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Rice Science, 2016, 23(3): 119−131

Impact of Nitrogen, Phosphorus and Potassium on Brown

Planthopper and Tolerance of Its Host Rice Plants

Md Mamunur RASHID1, Mahbuba JAHAN2, Khandakar Shariful ISLAM2

(1Plant Physiology Division, Bangladesh Rice Research Institute, Gazipur, PO Box 1701, Bangladesh; 2Department of Entomology,
Bangladesh Agricultural University, Mymensingh, PO Box 2202, Bangladesh)

Abstract: The brown planthopper (BPH), Nilaparvata lugens (Stål), appeared as a devastating pest of
rice in Asia. Experiments were conducted to study the effects of three nutrients, nitrogen (N),
phosphorus (P) and potassium (K), on BPH and its host rice plants. Biochemical constituents of BPH
and rice plants with varying nutrient levels at different growth stages, and changes in relative water
content (RWC) of rice plants were determined in the laboratory. Feeding of BPH and the tolerance of
rice plants to BPH with different nutrient levels were determined in the nethouse. Concentrations of N
and P were found much higher in the BPH body than in its host rice plants, and this elemental
mismatch is an inherent constraint on meeting nutritional requirements of BPH. Nitrogen was found as
a more limiting element for BPH than other nutrients in rice plants. Application of N fertilizers to the rice
plants increased the N concentrations both in rice plants and BPH while application of P and K
fertilizers increased their concentrations in plant tissues only but not in BPH. Nitrogen application also
increased the level of soluble proteins and decreased silicon content in rice plants, which resulted in
increased feeding of BPH with sharp reduction of RWC in rice plants ultimately caused susceptible to
the pest. P fertilization increased the concentration of P in rice plant tissues but not changed N, K, Si,
free sugar and soluble protein contents, which indicated little importance of P to the feeding of BPH
and tolerance of plant against BPH. K fertilization increased K content but reduced N, Si, free sugar
and soluble protein contents in the plant tissues which resulted in the minimum reduction of RWC in
rice plants after BPH feeding, thereby contributed to higher tolerance of rice plants to brown
planthopper.
Key words: Nilaparvata lugens; relative water content; host tolerance; nitrogen; phosphorus; potassium;
rice; nutrient subsidy

The brown planthopper (BPH), Nilaparvata lugens nitrogen, sugars, amino acids and semio-chemicals in
(Stål) (Homoptera: Delphacidae), is a major insect host plants (Fischer and Fiedler, 2000), and plant
pest of rice in Asian countries, causing heavy crop water content is another important factor (Slansky and
damage through ‘hopper burn’ (Bottrell and Schoenly, Rodriguez, 1987). Several studies have indicated the
2012; Ali et al, 2014). Nutrition management is one of importance of host plant quality on herbivorous
the most important practices for high production insects (Awmack and Leather, 2002; Bado et al, 2002).
system, but it may affect on host-insect interaction. Abiotic heterogeneity through crop nutrition can affect
Insect behavior and life parameters are affected by the susceptibility of plants to insect pests by altering
environmental factors, such as temperature, moisture, plant tissue nutrient levels (Altieri and Nicholls, 2003)
habitat morphological and chemical components of and morphology (Moon and Stiling, 2000). Excessive
host plants, especially by the nutrients, such as and/or inappropriate use of inorganic fertilizers can

Received: 11 May 2015; Accepted: 26 August 2015

Corresponding author: Md. Mamunur RASHID ([email protected])
Copyright © 2016, China National Rice Research Institute. Hosting by Elsevier B
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V This is an open access article under the CC BY-NC-ND license
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This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/)
Peer review under responsibility of China National Rice Research Institute
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120 Rice Science, Vol. 23, No. 3, 2016

