Mamestra brassicae (cabbage moth)

The eggs are relatively small, hemispherical, ribbed and reticulate. They are whitish in colour when newly laid, but turn gradually to purplish-brown with a brown to purple micropyle and basal ring. A few hours before hatching they darken to greyish black. The eggs are laid singly in regular batches of up to 70-80 eggs, mainly on the undersides of leaves. Korycinkska (2012) has described the eggs of M. brassicae using stereomicroscopy and scanning electron microscopy.

There are six instars. First- and second-instar larvae are about 3-10 mm long, greenish and more or less translucent with black hairs on black warts. First-instar larvae have a black head capsule, but after the first moulting it turns light brown. The prolegs on the third and fourth abdominal segments are poorly developed in the first two or three instars. From the third instar, the larvae are pale green with yellowish intersegmental bands. The dorsal region turns gradually darker with each moult, and in the last instar the majority of the larvae are brownish-green or blackish-green.

Heath and Emmet (1979) described full-grown larvae. The body is about 50 mm long, elongate, and with a slight dorsal hump on abdominal segment 8. The head capsule is light brown, and the dorsal region of the body is from fairly bright green, through brownish green to almost black. The dorsal line is fine and black. On each side there is one sub-dorsal line of blackish bars. The spiracular line is broad and pale green or pale ochreous. The spiracles are white. The ventral region is yellowish-green.

The pupae are elongate, 17-22 mm long, and reddish-brown and glossy. The wing- and limb-cases are finely sculptured. The abdominal segments are darker brown and evenly tapered, and there is a finely pitted anterior band on each segment. Segment 8 is sharply excavated to a narrow conical cremaster with two short apically hooked spines. Pupation takes place within flimsy cocoons in the soil (Heath and Emmet, 1979).

The adult moths have a wingspan of 34-50 mm. The forewings are mottled and may appear grey-brown, brown or blackish-brown, with variable reddish-brown scaling. Sub-basal, antemedian and postmedian lines are inconspicuous and slightly paler than the background colour, and have a fine dark edge. A kidney-shaped stigmata outlined in black with a whitish distal margin and a less clearly defined proximal margin, is placed near the centre of each forewing. The subterminal line is very variable. When present it is whitish and irregular, with two angular projections (like a W). The hindwings are fuscous and generally paler than the forewings. They are light greyish towards the base, and have a darker terminal shade. The fringe has a greyish central line. The forelegs have a characteristic brown, slightly curved, apically pointed tibial spur. Like other species in the subfamily Hadeninae, M. brassicae adults have hairy eyes (Seitz, 1913).

Mamestra brassicae can fly distances of up to 60 km, typically with the help of wind (Wu et al., 2015; Guo et al., 2020).

Mamestra brassicae has 31 chromosomes, which have been defined by Sahara et al. (2013). Expression sequence tags (EST) and fosmid libraries have also been constructed for this insect (Kamimura et al., 2012). Additional genetic studies have been conducted with M. brassicae, for example, to characterize odorant receptors and fatty acid transporters (Park et al., 2008; Vogt et al., 2009; Köblös et al., 2018).

The adult moths emerge from pupae in the soil. Shortly after emergence the moths mate, and the females deposit their eggs in regular batches of up to 70-80 eggs, mainly on the undersides of leaves. Egg deposition is unimodally distributed with a more or less distinct peak a few days after the onset of the oviposition period (Johansen, 1997a). The mean and maximum number of eggs per female is reported to be about 500-1500 and 2000-3000, respectively (see, for example, Noll, 1961; Poitout and Bues, 1982; Ogaard, 1983; Johansen, 1997a). Mean batch size is in the range of 14-37 eggs (Poitout and Bues, 1982; Hommes, 1983; Injac and Krnjajic, 1989; Johansen, 1996b). Number of eggs per batch is higher for young females than old females (Rygg and Kjos, 1975). Fecundity is affected by several factors, such as genetic constitution, development in the preceding immature stages, host plant, nourishment of the larvae and viral diseases (Noll, 1961).

The effect of temperature on fecundity is described by Johansen (1997a). The number of eggs laid per day increased from 27 at 11°C to 117 at 23°C. The mean egg deposition period was found to be 11-38 days within this temperature range. The egg deposition period becomes prolonged at low temperatures (10-13.5°C) (Noll, 1961; Johansen, 1997a), and is delayed or inhibited at temperatures higher than 30°C (Noll, 1961).

