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Indian Journal of Experimental Biology
Vol. 54, March 2016, pp. 163-174
Mini Review
Oviposition Deterrents in Herbivorous Insects and their potential use in
Integrated Pest Management
Archana Kumari* & Nutan Kaushik*
The Energy and Resources Institute (TERI), New Delhi-110 003, India
Received 21 July 2014; Revised 21 May 2015
In the life cycle of insects, oviposition is an important phenomenon, and it is influenced by many intrinsic and extrinsic
factors, especially in relation to suitable hosts for completion of their life-cycle. Oviposition deterrents which deter an
insect from laying eggs are important in the management of insect pests. Proper understanding of these deterrents shall
provide necessary insight into new vistas for Insect Pest Management. Chemicals from plants and insects play an important
role in attracting phytophagous insects for selecting host for oviposition. Considerable research has been done on
oviposition deterrents and their mode of actions. In the present review, we have consolidated the updated information on
this important aspect of insect behavior.
Keywords: Biological control, Host, Insect behavior, IPM, Pests
Overview and Perspective
Study of behavior of oviposition of insects and its
deterrence is one of the major aspects to understand
the ecology and evolution of interactions between
insects and plants. Various aspects related to
interactions between host plants and insects such as
the causes of the host specificity, host shifts,
sympatric speciation, co-evolution, etc., have been the
major subject of interest among the scientific
community. The discrimination by ovipositing female
insects often provide the initial basis for divergence of
insect populations onto different host plant species,
and it may drive the evolution of some plant defenses
and the origin of the host as well. Factors such as
communicative, genetic and ecological are known to
influence the oviposition behavior, preference for
plants and plant parts for oviposition in particular.
Oviposition behavior is that when a number of
potential host plants are available, a female will lay
maximum eggs on her most preferred plant species
(or habitat or part of plant), lesser number of eggs on
her next preferred plant, and so on1. Pheromones
operating oviposition activities in female insects have
been the point of attention in recent past by scientists
working on pheromones. For haematophagous adult
females finding and selection of a good site for egg
laying is a challenging task2. More so, as such insects
lack parental care and their decisions have far-
reaching consequences for their offspring. Selection
of oviposition site is influenced by pheromones,
which possibly will function either as deterrents or
stimulating substance in short range. These
pheromones may also act as insect repellents or
attractants in long range perception. For finding a
suitable site for oviposition or finding host for blood
feeding insects, they principally use olfactory and
visual cues. Different cues exploited by ovipositing
females influenced by varied arena such as habitat,
microbes, infusions and plant produced volatiles
besides egg and larva, influence the oviposition
behavior. Females of Pieris brassicae detect
conspecific eggs with the help of olfactory as well as
chemoreceptors3. The target insect pests can be
controlled and monitored by exploring the use of
pheromone in integrated pest management strategies.
Possible role of sex-peptides in oviposition has been
indicated by Singh & Singh in Drosophila sp.4.
In this review, we have focused on oviposition
deterrents from plants and insects which play an
important role in cues that inhibit oviposition, and
thus in the survival of phytophagous insects.
Behavioral sequence leading to oviposition
The gravid females follow certain sequence of
events culminating into oviposition. These include:
——————
*Correspondence:
Phone: +91 11 24682100; 24682111 Ext: 2519
Fax: +91 11 24682144; 24682145
E-mail: archanasrivastava08@gmail.com; kaushikn@teri.res.in
INDIAN J EXP BIOL, MARCH 2016
164
(i) searching, (ii) orientation, (iii) encounter, (iv)
landing, (v) surface evaluation, and (vi) acceptance5.
While searching, orientation and encounter together
form initial phase of the behavioral sequence,
landing, surface evaluation and acceptance or
rejection form the final phase. All the stages of the
host finding and acceptance sequence depend on a
wide variety of sensory cues. Most studies in this
area have focused on visual factors such as shape, size
and colour.
After alighting on a plant, surface perception, both
physical and chemical characteristics, gains
importance in determining the suitability for
oviposition6. The sensory receptors involved are
present on the tarsi, antennae, proboscis and
ovipositor of insects. They provide necessary inputs
to the central nervous system (CNS) which decides
finally whether to accept or reject the particular site
for oviposition. It involves balancing a number of
positive and negative signals from the plant, and often
the insect must respond to non-plant stimuli, such as
eggs, other insects, and pheromones. The outcome of
host evaluation behavior may depend to a large
extent on physiological factors such as age of the
female.
Oviposition deterrents/repellents
Oviposition deterrents/repellents are chemicals
which prevent insects from egg laying Oviposition
deterrence is common in many insects as an
evolutionary mechanism or tool to reduce/avoid
subsequent larval competition. Oviposition deterrents
can offer a first line of defense against insect pests.
