Eggplant, Solanum melongena L. (Solanales: Solanaceae), is an important vegetable crop in Southeast Asia. It was cultivated on 18.53 lakh ha (1,853,000 ha) with a production of 48,424,295 tonnes worldwide during 2012 (FAO 2014). Numerous insect pests infest eggplant, among them the fruit borer Leucinodes orbonalis Guenée (Lepidoptera: Crambidae) and sucking pests like the leafhopper Amrasca biguttula biguttula (Ishida) (Hemiptera: Cicadellidae) and the whitefly Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae), cause major damage in the Indo-Gangetic Plain region of India (Bhadauria et al. 1999). Synthetic broad-spectrum insecticides have been used by farmers to manage the insect menace in India (Alam et al. 2006) and Bangladesh (Rashid et al. 2003). Repeated insecticidal sprays resulted in the development of resistance in L. orbonalis to organophosphate and synthetic pyrethroids (Ali 1994; Alam et al. 2003; Botre et al. 2014), besides also resulting in residue on the produce, and in resurgence of non-target insect pests. To manage insect pests in an eco-friendly manner, a pest-suppressive agro-ecosystem has to be considered. A pest-suppressive agro-ecosystem can be designed by identifying a suitable intercrop having insect pest deterrence, and a border crop enhancing natural enemy activity by acting as a refugium (Landis et al. 2000). Since 300 B.C., intercropping has been practiced in Greece, which indicates that polyculture or intercropping is a traditional farming practice (Papanastasis et al. 2004). In India, the impact of intercropping on major insect pests and beneficial insects was studied in a wide range of crops including pulses (Prasad et al. 1987; Prasad et al. 1988; Mehto et al. 1988; Sekhar et al. 1997), cereals and oil seeds (Singh et al. 1991a,b) from the mid 1970s to early 1990s. Practicing multi cropping on a farm increases the vegetation and insect diversity compared with practicing monoculture. The continuous supply of floral rewards and alternate food sources for the natural enemies helps to increase their abundance, diversity and conservation. Herbivorous insect pests of eggplant may be less able to discern and respond to the odors of their host when additional non-host plants in the form of intercrop or border crop are present (Andow 1991). Chemicals from the intercrop exert an odor-masking effect on the insect seeking its host (Bernays & Chapman 1994), ultimately resulting in lower incidence of insect pests in the main crop. Thus, habitat management can be effectively integrated with biointensive integrated pest management (IPM) packages. Hence, in the present study, the suitability of 3 intercrops and 2 border crops was evaluated for the management of 3 major insect pests on eggplant in India.

Materials and Methods

Seeds of the eggplant cultivar ‘Pusa Kranti’ were sown in a raisedbed nursery during Jun 2010 and Jun 2011 with the onset on the monsoon season in India. Thirty day old healthy seedlings free from mechanical damage were chosen for planting on the experimental farm at the Division of Entomology, Indian Agricultural Research Institute, New Delhi 28.08 °N and 77.12 °E. The ratio of fertilizer (N:P:K) applied to the experimental field was 100:80:60/ha. Nitrogen was applied in 2 split doses, 50 per cent at field preparation before transplanting and 50 per cent at flowering to raise a healthy crop. Whenever soil moisture in the field was deficient, it was restored by flood irrigation. Five hand hoeings were done for managing the weeds.

OBSERVATIONS ON INSECT POPULATIONS AND YIELDS

In each treatment, 5 plants were selected randomly and tagged for weekly monitoring and recording of the insect pest and natural enemy populations. Weekly observations on the numbers of leafhoppers (A. biguttulla bigutulla) (32nd Standard Meteorological Week [SMW] to 41st SMW; i.e., 06-12-Aug to 08-14 Oct) were recorded from a leaf from the top, middle and bottom of each plant. Similar sampling methodology was followed for recording the white fly (Bemisia tabaci) population from 32nd SMW to 41st SMW (06-12-Aug to 08-14 Oct). The numbers of coccinellid beetles present on those 5 tagged plants in each plot were recorded from the 32nd SMW to 41st SMW. Egg plant fruits were harvested regularly every 8-9th day commencing from the first harvest i.e., 75 days after transplanting. The healthy and damaged fruits were sorted out by visual examination, and percentage fruit infestation both by number and weight of fruits were calculated for each treatment.