The eggs normally hatch in 6-14 days, and the larvae immediately start to feed on the leaves. Young larvae feed gregariously. In field experiments with white cabbage, Johansen (1997a) found that the larvae started to spread all over the host plant within a few hours after hatching. After 1-2 days they were found on the nearest neighbouring plants and rows, and they continued to disperse radially from the original infested plant throughout the larval stage. In the first three or four instars, the larvae feed mainly on the external leaves. From the fifth instar they display a negative phototaxis (Omino et al., 1973) and move into the heart of the plants. Nearly full-grown larvae are often concealed in the soil during daytime and enter the plants to feed at night. Larval development normally takes 4-7 weeks. Mature larvae leave the plants to pupate in thin cocoons in the soil at a depth of about 3-5 cm (Rygg and Kjos, 1975). Hibernation and aestivation take place in the pupal stage (Goto et al., 2001; Yamada et al. 2017).

Depending on the climate, M. brassicae has one to three generations per year. In Central Europe and most parts of southern Europe two or three generations occur, whereas in the northern parts of the distribution area M. brassicae is univoltine or partially bivoltine (Ogaard, 1983; Turnock and Carl, 1995). Skou (1991) states that two or three generations occur in Denmark. Degree-day calculations indicate that the species may be partly bivoltine in Denmark and Norway in warm years (Johansen, 1996b; Ogaard, 1983). In the UK, the species is also reported to be univoltine (Heath and Emmet, 1979) or partially bivoltine (Finch and Thompson, 1992). The species is bivoltine in Hokkaido in Japan (Tsutsui et al., 1988), Belgrade (Injac and Krnjajic, 1989), Moldova and other southern regions of the former USSR (Filippov, 1982), Germany (Hommes, 1983; Kahrer, 1984) and France (Poitout and Bues, 1982). The onset of the flight of the first generation in a growing season will vary according to the climatic conditions. In north-western Europe the first adults emerge in May-June (Finch and Thomson, 1992; Johansen, 1996a; Skou, 1991). In regions where M. brassicae is bivoltine, the adult flight of the first generation usually occurs in May-June and the second flight in August-September (see, for example, Poitout and Bues, 1982; Hommes, 1983). The flight period is often extended, and as a result, the generations will overlap in areas where more than one generation occurs. Thus, adults may be encountered throughout the growing season, with one to three more or less distinct peaks (see, for example Poitout and Bues, 1982; Hommes, 1983; Ogaard, 1983; Injac and Krnjajic, 1989). Flight and oviposition seem to be inhibited by heavy rainfall (Johansen, 1996b). Within a population, eggs are deposited over a period of several weeks. As a consequence, the age structure found on infested crops may consist of a mixture of eggs and different larval instars.

The longevity of the adults is approximately 23 days (Johansen et al., 2007).

The species is nocturnal (Heath and Emmet, 1979; Rojas et al., 2001), so emergence from pupae, flight, mating activity, egg deposition and feeding mostly take place during the dark period.

Mamestra brassicae larvae can be found in variable densities; in cole crops densities typically range between 0.1 and 0.7 larvae per plant (Cartea et al., 2009a; Hambäck et al., 2009; Bukovinszky et al., 2010).

According to Finch and Thompson (1992) the size of the adults is largely governed by the nutritional value of the host plant on which the larvae have been living.

The effect of temperature on development has been described by Ogaard (1983), Injac and Krjajic (1989) and Johansen (1997a). Johansen (1997a) and Ogaard (1983) have established lower developmental thresholds and thermal requirements for different developmental stages for a Norwegian and a Danish M. brassicae population, respectively. Mean developmental times were found to be 7.6-29.5 days for eggs, 39.8-98.3 days for larvae (temperature range 10.5-18.5°C), 18.2-96.9 days for pupae, and 3.3-9.4 days for the preoviposition period (temperature range 10.0-23.0°C) (Johansen, 1997a). Egg to adult development takes about 6 weeks at 25°C (Ogaard, 1983), 9 weeks at 20°C and 15 weeks at 15°C (Johansen, 1997a). The supercooling point of diapausing and non-diapausing pupae of M. brassicae has been found to be -20°C, but is reduced in contact with moisture (Tsutsui et al., 1988).

