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Journal of Chemical Ecology, Vol. 31, No.

9, September 2005 ( #2005)


DOI: 10.1007/s10886-005-6085-4

VOLATILE ALLELOCHEMICALS IN THE Ageratum


conyzoides INTERCROPPED CITRUS ORCHARD
AND THEIR EFFECTS ON MITES Amblyseius
newsami AND Panonychus citri

CHUIHUA KONG,1,2,3,* FEI HU,2 XIAOHUA XU,3 MAOXIN ZHANG,2


and WENJU LIANG1
1
Institute of Applied Ecology, Chinese Academy of Sciences, Shenyang 110016, China
2
Institute of Tropical and Subtropical Ecology, South China Agricultural University,
Guangzhou 510642, China
3
State Key Laboratory of Elemento-Organic Chemistry, Nankai University,
Tianjin 300071, China

(Received June 2, 2004; revised November 1, 2004; accepted May 14, 2005)

AbstractAgeratum conyzoides L. weed often invades cultivated fields and


reduces crop productivity in Southeast Asia and South China. However,
intercropping this weed in citrus orchards may increase the population of
predatory mite Amblyseius newsami, an effective natural enemy of citrus red
mite Panonychus citri, and keep the population of P. citri at low and non-
injurious levels. This study showed that A. conyzoides produced and released
volatile allelochemicals into the air in the intercropped citrus orchard, and
these volatiles influenced the olfactory responses of A. newsami and P. citri. At
test temperature (25-C), A. conyzoides fresh leaves, its essential oil, and major
constituents, demethoxy-ageratochromene, b-caryophyllene, a-bisabolene,
and E-b-farnesene, attracted A. newsami and slightly repelled P. citri. Field
experiments demonstrated that spraying A. conyzoides essential oil emulsion
in an A. conyzoides nonintercropped citrus orchard increased the population
density of A. newsami from below 0.1 to over 0.3 individuals per leaf,
reaching the same level as in an A. conyzoides intercropped citrus orchard.
However, this effect could not be maintained beyond 48 hr because of the
volatility of the essential oil. In contrast, in the A. conyzoides intercropped
citrus orchard, A. conyzoides plants continuously produced and released
volatile allelochemicals and maintained the A. newsami population for a
long time. The results suggest that intercropping of A. conyzoides not only
made the citrus orchard ecosystem more favorable for the predatory mite

* To whom correspondence should be addressed. E-mail: kongch@mail.edu.cn

2193
0098-0331/05/0900-2193/0 # 2005 Springer Science + Business Media, Inc.
2194 KONG ET AL.

A. newsami, but also that the volatile allelochemicals released from


A. conyzoides regulated the population of A. newsami and P. citri.

Key WordsVAgeratum conyzoides L., volatile allelochemical, citrus orchard,


intercropping, predatory mite Amblyseius newsami, citrus red mite, olfactory
response.

INTRODUCTION

The Compositae weed Ageratum conyzoides L. originated from Central


America and is now widely spread in Southeast Asia and South China. It in-
vades cultivated fields and reduces crop productivity in tropical and subtropical
agroecosystems (Roder et al., 1997; Singh et al., 2003). However, when grown
in citrus orchards, it effectively suppresses the growth of other weeds and
spore germination of several fungal pathogens through release of allelo-
chemicals into the soil (Kong et al., 2004c). Additionally, intercropping
A. conyzoides with citrus makes the orchards more favorable for predatory
mites (Amblyseius spp.), which effectively control the major arthropod pest
citrus red mite (Panonychus citri McG) in citrus orchards in South China (Tao
and Luo, 1992). Therefore, A. conyzoides has been advocated for intercrop-
ping in citrus orchards and is utilized on more than 150,000 ha of citrus
orchards in South China (Liang and Huang, 1994). The natural biochemical
interactions between A. conyzoides and other organisms in the intercropped
citrus orchard remain obscure.
A. conyzoides produces and releases volatile allelochemicals into the
environment at various growth stages (Kong et al., 1999, 2002, 2004a,b). The
concentration of volatiles in A. conyzoides intercropped citrus orchards is so
high that an unpleasant odor can be detected. Studies have shown that volatile
allelochemicals released by many plant species play an important role in tri-
trophic systems that include the host plant, herbivore, and parasitoid or predator
(Dicke et al., 1990; Bruin et al., 1992; Dicke, 1999; Sabelis et al., 1999;
Agrawal, 2000; Bruin and Sabelis, 2001; Kessler and Baldwin, 2001). It is
possible that volatiles released by A. conyzoides may affect the behavior and
population of mites in intercropped citrus orchards. Accordingly, our objectives
in this study were to determine and identify the volatile allelochemicals in the
A. conyzoides intercropped citrus orchard and to evaluate their effects on the
predatory mite (Amblyseius newsami Evans) and the citrus red mite (P. citri).

