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A brief review of Pentatomid Bug pheromones and their role in

Integrated Pest Management (IPM)
Ishana Qadir, Ayesha Qamar*, Iram Khan, Ashiq Hussain Mir and Rizwana Begum
Department of Zoology, Aligarh Muslim University, Aligarh-202002
E-mail : Ayesha.zoology@gmail.com
Abstract
Pentatomids constitute one of the largest heteropteran families with
almost 5000 species in 900 genera of 10 subfamilies worldwide. Phytophagous
pentatomid bugs are occasional to chronic pests in all types of crop systems.
They are a threat to cotton, corn, sorghum, soybeans, ornamental trees, shrubs,
vines, weeds, and many cultivated crops. These insects are known well for
producing blends of odoriferous compounds, i.e. pheromones which include
aliphatic hydrocarbons, aldehydes, oxoalkenals, and esters serving a variety of
functions such as communication, defense (allomones), aggregation, and
Corresponding Author finding mates. Defense pheromones have received considerable attention
Ayesha Qamar
because they are produced in large quantity and are easily identifiable, but it is
Department of Zoology,
the sex pheromones that are of particular interest to agricultural integrated pest
Aligarh Muslim University,
Aligarh - 202002 management programs. Sex pheromones are either present both in males and
Email : females or may be unique to only a particular sex. The content of this review
Ayesha.zoology@gmail.com focuses on the characterization of pheromonal gland constituents of the family
Article History Pentatomidae and the possible prospects of their commercialization and
Received on 16 February, 2015; application in integrated pest management of these important pests.
Received in revised form
25 April, 2015; Accepted Keywords : Pentatomidae, phytophagous, bugs, pheromone, allomones,
10 May, 2015 cotton, corn, sorghum, soybeans and IPM.

Introduction selective advantage (e.g. herbivore damaged plant

Pheromones are chemical compounds that
mediate interactions between individuals of the same
species, and allelochemicals are chemical compounds
that mediate interactions between individuals of
different species. Within the allelochemicals there are
three classes, depending on the interaction between the
organisms involved: if the chemical mediates an
interaction, that provides a selective advantage to the
emitter (e.g. an irritant that deters a predator), it is
referred to as an allomone; if the selective advantage is
to the receiver (e.g. when a predator uses a pentatomid
smell to locate its prey) it is referred as a kairomone;
if both organisms receive i.e. emitter and releaser
elicits volatiles that attract an insect that kills the
herbivore), it is referred to as a synomone. Karlson and
Luscher (1959) first defined pheromones as "substances
that are excreted to the outside by an individual and
received by a second individual in whom they release
a specific reaction, for example a definite behaviour
or developmental process". They further state that
"strict species specificity is not required" and that
"the principal of minute amounts being effective
holds". A few years later, and after the first pheromones
had been identified in a moth. Wilson and Bossert
(1963) suggested that rapid behavioural and slower
physiological effects can be distinguished by the
terms "releaser" and "primer" respectively. These terms