Recently, Seenivasagan et al.7 have demonstrated the
influence of insect repellant DEPA on egg retention
and oviposition behavior of mosquito vectors viz.,
Aedes aegypti, A. albopictus, Anopheles stephensi and
Culex quinquefasciatus. Extracts of non-host plants
have been effective in protecting hitherto susceptible
hosts. A search for active plant constituents that
cause avoidance of egg-laying has led to discovery of
unacceptable plant species which are closely related
to preferred species. Recent studies have
demonstrated that acceptance or rejection of a
particular plant by the gravid females for oviposition
is regulated not only by the presence or absence of
oviposition stimulants but also by negative stimuli
evoked by the co-occurring deterrents.
Pheromones related to oviposition and premating
sexual behavior appear to originate from female
accessory glands or the Comstock-Kellogg glands8,9.
Pheromones convey messages to conspecifics. The
physiochemical properties of such pheromones fulfill
these requisites. Oviposition deterrent pheromones
promote even spatial distribution of eggs in many
insect species10 and remain active for days. Their
stability, evaporation and degradation vary
considerably among insects.
Oviposition deterrent cues
Ovipositing females generally utilize plant volatiles
as cues for orientation to host plants and the
subsequent surface evaluation of plants by means of
less or non-volatile secondary metabolites are usually
of great significance in host recognition. Cues from
competitive herbivorous insects may already be
released at the moment of egg-laying. Such
oviposition deterrents are known to inform both
conspecific females11 as well as individuals of other
species10,12. However, it is interesting to note that not
only the ovipositing females but also larvae that co-
occur with ovipositing females produce oviposition
deterrents13-15. Larvae are reported to contain
oviposition deterrents in their frass16, regurgitate or as
secretions of their exocrine glands17. Most
lepidopterons appear to be induced to oviposit in
response to a single host-specific compound.
Conspecific deterrence through visual and chemical
cues has been demonstrated for a large number of
insect species across several orders18. Changes in
plant chemistry or exposure of chemicals following
oviposition can also deter conspecific gravid females
and may be induced through plant damage or as a
response to the egg itself19. It is still not clear
whether the use of such plant derived cues by the
insect is an adaptive mechanism (i.e. the insect has
evolved to recognize these new plant signals as a cue
in order to avoid repeated oviposition) or simply an
effect (i.e. the ovipositing insect no longer recognizes
that host as a preferred oviposition site because of the
altered chemical profile of the plant).
Mechanism of deterrence
Oviposition deterrent plants or non-host plants
modify the insect oviposition behavior. Non-host
plant is a plant that the insect does not accept for
oviposition or for feeding, whereas the host plant is a
plant that the insect accepts for oviposition and for
feeding20. Species specific plant substances
inhibiting oviposition play a decisive role in
determining the host plant range of egg-laying
females. The availability of the host plant leads to
rejection of other possible hosts or non-hosts as
KUMARI & KAUSHIK: OVIPOSITION DETERRENTS IN HERBIVOROUS INSECTS
165
oviposition substrate even if they are suitable for
larval development. However, in the absence of the
host plant, less preferred host or sometimes non-hosts
which are insufficient for larval development, may
become the choice for oviposition. In such insects, the
oviposition seems to be directed by stimuli
appropriate only to the egg-laying process and
without any nutritive value of the host substrate for
the larva. Such findings support the idea that adults
lay eggs on fewer hosts than those which could serve
as adequate food source for larvae21.
The effect of most potent stimuli or complex
of stimuli inducing oviposition could be masked
by inhibitory substances (anti-oviposition) at an
appropriate concentration. This assumption has been
supported by the study on various insect species
which indicated that the egg-laying behavior can be
disturbed by the presence of various substances acting
as contact chemical inhibitors22. The non-host plant
has both a strong antibiosis (highly toxic to the
feeding insect) and a strong antixenosis
(unacceptable or repellent to the ovipositing insect).
Oviposition deterrents from Plants
The oviposition deterrent (OD) works as a signal
that lets the female know that the plant is toxic and
hence to avoid laying eggs on that plant (Table 1)23-34.
