Development of a synthetic plant volatile‐based attracticide for

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Development of a synthetic plant volatile‐based attracticide for
Australian Journal of Entomology (2010) 49, 10–20
Development of a synthetic plant volatile-based attracticide for female
noctuid moths. I. Potential sources of volatiles attractive to Helicoverpa
armigera (Hübner) (Lepidoptera: Noctuidae)
aen_733
10..20
Alice P Del Socorro,1,2* Peter C Gregg,1,2 Daniel Alter2 and Chris J Moore3
1
Cotton Catchment Communities Cooperative Research Centre, Narrabri, NSW 2390, Australia.
School of Environmental and Rural Science, University of New England, Armidale, NSW 2351, Australia.
3
Animal Research Institute, Queensland Department of Primary Industries and Fisheries, Yeerongpilly, Qld 4105,
Australia.
2
Abstract
This paper is the first of a series which will describe the development of a synthetic plant volatile-based
attracticide for noctuid moths. It discusses potential sources of volatiles attractive to the cotton
bollworm, Helicoverpa armigera (Hübner), and an approach to the combination of these volatiles in
synthetic blends. We screened a number of known host and non-host (for larval development) plants for
attractiveness to unmated male and female moths of this species, using a two-choice olfactometer
system. Out of 38 plants tested, 33 were significantly attractive to both sexes. There was a strong
correlation between attractiveness of plants to males and females. The Australian natives, Angophora
floribunda and several Eucalyptus species were the most attractive plants. These plants have not been
recorded either as larval or oviposition hosts of Helicoverpa spp., suggesting that attraction in the
olfactometer might have been as nectar foraging rather than as oviposition sources. To identify
potential compounds that might be useful in developing moth attractants, especially for females,
collections of volatiles were made from plants that were attractive to moths in the olfactometer. Green
leaf volatiles, floral volatiles, aromatic compounds, monoterpenes and sesquiterpenes were found.
We propose an approach to developing synthetic attractants, here termed ‘super-blending’, in which
compounds from all these classes, which are in common between attractive plants, might be combined
in blends which do not mimic any particular attractive plant.
Key words
kairomone, moth attractant, olfactometer, plant volatile.
I NTRODUCTIO N
Plants emit volatile compounds that mediate insect–plant
interactions. These compounds can have either attractant or
repellent effects which can potentially be exploited to aid pest
management. We have recently registered an attract-and-kill
product (Magnet®) for use in integrated pest management
of the important noctuid pest species Helicoverpa armigera
(Hübner) and H. punctigera (Wallengren) in Australian cotton
and other crops (Australian Pesticides & Veterinary Medicines
Authority 2009). To our knowledge, this is the first synthetic
plant volatile-based attracticide which has been commercialised for noctuid pests of agriculture, despite the identification
in the laboratory of several attractive volatile compounds in
various host plants (Landolt 1989; Haynes et al. 1991; Heath
et al. 1992; Hartlieb & Rembold 1996; Bruce & Cork 2001;
Rajapakse et al. 2006), and experimental demonstrations of
the attractiveness of both crude plant extracts and synthetic
mixtures in the field (Zhu et al. 1993; Shaver et al. 1998;
Landolt & Alfaro 2001; Landolt et al. 2001; Landolt & Higbee
*[email protected]
© 2010 The Authors
Journal compilation © 2010 Australian Entomological Society
2002; Meagher 2002; Meagher & Landolt 2008). In this series
of papers, we discuss the theoretical underpinning of this
development as well as the demonstrations of field efficacy,
non-target impacts and other data required for registration of
products such as Magnet®. This paper describes the identification of potential sources of attractive volatiles, and a novel
approach to their combination in attractive blends.
The cotton bollworm, H. armigera, is an important economic pest of cotton and many other summer crops in Australia. The larvae are highly polyphagous, usually feeding on
the fruiting bodies, and the moths are attracted to many plants
either as food sources or oviposition sites (Zalucki et al. 1986;
Firempong & Zalucki 1990). In non-transgenic cotton, control
of this pest has usually been through insecticides targeted at
the larvae, which has led to H. armigera developing resistance
to a number of insecticides (Forrester et al. 1993). To help curb
resistance as well as to reduce environmental problems with
insecticides, the cotton industry has adopted an integrated
pest management approach including a resistance management scheme for H. armigera (Farrell 2008). More recently,
the extensive use of transgenic cotton expressing Bt toxins in
Australia (Fitt & Cotter 2005) has required the widespread
adoption of resistance management plans (Andow et al. 2008).
doi:10.1111/j.1440-6055.2009.00733.x
Plant volatiles as moth attractants
A range of approaches, including chemical, cultural and
behavioural manipulation, is incorporated in these plans.
However, there remains a need for new tools, including attracticides targeted at female moths (Gregg et al. 1998). In nontransgenic cotton, removing female moths from the population
could reduce oviposition, thus reducing the need for insecticides and allowing other components of integrated pest
management to work more efficiently. For transgenic cotton,
selective removal of potentially resistant moths using attracticides could reduce the frequency of resistance alleles. Alternatively attraction of female moths to refuge crops where they
might subsequently oviposit could enhance the production of
moths which have not been exposed to Bt toxin, an important
objective of the resistance management strategy (Farrell
2008).