After 55–60 days of transplanting, the numbers of natural enemies present in eggplant in each treatment were recorded visually and the insects were collected for identification. The numbers of individuals per species and numbers of individuals of all species in different treatments were used for diversity analysis through the Shannon-Wiener index. This index combines species richness and evenness in a habitat and was described by Shannon (1948). It is calculated by using the equation

where P_i = n/N (n = number of individuals of a species; N = number of individuals in each treatment) and ln = the natural logarithm.

Generally, for a sample size with more than 5 species, the index will range from 0 to 4.5 (Shannon 1948). A value near zero indicates that the treatment was dominated by a single species, and a value near 4.5 indicates that the number of individuals was distributed evenly overall the species.

Results

EFFECT OF BORDER CROPS AND INTERCROPS ON INCIDENCE OF NATURAL ENEMY (COCCINELLIDS)

From the 1st week Aug to the 2nd week of Oct, treatment T1 (maize as border crop and coriander as intercrop) harbored significantly higher numbers of coccinellids than T7 (sole crop) during 2010 and 2011(Table 1). The mean numbers of coccinellids during the 10 week observation period revealed that the largest population was recorded in T1 (1.25 cocinellids per plant) followed by T3 (1.00) > T5 (0.78) > T2 (0.67) > T4 (0.61) > T6 (0.55) > T7 (0.37). Thus, the smallest coccinellid population was recorded in the sole crop control.

The treatments with maize as border crop had more natural enemies than those with cowpea as border crop (Table 3, Table 4). Maize as a border crop attracted many unique natural enemies like Paederus sp. (Coleoptera: Staphylinidae), Chrysoperla zastrowi (Esben-Petersen) (Neuroptera: Chrysopidae), Eristalis sp. (Diptera: Syrphidae) and Brachymeria sp. (Hymenoptera: Chalcididae), apart from Cheilomenes sexmaculata (F.) (Coleoptera: Coccinellidae) and other ladybird beetles.

The Shannon-Wiener index for natural enemies present in different treatments varied from 2.356 to 1.171 and 2.462 to 1.241 in the years 2010 and 2011, respectively (Table 4). The highest index was recorded in treatment T1 followed by T3 > T5 > T2 > T4 > T6 during both years. Thus, coriander as intercrop and maize as border crop with eggplant had the highest diversity index. The lowest index was obtained in the sole crop control; all of the intercropped treatments had a higher index than the sole crop control.

Table 1.

Effect of intercrops and border crops on incidences of the leaf hopper, A. bigutula biguttula, the whitefly, B. tabaci and the coccinellid predators on eggplant (brinjal) during kharif (monsoon season) of 2010 and 2011.

Discussion

Pest outbreaks are rare in polycultures due to the ability of the diverse plant culture to self-sustain through natural pest control by increasing the occurrence of natural enemies (Altieri 1994; Scherr & McNeely 2008). The cumulative mean leafhopper population of 2010 and 2011 was smallest in treatments T1 and T3, followed by T2, T5, T4, T6, and T7. In other words, eggplant with maize as border crop (T1 & T3) and coriander as intercrop (T1) or marigold as intercrop (T3) had the lowest leafhopper incidence. All those treatments having maize as border crop (T1, T3 & T5) recorded lesser leafhopper population than cowpea as border crop (T2, T4 & T6). Maize likely acted as a barrier crop for the movement of leafhoppers, as maize plants were much taller than the main crop and when planted in the border, maize is known to act as barrier crop (Root 1973; Fereres 2000; Elanchezhyan et al. 2008). Insect movements in and out of the system are affected by the permeability of the vegetation. In and out migration patterns of insects in polycultures have been studied by Bach (1984), Risch (1981) and Wetzler & Risch (1984). Similarly leafhopper populations in pigeonpea were reduced by sorghum intercropping (Sekhar et al. 1997). During the present investigation it was noticed that maize harbored large numbers of coccinellids and syrphids, which might have helped to reduce the leafhopper nymphs on eggplant in those treatments. The border crop and intercrop change the microclimate of the main crop, which in turn hinders insect pest development and favors natural enemy proliferation by providing supplementary food and refugia (Staver et al. 2001). Moreover, the volatiles from coriander and marigold likely acted to repel leafhoppers, resulting in smaller populations in T1 and T3 compared with the sole crop control, T7. Insect pests have difficulty in locating their host plants due to presence of intercrops and border crops that emit volatiles that have either masking effects or repellency (Goel & Tiwari 2004; Gupta & Chourasia 2004). The 3 intercrops (coriander, marigold and mint) are odoriferous in nature. The odoriferous plants, when raised with host plants of insect pests, can deter recognition, feeding and reproduction of the pests on their host plants (Dethier et al. 1960; Schoonhoven 1968).

