Many insect pests hamper cabbage cultivation and the most destructive pest is Plutella xylostella (L.), (Diamondback Moth (DBM) (Lepidoptera: Plutellidae), which can reduced the yield of cabbage by 80% if huge number of pests appeared in the field 15. Other major insect pests on cabbage and cruciferous crops are cabbage cluster caterpillar, Crocidolomia pavonana (F.) (Lepidoptera: pyralidae)16, Cabbage webworm, Helulla undalis (F.) (Lepidoptera: Crambidae), Cabbage aphids (Brevicoryne brassicae (L.), imported cabbage worm (Pieris rapae), cabbage butterfly, Pieris brassicae (L.)17, Tobacco caterpillar, Spodoptera litura (F.), and cabbage looper, Trichoplusia ni (Hubner) (Lepidoptera, Noctuidae)18 .They infested the crucifers mostly in dry seasons and larvae start infesting the crops from their young stage and attacked the head at maturity19 C. pavonana fed on the under surface of the leaves by leaving the veins causing skeletonization of leaves. P.xylostella larvae initially fed on the leaves causing small holes and entirely damaged the cabbage. T.ni defoliate the leaves by burrowing through 3–6 layers of cabbage. H.undalis usually damage on outer surface of cabbage and continue feeding into the terminal bud damaging the entire cabbage plant 19,20 .
Current biological control of Crucifer pests
Habitat management
Habitat manipulation or management is one of the most sustainable ways of managing pests by promoting their natural enemies 21. It involves different approaches like intercropping, push pull method and insectary plant. Intercropping can be achieved by planting secondary or tertiary crop near the main crop or by incorporating non crop plants for certain specific functions for example, providing nectar and pollen for predator and parasitoids22. There are many reports on effective intercropping control method such as plantation of tomato inside the cabbage plot reduced the population of many adult butterflies of P.xylostella and P.rapae as compared to the monoculture cabbage plot. It is likely due to confusing visual cues and volatiles receive from tomato which masks the cabbage. However, it was reported that there was inconsistency between the damage index and population of pest. As suggested by Xu, Q. C et al. 23 decreasing pest population in intercropping plots in turn increase the pest damage index in monoculture plot. The cause of this might be due to the variation in nitrate concentration of outer layers of cabbage leaves which is higher in intercropped plot than monoculture plot. Another study concluded that, tropical basil (Ocimum gratissimum L) can reduce the population of three cabbage pest (H. undalis, P. xylostella L. and S. littoralis) when grow in an alternate row with cabbage24. Intercropping of Oscimum sanctum L. with Brassica rapa H. can reduce the pest population of H. undalis, S. litura and Phyllotrea sinuate F as compared to contro plot 25. In another study, using of onion and tomato as an intercropped plant with cabbage as host plant could be taken as the most reasonable and inexpensive pest management strategy when compared to other methods 26. With these studies, intercropping of certain plants like tomato, tulsi etc. with cabbage can be used preferably as an alternative for synthetic pesticides in management of cabbage pests
Enhancement of insectary plant species
Insectary plants are those plant species that attract beneficial arthropod i.e., predators of crop pest by releasing volatile compound and enhance their population by providing them the nectar27, 28. Nectar acts as a food source that supports the growth and development of beneficial arthropod. However nectar produced by all flowering plants are not able to support the predators as some flower produce volatile that may repel them29,30. Thus selection of suitable flowering plants should be considered for the benefit of proper biological control22. And it is necessary to recognize the flowering plant species that support only the predators, without assisting the pests31. Another study concluded that floral resources can be used as a biological control of cabbage moth, Mamestra brassicae (L.) (Lepidoptera: Noctuidae) by benefitting the pest enemies like parasitoids with its nectar. It has been reported that the three flowering plants Fagopyrum esculentum (L.) (Polygonaceae), (Fig.1) Centaurea cyanus (L.) (Asteraceae) and Vicia sativa (L.) (Fabaceae) significantly heightened the parasitization rate of parasitoid wasp, Microplitis mediator Haliday. (Hymenoptera: Braconidae). As a result of a large number of parasitoids, the parasitization of M.brassicae by the parasitic wasp M.mediator amplified without enhancing the longevity and fecundity of the pest M. brassicae 32. Apparently, the unfed parasitic wasp doesn’t waste their energy for host searching if they are found closer; rather they directly parasitize the hosts in lack of food 33.
