Full text of DOI:10.1080/096708700415571

INTERNATIONAL JOURNAL OF PEST MANAGEMENT, 2000, 46(3) 225±235
Impact of nitrogenous-fertilization on the population dynamics and natural control of rice
leaffolders (Lep.: Pyralidae)
(Keywords: Cnaphalocrocis medinalis, Marasmia patnalis, natural enemies, nitrogenous fertilization, population dynamics, rice)
²³
²
³
³
J. DE KRAKER* , R. RABBINGE , A. VAN HUIS , J. C. VAN LENTEREN and K. L. HEONG§
²
Laboratory of Theoretical Production Ecology, Wageningen University, Wageningen, The Netherlands
³Laboratory of Entomology, Wageningen University, Wageningen, The Netherlands
§
International Rice Research Institute, Los BanÄ os, Philippines
Abstract. The effect of nitrogenous-fertilization on the population
dynamics and natural control of rice leaffolders was studied in an
irrigated rice area in the Philippines. Nitrogen was applied at three levels
(0, 75 and 150 kg N haÐ 1), and its impact on crop growth and yield,
arthropod abundance, and rates of leaffolder parasitism and survival
was assessed with weekly samples. Rice plants were taller and had a
higher leaf nitrogen content with increasing levels of nitrogenous-
fertilization, but grain yield was highest at the medium nitrogen level.
Herbivores, predators, and parasitoids increased in abundance with
nitrogenous-fertilization level. The average density of rice leaffolder
larvae at the highest nitrogen level was eight times the density at zero
nitrogen level, and the peak percentage injured leaves increased from 5
to 35%. The strong increase in larval density was due to the positive
effect of nitrogenous-fertilization on egg recruitment and survival of
medium-sized larvae. The percentage parasitism of eggs and larvae
was not affected by nitrogenous-fertilization. The increase in survival of
medium-sized larvae with nitrogen levels was associated with lower
predator to leaffolder ratios. The strong effect of nitrogenous-fertilization
in the present small-scale experiment was attributed mainly to allowing
the moths an oviposition choice between plots with different application
levels of nitrogen. Therefore it is hypothesized that the effect of
increasing nitrogenous-fertilization level on leaffolder larval densities
will be less pronounced when implemented over a large area.
does not differ from that of the traditional cultivars (Heinrichs et
al., 1985, 1986; Khan and Joshi, 1990). A large number of field
trials, however, have shown that increasing nitrogenous-fertiliza-
tion usually leads to higher leaffolder injury levels (Dale, 1994).
The effects of nitrogenous-fertilization on leaffolder population
dynamics were not determined in these field trials, nor were the
mechanisms underlying the increased injury levels identified.
Laboratory experiments showed that nitrogenous-fertilization
affects several bionomic characteristics of rice leaffolders (table
1). As is usual for herbivores (Mattson, 1980), nitrogen appears
to be a limiting factor for growth, reproduction and survival. The
reported increase in leaffolder injury with nitrogenous-fertilization
level may thus have various causes, but the relative importance
of these factors under field conditions is not yet known.
In insecticide-free fields with current farmer crop manage-
ment practices, rice leaffolder infestations in the Philippines are
generally low and natural control seems to be effective in
keeping the infestation levels below the damage threshold
(Litsinger et al., 1987; Barrion et al., 1991; de Kraker, 1996). To
meet the ever increasing demand for rice, however, the
attainable yields will have to be raised, requiring higher
nitrogenous-fertilizer inputs (Kropff et al., 1994). As this increase
in nitrogen input could stimulate leaffolder population growth or
feeding rates, natural enemies may no longer be able to keep
the pest below damaging levels. This would trigger more
insecticide applications and the natural control of many other
rice pests would then also be at risk (Way and Heong, 1994).
To optimize nitrogenous-fertilization for stable, high yields,
not only agronomic effects, but also the effects of nitrogenous-
fertilization on pest development should be accounted for. In the
present field study, the effect of nitrogenous-fertilization on the
dynamics of rice leaffolders and their natural enemies was
investigated in detail by intensive sampling during one cropping
season. The objective was to identify the major mechanisms
leading to increased leaffolder infestation at high nitrogen levels.
Knowledge of these mechanisms will be helpful to determine
optimal nitrogen application levels in an integrated approach to
crop management.
1. Introduction
Since the mid-1960s rice leaffolders (Cnaphalocrocis med-
inalis (Guenee) and Marasmia spp., Lepidoptera: Pyralidae)
have increased in abundance, and in many Asian countries they
are now considered as important pests (Reissig et al., 1986;
Khan et al., 1988; Dale, 1994). The shift from minor to major
pest status has been attributed to the adoption of new rice
growing practices that accompanied the introduction of high
yielding varieties (Kulshreshtha et al., 1970; Litsinger, 1989).