The whitefly population was smallest in treatment T3 followed byT1, T4, T2, T5, T6, and T7. The results indicated that maize as border crop and marigold as an intercrop effectively reduced the whitefly population in eggplant. The volatiles from marigold have repellent action against whiteflies (Zavaleta-Mejía & Gomes 1995), explaining why treatments T3 and T4 had small whitefly populations. Coriander was the second best intercrop in reducing whitefly populations. Maize was a very good barrier crop against whitefly colonization and migration. Hence, the treatments having maize as border crop (T3, T1, and T5) had smaller whitefly populations than the other treatments and sole crop control, T7. Marigold intercropping in tomato reduced whitefly and nematode populations (Abid & Magbool 1990; Zavaleta-Mejía & Gomes 1995). Similarly, Trialeurodes vaporariorum (Westwood) (Hemiptera: Aleyrodidae) was repelled by Tagetes spp. (Asterales: Asteraceae) (Endersby & Morgan 1991). This bottom-up effect of marigold intercropping was accompanied by a top-down effect, as the marigold increased longevity and fecundity of natural enemies by providing nectar and pollen (Baggen 1999). Next to marigold, coriander supported the smallest whitefly populations in our study. Under greenhouse conditions, planting melon (Cucumis melo L.) or watermelon (Citrullus lanatus [Thunb.] Matsumara & Nakai) (Cucurbitales: Cucurbitaceae) with coriander reduced infestation by B. tabaci (Costa & Bleicher 2006). Similarly, Hilje & Stansly (2008) reported that B. tabaci abundance and begomovirus incidence were low on tomato intercropped with coriander. Our treatments using maize as border crop (T1, T3, and T5) had the smallest whitefly populations. Maize as barrier crop in beans reduced the B. tabaci population below economic threshold levels in Guatemala (Smith & McSorley 2000; Smith et al. 2000). Similarly, the whiteflies Aleurotrachelis socialis Bondar and Trialeurodes variabilis (Quaintance) (Hemiptera: Aleyrodidae) on cassava, Manihot esculenta Crantz (Malpghiales: Euphorbiaceae), were less abundant when cassava was intercropped with maize (Gold et al. 1990).

The presence of non-host plants might have repelled the adult moths resulting in less fruit infestation in polyculture treatments (T1 to T6) than in the sole crop control (T7). The repellency to different lepidopterous pests of various non-host crops was reported by Khan et al. (2000), McNair et al. (2000) and Liu et al. (2005). The results clearly revealed that maize acted as an effective barrier for the movement of adult fruit borer moths, thereby reducing the percentage fruit infestation in treatments T1 and T3. Non-host plants mixed in with host plants either act as a mechanical barrier to the dispersal of the insect pest (Kennedy et al. 1959; Root 1973) or physically repel them because of unpleasant morphological features such as hairy leaves (Levin 1973). Similarly, Nwilene et al. (2011) reported that intercropping maize and cassava with NERICA rice varieties had reduced stem borer attack on rice. They also concluded that cassava acted as refugia for generalist predators against stem borer. Coriander and marigold as intercrop resulted in lowering the numbers of sucking and borer pests than mint as intercrop and the sole crop control. Intercropping coriander with eggplant reduced L. orbonalis infestation and the amount of insecticide used by farmers (Khorsheduzzaman et al. 1997), and intercropping marigold with cabbage reduced oviposition by Pieris brassicae L. and larval incidence of Pieris rapae L. (Lepidoptera: Pieridae) on cabbage (Koehler et al. 1983; Metspalu et al. 2003). L. orbonalis orientation and oviposition on eggplant was reduced when it was planted along with coriander or fennel (Satpathy & Misra 2011). In the present study, the highest percentage increase in yield (based on numbers of uninfested fruit) compared with the sole crop control was recorded from treatment T1 during both years, and this result agrees with that of Hasheela et al. (2010).

