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Effects of Crop Protection and Fertilization Treatments on Cabbage Root Fly Infestation

Effects of Crop Protection and Fertilization Treatments on Cabbage Root Fly (Delia radicum) Infestation in Dutch White Cabbage





2.1. Life Cycle/ Damage

3.0. Crop Protection Methods against CRF

3.1. Organophasphate Pesticides (OPs):

3.2. Netting (Row Covers):

3.3. Collars:

3.4. Companion Planting (CPs):

4.0. The Effects of Soil Fertility on Plant Resistance to Insect Pests




A critical challenge for organic systems is ensuring a sustainable and efficient pest management system. Since the ban and restriction in the use of pesticides, conventional farmers have also needed to find alternative means of protecting their crops, especially vegetables. Due to the increased demand for more sustainable control methods, researchers have opened different inquests into best management options. One devastating pest of brassica family; such as cabbages and turnips in temperate regions is the cabbage root fly (Delia radicum). Methods such as biological control and bio pesticides are being investigated by researchers. Some methods adopted by farmers have no strong scientific literature to validate or dispute them, this may lead to yield losses if ineffective. We therefore evaluate previous literature on some selected control methods adopted by farmers which include organophosphates, netting, collars and companion planting on D. radicum in organic and conventional systems.

1.0.        CABBAGE

Cabbage (Brassica oleracea var: capitata) is a vegetable crop which belongs to the Brassicaceae family. Literature disagree on its origin but widely point at both the Mediterranean highlands and Western Europe (Rakow, 2004). The leaves are thick and alternating with wavy or lobed edges and the roots are fibrous and shallow. It is grown for consumption of the leafy tissues that make up the aboveground cabbage head which forms on a short thick stem. It is a popular vegetable in Europe and across other continents. Common types of cabbage include green, savoy, red, Napa, Dutch white and bok choy. The Dutch White Cabbage is commonly used in salads, as a boiled or fried vegetable and or as a component of stews.

In the United Kingdom, it is a biennial crop sown in spring and summer (March to August). Cabbages grow optimally in rich, moist, well-draining soils with a pH of 6.5. Optimum growth temperature is between 15–20°C. The plant requires at least six hours of direct sunlight every day. Seedling are usually planted at the final spacing for seeds (45–60 cm/18–24 in between plants and 0.6 to 1.2 m/2–4 ft between rows). A typical growth cycle takes about 14 – 18 weeks and all brassica crops are known to require high fertiliser inputs for optimum yields (DAFF, 1998). Organic producers apply manure before planting season and compost when needed in season. Common cultural practices include raising seedlings in nursery, mulching and thinning.

Brassicas are of very high economic and nutritional importance worldwide. In the UK, the area of land under Brassica production in 2013 was 27,841 hectares, worth almost £250 million (DEFRA, 2013). Cabbage contains a wide range of antioxidants including choline, beta-carotene, lutein, and zeaxanthin as well as glucosinolates and the flavonoids – kaempferol, quercetin, and apigenin (Podsedek, 2007; Wang et al., 1996). These antioxidants have been linked to the positive health impacts associated with cabbage consumption (Block et al., 1992, Veer et al., 2000). A wide range of herbivorous pests attack Brassica crops in any given year, especially Lepidoptera, Hymenoptera, Diptera, Coleoptera, and Homoptera (Deasy, 2015). In temperate regions cabbage yield is usually limited by pests such as Cutworms, Flea Beetles, diamondback moth and Cabbage loopers/ worms, popular amongst them is the Cabbage Root Fly (D. radicum).

2.0.        CABBAGE ROOT FLY

In the temperate (Palearctic and Nearctic) regions, a major belowground pest of crucifer/ brassica crops is the Cabbage Root Fly Delia radicum L. (Diptera: Anthomyiidae). It is also known as Erioischia brassicae (Bouché) and D. brassicae (Bouché) along with 20 other synonyms (Holliday, Andreassen and Dixon, 2013; Meyling et al., 2013). It is a member of a large family of root flies that also includes other pests like the turnip root fly (Delia floralis Fallén),  onion fly (Delia antiqua Meigen) and the bean seed fly (Delia platura Meigen). It has been reported to cause economic losses for farmers from North America and Western Europe ($100 million), Canada, Finland and the UK (Shuhang et al., 2016; Havukkala et al., 1984). Under heavy pressure, up to 90% of plants may be destroyed by cabbage maggot if unprotected (Finch and Thompson 1992). In the UK, crop losses are nearer 24% (Finch, 1989). Furthermore, cabbage root fly infestations cause substantial yield losses in various other brassica crops including broccoli, cauliflower, turnip, and rutabaga (Finch 1989; Shuhang et al., 2016).

