054 J. PIOUCEAU ET AL.
the high-nutrient treatment than for the low-nutrient treatment. The maximum phosphorus
content in leaves and culms was 4.3 and 3.5 g.kg−1DM respectively for the species BO.
These results are four times higher than those found in existing literature. Shanmughavel
and Francis (1997) reported, for a mature natural forest (without fertilization), that the
nitrogen content in culms and branches ranged from 6.0 to 8.9 g.kg−1, and the phosphorus
content in leaves from 0.8 to 1, and 0.6 to 0.9 g.kg−1in culm and branches for Bambusa
bambos (L.) Voss. These results suggest that when a high nutrient rate is supplied to the soil,
bamboo species are able to increase their ability to store nutrients in their tissues, especially
in the culms. Indeed the culms showed an increase of 102 to 349% in the nitrogen stored in
their tissue with the high-nutrient treatment. This increase corresponds to the storage ability
of old culms to store nutrients before the shoot emergence (Li et al. 2000; Kleinhenz and
Midmore 2001). Indeed, carbohydrates are stored in old culms’ parenchyma cells before
being remobilized and rapidly translocated through the rhizome system to provide the
growth of new culms.
We observed a significant increase of nitrogen and phosphorus content in leaves
and culms with the high-nutrient treatment but, for potassium, the increase was only
significant for the species DS. These results comply with Li et al. (1998) who report
no significant increase in potassium content in leaves with increasing fertilization for
Phyllostachys pubescens J. Houz. According to Kleinhenz and Midmore (2001), potassium
is the most element stored by bamboo tissues and the management of K application is
the most important measure to improve bamboo productivity. In our study the potassium
content did not show variations between treatments indicating that bamboo growth was not
limited by the lack of this element.
Biomass Yield and Sizing of Bamboo Plantation
for Wastewater Treatment
The species GW and BO were the most productive bamboo species among the seven
species studied, with a biomass yield range of 2.6 to 3.1 and 2.2 to 3.4 t DM ha−1yr−1
respectively. They were also the species that stored the highest amounts of nitrogen and
phosphorus in the total aboveground biomass per hectare, with the high-nutrient treatment
(Table 4). In its aboveground parts, the species GW may contain 55, 10, and 27 kg.ha−1
of N, P, and K respectively, and the species BO 73, 15, and 33 kg.ha−1of N, P, K, based
on a 4 year-old plantation with a plantation density of 400 clumps/ha. For a plantation of
1600 clumps/ha, we could expect an uptake of 290 kg.ha−1for nitrogen and 57 kg.ha−1
for phosphorus in the aboveground part of the species BO. These values are for a young
plantation, but a mature plantation will absorb more nitrogen and phosphorus. Kleinhenz
et al. (2001) reported an accumulation of 131 to 619 kg.ha−1of nitrogen, 54 to 97 kg.ha−1
of phosphorus and 178 to 277 kg.ha−1of potassium. According to these values, the surface
needed for wastewater treatment could be optimized according to the bamboo species’
ability for storing nitrogen and phosphorus in their aboveground parts. Thus, the optimal
volume of wastewater spread on the bamboo plantation could be determined to limit the
leaching of nitrogen and phosphorus away from the rhizosphere.
CONCLUSION
No adverse effects on the growth of young bamboos were observed by the application
of high nutrient rates. All the bamboo species studied produced more or the same amount
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EFFECTS OF HIGH NUTRIENT SUPPLY 1055
of aboveground biomass with the higher nutrient supply. Applying high nutrient rates
on several bamboo species induced different morphological responses depending on the
species. With the increase of nutrient rate, two growth strategies were observed: either the
number of culms increased and their diameter decreased, or the number of culm decreased
and their diameter increased. The latter result has never been reported to the best of
our knowledge. Both types of morphological pattern tended to increase the aboveground
biomass yield. Our results suggest that all the bamboo species studied can be used for
wastewater treatment. However, the species Gigantochloa wrayi Gamble and Bambusa
oldhamii Munro were the most productive bamboo species, storing the highest amounts of
nitrogen and phosphorus in their aboveground parts. These results need to be confirmed by
field trials, in order to quantify the nutrients stored by mature bamboo plantation and those
retained in the soil.
ACKNOWLEDGMENTS
The research was funded by the following French governmental funds: “Fonds unique
interministeriel”, as part of the “Run Innovation II” project, supported by Qualitropic, the
Reunion Island competitive cluster. We would like to thank all the team at Phytorem SA
for their support and Patrick Legier and Jocelyn Idmond at the CIRAD Laboratory (Saint
Denis, Reunion Island) for their availability and useful advice. We also would like to thank
Alexandre Perrusot (Bambouseraie du Guillaume, Reunion Island, France) who shared his
bamboo knowledge with us, and allowed us to carry out the experiment at his bamboo
nursery. Huge thanks go to Remi Hidouci, St´
ephane Maillot, Laurent De Fondaumi`
ere, and
Charles-Lee Hoareau for their help in collecting field data and for their technical support.
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Effects of High Nutrient Supply on the
Growth of Seven Bamboo Species
Julien Piouceau a b , Grégory Bois a , Frédéric Panfili a , Matthieu
Anastase a , Laurent Dufossé b & Véronique Arfi a
a PHYTOREM S.A., site d’Areva, chemin de l’autodrome , Miramas ,
France
b Université de La Réunion, Laboratoire de Chimie des Substances
Naturelles et des Sciences des Aliments, site ESIROI-IDAI,
Département Agroalimentaire , Sainte-Clotilde , France
Accepted author version posted online: 08 Jul 2013.Published
online: 06 Feb 2014.
To cite this article: Julien Piouceau , Grégory Bois , Frédéric Panfili , Matthieu Anastase ,
Laurent Dufossé & Véronique Arfi (2014) Effects of High Nutrient Supply on the Growth of
Seven Bamboo Species, International Journal of Phytoremediation, 16:10, 1042-1057, DOI:
10.1080/15226514.2013.810583
To link to this article: http://dx.doi.org/10.1080/15226514.2013.810583
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