Review on bio-intensive management of African bollworm , Helicoverpa armigera ( Hub . ) : Botanicals and semiochemicals perspectives

African bollworm, Helicoverpa armigera (Hübner), is a serious pest of cereals, sorghum, cotton, pepper, maize, sunflower, flax and niger. To control this insect pest, doses of insecticides have been used. The use of indiscriminate synthetic insecticides causes adverse effect like environmental pollution, human and animal health hazards, and development of pesticide resistance. To alleviate these bottleneck problems, botanicals and semiochemicals are the effective controlling methods and believed to be safe to environment and human health. For many years, many plants species having pesticidal effects have been tested against the insect pest; however, some of them are commercially not produced. And also semiochemicals are the worthy tools, especially in the insect pest monitoring, aggregation and mating disruption of the pest. The manipulation of these management options need to get attention in the development of integrated pest management strategies. To do so, compiling information regarding the research so far done in the area is important. Therefore, this paper emphasized on the review of the research has been done concerning botanicals and semiochemicals to control H. armigera. Thus, in this review paper, different botanicals that affect the insect pest through their juvenile hormone and growth regulatory activity, antifeedant action, larvicidal action, ovipositional deterrence, ovicidal and pupicidal effects have been reviewed. Additionally, semiochemicals which include pheromones, kairomones and allomones of H. armigera were included.

crop to crop.For instance, in India, 29.93 to 31.28% yield loss was recorded on chickpea (Dinesh et al., 2017).In Ethiopia, estimated yield loss on chickpea ranged from 21 to 36% (Geletu and Million, 1996), on faba bean it ranged from 3.5 to 57.5% pod damage, while on field pea it ranged from 32 to 42% yield loss (Kemal and Tibebu, 1994).
Therefore, to control this polyphagous insect pest, growers are forced to use indiscriminate synthetic insecticides repetitively which leads to deleterious effects of pesticides on the environment, human and animal health and causes insecticide resistance development in some species.Hence, to minimize these problems, there is an urgent need for the development of environmentfriendly to suppress the pest population and effective monitoring method and thus making it less abundant and less damaging than it would be otherwise.More specifically, the major target of this review, botanicals and semiochemicals are one of the promising options in the management of the pest (Grechanova, 1986).Consequently, these management options play paramount role in developing an IPM which will be sustainable management of this insect pest.To do so, compiling information regarding the research so far done in the area is important.To date, organized information concerning botanicals and semiochemicals is not available.Therefore, the objective of this pepper is to review the research work carried out on botanicals and semiochemicals with particular emphasis on H. armigera and their role in agriculture.

Life cycle H. armigera
The female can lay several hundred eggs mainly at night on leaves, flowers, and pods.The oviposition period lasts for 5 to 24 days.The incubation period depends on temperature and varies from 2 to 5 days.Duration of larval development depends not only on the temperature, but also on the nature and quality of the host plants, for instance, 15.2 days on maize and 23.8 days on tomato.The number of larval instars varies from 5 to 7 and pupate in the soil.The pre-pupal period lasts from 1 to 4 days.In non-diapausing pupae, the pupal period ranges from about 6 days.The diapausing period for pupa may last several months.Pale colored adults are produced from pupae exposed to temperatures exceeding 30°C.In captivity, longevity varies from 1 to 23 days for males and 5 to 28 days for females (Zhudong et al., 2004).The total life time from egg to adult ranges from 23 to 34 days (Figure 1) Adverse weather conditions of winter and summer induce diapause in H. armigera.The winter diapause resulted from exposure of the larvae to short photoperiods and low temperatures (Ken and Kenji, 2002).For example, in Australia, H. armigera undergoes diapause during winters when the temperatures are low.
The other condition that causes diapause is exposure of larvae to very high temperatures (43°C for 8 h daily) during summer (Fitt and Cotter, 2005;Zalucki and Malcolm, 2002).

Host range and nature of damage
H. armigera is or pests of cotton, pigeon pea, chickpea, sunflower, tomato, maize, sorghum, pearl millet, okra, Phaseolus species, vegetables, tobacco, linseed, a number of fruits (Prunus, Citrus, etc.), and forest trees, grapevine, apple, strawberries, finger millet, etc. Adult female can lay several thousand eggs, so numbers can build up rapidly, often resulting in severe crop damage caused by the feeding caterpillars.The larvae cause severe damage to reproductive and vegetative tissues of agricultural and horticultural crops.Caterpillars could bore into flower buds, fruits, bolls or inflorescence (Yadav and Patel, 2015).