These practices included increased cropping intensity, irrigation
and a high input of nitrogenous fertilizers and pesticides
(Loevinsohn et al., 1988). In particular the effects of variety
and nitrogenous-fertilizer on rice leaffolder infestation have been
the topic of numerous studies. The adoption of modern varieties
per se does not seem to be the cause of increased leaffolder
abundance, because their level of resistance to rice leaffolder
*To whom correspondence should be addressed at: TPE, PO Box 430, 6700 AK Wageningen, The Netherlands. Fax: +31 317 484892; e-mail:
joop.dekraker@staff.tpe.wau.nl
International Journal of Pest Management
ISSN 0967-0874 print/ISSN 1366-5863 online Ó 2000 Taylor & Francis Ltd
http://www.tandf.co.uk/journals

226
J. de Kraker et al.
2. Materials and methods
three hills per plot. Plant height, number of tillers and leaves per
hill, leaf colour and growth stage were recorded. Total leaf
nitrogen content (%) was determined with the Kjeldahl method,
at three crop growth stages: tillering (33 d.a.t.), panicle formation
(58 d.a.t.), and flowering (86 d.a.t.). At maturity, yield was
measured by harvesting 10m2 per plot. Grain yield was adjusted
to 14% moisture content based on fresh weight.
2.1. Location and lay-out of field experiment
The study was conducted during the wet season in a
farmer’s field in Pila, a municipality at about 20 km distance from
¢
¢
the International Rice Research Institute (13 14 N, 121 15 E),
8
8
Laguna Province, the Philippines. Laguna is a humid tropical
lowland area where rice is grown year-round under irrigated
conditions. The rice leaffolder population is a complex of three
related species: Cnaphalocrocis medinalis, Marasmia patnalis
Bradley, and M. exigua (Butler) (Arida and Shepard, 1986), the
first two species being the most abundant in Laguna (Barrion et
al., 1991; de Kraker, 1996).
2.3. Sampling of the arthropod fauna
The densities of rice leaffolder stages, their natural enemies,
and other arthropods were estimated by a combination of
sampling methods, starting 1 month after transplanting. Rice
leaffolder moths and other mobile arthropods were sampled
weekly with a suction sampler (D-Vac) in combination with a
plastic bucket enclosure, covering four hills. On each sampling
occasion, five D-Vac samples were taken per plot. Relative
density estimates of highly mobile species, such as the larger
hymenopterous parasitoids, were obtained by weekly sweepnet
sampling. Four samples, of five sweeps each, were taken per
plot. All suction and sweepnet samples were taken between
8.00 and 11.00 a.m. The collected arthropods were identified
and classified as rice pests, predators, parasitoids, or `other’.
The `other’ category consisted of Diptera, mainly of families with
aquatic larval stages (e.g. Ceratopogoniidae, Chironomidae,
Tipulidae, Culicidae). Predators and parasitoids of rice leaf-
folders were classified according to Barrion et al. (1991). The
efficiency of sweepnet samples decreased markedly as the crop
grew denser, and therefore sweepnet results were only included
in between-treatment comparisons for the insect taxa which are
less efficiently sampled with D-Vac.
The experiment was laid out in a randomized complete block
design, with three levels of nitrogenous-fertilizer in four replica-
tions. Blocks were located along a slope at increasing distance
to the water inlet from the irrigation canal. The size of the
2
treatment plots was 500 m . Treatment levels of nitrogenous-
fertilization were 0, 75 and 150 kg N haÐ 1, representing low,
standard recommended, and high levels respectively. Nitrogen-
ous-fertilizer was applied as ammonium sulphate in three split-
doses over the season: 50% at 3 days after transplanting
(d.a.t.), and twice 25% at 21 and 35 d.a.t.
ThericevarietyplantedwasIR70,along-durationvariety,which
is susceptible torice leaffolders, but(moderately) resistanttoother
common pests, like plant and leafhoppers and stemborers (IRRI,
´
1990).The fieldwas plantedwith2-week oldseedlings ina 20 20
cm spacing on 31 August 1991. Weeding was done by hand and
pesticides were notapplied. The fieldwas intermittentlyflooded.
2.2. Crop growth and yield
The densities of the immature leaffolder stages were
estimated by random, destructive sampling of rice hills, twice a
week. With a sample size of 15 hills per plot, less than 3% was
removed from the plots by the end of the season. In the
laboratory, the plants were examined for the presence of
leaffolder eggs, larvae and pupae, and leaves with leaffolder
injury. Larvae were classified in five size-classes, approximately
corresponding with the five larval instars. The immature stages
were kept in test tubes or petri-dishes until emergence of adults
or parasitoids, or until premature death. Leaffolders could be
identified to species only after moth emergence, because the
immature stages of the three leaffolder species are very similar
in appearance (Barrion et al., 1991).
Crop growth was assessed by taking hill samples every 2
weeks, starting 1 month after transplanting. Sample size was
Table 1. Effects of nitrogenous fertilization on bionomic parameters of
Ð
rice leaffolders: (+)=significant increase,
(
)=significant decrease,
(0)=no significant effect, (?)=effect unknown
Parameter
C. medinalis M. patnalis
Larval survival
Pupal survival
+
+
(4)
(4)
?
?
Ð
0a
Larval period
Pupal period
0
0
(4)
(4)
(6)
(3)
2.4. Parasitism and survival rates
a
Leaf area consumed per larva
Relative consumption rateb
+
Ð
(5)
(4)
+
(3)
(3)
?
As an indicator of parasitoid impact, a seasonal level of
parasitism was calculated by dividing the number of hosts with
clear symptoms of parasitism by the total number of hosts, after
pooling all samples per plot. Leaffolders that died of unknown
cause during rearing were excluded from the calculation on the
assumption that healthy and parasitized hosts had similar
chances of dying.
a
Pupal weight
Moth longevity
Moth fecundity
+
+
+
(4)
(4)
(4)
+
?
?
Oviposition (choice)
Oviposition (no-choice)
+
+
(1, 6)
(2, 6)
?
?