Regulating the planting period of Crucifers:
Regulating planting period of crucifers would be able to control certain insect infestations and can help in reducing the use of synthetic insecticides. Variables in climatic conditions play a significant role in the population of crucifer’s pest since they have a short generation time and rapid reproductive rates34. It also greatly depends on the temperature (Fig.2) which may lead to an increase in infestation by rapid rises of pest population or reducing mortality of pest35. Impact on crop performance by planting dates is because of the changed in abiotic and biotic factors. In the cabbage field plot, the pest population started increasing from February and the highest peak occurred in April. Multiplication of pests preferred the hot climatic condition (off-season) but in cold condition (Nov-Feb) very few insects infest the cabbage36. According to Tanyi37 late plantation of cabbage (April) reduce the pest population of cabbage looper larvae, webworm larvae and P. xylostella when compared to normal and early plantings. This method is considered a feasible, cost-effective pest management strategy that can be implemented by the farmers. Studies in Karnataka by Viraktamath et al.38 reported that P.xylostella highly damage the leaf of cabbage planted in the first week of January in comparision with those planted in the first week of December but the head of cabbage were not marketable in both cases. From these studies, it concluded that temperature plays an important role in regulating the pest population of crucifers as hot and dry condition increases the pest population as compared to cold condition 39.
Push-pull strategies
In push pull method, one repellent plant is planted within the crop to repel the pest and another attractant plant species is planted in the surrounding field to attract the pest 22. The “push-pull” strategy is a technique that brings together both negative and positive impulse to repel the pests from the host plant and consequently trap the herbivores by the trap plants grows at the surrounding of host target39. At present, this method has been implemented approximately by 70,000 agronomist40. Presently, the most effective technique of agricultural pest management, the push-pull method, was practiced successfully and developed in Africa. It required low efforts and it’s an organic agricultural pest management system41. The techniques include both the combined use of trap crops and intercrops. The plant used as trap crops and intercrops must be suitable for the farmers and should be able to damage the natural enemies42. Some of the repellent plants that have been used as a push for controlling stem borers in maize are molasses grass Melnis minutiflora (P.Beauv), silver leaf desmodium Desmodium unicinatum (Jacq.)DC or green leaf desmodium Desmodium intortum(Mill.), that can pull away target pests to the trap plants mainly Napier grass (Pennisetum purpureum Schumach.) or Sudan grass (Sorghum vulgare var sudanense Hitchc.)43. An example of trap plant is Barbara vulgaris (W.T.Aiton), which was reported and can attract the cabbage pest, Plutella xylostella but there were complications in field management practices as the plant is not suitable growing in arable fields44. Another case is using of onion and tomato (Fig. 3) as an intercropped plant with cabbage as host plant could be taken as the most reasonable and inexpensive pest management strategy when compared to other methods. Successful method of intercropping method using onion and tomato is probably due to the confusing volatiles and visual signals that can in return repelled the cabbage pests26.
Pheromone based product for cruciferous pest management:
Pheromones are a low molecular weight volatile organic molecule produced by insect to produce a behavioral response from other individual of the same species45. According to Witzgall et al.46 more than 1,600 pheromones and sex attractants have been reported. Sex pheromones are mainly used to control the pest in an agricultural field. One of the advantages of using pheromone in pest management system is showing no adverse effects on non-target and beneficial insects as they have higher degree of specificity to one specific insect species only47. Management of pest population can also be done by using synthetic pheromones where it can mask the natural pheromones produced by the lepidopteran pest and disrupt the olfactory communication of opposite sex which results in mating disruption. Mating disruption using synthetic pheromone has been considered as a feasible pest management technique48. However the efficacy of mating disruption is highly dependent on population density of pest as large number of pest populations are more difficult to control than less populations49. It has been reported that DBM sex pheromones isolated from the female moths i.e, (Z11-hexadecenal, Z11-hexadecenyl acetate in the range of 8+2 to 4+6 and addition of 1% Z11-hexadecen-1-ol were used in mass trapping of male moths in a cabbage field50.
Botanicals against Crucifer pests control
India is among the leading country that gains insight in developing natural botanical insecticides as most of the people still focused on indigenous traditional knowledge for controlling insect pest in the field 51. Botanicals are natural chemical compounds derived from plants52. They showed different biological activities such as repellents, insecticides, fungicides and bactericides53. Some of the plants that have been reported to protect crucifer crops against insect pests are shown in (Table 1).