Behaviors of H. armigera
Like other insect pests, H. armigera has its own behaviors through its life cycle.These behaviors form a continuum throughout the life table of the insect behavior from mating to the location and selection of appropriate host plants by females and subsequent feeding activities of larvae.Therefore, those behaviors play great role in monitoring, forecasting and drawing effective management methods.

Mating behavior
The most known mating behavior of H. armigera is the response of male to female pheromons.Female of the insect pest produces pheromones and some volatile substances to attract males for the sake of mating (Hetan et al., 2017).Hence, in monitoring the insect pest, use the pheromones which are extracted from the females is and effective method.Studies of male responsiveness to pheromone have been conducted in the field and the number of males attracted was recorded (Blanco et al., 2010;Rothschild, 1978).

Host selection and oviposition
The host selection process of phytophagous insects is regarded as a catenary process or linked sequence of behaviors involving a series of behavioral responses by the female to cues from the plant or its environment.Presence of flowers, plant height and application of soil fertilizer positively influence host plant selection.Specifically, the presence of flowers greatly increased a plant's attractiveness to oviposition.(Firempong and Zalucki, 1989).The females' ability to locate and utilize wide ranging crops for laying eggs, the females ability to select an egg laying site on or close to the flowering fruiting structures of the crops and voracious feeding habit of larvae help the insect to adapt and cause severe damage to crop.Therefore, it is beneficial in the pest management strategies either to counteract or exploit by understanding all aspects of female oviposition and larval feeding behaviors.

Sensory receptors and electrophysiology
Adults and larvae of H. armigera perceive their environment via range of sensory receptors like olfactory and contact chemoreceptor on the antennae, ovipositor, tarsi and proboscis and mechanoreceptors on various parts of the body.Larvae of the insects also have gustatory organ located on the epipharynx which is used in distinguishing host from non host plants (Chapman, 1982;Stadler, 1984).

BOTANICALS IN THE MANAGEMENT OF H. ARMIGERA
Botanical insecticides are naturally occurring chemical extracted or derived from plants or minerals.Plants have their own defense mechanisms against insect attacks via repellents and even insecticidal effects.More than 2400 plant species around the world are known to posses' pest control properties.Using these plant species, about 2402 pests have been known to be controlled (Singh, 2000).In Ethiopia, about 30 plant species are recoded as pesticidal plant to control African bollworm (Tesfahun et al., 2000).Some of the promising pesticidal plants along with their known effects against H. armigera known in literature are shown in Table 1.
The common mode of action of plant extracts repels the insect pests, deters them from feeding and oviposition, disrupts the normal behavior and physiology of the insect and even toxic to the developmental stage and acting also as synergist in combination with other environmental friendly insecticides.

JUVENILE HORMONE AND GROWTH REGULATORY ACTIVITY
Juvenile hormone and growth regulatory properties play a great role in controlling of insect pests, especially H. armigera.Dashpande et al. (1998) indicated that acetone extracts of Catharanthus roseus at 100, 250, and 500 ppm concentration significantly reduced the larval weight of 2nd, 3rd, and 4th instars of H. armigera.This affects the development of larva to adult and thus resulted in decrease of the population of the insect.The metanolic leaf extracts of Persea indica is shown to have negative effects against H. armigera larvae (Gomez et al., 1992).On the other hand, Solsoloy and Rejesus (1993) observed the juvenile hormone from Pyschic nut; Jatropha curcas effects on this insect larva in diet mediated bioassay.Petroleum ether extract of weed Tribulus terrestris is also reported to affect adult emergence and larval mortality against late instars larvae of H. armigera (Gunasekaran et al., 1985).The crude ethanol extract of Algea elaeagnoidea, Algea odorata and Algea roxyburghiana actively inhibits the growth of H. armigera (Koul et al., 1997).

