Ephestia kuehniella
(Mediterranean flour moth)

E. kuehniella is a cosmopolitan pest, being spread all over the world by international trade.

It occurs especially in warm, temperate areas, but is also common in cold, temperate areas and can occur in the tropics.

In the past, there have been several disputes over the origin of this species. Richards and Thompson (1932) discussed in detail the uncertainty in origin of this pest. Turkey may be the centre of dispersion: Asia Minor has 18 species of Ephestia (out of 60 classified). Danysz (1893) asserted that E. kuehniella had been known in French mills since 1840 and described it as 'cosmopolitan'. E. kuehniella is an anthropophilic species: after adaptation it has come to live closer to humans.

E. kuehniella is found primarily in flour mills and bakeries. It is also found in farmhouses, warehouses, stores and bilges (in ships in quarantine), including coarse canvas covers and maize sacks.

E. kuehniella is a storage pest that affects many cereals, including wheat (grain, bran, flour, meal, semolina), maize, rice, sorghum, oats and barley. It also attacks nuts (e.g. almonds), date palms, carob pods, fruits and flowers, pollen, leaves, roots (dried), biscuits, human food and animal feed.

This pest attacks after harvesting, on and in the spaces between stored grains, seeds, decorticated or split fruits and dried flowers and, in general, on nutritious substrates which remain in the fields or which are close to human habitation, farms or storage sheds.

Mating

A virgin (or insufficiently fertilized) female adopts the calling position, extending her ovipositor and raising her abdomen. This position, which enables her to emit pheromones, can be taken up again over several days (Daumal, 1987). The males 'take to the air' to look for a mate and perform a courtship display. Mating takes place within a few seconds (Traynier, 1968, 1970; Traynier and Wright, 1972), and usually lasts for 4-5 hours after dusk, but may continue for longer than this. Various abiotic factors may have caused sterility in the males, even if one or more spermatophores has been emitted (Raichoudhury, 1936; Tavares and Daumal, 1983; Daumal, 1987). The biotic potential of the females is not affected by the same factors. During mating the female's wings cover those of the male. When mating is complete the female no longer adopts the calling position, because a successful mating enables her to fulfil her entire reproductive potential, 6-10 hours after (or without) separation of the partners. The male, however, can fertilize five to six females during his life, although the later matings (over 6-8 days at 20°C) become increasingly less fertile (Norris, 1932, 1933, 1934; Williams, 1938).

During the day the adults remain immobile, with the antennae folded on the thorax, concealed under the wings, and the first pair of legs resting on the raised thorax (akinesis) (Sogaard-Andersen, 1968). The moths fly after dusk, with nocturnal movements ceasing before dawn; males possess a peak in activity just prior to sunrise (Edwards, 1962). The lifespan of the adults varies greatly. They can live for approximately 20 days if they do not find a mate, and for longer than this at low temperatures (10-18°C), providing that they have access to liquid feed sources (such as condensation, or fruit exudations). They tend to stay in shaded areas and almost always close to the highest thermal gradients (such as ceilings and flour-mill outlets). Emergence takes place from 17.00 to 22.00 h. Stretching and drying of the wings lasts for an average of 2 hours after the extension of the proboscis.

Egg Laying

The females are stimulated by flour and other dusts, such as talcum powder (Ullyett, 1945). The female can gather heaps of dust into fissures and then place eggs on them. Firstly the tips of the antennae and simultaneously the ovipositor become active when inserted into fissures. The combination of these two stimuli leads her to slide particles into the fissures, using the setae on the papillae of the ovipositor and movements of the abdomen, before laying eggs in the fissures in rows. The eggs may, however, also be scattered apparently at random. This behaviour is not heritable for a given population (Daumal, 1987, 1994). The structure, role and distribution of the setae of the antennae, of the tarsi and of the sensillae of the ovipositor have been studied by Anderson and Hallberg (1990). The females lay approximately 75% of their eggs in 48 hours, at 20-23°C. Females are deterred by high densities of larvae (Anderson and Löfqvist, 1996). The influence of light cycle and circadian rhythm on oviposition in E. kuehniella has been studied by Bell (1981).