The attractiveness of plants and plant odours to Helicoverpa
spp. and other noctuid moths is well documented. Extracts
from pigeon pea, Cajanus cajan, were shown to be attractive
to H. armigera moths (Rembold & Tober 1987; Hartlieb &
Rembold 1996). Rembold et al. (1991) demonstrated the
attractiveness of a synthetic chickpea (Cicer arietinum)
kairomone to H. armigera moths in laboratory and field
experiments. Floral compounds identified in the African marigold, Tagetes erecta, and their synthetic equivalents were
found to be attractive to H. armigera females (Bruce & Cork
2001). In the USA, volatiles emitted by the night-blooming
Gaura spp. have been shown to be highly attractive to Helicoverpa zea (Boddie) and other noctuid moths (Beerwinkle
et al. 1996; Shaver et al. 1998). The attraction of the cabbage
looper, Trichoplusia ni (Hübner), to various host plants and
host plant odours and to the floral compounds from nightblooming jessamine, Cestrum nocturnum, has also been
reported (Landolt 1989; Heath et al. 1992). Zhu et al. (1993)
demonstrated the attractiveness of various flowering plants to
the cutworm, Agrotis ipsilon (Hufnagel), the armyworm, Pseudaletia unipuncta (Haworth) and the corn earworm, H. zea.
Additional work has documented the existence of volatile
and non-volatile compounds which enhance oviposition.
Breeden et al. (1996) recorded oviposition stimulants for H.
zea from the isolated acids and alkane wax fractions of various
Lycopersicon (Solanaceae) species. Jallow et al. (1999) demonstrated that methanol, ethanol, acetone and pentane extracts
from leaves, squares and flowers of different cotton genotypes
influenced oviposition behaviour in H. armigera females in the
laboratory. Female moths laid more eggs on pentane extracts
of cotton flowers than extracts of leaves from pre-flowering,
early flowering and peak-flowering plants.
Plants which are not oviposition or larval hosts might also
provide a useful source of plant volatiles for use in attractand-kill formulations. Wilted (or fresh) leaves of the Chinese
wingnut tree Pterocarya stenoptera do not support larval
growth, but wilted leaves are attractive to H. armigera in China
(Xiao et al. 2002), as is also the case for wilted leaves of black
poplar (Wang et al. 2003). Gregg (1993) demonstrated the
widespread presence of pollen from non-larval host plants in
the genus Eucalyptus and family Brassicaceae on the proboscis of H. armigera moths, which indicates that moths were
11
feeding on nectar from these plants. For the purpose of developing attract-and-kill formulations, the ecological basis of the
attraction is of less consequence than the level of attraction,
and whether it varies according to the sex or mated status
of the moths.
In this paper, we report the attractiveness of various host
and non-host plants to unmated H. armigera moths in the
laboratory using an olfactometer. We document the volatile
compounds emitted by these plants which might be used in
attract-and-kill formulations, and describe an approach to
developing these formulations which does not involve mimicking the volatile emissions of particular attractive plants.
MAT ERIAL S AN D MET H ODS
Experimental insects
Laboratory-reared H. armigera moths from an insect culture
maintained in an insectary were used in the bioassays. The
culture originated from larvae collected from chickpeas in the
Darling Downs region of southern Queensland, and had been
maintained in the laboratory for at least 10 generations. Larvae
were reared individually in 35 mL plastic containers and
provided with a small block of soybean-based artificial diet
(Teakle 1991). Rearing conditions were 25–26°C, approximately 50% humidity and 16L : 8D photoperiod, with the dark
period between 09:30 and 17:30 h Australian Eastern Standard
Time (AEST). Day lighting was provided by six 40 W white
fluorescent tubes, and four 150 W incandescent bulbs. The
latter were connected to a time-controlled dimming system
providing 30 min transitions between the light regimes, to
simulate dusk and dawn (H. armigera moths fly throughout
the night, but simulating the natural transitions between day
and night could be important in initiating flight). Pupae were
sexed and upon emergence, moths were individually held in
150 mL plastic containers and fed distilled water only until
they were used in the olfactometer between 1 and 4 days of
age. Unmated moths were used because targeting females
which had not laid eggs would be expected to produce the
greatest reduction in oviposition. Moths were used once only
in the bioassays.
Bioassay system
A two-choice olfactometer based on the design of Beerwinkle
et al. (1996) was used in laboratory bioassays (Fig. 1). It consisted of a perspex box measuring 60 ¥ 25 ¥ 25 cm which had
two choice chambers on the floor in the upwind end. Entrance
by moths to each chamber was through a metal gauze funnel
(6 cm diameter) leading to a holding cylinder (10 cm diameter
and 17 cm high). Beneath this, and separated from it by a
metal gauze floor, was a sub-chamber which held either the
test plant or nothing (as control). Air was supplied from a
compressor located outside the building, and passed sequentially through two large PVC cylinders, one containing activated charcoal to remove extraneous volatiles, and the other
containing distilled water to humidify the air (approximately
© 2010 The Authors
Journal compilation © 2010 Australian Entomological Society
12
A P Del Socorro et al.
Fig. 1. The two-choice olfactometer system used in laboratory
bioassays.
50%), and bring it to room temperature (25–26°C). It was then
metered into each sub-chamber at the rate of 12 L/min and
extracted from the downwind end of the box to the outside
by a fan set to maintain a slight negative pressure (about
-10 kPa), to avoid any volatile contamination in the room.