cause nutrient imbalances and lower pest resistance can be expected to occur only during prolonged K
(Altieri and Nicholls, 2003; Marazzi et al, 2004). deficiency (Wyn Jones, 1999). It was reported that
Outbreaks of planthopper populations are sensitive plant damage by insect is comparatively less in K
barometers of crop mismanagement (Sogawa et al, 2009). applied plants due to reduced carbohydrate accumulation,
Nitrogen (N) content is regarded as an indicator of elimination of amino acids (Baskaran et al, 1985),
plant quality and also one of the most important higher silica content and increase in the sclerenchymous
performance limiting factors of herbivores (Lu and layer (Dale, 1988). The mechanism of rice plants
Heong, 2009). N application is reported to induce damaged by BPH through hopper burn is similar with
succulence in rice plants which makes them more that of drought stress which is closely related to the
prone to insect pests (Salim, 2002b). Heavy applications relative water content (RWC) of plants. Typical RWC
of N fertilizer may not affect insect biology directly in rice plants at wilting is in the range of 60% to 70%
but change the host-plant morphology, biochemistry (Lu et al, 2004).
and physiology, which can improve nutritional Host plant tolerance to BPH is an important issue
conditions for herbivores (Bernays, 1990), thus for management of BPH. A little information is
playing a key role in modifying and reducing host available on the effects of N, P and K on biochemical
resistance to them (Barbour et al, 1991). N limitation composition of BPH and its host rice plants.
is well documented in insect herbivores, but Information on the relationships between biochemical
phosphorus (P) limitation is poorly studied (Huberty compositions of rice plants and its tolerance to BPH
and Denno, 2006), although insect herbivores require particularly in reference to different nutritional status
not only N but also P to synthesize their proteins is also very limited. We studied the effects of three
(Sterner and Elser, 2002). P is required for ATP and major plant nutrients i.e. N, P and K on the
nucleic acid synthesis (RNA and DNA), and thus biochemical compositions of both BPH and its host
protein production (Sterner and Elser, 2002). As a rice plants, feeding of the insect, fluctuations of RWC
result, its limitation can impose severe consequences in plants, and tolerance of plants to the pest BPH.
for cellular function and ultimately the growth rate of
consumers (Elser et al, 2000; Sterner and Elser, 2002). MATERIALS AND METHODS
P limitation has been documented widely in many
Preparation of soil and host plant establishment
species of aquatic invertebrates, particularly in
Daphnia (Elser et al, 2001). Potassium (K) has a The potted plants of different nutrient levels were
critical role in plant physiology (Wyn Jones, 1999). In prepared separately for the experiments at nethouse of
rice, K provides regulatory control over different Bangladesh Rice Research Institute, Gazipur, Bangladesh.
processes like transpiration, starch synthesis, sucrose Pot soil was fertilized with three levels of each
translocation, respiration and lipid synthesis (Tisdale nutrient: N (0, 100 and 200 kg/hm2), P (0, 20 and 40
et al, 1985). K nutrition has a profound effect on the kg/hm2) and K (0, 60 and 120 kg/hm2) and combination
profile and distribution of the primary metabolites in of all the levels. The soil was slightly acidic (pH 5.3),
plant tissues. Changes in metabolite concentrations low organic carbon (0.72%) and deficient in N, P and
induced by K are multiple and it includes K K, where levels of all the three nutrients were below
dependence of metabolic enzymes, photosynthesis and the critical level. Approxiamately 2 kg dry soil was
long-distance transport. The primary metabolites such taken in each pot with 16 cm height and 14 cm
as soluble sugars particularly reducing sugars, organic diameter. The exact amount of input fertilizers was
acids and amino acids tend to increase in K deficient calculated based on the amount of soil in each pot.
plants (Amtmann et al, 2008). Approximately 60 Fifteen-day-old rice seedlings were transplanted (3
enzymes have been shown to depend on K in vitro for hills per pot and 2 seedlings per hill) in each pot. The
their activities, many of which are involved in sugar or rice variety BR3 was selected because of its year
N metabolism (Wyn Jones and Pollard, 1983). It is round growing habit and susceptibility to BPH. To
also important to note that a direct effect of K obtain continuous supply of host plant materials for
nutrition on enzyme activity occur only if cytoplasmic each BPH culture, the experiment seedlings were
K concentrations are changed (Amtmann et al, 2008). transplanted at a 15 d interval. Plants with different
Because of efficient cellular K homeostasis (Walker nutrient treatments were labeled and placed under
et al, 1996), a decrease of cytoplasmic K concentration natural condition in nethouse. All the factorial pot
Md Mamunur RASHID, et al. Nutrients Induced Tolerance in Rice Plants to BPH 121