The extracts/preparations, usually from non-host
plants, influence the behaviour of insect pests and
Table 1—Oviposition deterrents from various plants
Plant source Target insect/
Order Level of
oviposition deterrence
Chemical(s)
identified Extract
Annona squamosa Corcyra cephalonica
Lepidoptera23 Significant - Methanol
Apium graveolens Chilo partellus
Lepidoptera24 - Thymol Essential oil compounds
Azadiracta indica Cacopsylla pyri
Hemiptera25 Promising - Neem oil
Callosobruchus chinensis
Coleoptera26 Significant - Oils
Corcyra cephalonica
Lepidoptera23 Significant - Methanol
Chrysanthemum
cineraraefolium C. chinensis
Coleoptera26 Significant - Oils
C. morifolium Plutella xylostella
Lepidoptera 27 Low
oviposition - -
Chrysanthemum sp. Trialeurodes vaporariorum
Hemiptera28 - - Water-
suspended pongam
oil
Clerodendrum
phlomidis Earias vittella
Lepidoptera29 100% Pectolinaringenin Chloroform extract
Cymbopogon citratus
Callosobruchus maculatus
Coleoptera30 100% - Essential oils
C. nardus Helicoverpa armigera
Lepidoptera31 53-66% - Citronella oil
Elettaria
cardamomum C. maculatus
Coleoptera32 - 1,8-cineol, α-terpinylacetate
,
terpi
nene and fenchyl
alcohol
Essential oil
Erysimum
cheiranthoides Pieris rapae
Lepidoptera33 Significant Erysimoside and
erychroside Butanol-
soluble from the
alcoholic extract of foliage
Gossypium hirsutum Cacopsylla pyri
Hemiptera 25 Promising cotton seed oil
Heliotropium
bacciferum C. maculatus
Coleoptera27 - - -
Milletia ferrnginea C. chinensis
Coleoptera26 Significant - Oils
Piper nigrum Corcyra cephalonica
Lepidoptera23 Significant - Methanol
Rhazya stricta C. maculatus
Coleoptera27 Low
oviposition - -
Ricinus communis Plutella xylostella
Lepidoptera34 - -
Plant extract (20%) and oil
emulsion (5% and10%),
Highest toxic ricin oil
INDIAN J EXP BIOL, MARCH 2016
166
their natural enemies. The natural resistance of
plants to herbivorous insects could be due to the
presence of specific metabolites that act as toxins or
as behavior-modifying agents.
Essential oils and volatile oil) that have strong
aromatic components give distinctive odour, flavour
and scent to plants. They help in attracting or
repelling insects, protecting the plants from extreme
heat or cold, and also act as defense material. These
are by-products of plant metabolism and are
commonly referred as volatile plant secondary
metabolites. Essential oil constituents are primarily
lipophilic compounds that act as toxins, feeding
deterrents and oviposition deterrents to a number of
insect pests. This natural resistance against
oviposition has great potential for insect pest
management of crops.
Crucifers and other plants in the order Caparales
have effective chemical defense that requires
the hydrolysis of glucosinolates by myrosinase
(β-thioglucoside glucohydrolase) leading to the
formation of breakdown products that deter
herbivores35,36. In contrast to general herbivores,
which have tendency to avoid glucosinolates,
crucifer-feeding specialists such as Pieris rapae and
others recognize glucosinolates and their breakdown
products as stimulants for feeding and egg-laying.
Glucosinolates such as 2-propenylglucosinolate and
2-phenylethylglucosinolate when applied to the leaves
of Vigna sinensis stimulate feeding by P. rapae
larvae37,38.
Oils have a repellent effect that discourages egg
deposition and feeding. The residual film may inhibit
insects from attaching to plant surfaces39. The
deterrent effect of oil residues on oviposition has been
reported in the citrus leaf miner Phyllocnistis citrella
Stainton (Lepidoptera: Gracillariidae)40,41, codling
moth Cydia pomonella (L.) (Lepidoptera:
Tortricidae)42, the pear Psylla Cacopsylla pyricola
Foërster and C. pyri (Hemiptera: Psyllidae), whiteflies
Bemisia tabaci(Hemiptera: Aleyrodidae)43-45 and
white apple leafhopper Typhlocube pomaria
(Hemiptera: Cicadellidae)46.
Deterrence in Lepidopteran insects
Lepidopteran (moths and butterflies) are the
second most diverse pest insect order after beetles
(Coleoptera). Setiawati et al. 201131 demonstrated that
4000 ppm of citronella oil from Cymbopogon nardus
reduced egg-laying by 53-66% in Helicoverpa armigera.
Even the ovicidal activity was concentration
dependent, and egg hatchability decreased by 15-95%
compared to control. The field application of
citronella oil significantly reduced fruit damage by
72% and increased quality of the chili pepper. This
study suggests that citronella oil has potential to be
incorporated into the controlling program of
H. armigera on chili pepper. H. armigera is reported
to oviposit more eggs on cotton wool compared to
pigeon pea leaves47.