Fecundity

Most authors have noted the wide variation in biotic potential of this species: the number of offspring can range from 50 to 500 (Richards and Thomson, 1932). This variation may be attributable to genetic (Robinson, 1971; Leibenguth and Russell, 1986) or epigenetic factors (Daumal and Pintureau, 1985; Daumal and Boinel, 1994a). At emergence, females have eight ovarian sheaths, the content (chorionic oocytes during yolk formation, oogonia, atresia, the presence of corpora lutea) and length of each of which are a reflection of both the larval life of the female (quiescences, fasts, nutritional deficiencies, movements and competitiveness) and her genome. The pathogenic or physiological state of the male and female and conditions during mating will further affect the number of offspring. Male moths maintained under continuous illumination have a much lower reproductive capacity than males maintained under alternating light conditions (Riemann and Ruud, 1974).

Eggs and Embryonic Development

The eggs (centrolecithal egg: 0.028 mg) are laid singly or close together. They adhere to the substrate because they are coated with secretions from the neck glands. The structure of the chorion (Arbogast et al., 1980) and the remarkable resistance of the eggs to abiotic factors also constitute, at this stage of development, good scope for adaptation in this species (Daumal et al., 1974; Daumal and Boinel, 1994a, 1994b). Embryonic development takes 8 days at a constant 20°C. The lower heat threshold for development from primary division is 8°C (with 16 h light and 8 h dark cycle), and the upper heat threshold at this stage is 35°C (90% RH). These thresholds vary according to the developmental stage. Embryonic development was studied by Sehl (1931) and subsequently by Hawlitzky (1972).

Post-Embryonic Development

E. kuehniella has only a few hours of autonomy in its first stage after ingestion of the serous membrane. This is the most vulnerable stage (Daumal, 1987). Because development is heterogeneous, it is difficult to establish a precise duration: if a caterpillar deviates even slightly from the typical cycle described below, it may extend or even accelerate its development period (Daumal et al., 1981 a, b; Daumal and Pintureau, 1985). As an example, the complete cycle, from egg-laying to adult emergence, will take place within 60 days at 20°C for individuals fed exclusively on hard wheat semolina. Numerous studies have been carried out in this area, and all have demonstrated the plasticity of development of the five larval stages. This plasticity is due primarily to the polymorphism of the species, to the origin of the strain (Cox et al., 1981), and to a significant number of epigenetic factors which may or may not contribute to the expression of numerous pleiotropic genes.

Larval and Pre-Pupal Development and Behaviour

From hatching to pupation, the caterpillar of E. kuehniella exhibits a stereotypical and completely solitary behaviour which may be summarized as follows:

The first-instar larva immediately shows negative phototaxis and isolates itself in a woven network even before starting to feed. It only emerges to pick up dust particles of flour or semolina - which it incorporates into this network of silk threads. It takes its first feeds within this network, which it continuously adds to, thus forming its nutritional case. This behaviour continues throughout the four subsequent larval instars, during which the exterior of the case is extended and enriched with various types of food and non-food particles. The caterpillar remains in contact with the interior network by means of the setae on the cuticle. The hooks on the coronate legs stabilize the body during moulting (exuviation).

Aerotaxis behaviour may be observed from the fourth instar: the caterpillar taking measurements of space by swinging and stretching its thoracic segments. This behaviour is clearly marked during the fifth instar: measurement-taking is accentuated after the caterpillar stops feeding and starts to construct the first pupation cocoon. The measurement enables the pest to establish the amount of space available above the cocoon: it will enable the imago to stretch its wings shortly after emerging from the second pupation cocoon (Daumal et al., 1985; Daumal, 1987). This behaviour is exhibited on any ground-level area, but always occurs in the darkest part of the area. The study of this stereotypical behaviour has served as the basis for intensive breeding of E. kuehniella for production of biological control agents (Daumal et al., 1975).