The bioassay room had the same temperature and photoperiodic conditions as the insect rearing room. During the
scotophase (09:30–17:30 h AEST), the bioassay room was lit
by two 40 W red fluorescent photographic safelights. Day
lighting with simulated dusk and dawn similar to that in the
insectary was provided for the olfactometers in the bioassay
room.
In most cases, 50 moths were tested as a group in the
olfactometer for each run of each sex. They were placed in the
olfactometer at 08:30 h AEST (i.e. beginning of the simulated
dusk period) and a barrier separating them from the choice
chambers was removed at the start of full scotophase at
© 2010 The Authors
Journal compilation © 2010 Australian Entomological Society
09:30 h. After 8 h the moths which had entered each chamber,
and those which remained in the box, were counted. Moths
which died during the 8 h run (usually <2%) were excluded
from the counts.
We used two measures to determine attractiveness in the
olfactometer:
% positive response (100*T/N), and
% total response (100*(T + C)/N),
where
T = number of moths entering the test chamber
C = number of moths entering control (blank)
chamber
N = total number of moths in the olfactometer
We considered % positive response to be our primary
criterion of attractiveness. The extent to which moth activity,
especially upwind movement, is stimulated by the presence
of volatiles in the body of the olfactometer might influence %
total response. However, % positive response is the best indicator of the choice of moths to enter the test chamber.
We preferred the use of two separate measures of attraction
over the common approach of using ratios such as the coefficient of discrimination, CD = (T - C)/(T + C), because it is
less susceptible to the effects of low numbers entering either
chamber, as occurred in the blank olfactometer and with some
plants. Also the use of these two % response parameters recognises that moths which remain downwind, in the body of the
olfactometer, may not be neutral – they may in fact be responding negatively to volatiles from the test plants. The analysis
of the parameters, implemented by GLM models, is discussed
by Hern and Dorn (2001).
Each trial for a given test plant was replicated three times for
each sex. The sub-chamber which held the plant material (left
or right) was rotated between replicate trials to remove the
effects of any positional bias which may have occurred in the
olfactometer. A set of blank experiments (three replicates) was
done in which both sub-chambers had no test plant material.
One chamber was designated as ‘test’ and the other as
‘control’, and the two were alternated between replicates.
After each run, the olfactometer was dismantled and the component parts thoroughly cleaned using Pyroneg alkaline detergent in hot water followed by rinsing in cool water to remove
any volatiles originating from either plant or insect sources in
the previous run.
Plant materials
A total of 38 host and non-host plants (for larvae) of Helicoverpa spp. were tested in the olfactometer. These plants were
grouped into crops, weeds, ornamentals, Australian natives
and a Chinese tree (Table 1). Plants were collected from the
university glasshouses and farms, natural environments or
household gardens around the Armidale region. The Chinese
wingnut tree, P. stenoptera, originated from the Royal Botanic
Gardens at Mount Tomah, NSW. In most cases, plant materials
were collected within 30–60 min before testing. Fresh bouquets (about 50 g, containing both flowers and leaves) of
plants in small containers of water were held in the sub-
Plant volatiles as moth attractants
13
Table 1 List of plants tested for attractiveness to H. armigera moths in the olfactometer
Group
Australian native plants
Crops
Weeds
Ornamentals
Chinese tree (wilted leaves)
Plant name
Common name
Family name
Angophora floribunda‡
Eucalyptus viminalis†
Eucalyptus caliginosa†
Eucalyptus nova-anglica‡
Eucalyptus melliodora†
Acacia subulata
Acacia cambadgeii
Acacia sp. (not identified)
Eremophila gilesii
Eremophila sturtii
Helipterum floribundum
Ixiolaena brevicompta
Nicotiana velutina
Helianthus annuus†
Sorghum bicolor
Zea mays†
Lablab purpureus‡
Cajanus cajan†
Cicer arietinum†
Medicago sativa
Linum usitatissimum†
Gossypium hirsutum†
Brassica napus‡
Malus domestica†
Sonchus oleraceus‡
Galinsoga parviflora†
Bidens pilosa
Chicorium intybus†
Echium plantagineum†
Hirschfeldia incana‡
Araujia hortorum†
Calendula officinalis†
Gaura lindheimerii†
Westringia fruticosa
Jasminum officinale†
Lonicera japonica
Oenothera stricta
Pterocarya stenoptera
Rough barked apple
Manna gum
Broad-leaved stringybark
New England peppermint
Yellow box
Awl-leaf wattle
Gidgee
Myrtaceae
Myrtaceae
Myrtaceae
Myrtaceae
Myrtaceae
Mimosaceae
Mimosaceae
Mimosaceae
Myoporaceae
Myoporaceae
Asteraceae
Asteraceae
Solanaceae
Asteraceae
Poaceae
Poaceae
Fabaceae
Fabaceae
Fabaceae
Fabaceae
Linaceae
Malvaceae
Brassicaceae
Rosaceae
Asteraceae
Asteraceae
Asteraceae
Asteraceae
Boraginaceae
Brassicaceae
Asclepidiaceae
Asteraceae
Onagraceae
Lamiaceae
Oleaceae
Caprifoliaceae
Onagraceae
Juglandaceae
Charleville turkey bush
Turpentine
Large white sunray
Plains plover daisy
Wild tobacco
Sunflower
Sorghum
Corn
Dolichos lablab cv. Koala
Pigeon pea
Chickpea
Lucerne
Linseed
Cotton
Canola
Apple
Sow thistle
Yellow weed
Cobbler’s peg
Chicory
Paterson’s curse
Buchan weed
Moth vine
Marigold
Butterfly bush
Coast rosemary
Jasmine
Honeysuckle
Evening primrose
Chinese wingnut tree
†Volatile collections were done from these plants using solid-phase micro extraction. ‡Volatile collections were done from these plants using Tenax
collection.
