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Repellency of volatile organic chemicals of kakawate, Gliricidia sepium (Jacq)

Walp., to Rice Green Leaf Hopper, Nephottetix virescens (Distant) (Hemiptera:
Cicadellidae)

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PHILIPP AGRIC SCIENTIST ISSN 0031-7454
Vol. 97 No. 2, 000–000
June 2014

Repellency of Volatile Organic Chemicals of Kakawate, Gliricidia

sepium (Jacq.) Walp., to Rice Green Leafhopper, Nephotettix virescens
(Distant) (Hemiptera: Cicadellidae)
Susan May F. Calumpang*, Marcela M. Navasero, Gideon Aries S. Burgonio and Mario V.
Navasero
National Crop Protection Center- Crop Protection Cluster, College of Agriculture, University of the Philippines Los
Baños, College, Laguna, 4031, Philippines
*
Author for correspondence; email: [email protected]; Tel.: +6349 536 2409

The behavioral and olfactory responses of male and female rice green leafhopper (GLH), Nephotettix
virescens (Distant), an important vector of tungro, was studied to elucidate the mechanism for reduced
green leafhopper populations in rice with kakawate (Gliricidia sepium (Jacq.) Walp.) trees growing near
rice fields as observed by farmers. The methods include leaf disc assay to determine possible effect of
organic chemical volatiles and the Y-tube olfactometric bioassays to be able to pinpoint the specific
organic component(s) among the extracted headspace volatiles responsible for the repellent property
of kakawate.
Our results demonstrated that only females of GLH were apparently repelled by the odors released
from the leaf discs of kakawate. ß-Farnesene and trans-2-hexenol repelled GLH in Y-tube olfactometric
bioassays and strongly suggest that repellency is a mechanism for reduced GLH populations in the rice
field. Kakawate planted along rice fields can be promoted for insect pest management in rice
production to promote sustainability and reduce dependence on synthetic insecticides. It can be a
useful pest management strategy in organic and low-input rice production.

Key Words: Gliricidia sepium, leaf disc, Nephotettix virescens, organic agriculture, Petri plate bioassay, rice green
leafhopper, volatile organic chemicals, visual cue, Y-tube olfactometer

INTRODUCTION insect chemical ecology is generally essential.

Semiochemicals, when employed alone, often give
Farmers have used non-host chemicals for insect pest ineffective or insufficient robust pest control. Use of
management in crops by experimentation and semiochemicals should therefore be combined with
observation. Non-host plant volatiles interfere with other approaches in integrated management strategies.
orientation to the host plant and affect the olfactory, The main components of such strategies are pest
feeding and oviposition behavior of major insect pests monitoring, to allow accurate timing of pesticide
and various natural enemies (Brevault and Quilici treatments; combined use of semiochemicals, host
2010; Bruce et al 2005; Finch and Collier 2000; plant resistance and trap crops, to manipulate insect
Forbes and Feder 2006; Koschier et al 2000; van Tol behavior; and selective insecticides or biological
and Visser 2002). The evaluation of the potential of control agents, to reduce pest populations (Pickett et
biologically active plant volatiles may therefore al. 1997).
provide a new approach to the development of Repellents emitted by plants in the ecosystem can
integrated pest management strategies (Koschier et al. be utilized to reduce insect pest populations. Planting
2002). hedgerow species, reported to have a repellent
The study of chemical ecology, particularly chemistry, adjacent to host species may interfere with
involving pheromones and other semiochemicals olfactory cues used by insect pests (Altieri et al. 1977).
(repellents, attractants, stimulants and deterrents) that This approach will reduce the use of insecticides as it
influence insect behavior, promises methods of pest will explain the mechanism for insect population
control as alternatives to the exclusive use of broad- reduction, thereby strengthening farmer extension
spectrum toxicants. However, if the potential of activities, and at best, provide additional farmer
semiochemicals in crop protection is to be realized, a options for organic agriculture. A deeper
greater understanding of insect-plant interactions and understanding of the chemically-mediated behavior of
insects would lead to the development of an integrated
The Philippine Agricultural Scientist Vol. 97 No. 2 (June 2014) 21
Repellency of Volatile Organic Chemicals of Kakawate Susan May F. Calumpang et al.