Singh et al.24 who evaluated the influence of eight
essential oil compounds on oviposition and feeding
behavior of maize borer, Chilo partellus (Swinhoe)
revealed thymol to be the most active oviposition
deterrent compound. When the experiment was
performed in greenhouse the egg laying on maize
plants was inhibited significantly, 15 times more as
compared to the inhibition observed under laboratory
condition with the same concentration. Apparently,
though toxicity plays an important role in predicting
host plant choice, the behavioral response in terms of
oviposition preference is quite independent of toxic
action, particularly for non-host toxins. Therefore, the
same compounds affecting oviposition behavior on
one hand and having ovicidal or feeding deterrent
properties on the other could be useful in field
situations in any area-wide integrated pest
management model. Guerra et al.48 also reported that
essential oils of Minthostachys spicata and
Minthostachys glabrescens deterred the oviposition
and reduced the egg laying about 80% in potato tuber
moth Phthorimaea operculella. Tounou et al.34
reported oviposition deterrence, low rates of
oviposition, immature mortality, as well as relatively
low persistence of the toxic ricin oil. Different
treatments of Ricinus communis extract and oil
emulsion on mortality and oviposition behaviour of
Plutella xylostella in laboratory and field cage
experiments have revealed strong larvicidal and
oviposition deterrent index on in the field cage
experiments. The oviposition deterrence index was
highest with castor bean oil at a concentration of
10%. Diamondback females clearly discriminated
between plants sprayed with R. communis products
and those with water. Treatments of diamondback-
infested cabbage plants with plant extracts and oil
emulsions have resulted in more than 59% mortality
even after 7 days of application.
Methanol extracts of 18 plants of 13 families
evaluated for their effects on the oviposition and
larval mortality against Corcyra cephalonica showed
KUMARI & KAUSHIK: OVIPOSITION DETERRENTS IN HERBIVOROUS INSECTS
167
significant variations in toxicity and oviposition
deterrence when compared with the control. Among
the 18 plants evaluated, leaf and seed extracts of
Azadiracta indica and the seed extract of Piper
nigrum were the most effective causing 100% larval
mortality. This was followed by leaf (81%) and seed
(84%) extracts of Annona squamosa. Maximum
ovipostion deterrence was observed with P. nigrum
followed by A. indica and A. squamosa. None of the
plant extracts showed any adverse effect on the
viability of maize seeds23.
The effects of extracts of Chrysanthemum
morifolium, a non-host plant of the diamondback
moth, Plutella xylostella on the olfactory and
oviposition responses of this phytophagous insect
and on the levels of parasitism by its specialist
parasitoid Cotesia plutellae (Kurdjumov) were
examined, using Brassica campestris L. subsp.
pekinensis (Chinese cabbage) as the test host plant
by Liu et al.27. Olfactometer tests revealed that
volatiles of Chrysanthemum extract-treated host
plants were less attractive to P. xylostella females
than those from untreated host plants; and
interestingly, volatiles of the Chrysanthemum
extract-treated host plants were more attractive to
females of its parasitoid Cotesia plutellae than those
from untreated ones. Oviposition preference tests
revealed that P. xylostella females laid only a small
proportion of eggs on host plants treated with
chrysanthemum extract, while ovipositing parasitoid
females parasitized a much higher proportion of
host larvae feeding on the treated host plants than
on untreated ones. This supports the view that
certain non-host plant compounds, when applied to a
host plant, are likely to render the plant less
attractive to a phytophagous insect and more
attractive to its parasitoids. Utility of such non-host
plant compounds can be explored to develop push-
pull systems to reduce oviposition by a pest insect
and at the same time enhance parasitism by its
parasitoids in crops.
Erysimum cheiranthoides is a crucifer species
which is generally avoided by the crucifer pest,
Pieris rapae. The deterrent compound has been
isolated in n-butanol-soluble from the alcoholic
extract of its leaves. The active fraction contained
three cardiac glycosides, which were isolated by silica
gel column chromatography and reversed-phase
HPLC. Chemical and spectral evidences led to
characterization of these compounds as Erysimoside,
Erychroside and Erycordin. Erysimoside and
Erychroside were strongly deterrent to P. rapae, but
Erycordin was inactive. Both active compounds have
the same aglycone, strophanthidin and the inner sugar
in both compounds is a 2,6-dideoxy hexose to which
the outer sugar is attached at C-4 position. It is quite
possible that these structural features, which are not
present in the inactive compound Erycordin, may
represent specific requirements for oviposition
deterrent activity33. Recently, oviposition deterrent
activity of Clerodendrum phlomidis was evaluated
against Earias vittella by Muthu et al.29. They have
isolated Pectolinaringenin [5,7-dihydroxy-4′,6-
dimethoxy-flavone (C17H14O6)], a flavonoid
compound from chloroform extract of the plant and
found that the isolated compound exhibited 100%
deterrent activity at 100 ppm concentration against
E. vittella.
Avoidance of those plants which release herbivore-
induced volatiles in relation to oviposition has been
reported in some Lepidopteran species. Anderson &
Alborn49 reported that females of Spodoptera
littoralis choose to lay eggs on undamaged plants of
cotton, in two-choice test with damaged plants. The
females could discriminate between damaged and
undamaged cotton plants up to 10 days after the
termination of herbivory revealing how the induced
defense affects the oviposition pattern in such
insects. Herbivory by S. littoralis larvae induce
changes in female decision of oviposition on cotton
plants. The decision of the gravid female on number
of eggs to lay/oviposit appears to be controlled at two
levels. According to Svensson50, S. littoralis can
control both the number of egg batches as well as the
number of eggs per batch in their choice between
different oviposition places.