METHODS AND MATERIALS

Sampling Citrus Orchards. Two orchards planted with Citrus sinensis (L.)
Osb. (plants, 2.5  4 m) in Guangzhou Suburb, China (23-06 0 N, 113-18 0 E),
VOLATILE ALLELOCHEMICALS IN THE Ageratum conyzoides 2195

were selected. One orchard had been intercropped with A. conyzoides since
2001. The A. conyzoides plants grew luxuriantly and covered the orchard floor
that was free from other weeds. Another citrus orchard without A. conyzoides
served as the control. The major weeds in this orchard were Bidens pilosa,
Digitaria sanguinalis, and Cyperus difformis. If any A. conyzoides appeared in
the control site, they were hand-weeded since October 2002. The experimental
orchards were in a subtropical climate zone, with a mean annual temperature of
21.8-C and a mean annual rainfall of 1682 mm. There were no significant
differences in pH, organic matter content, and fertility status between the
intercropped and control site soils (pH 5.6; organic matter 19.7 g kgj1; total
N 0.97 g kgj1; available N 40.8 mg kgj1; total P 0.48 g kgj1; available P 13.8
mg kgj1; total K 102.9 g kgj1; available K 98.7 mg kgj1).
Population Densities of Mites. A. newsami and P. citri were used because
A. newsami is the most common Amblyseius spp. predatory mite and P. citri is a
major citrus arthropod pest in citrus orchards in South China. Fifteen citrus
plants, whose canopies did not touch each other, were randomly selected from
two orchards, respectively. For the population census, 50 representative spatial
leaves of each citrus plant were selected, and adult mites were counted twice a
day (10: 00 a.m. and 4:00 p.m.) for three consecutive days (Tao and Luo, 1992).
Data were subjected to ANOVA with Duncans multiple range test. The mean
number of individual mites (A. newsami or P. citri) per leaf indicated their
population densities in the orchards.
Effect of the essential oil on the mites was studied in a nonintercropped
citrus orchard (i.e., control without A. conyzoides). Twenty-seven citrus plants
(3  9), whose tree canopies were separated from one another by at least 15 m,
were randomly selected. Then, a 5% essential oil emulsion (10 kg) of
A. conyzoides was sprayed on 18 citrus plants (2  9). Ten kg water served
as a control (1  9 citrus plants). After 24 and 48 hr, the population densities
(mean individuals per leaf ) of adult mite A. newsami and P. citri on each of 50
representative spatial leaves of each plant were counted as described above.
Experiments were carried out in June 2003, when A. conyzoides was at its
peak flowering stage, and mites A. newsami and P. citri were active and
abundant. Sampling dates were cloudy with a 27 T 5-C air temperature and 70 T
10% relative humidity. Pesticides have never been applied in either citrus
orchard since October 2002.
Collection and Analysis of Volatiles. Collection and analysis of volatiles in
the orchards was as follows (Kong et al., 2004a). Nine sampling locations were
randomly selected from both citrus orchards. Air samples 1 m above the ground
at 2  9 locations each were collected by Timing Minipump air samplers with a
flow meter TMP-1500 (China Electrical Instruments Co.) and pumped through
the sampling tubes (Tekmar Co., USA) packed with Tenax and Carbonsieve at a
flow rate of 0.5 l/min for 30 min. The volatile chemicals in air samplers were
2196 KONG ET AL.