Diapause is facultative and occurs in the pupal stage; it is regulated mainly by temperature and photoperiod (Goto et al., 2001; Yamada et al., 2017). Winter diapause is induced by a function of low temperature and decreasing day length (Goto et al., 2001; Denlinger, 2002). In areas with hot and dry summers, a summer dormancy (aestivation) is induced by high temperature and a long photoperiod (see, for example, Poitout and Bues, 1982; Grüner and Sauer, 1988). The critical day length triggering winter diapause and aestivation is found to be about 14-16 h. The temperature affects the response level and critical day length (see, for example, Furunishi et al., 1982; Ogaard, 1983; Grüner and Sauer, 1988). However, the factors inducing diapause seem to differ according to the climatic zone. For example, in northern Russia, the diapause seems to be more dependent on temperature than day length (Bonnemaison, 1965). The time of adult eclosion from the pupal stage is mainly dependent on temperature (Tanaka et al., 2013).

Johansen (1997a) found that the weight of the pupae decreased with declining temperature during the larval period within the range 10.5-18.0°C. In laboratory experiments, larval mortality increased with decreasing temperature within the range 10.5-18.0°C and eggs and larvae did not survive at 8.5°C (Johansen, 1997a). In the field, mortality has often been found to be very high during the larval stage (Hommes, 1983; Johansen, 1996b; 1997b). Winter mortality was also found to be very high. The generation survival ratio was 0.0016-0.0041 over a 5-year period (Johansen, 1996b; 1997a, b). Life-tables for a Norwegian M. brassicae population on white cabbage have been constructed and analysed (Johansen, 1996b).

Cultural Control and Sanitary Methods

Damage to early cabbage can be reduced by early planting of the seedlings, so the development of marketable heads occurs before the mass emergence of larvae (Filippov, 1982).

Autumn ploughing has been found to increase winter mortality of M. brassicae pupae in Japan (Tsutsui et al., 1988); this is probably the result of factors such as increased predation, mechanical damage and exposure to low temperature. Filippov (1982) found that summer harrowing, ploughing after harvesting, and early autumn ploughing destroyed about 70-90% of the pupae.

Nets and fleeces prevent damage from M. brassicae provided there are no pupae in the soil when the crop covers are applied (Steene et al., 1992).

Intercropping has been found to decrease populations of M. brassicae in cabbage and Brussels sprouts (Theunissen and Ouden, 1980; Theunissen et al., 1992; 1995; Wiech, 1996; Finch and Kienegger, 1997; Brandsæter et al., 1998).

Host Plant Resistance

An Australian cauliflower line has been found to be resistant to infestation of M. brassicae in the Netherlands (Finch and Thompson, 1992). Different varieties of white and red cabbage and Savoy cabbage differ in susceptibility to M. brassicae; red cabbage has been found to be less infested with larvae than white cabbage and Savoy cabbage (Hommes, 1983). A red-foliaged variety of Brussels sprouts has also been found to show some resistance against M. brassicae (Dunn and Kempton, 1976). Some varieties of cabbage and kale have been identified as showing some resistance to M. brassicae (Cartea et al., 2009b; 2010). High glucosinolate content is a resistance factor that slows down the feeding and development of M. brassicae larvae (Badenes-Pérez and Cartea, 2021).

Biological Control

Mamestra brassicae has a wide range of natural enemies, but their effectiveness in suppressing this insect is variable. However, natural enemies may play an important role in population regulation, and measures that preserve and help the build-up of natural enemies should be integrated into pest management programmes and production practices. For instance, intercropping cabbage with different flowering crops has been found to increase the number of natural enemies (Theunissen et al., 1992). Only a few of the natural enemies of M. brassicae have been used commercially, such as the egg parasitoid Trichogramma. Different species of Trichogramma (e.g. Trichogramma evanescens, Trichogramma chilonis and Trichogramma dendrolimi) have been tested to control M. brassicae; a relatively high summer temperature and dense host population is required to achieve a high parasitization rate by these parasitoids (Finch and Thompson, 1992). The parasitization rates that can be achieved are variable, but rates of parasitism of up to almost 100% have been reported (see, for example, Filippov, 1982; Kahrer, 1984; Finch and Thompson, 1992). Other parasitoids that have been studied for biocontrol of M. brassicae include Eulophus pennicornis (Veire, 1993; Butaye and Degheele, 1995), Meteorus gyrator [Meteorus pendulus] (Smethurst et al., 2004), Microplitis mediator (Belz et al., 2014) and Telenomus laeviceps (Barloggio et al., 2019).