chambers below the choice chambers. Leaves of P. stenoptera
were wilted at room temperature for 3 days prior to use
(including transit time from Mount Tomah), because this is the
method used in China, where fresh leaves proved unattractive
to H. armigera moths (Xiao et al. 2002).
Identification of plant volatiles
Collections of plant volatiles were done for 23 of the plant
species tested. For 16 plants, collection was done by means of
solid-phase micro extraction (SPME) in the test air stream
of the olfactometer, followed by thermal desorption from the
SPME fibre in the gas chromatograph-mass spectrometer
(GCMS) (Tholl et al. 2006). Freshly cut flowering bouquets
(also about 50 g of flowers and leaves) of the test plants were
held in the test sub-chamber for volatile collection. This was
done to ensure that the conditions of the plant materials during
the collection process were similar to those when moths were
used in the presence of these plants in the olfactometer.
Volatiles were collected for 30–60 min. In earlier testing of the
other seven plants, volatile collection was done by headspace
methods using adsorption onto the commercial substrate
Tenax, followed by thermal desorption in the GCMS (Tholl
et al. 2006).
To identify and quantify the volatiles, analysis was done by
conventional GCMS techniques on a Hewlett Packard 6890
series GC and HP 5973 mass selective detector (HewlettPackard, Palo Alto, USA). The column used was a HP-5MS
(5% phenyl methyl siloxane, 30 m ¥ 0.25 mm i.d., 0.25 mm
film thickness; J & W Scientific, Folsom, USA) fused capillary
column. The carrier gas was ultrapure helium set at a flow rate
of 0.8 m/s. The column temperature was programmed to
increase from 40°C (0.50 min hold) to 250°C at 20°C/min.
Temperatures of the splitless injector and the GCMS interface
were set at 280°C and 300°C respectively. Total run time was
30 min. A mass spectrum was scanned from m/z 30–300 and
© 2010 The Authors
Journal compilation © 2010 Australian Entomological Society
14
A P Del Socorro et al.
acquired data were collected and analysed on a HewlettPackard workstation using HP Chem/Station software, with
mass spectra from the NIST database and additional spectra
derived from authentic compounds.
Statistical analyses
For each test plant, the numbers of moths that entered the test
and control chambers in the three replicate runs for each sex
were compared with those in the ‘blank’ olfactometer using
R-analyses (Dalgaard 2002). Two sets of three blank runs
(nothing in either chamber of the olfactometer, with one set for
females and the other for males) were done for comparison
with the runs using test plants. Two statistical analyses were
done, using the GLM procedure in R with a quasibinomial
distribution appropriate to proportional data. The first one
dealt with the number of moths caught in the test chamber as
a percentage of the total moths placed in the olfactometer (%
positive response), while the second one, with the number of
moths caught in both the test and control chambers as a percentage of the total (% total response). The advantages of the
GLM approach using multiple measures in behavioural assays
are discussed by Hern and Dorn (2001).
R ESULTS
Attractiveness of plants in the olfactometer
Helicoverpa armigera moths showed significantly greater %
positive response to the test compared with the blank chamber
in 33 of the 38 plants tested (Table 2). Using the % total
response criterion, 27 of 38 plants were significantly more
attractive than the blank olfactometer. No plants were significantly less attractive than the blank olfactometer (i.e. repellent)
using the % positive response criterion, and only one (Acacia
cambadgeii) was repellent using the % total response criterion.
The three most attractive plants were the Australian native
plants, Eucalyptus nova-anglica, Angophora floribunda and
Eucalyptus melliodora. The other two Eucalyptus spp., viminalis and caliginosa, were also highly attractive to moths.
These plants are not known larval or oviposition hosts of H.
armigera. All the crop plants which are known hosts of H.
armigera as well as the seven weed plants showed significant
attraction to moths. Four of the six ornamentals tested were
also significantly attractive to moths. The non-attractive plants
included the native plants, Acacia subulata and A. cambadgeii,
the ornamentals L. japonica and Jasminum officinale and
wilted leaves of the Chinese wingnut tree, P. stenoptera.
Responses of males compared with females
Our two criteria to determine attractiveness in the olfactometer
(% positive response and % total response) were strongly
correlated with each other, and on both criteria the responses
of the two sexes were strongly correlated across all plants.
On the % positive response criterion, attractiveness to
males was strongly correlated with attractiveness to females
© 2010 The Authors
Journal compilation © 2010 Australian Entomological Society
(Male = 7.63 + 0.98 ¥ Female, P < 0.001, R2 = 0.87). A
similar correlation (Male = 10.7 + 0.96 ¥ Female, P < 0.001,
R2 = 0.84) was found using the % total response criterion. In
both cases, both the intercept and the slope were significant.