adsorbed onto the solid adsorbents, and sampling tubes were installed into a
Tekmar 6032 Aero-trap Autosampler for thermal desorbing. The tubes were
rapidly heated to 225-C, and their volatiles were desorbed and carried by
helium to a Tekmar 3000 Purge & Trap Concentrator where they were trapped
again. The concentrator was heated at a rate of more than 400-C/min, and the
trapped volatiles were transported to a Hewlett-Packard P 5972 GC/MSD with
an HP-5 bonded stage fused-silica capillary column (30 m  2.5 mm) for
analysis. The initial oven temperature (70-C) was maintained for 2 min and then
increased to 180-C at a rate of 10-C/min. The column was maintained at 180-C
for 5 min, and then the oven temperature was raised to 250-C at 15-C/min.
Mass spectra were repetitively scanned from 35 to 450 amu every 2 sec.
Ionization was selected in the electron impact mode (EI) at 70 eV. The chemical
constituents were identified by peak matching against standards in the NIST 95
Computer Library or by spectral similarity to an authentic reference compound
(Aldrich Chemical Co.). The relative amounts of the chemical constituents were
calculated by integrating all peaks with an area greater than 0.1%.
Collection and analysis of volatiles from fresh leaves and the essential oil
of A. conyzoides were performed using the technique of multiple headspace
solid-phase microextraction (Augusto et al., 2003; Ezquerro et al., 2003). GC/
MSD and manipulation was the same as described above.
The essential oil was obtained by placing fresh leaves of A. conyzoides into
a desiccator with a liquid nitrogen cold trap and pumped into a vacuum (Kong
et al., 2002). It was then subjected to silica gel column chromatography with n-
hexane/ether (9:1 and then 4:6; v/v) mixture. It produced five major
components, ageratochromene, demethoxy-ageratochromene, b-caryophyllene,
E-b-farnesene, and a-bisabolene.
Olfactory Responses of Mites to Volatiles. Adult mites of both A. newsami
and P. citri were collected from citrus orchards and reared in a petri dish (9-cm
diam.; 1.8-cm depth) at 25-C and 50% relative humidity. The dish was placed in
a transparent container over a pad of black colored velvet and a sponge (8-cm
diam.; 1 cm thick). Because the mites are translucent, the black background
enhanced visual detection. The sponge was allowed to imbibe and maintain
water by partially adding water daily.
The olfactory response of the mites to volatiles was studied with a slightly
altered airflow four-armed olfactometer designed by Pettersson (1970). The size
of the exposure chamber was halved (ray of crescents: 67.5 mm, inner height: 5
mm, inner diameter of stainless tubes: 3 mm). A flow rate of 300 ml/min
through each arm was maintained to create odor fields with sharp boundaries.
The exposure chamber and TV monitor screen (21 00 ) were interfaced with a
multifunctional MC-1 camera (China Optical Co.) with the following features:
sensitive element, 1/3 00 , 500(H)  582(V) lines; resolution, 420 lines; optical
attachment, eyepiece adapter (39-mm diam for stereomicroscope and 23.3-mm
VOLATILE ALLELOCHEMICALS IN THE Ageratum conyzoides 2197