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unfortunately have led to some confusion because
some pheromones can induce both priming and releaser
effects (Sorensen et al., 1989). Over the past four
decades, extensive research on insect pheromones has
resulted in the chemical and/or behavioral elucidation
of pheromone components from thousands of insects.
Defining features of insect pheromone systems are
that the pheromones are frequently multicomponent
blends (Silverstein and Young, 1976) of geometric or
optical isomers. Seybold (1993) reported role of
chiratity in olfactory directed behaviour aggregation
of pine engraver bettle of genus Ips (Coleoptera :
scolytidae). Insect pheromone systems can also vary
geographically among populations of the same species
(Seybold et al., 1995; Miller et al.,1997). In a number
of cases the acquired knowledge of insect pheromones
has found application in integrated pest management
(IPM) tactics. Although insect pheromones represent
a myriad of chemical functionalities (Favaro and
Zarbin, 2012), the composite pheromones have been
classified into six behaviorally functional groups: sex,
aggregation, dispersal (spacing or epideictic), alarm,
recruitment (trail), and maturation (Harbourne, 1993).
Role served by pheromones in pentatomids
Pentatomidae, Greek pente meaning five and
tomos meaning section, are a family of insects belong-
ing to order Hemiptera including stink bugs and
shield bugs. It is one of the largest Heteropteran
families with almost 5000 species in nearly 900
genera of 10 subfamilies. As a group, stink bugs use
their piercing and sucking mouthparts to feed on a
variety of plants and insects. These insects are one of
the main agricultural pests in the world and have
become increasingly problematic with the advent of
genetically modified crops (Bundy and McPherson,
2000). Stink bugs as their name suggests are
characterized by the production of large quantities of
strong odoriferous compounds, i.e. pheromones which
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include aliphatic hydrocarbons, aldehydes, oxoalkenals,
and esters serving a variety of functions such as
communication, defense (allomones), aggregation, and
finding mates. In adults, the defensive compounds
are produced in large, well defined, and usually
colored meta thoracic glands (MTGS), which are not
present in the immature stages. Instead, the nymphal
defensive compounds are produced in dorsal abdominal
glands (DAGS) (Staddon, 1979). Our ongoing study on
pheromone glands of Halyomorpha halys revealed
the location and structure of meta thoracic glands by
scanning electron microscopy (Fig. 1, 2 and 3). It is
well-known that the proportions of compounds present
in DAG secretions differ among the five nymphal
instars (Favaro and Zarbin, 2012). However, it has also
been reported that the composition of the pentatomid
MTG secretions may also differ according to the insect
adult age. The identification of the contents of MTG
secretions has received considerable attention, partly
because these secretions constitute such an obvious
defense, and because large quantities of simple
compounds produced are easy to analyze and (Favaro
and Zarbin, 2012).
Role of pheromones in IPM
IPM also known as Integrated Pest Control (IPC),
is a broad-based approach that integrates practices
for economic control of pests. IPM aims to suppress
pest populations below the economic injury level
(EIL). The use of chemical pesticides dominates the
pest control strategies ever since World War II, but
their serious health implications, to man as well as
environment, have prompted mankind to seek other
viable and eco- logically acceptable ways to suppress
pest populations. The toxicity of various groups of
chemical pesticides is now a well established fact
and various studies have demonstrated their health
implications like severe neuronal, reproductive,
immunological, and carcinogenic complications,
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genetic toxicity and severe oxidative stress have been Hence similar experiments were carried out to
reported from various laboratory studies on mammals demonstrate the efficacy of pheromone traps.
and insect models (Abdollahi et al., 2004; Mehdi and Compounds used by pentatotomids as pheromones
Qamar, 2013). The first sex attractant determined from a stink
However, recent changes in crop protection bug was obtained from Nezara viridula L. Sexually
methods involve more specific control strategies
and pheromones take the first place in this order. To
date, it has been demonstrated that the pheromone
blends for the various stink bug species are species
specific and are attracted to one and in some cases
possibly both sexes in laboratory, field cage, and full
field bioassays. The effectiveness of the synthetic
sex pheromone of the Neotropical brown stink bug,
Euschistus heros, was evaluated both in laboratory
Fig.-1. External opening (red arrow), situated between
and in field assays (Borges et al., 1999). The Pentatomid the second and third pair of legs (blue arrows), of the
bug P. guildinii was caught in large numbers in phero- metathoracic scent gland system (MTGs) of H. halys
mone traps baited with 2,6,10- trimethyltridecanoate
male produced pheromone of E. heros, this pheromone
was also helpful in catching egg parasitoid used as
a kairomone (Borges et al., 1998). Females, males, and
nymphs of E. conspersus, E. tristigmus, E. Servus and
E. politus were significantly attracted to methyl (2E,
4Z)- decadienoate in field tests conducted in California
and Maryland. Tests in Maryland also demonstrated
that the parasitic tachinid flies use the Euschistus
unsaturated methyl-ester as a host - finding kairomone. Fig. 2. Cuticular microsculptures in the pleural scent
A 2-yr on-farm study to examine the attractiveness area of the MTGs
and possible cross-attraction of the reported pheromones
for N. viridula and A. hilare and those previously
discovered for Euschistus servus (Say) and Plautia
stali Scott to N. viridula, A. hilare, and E. servus. The
attractiveness of selected pentatomid pheromones to
tachinid parasitoids of stink bugs was also examined.
It was shown for the first time under field conditions
that N. viridula can be trapped with its reported
pheromone, a 3:1 trans- to cis-(Z)-alpha-bisabolene
epoxide blend. It was also shown that attraction of
N. viridula increased with higher phero- mone doses. Fig. -3. SEM image of Meta thoracic gland in H. halys