Outliers from these regressions are indicated in Table 2 by
the presence of separate means for each sex. In most cases,
outliers represent cases where even more males entered the
test and control chambers than would be expected from the
regressions.
Identification of plant volatiles
Plant volatiles were grouped into floral volatiles (fatty acid
derivatives, mostly short-chain alcohols and acetates, which
are products of nectar fermentation), green leaf volatiles (C6
fatty acid derivatives, straight chain alcohols, aldehydes and
esters mostly present in leaves), aromatic compounds (cyclic
C6 compounds and their derivatives, found in flowers and
leaves) and isoprenoids (mono- and sesquiterpenes which can
be found in both leaves and flowers) (Table 3). These groupings were based on the classifications of plant volatiles by
Knudsen et al. (1993) and Metcalf (1987).
Among the floral volatiles, ethanol and ethyl acetate were
the most commonly found, and were abundant in the highly
attractive Eucalyptus and Angophora spp. Green leaf volatiles
were found in most plants, whether highly attractive or not,
frequently in large quantities. Aromatic compounds were
usually found in small quantities, and rarely in the most attractive plants. The plants which produced the greatest quantities
of aromatic compounds, pigeon peas and jasmine, were among
the least attractive in the olfactometer. Monoterpenes were
found, often in large quantities, in the most attractive plants,
including (but not limited to) Eucalyptus and Angophora
spp. Prominent monoterpenes included cineole, a-pinene,
limonene, E-b-ocimene and g-terpinene. Sesquiterpenes were
also abundant, but less clearly associated with attractive plants.
Prominent ones included aromadendrene and caryophyllene.
DIS CUS S ION
Most plants tested in the olfactometer were significantly
attractive to one or both sexes of H. armigera moths (Table 2).
Of the 38 plants tested, only five (Acacia subulata, Lonicerus
japonicum, P. stenoptera wilted leaves, J. officinale and
A. cambadgeii) were not significantly different from the blank
olfactometer, using the % positive response criterion. This
result suggests that volatile compounds generating at least
some level of attraction to Helicoverpa moths are widespread
in plants.
In general, plants attractive to female moths were also
attractive to males. The significance of the intercepts in the
regression lines described above, the fact that the slopes of the
regressions were close to 1, and the results in the blank olfactometer (where the % total response was significantly different
between the sexes) all suggest that the main reason for significant sex differences in % total response was that males were
Plant volatiles as moth attractants
15
Table 2 Summary of results for the different plants used in the olfactometer
Plant material
% response†
E. nova-anglica
A. floribunda
E. melliodora
A. hortorum
E. caliginosa
N. velutina‡
C. officinalis‡
H. annuus‡
E. viminalis
B. pilosa
Z. mays‡
H. floribundum‡
G. lindhemerii
H. incana
M. domestica‡
L. usitatissimum‡
M. sativa‡
S. oleraceus‡
E. plantagineum‡
C. arietinum‡
L. purpureus‡
W. fruticosa
C. intybus‡
E. gilesii
Acacia spp. 2
I. brevicompta‡
E. sturtii
G. hirsutum‡
G. parviflora
S. bicolor‡
C. cajan‡
O. stricta‡
B. napus‡
A. subulata
L. japonica
P. stenoptera
J. officinale
A. cambadgeii
Blank
% total response ((test + control)/total)
% positive response (test/total)
67.4
64.3
54.6
52.3
51.0
48.8,
46.8
46.0
50.7,
43.8
42.6
53.5,
42.0
49.3,
50.3,
45.5,
39.2
48.6,
38.8
38.2
48.5,
37.3
35.4
34.9
39.8,
33.3
39.6,
30.8
29.7
†28.6
27.7
25.7
30.7,
19.9
24.7,
15.8
15.3
17.1,
18.9,
32.3
39.5
31.3
33.3
32.0
35.2
29.2
26.6
27.9
25.9
19.4
14.6
11.1
14.0
Sex
Attractant
Sex ¥
attractant
ns
ns
ns
ns
ns
0.004
ns
ns
0.030
ns
ns
0.018
ns
<0.001
0.002
0.009
ns
<0.001
ns
ns
0.006
ns
ns
ns
0.033
ns
0.025
ns
ns
ns
ns
ns
0.010
ns
0.003
ns
ns
0.05
ns
<0.001
<0.001
<0.001
<0.001
<0.001
<0.001
<0.001
<0.001
<0.001
<0.001
<0.001
<0.001
<0.001
<0.001
<0.001
<0.001
<0.001
<0.001
0.009
0.004
0.002
0.001
<0.001
<0.001
0.0001
<0.001
0.001
0.001
0.002
0.010
0.020
0.010
0.030
ns
ns
ns
ns
ns
–
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
–
% total
response†
72.6
73.2
68.3,
60.3
66.4
59.8,
70.0,
62.7,
68.7,
52.6
61.6
62.5,
52.3
60.0,
64.5,
57.7,
49.8
58.6,
65.9,
63.6
58.9,
55.4,
39.3,
48.9,
49.3,
45.3
63.6,
48.0,
45.7
43.4
40.6
33.8
47.9,
30
42.0,
34.6,
48.4,
31.2,
32.9,
59.1
48.7
58.5
51.5
55.1
48.2
46.0
41.9
45.9
43.0
46.6
43.1
48.8
44.5
41.6
37.6
41.3
38.6
30.3
30.6
36.4
38.0
20.3
29.3
Sex
Attractant
Sex ¥
attractant
ns
ns
0.042
ns
ns
<0.001
<0.001
0.008
<0.001
ns
ns
0.017
ns
<0.001
<0.001
<0.001
ns
<0.001
0.013
ns
0.020
0.040
ns
0.040
0.020
ns
<0.001
0.010
ns
ns
ns
ns
<0.001
ns
<0.001
ns
0.020
<0.001
0.036
<0.001
<0.001
<0.001
<0.001
<0.001
<0.001
<0.001
<0.001
<0.001
<0.001
<0.001
<0.001
0.001
<0.001
<0.001
<0.001
0.001
<0.001
0.003
0.010
0.017
<0.001
ns
0.001
0.040
0.050
<0.001
0.010
ns
ns
ns
ns
ns
ns
ns
ns
ns
<0.001
–
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
0.001
ns
ns
ns
ns
ns
ns
ns
0.011
ns
ns
ns
0.003
ns
ns
ns
ns
ns
ns
ns
ns
0.010
ns
ns
–
†For plants with significant effect of sex or a significant interaction between sex and attractant, the data in the format x, y are for males (x) and females
(y). For plants where no such effects existed, the single figures are means for combined male and female runs. ‡Known host plant for larvae (Zalucki
et al. 1986, 1994 or PC Gregg unpubl. data 1993).