2.1.      Life Cycle/ Damage

In the UK, there are up to three generations of cabbage root fly per year (Collier, 2013), which can account for crop losses of 5-7% depending on the year (Deasy, 2015). The first of the two to three generations of adult D. radicum emerge in the UK in late April/ early May (Coaker and Finch, 1971; Hill, 1987). In favourable conditions mating takes place near the emergence site on the 4th day (Coaker and Finch, 1971). Mated gravid females (but not males or unmated females) then become responsive to host-plant odour. Females use chemical and visual cues to locate oviposition habitat. At potential oviposition sites, females make repeated short flights and landings: an uninterrupted series of landings on chemically appropriate leaf surfaces leads to oviposition. Oviposition in the soil around host-plants commences on the 5th and 6th days after emergence (Coaker and Finch, 1971). Most eggs, each fly lay up to 100, are laid singly and concealed in soil close to a host plant (Hill, 1987).

Figure 1: Lifecycle of a Cabbage Root Fly (source:

Plants with thick stems or that have been damaged by conspecific larvae (Bauer et al., 1996) receive most eggs. Larvae hatch within 3–10 days and feed initially on the root surface of the host plant. Development through three instars takes 3–4 weeks, and older larvae tunnel into the root. Pupation occurs within a puparium either in the root or nearby soil. This destroys the plants root uptake system causing draught-like symptom aboveground due to reduced turgidity of the plant (Abu Yaman, 1960; Caldwell et al., 2013). The plants wilt during the day and their leaves change colour after which the whole system decays. They then become stunted and die (Caldwell et al., 2013). This damage is classified as indirect because it doesn’t affect the edible head. (Finch, 1993).

3.0.        Crop Protection Methods against CRF

The cabbage root fly has been extensively investigated from different perspectives ranging from its oviposition, egg deposition, chemical and biological control methods. Mechanical/cultural control methods such as early winter ploughing, crop rotation and delayed planting have also been found to reduce pest populations albeit not below economic threshold levels (Finch, 1989). Bio-pesticides such as Bacillus thuringiensis, Metarhizium anisopliae and Steinernema feltiae have been tested against CRF (Vanninen, Hokkanen and Tyni-Juslin, 1999).This interest stems from its economic importance in crucifers and its ubiquity across a wide geographic range. Some successes in integrated pest management have been recorded, however, most have either been ineffective, costly or laborious (Finch, 1993; Shuang et al., 2016). Other methods being developed include breeding tolerant varieties and transferring antibiosis resistant genes (Felkl et al., 2005; Shuang et al., 2016). However, these methods may not be acceptable in organic systems.

3.1.      Organophasphate Pesticides (OPs):

Since the green revolution, pesticides have been the main control method for pests of most crop categories. D. radicum is often controlled using organophosphates. Popular among them areAzinphos-methyl, Chlorpyriphos, Diazinon and Parathion. In the UK, pest management strategies against D. radicum for transplanted brassicas under conventional cropping systems predominantly rely on a single preventative pre-planting root drench application of an organophosphate pesticide (chlorpyrifos). Their mechanism of action on insects and other animals is by phosphorylation of the acetylcholinesterase enzyme which results in an accumulation of acetylcholine, causing unregulated nervous impulses. On exposure, symptoms emerge within minutes / hours leading to nerve failure and death (Fishel, 2014; Roberts and Reigart, 2013). Standard dosage of chlorpyriphos are more effective against CRF than other OPs such as Cyazypyr and Lorsban (Van Herk et al., 2017). To improve resource use efficiency, forecasting systems are used to determine pests attack period (Finch, 1993). Recently, Joseph and Zarate (2015) found that 11 of tested insecticides were highly efficient against D. radicum in the laboratory. Notable among them is cyantraniliprole which was reported to be twice as toxic to D. radicum larvae 30 days after it was applied to the soil than at 1, 3, 7, and 14 days after application.