experiments with 27 treatment combinations were laid determination of the nutrient content of BPH, four
out in a completely randomized design and replicated samples each with 25 emerging adult planthoppers of
four times considering each pot as a replicate. each treatment was collected and oven-dried prior to
analysis. They were ground in a Wiley Mill (Thomas
Effects of nutrient subsidies on biochemical
Scientific Inc., USA) and analyzed for contents of N,
constituents of rice plants and BPH
P and K. The grand mean of all experimental
Effects of N, P and K treatments on biochemical treatment plants and BPH were used to assess the
compositions of rice plants were determined on plants overall chemical contents of rice plants and BPH.
that were never exposed to BPH. The effects on rice Mismatch in N, P and K contents between rice plant
plants at four stages, namely mid-tillering, panicle and BPH was compared.
initiation, heading and maturity (soft dough) stages,
Effects of nutrient subsidies on honeydew secretion
were determined from four randomly chosen pots for
each treatment. Four plants were taken randomly from Amount of feeding BPH was measured indirectly by
each pot and oven-dried at 70 °C ± 5 °C for 72 h. the quantity of honeydew secretion. The honeydew
Plant samples were then ground in a Wiley Mill excreted by BPH reared on rice plants with different
(Thomas Scientific Inc., USA) and analyzed for nutrient treatments were collected in a feeding
contents of N, P, K, silicon (Si), total free sugars and chamber following the method developed by Pathak
soluble proteins. For analysis of total N, 200 mg and Heinrichs (1982) with partial modification. The
ground sample was digested in a micro Kjeldahl flask feeding chamber consisted of an inverted transparent
with the same weight of catalyst mixture plastic cup resembling a conical funnel and placed
(K2SO4:CuSO4:Selenium, 50:10:1) and 3 mL of over a filter paper treated with 0.2% Bromocresol
concentrated H2SO4 until clear, cooled and brought up green solution. The whole apparatus was rested on a
to the volume with distilled water. N was determined plastic petridish. Adult females with uniform age and
volumetrically by the micro Kjeldahl distillation size were collected from the mass culture and starved
method (Yoshida et al, 1976). For analysis of P and Si for 3 h. The leaf sheaths of the plants in each
concentrations, 1 g sample was digested with 10 mL treatment were wiped well with tissue paper to remove
acid mixture of HClO4, HNO3 and H2SO4 any kind of moisture on the surface. Five 3-day-old
(300:750:150) on a hot plate at 500 °C until a BPH adult females were placed into the conical
gelatinous white residue remained to which distilled chamber through a hole at the top of the cup. A
water was added after cooling. The mixture was cotton-wad was then placed in the hole to prevent
filtered through Whatman #42 filter paper. P from escaping of the insects. The BPH was allowed to
concentration was determined colorimetrically through feed for 48 h and then the filter paper was removed.
a Spectro Photometer (V-630, JASCO, Japan) at 420 Areas of the filter paper receiving the honeydew
nm wavelength. The residue on the filter paper was turned purple bluish. The spots were marked on
burnt at 500 °C for 4 to 5 h for gravimetric tracing paper and the feeding areas were measured by
determination of crude Si concentration. For analysis counting the squares in mm2 girded transparent graph
of K concentration, 1 g plant sample was soaked in 25 paper.
mL of 1 mol/L HCl for 24 h and filtered through
Effects of nutrient subsidies on tolerance of rice
Whatman #43 filter paper. K concentration was
plants to brown planthopper
analyzed in the filtrate using a Flame Photometer (410
FP, Sherwood, UK) at 214 nm wavelength. For The changes of RWC in rice plants and the severity of
estimation of soluble protein and total free sugar plant damage due to BPH feeding were determined. A
concentrations, plants were analyzed based on dry total of 100 the second instar nymphs were introduced
weight (Lowry et al, 1951; Yoshida et al, 1976). into mylar cage containing 35-day-old potted rice
Brown planthopper population required for the plants trimmed to 6 tillers for all the 27 treatments.
experiments were obtained from a mass culture raised The RWC of each treatment was measured twice, first
on rice plants with native nutrients maintained in before infestation and then at 5 d after release of BPH
nethouse. A total of 200 the first instar nymphs of on rice plants, and the reduction of RWC in plants due
BPH were released on 30-day-old potted rice plants to BPH feeding was calculated. To determine RWC in
established with different nutrient treatments. For rice plants, four samples were collected from each
122 Rice Science, Vol. 23, No. 3, 2016

