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Mealy cabbage aphidIdentification & Distribution Biology & Ecology Damage & Control
Identification & Distribution:Brevicoryne brassicae apterae are green and covered with a greyish white mealy wax that is also secreted on the plant and spreads throughout the colony. The head, tips of the antennae and the legs are dark. Some abdominal segments have small sclerites and there are also intersegmental muscle sclerites. Their siphunculi are thick and very short, 0.06-0.07 times the body length. and 0.8-1.0 times the length of the cauda. The cauda is triangular and broad. The body length of Brevicoryne brassicae apterae is 1.9-2.7 mm.
The alate above right is with her group of offspring. The alate Brevicoryne brassicae has a dark head and thorax, 50-70 secondary rhinaria on the third antennal segment, marginal sclerites and dark dorsal cross bands.
The clarified slide mounts below are of adult viviparous female Brevicoryne brassicae : wingless, and winged.
The mealy cabbage aphid does not host alternate but spends its entire life cycle on cabbage (Brassica oleraceae) or other brassicas. In cold climates oviparae and small thin winged males occur in autumn, and the population overwinters as eggs. Where winters are mild Brevicoryne brassicae overwinters parthenogenetically. It has a cosmopolitan distribution.
Biology & Ecology:
The biology and ecology of Brevicoryne brassicae has been reviewed by Pal & Singh (2013) with an emphasis on recent work carried out on the Indian subcontinent. Gabrys (2008) provides a concise account of the biology and pest status of Brevicoryne brassicae in the Encyclopedia of Entomology.
The morphology and biology of the different instars and forms was described by Bonnemaison (1951) who also carried out an extensive study of the factors which affect morph determination. Markkula (1953) gives a general account of the species. Lamb & White (1966) found that brief temperature treatments of adult apterous Brevicoryne brassicae independent of the host plant affected the form of their young. More aphids produced alate young after exposure to low temperatures (10-15°C), while alate production was suppressed at high temperatures (25-30°C). Starvation or crowding of adults for times up to twenty-four hours did not affect the form of the young.
Debaraj et al. (1995) studied the biology of Brevicoryne brassicae on six food plants in the laboratory. Depending on the temperature and humidity conditions, one cabbage aphid generation develops in 7-10 days. Satar (2005) evaluated the developmental time, survival rate and reproduction of the cabbage aphid, Brevicoryne brassicae on detached cabbage leaves. The optimal range of temperature for the population growth of Brevicoryne brassicae on white cabbage was 20 to 25/30°C. Ulusoy and Olmez (2006) studied the development time, mortality, survivorship and reproduction of the cabbage aphid on detached leaves of six Brassica species at a constant temperature of 20°C.
Host selection & nutrition
Brevicoryne brassicae is restricted to feeding on members of the Brassicaceae. The chemical basis for this restriction was investigated by Wensler (1962) who showed that sinigrin (a mustard oil glucoside) provides the necessary chemical stimulus to elicit a feeding response. He introduced sinigrin into young leaves of the broad bean, Vicia faba, and then gave aphids a choice between such a sinigrin-treated leaf and a similar but untreated leaf, standing side by side. After 24 h an average of 93 per cent of the aphids were found settled and feeding on the sinigrin-treated leaf, with an average of four new-born larvae each. Brevicoryne brassicae were reared on sinigrin-impregnated broad bean leaves continuously to the fourth generation when the culture was still healthy. The picture below shows two alate Brevicoryne brassicae colonizing wild mustard. Note the first instar nymphs below the alate on the left.
Nottingham & Hardie (1993) were unable to detect any effects of host plant odours on either walking or flying Brevicoryne brassicae. Gabrys & Tjallingi (2002) proposed that aphids recognise their host plant from the glucosinalates in the mesophyll tissue before they start ingestion from the phloem vessels. Ruiz-Montoya (2005) described the morphological variation of populations of Brevicoryne brassicae associated with two host species, Brassica oleracea and Brassica campestris, which occur sympatrically in the highlands of Chiapas, Mexico. The average phenotype of Brevicoryne brassicae individuals inhabiting different host-plant species was found to differ as a consequence of the contrasting feeding environments the host species provide.