From the time series of leaffolder population samples,
estimates were made of stage to stage survival rates using
Southwood and Jepson’s `graphical method’ (Southwood,
1978). The densities of the various leaffolder stages were
adjusted according to their sampling efficiency. A previous
experiment showed that relative to large larvae (L4, L5, L6),
References: (1) Fukamachi, 1980; (2) Liang et al., 1984; (3) Arida et al.,
1990; (4) Dan and Chen, 1990; (5) Fabellar and Heong, 1991; (6) de
Kraker, unpublished.
aNitrogen-effect inferred from tested effect of leaf age and position, leaf
nitrogen content was not measured.
bLeaf biomass consumed per larval biomass.

227
Impact of nitrogenous-fertilization on rice leaffolder
sampling eggs was ca 50% efficient, and sampling medium-
sized larvae (L2, L3) ca 60%. Sampling efficiency of the cryptic
and tiny first instar larvae is very low, and therefore this stage
was excluded from the survival analysis. Survival rates were
calculated from egg to larva, egg to medium-sized larva, and
from medium-sized larva to large larva for each plot. Data on
pupal densities were not sufficient to include in the analysis.
The calculated parasitism and survival rates are approx-
imate values, meant for comparison between treatments and
correlation with potential mortality factors. Further details on the
calculation of parasitism and survival rates are given in de
Kraker (1996).
due to large inter-plant variation. Grain yield per hill was highest
in the medium nitrogen (75 kg haÐ 1) treatment.
Nitrogenous-fertilization also had an impact on higher trophic
levels. All four arthropod categoriesÐpests, predators, para-
sitoids, and `others’Ðincreased in abundance with nitrogenous-
fertilization level (table 2). For the parasitoids this effect was
highly significant when sampled with a sweepnet (F2,6 = 13.88,
<
P
0.01), but not with D-Vac sampling. Within the pest category,
the abundance of Homoptera and Heteroptera did not increase
significantly, in contrast to the Lepidoptera (adults) which
increased about six times in average density (table 2). Within
the Lepidoptera, the share of rice leaffolder moths increased
with nitrogenous-fertilization level from 25 to 70%. Other
common moths were green hairy caterpillar Rivula atimeta
(Swinhoe) (Lepidoptera: Noctuidae), and yellow stemborer
Scirpophaga incertulas (Walker) (Lepidoptera: Pyralidae). The
temporal pattern of pest abundance was very similar for the
three treatments. During the first part of the growing season sap-
feeding homopteran pest species (plant- and leafhoppers)
dominated, while after the flowering stage the seed-feeding
hemipteran rice bugs (Leptocorisa spp.) were the most
abundant.
2.5. Statistical analysis
All statistical tests were performed with the GLIM package
(Crawley, 1993). Count data and ratios were log-transformed
prior to analysis. Treatment effects on arthropod abundance,
natural enemy to rice leaffolder ratios, rates of parasitism and
survival ratios were assessed with an F-test in an ANOVA for
completely randomized block designs. The effect of nitrogen
application level and sampling method on rice leaffolder species
composition in the samples was assessed with a G-test of
independence (Poisson errors), with all samples pooled per
treatment level. Simple linear correlation coefficients (r) were
calculated to detect significant associations between rice
leaffolder and natural enemy densities, natural enemy to
leaffolder ratios, rates of parasitism, and survival ratios per plot
(n = 12).
3.2. Population dynamics of rice leaffolders
M. patnalis was the dominant leaffolder species, both for
moths and larvae (table 3). The species composition of the
samples differed per method: in the moth samples (D-Vac,
sweepnet) M. exigua was practically absent, while this species
constituted a considerable proportion of the larval samples.
Nitrogenous-fertilization had no effect on the species composi-
tion of the sampled moths, but did affect the species composi-
tion of the sampled larvae, as the proportion of M. patnalis
larvae increased with nitrogenous-fertilization level. The species
composition of leaffolder larvae and moths differed significantly
per crop growth stage. C. medinalis and M. patnalis were about
equally abundant during the tillering stage, while M. patnalis was
dominant from booting till maturity. M. exigua only made up a
considerable part of the larval population (25%) after flowering.
Densities of leaffolder moths, eggs and larvae increased
strongly with nitrogenous-fertilization level (table 4, figure 1).
The average larval density in the high nitrogen treatment was
3. Results
3.1. Impact of nitrogenous-fertilization on rice crop growth
and arthropod abundance
Nitrogenous-fertilization had a clear impact on rice crop
growth (data not shown). Plants were taller and darker green at
higher fertilization levels. Leaf nitrogen content was also
positively correlated with nitrogenous-fertilization level, although
differences were only significant during the active tillering stage.
The average tiller and panicle number per hill increased with
nitrogenous-fertilization level, but the effect was not significant
Table 2. Effect of nitrogenous fertilization on the abundance of rice arthropod groups (no. per four hills, seasonal average of D-Vac samples). Ratio high/
low is the quotient of abundance at 150 N and 0 N treatment levels
Treatment level (kg N haÐ
)
1
Arthropod group
0
75
150
Ratio high/low
Treatment effecta
F = 5.29
Pests
3.4
2.3
0.5
0.1
3.8
2.1
0.9
0.2
4.7
2.6
1.0
0.6
1.4
1.1
2.0
6.0
*
Homoptera
Heteroptera
Lepidoptera
F = 3.40
F = 2.54
F = 19.36
n.s.
n.s.