Plants are listed in order of attractiveness (average of males and females). ‘Sex’ indicates the significance (P-value) of a GLM R analysis comparing
males and females. ‘Attractant’ indicates the significance (P-value) of a GLM R analysis comparing the plant with the blank olfactometer.
ns, not significant (P > 0.05).
generally more active in the olfactometer, and more likely to
move upwind into either chamber. Thus, plants which were
differentially attractive to one or other sex could only be identified by a significant sex–attractant interaction. No such plants
were identified using the primary criterion of % positive
response, and only four were indentified using the secondary
criterion of % total response. These four plants were Malus
domestica, Chicorium intybus, Eremophila sturtii and P.
stenoptera.
Potential sources of moth attractants which might be used in
managing H. armigera include any plant which is attractive for
adult nectar foraging and, in the case of females, for oviposi-
tion. Helicoverpa spp. has a wide host range for oviposition
and larval development. Zalucki et al. (1986, 1994) recorded
H. armigera from 101 plants in 30 families and the endemic
species H. punctigera from 172 plants in 40 families. Less is
known about hosts for adult feeding, but studies on mothborne pollen have shown that Helicoverpa moths feed on
flowers from many non-host plants such as Eucalyptus spp.
and weeds in the Brassicaceae, as well as many larval host
plants (Gregg 1993; A Del Socorro & P Gregg unpubl. data
2001).
The attraction of H. armigera moths to some plants in the
olfactometer in our study was probably for adult feeding rather
© 2010 The Authors
Journal compilation © 2010 Australian Entomological Society
Class
F
F
F
F
F
F
F
F
F
C6F
C6F
C6F
C6F
C6F
C6F
C6F
C6F
C6F
C6F
C6F
C6F
A
A
A
A
A
A
A
A
A
A
A
A
A
A
A
A
M
M
M
M
M
M
M
M
Compound†
Butanoic acid
Butyrolactone
Ethanol
Ethyl acetate
Octanoic acid
1-dodecanol
1-octen-3-ol
Decanal
Nonanal
(E)-2 hexenal
(E)-2-hexen-1-ol
(E)-2 hexenyl acetate
(E)-2 hexenyl hexanoate
(E)-3 hexenol
(Z)-3 hexenol
(Z)-3 hexenyl acetate
(Z)-3 hexenyl butyrate
(Z)-3 hexenyl formate
Ethyl hexanoate
Hexenal
Hexyl hexanoate
Benzoic acid
Benzyl acetate
Benzaldehyde
Benzyl alcohol
Benzyl propanal
Cinnamaldehyde
Durene
Indole
Methyl salicylate
Phenol
Phenylacetaldehyde
2-phenoxyethanol
Phenylethanol
p-acetylethylbenzene
p-cresol
2,4-tert-butylphenol
Azulene
(E,E) alloocimene
Camphene
Cineole
Geraniol
Geraniol acetate
Geranylacetone
Isoeugenol
© 2010 The Authors
Journal compilation © 2010 Australian Entomological Society
+
++
+++
En
+
+
+++
+
+
+++
+
+
+++
+++
+++
+
+
+
Ec
++
tr
+
Ah
+
++
++
Em
+++
+++
Af
Table 3 List of compounds identified from various plants
++
Co
+
++
++
+++
Ev
++
+++
Ha
+++
++
+
++
+
Zm
tr
+++
tr
Gl
+
+++
+++
Hi
tr
++
++
tr
++
++
++
++
+++
tr
++
++
Md
+++
Lu
So
+
+
+++
+++
Ep
+
+++
Ca
+
+++
+++
+++
+++
Lp
+++
Ci
+++
tr
++
++
+
Gh
++
+++
Gp
++
++
++
++
++
++
Cc
++
+++
Bn
++
+++
+++
+
+
Jo
16
A P Del Socorro et al.