High diversity in predatory insect and parasitoid species was recorded from treatments T1, T3, and T5 wherein maize supplied pollen and nectar as supplementary feed to the natural enemies (Bianchi et al. 2006). The ample availability of pollen and nectar from the tassel and silk of maize crop attracted many natural enemies. Apart from this, maize also offers honeydew produced by Rhopalosiphum maidis (Fitch) (Hemiptera: Aphididae) which attracts aphidophagous predators and parasitoids. This supplementary food resource increases the parasitoid fecundity, longevity (Tylianakis et al. 2004) and also favors rapid colonization of generalist predators (Symondson et al. 2002). The dense vegetation created by the presence of eggplant with intercrop and border crop had led to rapid colonization and occurrence of natural enemies in higher densities. This is in accordance with reports of Sprenkel et al. (1979); Horn (1981). Similarly, Letourneau & Altieri (1983) and Letourneau (1990) also suggested that predator colonization rates could be manipulated through vegetational diversification of the crop habitat.

Table 2.

Effect of intercrops and border crops on infestation of eggplant by the fruit and shoot borer L. orbonalis during the 2010 and 2011 monsoon season.

Natural enemies harbored by maize consist primarily of ants, spiders, rove beetles, predaceous mites, and ground beetles (Rose & Dively 2007). Similar report of intercrops increasing natural enemy diversity is reported by Singh et al. (1991a). They found that sorghum as an intercrop significantly increased the natural enemies like Laius mallifer, C. septumpunctata, Orius sp. and C. sexmaculata which had controlled thrips infesting groundnut. Treatment T1 yielded the highest numbers of natural enemy individuals and species and the highest Shannon-Wiener index in 2010 and 2011. The present finding is in agreement with that of Amin et al. (2005), who reported that eggplant with coriander as intercrop had the highest diversity index during the early growth phase of eggplant. The present result is also in concurrence with the reports of Midega & Khan (2003). They concluded that habitat management for maize stem borers by using “push pull system” had increased the abundance of natural enemies like Cheilomenes sp, Chrysopa sp., ants earwigs and spiders concurrently with reducing target pest i.e. stem borers.

Table 3.

List of natural enemies recorded in various treatments with intercrops and border crops to determine infestation levels of eggplant pests.

Push - pull strategy involves manipulation of insect and natural enemy behavior through the integration of stimuli that act to make the protected resource unattractive or unsuitable to the pests (push) while luring them toward an attractive source (pull) from where the pests are subsequently removed (Cook et al. 2007). The push-pull strategy was well established for cereal stem borer management in Africa, wherein the molasses grass, Melinis minutiflora P. Beauv. or silver leaf desmodium, Desmodium uncinatum (Jacq.) DC. or D. intortum is used as push component and napier (Pennisetum purpureum Schumach) or sudan grass (Sorghum sudanense Stapf) is used as pull component. The adult moths were pushed from maize by the molasses grass or by Desmodium sp. simultaneously they were pulled by napier grass or sudan grass, as these 2 are preferred for oviposition by the adults (Khan et al. 2000, 2006). The pull components used here were putative trap crops (i.e., they would not support larval feeding) the stem borer population starts reducing by the use of this push-pull strategy. This strategy not only reduced cereal stem borers but also reduced the parasitic weed, Striga hermonthica (Del.) Benth. and thereby sustained the cereal production in sub Saharan Africa (Khan et al. 2010).

Table 4.

Predatory insect diversity in various treatments with intercrops and border crops to determine infestation levels of eggplant pests.

Coriander leaf volatile consists of carvyl acetate and carvone in the present investigation. Carvacrol from coriander leaf volatiles was reported to strongly deter oviposition by the cotton leafhopper, Amrasca devastans (Hemiptera: Cicaidae), and the volatiles suppressed the nymph arrival (Saxena & Basit 1982). The colonization and residence time of the leafhopper on a host plant were influenced by the presence of the nonhost plants. The airborne volatiles of Melinis minutiflora P. Beauv. (Poales: Poaceae) a non host plant of spotted maize stem borer had repelled it from ovipositing on maize. This is due to the presence of the plant volatiles ocimene and nonatriene from the intercrop (Kimani et al. 2000). Farnesene present in the coriander leaves is an aphid alarm pheromone and thus helps in repelling aphids and acts as a kairomone for carabid beetles (Keilty et al. 1996). Similarly, whiteflies are known to avoid plant species that contain aromatic oils such as ginger oil. Hence, aromatic plants like coriander and marigold might have repelled the whitefly from the eggplant (Zhang et al. 2004). Repellent and antifeedant properties of mint against agricultural pests were reported by Koschier et al. (2002), Odeyemi et al. (2008), and Kumar et al. (2009). Similarly, Rattan (2010) reported that mint volatiles blocked the chemosensory receptor cells of lepidopteran larvae. Hence in the present study the intercrops (coriander, marigold and mint) repelled the leafhoppers, whitefly and eggplant fruit borers significantly. This is evident from the sucking pest population and fruit damage in control (T7).