The dispersion of the different stages, and particularly of the fifth-instar larvae, which might appear to indicate negative geotaxis-type behaviour in warehouses or flour mills, is in fact only deterrence behaviour (when there is a high degree of competition in an area), or reactions to the discovery of a light and heat gradient.`Flight'-type behaviour is exhibited when the caterpillar is parasitized by a microbial agent or by an endoparasite which causes it to deviate from its normal behaviour. It should also be noted that the aggressive `cannibal' behaviour in situations where there is a high population density, described by various authors, is not a biological reality: the caterpillars competing for a case or a territory only `deter' each other by advancing and retreating, and following an excess of secretions from the mandibles some caterpillars abandon their territory. At high population densities (particularly in overcrowded laboratory production systems), an excess of secretions from older caterpillars can also lead to death by poisoning of younger first- and second-instar caterpillars. Nonetheless, particularly in flour mills, a series of cocoons may be discovered, in which fifth-instar larvae are living among fragments of parasitized or healthy pupae or pro-pupae which they have partially devoured while the pupae were in an inactive, immobile state. These fifth-instar larvae may, in their turn, be displaced by another healthy or parasitized specimen seeking to use their niche (J Daumal, INRA Laboratoire de Biologie des Invertébrés, Antibes, France, personal communication, 1996).

Information on developmental times in relation to temperature and humidity are given by Siddiqui and Barlow (1973), Bell (1975) and Jacob and Cox (1977). The effect of cultural factors on development can be found in Bell(1976) and Cerutti et al. (1992). Some earlier studies are referred to in Richards and Thomson (1932) and information on the development of the eggs in relation to temperature can be found in Voute (1936). A simulation model on the population dynamics of E. kuehniella has been presented by Skovgård et al. (1999).

Diapause

According to Cox et al. (1981) diapause in E. kuehniella is recognized as a delay in development between cessation of feeding and the start of pupation. Diapause is influenced by the strain and nutrition as well as by temperature and photoperiod (Cole and Cox, 1981; Cox et al., 1981, 1984a; Cox, 1987). Diapause increased the tolerance of larvae to fumigants at low temperature (Cox et al., 1984b). High temperature and darkness during larvae development, conditions common in flour mills, will result in a high number of diapausing larvae (Cox et al., 1981).

Note: the natural enemies listed occur in the `natural' conditions of flour mills or warehouses

Cocoons of E. kuehniella may contain solitary larvo-pupal parasitoid Hymenoptera such as Venturia canescens. When cocoons are pinkish-white, measure 1.8-2 mm and are found in groups of five to ten near larval exuviae, they are infected by the exoparasitoid Bracon hebetor. Third-instar larvae are sometimes attacked by Apanteles sp.

The pupae may also contain Diadegma chrysostictos, a solitary endoparasitoid. It should also be noted that fourth- or fifth-instar E. kuehniella larvae which are seeking a place for moulting or pupation may devour healthy or parasitized pupae of their own species.

When brown carcasses of the third- to fifth-instar caterpillars are found outside the cocoons, this may indicate an infection by the endocellular protozoan Mattesia dispora. When the caterpillars are infected before the fifth instar, they will eventually shrivel up and die (the cuticle turning red in colour), but they may survive for a considerable time. Examination of the larvae haemolymph under high binocular magnification against a black background will show a large quantity of diamond-shaped refractive particles, which are characteristic of the complete invasion of the caterpillar's cells by the spores of M. dispora. This protozoan often infests laboratory cultures, but procedures have been described which take care of the problem (Hansen et al., 1999).

Very black fifth-instar larva carcasses indicate an earlier infection by the bacterium Bacillus thuringiensis (e.g. in dried fruits) or by other entomopathogens which are difficult to identify because of the condition of the tissues.

Eggs may be parasitized by Trichogramma spp., particularly in stored food products, causing the healthy eggs (white to pinkish-beige in colour) to turn completely black. Eggs will also be attacked and sucked out by the predatory mite Blattisocius tarsalis. The eggs may also be sucked by acarids or by reduviids or anthocorids in warehouses where dried fruits are stored.

Predators include: anthocorids, reduviids, Psocoptera, spiders, acarids and pyemotids. Birds and bats may eat caterpillars, cocoons and adults.

Some records of natural enemies are given by Richards and Thomson (1932), Abdel Rahman et al. (1977) and Gordh and Hartman (1991).

Adults

Adults may be caught in light traps, or in pheromone traps placed in warehouses, flour mills or shops (Fleurat-Lessard, 1986). Identification may be confirmed by examination of the male genitalia.

In flour mills the adults are often to be seen at rest on walls, especially in the warmer parts of the mill.