pest management (IPM) component in crop used in many tropical and sub-tropical countries as a
production. For example, Filipino farmers in Infanta, live fence. That is, it is planted along the sides of
Quezon use the stalks of tagbak [Alpinia elegans (C. fields, and the trunks are used as fence posts. During
Presl.) K. Schum] staked into the rice paddies to the dry season, when much of the forage is gone, the
control rice insect pests. tree limbs are cut and the foliage is offered to
The green leafhopper (GLH), Nephotettix livestock. In sub-Saharan Africa, kakawate is
virescens (Distant), is an important vector of tungro, a intercropped with maize (Makumba et al. 2006).
major disease of rice. Olfactometric bioassays Kakawate is reported to have insecticidal properties
demonstrated the repellency of certain organic volatile (Grainge and Ahmed 1988; Méndez-Bautista et al.
chemicals emitted by tagbak against GLH; these are: α 1993; Montes-Molina et al. 2008). In particular, it is
-pinene, α-terpinene, linalool, β-pinene, cymene, reportedly used as a mosquito repellent (Nazli et al.
camphene, 1,8 cineole and citronellol (Calumpang et 2008) and also has antifungal and antimicrobial
al. 2013). This indigenous pest management practice is properties (Rahalison et al. 1993). A new isoflavan,
based on chemical ecology principles and can be used 7,4'-dihydroxy-3'-methoxyisoflavan, has been isolated
in organic and low-input rice production. Another from the insecticidally active extract of the heartwood
farmer observation involved the lower incidence of of G. sepium (Herath et al. 1998).
corn borer infestation in corn fields with Ipomoea The essential oil of G. sepium leaves reportedly
triloba, a weed closely associated with corn. The contains the following major organic chemicals:
chemical basis for this phenomenon was due to the propylene glycol, coumarin, [Z]-3-hexenol, ß-
presence of a repellent compound in headspace farnesene, (E)-2-hexenol, thymol, benzyl alcohol,
emissions when corn was entwined by the weed caryophyllene and α-farnesene while the minor
(Calumpang et al. 2000). components include 2-pentene-1-ol, isovanillin,
Other volatile organic chemicals, e.g., toluene and isobutyl alsohol, phenylethyl alcohol, phenol and
ethylbenzene, which are present in the leaf of olive crotonic aldehyde at levels less than 1% (Jose and
and in half-ripe olive proved attractive, while (E)-2- Reddy 2010; Kaniampady et al. 2007).
hexenal emitted by crushed olives was found to be In the Philippines, kakawate is usually found along
very repellent to the olive fruit fly, Dacus oleae rice paddies and some farmers believe that it can
Gmelin. (E)-2-hexenal and hexanal displayed an reduce rice insect pests in their fields. Live kakawate
oviposition deterrent effect as well (Scarpati et al. as posts of trellises are also used in tomato in Laguna
1993). Alpha-pinene, limonene, citronellol, citronellal, and in string bean production in Batangas (Fig. 1),
camphor and thymol have been shown to possess high where farmers claim they encountered fewer pest
repellent activity and have the potential to provide problems. These farmer observations have not been
efficient and safer repellents for humans and the validated to elucidate the working mechanism in the
environment (Nerio et al. 2010). Alpha-terpineol, field.
nerolidol, δ-cadinene, β-eudesmol, terpinolene and In the current study, we examined the influence of
cedrol showed high repellent activity against kakawate leaf discs on the host-finding behavior of
Cryptomeria bark borer (Yatagai et al. 2002). GLH in Petri plate bioassays. Furthermore, we
Benzaldehyde (iso-vanillin), phenyl acetaldehyde determined the olfactory response of GLH to each of
and 2-phenylethanol have been detected in floral the volatile chemical components of kakawate.
fragrance constituents in cruciferous flowers (Tollsten
and Bergstrom 1988; Evans and Allen-Williams 1992;
Nielsen et al. 1995). Authentic 2- MATERIALS AND METHODS
phenylethanol elicited electroantennograms, single cell
responses and sexual excitation in the male cabbage Plants and Insects
looper moth, Trichoplusia ni (Hubner) (Jacobson et al. Initial stock of GLH was obtained from the Field
1976). It is also an anti-aggregation pheromone for the Crops Laboratory, Crop Protection Cluster, of the
mountain pine beetle, Dendroctonus ponderosae University of the Philippines Los Baños, College,
Hopkins (Borden et al. 2004). It has also exerted Laguna. The stock was used in the laboratory in the
pronounced repellent effect against ticks and yellow bioassay of volatile organic chemicals (VOCs) of
fever mosquitoes (Tunόn et al. 2006). kakawate. GLH adults were reared on TN1 rice
Kakawate, Gliricidia sepium (Jacq.) Walp., is a seedlings, planted in size-4 clay pots in the laboratory
leguminous tree and belongs to the family Fabaceae. (oviposition phase) and reared in cages in the
Gliricidia, which originated in Central America, is greenhouse until adulthood prior to testing.

