cabbage aphid (Brevicoryne brassicae)

Direct feeding on young growth leads to visible wilting of plants. Early attack may lead to stunted growth. Symptoms of viruses transmitted by B. brassicae include mosaic, chlorotic and necrotic lesions on leaves, premature leaf senescence and various degrees of stunting, leaf rolling and leaf distortion.

Chemical Control

A range of organophosphates, carbamates and other pesticides have been recommended against B. brassicae in the literature. These have provided satisfactory control on brassicas. Application is usually as sprays, while granular application of systemic insecticides to soil is also common. Jukes et al. (1994) reported that deep-side placements prolonged efficacy. Threshold-based spray programmes have been shown to be more economical than calendar-based applications (Ellis et al., 1988).

Adverse effects of insecticides on the natural enemies of B. brassicae have been reported (e.g. Gamal et al., 1992). Insecticide resistance has developed in some areas. Simple bioassays, based on differential esterase production in susceptible and resistant aphids, are available to detect insecticide-resistant populations. Certain broad-spectrum insecticides are detrimental to natural enemies, therefore some selective aphicides, such as pymetrozine, which is harmless to natural enemies, are especially useful in IPM programmes (Fluckiger et al., 1992).

An adjuvant is often needed to help spray solutions adhere to the waxy leaves of cruciferous crops. Some adjuvants, such as Sylgard, are not a good fit for IPM, although they increase the efficacy of the pesticide (Acheampong and Stark, 2004).

Insecticidal soaps are used in IPM against B. brassicae on various brassica crops in the greenhouse. Control of other pests, e.g. Lepidoptera, using Bacillus thuringiensis (Bt.) is advantageous for aphid control by natural enemies. A preparation of Bt that is effective against B. brassicae has also been reported (Shevtsov et al., 1996). Neem-based insecticides are effective against B. brassicae, and these are also favourable to the natural enemies of aphids, unlike many conventional insecticides (Manger et al., 1997).

Biological Control

Early biological control attempts made in Australia were all unsuccessful (Wilson, 1960). Habitat manipulation to enhance biological control of brassica pests by hoverflies (syrphid larvae) has been carried out in New Zealand (White et al., 1995). The predacious midge Aphidoletes aphidimyza has shown potential as a biological control agent of B. brassicae in greenhouses. Pfrommer and Mendgen (1992) described control attempts with the fungal pathogen Verticillium lecanii against B. brassicae, in which they mixed a water suspension of spores with polysaccharides and detergents to produce an effective spray.

Predation by syrphid flies, e.g. E. balteatus, is frequently low due to presence of several parasitoids,such as Diplazon laetatorius, which reduce the impact of these natural enemies (Lowe, 1968; Oatman and Platner, 1973).

D. rapae is an important and efficient parasitoid of B. brassicae (Hagen and van den Bosch, 1968; Hagvar and Hofsvang, 1991; Fathipour et al., 2006). However, it has limitations as a natural enemy. The rate of parasitism by D. rapae is generally low on various cruciferous crops (Pimental, 1961; Hughes, 1963; van Emden, 1966a; Lowe, 1968). van Emden (1966a) and Chua (1977) concluded that D. rapae was ineffective in controlling B. brassicae in England, due to a lack of  synchronization as well as hyperparasitoid pressure. In general, parasitism of B. brassicae by D. rapae approached the highest level when host density started to decline (Nematollahi et al., 2014b).

Several wasps have been reported as hyperparasitoids of D. rapae (Hughes, 1963; van Emden, 1966a; Oatman and Platner, 1973; Chua, 1977). Hyperparasitoids are considered as a possible factor contributing to the failure of D. rapae to control B. brassicae (van Emden, 1966a; Chua, 1977).The population dynamics of B. brassicae, its parasitoid (D. rapae) and hyperparasitoids (Pachyneuron spp.), were quantified under field conditions (Nematollahi et al., 2014b). This study showed that D. rapae had good spatial coincidence with its aphid host but low impact on the host population because of a lack of parasitoid-host synchronization and low parasitoid: aphid ratio.

D. rapae parasitizes many aphid species on cruciferous crops and may be more effective for biological control of Myzus persicae than B. brassicae (Stark and Acheampong, 2007). The efficiency of D. rapae may therefore be reduced on some cruciferous crops such as oilseed rape, which are attacked by both aphids (Nematollahi et al., 2015).

Parasitism rate can be influenced by plant quality, probably due to the nutritional status of the aphids or to toxic compounds ingested through the plant. Cabbage, cauliflower and broccoli were found to be suitable plants for D. rapae, considering the development time of pre-adults, and the parasitization rate on B. brassicae (Bayhan et al., 2007).