**
Predators
Parasitoids
Others
5.0
3.0
6.6
3.9
8.2
4.2
1.6
1.4
1.8
F=26.83
F=2.88
**
n.s.
**
12.0
15.7
21.7
F=43.42
adf=2, 6; n.s.=non-significant; *= P<0.05; **=P<0.01; ***= P<0.001.

228
J. de Kraker et al.
Table 3. Species composition of the rice leaffolder complex, as a percentage of seasonal totals (N), determined with three sampling methods (D-Vac,
sweepnet, and hill samples)
Treatment level (kg N haÐ
)
1
Sampling method
Species
0
75
150
Treatment effecta
D-VAC
(moths)
C. medinalis
M. patnalis
M. exigua
(N)
67
33
0
38
62
0
34
65
1
(6)
(26)
(107)
G = 3.10
n.s.
n.s.
***
Sweepnet
(moths)
C. medinalis
M. patnalis
M. exigua
(N)
30
70
0
46
54
0
40
60
0
(30)
(63)
(184)
G = 2.25
Hill sample
(larvae)
C. medinalis
M. patnalis
M. exigua
(N)
27
44
29
21
57
22
13
76
11
(66)
(180)
(886)
G = 48.05
Effect of sampling methoda
G = 21.69
G = 41.86
G = 115.73
***
***
***
aEffect on species composition: df=4; n.s.=non-significant, P>0.05; ***=P<0.001.
Table 4. Effect of nitrogeneous-fertilization on abundance of rice leaffolder stages and injured leaves (seasonal average of samples). Ratio high/low is
the quotient of abundance at 150 N and 0 N treatment levels
Treatment level (kg N haÐ
)
1
Leaffolder stage (units)
0
75
150
Ratio high/low
Treatment effecta
F = 10.37
Moths
(no. per five sweeps)
0.18
0.03
0.13
0.24
0.01
2.0
0.33
0.11
0.25
0.57
0.02
4.3
0.96
0.46
0.60
1.92
0.06
13.3
5.3
15.3
4.6
8.0
6.0
*
*
Moths
Eggs
Larvae
Pupae
Injured leaves
(no. per four hills)
(no. per hill)
(no. per hill)
(no. per hill)
(no. per hill)
F = 8.88
F = 31.40
F = 11.44
F = 4.56
F = 10.92
**
**
n.s.
**
6.7
adf= 2, 6; n.s.= non-significant, P > 0.05; *= P < 0.05; **= P=<0.01.
eight times the density in the zero nitrogen treatment. The
average number of injured leaves per hill was positively
species. Of all groups of leaffolder natural enemies only the
Coccinellidae and Araneae did not increase significantly with
nitrogenous-fertilization level, neither in the D-Vac nor in the
sweepnet samples. Natural enemies increased less in abun-
dance with nitrogenous-fertilization level than leaffolders. This is
illustrated by the curvilinear relationship between the seasonal
total D-Vac catches per plot of the gryllid and carabid predators
and their leaffolder prey stages, eggs and larvae respectively
(figure 2). As a consequence, the natural enemy to leaffolder
ratios decreased with nitrogenous-fertilization level (table 6).
Differences between treatments in natural enemies to leaffolder
ratio were smallest for the group of major leaffolder parasitoids.
The temporal pattern of predator abundance was similar for
the three treatments: the first half of the growing season spiders
and hemipterans were most abundant, while during the second
half coleopterans and orthopterans dominated. In addition to the
natural enemy to leaffolder abundance ratios, the degree of
overlap in temporal occurrence between these natural enemies
and their leaffolder prey was also calculated (see Van den Berg
and Cock, 1993). Overlap in phenology ranged from 35 to 75%,
and was lowest for the Coccinellidae and Tettigoniidae. These
species were present mainly around or after flowering, when the
<
correlated with larval density (r = 0.99, df = 10, P 0.001), and
increased with nitrogenous-fertilization level. While the percen-
tage of injured leaves did not exceed 10% in the zero and
medium nitrogen treatment, it reached as high as 30 ± 35% in
the high nitrogen treatment during the ripening stage (figure 1).
3.3. Diversity and abundance of leaffolder natural enemies
A total of 33 leaffolder natural enemy taxa were identified
from the arthropod samples: 21 predator and 12 parasitoid taxa.
This seasonal total of taxa was the same for each treatment,
although the number of taxa per sampling date was usually
lower in the zero nitrogen treatment. This is most probably a
result of the lower natural enemy density in this treatment.
The abundance of most natural enemies of rice leaffolder
increased with nitrogenous-fertilization level (table 5). The
increase of the tettigoniid Conocephalus longipennis (de Haan)
(Orthoptera) was not significant in the D-Vac samples, but highly
<
significant in the sweepnet samples (F2,6 = 99.30, P 0.01). A
sweepnet is more suitable to sample this large and fast-moving

229
Impact of nitrogenous-fertilization on rice leaffolder
leaffolder population was declining already. Between the
treatments, the differences in the percentage temporal overlap
were small (5 ± 10%).
nitrogenous-fertilization level (table 7). Both egg and larval
parasitism (%) decreased with crop age, but were independent
of rice leaffolder density. The seasonal percentage larval
parasitism per plot was not correlated with average parasitoid
abundance, nor with the parasitoid to larva ratio.