Despite these successes, insects develop resistance to these pesticides (e.g. Chlorpyriphos in Rutbaga growing areas of Canada have been confirmed), sometimes within short periods, making them ineffective (Finch, 1993; Herk et al., 2016). They have been implicated in biodiversity decline and have been found to eliminate non-target species such as earthworms, beneficial insects and soil microorganisms. These losses have huge implications on ecosystem services such as climate control, detoxification, pollination, seed dispersal, pest and disease regulation (Chagnon et al., 2015). Due to prevailing weather, they sometimes drift to unwanted areas thereby causing losses or conflict (Ahmed et al., 2011). The centre for disease control and prevention (CDC) advises that long-term exposure to organophosphates can cause confusion, anxiety, loss of memory, loss of appetite, disorientation, depression, and personality changes in man (Roberts and Reigart, 2013; CDC, accessed: 02 Jan 2017). Other symptoms such as weakness, headache, diarrhoea, nausea and vomiting may also occur (Fishel, 2014). Consequently, many of these chemicals have been banned or restricted within Europe with UK showing a decrease of up to 44% (Buffin et al., 2003; Pretty and Bharucha, 2015). These restrictions have also been attributed to existing and emerging consumer groups which call for boycotts of foods produce containing pesticides and other synthetic input. As a result, many farms have seen increased losses due to poor control of the cabbage root fly (Shuang et al., 2016).

3.2.      Netting (Row Covers):

Insect nets are widely adopted by both organic and conventional farmers in the control of flying insect pests of vegetable crops. They create a physical barrier between the plants and pests thereby reducing the need for pesticide sprays. Nets vary in thickness and fabric type such as the perforated polyethylene and polypropylene fabric – which is the most commonly used. They are usually supported by hoops or applied as floating covers – weighed down on the sides by sand bags or soil. The all-purpose nets allow through 90% sunlight and rain and about 70% of natural air flow. In temperate regions, these characteristics improve the microclimate enabling farmers to grow crops earlier. They are preferred by organic farmers and small garden owners because it also protects plants from birds, rabbits and strong winds (Cheser, 2010; Shrefler and Brandenberger, 2014).

Row covers provided similar levels of control to chlorpyrifos in transplanted and direct-seeded rutabaga (Holliday et al., 2013). In some cases, treated nets have been used against various pests such as alphacypermethrin-treated nets against Myzus persicae and its parasitoid Aphidius colemani in cabbage field (Martin et al., 2012). This was used because secondary pests e.g. aphids build up with ordinary row covers and are more effectively controlled with chemical treatments. However, these treatments may contaminate the vegetables, hence making them disallowed in organic practices.

Nets have been used by farmers to mitigate or eliminate damage from root maggots by preventing adult flies from laying eggs at the base of host plants (Simon et al., 2014). Researchers have also investigated the prospects and challenges of using row covers in different climates and cultural practices. For instance, Hough-Goldstein (1987) concluded that row covers reduced cabbage insect pests as well as numbers of insect-damaged cabbage heads. Nets can also have indirect effects on pest behaviour by masking the crops thereby disrupting the visual signal of the pest. Dixon et al. (2004) used row covers to protect cabbages from first generation of D. radicum in Newfoundland. They are sometimes combined with other integrated management approach such as natural/biological control and trapping (Simon et al., 2014).

There are a few disadvantages to using floating row covers. It will be ineffective if the eggs or larva are present before applying the cover, therefore timing is important (Hough-Goldstein, 1987). It is expensive for some farmers because it is frequently replaced due to tear during handling (Simon et al., 2014; Shrefler and Brandenberger, 2014). It is also difficult to manage weeds under the covers and the wind may cause abrasion to the growing terminal and foliage of plants. Less abrasion damage occurs on crops that do not have a vertically growing terminal such as broccoli and cauliflower. In areas of high humidity, poor air circulation under the plastic covers can contribute to algae growth on soil and foliage fungal diseases and other detrimental pathogens on vegetable crops (Finch, 1989; Simon et al., 2014). Finally, in subequatorial climatic conditions, fine mesh netting did not improve pest protection and induced an increase in temperature under the netting, which disturbed the plant physiology. In addition, having to handle the netting twice daily discourage farmers from adopting this technology (Simon et al., 2014).