Host-Plant Resistance

Most of the world’s economically important brassicas are sourced in either the A genome (e.g. B. rapa) or the C genome (e.g. B. oleracea), with B. napus, formed by hybridisation of the A and C genomes, being one of the most important oilseed crops in Europe and the Americas (Ellis et al., 2000).

Antibiosis resistance and antixenosis (non-preference) resistance to B. brassicae have both been demonstrated in a range of brassicas (Ellis and Farrell, 1995; Ellis et al., 1996; Ellis et al., 2000). Partial levels of antixenosis resistance were discovered in red accessions, the cabbage accessions Ruby Ball and Yates Giant Red, the Brussels sprout accession Rubine, and Italian Red kale. Glossy accessions of cabbage and cauliflower possessed antixenosis and antibiosis resistance that lasted throughout the season of crop growth in the field. Other accessions were shown to withstand aphid attack and therefore possessed tolerance. In a study of a collection of around 400 Brassica oleracea accessions, the most promising gene pool was kale, where a higher than expected number of resistant accessions was found (Ellis et al., 1998). In cabbage, antixenosis is an important resistance mechanism against B. brassicae in the red-leaved cultivar Ruby Ball whereas the green-leaved Minicole exhibits antibiosis to B. brassicae (Singh and Ellis, 1993; Ellis et al., 1996).

Laboratory studies have shown that some oilseed rape cultivars are more resistant to B. brassicae than others (e.g., Moharramipour et al., 2007; Mirmohammadi et al., 2009). Four wild species, Brassica fruticulosa, B. spinescens, B. insularis and B. villosa, have been shown to possess resistance to B. brassicae through antibiosis whereas others have shown variable resistance in glasshouse and field trials (Singh et al., 1994). Many field experiments have been conducted to evaluate resistance of different oilseed rape genotypes to B. brassicae (e.g., Monfared et al., 2003; Mousavi-Anzabi et al., 2009, 2013). For example, field evaluation of 20 oilseed rape cultivars showed that 'Okapi' and 'Opera' genotypes had the highest plant resistance index (Mousavi-Anzabi et al., 2013). In a series of field experiments, four wild Brassica species, two 8 chromosome species with similarities to the B genome of Brassica nigra (Brassica fruticulosa and Brassica spinescens) and two 9 chromosome species containing the C genome (Brassica incana and Brassica villosa) were identified as possessing consistently high levels of antibiosis-mediated resistance to B. brassicae (Ellis et al., 2000).

Compatibility of management tactics

It may be possible to improve the level of aphid control by combining plant resistance and biological control (van Emden and Wratten, 1991; Verkerk et al., 1998) which remains relatively limited when each control method is applied separately. The compatibility between these management tactics was studied by Kalule and Wright (2002a, b, 2004). Kaule and Wright (2002a) found that cabbage cultivar Minicole (green-leaved, partially resistant with antibiosis factors for B. brassicae) had the greatest proportion of aphids parasitized by Aphidius colemani and Derby Day (green-leaved, susceptible to B. brassicae), the least. Plants can have a positive or negative effect on parasitoids depending on the level and category of resistance (van Emden, 1991; Hare, 1992) and understanding the interactions that may arise from plant-aphid-parasitoid systems is therefore important in developing a pest management system for these insects. Another study showed that the composition of food consumed by B. brassicae modified its quality as food for A. colemani hence prolonging the parasitoids development on Minicole (Kaule and Wright, 2005). The secondary metabolite, sinigrin, produced in wild cabbage plants, resulted in smaller colony size B. brassicae (Newton et al., 2009). Experiments with Brassicaceae species including different amounts and kinds of glucosinolates (GLS) showed increased ladybird larval mortality at higher GLS concentrations (Francis et al., 2001).

Cultural Control

The practice of mulching has been shown to reduce pest incidence (as well as contributing to weed control) in brassicas. Baskey (1984) reported that incidence of virus inoculum in plants due to B. brassicae and other aphids was reduced by 70% in plots mulched with transparent plastic film and 77% with blue plastic film compared to unmulched plots. Mulching with rice straw is often practised in subtropical areas. Beneficial effects of intercropping and the use of 'living mulches' of undersown clover on the incidence of B. brassicae have been reported (e.g. Coaker, 1980; Wiech and Wnuk, 1991; Finch and Kienegger, 1997; Lehmhus et al., 1997) with the incidence of cabbage aphids reduced by 70-80% in some cases. However, undersown clover may also significantly reduce brassica crop yields (Wiech, 1996). Many studies have examined the responses of pest and beneficial arthropods to plant diversification, through intercropping, undersown, non-host plants and vegetation borders, in ephemeral cropping habitats. Ponti et al. (2007) showed that aphid pressure decreased and natural enemies of B. brasssicae were enhanced in intercropping treatments, but this varied with the intercropped plant and season (summer vs. autumn). Mustard as a non-crop plant, sowed 1 week after broccoli transplanting showed no reduction of broccoli yield and tended to reduce numbers of B. brassicae, while increasing effective predation by syrphid larvae (Kloen and Altieri, 1990).