M
M
M
M
M
M
M
M
M
M
M
M
M
M
M
M
M
M
M
S
S
S
S
S
S
S
S
S
S
O
O
O
O
++
tr
++
tr
tr
tr
++
tr
++
++
+
++
tr
tr
+++
+++
tr
+
++
+++
tr
tr
+++
++
+
+
+++
++
tr
+
+
+++
++
++
++
+++
++
++
++
++
+++
tr
tr
+
++
tr
+
+++
++
+++
++
++
tr
+
+
++
+
++
++
++
+
++
tr
+++
+
++
++
++
++
+
+++
++
++
++
+++
+
++
+
++
+++
+++
+
+
++
†Classifications were based from those of Knudsen et al. (1993) and Metcalf (1987). F – floral volatiles, C6F – C6 fatty acid derivatives found in leaves (green leaf volatiles), A – aromatic compounds,
M – monoterpenes, S – sesquiterpenes, O – other. Relative abundance of the volatiles is denoted by tr = < 0.1%, + = 0.1 - 1%, ++ = 1 - 10%, +++ = >10% of total volatile compounds identified for that plant. Plants
are arranged left to right in order of attractiveness in the olfactometer (Table 2). En – Eucalyptus nova-anglica, Af – Angophora floribunda, Em – Eucalyptus melliodora, Ah – Araujia hortorum, Ec – Eucalyptus
caliginosa, Co – Calendula officinalis, Ev – Eucalyptus viminalis, Ha – Helianthus annuus, Zm – Zea mays (silk), Gl – Gaura lindhemerii, Hi – Hirschfeldia incana, Md – Malus domestica, Lu – Linum usitatissimum,
So – Sonchus oleraceus, Ep – Echium plantagineum, Ca – Cicer arietinum, Lp – Lablab purpureus, Ci – Chicorium intybus, Gh – Gossypium hirsutum, Gp – Galinsoga parviflora, Cc – Cajanus cajan, Bn – Brassica
napus, Jo – Jasminum officinale.
Isopulegol
a-guajene
Limonene
Linalool
E–b–ocimene
Sabinene
Terpinolene
a-terpinolene
a-phellandrene
b-phellandrene
a-pinene
b-pinene
b-myrcene
o-cymene
p-cymene
a-terpinene
g-terpinene
a-terpineol
a-thujene
Aromadendrene
Copaene
Viridiflorene
Ylangene
g-cadinene
d-cadinene
a-Caryophyllene
b-Caryophyllene
a-himachalene
b-elemene
Cyclohexene
Cyclopentene
Dimethyl disulphide
Allyl isothiocyanate
Plant volatiles as moth attractants
17
© 2010 The Authors
Journal compilation © 2010 Australian Entomological Society
18
A P Del Socorro et al.
than oviposition particularly as unmated females were used
in the experiments. This is suggested by the attractiveness of
plants like the four Eucalyptus spp. and Angophora floribunda.
These plants are not known hosts for either larval feeding or
oviposition of Helicoverpa spp. The attractiveness of these
non-host plants as well as most of the other plants tested in the
olfactometer could have been largely due to the presence of
flowers in the test plant materials, as floral odours release
food-seeking or feeding behaviour in moths (Brantjes 1973,
1978 as cited by Dobson 1994). A similar lack of correlation
between the larval host status and attractiveness in the olfactometer is indicated by the two native Asteraceae we tested,
Helipterum floribundum and Ixiolaena brevicompta. Both are
good larval hosts for H. armigera and H. punctigera (Zalucki
et al. 1994), and I. brevicompta has been proposed as a
‘primary host’ for the latter species (Walter & Benfield 1994).
However, in our assays I. brevicompta was much less attractive
than H. floribundum.
It is not surprising that all the crop plants tested were
significantly attractive to both sexes. They are mostly known
hosts of larvae. Crops such as corn and sunflower are preferred
oviposition hosts (Firempong & Zalucki 1990; Fitt 1991).
Pigeon pea extracts and synthetic chickpea kairomones have
been reported to be attractive to mated H. armigera female
moths (Rembold & Tober 1987; Rembold et al. 1991; Hartlieb
& Rembold 1996), and these plants are highly attractive for
oviposition in the field, so much so that pigeon pea is a preferred species for refuge crops, which are used to breed susceptible moths for the management of resistance to transgenic
cotton (Baker et al. 2008; Farrell 2008). However, they were
not especially attractive in our study, perhaps indicating that
they are not good adult feeding hosts. Similarly, cotton, the
crop which suffers the greatest economic losses to Helicoverpa spp. in Australia (Adamson et al. 1997), was not especially attractive by comparison with other hosts. Cotton has
also been shown to be a less preferred plant for oviposition by
H. armigera females under laboratory conditions (Firempong
& Zalucki 1990; Jallow & Zalucki 1996).
The majority of the weed plants we tested in the olfactometer are known larval or oviposition hosts of H. armigera,
and were observed to be attractive to the moths. Sow thistle,
Sonchus oleraceus, which is well known as a weed host for
larval H. armigera (Gu & Walter 1999) was highly attractive to
the adults. However, Buchan weed (Hirschfeldia incana)
which is not a larval host was also highly attractive. Of further
interest among the weeds is the attractiveness of moth vine,
Araujia hortorum. This species is closely related to A. sericofera (bladder flower), which has been reported to produce the
volatile compound phenylacetaldehyde and was found to be
attractive to noctuid moths (Cantelo & Jacobson 1979).