3.3.      Collars:

Barriers that impede D. radicum females can be used to prevent oviposition. Collars are a form of barrier which are used to exclude insects from laying eggs at the base/stem of plants. In Europe, small-scale growers use ‘circles’ of a material e.g., foam rubber, carpet underlay, or a recycled plastic (Havukkala et al., 1984).  They found that plant protected by a foam-rubber collar received 66 % fewer eggs than the control plants and it was the only treatment that caused a lateral shift in the site of oviposition; 57 % of the eggs were laid outside the barrier at distances > 4 cm from the stem. Dry barriers were more effective but field results may only result in 26 -35% reduction in eggs. Similarly, Skinner and Finch (1986) found Foam-rubber and carpet underlay discs placed around stem bases during transplanting resulted in control levels similar to recommended insecticides. They concluded that discs were a reasonable method for CRF control in small-scale farms if timely applied. The root zone is protected from direct sunlight thereby excluding competition from weeds and conserving moisture in the root area. The conserved water enabled the plants to tolerate greater amounts of damage. In a greenhouse experiment using non-woven fibre barriers (collars), Hoffman et al. (2001) found that the number of D. radicum eggs were reduced by 64 -98% while the field trials showed a significant reduction in number of cabbage and onion maggots infesting plants. Finally, Kroschel et al. in 2009 also found that barriers reduced the flightless Andean potato weevil in the high Andes area by more than 13%.

For most experiments, disc sizes ranged between 5 – 26cm diameters, however the optimum size is 15cm as further increase in size caused no further reduction in root damage (Skinner and Finch, 1986). Recent commercial variants are available in degradable fibre material thereby eliminating environmental degradation. A drawback of this method is the need to provide other protection method against above-ground pests.

Figure 2: Cabbage protected in an organic fyba collar

Only few experiments have been conducted on the use of root collars against CRF, most available information dates to about 30years ago. This may be attributed to the dependency on pesticides and nets. With the restrictions on pesticides, cost of novel bio-pesticides and challenges in adopting row covers, collars may become a suitable alternative. Upcycled or recycled disc material which may be free or low cost can be adopted by farmers.

3.4.      Companion Planting (CPs):

Many organic and low input farmers claim that intercropping is effective against insect pests and even diseases. Entomologists such as Stan, Collier and Finch have conducted several experiments to understand the effect of the relationship between host and non-host plant on Delia spp. Some argue that increasing vegetation diversity interrupts the sequence of appropriate landings required before oviposition (Holliday, Andreassen and Dixon 2013). An alternative hypothesis is that the cruciferous plants in intercropped systems attract fewer pest insects than the plants in the monoculture because they are smaller and thus less attractive to insects during the host-plant selection process (Finch, 1989). He however mentions that these effects are not always predictable due to other confounding factors that are not considered in experiments.

More recent experiments have taken such limitations into account therefore reducing methodological bias. The different mechanisms, such as the push-pull strategy and oviposition disruption by a non-host plant, through which CPs impact on CRF infestation has been investigated separately and in unison. Finch, Billiald and Collier (2003) concluded that companion planting is effective against CRF using aromatic plants such as Tagetes whose green leaves attract CRF thereby disrupting host-plant finding mechanism. Push-pull strategy depends on the distances over which ‘repellent’ chemicals influence the behaviour of insects, inferring that repellent crops be planted in inter-rows spaces (Schoonhoven et al., 2005). Finch and Collier in 2012 suggested that volatile plant chemicals only stimulate receptive flying insects to land and have little if any effect once the insects have landed. In Kenya, Cook et al., 2007, reported that molasses grasses were successfully used in controlling spotted stem borer in maize using the push-pull strategy. Similarly, intercropping Chinese cabbage with garlic was found to be effective in suppressing Diamondback Moth in a long period (Cai et al., 2011).

While scientists continuously investigate the mechanism of action to arrive at long-lasting solutions, farmers are more driven by immediate results. This experiment will investigate the efficacy of using Allium spp in controlling CRF. Denloye (2009) found that bean weevil was controlled using extracts and powder from garlic and spring onion. Allium spp is also suggested to be effective against Diamondback Moth when intercropped with cabbage (Luchen, 2001).