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mature males of the southern green stink bugs
release a pheromone attractant in the field to con-
specific females, males, and late-stage larvae and to the
parasitoid Trichopoda pennipes (Diptera: Tachinidae)
which uses it as kairomone. The pheromone blend
typically includes (Z)--bisabolene (17%), Trans- and
cis-1, 2-epoxides of (Z)--bisabolene (44 and 15%,
respectively), (E)- nerolidol (1.4%), and n-nonadecane
(7.4%). The existence of Nezara pheromone strains,
first suggested by different Trichopoda parasitization
of geographically isolated N. viridula populations, has
been chemically verified (Aldrich et al., 1987).
Chemical analysis of the pheromone gland
extract of another pentatomid bug P. distinctus male
(Zanuncio et al., 1997) indicated that this species
produces a pheromone containing the major compounds
of P. nigrispinus and S. cincticeps. Species in the
genus Podisus (Heteroptera: Pentatomidae) are
considered as a generalist predator (Borges, 2011) and
several are key predators in agricultural ecosystems
of the western hemisphere. The most common North
American species, Podisus maculiventris (Say) (called
the spined soldier bug), was the first predaceous
insect for which a long-range attractant pheromone
was identified (Aldrich et al., 1984). Exocrine secretions
of the male dorsal abdominal gland secretion of
P. nigrispinus contained little (E)-2-hexenal or linalool,
each of these compounds was found to be a major
component of the male dorsal abdominal gland
secretion of P. distinctus.
Gland extracts of Podisus (Heteroptera: Penta-
tomidae : Asopinae) and Supputius species have been
analyzed by Jeffrey et al. (1997). Dorsal abdominal
gland contents were found to be sex and species
specific. The dorsal abdominal gland secretions of
P. nigrispinus and P. distinctus nymphs were found to
be of similar composition, whereas that for S. cincticeps
contained much more undecane than tridecane. Dimers
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(probably artefacts) of (E)-4-oxo-2- hexenal where
detected in each exuvial extract. The metathoracic
scent gland contents are essentially the same for
males and females and are not species-specific except
for very minor components (e.g. benzyl acetate in
P. distinctus). However, as for nymphs, the meta-
thoracic scent gland chemistry of these species exhibits
specificity at the generic level in that the secretion
from S. cincticeps adults have relatively more undecane
and (E)-2-octenal than is produced in the metathoracic
scent glands of the Podisus spp. Whereas the male
dorsal abdominal gland secretion of P. nigrispinus
have been found to contain little (E)-2-hexenal or
linalool, each of these compounds were found to be a
major component of the male dorsal abdominal gland
secretion of P. Distinctus.
Piezodorus guildinii is a member of the stink bug
complex in soybeans that is economically important
pests in Brazil (Correa et al., 1996). Compounds used
by these bugs as alarm pheromones have been studied
(Paulo et al., 2000) by analysis of the male meta-
thoracic glands of adult bugs. It was reported previously
that methy l 2, 6, 10- trimethyl dodecanoate and methyl
2, 6, 10-trimethyltridecanoate are male-produced sex
pheromones in this species (Borges et al., 1999). Field
experiments were taken to determine the potential for
utilizing these compounds in an integrated pest
management program. Gland secretions of P. guildinii
showed seven peaks and comparison of these natural
products with those on the computerized mass spectra
data base, (E)-2-hexenal, (E)-2-octenal, nun decane,
n-dodecane, n-tridec-1-ene and n-tridecane, were
determined. DAG extracts of second-instar nymphs
of Euschistus heros contained four compounds, and one
of these had a MS consistent with the mass spectrum
data of the component. GC-MS co-injection of the
MTG extract of P. guildinii with a DAG extract of E.
heros showed that compound (E)-4- oxo-2-hexenal had
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the same retention time and mass spectrum of the
compound identified as (E)-4-oxo-2-hexenal. Com-
pounds in metathoracic glands of adults and dorsal
abdominal glands of nymphs of the stink bugs
Chlorochroa uhleri, C. sayi, and C. ligata (Hemiptera:
Pentatomidae) has been reported by Hsiao - Yung
HO and Jacelyn G. Miller (2001). The contents of
metathoracic glands of adults and dorsal abdominal
glands of nymphs of 3 Chlorochroa species, (C. sayi,
C. uhleri, and C. ligata) have also been analyzed.
Tridecane was the major component in the defensive
glands of both adults and nymphs. Other compounds
identified include (E)-2-hexenal, (E)-4-oxo-2-hexenal,
(E)-2-octenal, (E) -2-octenyl acetate, (E) -4-oxo-2-
octenal, (E)-2-decenal, undecane, dodecane, tetradecane,
and pentadecane.
Volatile compounds from the MTG, DAG, and
sternal setae of the generalist predatory stink bug
Eocanthecona furcellata (Wolff) have been studied
by gas chromatography - mass spectrometery (Ho et al.,
2003). MTGs of both male and female bugs have
shown to contain (E)-2-decenal as the major compo-
nent, with lesser amounts of (E, E)-2, 4-decadienal,
(E, Z)-2, 4-decadienal, and (E)-2, 9-decadienal. The
relative amount of (E)-2, 9-decadienal in the MTGs
of female bugs was found to be higher than in male
bugs. It was reported that there was no dimorphism in
the morphology of the DAGs of adults. However, the
DAG contents of adult bugs differ between the sexes.
Geraniol was found only in the DAGs of males, and
limonene and -terpineol were found only in the DAGs
of females, whereas linalool oxide isomers, linalool,
neral, and geranial were found in DAGs of both sexes.
The DAG contents of nymphs were also analyzed, with
4-oxo-(E)-2-hexenal, 4-oxo-(E)-2-octenal, tridecane,
and tetradecanal being major components. Male bugs
but not females possess sternal setae, and 6, 10, 13-
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trimethyltetradecyl isovalerate was detected from
extracts of the sternal setae of males.
Dorsal abdominal gland and metathoracic gland
contents of nymphs (10, 20, 30 days old) and adults
respectively (male and female), of the stink bug
Pallantia macunaima were verified by Fvaro et al.
(2011). The major component for nymphs has been
detected as tridecane, with lesser amounts of other
aliphatic hydrocarbons, aldehydes, oxo-alkenals and
esters. The five nymphal instars showed significant
differences in the proportions of the compounds
present, mainly between those of the first instar
compared to the dorsal abdominal glands components
of later instars. No significant differences were detected
in the proportion of metathoracic gland components
between the sexes but, between individuals of different
ages, (E)-2-hexenal and (E)-2-decenyl acetate signi-
ficantly decreased in adults from 10 to 20 days of age.
P. macunaima nymph spectral data revealed compounds
such as (E)-2 hexenal, (E) -2 octenal, undecane,
dodecane, (E) -2 decenal, 1 tridecene and tridecane.
Carpocoris fuscispinus is a cosmopolitan species
and feeds on Umbelliferae, Gramineae, and Fabaceae
(Hoberlandt, 1955). They are one of the most
destructive wheat pests in Turkey. C. fuscispinus is
found at low densities almost everywhere. If the
population levels grow in the host, they can become a
significant pest. In the MTGs of C. fuscispinus, 24
and 21 compounds were detected in females and
males, respectively. Most of the chemical compounds
were found to be qualitatively similar in each male
and female but differ in quantity. In the females of
C. fuscispinus, the following substances were found: 7
types of alkanes (cyclohexane, n-undecane, n-dodecane,
heptylcyclohexane, n-tridecane, n-tetradecane, and n-
pentadecane), 2 types of alkenes [(Z)-cyclodecene and
(Z)-9- tricosene], 4 types of aldehydes [(E)-2-hexanal,
(E)- 2-octenal, (E)-2-nonenal, and (E,Z)-2,6-nonadienal],
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Table - 1. Classification of pheromones reported so far in pentatomid bugs