Van Emden & Bashford (1969) looked at the reproduction of Brevicoryne brassicae in relation to soluble nitrogen concentration and leaf age. Wide variations in total soluble nitrogen occurred in different leaves of Brussels sprouts plants. These variations were partly the result of leaf age (leaf position) and partly the result of different fertiliser application to the plants. The fecundity of Brevicoryne brassicae caged on such leaves also varied greatly and was correlated with total soluble nitrogen within leaves of the same age, but not between leaves of different ages. Van Emden & Bashford (1971) looked at the performance of Brevicoryne brassicae and Myzus persicae in relation to plant age and leaf amino acids. With increasing plant age, total soluble nitrogen of Brussels sprout plants decreased after a peak at 6-9 weeks. The plants then became less suitable for Brevicoryne brassicae and Myzus persicae (particularly the latter) as shown by estimates of the mean relative growth rate of the aphids. Growth rate was, however, only poorly correlated with total soluble nitrogen, and this lack of correlation was particularly marked on plants less than 9 weeks old. It was felt that the negative relationship of one amino acid, amino-butyric acid, with the growth rate might be particularly important in the aphid/hostplant relationship. Wearing (1972) found that intermittent water stress is largely beneficial, and continuous water stress is largely detrimental to the reproduction and survival of both Myzus persicae and Brevicoryne brassicae feeding on Brussels sprouts. However, there are differences between the species on different leaf ages. During intermittent water stress in the old leaves, the normal feeding stratum of Myzus persicae, this aphid is relatively more successful than Brevicoryne brassicae. During continuous water stress in the young leaves, the normal feeding stratum of Brevicoryne brassicae, this aphid is relatively more successful than Myzus persicae.
Plant and aphid defence
Cruciferous plants produce a range of glucose-derived, sulphur containing secondary metabolites, commonly named glucosinolates (Grubb & Abel, 2006 ). Upon tissue damage caused by herbivores, these components are hydrolysed by mrosinases into a range of toxic or deterrent products. Because of the spatial separation of glucosinolates and myrosinase in plant tissues only the breakdown of cellular integrity is believed to initiate massive glucosinalate hydrolysis. As well as glucosinolates, jasmonic acid, salicylic acid, and ethylene (along with their hydrolysis products) also play important roles in plant protection and plant-insect communication. Kusnierczyk et al. (2008) looked at how the plant Arabidopsis thaliana responded when subjected to attack by Brevicoryne brassicae. Extensive gene expression changes were initiated during the first 6 h of infestation. Reactive oxygen species and calcium were involved in early signalling, and salicylic acid and jasmonic acid in the regulation of defence responses. Follow-up studies of defence-involved secondary metabolites revealed, amongst other changes, depositions of callose at the insects' feeding sites. The novel role of camalexin, induced as a part of defence against aphids, was verified experimentally. The picture below shows a young colony of Brevicoryne brassicae on red cabbage.
Broekgaarden et al. (2008) used an ecological and molecular approach to look at the responses of Brassica oleracea cultivars to infestation by the aphid Brevicoryne brassicae. They studied the interaction between Brevicoryne brassicae and four white cabbage cultivars. Both under glasshouse and field conditions, two of the cultivars clearly supported a faster aphid population development than the other two. Molecular analysis revealed a possible role for a trypsin-and-protease inhibitor in defence against Brevicoryne brassicae, whilst a xyloglucan endotransglucosylase seemed to have no effect on aphid performance. Overall, the study showed clear intraspecific variation in Brevicoryne brassicae susceptibility among cabbage cultivars that can be partly explained by certain differences in induced transcriptional changes.
The plant defences against herbivores are used in turn by the cabbage aphid to provide a unique defense mechanism against predators. Francis et al. (2001) used three Brassicaceae species, Brassica napus (low glucosinolate content), Brassica nigra (including sinigrin), and Sinapis alba (including sinalbin) as host plants for two aphid species: the generalist Myzus persicae and the specialist Brevicoryne brassicae. Each combination of aphid species and prey host plant was used to feed the polyphagous ladybird beetle, Adalia bipunctata. There was increased ladybird larval mortality at higher glucosinolate concentrations. When reared on plants with high glucosinolate concentrations, the specialist aphid, Brevicoryne brassicae, was found to be more toxic than Myzus persicae.
Kazana et al. (2007) showed that the aphids produce a myrosinase enzyme in head and thoracic muscles. The aphids also uptake glucosinolates, particularly sinigrin, from the plants on which they feed, storing the glucosinolates in their haemolymph. The combination of the glucosinolates and the myrosinase enzyme produces a violent chemical reaction that releases the mustard oil chemical allyl isothiocyanate. The defense mechanism has a dramatic negative effect on the survival of the larval ladybird predator Adalia bipunctata. The chemical defence of the aphids has been likened to a walking mustard oil bomb. Pratt et al. (2007) demonstrated that the presence of sinigrin in the diet of the cabbage aphid makes this aphid unsuitable as a food source for Adalia bipunctata but not for Coccinella septempunctata. However, for this ladybird species, there are costs associated with feeding on aphids that contain sinigrin as its presence in the aphid diet decreases larval growth and increases the time necessary for larvae to reach second instar.