European grapevine moth females (Lobesia
botrana), select an oviposition site by tasting the host
plant surface and then gluing a single egg on berries
from grapes or from several other host plant species.
When 20-hydroxyecdysone (20E) from Leuzea
carthamoides were tested against larvae and adults of
European grapevine moth, the larvae avoided feeding
while the adults avoided egg laying on the treated
surface of 20-hydroxyecdysone, at a threshold of
8 ng/cm2 51. Microbial biopesticides which have
already made a place in the field of insect pest
management as an alternative of synthetic pesticides
to control the economically important lepidopteran
insect pest Helicoverpa armigera has been found to
INDIAN J EXP BIOL, MARCH 2016
168
deter oviposition also. The treatment of HD-1 besides
severally affecting the growth & development
adversely affected the oviposition of H. armigera,
S. litura and S. littoralis52-54 suggesting the possible
role of HD-1 in oviposition deterrence.
Deterrence in Coleopteran insects
Beetles are the largest group with more
than 300000 species. About 50% of all insect
species, 30% of all animal species and 24 % of all
organisms are beetles. They cause significant
damage to stored grains and pulses. Plant essential
oils have potential as products for control of stored
product pests because some of them are selective and
have little or no harmful effects on non-target
organisms55. Abbasipour et al.32 reported that essential
oil from cardamom, Elettaria cardamomum (L.)
(Maton) is toxic to the bruchid beetle, Callosobruchus
maculatus Fabricius and it has good efficacy on
oviposition deterrence against C. maculatus females
too. The major chemical constituents of cardamom
were identified as α-terpinyl acetate, terpinene,
1,8-cineol, and fenchyl alcohol. In another study,
essential oils extracted from five plant materials
showed a significant inhibition of oviposition and
F1 adult emergence compared to the control during
no-choice tests cowpea bruchid, Callosobruchus
maculatus on cowpea seeds32.
Cymbopogon citratus and C. nardus showed
higher effect on oviposition and F1 adult emergence
on C. maculatus than the essential oils of Alpinia
calcarata, Cinnamomum zeylanicum and Murraya
koinigii. In the choice test, the percentage ovipositions
in all oils treated samples were significantly lower
than that of the control and ethanol treated samples.
The percentage eggs deposited decreased with
increasing doses of the oils ranging 10-160 mg. The
percentage of eggs laid was zero in samples treated
with 40 mg of C. nardus or A. calcarata, 80 mg of
C. citratus and 160 mg of C. zeylanicum. The
essential oils of M. koinigii showed the lowest effect
on oviposition when compared to other four essential
oils30. Elhag55 tested 9 plant extracts in choice and no-
choice tests as oviposition deterrents against cowpea
bruchid, Callosobruchus maculatus on chickpea,
Cicer arietinum. Seed treatment with crude extract of
materials (0.1%) resulted in a significant reduction in
ovipositional preference of the bruchid. The
maximum repellency was found in Rhazya stricta
leaves (82%), followed by Azadirachta indica seeds
(76.8%), Heliotropium bacciferum aerial parts
(59.2%) and citrus peels (58.6%). Progeny production
was significantly reduced. Only 11.5, 11.9, 12.4, 13.4
and 14.8% of the eggs deposited matured to adult in
R. stricta, A. indica seeds, Piper nigrum, citrus peels
and H. bacciferum, respectively. Notably, F1 females
laid significantly fewer eggs in response to
R. stricta, neem seeds, H. bacciferum, citrus peels and
P. nigrum. Percentage reduction in F2 progeny ranged
between 71.4% with R. stricta-treated seeds and
24.5% in the P. nigrum treatment.
The oviposition-deterrent and toxic effects of
seven plant species with known biological effects
were tested by Mulatu & Gebremedhin26 against the
Adzuki bean beetle, Callosobruchus chinensis on
stored fava bean seeds for two years. Oils of
Chrysanthemum cinerarae folium, Azadirachta
indica, and Milletia ferrnginea were the most
effective in partially or completely preventing
oviposition and no bruchids emerged from the few
eggs laid. Whereas in case of Eucalyptus globulus
seed powder treatment caused the death of only
emerging adult beetles.
Jayakumar56 who studied oviposition deterrence of
aqueous extracts of Acorus calamus root (Acoraceae),
Artemisia nilagirica (Asteraceae), Cassia auriculata
(Fabaceae), Cassia siamia (Caesalpiniaceae),
Citrusaurantium peel (Rutaceae) and Percularia
daemia (Asclepiadaceae) in Callsobruchus maculatus
revealed that maximum oviposition deterrent activity
was shown by C. siamia (84.66%) followed by
C. aurantium peel (82.11%) at higher concentration.
Even at lower concentration (1.25%), these two
extracts showed >50% oviposition deterrent activity.