diam for the biological microscope); minimum illumination, 3 lx; shutter, 1/


50Y1/1000 sec autocontrol; objective, F = 8 mm, focus from 10 mm to infinity.
A vacuum pump/compressor was connected to a hole in the center of the floor of
the exposure chamber by silicone rubber tubing and was used to suck air through
the arms of the device into the exposure chamber. Test mites were introduced
into the exposure chamber through this hole with the extractor tube removed.
Activated charcoal enclosed in dry cotton wool at each flow meter purified
incoming air.
Trials were conducted in accordance with the protocols suggested by Vet et al.
(1983). Each arm of the exposure chamber was connected to a set of three 50-ml
glass vials. The vial closest to the chamber served as the trap to catch mites, the
second one provided an odor source, and the outside vial contained distilled
water over which the incoming air was passed to create uniform humidity. The
odor source, A. conyzoides fresh leaves (500 mg), the essential oil (100 mg), or
five components (100 mg) were each placed in the odor vial. An olfactometer
with a single arm of humidified air served as control. With proper air pressure,
four air streams of 300 ml/min were introduced into the central region through
the flow meters into each of the different arms of the olfactometer. Fifty adult
mites were individually introduced into the chamber, and they could make two
choices. The first choice was made when a mite reached the arbitrary transverse
diagonal of one of the odor compartments. Before the first choice was made,
each mite was given 2 min in the exposure chamber, at the end of which it was
regarded as unmotivated and not recorded. The remaining 8 min was allocated
for the second choice that was recorded as the mite stayed in any of the odor
compartments beyond the first choice line. Thus, a mite could express both
choices or the first choice only. The total number of mites that expressed the
first choice or both choices was recorded. To neutralize any asymmetry in the
experimental setup, vials containing odor sources were reordered after testing
10Y15 mites, followed by a thorough cleaning of the chamber with absolute
alcohol and allowing the solvent to dry for 10Y15 min. The experimental
environment was at 25-C and 60Y70% relative humidity.
Olfactory responses were analyzed using ANOVA with Duncans multiple
range test. The impacted degree (ID) was calculated based on the following
formula (Mumcuoglu et al., 1996): degree of attraction = [1 j (C/T )]  100%
and degree of repellency = [1 j (T/C )]  100%, where T is number of mites in
the treatment and C is number of mites in the control.

RESULTS

Population of Mites in the Citrus Orchards. Figure 1 shows that A.


newsami and P. citri occurred in both the A. conyzoides intercropped and
2198 KONG ET AL.

FIG. 1. Population density (mean individuals per leaf ) of mites on citrus trees (A, in the
A. conyzoides intercropped citrus orchard; B, in the A. conyzoides nonintercropped citrus
orchard; C, in the A. conyzoides nonintercropped citrus orchard, after 24 hr of spraying
5% A. conyzoides essential oil emulsion; D, in the A. conyzoides nonintercropped citrus
orchard, after 48 hr of spraying 5% A. conyzoides essential oil emulsion).

nonintercropped citrus orchards, but that their population densities had obvious
differences. In the A. conyzoides intercropped orchard, the population density of
A. newsami reached 0.3 individual per leaf, and the P. citri population was
markedly decreased. In the A. conyzoides nonintercropped orchard, the A.
newsami population was below 0.1 individual per leaf, and the P. citri
population was increased over 0.2 individual per leaf. This indicated that
intercropping with A. conyzoides in citrus orchards increased the A. newsami
population and reduced the population density of citrus red mite to low and
noninjurious levels. This was possibly correlated with volatiles in the air.
Volatile Allelochemicals and Their Effects on Mites. Several terpenes, such
as carene, cubebene, copaene, limonene, myrcene, and pinene, were detected in
the air in both the A. conyzoides intercropped and nonintercropped orchards.
Abundant ageratochromene, demethoxy-ageratochromene, a-bisabolene, b-
caryophyllene, and E-b-farnesene were found in samples from the A. conyzoides
intercropped orchard, fresh leaves, and the essential oil of A. conyzoides, but
these were not detected in the air samples above the A. conyzoides noninter-
cropped orchard (Table 1). These volatile components in the orchards might
come from understory plants, soil, or other organisms, but ageratochromene,
demethoxy-ageratochromene, b-caryophyllene, a-bisabolene, and E-b-farnesene
were all major components of A. conyzoides fresh leaves and essential oil.
Particularly, ageratochromene and demethoxy-ageratochromene are specific in
the Ageratum genus (Kong et al., 2002, 2004a; Okunade, 2002). These
VOLATILE ALLELOCHEMICALS IN THE Ageratum conyzoides 2199