treatment. The top most fully expand leaves were tolerance to the pest.
sampled and the mid leaf section of about 5–10 cm2
was cut with scissors and then subsequently placed in RESULTS
a pre-weighed airtight vial to obtain leaf sample
weight (W). The leaf samples were immediately Effects of nutrient subsidies on biochemical
hydrated by distilled water up to full turgidity in the compositions of rice plants and BPH
refrigerator at about 10 oC for 4 h. They were then Nitrogen fertilizer application to the rice plants
taken out of water, well dried with filter paper and resulted in a significant increase in N content (P <
weighed to obtain the fully turgid weight (TW). 0.001) in both rice plants and BPH (Table 1 and Fig.
Samples were then dried at 80 oC for 24 h and 1-A). Application of K decreased N content in rice
weighed to calculate the dry weight (DW). Relative plants significantly (P < 0.001) but not in BPH (P =
water content was computed as: 0.069) (Table 1 and Fig. 1-C). However, P application
RWC (%) = [(W – DW) / (TW – DW)] × 100. did not significantly change N content of both rice
Damage to the rice plants was rated daily based on plants (P = 0.078) and BPH (P = 0.14) (Table 1 and
the standard evaluation system for rice (IRRI, 1980) Fig. 1-B). Fertilizing with P significantly increased the
as follows: 0, no damage; 1, very slight damage; 3, P content in rice plant tissues (P < 0.001) but not in
partially yellowing of the first and second leaves of BPH (P = 0.068) (Table 1 and Fig. 1-E). Different
most plants; 5, pronounced yellowing and stunting or levels of N and K subsidies to rice plants did not alter
wilting of 10% to 25% of the plants; 7, wilting or dead P content in both rice plants and BPH (Table 1 and
of more than half of the plants and severely stunting Fig. 1). Increase of K application significantly
or dying of the remaining plants; 9, death of all plants. increased K content in rice plants (P < 0.001), but K
The survival duration of rice plants or the duration content remained unchanged in BPH (P = 0.172)
from infestation with BPH to the death of rice plants (Table 1 and Fig. 1-I). Different levels of N and P
was recorded. application to rice plants did not alter K content in
both the organisms (P > 0.05, Table 1 and Fig. 1).
Statistical analysis
Application of the nutrients N and K was found to
Analysis of variance (ANOVA) was performed using decrease the Si content in rice plants significantly (P <
Crop Stat 7.2 (IRRI, 2007). The mean differences 0.001, Table 1 and Fig. 2). This decreasing rate of Si
among the treatments were compared by multiple was more than 50% with N application but it was
comparison tests using the Duncan’s multiple range about 11% with K. The amount of Si remained
test (DMRT). A statistic paired sample t-test was used unaffected with the application of P fertilizer to rice
to assess the mismatch in N, P and K stiochiometry plants (P = 0.133, Table 1 and Fig. 2-B). No
between rice plants and BPH (SPSS, 2007). significant change in total free sugar content in rice
Regression analysis was conducted using Crop Stat plants was found due to application of N (P = 0.477)
7.2 (IRRI, 2007) to examine the effect of independent and P (P = 0.885), but it caused a significant reduction
variables plant tissue nutrients i.e. N, P, K, Si, total with the application of K (P < 0.001) (Table 1 and Fig.
free sugars and soluble proteins on the dependent 2). There was an increase in soluble protein content in
variables, honeydew secretion by BPH and plant rice plants with increasing levels of N (P < 0.001, Fig.

Table 1. Analysis of variance for biochemical compositions in rice plants and brown planthopper (BPH) affected by nitrogen (N), phosphorus
(P) and potassium (K) subsidies (F values).
Source of Nitrogen Phosphorus Potassium Silicon Total free sugar Soluble protein
df
variance Rice BPH Rice BPH Rice BPH in rice in rice in rice
N 2 2166.51** 12.87** 2.45 0.16 0.11 0.01 2 486.75** 0.73 3 300.13**
P 2 2.58 2.04 544.36** 2.77 0.45 0.15 2.33 0.12 0.72
K 2 392.74** 2.80 2.08 0.50 440.21** 1.77 33.03** 573.66** 822.94**
N×P 4 2.05 0.25 2.44 0.19 0.20 0.70 0.87 0.29 0.17
N×K 4 53.12** 0.85 0.94 0.56 0.03 0.92 3.73** 0.61 15.65**
P×K 4 2.21 1.04 2.28 0.74 0.14 0.67 0.75 0.07 0.21
N×P× K 8 1.40 0.60 1.26 0.58 0.17 1.69 0.86 0.10 0.29
Error 81
CV (%) 2.65 3.22 4.18 4.45 2.92 1.75 5.33 1.98 2.48
**, Significant at the 1% level of probability.
Md Mamunur RASHID, et al. Nutrients Induced Tolerance in Rice Plants to BPH 123