Khan et al. (2010) looked at the glucosinolate levels and the performance of two aphid species on brussels sprouts, the specialist Brevicoryne brassicae and the generalist Myzus persicae, in relation to water stress conditions. Plants grown for 2 weeks under drought stress were significantly smaller and showed decreased levels of total glucosinolate when compared with glucosinolate contents of well-watered plants. Significantly larger populations of Myzus persicae were recorded on plants with a limited water supply than on plants grown under well-watered conditions. The specialist Brevicoryne brassicae was unaffected by changes induced under water stress conditions.
Hafez (1961) studied the population dynamics of Brevicoryne brassicae in The Netherlands, where the aphid has sexual forms in the autumn and overwinters in the egg stage. Hughes (1963) looked at the population dynamics of the cabbage aphid for 3 years in Australia where the sexual cycle is suppressed and parthenogenetic reproduction occurs throughout the year. The aphids spend autumn and winter on Brassica crops, and spring and summer on Brassica seed-crops or cruciferous weeds. Aerial migration was essential to cabbage aphid survival as its host-plants are not perennial. After the initial colonization of a host-plant the aphid population increases rapidly until physiological changes occurring within plant and aphid ensure that a large proportion of the progeny emigrate, escaping the direct consequences of overpopulation, with a finite chance of finding a new host-plant. The survival of the host-plant species is ensured partly by regeneration after aphid damage and partly by the interactions between emigration, a fall in the reproductive rate, and the extrinsic mortalities, which together result in a rapid decline of aphid numbers from peak levels. The picture below shows a cabbage aphid colony late in the season together with a predatory cecidomyiid larva.
Raworth et al. (1984) studied the population dynamics of the cabbage aphid, Brevicoryne brassicae at Vancouver, British Columbia. Peak numbers of Brevicoryne brassicae differed between plots, but the pattern of monotonic increase in the spring, followed by an abrupt decline in the rate of increase, a mid-summer peak, and an autumn population decline was consistent throughout. The first major decline in the rate of increase of Brevicoryne brassicae was correlated with the appearance of cecidomyiid larvae (Aphidoletes aphidimyza) and syrphid larvae. Declining adult aphid weight, which suggested declining fecundity, increased alate production at high aphid densities, parasite pressure, and leaf fall added to the damping effect of predators. In autumn, cool temperatures and production of sexual forms further reduced the rate of increase of the aphid.
Damage and control
Acheampong & Stark (2004) investigated the potential of using reduced rates of the selective aphicide (pymetrozine) and two biological control agents both in the laboratory and in the field to control Brevicoryne brassicae. In the laboratory the highest reduction of aphids (98%) was obtained when the low dose of pymetrozine was combined with both biological control agents. In caged field experiments, when pymetrozine was used at half field rate a 99.8% reduction in aphid numbers was obtained. This rate of suppression with pymetrozine was too effective for the potential additive reduction of aphids by biological control agents to be evident. Bacci et al. (2009) evaluated the toxicity of six insecticides to Brevicoryne brassicae, the coccinellid Cycloneda sanguinea, and Acanthinus sp. and the aphidiid parasitoid Diaeretiella rapae. Pirimicarb caused the lowest mortality to the natural enemies. Overall the predators were more tolerant of the insecticides than was the parasitoid Diaeretiella rapae.
Koritsas & Garsed (1985) looked at the effects of two levels each of nitrogen and sulphur nutrition and of infestation by Brevicoryne brassicae on the growth of Brussels sprout plants. All the plants receiving high nitrogen treatments grew more rapidly than those with low, but in infested plants the improvement in growth at the higher levels of nitrogen was offset by the increased size of aphid populations. It was concluded that the benefits of increased yield resulting from high nitrogen levels must be balanced against the greater potential for damage by aphids.
Dunn & Kempton (1972) carried out much of the early work of resistance of Brassica to attack by Brevicoryne brassicae. Uncolonized plants of Brussels sprouts were singled out from plots heavily infested with the aphid, as possibly being resistant to attack. Clones of these plants were established from cuttings and tested in a controlled environment by inoculation with Brevicoryne brassicae and later, in the field, by natural infestation. The tests confirmed that some of the plants were resistant to the aphid. It was also found that biotypes of the aphid, with differing abilities to colonize respective sprout clones, existed in different geographical areas.