4.0.        The Effects of Soil Fertility on Plant Resistance to Insect Pests

Soil properties have often been investigated with regards to plant nutrition, biomass accumulation and crop yield parameters. Researchers are increasingly showing that the ability of a plant to tolerate or resist pests and diseases is related to the chemical and more importantly, biological properties of the soil. This relationship has been linked to soil organic matter levels and soil biodiversity.

Lampkin (1990) suggests that lower pest pressure in organic systems could be due to use of crop rotation and/or preservation of beneficial insects in the absence of pesticides. Crop rotation will break the food chain of the insect pests while beneficial insect may prey upon harmful insects (Altieri, 1995). Besides, organic systems are characterised by a diversity of crops in the rotation that improves the potential for cultural control of pests and diseases (Altieri, 1995).

Phelan et al. (1995) recorded a negative relationship between soil organic matter levels and oviposition preference of above-ground pest Ostrinia nubilalis. He attributed this to plant health; this may be due to higher biomass accumulation in organic crops which make them more turgid and resistant to infestation.  Magdoff and Van Es (2000) also attributed this to high organic matter and active soil biology which lead to increased competition, parasitism and predation in the rhizosphere thereby preventing infection. For example, Culliney and Pimentel (1986) found that plots treated with slurry and organic manure had a significant lower number of flea beetles than both mineral fertilizer and control plots. He also noted the presence of birds in both plots which may be responsible for reduced pest populations. A study on the use of vermicomposts revealed that it suppressed aphid and mealy bug populations thereby decreasing losses in peppers, tomatoes and cabbages (Aracon, Galvis and Edwards, 2005). Similarly, Hsu, Shen and Hwang (2009) assessed the effect of fertilization on Pieris rapae crucivora, they found that cabbages planted in organic plots showed lower pest occurrence on foliage compared to synthetic fertilizer plots. The organic plants also had a higher leaf biomass.

The relationship between mineral-nutrient content of crops and pest susceptibility is well documented (Dale 1988); high mineral N content has been linked to plant resistance to pest attacks. According to Altieri and Nicholl (2003) high levels of chemical fertilizer applications may cause nutritional imbalances in crops, in turn making them more susceptible to insect and disease pressure. He also suggests that increase in the nutrient content of the plant may increase its acceptability as a food source to pest populations.


The cabbage root fly remains an important pest of brassica species. From temperate to Mediterranean regions, it causes devastating losses for organic and sometimes conventional farmers. Solutions such as the use of bio-pesticides and netting pose problems for small scale and warm climate farmers. They are often expensive and netting may cause increased humid microclimate which promote fungi and other disease causing pathogens. Similarly, natural predators and mechanical control have been neglected by the farmers largely due to difficulties in management and adoption.

Many small-scale farmers adopt the use of collars; but the question of its efficacy remains. Recent and comprehensive literature on collars is missing. If farmers readily adopt the use of collars, can it be compared to using net or other established protection methods? Does it have additional advantages for the farmer?

Likewise, companion planting is a common practice in organic systems. Unlike collars, they have been studied extensively. However, data on their efficacy vary widely between regions and production systems. Some growers are now experimenting with garlic chives; a farmer in Northumberland, a few miles from our study site (Nafferton farm), claimed that combined with insect trapping, garlic is acceptable as the second-best option to Birlane for controlling cabbage root fly (Buffin et al., 2003). How acceptable is it? Does it control D. radicum below economic threshold levels? What will be the effect of intercropping garlic chives alone with cabbage on D. radicum? If comparably effective, intercropping with garlic chives will have an advantage over netting because it will remove the rigour of placing and adjusting the net during the growing season. It will also eliminate the problem of increased humid micro climate in nets and may provide an extra income for the farmer. Will it be a win-win solution for the farmer?

Fertility management has been found to influence pest abundance and plant tolerance to Insect attacks. Literature suggests that systems which build up soil organic matter protect plant health through various mechanisms discussed in section 4.0. If these crop control methods are adopted by conventional farmers, will it yield the same result?

In conclusion, this research aims to determine an effective alternative crop protection method on cabbage root fly in organic systems while comparing it against conventional results. This research will contribute to the knowledge on CRF control by investigating the questions above. It will also help farmers make more informed decisions when selecting a control choice against CRF.


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