Antifeedant action
Antifeedant do not cause mortality of the insect directly, but lower their feeding potential and make them vulnerable to other mortality factors.An antifeedants are a behaviour-modifying substance that acts directly on the chemosensilla, thereby results in the feeding deterrence (Isman, 1994).
There are many antifeedants from plant species against H. armigera.Aqueous extracts from wild species of pigeon pea have significant antifeedant effect on H. armigera larvae (Shanower et al., 1997).In addition to this, acetate extracts seed of Trichilia havenensis gave antifeedant activity at 5000 ppm against 5th instars of the insect larvae.The mixture of havenensin-1,7-diacetate and havenesin-3,7-diacetate compounds fractionated by chromatography and showed the maximum antifeedant activity at 1000 ppm under choice and non choice feeding assays (Lopez et al., 1998).
Neem has diverse mechanism of biological effects on the insects, while antifeedant and growth retardant effects are the major important effects (Mohammed et al., 2004).Lulie and Raja (2012) obtained significantly lower pod damage using neem seed extracts in chickpea when compared with untreated plots.Some recommendations of neem based pesticides for H. armigera are listed in Table 2.
Apart from the extracts, essential oil owing volatile nature has also been evaluated for antifeedanty.Rao et al. (2000) reported that oil of Tagetes minuta gave the highest antifeedant activity (86.3) at 0.5% concentration on the second instars H. armigera larvae on cotton leaves.

Larvicidal action
Most of the studies on biological activity of plants have shown that early instars are the most susceptible stage to larvicidal activity of botanicals (Choi and Boo, 1989).This suggests the sensitivity of early instars larvae as target stages of pest for their possible application in pest management.
The methanolic extract of Malia azadrach stems at 7.5% concentration was observed to be larvicidal and ovicidal action against H. armigera (Rani et al., 1999).Sundararajan ( 2001) also evaluated the effect of leaf methanolic extract of Alstonia venenata, Ailanthus excels, Abutilan indicum, and Azima tetrachantha under laboratory conditions against H. armigera on tomato.A. venenata and A. tetrachantha gave up to 73 and 51% larval mortality, respectively.Neem product of RD-9 Replin (1 and 2%), Neemark (0.5 and 0.75%) and Neemarch 20EC (0.1 and 0.15%) have been tested against young larvae of the insect pest in cotton and resulted in mortality levels of 70, 70, and 66.7%, respectively (Dhawan and Simwat, 1995).Ankita and Sangeet (2017) tested Nigella sativa extract and it performed well against H. armigera causing 72.99% mortality.Manoharan and Uthamasany (1993) found that addition of Azadrachta indica oil to endosulfan and phosalone increased the mortality of the insect larvae by 16.7 and 25% as compared with insecticides alone.Babu et al. (2000) and Singh et al. (2013) reported that the synergistic effect of methanolic neem seed kernel extract is very effective in larval mortality and also delayed the metamorphosis of the pest.

SEMIOCHEMICALS
The term semiochemicals was proposed by Law and Regnier (1971), for chemicals converting signals between organisms.The chemicals under semiochemicals influence and regulate insect behavior and physiology.Dethier et al. (1960) classified the semiochemicals on the basis of the chemical stimuli and response as arrestants, locomatory stimulants, attractants, repellants, feeding, mating, ovipositional stimulants or deterrents.
There are two major groups of semiochemicals, the pheromone and allelochemicals.Pheromone affects intraspecifically the behavior and physiology of another individual of the same species, while the allelochemicals act interspecifically between members of different species.

Pheromones
Monitoring the population of a highly mobile and polyphagous pest like H. armigera requires holistic approach to the component of cropping system.Pheromones have the potential advantage of low mammalian toxicity, no development of pesticidal resistance and inexpensive method of control unlike that of conventional pesticides.Pheromones technology for H. armigera assists in pest population monitoring as well as in other methods including mass trapping, enhancing biocontrol impact, pesticidal resistance, monitoring and mating disruption (Mohammed et al., 2004).Z-11hexadecan-1-01 and Z-9-hexadecane-1-01 resulted in two to three-fold reductions in pesticides application (Zebtiz, 1997).
Pheromone dispensers are made up of rubber and cork septa found to catch more males than cigarette and filter pepper when loaded at a rate of 1 mg per septa than with lower concentrations (Krishna et al., 1998).The efficacy of funnel, sleeve and sticky traps was tested in the fields of Tikamgarh, in India (Rai et al., 2000).