Fig. 1. Response of nutrient levels on nutrient contents of brown planthopper (BPH) and its host rice plants.
Bar indicates the standard error (SE).

2-A), but no change was recorded with the addition of

Mismatch in N, P and K content between rice
P (P = 0.494, Fig. 2-B). However, the concentration of
plants and brown planthopper
soluble proteins in rice plant tissues decreased
significantly with the application of K (P < 0.001, Nutrient content varied significantly between BPH and
Table 1 and Fig. 2-C). The interaction between its host rice plants as shown in Fig. 3. Concentrations
applied N and K was significant for concentration of of N and P in the body of BPH were significantly
N (P < 0.001), Si (P = 0.017) and soluble proteins (P higher than those in rice plant tissues at all the four
< 0.001) in the tissue of rice plants. growth stages, mid-tillering, panicle initiation,

Fig. 2. Response of nutrient levels on silicon (Si), total free sugar (TFS) and soluble protein (SP) contents in rice plants.
Bar indicates the standard error (SE).
124 Rice Science, Vol. 23, No. 3, 2016

a a

Fig. 3. Status of elemental contents in brown planthopper (BPH) and rice plants at different stages.
Bar indicates the standard error (SE).

100

Fig. 4. Feeding of brown planthopper (BPH) measured indirectly by honeydew excretion in different nutrient treated rice plants.
Bar indicates the standard error (SE).

heading and maturity stages (P < 0.001, Table 2). The of BPH was also around three times higher than that
concentration of N in BPH was around four times of the plants. In contrast, the concentration of K had
higher than that of rice plants. Similarly, the P content an opposite trend and it was significantly higher in
rice plant tissues at mid-tillering, panicle initiation and
Table 2. Mean comparison results for nitrogen (N), phosphorus (P)
heading stages than that of BPH (P < 0.001, Table 2).
and potassium (K) contents between brown planthopper However, K concentration did not differ significantly
(BPH) and its host rice plants (t value). between BPH and rice plants at the maturity stage of
Rice stage df N content P content K content the plants (P = 0.057, Table 2).
Mid tillering 26 150.32** 111.80** 80.90**
Panicle initiation 26 106.79** 134.16** 21.95**
Effects of nutrient subsidies on honeydew excretion
Heading 26 163.32** 136.40** 162.92**
Maturity 26 163.72** 108.38** 1.94
Effects of varying levels of N, P and K on honeydew
**, Significant at the 1% level. secretion by BPH are presented in Fig. 4. Amount of
Md Mamunur RASHID, et al. Nutrients Induced Tolerance in Rice Plants to BPH 125

Table 3. Analysis of variance for honeydew secretion, changes in relative water content (RWC) and complete damage duration of rice plants
feeding brown planthopper (BPH) as affected by nitrogen (N), phosphourus (P) and potassium (K) subsidies (F value).
Source of RWC of BPH RWC at 5 d after 9th grade plant damage
df Honeydew secretion Reduction of RWC
variation free plants infestation by BPH duration
N 2 601.80** 274.53** 1 338.95** 1 385.84** 242.70**
P 2 0.04 9.36** 0.55 0.56 0.66
K 2 2.74 37.75** 17.56** 16.46** 19.70**
N×P 4 0.08 0.82 0.18 0.17 0.69
N×K 4 0.14 4.55** 11.48** 10.41** 2.62*
P×K 4 0.06 0.72 1.45 1.44 1.43
N×P× K 8 0.08 1.24 1.46 1.39 1.01
Error 81
CV (%) 4.78 0.78 1.25 2.43 8.54
* and **, Significant at the 5% and 1% levels of probability, respectively.