Dodd & van Emden (1979) tested seven cultivars of Brussels sprouts from different sources for their relative degrees of resistance to the cabbage aphid (Brevicoryne brassicae) by estimating the potential increase rate of aphid infestations. Two cultivars were selected as susceptible and resistant respectively and tested further. Analysis of the amino acid content of leaf tissues collected at monthly intervals through the aphid season enabled "risk rating" predictions of aphid resistance to be made. These conformed with the shifts towards greater resistance as the plants aged noted in the glasshouse trials and endorsed the part played by amino acids in the mechanism of resistance.
Enhancing parasitism rate
Bahana & Karuhize (1986) studied the role of Diaeretiella rapae in the population control of Brevicoryne brassicae in Kenya. Diaeretiella rapae was the only parasitoid present. High parasitism coincided with a decline in aphid population. Because of these high levels of parasitism and other attributes of the parasitoid, it was concluded that Diaeretiella rapae played a significant role in suppressing populations of Brevicoryne brassicae and should be taken into consideration in any control programme aimed at protecting Brassica crops against aphid pests in Kenya. The picture below shows some cabbage aphids mummified by Diaeretiella rapae.
Titayavan & Altieri (1990) investigated an interaction apparently mediated by synomones between Diaeretiella rapae and Brevicoryne brassicae under field conditions. Direct application of an allylisothiocyanate emulsion consistently gave higher aphid parasitization rates and/or number of wasps per plant than those observed on plants treated with water or wild mustard extract. These results suggested the existence of a chemical-mediated interaction between the species, indicating potential avenues to enhance field parasitization rates through manipulation of the chemical environment of sole cropping systems. Gabrys et al. (1997) identified the sex pheromone of Brevicoryne brassicae as neptalactone. The compound proved attractive not just to male Brevicoryne brassicae, but also to the parasitoids Diaeretiella rapae and Praon volucre.
Lotfalizadeh (2002) carried out a survey on parasitoids of Brevicoryne brassicae on rapeseed in Iran. Two parasitoids, Pachyneuron aphidis & Diaeretiella rapae and a hyperparasitoid Alloxysta fuscicornis were found. Among them, Diaeretiella rapae was the most important parasitoid of the aphid with the rate of parasitization about 17 percent in May. Zhang & Hassan (2003) investigated the use of the parasitoid Diaeretiella rapae to control the cabbage aphid Brevicoryne brassicae. They found that one release of cabbage plants with mummies enhanced the spread of the parasitoid Diaeretiella rapae and increased parasitism of the aphids in the field. However, multiple releases of the parasitoid are needed to control the aphid effectively. The picture below shows a live adult Diaeretiella rapae searching for suitable hosts to parasitize.
Fathipour et al. (2006) examined the functional response and mutual interference of Diaeretiella rapae when parasitizing Brevicoryne brassicae. Logistic regression suggested a type II functional response on Brevicoryne brassicae nymphs. The per capita parasitism decreased significantly from 80.80 to 11.85 as parasitoid densities increased from 1 to 8 females. Consequently, the per capita searching efficiency decreased significantly from 1.173 to 0.205 as parasitoid densities increased from 1 to 8. It was concluded that different host-parasitoid ratios could affect the efficacy of Diaeretiella rapae. Duchovskien & Raudonis (2008) examined the seasonal abundance of Brevicoryne brassicae and Diaeretiella rapae under different cabbage growing systems in Lithuania. Diaeretiella rapae reduced the populations of cabbage aphid by around 25% during both experimental years. The abundance of aphids and parasites was highest on manure fertilized cabbage. The highest parasitism rates were observed in the periods when the number of aphids on the plants was the lowest at the end of their occurrence on the plants.
Van Emden (1965) monitored the numbers of the cabbage aphid Brevicoryne brassicae and its parasites and predators in a crop of Brussels sprouts during a season. The results were grouped so that the centre, two unsheltered edges and an edge of the field sheltered by trees could be compared to demonstrate the operation of edgegrowth effects on a natural infestation of the aphid. The deposition of alate aphids was increased by shelter to windward, resulting in the heaviest initial infestation at the sheltered edge of the crop. The edgegrowth crucifers became heavily infested at flowering. The aphids at the sheltered edge reproduced more slowly than at the centre of the crop and appeared to suffer heavier mortality from rainfall, with the result that aphid numbers were about half those found at the centre of the crop. Syrphidae were the more important predators, and their eggs were one and a half times as numerous near flowers as at the centre of the crop or elsewhere at the open edges. As a result aphids at the open edges suffered most from predation, which kept numbers rather below half the level at the centre of the crop.