3.4. Parasitism and survival of leaffolders in relation to
nitrogenous-fertilization level
Survival from egg to medium-sized larva was similar for
all nitrogenous-fertilization levels, but survival from medium-
sized to large larva increased markedly with nitrogenous-
fertilization level (table 7). Survival rates from egg to medium-
sized larvae were larger than 1.0, indicating that the sampling
efficiency of leaffolder eggs was probably lower than
assumed. The survival from egg to medium-sized larva was
not correlated with the seasonal percentage egg parasitism.
Neither was the survival from medium-sized to large larva
correlated with percentage larval parasitism. However, larval
Ten species of hymenopterous parasitoids were reared from
the field-collected rice leaffolder eggs, larvae, and pupae (for
details, see de Kraker, 1996). Eggs were parasitized by
Trichogramma sp. (probably T. japonicum Ashmead), while
the braconids Macrocentrus philippinensis Ashmead and Cardi-
ochiles philippinensis Ashmead were the most common para-
sitoids in the larval samples. Seasonal percentages of
parasitism of leaffolder eggs and larvae were independent of
Figure 1. Mean densities of rice leaffolder moths, eggs, larvae, injured leaves and percentage injured leaves, at three levels of nitrogenous-fertilization: 0, 75 and 150
kg N haÐ 1. Standard errors were ca 20% of sample means.

230
J. de Kraker et al.
Table 5. Effect of nitrogenous-fertilization on abundance of natural enemies of rice leaffolders (no. per four hills, seasonal average of D-Vac samples).
Ratio high/low is the quotient of abundance at 150 N and 0 N treatment levels
Treatment level (kg N haÐ
)
1
Natural enemy taxon
0
75
150
Ratio high/low
Treatment effecta
Predators:
Coleoptera
Coccinellidae
Carabidae
1.81
1.18
0.35
0.28
2.35
1.40
0.49
0.46
2.92
1.36
0.85
0.73
1.6
1.2
2.4
2.6
F = 9.77
*
n.s.
**
F = 2.69
F = 14.55
F = 9.92
Staphylinidae
*
Orthoptera
Gryllidae
Tettigoniidae
0.66
0.49
0.16
1.14
0.89
0.25
1.48
1.02
0.48
2.2
2.1
3.0
F = 13.10
F = 16.28
F = 4.64
**
**
n.s.
Hemiptera
Araneae
1.14
1.17
1.74
1.16
2.35
1.10
2.1
0.9
F = 40.98
F = 0.08
**
n.s.
b
Parasitoids:
Hymenoptera Ð potential
Hymenoptera Ð major
1.48
0.12
2.18
0.24
2.41
0.43
1.6
3.6
F = 6.05
F = 9.69
*
*
adf= 2, 6; n.s.=non-significant, P > 0.05; *=P < 0.05; **= P < 0.01.
bPotential: species recorded as RLF larval parasitoids; major: species accounting for 85% of observed parasitism.
Figure 2. Seasonal total catch of predators (D-Vac samples) versus their rice leaffolder prey stage (hill samples) per treatment plot: Gryllidae vs leaffolder eggs and
Carabidae vs leaffolder larvae. Dashed lines are eye-fitted curves to indicate general trend.
survival rates were negatively correlated with predator to
log(NLL) = log(NE GG) + log(SE GG) + log(SML)
leaffolder immature and parasitoid to larvae ratios (df = 10, r
Ð
Ð
<
<
=
0.82, P 0.01 and r =
0.83, P 0.001, respectively)
To determine which of the three terms alone explained most
of observed variation in abundance of large larvae per plot,
correlation coefficients were calculated between log (NLL) and
each of the terms. Survival from egg to medium-sized larva did
not explain a significant part of the variation (r = 0.14, df = 10,
and positively correlated with average density of eggs and
<
medium-sized larvae (df = 10, r = 0.80, P 0.01 and r =
<
0.77, P 0.01, respectively).
The last larval instars of rice leaffolders are responsible
for more than 90% of the total leaf area consumed during
the larval stage (Heong, 1990), and leaf injury is thus
mainly dependent on the density of these instars. The
abundance of large leaffolder larvae (NLL) depends on egg
recruitment (NE GG), and subsequent survival from eggs to
medium-sized larva (SEGG), and from medium-sized to large
larva (SML). By taking the log-values the equation for NLL
becomes additive:
<
P
0.1). Abundance of large larvae was best correlated with egg
<
recruitment (r = 0.97, df = 10, P 0.001), and, somewhat less,
with survival from medium-sized to large larva (r = 0.92, df = 10,
<
P
0.001). In fact, survival from medium-sized to large larva
cannot be viewed completely separate from egg recruitment, as
this survival rate was positively dependent on egg recruitment.
Thus, egg recruitment is probably the major factor determining
the density of large larvae.

231
Impact of nitrogenous-fertilization on rice leaffolder
Table 6. Effect of nitrogenous-fertilization on the natural enemy to rice leaffolder (RLF) ratio, calculated over the entire season (ratios of average density
per hill, D-Vac and hill samples)
Treatment level (kg N haÐ
)
1
Natural enemy: Leaffolder ratio
0
75
150
Treatment effecta
F = 33.63
F = 30.93
F = 33.93
F = 35.77
F = 5.74
Predatorsb : RLF moths
45.74
2.39
1.64
1.54
0.12
11.11
1.57
1.05
0.97
0.10
2.94
0.67
0.44
0.31
0.06
**
**
**
**
*
Predatorsc : RLF immatures
Predatorsd : RLF immatures
Potential parasitoidse : RLF larvae
Major parasitoidsf : RLF larvae
adf= 2, 6; n.s. = non-significant, P > 0.05; *= P<0.05; **=P < 0.01.
bAraneae, Odonata; cColeoptera, Orthoptera, Hemiptera; dColeoptera, Orthoptera.
f
eHymenoptera recorded as RLF larval parasitoids; Species accounting for 85% of observed parasitism.
