Published in : Biological Control (2012), vol. 60, pp. 108-112
Status : Postprint (Autor’s version)
The functional significance of E-β-Farnesene: Does it influence the
populations of aphid natural enemies in the fields?
Liang-Liang Cuia, Frédéric Francis5, Stéphanie Heuskinc, Georges Lognayc, Ying-Jie Liua, Jie Donga, Ju-Lian
Chend, Xu-Ming Songe, Yong Liua
a
College of Plant Protection, Shandong Agricultural University, Taian, Shandong 271018, PR China
b
Functional and Evolutionary Entomology, Gembloux Agro-Bio-Tech, University of Liège, Passage des Déportés 2, 5030 Gembloux,
Belgium
c
Laboratory of Analytical Chemistry, Gembloux Agro-Bio Tech, University of Liège, Passage des Déportés 2, 5030 Gembloux, Belgium
d
State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural
Sciences, 2 West Yuanmingyuan Road, Beijing 100193, PR China
e
Tobacco Limited Company of Weifang, Anqiu Branch, Anqiu, Shandong 262100, PR China
ABSTRACT
Aphids cause much damage to Chinese cabbage in northern China. Over reliance on pesticides have large
environmental and human health costs that compel researchers to seek alternative management tactics for aphid
control. The component of aphid alarm pheromone, E-β-Farnesene (EβF), extracted from Matricaria chamomilla
L., which attracts natural enemies in the laboratory, may have significant implications for the design of cabbage
aphid control strategies. The purpose of this paper is to understand the effects of EβF on natural enemies to
cabbage aphid control in Chinese cabbage fields. Ladybeetles on Chinese cabbage leaves in EβF released plots
and Aphidiidae in EβF released yellow traps were significantly higher than those of in controls. No significant
differences were detected in the interactions of different treatments and the two years for all natural enemies.
More important, lower aphid densities were found in EβF released plots. Our results suggested that the EβF
extracted from M. chamomilla L. could attract natural enemies to reduce cabbage aphids in the Chinese cabbage
fields.
GRAPHICAL ABSTRACT
Aphidiidae were significantly higher in EβF released yellow traps than in control yellow traps while ladybeetles
were significantly higher on EβF released plots plants than on control plots plants both in the two years (Figs. 1B
and 2A).
KEYWORDS : Chinese cabbage ; E-β-Farnesene ; Aphid alarm pheromone ; Biological control
HIGHLIGHTS




The stable component E-β-Farnesene (EβF) extracted from Matricaria chamomilla L.
We reported practicability of EβF on aphid natural enemies in Chinese cabbage fields.
Natural enemies on plants and in yellow traps were analyzed synchronously.
The EβF could reduce cabbage aphids by attracting natural enemies in the fields.
Published in : Biological Control (2012), vol. 60, pp. 108-112
Status : Postprint (Autor’s version)
1. Introduction
In Chinese cabbage production, the cabbage aphids (Hemiptera: Aphidiidae), Lipaphis erysimi (Kaltenbach) and
Myzus persicae (Sulzer) can frequently cause economic damage, if routine insecticide use is not employed. To
reduce insecticide inputs and associated economic, environmental and health costs, researchers are exploring
alternative, more sustainable strategies for managing pest populations. There is increasing interest in the use of
biological control agents to replace chemical pesticides (Cañamás et al., 2011 ). Biological control of vegetable
aphids using aphid natural enemies are likely to be preferred in future (Duan et al., 2011). The use of
semiochemicals has been recognized as a potential tool for the control of pest aphid populations (Rodriguez and
Niemeyer, 2005). The most prominent aphid semiochemical, alarm phero-mone, is an efficient signal molecule
that warns aphids of attack by natural enemies (Schwartzberg et al., 2008; Sun et al., 2010). The alarm
pheromone emitted by more than 40 aphid species (Xiangyu et al., 2002) contains the sesquiterpene, E-βFarnesene (EβF). EβF has been demonstrated to attract some aphid predators and parasitoids in the laboratory,
including ladybeetles (Nakumuta, 1991 ; Kielty et al., 1996; Zhu et al., 1999; Acar et al., 2001 ; Francis et al.,
2004; Verheggen et al., 2007), syrphid flies (Almohamad et al., 2007), lacewings (Boo et al., 1998; Zhu et al.,
1999) and Aphidius parasitoids (Micha and Wyss, 1996; Du et al., 1998). It may be exploited by natural enemies
that have developed the ability to locate their prey by perceiving and responding to this compound (Verheggen et
al., 2009).