Oviposition deterrence in Hemipteran insects
Many Hemipterans, mainly aphids and scale
insects, are important pests of crops and gardens.
Researchers have demonstrated the repellent activities,
including host deterrence and anti-oviposition, of pongam
oil against the adults of the common greenhouse whitefly
(Hemiptera) Trialeurodes vaporariorum Westwood in
greenhouses. Chrysanthemum plants treated with
different concentrations (0.5%-2.0%) of water-
suspended pongam oil showed relatively long lasting
host deterrent and anti-oviposition effects on the
adults of greenhouse whitefly. However, the repellent
effect declined according to concentration and time.
Strong effects were evident depending up on
concentration even after 12 days of application28.
Oviposition deterrents have great potential to prevent
insect infestations. The level and duration of this
KUMARI & KAUSHIK: OVIPOSITION DETERRENTS IN HERBIVOROUS INSECTS
169
behavioral effect was evaluated by Erler25 against
pear psylla, Cacopsylla pyri (L.), a serious pest of
pears in Turkey. The activity of four oily substances
(cotton seed oil, neem oil, summer oil and fish-liver
oil) was evaluated against winter and summer forms
females of the pest in the laboratory and in the field
experiments to determine their oviposition deterrence
and stability as deterrents. In the laboratory assays,
the initial (3 days after treatments) deterrence of all
test materials was 100%. While decrease in initial
deterrency started after 1 wk for neem oil and after
2 wk for cotton seed oil. Summer oil and fish-liver oil
exhibited 100% deterrent activity against winter
forms, but not against summer forms during the 3 wk
test period. Fish liver oil and summer oil exhibited
strong oviposition deterrent activity for both forms of
C. pyri females in field trials. A significant reduction
in the total number of eggs laid was observed in the
field plots. Summer oil and fish-liver oil appeared to
be the most promising oviposition deterrents against
pear psylla females.
Pheromones and related volatiles from insects
Pheromone communication involves release of
specific chemicals from a pheromone producer
(emitter), the environmental transmission of these
chemicals to a receiver, followed by processing of
these chemicals to mediate appropriate behavioural
responses in the receiver57. Nufio & Papaj11 outlined
the kinds of evidence used to document the existence
of oviposition deterring pheromones and their
significance. Agboka et al.58 have reported that
chemical signals play a major role in host selection.
Both parasitic and phytophagous insects are known to
deposit chemical signals following egg laying that
modify the behaviour of conspecifics who
subsequently avoid depositing future eggs into
previously utilized host resources. These signals
have been termed oviposition deterring pheromones,
marking pheromones, or epideictic pheromones10,11,59,60.
It is believed that these signals have evolved under the
selection pressures of limited host resources for brood
development and notify the receiver of a previously
exploited, sub-optimal resource, thus reducing
competition among the offspring’s10. A large number of
studies have been conducted on evaluation and
effectiveness of pheromones (Table 2)61-64. Scientists
have observed that gravid females avoid previously-
marked host resources vs. unmarked controls. They
have also distinguished the behavioural effect of the
oviposition-deterring pheromones from other potential
stimuli associated with oviposition such as eggs or fecal
matter. Work has also been done on identification and
synthesis of putative pheromones and the comparison of
the effects of the synthetic vs. naturally-deposited
compounds There are also reports of stereotypical
behaviours of females immediately following the
oviposition event such as dragging the ovipositor on the
host resource while depositing a clear liquid.
Deterrence in Lepidopteran insects
Gomaa63 has reported that coating of Nerium
oleander leaves with aqueous egg-wash from
Spodoptera littoralis egg-masses deterred the mated
conspecific female moths from ovipositing their eggs
on treated leaves. This also caused decrease in the
total number of deposited eggs per female during the
moth's life span. Aqueous and solvent extracts of egg
masses laid by mated S. littoralis females were
prepared and evaluated against S. litura. The highest
deterrent effect on conspecific female was obtained in
petroleum ether or ethanol egg-wash extracts. The
effects of the tested egg-wash extracts was
concentration dependent as an increase in the
concentration of any extract caused a decrease in the
number of deposited egg-masses.
Table 2—Oviposition deterrent pheromones from insects
Pheromone source
Target insect identified/
Order of insect Oviposition deterrent activity Extracts
Conspecific larvae61
Adalia bipunctata Coleoptera Deterrence in young and naïve females 82 %t -
Coccinella
septempunctata62 Menochilus sexmaculatus
Coleoptera Density dependent inhibition -
C. transversalis62 M. sexmaculatus Density dependent inhibition -
Propylea dissecta62
M. sexmaculatus Density dependent inhibition -
Spodoptera
littoralis63 mated conspecific female
Lepidoptera Highest in petroleum and ethanol extracts Petroleum Ether, ethanol and
Ringer's solution extract
Lasioderma
serricorne (F.)64 Conspecific Females
Coleoptera - Saline, methanol acetone and
hexane
INDIAN J EXP BIOL, MARCH 2016
170
Deterrence in Coleopteran insects
Experiments by Frechette et al.61 showed that the
two-spot ladybird beetle Adalia bipunctata (L.) was
reluctant to lay eggs in a patch of prey contaminated
by the oviposition-deterring pheromone produced
by conspecific larvae. An experiment was conducted
to test whether the internal state of an A. bipunctata
female in any way affects its oviposition response
to oviposition-deterring pheromone. First of all,
the oviposition response to oviposition-deterring
pheromone of young and old females was compared.