Nitrogenous compounds are often scarce in plant tissues, particularly in phloem sap. Sucking insects such B. brassicae show a strong response to changes in nitrogen level in host plants (van Emden, 1966b). Several studies (e.g., Leal-Aguilar et al., 2008; Zarghami et al., 2010) have shown that higher nitrogen fertilization improves the suitability of oilseed rape for B. brassicae, whose performance is then increased.

The type of fertilizer used affects the survival of natural enemies. Banfield-Zanin et al. (2012) compared mortality of the predatory coccinellid, Adalia bipunctata, on plants in organic and synthetic fertilizers, and found that mortality increased by 10% when the predator-eating aphids on plants in synthetic fertilizer. The study on broccoli showed that intercropping and composting decreased pest abundance. Intercropping also enhanced parasitism of B. brassicae depending on the intercropped plant and the growing season (summer vs. autumn). The seasonal effectiveness of D. rapae was increased by composting despite lower aphid abundance in compost-fertilized broccoli (Ponti et al., 2007).

Crops which can suffer severe attack by B. brassicae include cabbage, cauliflower, broccoli, radish, swede and mustard. Kale, oilseed rape and Brussels sprouts are usually only lightly infested, while turnips appear immune. Large colonies feed on the undersides of young leaves, draining plant nutritional resources, and on the flower heads of seed crops, reducing the setting of seed (Blackman and Eastop, 2000).

On cabbage in Germany, numbers of aphids on the plants peaked in June-July and again in September-October. The yield was most affected by attack in the second population peak. Control thresholds for fresh consumption were 20% plants attacked with more than 10 apterae/plant, or 10% attacked plants when one or more plants had more than 100 aphids (Hildenhagen and Hommes, 1997).

B. brassicae was very numerous on yellow mustard (Sinapis alba) in a study in Poland, in which early infestations (at the bud development stage) prevented stalk development and caused premature plant death; while later infestations (at the peak or end of blooming) caused high yield reductions (Hurej and Preiss, 1997).

Among several aphids infesting brassica crops, B. brassicae was generally the most prevalent during the growing season (e.g. Trumble, 1982; Raworth, 1984; Nematollahi et al., 2014a). It occurred primarily on the highest and youngest leaves and stems, with the highest aphid density recorded at the head formation stage on broccoli and the stem elongation stage on oilseed rape (Trumble, 1982; Nematollahi et al., 2014a). B. brassicae significantly preferred the upper parts (upper 10-15 cm of the stem) of oilseed rape plants to the lower parts (the rest of the stem) (Nematollahi et al., 2014a).

In regions with warm climates, parthenogenetic reproduction can occur throughout the year. Considerable damage can occur to vegetables, particularly those grown for seed. In the Middle East, alatae migrate to cruciferous vegetable crops in autumn-early winter, migrating to wild Cruciferae in spring where they pass the summer. In Nigeria, cabbages with high uncontrolled infestations usually suffer stunted growth, plant death and low yields (Parh et al., 1987).

In Himachal Pradesh, India, the avoidable yield losses caused by an aphid complex (B. brassicae, Lipaphis erysimi and Myzus persicae) to three different cruciferous oilseed crops, Brassica campestris var. toria, B. campestris var. sarson and B. juncea, were 67.61, 62.51 and 50.00%, respectively. Most of the losses occurred when the infestation was prevalent during the flowering stage. These losses were checked by insecticide applications at the initiation of flowering (Sharma and Kashyap, 1998).

Late-season insect infestation of Brassica napus, B. rapa, B. juncea and Sinapis alba was studied in Idaho, USA. Aphid colonization (primarily B. brassicae) was observed on all these plant species, but infestation on S. alba and B. rapa occurred too late to have a major effect on seed yield. Seed oil content of rape species was significantly reduced by insect damage (B. brassicae, along with Ceutorhynchus assimilis and Plutella xylostella), although oil quality (indicated by fatty acid profile) was not affected. Uncontrolled insect infestation reduced seed yield of rape species by 37 and 32% in B. napus and B. rapa, respectively (Brown et al., 1999).

B. brassicae is a vector of about 20 plant viruses, including Turnip mosaic virus (as cabbage black ringspot, cabbage ring necrosis and radish mosaic) and Cauliflower mosaic virus (Blackman and Eastop, 2000).