Mamestra brassicae larvae can be controlled by baculoviruses (Poitout and Bues, 1982; Geissler et al., 1991; Finch and Thompson, 1992) and Bacillus thuringiensis (Filippov, 1982; Ter-Simonjan et al., 1982; Terytze and Terytze, 1987; Collier et al., 1996). The bacterial or viral preparations should be applied when the larvae are small. Commercial products of B. thuringiensis and baculoviruses are available in some countries. Laboratory studies in France have indicated that the entomopathogenic fungi Paecilomyces fumosoroseus [Cordyceps fumosorosea] and Nomuraea rileyi are potentially valuable biological control agents (Maniania and Fargues, 1992). The entomopathogenic nematode Steinernema carpocapsae can also lower damage by M. brassicae larvae (Beck et al., 2012).

Chemical Control

In areas where two generations of M. brassicae occur during the growing season, several treatments with insecticides are often needed to control M. brassicae larvae (see, for example, Steene, 1994). In northern countries, where M. brassicae is univoltine, a single properly timed insecticide treatment may be sufficient (Finch and Thompson, 1992; Johansen, 1996a). In Belgium, insecticides are often applied to Brussels sprouts every 2-3 weeks to control M. brassicae larvae (Steene, 1994).

To be effective, insecticides must be applied when the larvae are small (less than 12-20 mm, first- to fourth-instar larvae) (Rygg and Kjos, 1975; Kahrer, 1984; Finch and Thompson, 1992). Older larvae bore into the heart of the plants and are protected from the treatment. Older larvae may also be more resistant to insecticides than younger larvae (Rygg and Kjos, 1975; Kahrer, 1984; Steene, 1994). Insecticides should be applied about 10 days after peak egg deposition (Kahrer, 1984). Thus, it is necessary to monitor the occurrence of M. brassicae (see Field Monitoring section below).

Insecticides currently in use are within the groups of organophosphates, pyrethroids, carbamates, organochlorines and insect growth regulators. Formulations of natural plant extracts have been tested and great attention has been paid to seed extracts from the neem tree (Azadirachta indica), which have shown promising results for the control of M. brassicae larvae (Schmutterer, 1985; Karelina et al., 1992; Mordue et al., 1993; Meadow and Seljåsen, 1996; Seljåsen and Meadow, 2006). Narrow-spectrum insecticides should be chosen when possible to preserve and encourage the build-up of natural enemies.

Timing of chemical and biological control tactics is essential to achieve a good control of M. brassicae, because insecticides and biological agents must be applied at the vulnerable stage. Temperature-dependent development and the lack of synchrony of the different life stages make precise timing difficult.

Pheromone traps can be used to detect and monitor the populations of the insect (see, for example, Terytze and Adam, 1981; Poitout and Bues, 1982; Hommes, 1983; Veire and Dirinck, 1986; Terytze et al., 1987; Bues et al., 1988; Injac and Krnjajic, 1989; Johansen, 1996a). Light traps can be used to monitor the flight of M. brassicae (Hommes, 1983; Injac and Krnjajic, 1989). The adults are also attracted to sugar (Skou, 1991). Sex pheromone traps have been found to be more effective than light traps in catching the first adults of the first generation (Injac and Krnjajic, 1989). Sex pheromone dispensers and traps are commercially available.

A degree-day model for the prediction of field occurrence of adults, eggs and small larvae, and favourable spraying time has been developed (Johansen, 1996a). The prediction model is implemented as a voice board response system for prognosis and advice for growers in Norway.

Hommes (1983) developed preliminary action thresholds for the different developmental stages of M. brassicae. Damage thresholds for injurious lepidopterous larvae on cabbage have been used in several European countries (Hommes et al., 1988).