Then, the oviposition response to oviposition-
deterring pheromone of females previously exposed
continuously to oviposition-deterring pheromone
was compared with that of females of the same
age but with no previous experience of oviposition-
deterring pheromone. Old females and females
with previous experience of oviposition-deterring
pheromone were less reluctant to lay eggs in the
presence of oviposition-deterring pheromone than
young and naive females. These findings are in
agreement with the predictions of optimal foraging
theory.
Howlader & Ambadkar64 studied the effect of
ovipositional deterrency of whole body wash of
tobacco beetle Lasioderma serricorne (F.) against the
conspecific females. Different solvents were used for
the body washings. All the body washes reduced egg
laying in the treated samples more than those of their
controls. Among all tested solvents, Hexane wash was
most effective (about 82% deterrence). Bioassay
established a clear relationship between the
concentration (female equivalents) of the hexane
extract and the deterrence of oviposition.
Oviposition deterrent pheromone in conspecific
and their role in deterrence have been well reported in
coleopteran insects but study of sensitivity of
heterospecific has not yet on tracks. Mishra et al.62
have disclosed the oviposition deterrent behavior of
Menochilus sexmaculatus due to the presence of
heterospecific life stages and their semiochemicals.
They have reported that presence of all life stages of
heterospecific inhibits the oviposition of the insect.
Frass of larvae as oviposition deterrents
The fine powdery material released by plant-eating
(phytophagous) insects as waste after digesting plant
parts are used to convey the information about their
earlier or actual presence. When individual females
were provided simultaneously with a pine bolt applied
with methanol extract of larval frass and another bolt
applied with methanol alone, significantly less eggs
were deposited on methanol extract of larval frass
applied bolts for 24 h. A number of insects have been
reported to be deterred from oviposition by larval frass
of phytophagous insects due to some non-volatile
compounds released from these frass (Table 3)65-71.
Table 3—Oviposition deterrents from Lepidopteron frass
Frass source activity Target insect Oviposition deterrent Chemical identified Extracts
Helicoverpa armigera H. armigera65 - Palmitic & Oleic acid Water & Hexane
Monochamus alternatus (Larvae) M. alternatus66 Low
oviposition - -
Ostrinia nubilalis (Larvae) O. nubilalis67 Activity
up to 72 h. - Methanol
O. zealis (Larvae) O. furnacalis68 Significant
Mix. of palmitic, stearic,
oleic, linoleic, and
linolenicoleic acids
Acetone
O. zealis (Larvae) O. latipennis68 Significant -do- -do-
O. zealis (Larvae) O. scapulalis68 Significant -do- -do-
O. zealis (Larvae) O. zealis68 Significant -do- -do-
Spodoptera littoralis (Larvae) S. littoralis69 100 % deterrence in
S. littoralis Phenols & flavonoids Distilled water
S. littorali (Larvae) Agrotis ipsilon69 -do- -do-
S. littoralis &
Agrotis ipsilon S. littoralis70 Deterrent Fatty acids Ethanolic extracts
S. littoralis &
Agrotis ipsilon A. ipsilon70 Deterrent -do- -do-
S. littoralis (Larvae) S. littoralis71 -
Benzaldehyde, Eugenol,
Nerolodol, etc.
(15 compounds)
-
KUMARI & KAUSHIK: OVIPOSITION DETERRENTS IN HERBIVOROUS INSECTS
171
Deterrence in Lepidopteran insects
Oviposition deterrent activity of Spodoptera littoralis
larval frass have been evaluated by Hashem et al.69.
Aqueous extract of frass of different larval stages of
S. littoralis was effective against S. littoralis and Agrotis
ipsilon. Extract of L6 frass completely inhibited
oviposition in S. littoralis adult and very less number of
eggs was laid by A. ipsilon adult (11.8 eggs/female)
when compared with control (1026.0 and
848.2 eggs/female, respectively). Ethanolic extracts of
larval frass of the cotton leaf worm and the black
cutworm were evaluated for oviposition deterrent
activity and the extracts were identified using gas
chromatography-mass spectrometry. Ahmed et al.70
have reported dose dependent deterrent activity of
the same and extracts of larvae reared on artificial
diet was comparatively more effective than the larvae
reared on natural food. A number of fatty acids were
isolated and identified in the larval frass of both the
insects but except palmitic acid nature and quantity of
other fatty acids mainly depends upon the larval stage
and source of food. According to Williams et al.72 adult
of Spodoptera frugiperda (Polyphagous) is prevented
from oviposition after its contact with frass of larvae
when the larvae have been fed with leaves of maize.