Table 7. Effect of nitrogeneous-fertilization on parasitism and stage
survival of leaffolder eggs and larvae, calculated over the entire season
economic thresholds (Bautista et al., 1984; Bandong and
Litsinger, 1988; Smith et al., 1989; Heong, 1993) for rice
leaffolder control were all exceeded in the high nitrogen
treatment, both in terms of percentage injured leaves and larval
densities.
Treatment level (kg N haÐ
)
1
Parameter
0
75
150
Treatment effecta
A number of possible explanations for the increase in rice
leaffolder injury with nitrogenous-fertilization level (see table 1)
can be discarded in the present study. As the number of
injured leaves was linearly correlated with larval density and
the ratio of injured leaves to larvae even tended to decline
with nitrogenous-fertilization level (cf. table 4), the effect on
leaf injury cannot be due to increased larval feeding rates. The
phenology of immature leaffolder stages was similar for all
treatments, indicating that the duration of immature stages was
not markedly affected. Differences in leaf nitrogen content
between the treatments may have led to better larval growth,
heavier pupae, and increased female fecundity. However, this
could only have affected the size of the second generation,
but was even then probably unimportant considering the
mobility of leaffolder moths and the proximity of the treatment
plots. The major effects of nitrogenous-fertilization on rice
leaffolder identified in the present study were increased egg
recruitment (i.e. total number of eggs laid in the crop), and
subsequently higher larval survival rates, both leading to a
strong increase in the abundance of large larvae, the most
injurious stage of rice leaffolder (figure 3).
Egg parasitism (%)
Larval parasitism (%)
16.1
33.7
20.2
31.3
13.1
37.9
F = 0.88
F = 1.16
n.s.
n.s.
EggÐ medium larva
(survival ratio)
MediumÐ large larva
(survival ratio)
1.08
0.23
1.08
0.29
0.97
0.66
F = 0.76
n.s.
**
F = 14.98
adf= 2, 6; n.s.= non-significant, P > 0.05; **= P<0.01.
4. Discussion
4.1. Impact of nitrogenous-fertilization on the rice
ecosystem
The input of additional nitrogen to the irrigated rice
ecosystem led to an increase in biomass at three trophic levels,
suggesting that the system is nitrogen-limited (White, 1978).
Nitrogenous-fertilization increased the production of rice plant
biomass and enhanced leaf nitrogen content, thus forming the
basis for the increase in rice pest herbivore abundance (table 2).
The additional nitrogen supply probably also led to increased
production of algae and other microflora in the floodwater and on
the soil surface (Craswell and Vlek, 1979), supporting higher
populations of Diptera with aquatic larval stages, comprising
most of the `other’ category in table 2 (Roger et al., 1994). In
turn, predators and parasitoids at the third trophic level
responded numerically to the increased abundance of their
herbivore prey.
4.2.1. Effect of nitrogenous-fertilization on rice leaffolder egg
recruitment. The strong positive effect of nitrogenous-fertiliza-
tion on leaffolder egg density (table 4) has been observed
before, both in small and large-scale experiments with C.
medinalis (Fukamachi, 1980; de Kraker, unpublished). Maras-
mia patnalis and M. exigua apparently have a similar oviposition
response, reflected in the increase of their larval densities with
nitrogenous-fertilization level. Among the three species, M.
patnalis probably responded most strongly, as its share in the
larval samples increased from 44 % in the zero nitrogen to 76%
in the high nitrogen level (table 3). Increased egg recruitment is
probably a result of aggregation of ovipositing females in well-
fertilized plots (preference), as well as an increase in the number
of eggs deposited per female. Oviposition experiments with
small plots fertilized with different levels of nitrogen with either a
confined or a free-moving moth population indicated that
4.2. Response of rice leaffolder populations to
nitrogenous-fertilization
Application of 150 kg N haÐ resulted in larval peak
1
densities that were at least three times higher than densities
commonly observed in Laguna Province (cf. de Kraker, 1996),
and about six times higher than the peak density in the plots with
a standard (medium) fertilization level (figure 1). Recommended

232
J. de Kraker et al.
Figure 3. Effects of nitrogenous-fertilization on the density of rice leaffolder (RLF) larvae: RLF moths lay many more eggs in plots receiving a high level of nitrogenous-
fertilizer (a, cf. table 4), resulting in fewer predators and parasitoids per rice leaffolder egg or larvae (b, cf. table 6). The level of egg and larval parasitism is not affected
(c, cf. table 7), but the survival of medium-sized larvae increases with nitrogenous-fertilization level (d, cf. table 7), probably as a result of the lower predator to RLF
ratios (b). More eggs (a) and better larval survival (d) result in a steep increase in larval density with nitrogen application level (e, cf. table 4). Error bars indicate standard
errors of the treatment means.
preference was the major cause of the increase in egg density
from medium to high nitrogen levels (de Kraker, unpublished).
leaf nitrogen content of the present study. A closer look at the
field data also indicates that a direct effect of host plant quality is
unlikely: while leaf nitrogen content tended to be higher in the
lower blocks, larval survival was generally lower. Indirectly,
nitrogenous-fertilization may lead to better nutrition and reduce
the larval development period, thus decreasing the risk of attack
(Price et al., 1980). However, the effect of leaf nitrogen content
on the larval development period of leaffolders is small (Dan and
Chen, 1990; de Kraker, unpublished), and the phenology of
immature leaffolder stages was similar for all treatments.