Pest monitoring by pheromone
Sex pheromone traps have been widely used for decision making, intervention, using insecticides.Most of the research on the use of pheromone technology for trapping of H. armigera has so far been in China, India, Israel, New Zealand and Russia (Dunkelblum et al., 1980;Kehat and Dunkulbum, 1993;Parasad et al., 1993;Natarajan et al., 2002).Use of pheromones for monitoring H. armigera in tomato and maize field in Newzealand result in reduced crop in inspection time and more accurate timely insecticide application (Walker and Camegon, 1999).Short term forecast for 5 days could be worked out based on moth catches of H. armigera in Azerbaidzhan, USSR and time release of Tricogramma species against the pest.A total of 30 to 40 males of H. armigera trapped in 3 days were found to be reliable indicator of exceeding threshold level of 3 to 5 larvae/100 cotton plants in Tadzhik, USSR indicating the need for intervention measure (Grechanova, 1986).In addition to this, Reddy and Manjunatha (2000) suggested that integrated pest management should be initiated against H. armigera when 7 moths per trap per night are observed.In Ethiopia, on station monitoring of adults H. armigera as a key pest of cotton has been undertaken by pheromone trap at the cotton research center in Melka werer.The pheromone trap catch for 3 years indicated that higher Helicoverpa catches were observed in August and September and these catches were consistent with the field count of H. armigera eggs and larvae (Mohammed et al., 2004) (Figure 2).

ENHANCING OF BIOLOGICAL IMPACTS
Pheromone trapping for insect biological control agent is a valuable tool that can help to determine and improve parasitoids purpose.Sex pheromone of H. armigera was found to attract the eggs parasitoids, Trichogramma chilonis.Hosny (1988) reported that number of predators under pheromone treated cotton field is three times than that treated by insecticide under the same crop (Table 3).

Kairomones
These are natural chemicals present in plants or animal hosts that direct the insect pest towards the suitable site for feeding.Kairomones can be used mainly for two purposes: controlling the insect pests and for enhancing the performance of beneficial insects.As phytophagous insects use kairomone to locate and recognize host plants for feeding and oviposition, they can be used directly to disrupt the location and recognition of host plants, for mass trapping and indirectly for forecasting and monitoring pests (Singh, 2008).Additionally, the use of kairomone manipulates and enhances interaction of beneficial insects with their hosts or prey (Tamoghna and Nithya, 2017).The great potential utility at this time appears to be for aggregating natural parasitoids and predators in the targeted location.
Studies of parasitism rates of H. armigera eggs by T. chilonis in Petri dishes in response to different treatments of H. armigera by kairomones were made by Lewis et al. (1975).The results indicated that kairomonal compounds from H. armigera moth scales increased parasitization when applied over target sites.An analysis of H. armigera and Corcyra cephalonica moth scales for possible kairomonal substances using gas chromatography indicated the presence of hexatriacontane, nonacosane, docosane, pentacosane and heptadecane.The result strongly indicates the role of moth scale extracts in enhancing the parasitization rate of T. chilonis on H. armigera eggs.Laboratory observations on parasitism rates by T. chilonis in response to scale extract treatments reveal the importance of kairomones.

Allomones
These pheromones released by individuals of one species and influence the behavior of other species in  Source : Hosny (1988).
Allomones offer great potential as oviposition and feeding disruption and important to host plants as key mechanism of defense against phytophagous insects like H. armigera by employing the allomones in various ways for improving crop breeding program (Pickett, 1988) (Figure 2).

CONCLUSION AND RECOMMENDATIONS
To effectively manage any insect pest and prevent their further expansion, there is a need to study the detailed biological and ecological aspects of the insect populations.Before application of any control measure, complementary investigation of morphological, ecological, and biological aspects of the insect are desirable.Followup studies should be carried out on the distribution pattern and preferred host plants.Therefore, semiochemicals are an essential tool for monitoring and detecting the insect.There is seldom published information on sex pheromone composition against H. armigera.Therefore, effectiveness needs to be verified with different ratio combinations to increase the efficacy of sex pheromones.Different plant species that have insecticidal, antifeedant, repellent, and ovicidal effects have been evaluated against H. armigera.Therefore, from the base of their effectiveness and environmental friendly, more plant species need to be evaluated.In addition, the mechanism by which they cause mortality requires study to enable commercialization.Plant-insect interaction is an under researched area for this insect pests.

Figure 2 .
Figure 2. Monthly total catches of Helicoverpa armigera moths, egg and larvae Melka Wera, Ethiopia.(A) Catches of moths using pheromone traps.(B) Average number eggs and larvae (based on 400 cotton plants sampled).These figures illustrate that the peak moth catch during 1981/1982 was in June month, whereas during 1982/1983 and 2001 in August.The peak observed by pheromone trap of moths and eggs and larvae sampled from cotton plants shows that the pheromone trap is effective in monitoring H. armigera.

Table 2 .
Some recommendations of neem based pesticides for H. armigera management.

Table 3 .
Number of predator insects per hectare sampled by D-vac suction in cotton fields treated with pheromone compared with insecticide treated fields, Egypt.