honeydew excretion increased significantly with N

Effects of nutrient subsidies on tolerance of rice
application to rice plants (P < 0.001, Table 3). However,
plants to brown planthopper
it did not increase linearly with the N application rate.
The highest amount of honeydew secretion was recorded Effects of different levels of N, P and K on RWC of
from the individuals feed on plants treated with BPH unfed and fed rice plants are presented in Fig. 5.
nitrogen level at 100 kg/hm2 followed by the levels at RWC in BPH free rice plants increased significantly
200 and 0 kg/hm2. Honeydew secretion by BPH did with the application of all the three nutrients N, P and
not differ significantly among different P treatment K (P < 0.001, Table 3). Reduction rate of RWC in rice
levels (P = 0.959, Table 3). Increasing amount of K plants due to BPH feeding differed significantly
fertilizer application to rice plants promoted to a slight among different nutrient treatments. It decreased
decrease in the honeydew excretion by BPH, but it significantly at higher rate in N applied plants than
was statistically insignificant (P = 0.07, Table 3). without N application (P < 0.001, Table 3). Reduction
Analysis of variance did not detect significant effect of RWC by BPH infestation was significantly less in
from the interactions of the three nutrients (N, P and K) plants fertilized with any level of K than in plant
for honeydew secretion by BPH (P > 0.05, Table 3). without K application (P < 0.001) and interaction

Fig. 5. Relative water content (RWC) and reduction of RWC due to brown planthopper (BPH) feeding after 5 d in different nutrient treated
rice plants after release of BPH.
Bar indicates the standard error (SE).
126 Rice Science, Vol. 23, No. 3, 2016

P0 K0
N0
P20 K60
N100
P40 K120
N200

Fig. 6. Dynamics of damage grade of rice plants by brown planthopper (BPH) as affected by different levels of nutrient application.
Bar indicates the standard error (SE).

between N and K was significant (P < 0.001, Table 3). duration to cause complete damage when K was
However, there was no significant difference among P applied to the plants (P < 0.001) and interaction
fertilization treatments in changing RWC of rice between N and K was significant (P = 0.047) (Table
plants damaged by BPH (P = 0.587, Table 3). 3). Complete plant damage duration (9th grade)
Interaction effects of N and P, P and K and all the remained unaffected with whatever the level of P was
three nutrients (N, P and K) were insignificant for applied (P = 0.821, Table 3). No significant difference
reduction of RWC of rice plants by BPH feeding (P > was evident in the duration for complete plant damage
0.05, Table 3). by BPH when the interactions of N and P, P and K
Complete damage (9th grade) durations by BPH and all the three nutrients (N, P and K) were taken into
injury varied significantly among rice plants fertilized consideration (P > 0.05, Table 3).
with different nutrient treatments and are presented in Relationships between life parameters of BPH and
Fig. 6. The duration from infestation with the second chemical contents in rice plants
instar BPH nymphs to the death of rice plants declined
significantly with the increase of N application rate (P < All the relationships of dependent variables (honeydew
0.001, Table 3). While, it required significantly more secretion by BPH and rice plant tolerance to the pest)

Fig. 7. Relationship between brown planthopper (BPH) feeding and different nutrients nitrogen (N), phosphorus (P), potassium (K), silicon
(Si), total free sugar and soluble proteins contents in rice plants.
Md Mamunur RASHID, et al. Nutrients Induced Tolerance in Rice Plants to BPH 127

Fig. 8. Relationships between nitrogen (N), phosphorus (P), potassium (K), silicon (Si), total free sugar and soluble protein contents in rice
plants and its 9th grade damage by brown planthopper (BPH).