Another possible indirect effect is a reduced searching efficiency
of leaffolder natural enemies at higher nitrogenous-fertilization
levels, due to the higher crop density and larger leaf area (e.g.
4.2.2. Effect of nitrogenous-fertilization on rice leaffolder larval
survival. Survival rates were also significantly affected by the
level of nitrogenous-fertilization, notably the survival from
medium-sized to large larva (table 7). This effect might be either
direct, by enhancing larval survival through improved host plant
quality, or indirect, through the impact of natural enemies. Dan
and Chen (1990) reported a direct effect of nitrogenous-
fertilization on C. medinalis larval survival in pot experiments,
but they did not specify the magnitude of this effect. Our own
observations suggest that this effect is small within the range in

233
Impact of nitrogenous-fertilization on rice leaffolder
de Kraker, 1996). This might indeed have contributed to the
increased larval survival in the high nitrogen treatment, but does
not explain the large difference with the medium nitrogen
treatment, as differences in crop density and plant height
between these treatments were relatively small.
nitrogen treatment. The high pest infestation levels in the latter
treatment may well be the cause of this discrepancy.
In an integrated crop management approach, optimization of
nitrogenous-fertilization should take these effects on pest
infestation into account, in particular when reliance on chemical
pest control is to be reduced. This does not necessarily imply
that the recommended fertilization levels will be agronomically
sub-optimal. Although higher nitrogenous-fertilization levels
generally cause an increase in rice leaffolder infestation, this
effect may be (partly) avoided by adapting application method
and timing. In particular early application of all fertilizer leads to
high infestation levels (Saroja et al., 1981), but this timing is also
unfavourable from an agronomic viewpoint, as it leads to
inefficient uptake and use of nitrogen for yield formation
(Thiyagarajan et al., 1995).
The increase in survival of medium-sized larvae with
nitrogen level is most likely due to the less-than-proportional
increase in leaffolder natural enemies, reflected in the decrease
in the natural enemy to leaffolder ratios (table 6). Leaffolder egg
density increased more than 4.5 times from the zero nitrogen to
the high nitrogen level, while the density of most natural enemy
groups increased less than three times (tables 4 and 5). The
less-than-proportional numerical response of the leaffolder
natural enemies may be due to their predominantly generalist
nature. Their numerical response is then expected to be based
on overall prey density (table 2: Pests and Others), which
increased less dramatically with nitrogen level than leaffolder
density. The relatively high numerical response of the more
specialized leaffolder enemies, the major larval parasitoids
(tables 5 and 6), confirms this relationship between specializa-
tion and numerical response. A less-than-proportional numerical
response could be compensated by a functional response to
leaffolder density, resulting in similar levels of mortality at high
and low leaffolder densities. Egg and larval parasitoids probably
displayed such a functional response, as percentages of egg
and larval parasitism were independent of leaffolder density and
fertilization level while parasitoid to leaffolder ratios declined
(table 7). In the more generalist predators, such a compensatory
functional response may well have been absent or insufficient,
resulting in the observed increase in leaffolder larval survival.
The question remains why survival from egg to medium-
sized larva was not affected by the changes in predator-prey
ratio, while survival from medium-sized to large larva was. It
could be that predation is not a major factor in survival from egg
to medium-sized larva, unlike in medium-sized to large larval
survival. The effect of abiotic factors, such as heavy rainfall, on
successful settling of young larvae might be a more important,
density-independent factor (de Kraker, unpublished). Another
possible explanation concerns the functional response of the
larval predators. These predators can consume large numbers
of small larvae per day, but only a few medium-sized or large
larvae (Yuen, 1982; Win, 1989). Therefore their functional
response to changes in young larval density may have been
much stronger. In a choice situation, they also might have a
preference for young larvae, resulting in switching to these
stages when total prey abundance is high, as in the high
nitrogen treatment.
4.4. Effect of large-scale nitrogenous-fertilization on rice
leaffolder infestation
The present study and numerous others were all small-
scale, one-season experiments (for
a compilation of 15
published field trials, see de Kraker, 1996). What would the
effect on rice leaffolder infestation be, if the nitrogenous-
fertilization level was raised over a large spatial and temporal
scale? The strong effect of nitrogenous-fertilization in small-
scale experiments appears primarily due to the preference of
ovipositing females for a well-fertilized crop, relative to other rice
crops and perhaps also to surrounding grassy vegetation.
Increasing nitrogenous-fertilization over a large spatial scale
would diminish this form of `associated susceptibility’, and
probably have a far less pronounced effect on leaffolder
infestation levels. The relationship between spatial scale of
enhanced fertilization and egg deposition rate could be
quantified with knowledge of the dispersal range of ovipositing
leaffolder moths (cf. Kareiva, 1982).