22 The Philippine Agricultural Scientist Vol. 97 No. 2 (June 2014)

Repellency of Volatile Organic Chemicals of Kakawate Susan May F. Calumpang et al.

done by arranging the Petri plates equidistantly on a

black plastic under dim light to avoid distraction of the
GLH by light and to enable data gathering.
To start the bioassay, GLH were released
individually at the side of the Petri plate and the times
when they alighted on the leaf discs were recorded, as
well as the length of stay or duration, and frequency of
alighting. Observations were recorded using a
stopwatch. Unresponsive males and females of the 30
replications performed within the 3-h observation
period were also recorded but not included in the
statistical analysis.

Fig. 1. Live kakawate (Gliricidia sepium (Jacq.) Walp.)

Y-tube Olfactometer Bioassays
posts used as trellis in tomato production in The responses of female GLH to essential oils found
Majayjay, Laguna (Photo courtesy of Rodel H. in kakawate were assayed in a Y-tube olfactometer
Maghirang, Institute of Plant Breeding, Crop enclosed in a black cage (60 cm x 60 cm x 60 cm)
Science Cluster, University of the Philippines (Fig. 2). The Y-tube olfactometer and the black cage
Los Baños). were modified from the ones used with Cicadulina
storeyi (Oluwafemi et al. 2011). Each arm of the
Petri Plate Bioassays olfactometer was connected to a glass odor chamber
Starved adults were tested separately by sex; 3- to 7-d- by a ground glass joint. A mini-vacuum pump (Sibata
old unmated adult females and males were starved for MP-2N, Japan) was fixed at the stem of the Y-tube,
1–3 h prior to the experiment. One adult was used per pulling air from the opposite ends. Air was filtered by
replicate with 30 replicates per treatment. The adults activated charcoal inside a glass tube attached to each
were used only once. The bioassay was conducted in odor chamber. The olfactometer was placed on the
an air-conditioned room at 27–28 °C. surface of the black cage where green light (5 watts,
The three different treatment set-ups used: 1) two filtered with plain white paper) was positioned 15 cm
strips of 2.5-cm leaf strip of TN1 (T-1), 2) one-leaf above the Y-tube junction. The essential oil
disc of 2.5-cm diameter of kakawate (T-2), and 3) two components of kakawate that were tested included:
strips of rice leaves placed on top of a 2.5-cm leaf disc trans 2-hexenol, β-farnesene, thymol, 2-penten-1-ol, β-
of kakawate (T-3) to test repellency of kakawate caryophyllene, propylene glycol, phenol, benzyl
volatiles to GLH when exposed to these substrates. alcohol and trans 3-hexenol. These are VOCS which
Treatments 1 and 2 were used for the no-choice tests could influence insect host-finding behavior. These
and treatment 3, for the two-choice tests. were dissolved in hexanes (AR, JT Baker) to obtain a
TN1 leaves were obtained from 35- to 45-d-old solution of about 60 μg mL-1 and 0.5 mL was used in
potted plants in the screenhouse. Kakawate leaves the assay. Hexanes (0.5 mL) were used as control.
were detached from kakawate plants that were Treatments and control were applied on filter paper
carefully chosen from a crop stand at the National discs (Whatman # 3, 2.5 cm diameter) using a pipette.
Crop Protection Center, College of Agriculture, Treated filter paper disc was inserted at the distal end
University of the Philippines Los Baños. of one odor chamber and the control filter paper disc
Fresh Petri dishes were prepared by lining the was placed at the other end. All filter paper discs were
bottom with 9-cm diameter filter paper (Whatman #3) used only once.
which was wetted with 2 mL of distilled water. Two Virgin females starved for 1–3 h were used in the
strips of rice leaf were placed across each other upside experiment. Every treatment was replicated 30 times
down at the middle of the filter paper. Thirty plates with one individual per replicate. For each replicate, a
were prepared in this manner. Another 30 plates were single GLH was carefully laid inside the stem end of
prepared in the same manner, but this time, leaf discs the Y-tube. GLH was used only once and discarded.
of kakawate were used, placed upside down at the Within 10 min, the first choice of GLH between the
middle of the dish. Also, 30 plates were similarly two arms of the Y-tube olfactometer was noted and
prepared and leaf discs of kakawate were placed in the considered repelled if it entered the control arm. One
middle of the plate before placing two strips of rice fresh set of olfactometer was used in each replicate.
leaf side by side on top of the disc. Evaluations were The set-up was washed with mild detergent, rinsed

