Intercropping Empower Reduces Insect Pests and Increases Biodiversity in Agro-Ecosystem

Currently insect pest management solely depends on chemical pesticide that continuously affects on environment, biodiversity, animal as well as human health. Outbreak of secondary insect pest is also the cost of pesticide use in field leading crop more vulnerable to more pests. These negative impacts of pesticides have provoked growing interest in the adoption of multi-function agricultural biodiversity that promote pest management, creating interesting challenge for traditional approaches to regulatory compliance. To address multi-function agricultural practice, we tested several intercropping systems with mustard and their effect on pest management. Our results revealed that intercropping systems mustard with onion, garlic, radhuni and coriander significantly reduced pest population over sole crop. However, intercropping mustard with wheat and gram increased pest population in mustard field. This result indicated that all crops are not suitable for intercropping system. Among the tested intercropping systems, mustard with onion and coriander significantly reduced branch and flower infestation and increased pod formation per plant. These four intercropping systems did not significantly affect on honeybee pollinator which are crucial for mustard crop yield. A significant linear relationship was also found between honeybee population and pod formation. Our results indicate that suitable intercropping system can be a potential multi-functional agricultural practice for pest management in mustard crop.


Introduction
Mustard (Brassica spp) is a major oilseed crop in the world which is grown in 53 countries including Bangladesh [1]. It is the most dominant oilseed crop in Bangladesh and covers alone 80% of the total area under oilseed crops [2]. The area under mustard cultivation in 2001 was 317,800 ha and reached 294,206 ha in 2014 along with total production increased from 238,000 t to 296,000 t [3]. Currently, Bangladesh is producing 0.36 million tons of edible oil but total requirement is far from actual demand (1.4 million tons) [4]. As a result, Bangladesh needs to invest to import edible oils from other countries for mitigating the demand for additional population and changing of dietary habits and nutritional awareness for total population. The investment for the import of mustard oil increased substantially from 2006 (2.42 million BDT) to 2014 (50.59 million BDT) [3]. This statement indicates that production of mustard crop urgently needs to be increased in Bangladesh. However, increasing of mustard cultivation area is difficult due to several reasons. Among them, climate change and insect pest infestation are the major obstacles to produce mustard crop.
Several insect pests are responsible for hampering mustard production and yield reduction in Bangladesh. To date, 38 insect pests are documented with rapeseed-mustard crop in India [5]. Among them, mustard aphid, Lipaphis erysimi Kalt. (Homoptera: Aphididae) is the most destructive pest in all the mustard growing regions of the country [6]. Both nymphs and adults of the mustard aphid infest the leaves, inflorescences and immature resulting poor pod setting and yield reduction [7]. They also induce growth of fungus that causes dirty and black pods and leaves [8]. L. erysimi causes 35.4% to 96% yield loss, 30.9% seed weight loss and 2.75% oil loss [5] [9]. Application of control measure for this pest is necessary to reduce the yield loss and increase mustard production.
However, currently farmers rely only on chemical insecticide for controlling this pest. This insecticide has tremendous effects on environment, biodiversity, human and animal health. To mitigate these problems, alternative approach is needed. So, there is a big challenge for agriculturist to explore alternative approaches to increase sustainable production [10].
Conventional farming practices contributed to increase yields during the 20 th century, but are today contested for their negative impact on the environment [11] [12], human health [13] and imbalance of ecosystem [14]. Industrialized monoculture systems, which are highly dependent on the use of external inputs such as agrochemicals (i.e. synthetized fertilizers, chemical pesticides, growth regulators), favoured the simplification of agroecosystems [15] [16]. In contrast, promoting functional biodiversity, which supports ecological processes, may allow agricultural systems to benefit from various ecosystem services, including nutrient cycling, soil structuration and pest control [17] [18]. One of the "agrobiodiversity strategies" to improve the sustainability of wheat production [19] is to increase plant species diversity at the field scale though intercropping designs  [27]. It involves the cultivation of at least two crop species simultaneously in the same land [28] [29]. Mechanisms behind managing pest by intercropping system where the crops grow rather than main crops are not likely to be infested by the same insect pest [25]. It is a potential cultural practice for pest management since it diversifies crops in a given agro-ecosystem to reduce the population of insects and consequently their attack [30] [31] [32].
Research findings demonstrate that intercropping saves the target crop using several mechanisms. Non-host crops grown in intercropping can emit organic chemicals which adversely affect the pest insects, providing some degree of protection [27]. This might be happened due to the attention of biocontrol agents (nat- [39]. This study was undertaken to select best associated crop in mustard production by controlling major pest, L. erisimi.

Materials and Method
Experimental site

Experimental Procedure
The experimental plot was opened in the first week of November 2012 with a power tiller, and was exposed to the sun for a week, after which the land was harrowed, ploughed and cross-ploughed several times followed by laddering to obtain a good tilth. Weeds and stubble were removed, and finally obtained a de-

Impact of intercropping on aphid population and plant infestation
The results showed that intercropping mustard with other six crops had a significant (p < 0.05) effect on aphid population during the crop growing period.
The pest incidence varied across the intercropping systems. The intercropping systems mustard with onion, mustard with coriander, mustard with garlic and mustard with radhuni showed lower population levels (  between them (Figure 2). Significant higher % branch infestation was found in sole crop followed by T 1 , T 2 and T 3 intercropping systems. The result indicates that intercropping of mustard with spices reduced aphid infestation over sole crops in the field. Flower is the most attractive part of mustard plant and highly infested by aphids in field. Significant variation was observed in terms of flower infested by aphid at different intercropping systems. The mustard with onion (T 2 ) intercropping system sowed the lowest % of flower infestation. But the highest % of flower was infested by aphid was recorded in sole mustard crop ( Figure 3). All tested intercropping systems showed significant lower pod infestation (%) than that of sole cropping system (data not shown). Among the intercropping systems, T 5 intercropping system showed the lowest pod infestation but statistically similar with T 4 intercropping system (data not shown).