The importance of other effects of nitrogenous-fertilization on
rice leaffolder performance (table 1) appeared to be small in the
present one-season study. However, on a larger scale their
combined effect may result in higher intrinsic rates of increase of
rice leaffolders. Leaffolders will then become more abundant
when their mortality factors, such as natural enemies, are not
proportionally and positively density-dependent. An increased
potential for population growth also implies that leaffolder
outbreaks may occur more frequently (McNeill and Southwood,
1978), especially when natural enemies suffer relatively more
from the use of broad-spectrum insecticides or from adverse
weather conditions (e.g. Rajapakse and Kulasekare, 1982; Patel
et al., 1987; Qadeer, 1988). In this way, the widespread
adoption of chemical nitrogenous fertilizers has probably
contributed to the reported increase in leaffolder abundance
and outbreak frequency since the mid-1960s (Khan et al., 1988).
In unsprayed fields, however, current levels of nitrogenous-
fertilization do generally not result in leaffolder population levels
causing economic damage (de Kraker, 1996). Way and Heong
(1994) postulate that even in intensified irrigated rice systems,
natural controls are adequate for most insect pests, if not upset
by insecticide use. The question is whether natural control would
still be sufficient with a further major increase in nitrogenous-
fertilization level. In the present study, the abrupt nitrogen-
induced rise in leaffolder egg recruitment was not compensated
4.3. Implications for integrated crop management
Modern rice varieties are highly responsive to nitrogenous-
fertilization (Yoshida, 1981). Apart from raising the attainable
yield level, increased nitrogen supply can make the crop less
sensitive to pest injury (Peng, 1993). However, high fertilizer
inputs may also lead to increased pest infestation levels, which
reduce the expected gains in rice yield. Several reports
demonstrate this effect (Hu et al., 1986; Saroja et al., 1987;
Inoue and Fukamachi, 1990). In the present study, grain yield
per hill was highest in the medium nitrogen treatment, although
crop biomass and nitrogen content were higher in the high

234
J. de Kraker et al.
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by a response of the natural enemies, as in the case of brown
planthopper (Kenmore, 1991). Natural enemies might respond
better to the more gradual and general increase in leaffolder
density resulting from a large-scale increase in nitrogenous-
fertilization, but ecological theory does not permit a simple
prediction regarding this matter (Crawley, 1992). Interactions
among three trophic levels are highly complex, and can work in
opposite directions (Price et al., 1980).
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5. Concluding remarks
DALE, D., 1994. Insect pests of the rice plantÐtheir biology and ecology. In E.A.
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The present experiment confirms the finding of previous
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a choice situation leaffolder infestations
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growth, development, and reproduction of rice leafroller. Acta Phytophy-
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increase with the level of nitrogenous-fertilization. In our study,
the increase in infestation was primarily a result of higher egg
recruitment, probably due to ovipositional preference. As the
increase in natural enemy abundance was less than the
increase in leaffolder egg and larval density, natural enemy to
leaffolder ratios decreased with nitrogen level, while larval
survival increased. At a single field scale, the effect of relatively
high nitrogen levels on leaffolder infestations may be reduced by
adapting the timing and method of nitrogen application. An
increase in the spatial scale over which high levels of nitrogen
are applied will probably also reduce the leaffolder density
response, which appears mainly based on preference. Both
aspects indicate options to optimize nitrogenous-fertilization in
an integrated approach to crop management, at individual as
well as community levels of decision making.
DE KRAKER, J., 1996. The potential of natural enemies to suppress rice
leaffolder populations, PhD thesis, Wageningen Agricultural University,
The Netherlands.
FABELLAR, L. T. and HEONG, K. L., 1991. Leaf consumption of rice leaffolder
Cnaphalocrocis medinalis larvae on different crop ages and N-levels.
Poster presented at the 22nd Anniversary and Annual Convention of the
PMCP, Manila, May 9 ± 10, 1991.
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moth, Cnaphalocrocis medinalis, Guenee. Proceedings of the Association
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Acknowledgements
Many thanks are due to D. Almario, E. Hernandez, F. de
Leon, and I. Salon for their technical assistance; A.T. Barrion for
taxonomic determinations; and Mrs F. PenÄaranda for allowing
the use of her field. R.J. Zhang and M. Nakai provided valuable
translations of Chinese and Japanese publications respectively.
This research was a collaboration between Wageningen
University and the International Rice Research Institute,
financed by the Netherlands Ministry of International Coopera-
tion. The senior author was supported by the Foundation for
Biological Research of the Netherlands Organization for
Scientific Research (NWO).
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rice leaffolder management in China, Proceedings of the International
Workshop on Economic Threshold Level for Rice Leaffolder in China,
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Institute), pp. 8 ± 11.
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paddy fields and consequent rice yield. Acta Entomologica Sinica, 29,
4955 (in Chinese, English abstract).
INOUE, H. and FUKAMACHI, S., 1990. Infestation and yield losses caused by
Cnaphalocrocis medinalis Guenee under differential fertilization and
control procedure. Proceedings of the Association for Plant Protection,
Kyushu, 36, 103 ± 107 (in Japanese).
IRRI, 1990. Resistance of IR Varieties to Insect Pests (Los BanÄ os, Philippines:
International Rice Research Institute), 1 p.
KAREIVA, P., 1982. Experimental and mathematical analyses of herbivore
movement: quantifying the influence of plant spacing and quality on
foraging discrimination. Ecological Monographs, 52, 261 ± 282.
KENMORE, P. E., 1991. How Rice Farmers Clean Up the Environment,
Conserve Biodiversity, Raise More Food, Make Higher Profits. Indonesia’s
IPMÐa Model for Asia (Manila, The Philippines: FAO Rice IPC
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