Studies of the ecological importance of aphid alarm pheromone under natural conditions are necessary to
demonstrate its potential effects in the fields. However, so far, few experiments have been undertaken to show its
effects on natural enemies which control aphids on crops. The application of EβF in the field has been hampered
by its inherent instability. The EβF extracted from plant essential oils provides a solution to this problem,
because it appears to be highly stable, with a shelf-life spanning several years (Bruce et al., 2005). The EβF
extracted from the essential oil of Matricaria chamomilla L. (Asterales: Asteraceae) (Heuskin et al., 2009, 2010)
was used in our experiments. The M. chamomilla-derived EβF was demonstrated that it could attract parasitoid
Aphidius ervi Haliday by olfactometry (Heuskin et al., 2011) and predatory hoverfly in field experiments (Dr. S.
Heuskin, unpublished data). Our study system included Chinese cabbage fields with Brassica rapa pekinensis
(Brassicales: Brassicaceae), wherein occurred cabbage aphids and their natural enemies. We investigated the
effect of the aphid alarm pheromone component, EβF, on natural enemies of cabbage aphids, unaffected by
insecticide sprays in order to show the effects and practicability of EβF on aphid management in the field.
2. Materials and methods
2.1. Field experimental design
Field experiments were conducted at the experimental farmland of Shandong Agricultural University, Shandong
Province of China in 2009 and 2010. The trials consisted of two treatments as follows: (a) control plots and (b)
EβF [83.8 ±0.3%, extracted by flash chromatography from essential oil of M. chamomilla L (Heuskin et al.,
2010). Provided by Dr. S. Heuskin and Prof. F. Francis] released plots. A completely randomized design was
arranged in all treatments and each treatment was replicated three times. Plots measured 10 × 10 m, and were
separated along all edges by paths (10 m) to decrease the possibility of natural enemies dispersing among
treatments. About 2000 m2 area of grasses and groves distributed in the surroundings of the experimental plots.
They could provide partial source of natural enemies for the experiment.
Chinese cabbages ('Beijing new 3', Beijing Jingyanyinong SciTech Development Center) were planted in rows
with a row space of 60 cm and were sown on August 15, 2009 and August 17, 2010. All treatments were
fertilized with 110-50-150 (N-P-K) kg ha-1 and no herbicide and insecticide were used during the growing season
in each of the experimental plots. Plots were irrigated four times both in 2009 and 2010 (at the period of rosette
stage and heading stage).
Yellow pan traps (26 cm diameter 10 cm depth) (Provided by Prof. F. Francis) were put 10 cm above the ground
in the center of all the experimental plots. These traps were filled with a dilute detergent solution (Diao Brand,
Nice Group Co., Ltd.). Alarm pheromone component EβF releaser was mounted centrally in a 1-cm (in
diameter) rubber septum and close to the liquid surface of the traps in the treatment plots, allowing the chemical
to be released slowly. One hundred microliters of EβF solution in paraffin oil were deposited in releaser every
seven days. Seventy-six micro-grams of EβF was released from the formulation per seven days under the
conditions of 20°C, relative humidity of 65% and air flow: 0.5 1/min (Dr. S. Heuskin, unpublished data). The
first application of the chemical began on 15 September 2009, and 22 September 2010 at the rosette stage of
Chinese cabbage, and in all gave five applications both in 2009 and 2010.
Published in : Biological Control (2012), vol. 60, pp. 108-112
Status : Postprint (Autor’s version)
2.2. Sampling of natural enemy species and aphids
Natural enemies and aphids were sampled at 7-day intervals from 24 September to 20 October 2009 and from 29
September to 26 October 2010. On each sampling date, 20 Chinese cabbages were selected (five-point sampling
method, four plants per point) in each plot, Natural enemy and aphid species were selected based on their
abundance on the Chinese cabbage leaves and their potential to control cabbage aphids. Spiders, ladybeetles
(including adults and larvae) and mummified aphids on the plants were counted and recorded. Water in yellow
traps and EβF were renewed every seven days. All of insects in yellow traps were collected and brought back to
laboratory to be identified under a dissecting microscope, the species and the amounts were recorded. There were
few spiders in the traps, so their species and numbers were only identified and counted on the sampling plants.
Table 1 : Major natural enemies found in the Chinese cabbage fields during the whole period of sampling.