The Philippine Agricultural Scientist Vol. 97 No. 2 (June 2014) 23

Repellency of Volatile Organic Chemicals of Kakawate Susan May F. Calumpang et al.

140

Length of stay (min)

p = 0.0161 Male p = 0.8699
120
100
80
60
40
20
0
Rice Kakawate Rice Kakawate

No choice 2-choice
140 F e m a le

Length of stay (min)

p = 0.0074 p = 0.9163
120
100
80
60
40
20
Fig. 2. Y-tube olfactometer set-up for rice green leaf-
0
hopper, Nephotettix virescens (Distant).
Rice Kakawate Rice Kakawate
twice with technical acetone and allowed to air-dry. No choice 2-choice
All assays were performed in an air-conditioned Fig. 3. Length of stay (min) of green leafhopper (GLH,
laboratory with an ambient temperature of 25 ± 1 °C Nephotettix virescens) on rice (Oryza sativa)
from April 18, 2013 to July 2013. Percent repellence leaf strips and kakawate (Gliricidia sepium) leaf
was determined based on the number of individuals dics in no-choice tests and 2-choice tests in a
responding negatively, divided by the total number of Petri dish arena. Values are means ± SE (n =
30); t-test; p-value <0.05 was considered
individuals tested and multiplied by 100. significant.

Statistical Analysis kakawate, which strongly suggests that only the

The data obtained in the Petri plate and Y-tube female GLH was repelled by the volatiles released by
bioassays were analyzed statistically and significant kakawate.
differences of means were determined using the The reduced number of GLH in fields with
Independent Sample T-test (SAS 2001). kakawate was possibly due to less females ovipositing.
Time lapse before first alighting. The time lapsed
for alighting for the first time by both the male and
RESULTS AND DISCUSSION female GLH (Fig. 4) on either kakawate leaf disc or
rice leaf-strips (no-choice) showed no statistical
Comparative Response of Male and Female GLH difference. However, male GLH took a much shorter
to Volatiles from Kakawate Leaf Discs and Rice time to alight on rice than on kakawate in choice test.
Leaf-Strips The male GLH was not repelled by kakawate, which is
Length of stay. In terms of the response of male and consistent with the length of stay shown in Fig. 3. In
female GLH to volatiles from kakawate leaf discs and contrast, it took a longer time for the female GLH to
rice leaf-strips, the male GLH spent shorter time on alight on either rice or kakawate when given the
kakawate leaf discs than on rice leaf-strips in the no- choice, an increase from 20 min to 40 min, suggesting
choice tests or when kakawate leaf discs and rice leaf- that the female GLH was repelled by the VOCs
strips were offered separately (Fig. 3). However, when emitted by kakawate.
kakawate and rice was offered simultaneously, male Frequency of alighting. In terms of frequency of
GLH did not discriminate between the two plants and alighting in no-choice tests with leaf discs of kakawate
length of stay on both plants was as long as when it and rice leaf-strips, the male GLH showed no
was on rice alone. Hence, the male attraction to rice as significant difference in response (Fig. 5) but response
its host was not affected in the presence of kakawate. was highly significant in the two-choice tests.
Female GLH showed similar response with male Although the frequency of male alighting on kakawate
GLH (Fig. 3) but its length of stay was apparently was higher, the duration of its stay was shorter than on
much shorter on both rice and kakawate when offered rice (Fig. 3) where mean duration of all its alightings
simultaneously. Female GLH appeared to be distracted was not significantly different. In contrast to the
in finding or going to its host in the presence of behavior of male GLH, the female GLH made