TABLE 1. CHEMICAL CONSTITUENT OF VOLATILES IN AIR SAMPLES COLLECTED FROM


DIFFERENT SOURCES

Fresh leaf of Essential oil of


Chemical Nonintercropped Intercropped A. conyzoides A. conyzoides
constituent citrus orchard* citrus orchard* (headspace) (headspace)

Ageratochromene 0a 6.6 T 1.3b 10.3 T 1.0c 31.2 T 5.1d


Demethoxy- 0a 8.9 T 1.7b 9.8 T 1.1b 21.5 T 4.4c
ageratochromene
b-Caryophyllene 0a 19.6 T 4.5b 28.1 T 2.4c 16.9 T 3.3b
a-Bisabolene 0a 9.8 T 1.9b 12.5 T 2.9a 10.1 T 1.7b
E-b-Farnesene 0a 10.2 T 2.1b 13.4 T 2.3c 9.3 T 1.1b
Carene 6.7 T 0.9a 2.2 T 0.9b 0c 0c
Cubebene 8.6 T 1.1a 7.8 T 1.7a 9.3 T 1.5b 3.9 T 0.3c
Copaene 9.7 T 2.3a 11.1 T 2.6a 5.4 T 1.7b 1.5 T 0.7c
Myrcene 11.2 T 1.7a 3.1 T 1.0b 0c 0c
Pinene 15.0 T 4.1a 2.3 T 0.7b 2.3 T 0.5c 0.9 T 0.2d
Limonene 33.2 T 6.8a 5.5 T 1.2b 0c 0c
Other unknown 15.6 T 3.8a 12.9 T 2.1b 8.9 T 2.2c 4.7 T 1.9d
components

Data were the relative amounts (%) of constituents from each sample.
* Means T SE from three independent experiments with nine sampling locations in the A. conyzoides
intercropped or nonintercropped citrus orchards for each determination are shown. Data not
followed by the same letter in a line are significantly different at P < 0.05, with Duncans multiple
range test.

chemicals did not occur in the air samples of the citrus orchard without
A. conyzoides, indicating that they were primarily released from A. conyzoides.
The presence of these volatile allelochemicals thus may make a contribution
toward regulating the population of the mites in the A. conyzoides intercropped
orchard.
Olfactometer trials showed that A. conyzoides fresh leaves, the essential
oil, and its four components had different effects on the olfactory responses of
A. newsami and P. citri (Table 2). The fresh leaves and essential oil as well as
demethoxy-ageratochromene, b-caryophyllene, a-bisabolene, and E-b-farnesene
strongly attracted A. newsami and slightly repelled P. citri at the test tem-
perature (25-C). It is noted that an olfactory response of mites to ageratochro-
mene was not achieved because ageratochromene is a crystal (mp 46Y47-C) and
difficult to volatilize at this test temperature. The olfactory response of
A. newsami to each individual component was clearly lower than to those of
A. conyzoides fresh leaves and the essential oil (Table 2), suggesting that this
effect could be intensified with the combinations of several components from
A. conyzoides.
Field experiments (Figure 1) showed that spraying the essential oil of
A. conyzoides on the citrus trees in the A. conyzoides nonintercropped citrus
2200 KONG ET AL.

TABLE 2. OLFACTORY RESPONSE OF MITES ON VOLATILES AND ITS MAJOR


CONSTITUENTS FROM A. conyzoides

Degree of attraction or repellency (%)


Volatiles A. newsami P. citri

Fresh leaf 61.11A (attraction) 7.69A (repellency)


Essential oil 95.45B (attraction) 14.81B (repellency)
b-Caryophyllene 59.09C (attraction) 7.69A (repellency)
a-Bisabolene 40.91D (attraction) 7.69A (repellency)
E-b-Farnesene 38.89D (attraction) 7.69A (repellency)
Demethoxy-ageratochromene 22.22E (attraction) 0.00C (repellency)