Insects
Order: family
Species
sampled
Predators
Araneae: Thomisidae
Misumjenops tricuspidatus Fabricius
Araneae: Linyphiidae
Eringonidium graminicola Sundevall
Araneae: Lycosidae
Lycosa sinesis Schenkel Pardosa astrigera L. Koch
Coleoptera: Coccinellidae Propylaea japonica Thunberg
Harmonia axyridis Pallas Coccinella septempunctata L.
Parasitoids
Hymenoptera: Aphidiidae Diaeretiella rapae McIntosh Aphidius gifuensis Ashmead
2.3. Statistical analysis
Because the populations of natural enemies during the whole sampling date were not significantly larger, so each
statistic data was the total number of five samples during investigation. All data on population densities of
natural enemies sampled in different treatments were analyzed using Independent-Samples t-test. The dependent
variable was the total number of predators and parasitoids observed on all 20 plants. The grouping variable was
the two treatments (EβF released plots and control plots). Effects of two treatments and two years were analyzed
using General Linear Model (GLM) procedure. Where necessary, the data used in t-test were transformed using
log10(x + 1) to meet assumptions of normality (SPSS, version 13.0 for Windows).
3. Results
3.1. The main natural enemy species in the experimental plots
The major natural enemy species of cabbage aphids in the Chinese cabbage fields were listed in Table 1.
Predators belonged to two orders, Araneae (Thomisidae, Linyphiidae and Lycosidae) and Coleoptera
(Coccinellidae). Parasitoids belonged to Hymenoptera (Aphidiidae).
3.2. Effects of E-β-Farnesene on the abundance of natural enemies of cabbage aphids on Chinese cabbage
leaves
Ladybeetles on Chinese cabbage leaves were significantly higher in EβF released plots than those of in control
plots (2009: P< 0.05; 2010: P< 0.05; Fig. 1B). There were no significant differences for mummified aphids and
spiders (Mummified aphids: 2009: P>0.05; 2010: P>0.05; Fig. 1A; Spiders: 2009: P>0.05; 2010: P>0.05; Fig.
1C).
3.3. Effects of E-β-Famesene on the abundance of natural enemies of cabbage aphids in yellow traps
Aphidiidae parasitoids in traps were significantly higher in EβF released yellow traps than those of in control
yellow traps both in 2009 and 2010 (2009: P< 0.05; 2010: P< 0.05; Fig. 2A). But there were no significant
differences for ladybeetles in the two years (2009: P>0.05; 2010: P>0.05; Fig. 2B).
3.4. Two-factor effects
A summary of the statistical analysis on the effects of treatment and year on the mean numbers of natural enemy
species were listed in Table 2. Significant differences were detected in ladybeetles on Chinese cabbage leaves
(P<0.01) and Aphidiidae parasitoids in yellow traps in treatment (P<0.01 ). Between the two years, there were
significant differences in mummified aphids (P<0.01), spiders (P<0.05) on plants, and ladybeetles in traps (P
<0.01). But no significant differences were detected in the interactions between year and treatment.
Published in : Biological Control (2012), vol. 60, pp. 108-112
Status : Postprint (Autor’s version)
3.5. Aphids populations on the plants of EβF and non-EβF plots
Aphids populations in EβF released plots were significantly lower than those of non-EβF plots in the two years
(2009: P<0.01; 2010: P<0.05; Fig. 3).
Fig. 1. Effects of E-β-Farnesene on natural enemies on Chinese cabbage leaves. Mean (±SE) abundance of
natural enemies (numbers on 20 Chinese cabbages) in Chinese cabbage fields with EβF released and control
plots. Each histogram is the total of five samples from 24 September to 20 October in 2009 and 29 September to
26 October 2010, different letters show statistically significant difference according to Independent-Samples ttest (P< 0.05). The sampling and statistical method are the same as in Fig. 2 and Fig. 3.
Published in : Biological Control (2012), vol. 60, pp. 108-112
Status : Postprint (Autor’s version)
Fig. 2. Effects of E-β-Farnesene on natural enemies in yellow traps. Mean (±SE) abundance of natural enemies
in yellow traps (numbers in traps).
Fig. 3. Effects of the attracted natural enemies by E-β-Farnesene to aphids control. Mean (±SE) abundance of
cabbage aphids (numbers on 20 Chinese cabbages).