Impact of intercropping on honeybee population
Intercropping enhances biodiversity and interactions among plants, arthropods, mammals, birds and microorganisms providing in a more stable agroecosystem and a more efficient use of natural resources (such as space, water, S. Afrin et al.   (Table S1). The highest number of branches/plant was recorded in mustard sole (T 7 ) followed by T 6 (mustard with gram), T 3 (mustard with garlic) and T 5 (mustard with coriander) intercropping system having no significant difference among them (Table S1). On the other hand, the lowest number of branch/plant was recorded in mustard with onion (T 2 ) intercropping system. Significant variation was also observed in terms of flower at different treatments (Table S2). Results showed that the highest number of flower/branch was recorded in mustard with coriander (T 5 ) which was statistically similar in mustard with garlic (T 3 ) intercropping system. The lowest number of flower/branch was recorded in mustard with wheat (T 1 ) intercropped combinations. Number of pods/plant is one of seed components of mustard.
Highest number of pod/plant was recorded in mustard with onion (T 2 ) intercropping system which was statistically similar in mustard with coriander (T 5 ) and lowest number of pod/plant was recorded in mustard with gram (T 6 ) ( Figure 5). Treatment of intercropping mustard with onion caused a significant increase in number of seeds/plant (g) compared to other treatments ( Figure 6).
Lowest amount of seeds/plant was recorded in mustard with gram intercropping system. Number of pod formation increased with the increased of honeybee population in crop field. There was a significant linear correlation found between pod formation and honeybee population (Figure 7, F = 51.55; p = 0.001).
Intercropping systems also increased honeybee population in mustard field that indicated that some intercropping systems indirectly increased the yield of mustard crop.  Our study revealed that intercropping systems mustard with wheat and gram increased aphid population over sole crop (Figure 1). This may be happened due to companion crops because companion crop, wheat itself acts as a host for aphid [41]. Intercropping with onion, garlic, coriander and radhuni significantly reduced aphid population (Figure 1). This was happened due to companion crops since they can act as repellents or barrier for movement of aphid population. Companion crops in intercropping system hinder the movements of insect pests and thus the main crop will suffer less damage [38]. Non-host crops that are grown in intercropping system also can emit organic chemicals which adversely affect the pest insects [27]. Other explanation can be applicable that reduction of pest population can be done due to attraction of biocontrol agents (natural enemies) of insect pests by the emission of volatile organic compound or acts repelling the insect pest [33] [34] [35] [36] [37]. In our study, data of natural enemies were not collected, however we can hypothesize that intercropping system enhanced biocontrol agents that reduced pest population in mustard crop. Dhaliwal and Arora [42] reported that pearl millet under intercropping enhanced number of parasitoid and predators. Sometimes intercropping system reduced up to 30% crop pest by increasing natural enemy effect [24]. In this way, intercropping systems can protect crop from pest infestation. Debra and Misheck [43] reported that intercropping cabbage crop with onion and garlic reduced the incidence of insect pest significantly. Particularly intercropping with wheat and garlic reduced aphid population from wheat field [44] and onion is usually used as control of aphid in intercropping system [45]. Besides these, similar to our findings were found in other many scientific studies [18] [32] [46] [47] [48] [49]. In our study, intercropping with mustard and coriander also showed significant pest population decreased over the sole crop ( Figure 1). Similar result was found when mustard grown with coriander [50]. It may be happened due to emission of organic volatile compound by the coriander crop that acts as repellent of aphid or attraction of biocontrol agents of aphid.

Discussion
In our study, intercropping systems did not significantly influenced the population of honeybee in mustard field. Visiting honeybee or other pollinators is important for mustard yield. Intercropping system will not affect the visiting of pollinators in mustard field. Our results showed that intercropping system influenced the pod formation per plant. Intercropping system mustard with onion showed significant higher pod/plant ( Figure 5). Higher amount of seed/plant was also recorded in mustard with onion intercropping system ( Figure 6). This may be happened due to higher pod formation/plan and lower flower infestation. Our study showed that intercropping system mustard with onion reduced flower infestation (Figure 3) which enhanced higher pod formation ( Figure 5).
Besides the main crop production, intercropping system also enhanced other crop yield that can maximize the production per unit land. Wszelaki [51] stated that the practice of intercropping can make benefits in a crop production system by decreasing insect pest infestation, lowering external inputs, enhancing biodi-versity, increase yield and reduce economic risk.
Based on our experimental results, it can be mentioned that multiple crop species grown in a single land increase biodiversity and encourage natural enemies. Developing mutual interactions misguide insects for host detection, reducing insect pests, lowering pest infestation and lowering external inputs.
Plantation of multiple crops exploits different environmental niches, enhancing the total productivity per unit of land, providing financial diversification, as well as lowering the financial risk in case of target crop failure.

Conflict of Interest
Authors declared that they have no conflict of interest.