24 The Philippine Agricultural Scientist Vol. 97 No. 2 (June 2014)

Repellency of Volatile Organic Chemicals of Kakawate Susan May F. Calumpang et al.

with 60% to 67% repellency (Fig. 7 and 8). Benzyl

alcohol and trans 3-hexenol did not exert any
repellency against GLH.
The repellency demonstrated in the Y-tube
bioassays further support the behavioral changes
observed in the Petri dish assays. VOCs emitted by
kakawate repelled the GLH from rice plants.
Some of the tested VOCs are biologically active
and some possess repellency effects on other insects.
(E)-β-Farnesene is a sesquiterpene semiochemical that
is used extensively by both plants and insects for
communication (Bernasconi et al. 1998). Volatiles of
green ash, Fraxinus pennsylvanica, proved to be
significantly repellent to gypsy moth larvae due to the
combined repellencies of farnesene, linalool and
methyl salicylate (Markovic et al. 1996). The major
components of the essential oil of Chrysanthemum
cinerariaefolium include trans-β-farnesene, β-
Fig. 4. Mean (± SE) time lapse (min) for first alighting
of male (left) and female (right) GLH, cubebene and δ-nerolidol (at 41.36%, 17.27% and
Nephotettix virescens, on rice and kakawate in 14.23%, respectively). Likewise, trans-β-farnesene
no-choice tests and 2-choice tests using also repelled the grain aphid, Sitobion avenae F.
kakawate (Gliricidia sepium) leaf discs and rice (Bruce et al. 2005) while β-caryophyllene, as well as
leaf strips in a Petri plate arena (t-test; p-value (−)-sabinene, β-pinene, limonene, α-pinene and
<0.05 was considered significant). bergamotene, significantly reduced probing activity of
Aedes aegypti (L.) (Jaenson et al. 2006).
significantly more alightings on kakawate in the no-
choice tests but not in the two-choice tests. Relating
this observation with mean length of stay in the no- CONCLUSION
choice test (as shown in Fig. 3), female GLH stayed
much longer in rice than in kakawate. The results The behavioral responses to the leaf discs and the
suggest that frequency of alighting is not a good repellent reaction of N. virescens to volatiles of G.
measure or indicator of repellency under this sepium provide evidence for an interaction between
experimental set-up. visual and olfactory stimuli during host-finding/
In addition, some GLH adults did not respond or selection for this species of leafhopper. VOCs from
remained immobile in the bioassays. The percentage kakawate repelled GLH, thus reducing the possibility
of unresponsive males increased from 10% to 40% on of mating and oviposition of GLH in the field. The use
rice alone and on rice + kakawate (Fig. 6). This result of kakawate for insect pest management in rice
is consistent with the decreased alighting activity production can be promoted to reduce dependence on
when kakawate is presented together with rice. On the synthetic insecticides. It can also be a useful pest
other hand, the number of unresponsive females was management strategy in organic rice production.
only 20% and 27%, whether in rice alone or in rice +
kakawate, respectively. These results indicate the
presence of kakawate VOCs acting as arrestant(s) for ACKNOWLEDGMENT
male GLH, thus inhibiting a greater proportion of
males from alighting on either rice or kakawate, and The authors acknowledge the financial support of the
contributing to less opportunity for GLH mating in the National Research Council of the Philippines (NRCP),
field. Department of Science and Technology (DOST),
Philippines for this research.
Y-tube Olfactometer Bioassay
GLH showed 70% to 73% repellency for volatile
organic compounds: trans 2-hexenol (a fatty acid
derivative), β-farnesene, followed by thymol, 2-penten
-1-ol, β-caryophyllene, propylene glycol and phenol,

The Philippine Agricultural Scientist Vol. 97 No. 2 (June 2014) 25

Repellency of Volatile Organic Chemicals of Kakawate Susan May F. Calumpang et al.

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