with independent vatiables plant tissue nutrients (N, P, levels of N, P and K were used in this study. The
K, Si, total free sugars and soluble proteins) are ranges of N, P and K were chosen to bracket those
summarized in Figs. 7 and 8. Relationships between used in previous laboratory experiments and to
honeydew secretion and plant tissue nutrients N, Si, include the spectrum of nutrient contents that has
total free sugars and soluble proteins fitted the linear occured in cultivated rice fields in Bangladesh.
model. Honeydew secretion positively correlated (P < Usually, for rice cultivation, the nutrients N, P and K
0.001) with concentrations of N, total free sugar and are recommended at the rates of 100, 20 and 60
soluble protein but negatively with Si in rice plant kg/hm2, respectively, but sometimes some of the
tissues. However, linear but weak relationship was farmers exceed the usual level with the expectation to
observed between honeydew secretion by BPH and obtain higher yield. In many cases, the increase of the
nutrients concentration of P (P = 0.052) or K (P = nutrients by them is not proportionate. Application of
0.059) in rice plant tissues. Relationship between over doses of N is frequently common and this can be
complete damage duration of rice plants due to BPH a reason for the BPH outbreak in rice fields.
feeding and N, K, Si, total free sugar and soluble Considering this context, the doses of the present
protein contents in rice plant tissues also showed experiment were selected to determine the consequences
linear model. Complete plant damage duration was of variable amount of N, P and K as subsidies to the
negatively correlated with plant tissue N, total free plants and its pest BPH. In general, enhancement of
sugar and soluble protein contents in rice plant tissues nutrient subsidies results in higher nutrient content in
(P < 0.001), while positively correlated with K and Si rice. Increased supply of inorganic fertilizers enhances
contents in rice plant tissues. However, relationship nutrient uptake through their roots. In the present
between damage duration of rice plants and its P study, increasing levels of N application to rice plants
content was also linear but weak (P = 0.053). resulted in a significant increase in N content in plant
tissues. Moreover, it also increased soluble protein
DISCUSSION content and decreased Si content in the leaf sheath of
rice plants, which might play a vital role in BPH
N, P and K are essential macronutrients of rice that feeding and host plant tolerance. A report indicates
must often be applied in rice fields through different that supplementation of N had similar effect and also
forms of fertilizers to maintain the productivity of found to decrease the level of Zn in rice plants (Salim,
cropped soil and prevent deficiencies of these 2002b). P content in rice plant tissue was found higher
essential nutrients from limiting crop yields. Three due to application of P and the maximum amount of P
128 Rice Science, Vol. 23, No. 3, 2016

was recorded when the plant was treated with 20 any significant change in feeding of the pest probably
mg/kg P, which is in agreement with the reports of for its lower requirements than N. However, it is quite
Subbaiah (1991) and Mongia et al (1998). Application difficult to draw a complete conclusion about the
of K fertilizer to the rice plants increased the mismatch of P between the BPH body and rice plant
concentration of K in plant tissues, but it decreased the tissues, which demands further investigation.
contents of N, Si, soluble protein and total free sugar. Concentration of K in rice plant tissues was higher
It was reported that increase in the application of K in than that of the BPH bodies, suggesting that rice plant
the culture solution increased K content, but decreased itself is a good food source of K for BPH at anywhere
N, Si and soluble protein contents in rice plants (Salim, grown at any level.
2002a). Other reports showed K fertilization seemed Feeding of BPH is usually determined indirectly by
to increase K level (Stiling and Moon, 2005; Sarwar, measuring the amount of honeydew secretion. In the
2012) and decreased N level (Clark, 1982) in plant present study, honeydew excretion by BPH increased
tissues. Experimental results clearly indicated that with the increase of the N level but not with P and K
increasing application rate of N fertilizer to rice plants levels. Nitrogen application to the rice plants up to
have significantly increased the N content of BPH but 100 kg/hm2 resulted in the increase of honeydew
the levels of P and K remained unchanged. Fertilization excretion. This might be for the higher preference of
with P and K to rice plants did not significantly alter BPH to suck more on plants fertilized with 100
the N, P and K contents in the body of BPH. kg/hm2 N containing higher concentrations of N and
Study on nutrient mismatch between the plant and soluble protein and lower Si concentration than those
insect is quite important for studying the feeding of plants without N fertilization. However, further
aspects of insects. The difference in the particular increase of the N dose to 200 kg/hm2 reduced
nutrient level in host plants and harbivour will play a honeydew excretion by BPH. This might be due to
vital role in causing damage to the plant. Some reports BPH decrease food consumption on better quality
showed that stoichiometric mismatches between the food resources, probably as it had reached the
insects’ requirements and their diet play an important saturation point earlier. There are many similar reports
role on the insect body elemental concentrations and that the rice plants supplied with N fertilizer have high
life history traits (Elser et al, 2000; Huberty and feeding rates and honeydew excretion (Lu et al, 2005;
Denno, 2006; Visanuvimol and Bertram, 2011). In the Prasad et al, 2005; Lu and Heong, 2009). Regression
present study, the concentrations of N and P in rice analysis showed that honeydew secretion was
plants were found remarkably low compared to those positively correlated with N, total free sugar and
in BPH bodies. This mismatch highlighted the poor soluble protein contents but negatively correlated with
nutrient quality of rice plants for BPH. Many authors Si content. Relatively less amount of honeydew
reported that the concentrations of mineral nutrients secretion by BPH was recorded on N deficient. This
are lower in plants than in herbivores (Elser et al, could be explained in the ways that, the stylet of the
2000), and specially, phytophagous insects have much BPH might not reach the phloem in those plants
higher N and P contents than their host plants (Elser containing more Si due to change in plant texture and
et al, 2000; Fagan et al, 2002; Visanuvimol and some chemical reasons (Dale, 1988) or BPH could not
Bertram, 2011). Insects with relatively high body suck the phloem sap due to absence of feeding
nutrient concentrations require nutrient-rich foods stimulants like soluble proteins and free sugars
otherwise they would suffer reduced growth. As a (Baskaran et al, 1985). Phosphorus addition did not
consequence, insects choose foods that match their contribute to feeding status BPH as no effect was
stiochiometric requirements (Jensen et al, 2006). Our evident in changing concentrations of nutrients in rice
study clearly showed that BPH body contained very plants except its own level. However, K application
high amount of N, which indicated that requirement of reduced the concentrations of total free sugars and
this particular element is always demanding, as the soluble proteins in plant tissues, and at the same time,
host plants normally supplied insufficient amount of N. it reduced Si content. This might be the reason why no
These might be the important reasons why most marked change of honeydew secretion was found by
herbivores feed more on host plants with high N K application. It was reported that soluble sugar and
content. Although the concentration of P in rice plants amino acid contents tend to increase in N sufficient
is also lower than BPH, P fertilization can not cause and K deficient plants (Marschner, 1995). Nitrogen
Md Mamunur RASHID, et al. Nutrients Induced Tolerance in Rice Plants to BPH 129