In China, farmers trap H. armigera moths in cotton fields
using branches of wilted leaves of the wingnut tree, P.
stenoptera (J-W Du pers. comm. 1997). Extracts of this plant
were also found to be attractive to the Chinese H. armigera
moths in an olfactometer (Xiao et al. 2002). As this tree does
not appear to provide nectar for adults, and is not a suitable
larval host, the presence of volatiles attractive to H. armigera
© 2010 The Authors
Journal compilation © 2010 Australian Entomological Society
would seem to be serendipitous, as is the case for wilted poplar
leaves (Wang et al. 2003). We tested wilted P. stenoptera
leaves sourced from the Royal Botanic Gardens at Mount
Tomah, NSW but they were not attractive to Australian H.
armigera moths. Australian H. armigera moths were also not
attracted to steam distilled extracts of P. stenoptera sourced
from China (A Del Socorro & P Gregg unpubl. data 2002).
Whether there are physiological differences between the
Chinese and Australian H. armigera in response to plant
volatiles from P. stenoptera is not known.
The chemical composition of volatile emissions from
flowers and other plant parts varies according to whether the
parts are picked or cut, or left attached to the plant. Mookherjee et al. (1990) showed that the composition and quantity of
odours emitted by picked flowers differed significantly from
those left intact or attached to the plant. Matile and Altenburger (1988) also reported that periodicity of flower fragrance
changes in detached or intact flowers. In our olfactometer
studies, freshly cut bouquets of flowers and leaves were used
as it was not physically feasible to use whole or intact plants
with the olfactometer design. Hence, it is possible that the
volatile profiles of our test plant materials would have been
different from those of intact plant materials. The degree of
damage and the time between cutting and testing in the olfactometer may have influenced the amount of some volatiles. For
this reason, caution must be applied when extrapolating from
our results to the relative attractiveness of crops and other
plants in the field. However, the primary purpose of our study
was to identify plant volatiles which might be useful in synthetic attractants for management of H. armigera. The plant
materials used for volatile collections were in the same conditions as the test plants used in the olfactometer (i.e. freshly
cut bouquets), and the collection source was identical (the
airstream of the olfactometer) so we would have expected
similar volatile profiles from the same plants, whether used for
volatile collection or for moth response testing.
In developing moth attractants for a highly polyphagous
species like H. armigera, the question of which plant to mimic
arises. Previous attempts to develop synthetic plant volatile
attractants have mimicked the volatile profiles of particular
larval host plants, such as Gaura suffulta (Shaver et al. 1998),
pigeon pea or chickpea (Hartlieb & Rembold 1996) and
the African marigold, Tagetes erecta (Bruce & Cork 2001).
However, we have shown here that non-host plants can be
highly attractive, at least to unmated unfed moths such as those
used in our experiments. For attract-and-kill of females, targeting unmated females is advantageous because they have not
already laid eggs. Each female killed represents a loss to the
population of her entire potential fecundity (1000–2000 eggs
in the case of Helicoverpa spp.; Zalucki et al. 1986). Clearly,
volatiles from non-host plants should be considered as potential candidates for inclusion in synthetic attractant blends.
Another possible complication in using plant mimics as
attractants for polyphagous insects is learning. Learning in
feeding and oviposition behaviour has been demonstrated in
H. armigera (Cunningham et al. 2004, 2006). In natural habitats, preferences of moths for different hosts (with different
Plant volatiles as moth attractants
volatile profiles) are likely to be influenced by the abundance
of these hosts (Cunningham et al. 1999). Developing a synthetic blend which mimics a particular host could be ineffective if that host is rare in a region where the formulation is
to be used. Conversely, even a less attractive host in a monoculture may be preferred to a synthetic attractant mimic, if
the insects are conditioned to respond to that plant.
Our approach to developing synthetic attractant blends,
which we term ‘super-blending’, does not involve mimicking
the composition of volatiles in any one host plant. Instead, we
propose identifying compounds that are in common between
the highly attractive plants (regardless of the relative quantities
in these plants), and then blending those compounds in combinations which may not occur in nature. This approach could
potentially avoid any difficulties of learned responses, and
allow the inclusion of volatiles from non-host plants which
might enhance the attractiveness of the blend to unmated
females. In such an approach, volatiles worth considering
could include representatives from all the classes we considered, but especially monoterpenes such as cineole, limonene
and a-pinene, most of which have not previously been used in
noctuid moth attractants. Additional candidate volatiles could
be derived from electroantennogram studies, either using
single cell responses (Røstelien et al. 2005) or whole antennae
(Cribb et al. 2007). However, caution is required in extrapolating from these responses to behavioural responses in the
olfactometer or in the field. In subsequent papers we will
describe laboratory and field-based bioassays of super blends
containing volatiles, identified from this study and from the
literature, against H. armigera and H. punctigera (Del Socorro
et al. 2010; Gregg et al. 2010).
ACKNOWLE DG E ME NT S
We thank George Henderson for technical assistance in the
olfactometer experiments, and Jackie Reid for assistance
with statistical analyses. The Australian Cotton Cooperative
Research Centre provided funding. Myron Zalucki and Lewis
Wilson provided useful comments on earlier drafts of the
paper.
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Accepted for publication 27 August 2009.

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