Botanical insecticides served as effective and safer alternatives of synthetic insecticides, as they are readily available and safer for the non-target organisms and for the environment54-56. Some common chemical compounds reported from plants are Pyrethrins, Nicotine, Rotenone, Azadirachtin, Limonene, Limone, Linalool, Citronellal, Artemisinin, Diterpene, Coumarins, Annonin57, 58. According to 2012 report, Ministry of agriculture approved nine botanicals insecticides along with garlic and neem extracts. Those seven botanical insecticides include Cymbopogon spp. Spreng., Sophora spp.L., Annona squamosa L., Tripterygium wilfordii Hook.F., Apocynum venetum L., Eucalyptus globulus Labil., Milletia pinnata L. They have been commercilaised by Ministry of Agriculture59. Studies have reported that azadirachtin from Neem (Azadirachta indica) and lantanine from Lantana camara exhibit defensive mechanism against insects pests. Azadiractin is considered as one of the most effective botanical insecticide and helped in management of many agricultural pests60, 61. Some of the insecticidal plant used in management of pests in cabbage and cauliflower are leaf extract of Aloe brevifolia, Melia azedarach62. Eupatorium adenophorum, Lantana camara63, Worm wood (Artemisia maritime)64. Although some agricultural organisations often recommended using botanical insecticides over synthetic pesticdies there are some drawbacks like having poor scientific evidences on the efficacy and safety of botanical insecticides65. One of the factors that control the efficacy of the botanical insecticides mainly depends on concentration of active constituents and its varying contents 66. Variable concentration of active constituents mainly resulted from the varying concentration of secondary metabolite contents which is caused by an extensive factor like the genotype of plants, different environmental factors and plant developmental stage67. Besides the above factor, an important factor could be due to the storage condition as the active constituents present in botanical insecticides may deteriorate gradually while storing65. Some other factors like a method of application of bioactive compound and a structural membrane of the target pest and its body conformation is responsible for altering the bioactivity of compounds and its toxicity 68. It has been reported that the synergistic activity of plant essential oil constituents based on, insecticidal activity on 3rd instar larvae of the cabbage looper, may help in penetration-enhancing effect into the insect integument. Lemongrass consists of citral as the main active compound but some minor constituents also observed greater insecticidal activity than citral against the cabbage looper, Trichoplusia ni. so it indicates that greater efficacy of lemongrass oil than its main component in an isolated way gives an idea of positive (synergistic) interactions69 and it was also reported that the combination of three major components (thymol, p-cymene and linalool) of thyme oil which were obtained from Thymus vulgaris (Thyme) the binary mixtures have shown synergistic activity against the third instar larvae of tobacco cutworm, spodoptera litoralis 69.
Microbial control agent against Crucifer pest
Microbial biopesticides are products developed from microorganisms like bacteria, fungi, nematode and viruses that are used to control the agricultural pest and also play an important role as an alternative tool to chemical pesticides for their eco-friendly nature 70. According to NBAIR 2017 report, minimum of 15 biopesticides based on microbes have been developed in India with 970 commercial formulations registered. Some of the microbial control agents against crop pests are discussed here (Table 2).
Fungi species which are pathogenic to insect pests are called entomopathogenic fungi. The most commonly used entomopathogenic fungi are Beauveria bassiana, B. brongniartii, Metarhizium anisopliae, Lecanicillium lecnii, Hirsutella thompsonii, Cladossporium oxysporium and Isaria fumosorosea. Based on the report of entomopathogenic bacteria, the most commercially used microbial pesticide is Bacillus thuringiensis 71. More than 30 products developed from the sub species kurstaki of B.thuringiensis are effective against Bollworms, Loopers and other lepidopterans while two viruses namely Helicoperva armigera nucleopolyhedrovirus and Spodoptera litura mucleopolyhedrovirus were registered to control two lepidopteran pests i.e, Bollworms (Helicoverpa spp.) and Armyworms (Spodoptera litura)72.
Although microbial pesticides have many advantages for control of crucifer pest, several factors limits the commercial production and their efficacy also varies among the stage of larvae, strains, environmental condition and target pests. The efficacy of these products is highly effective when applied to the young larvae (first and second instars larva) and reapplication when insect population increases73-75. Some of the factors that limit the commercialization of microbial pesticides are discussed here. Low microbial counts is one of the factors, as rapid production of entomophthoralean fungi species is quite low due to difficulty in development of conidia and its short-lived which makes impossible in creating a period of vast applications. For this one should try to increase the production of resting spores and competent mycelia of entomophthoralean species by developing effective methods which will ultimately increase the efficacy of these fungi76. Another factor is the shelf life of entomopathogenic microbes, where storage facilities are not yet developed in rural areas. Poor solubility of the some of the formulations in water is also one of the challenges77, 78. Despite of all the challenges, several methods needs to be followed like enhancing the microbial production and formulation, learning the proper idea of microbial pesticides being incorporated into integrated systems and their relations with the external environment, accepting the advantages like efficacy, safety etc. while comparing with synthetic pesticides and approved 76.