Aldehydes Alkanes Alkenes Terpenes Esters Acids
2-Hexenal Undecane Z- cyclodecene (Z)-- Pentafluoropropio Methoxyacetic
bisabolene inic acid undecyl acid
ester
2-Octenal Dodecane Z (9) Tricosene Trans-1,2 bromoacetic acid (E)-2-octenyl
epoxides of decyl ester acetate
(Z)--
bisabolene
2-Decenal Tridecane N tridec-1-ene Cis1, 2 epoxides butyric acid (E)-2-hexenyl
of (Z)-- hexadecyl ester acetate
bisabolene
2,4-Decadienal Pentadecane Tridecene (E)-nerolidol Linoleic acid Methyl(2E,4C)-
ethyl ester decadienoate
E-2 hexenal Tetradecane Geranyl acetate 2,3dihydroxypop Methyl(2Z,4C)-
yl ester decadienoate
4 keto hexanal Cyclohexane Methoxyacetic Decanoic acid
acid tridecyl ester
(E)-2 decenal Heptylcyclohexane 2,3-dihydroxy- 11, octadecynoic
propyl ester acid
(E) 4-oxo-2 hexenal n- tetradecane n-hexadecanoic Pentafluoropropi
acid onic acid
E (Z) 2,4 decadienal dodecane 2,6,10 trimethyl
dodecanoate
E hexenal Nun- decane (E)-2-decenyl
acetate
Tetradecenal n-tetracosane Acetic acid undec
-2-enyl ester
(E) 4-oxo 2 decenal 11-octadecynoic
acid methyl ester
E,E-2-4 decadienal Z)-13-tetradecen-
1-ol acetate
(E) 2 nonenal