Nieto et al. (1966) found that cabbage aphids predominately colonized the outer leaves of a broccoli plant, but these colonies did not significantly influence infestation at harvest. Center-located aphids were correlated with head infestation for both field seasons. Aphid arrival time into a field was strongly correlated with infestation at harvest, with early arriving aphids being less likely to infest a head. This was in part caused by natural enemies, particularly syrphid larvae (Syrphidae), which were in greatest abundance in response to early aphid colonizers.
Smith (1969) caught more Brevicoryne brassicae and other alate aphids in yellow water-traps in a weed-free crop of Brussels sprouts than in a crop with a weedy background. More Brevicoryne brassicae colonized Brussels sprout plants in bare soil than in weeds. However, initially larger populations on the weed-free sprouts became smaller than populations on the weedy sprouts because the larger aphid population attracted more natural enemies. The maintenance of a limited weed cover was considered potentially useful in integrated control of some Brassica pests. The picture below shows a heavy late infestation on a common wild member of the Brassicaceae, garlic mustard.
Pollard (1969) described an experiment on the effect of predator removal and exclusion upon Brevicoryne brassicae on Brussels sprouts. Two syrphid species were responsible for a rapid decline in aphid numbers at the beginning of the experimental period. In two treatments where syrphids were removed a cecidomyiid predator responded to the larger numbers of aphids and, in the treatment in which they were not removed, completely eliminated the aphids. In the treatment in which all predators were removed aphid numbers remained relatively high until the end of the season. Pollard (1971) made a study of aphidophagous syrphids and syrphid predation on Brevicoryne brassicae on brussels sprouts in contrasting areas of farmland. One area was rich in hedges, woodland, pasture and other habitats outside the crop and the other was mainly arable. The areas were 5 km apart. Some syrphid species were found to be in woodland and also in an adjoining hedge. However, these woodland based species did not lay many eggs on sprouts. Even 30 m from the hedge no more eggs were laid than in a site in the middle of an arable area. Neither was there any evidence that syrphid species which were more generally distributed and those which were mainly found in open habitats laid more abundantly in the area of diverse habitats than in the mainly arable area. The experimental study of aphid populations showed that syrphids reduced aphid numbers significantly only in the mainly arable area. This supports the view that the presence of rich non-crop habitats does not increase syrphid oviposition.
Tukahirwa & Coaker (1982) showed that intercropping brassicas with taxonomically unrelated plant species reduced infestations of the aphid Brevicoryne brassicae and cabbage root fly Delia brassicae by more than 60% compared with those on brassicas grown in pure stand. Costello & Altieri (1995) compared populations of the cabbage aphid, Brevicoryne brassicae, and the green peach aphid, Myzus persicae, on broccoli interplanted with three leguminous cover crops (the living mulches) with broccoli without cover crop (clean cultivation). No effect of cropping system on population growth rate was seen for cabbage aphid, but for green peach aphid growth rates were higher in living mulches compared with clean cultivation. Parasitism for both species tended to be higher on clean cultivated broccoli. This suggested that differential population growth rates for green peach aphid were a result of inhibition of Diaeretiella rapae in the living mulches.
Grez & Prado (2000) assessed the effect of plant patch shape and surrounding vegetation on the density, emigration, and immigration of predatory coccinellids, and on the density of their aphid prey Brevicoryne brassicae. They set up square and I-shaped patches of Brassica oleracea surrounded by alfalfa (Medicago sativa) or leeks (Allium porrum). Alfalfa is frequently used by coccinellids, whereas leeks are not. All insects were more abundant in patches surrounded by leeks than in those surrounded by alfalfa. Coccinellids emigrated less from square patches, either surrounded by leeks or alfalfa, and immigrated more to patches surrounded by leeks. Aphids showed a higher population increase, and plants of Brassica oleracea ended up being heavier in patches surrounded by leeks, particularly in I-shaped patches. It was concluded that surrounding vegetation and plant patch shape had both direct and indirect effects on the density of coccinellids. Ponti et al. (2007) looked at the effects of intercropping via competition on crop yields, cabbage aphid Brevicoryne brassicae abundance, and natural enemy efficacy in Brassica oleracea fields. Insect populations and yield parameters were compared in broccoli monoculture and polyculture systems with or without competition from Brassica spp. (mustard), or buckwheat. Competition from buckwheat and mustard intercrops did not influence pest density on broccoli; rather, aphid pressure decreased and natural enemies of cabbage aphid were enhanced in intercropping treatments. In compost-fertilized broccoli systems, seasonal parasitization rates of Brevicoryne brassicae by Diaeretiella rapae increased.