Published in : Biological Control (2012), vol. 60, pp. 108-112
Status : Postprint (Autor’s version)
Table 2 : F-test on effects of treatments and years on the abundance of natural enemies.
Source of
df
F-values, natural enemies on plantsa
F-values, natural enemies in trapsa
variation
Mummified aphids Ladybeetles Spiders Aphidiidae parasitoids Ladybeetles
Treatment
1
4.062NS
22.000** 0.324NS
20.082**
0.400NS
Year
1
12.627**
0.000NS
9.596*
8.672*
0.711NS
Treatment*
1
2.051 NS
1.636NS 1.121NS
0.016NS
0.178NS
Year
a
NS: - not significantly different or P > 0.05.
* P < 0.05.
** P < 0.01.
4. Discussion
The quantity of target insects captured in the yellow traps is affected by many factors (Hou et al., 2006). In our
experiment plots, the same traps under the same condition were used for all species of natural enemies, the data
of the yellow traps may not always accurately show the effect of EβF, so we analyzed the amounts of natural
enemies on the Chinese cabbage leaves as a complementary approach to illustrate our conclusion.
Vinson's (1976) terminology described the host foraging behavior by both parasitoids and predators as a
succession of three steps: host habitat location, host location and host acceptance. It is possible that EβF released
in the experimental fields mainly enhance the efficiency of the natural enemies on the host location step. Host
location by the natural enemy on the food plant is guided by semiochemicals that mostly originate from the
aphids, in particular aphid alarm pheromone, honeydew, or the smell of the aphid itself (Hatano et al., 2008).
Host acceptance is guided by contact chemicals (Vinson, 1976). A preference to the color yellow has also been
shown to be a significant factor in the habitats location of parasitoids (Wäckers, 1994; Romeis et al., 1998). And
the parasitoids can be strongly attracted by aphid alarm pheromone under the color yellow (Powell et al., 1998).
Ladybeetles has also been demonstrated to prefer yellow cues, but this response to yellow is not fixed, since
ladybeetles prefer to select the color which was reinforced with food during conditioning (Seagraves, 2009). This
conclusion is supported by the results of our study that the number of Aphidiidae parasitoids was significantly
higher in EβF released yellow traps than those of in non-EβF released yellow traps while ladybeetles were
significantly higher on plants in EβF released plots than those of in non-EβF released plots (Figs. 1B and 2A).
Some compounds emitted by plants of the Brassicaceae in response to insect feeding damage can be exploited by
natural enemies to locate their preys (Francis et al., 2004; Jonsson et al., 2005; Yang et al., 2009). A complex
chemical cue of infected plants and herbivore pheromones (e.g. EβF) has been shown to be more attractive to
foraging parasitoids or predators than the individual components of the system (Blande et al., 2007). In our
experimental fields, a larger population of natural enemies was found in the traps or plants of EβF-treated plots.
It might show that EβF in combination with compounds of aphid-damaged Chinese cabbage plants (e.g.
Isothiocyanates) could strongly attract natural enemies to control cabbage aphids (Francis et al., 2004).
To understand the effects of the attracted natural enemies by EβF released in the fields on the cabbage aphid
control, we also investigated and analyzed the data of cabbage aphid population on the Chinese cabbage leaves.
The two main species of aphids, M. persicae (38.15%) and L. erysimi (61.85%) usually occurred concurrently on
Chinese cabbages in the fields of Shandong province. Significantly lower aphids populations were found in EβF
released plots than non-EβF released plots (Fig. 3). It was suggested that the attracted natural enemies by EβF
could reduce aphid population in the fields.
However, the component of aphid alarm pheromone, EβF, released in the fields could not only attract natural
enemies, but also greatly affect the behavior, life history, physiology, and morphology of cabbage aphids
(Kunert et al., 2005; Su et al., 2006). It also could play a role in aphid population fluctuation.
Given widespread adoption, exploiting this EβF from plants to attract natural enemies to control cabbage aphids
in the fields would appear to hold great promise for improving sustainable pest management while reducing
reliance on insecticides. However, more detailed work on its application rate, dose and duration under field
conditions need to be done before it turns to be a recommended approach for aphid control.
Acknowledgments
This study was supported by the research project Inter-University Targeted Project between Belgium and
China(PIC SHANDONG) and International Cooperation Project of The Ministry of Science and Technology of
the People's Republic of China (2010DFA32810).
Published in : Biological Control (2012), vol. 60, pp. 108-112
Status : Postprint (Autor’s version)
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