After the identification of the female sex pheromone components in E. kuehniella in the 1970s, one of the components (Z,E)-9,12-Tetradecadienyl acetate (ZETA or TDA), has been used for monitoring (Trematerra, 1994a). Commercial pheromone traps are now used in many modern industrial flour mills as an effective tool in the early detection of pest problems. Research on pheromones in mass-trapping, mating disruption and as attracticides have been conducted in industrial flour mills (Trematerra, 1994a, b). Some positive results have been obtained, but the effect have been influenced by other factors such as cleaning routines. One of the main limitations on the use of pheromone traps is that only males are caught and that the numbers caught over a period will be a relative estimate of population size, certainly reflecting activity as well (Nielsen, 2000a). The use of pheromone traps has demonstrated that male E. kuehniella fly out of doors (Wohlgemuth et al., 1987; Nielsen 2000b).

Larvae and Pupae

Larvae and pupae may be detected by a visual examination of the various cracks in ceilings and discharge outlets, of the corners of walls, and under tracks or runners of equipment that is mobile but which includes dark areas. The covers and casing of all equipment, if they have any type of slit, may contain larvae and pupae. Clusters of silk may be detected with cocoons, containing caterpillars at different stages or their exuviae (head capsule) or carcasses. Pupae are protected by a double cocoon. The external cocoon is composed of a variety of dejecta.

Eggs

Eaggs of E. kuehniella are very difficult to detect under natural conditions. The eggs may be concealed in old cocoons near flour dust or scattered in any shaded location where only traces of such dust remain. The eggs are particularly resistant to abiotic factors such as high or low temperatures or humidity levels, or mechanical disturbances. If situated in flour, the eggs can be detected by passing the flour through a sieve with a mesh size of 200 µm.

(See also Symptoms.)

For flour and semolina

Pyralis farinalis caterpillars may be found in the same habitat as E. kuehniella: they are detitrivorous and often found in dark, humid areas in flour warehouses. They appear different, however: P. farinalis caterpillars have blackish cuticles, whereas E. kuehniella have pink or whitish cuticles. The P. farinalis imago has a wing-span of 28-30 mm and is yellow and brown with white lunulae.

For stored fruits and dried fruits

E. kuehniella may also be confused with Cadra cautella, Cadra figulilella, Plodia interpunctella, Ephestia elutella, Ectomyelois ceratoniae [Apomyelois ceratoniae] or Paramyelois transitella [Apomyelois transitella]. Imagos of Ephestia sp. and Ectomyelois sp., which often have the same habitat (dried fruits), can be confused: the species can be distinguished by examining the genitalia of both sexes. These species are all of similar shape, and when worn, specimens are difficult to distinguish from each other.

Corcyra cephalonica is also superficially similar.

Due to the variable regulations around (de)registration of pesticides, your national list of registered pesticides or relevant authority should be consulted to determine which products are legally allowed for use in your country when considering chemical control. Pesticides should always be used in a lawful manner, consistent with the product's label.

For large volumes of produce, disinfestation should be carried out in accordance with the standards of the various countries.

This banning of methyl bromide has increased research activity to finding new and alternative methods for control of E. kuehniella which can be adopted in the future. Many of the alternatives can only be expected to function in IPM systems (Taylor, 1999).

Biological control methods are expected to become an important component of IPM strategies for many types of stored commodities (Brower et al., 1996; Schöller, 1998). Promising results have been obtained with Trichogramma species (Schöller et al., 1996; Prozell and Schöller, 1997, 1998; Hansen, 2000) and Blattisocius tarsalis (Nielsen, 1998a, 1999a, b). Habrobracon hebetor is another potentially useful species in this area (Schöller and Prozell, 2000).

Disinfestation and cleaning of warehouses before they are used for storage are effective but costly measures. In France, the INRA research stations at Bordeaux and Antibes are researching this area and considering control measures using trichogrammatids, braconids and predators.

E. kuehniella are intensively bred as a basis for the commercial production of various parasitoids and predators to combat pests such as Lepidoptera and aphids (Wajnberg and Hassan, 1994).

Diatomaceous earth can be used against E. kuehniella (Trewin and Reichmuth, 1997; Nielsen, 1998b). The efficacy of diatomaceous earth is generally improved at higher temperatures (Fields and Korunic, 2000) and these products can be combined with heat treatment of food processing facilities (Fields et al., 1997).