(E,Z) 2,6 nonadienal

6 types of esters (methoxyacetic acid tridecyl ester,
pentafluoropropionic acid undecyl ester., bromoacetic
acid decyl ester, butyric acid hexadecyl ester., linoleic
acid ethyl ester, and 2, 3-dihydroxypropyl ester), 2
types of acids [n-hexadecanoic acid and (Z,Z)- 9, 12-
octadecadienoic acid], and 3 types of alcohols (2-
cyclohexen-1-ol, 1-tridecanol, and octadecanol). In the
analysis of MTGs of females of C. fuscispinus,
n-tridecane (57.76%) was most abundant and bromo-
acetic acid decyl ester (0.04%) was less abundant. In
the males of C. fuscispinus, the following substances
have been found: 8 types of alkanes (cyclohexane,
n-undecane, n-dodecane, n-tridecane, n-tetradecane,
n-pentadecane, n-tetracosane, and n-octacosane), 1 type
of alkene [(Z)-cyclodecene], 3 types of aldehydes [(E)-
2-hexanal, (E)-2-octenal, and (E,Z)- 2,6-nonadienal],
5 types of esters (methoxyacetic acid tridecyl ester., 2,
3-dihydroxypropyl ester., acetic acid undec-2-enyl

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ester., 11-octadecynoic acid methyl ester, and (Z)-13-
tetradecen-1-ol acetate), 1 type of acid [(Z,Z)-9,12-
octadecadienoic acid], and 3 types of alcohols (2-
cyclohexen-1-ol, (E)-2-hexen-1-ol, and (E)-2-decen-1-
ol). In the analyses of MTGs of males of C. fuscispinus,
n-tridecane (49.26%) was most abundant and 2, 3-
dihydroxypropyl ester (0.06%) was least abundant
(Durak and Kalender, 2012).
From the above discussion, it is elucidated that
the following classes of compounds have been found
and characterized in pentatotomid bugs. Aldehydes
form the largest class of compounds found in
pheromone secretions followed by alkanes, esters acids
and lower amounts of alcohol (2-cyclohexen-1-ol, (E)-
2-hexen-1-ol, and (E)-2-decen-1-ol etc) (Table 1).
Conclussion
This review contains information on the
pheromone secreted by pentatomid bugs which is very
useful for Integrated Pest Management strategy.
Aldehydes from the largest class of compounds in the
pheromones secretions of pentatomid bugs.
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Corresponding Author : Ayesha Qamar, Department of Zoology, Aligarh Muslim University, Aligarh 202002, Email :
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