Similarly, a methanol-soluble oviposition deterrent
extract was reported by Dittrick et al.67 in the frass of
fifth-instar larvae of Ostrinia nubilalis, the European
corn borer. Bioassays established a significant linear
relationship between reduction in oviposition and
concentration of extract applied on the oviposition
substratum. Under the laboratory condition the deterrent
activity was persisted for 72 h when exposed to air,
indicating a low volatility of the extract. Guoqing &
Ishikawa68 have reported that volatile oviposition-
deterring chemicals were present in larval frass of
Ostrinia zealis, Ostrinia. latipennis, Ostrinia. furnacalis
and Ostrinia. scapulalis. These volatile chemicals were
extractable with acetone, and could be partitioned into a
polar lipid fraction. This fraction mainly contained
stearic palmitic, oleic, linoleic and linolenic acids.
Among the four Ostrinia species no significant
differences were found in the amount and composition
of these free fatty acids. They also observed that a
mixture of the 5 authentic fatty acids of the composition
found in the larval frass of O. zealis caused significant
oviposition-deterring effects on all four species of
Ostrinia. Oviposition of Spodoptera littoralis was
strongly deterred by a mixture of 6 compounds,
benzaldehyde and 5 terpenes: carvacrol, eugenol,
nerolidol, phytol and thymol, isolated from conspecific
larval frass. It was observed that if one of the
compounds was excluded from the mixture, the
deterrent effect was lost.
An electroantennogram-screening was performed
on 15 compounds identified from the larval frass. Of
these behaviourally active compounds, dose-response
relationships were obtained for benzaldehyde,
eugenol and nerolidol and seven types of receptor
cells specifically tuned to compounds from the larval
frass which were also identified by single-sensillum
recordings from olfactory sensilla on the female
antenna. The most abundant of these was a receptor
cell type responding equally well to the 3 aromatic
terpenes: carvacrol, eugenol and thymol. Receptor
cells responding to only a single terpene were found
for carvacrol, eugenol, nerolidol and phytol. Besides
these receptor cells responding to other frass
compounds, green leaf odours and sex pheromone
components were also found. No receptor cell
responding to benzaldehyde was identified16.
Oviposition deterrents in the frass of cotton
bollworm, Helicoverpa armigera were investigated
by Haiyan et al.65 by behavioral bioassays and
electroantennography analyses. It was found that a
water suspension or a hexane extract of the frass in
comparison to the corresponding foods, deterred
oviposition of conspecifics significantly. When
hexane extracts of the frass were further partitioned
into polar and neutral lipid fractions, two polar
fractions obtained thus significantly reduced
oviposition. The polar lipid fractions contained
several fatty acids including palmitic acid and oleic
acid as the main component at the ratio nearly 1:1.
Anbutsu & Togashi66 determined the effect of
larval frass of Monochamus alternatus on oviposition
preference of the female adults. Individual females
were provided with a frass-coated, Pinus densiflora
bolt and an untreated bolt simultaneously and were
allowed to oviposit for 24 h. The females supplied
with frass-coated bolts deposited no eggs on them,
which indicated that the larval frass deterred the
females from egg-laying. When individual females
were provided simultaneously with a pine bolt applied
with a methanol extract of larval frass and another
bolt applied with methanol alone, significantly
smaller number of eggs were deposited on methanol
extract of larval frass applied bolts for 24 h. These
results were indicative of presence of a putative
oviposition deterrent in larval frass of M. alternatus.
INDIAN J EXP BIOL, MARCH 2016
172
Conclusion
Non-host plant extracts and preparations,
pheromones and larval frass have been found to
influence oviposition behaviour of insect pests and
their natural enemies. Certain non-host plant
compounds, when applied to a host plant, are likely to
render the plant less attractive to a phytophagous
insect and more attractive to its parasitoids. Utility of
such non-host plant compounds can be explored to
develop push-pull systems to reduce oviposition by a
pest insect and at the same time enhance parasitism by
its parasitoids in crops. There are several reports
about oils derived from plants also having a repellent
effect that discourages egg deposition and feeding.
Both parasitic and phytophagous insects are known to
deposit chemical signals following egg laying that
modify the behaviour of conspecifics who
subsequently avoid depositing future eggs into
previously utilized host resources. These signals
called oviposition-deterring pheromones, marking
pheromones, or epideictic pheromones are important
aspects of oviposition behavior of insects and require
more elaborate studies. Role of frass of phytophagous
larves may also be considered while searching for a
viable oviposition deterrent, as a number of insects
have been reported to be deterred from oviposition by
larval frass of phytophagous insects due to some
non-volatile compounds released from these frass.
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