(including nitrogen in amino acids and proteins) and decreased slightly when infested with BPH nymph
sugar are two major kinds of herbivore feeding compared to BPH free plants. RWC of 68.44% in rice
stimulants (Fischer and Fiedler, 2000), while higher plants with 200 kg/hm2 N supply damaged by 100
silica content and sclerenchymous layer can reduce nymphs for 5 d reached the wilting scale of RWC
the feeding rate on different host plants (Dale, 1988). (Panda and Khush, 1995). It may be explained that
Insects have intimate and subtle relationships with rice plants with higher N content bearing higher water
their host plants which can profoundly affect its potential can provide planthoppers at low density with
suitability to insect pests even minor changes in enough sap for their higher survival and faster growth.
physiological or chemical attributes of plants. In the However, at higher density of BPH, RWC of the
present study, duration to cause complete damage of plants was reduced sharply and the plants became
rice plants by BPH infestation was found to decrease wilted. This might due to the amount of sap sucked by
with the increase of N level. The increasing high density BPH exceeded those supplied by rice
susceptibility of rice plants was associated with higher plants, as there was more feeding rate of sap from host
feeding activities of BPH on rice plants with high N plants with N application. Hence, rice plants with
rate as this plant contains higher concentrations of enhanced N and soluble proteins and less effective
tissue N and soluble proteins but lower amount of Si. qualitative defensive chemicals can be more attractive
Heavy application of N fertilizers may be responsible to herbivores, suffering from increased levels of
for the heavy crop damage by insects (Lu et al, 2004). feeding and more plant damage.
Nitrogen has active role in amino acid production and
protein synthesis (Sterner and Elser, 2002). As a result ACKNOWLEDGEMENTS
concentrations of the primary metabolites amino acids
(main nutritional resource of insects) in the plant Authors thank M. Mahir UDDIN, Mainul HAQUE, M.
shoots were increased with increasing N availability Nazmul BARI, M. A. SALEQUE and Rumena
(Kajimura et al, 1995; Sauge et al, 2010). Many YASMEEN for their technical support in conducting the
secondary metabolites produced by plants act as experiments.
toxins and deterrents for pests and pathogens which
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