Data were mean value of three independent experiments with 50 mites for each determination and
not followed by the same letter in a column are significantly different at P < 0.05, with Duncans
multiple range test.

orchard increased the A. newsami population greatly. It increased from below


0.1 to over 0.3 individual per leaf at 24 hr after the essential oil emulsion spray,
which reached the same level as in the A. conyzoides intercropped citrus
orchard. It then decreased to 0.13 individuals per leaf after 48 hr. The results
indicate that the volatiles from A. conyzoides attract the predatory mite
A. newsami and increase its population on citrus tree leaves in the field. This
attraction was time-dependent, however, and could only be maintained for 48 hr
because of the oils volatility. The results suggest that the stable population
density of A. newsami in an A. conyzoides intercropped citrus orchard is
correlated with the continued release of volatiles from understory A. conyzoides
plants. Thus, intercropping A. conyzoides may increase the predatory mite
A. newsami population in citrus orchards.

DISCUSSION

The role of orchard ground cover plants in improving habitat and enriching
natural enemies of pests has been known for a long time (Bugg et al., 1990; Fye,
1983; House and Alzugaray, 1989; Lawton, 1982). It is necessary to select
beneficial plant species and pay attention to their chemical interactions with
understory plants and other organisms in the orchards. A citrus orchard is a
relative stable and complicated ecosystem. The population dynamics of mites in
citrus orchards often depends on the associated organisms, atmospheric tem-
perature, precipitation, and other factors (Liang and Huang, 1994). In this study,
A. conyzoides produced and released volatile allelochemicals into the air. These
were at least, in part, responsible for the population variations of mites,
VOLATILE ALLELOCHEMICALS IN THE Ageratum conyzoides 2201

particularly the predatory mite A. newsami. However, it remains obscure why


and how A. conyzoides manipulates the relationship between predatory mite and
citrus red mite through releasing volatiles.
Many plants defend themselves from herbivores by releasing volatiles that
manipulate the relationships among plants, herbivores, and their natural enemies
as soon as the plants are under attack (Dicke et al., 1990; Bruin et al., 1992;
Dicke, 1999; Sabelis et al., 1999; Agrawal, 2000; Bruin and Sabelis, 2001;
Kessler and Baldwin, 2001; Rausher, 2001). Many predatory mites are known to
respond to odors released by plants (Janssen, 1999; Shimoda and Dicke, 1999;
Maeda et al., 2001). However, most studies on the attraction of natural enemies
have been carried out with host plants infested with herbivores. Our research
suggests that the chemical interactions among predator, pest, and citrus can also
be achieved through intercropping.
It is noted that allelopathic inhibition was not apparent in the intercropped
citrus orchard. Generally, allelopathy occurs at the time of seed germination and
in early growth stages of plant species. Perennially adult citrus trees may resist
the allelochemicals released from understory A. conyzoides plants, or bulk
rhizosphere and soil microflora of the citrus may be able to rapidly biodegrade
any allelochemicals released into the soil from A. conyzoides (Liang and Huang,
1994; Kong et al., 2004c).
A. conyzoides has been a historical folk medicine in China and in several
countries of the world. It contains a wide range of secondary metabolites
including flavonoids, chromenes, benzofurans, and terpenoids that serve as
antimicrobial, insecticidal, and nematocidal agents (Ming, 1999; Okunade,
2002). This species also appears to be a valuable agricultural resource. Its
intercropping in citrus orchards has become popular in South China, and
substantial ecological and economic benefits have been achieved. Our results
suggest that there are natural chemical interactions among the organisms in
A. conyzoides intercropped citrus orchards, and that further clarification and
utilization of these interactions should be beneficial to integrated pest manage-
ment in citrus orchards.

AcknowledgmentsVThe authors thank professor S. S. Narwal, Haryana Agricultural


University, India, and two anonymous reviewers. This work was supported by the National Natural
Science Foundation of China (NSFC grant 30170182 and 39670141) and Hundreds-Talent Program,
Chinese Academy of Sciences (BR04135).

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