Table 5.

Constituent volatiles present in leaves of coriander, marigold and mint.

These inter crops can be employed as a “push factor” in line with the well established push-pull management strategy employed in cereal stem borers in Africa (Khan et al. 2000, 2006). The border crop maize and cowpea acted as refugia for generalist natural enemies and these also helped in further reducing the pest populations in eggplant. Beyond this, maize also acted as a barrier to fruit borer and sucking pest of eggplant, thereby preventing the pest colonization in eggplant. Hence this system can be called as “push & prevent” strategy for managing the eggplant insect pest. Cook et al. (2007) has listed various cues that affect insects' long range and short range stimuli during the host searching process. The presence of non host volatiles and visual cues have under long range action, while ovipositional deterrents and antifeedancy serve as short range cues. In the present investigation the presence of non host volatiles from coriander, marigold and mint might have either repelled or confused the pest of eggplant, ultimately resulting in smaller pest population in the polyculture treatments. The latter case of confusion is attributed to the odor masking effect of the volatiles produced from intercrops. Similar report of non host volatiles of angiosperms resulted in reduction of colonization of bark beetles in conifers (Zhang & Schlyter 2004).

Fig. 1.

Total ion current (TIC) mode chromatographic plot of coriander leaf volatiles sampled and analyzed by the thermal desorption (TD) technique.

In a crop diversification system like coriander or marigold or mint with eggplant will result in poor quality or dilution of eggplant volatiles. This diluted or mixed odor may signal as poor quality host to the insect pest leading to repellent behavior. In polyculture, the odors released by some plants may mask the effect of those released by other plants. The codling moth (Cydia pomonella) was repelled by the odors of apple at inappropriate phenological stages Vallat & Dorn (2005). Under these circumstances, the insects find it difficult to locate the hosts on which to feed and reproduce (Altieri 1986).

In summary, the treatments (T1 to T6) recorded significantly reduced leafhopper, whitefly, and fruit borer populations compared with the sole crop control (T7) in eggplant during the years 2010 and 2011. Treatment T1, using coriander as an intercrop and maize as a border crop with eggplant, had the lowest mean number of leafhoppers (A. biguttulla biguttulla) per 3 leaves per plant (6.90). Treatment T1 also had the lowest percentage fruit infestation by L. orbonalis determined by number and weight of infested fruit (by number: 27.72%; by weight: 27.81%). The mean number of whiteflies (B. tabaci) per 3 leaves per plant on eggplant was lowest (8.36) in treatment T3, using marigold as intercrop and maize as border crop, followed by T1 (9.64). The highest number of coccinellids per plant on eggplant was recorded from treatment T1 (1.25), followed by T3 (1.00), T5 (0.78), T2 (0.67), T4 (0.61), and T6 (0.55). Maize as a border crop attracted many unique natural enemies like Paederus sp., C. zastrowi, Eristalis sp., and Brachymeria sp. in treatments T1, T3, and T5. In contrast, the sole crop control (T7) harbored only a few natural enemies. This was reflected in the higher Shannon-Wiener index recorded in the treatments T1, T3, and T5 compared with T7. We concluded that intercropping eggplant with either marigold or coriander coupled with border cropping with maize offers great potential for suppressing sucking pest and fruit borer pest populations besides conserving natural enemy populations. Thus the intercropping of coriander or marigold with eggplant and border cropping with maize can be used as “push & prevent” strategy for reducing the fruit and shoot borer and sucking pest especially jassids and whiteflies. This “push & prevent” management system will help in sustaining the ecosystem as well as productivity and profitability of farmers. Thus crop diversification in eggplant with intercrop and border crop will help in reducing the insecticidal application on fruit and thereby reducing environmental pollution in one hand simultaneously helping as a good strategy in insecticide resistance management. As crop diversification manipulates insect behavior, it is a sustainable solution for managing the insect herbivores of eggplant in an eco-friendly manner.

Fig. 2.

Total ion current (TIC) mode chromatographic plot of marigold leaf volatiles sampled using the thermal desorption (TD) technique.

Fig. 3.

Total ion current (TIC) mode chromatographic plot of mint leaf volatiles sampled using the thermal desorption (TD) technique.