Anagyrus pseudococci — Parasitoid wasp

Anagyrus pseudococci is a well-known parasitoid wasp in the family Encyrtidae. It is capable of developing on a variety of species of mealybugs (Planococcus spp. and Pseudococcus spp., Hemiptera: Sternorrhyncha: Pseudococcidae). Entomophage is used in biological control programs and is the most commercially common parasitoid bred to control mealybug. By its nature, it is an internal parasitoid. Females lay one egg each in the host’s body, in which development takes place up to the imago stage.

Synonymy

Joseph-Etienne Girault originally described it as Epidinocarsis pseudococci.

Distribution

The natural habitat of Anagyrus includes countries such as China, Cyprus, Italy, Israel, Saudi Arabia and CIS countries (including former USSR countries). In 1934, it was introduced to Argentina, Brazil, South Africa and the USA, in order to suppress colonies of mealybug infecting citrus fruits and grapes (Planococcus citri (Risso)). In the USA, it was necessary to import Anagyrus repeatedly. Re-importation was carried out to California from South America in 1953, after which it became widespread in the United States, especially in the states engaged in winemaking. The species is widespread and popular in California and is used for biological control of the invasive vine mealybug (Planococcus ficus).

Its documented distribution correlates with the areas of viticulture and citrus cultivation. Documented locations include Argentina, where it was imported using grape seedlings from Italy, Uzbekistan to control Planococcus citri, South Africa and Turkey to control Planococcus citri on citrus fruits. The use of entomophage as a biocontrol agent in greenhouses began relatively recently — 1994. During the use of Anagyrus pseudococci, they proved to be an effective method of suppressing mealybug. Entomophage is especially popular in greenhouses in Europe and the USA.

Description

Egg: Yellow-white eggs, measuring 0.24 × 0.15 mm. The insertion of the ovipositor usually occurs on the dorsal side near the edge of the victim’s body. A day after the introduction of the egg, a black scar forms on the host, at the place of attachment. The egg is attached to the host’s body with the help of a “rod”. Part of the core of the egg will appear through the exoskeleton of the mealybug and is visible from the outside.

Larvae: The larvae of the parasitoid wasp are white, and pass five instars.

The first and second instars are transparent to pale white and with light brown sclerotized mouthparts. These age groups remain attached to the host’s integument with the help of the egg shaft. The third and fourth instars (hymenopteran in shape) are white, with well-developed mandibles. The connection with the core of the egg is broken by the fourth age.

The fifth stage occupies most of the body of the mummified host and consists of 13 segments. A dark brown faecal mass in the anterior part of the host is visible at the end of the last larval stage.

Pupae: The pupae face their anterior part towards the posterior end of the mummified hosts. Their size is 1.4-2.1 mm (females) and 1.1-1.4 mm (males). The pupae are similar in colour to adults — the orange-brown colour of the female, and the male pupae are black, like adult males.

Imago: Adult individuals have pronounced sexual dimorphism

The size of the females is 1.5–2.0 mm (the smallest recorded value was 0.75 mm). The colour ranges from dull orange to brownish with a yellow triangular head. The lower part of the head has dark brown markings. The antennae have distinct black and white stripes; the first segment has the basal half black, and the distal part is white. The sixth segment is slightly longer and wider. They have a complex structure of gray-brown eyes with a pink faceted eye. The legs are white to yellowish, with a dark pelvic part and thighs on the distal surfaces. The wings are transparent with brown streaks. The ovipositor is short and slightly convex.

Males of Anagyrus pseudococci differ from females in size, head structure, antennae, wings, and abdomen. Adult males are smaller than females 0.71–1.25 mm and mostly black. The lower part of the head is covered with noticeable silvery bristles forming lines. The antennae of the parasitoid wasp have a white colour near the junction with the head (scapus). The coxas, like the body, are black, but the rest of the legs are white with a yellow tinge. The abdomen is shorter than the thorax. The head is flatter than that of the female. The antenna is 9-segmented, threadlike, with a triangular pedicel. Compound eyes of male are smaller than of female, and are reddish-brown rather than gray. Compound eye, are also pink.

Life cycle

Egg: Females of Anagyrus pseudococci lay one egg (which will develop inside the victim) in the host, which makes it a single endoparasitoid. Even if several eggs are laid in one host, only one develops anyway. The egg-laying of the entomophage lasts 15-40 seconds. Females of Anagyrus pseudococci lay eggs between wax threads on the lateral edge of the body of the mealybug. Oviposition can occur both inside the nymphs of the mealybug and inside the adults, but larger hosts are preferred.

Egg development takes 1-2 days at 28 °C. The optimal temperature for egg development is about 25 °C, but development can also occur in the range of 14 °C — 34 °C. The air temperature will affect the life cycle duration.

Larvae: The larvae of the parasitoid wasp are white and fully develop inside the host. Development includes 5 ages. Parasitized mealybugs do not die and remain motile during the first and second instars of the larva of Anagyrus pseudococci. Immobilization of the worm occurs when the entomophage reaches the 3rd larval stage. Development to the 3rd age and immobilization of the host occur by the fifth day at 28-32 °C. The third age lasts about one day. Development to the fifth stage takes 6-8 days at 32 °C and 4-5 days at 28 °C, with an additional day for pre-pupal development. The host is completely mummified by the eighth day at 28 °C and acquires a yellow-brown colour.

The life cycle duration decreases when the temperature rises to 34 °C. So the development time at 14 °C was 79.3 ± 3.3 days, while at 34 °C it was only 10.5 ± 0.7 days. At 35 °C, the development of the entomophage stops, and death occurs at 40 °C. The lower temperature threshold is 14 °C. Although development may stop at slightly higher temperatures, Anagyrus pseudococci are able to survive short periods of exposure to high or low temperatures.

Pupae: Pupation takes place inside the mummified host and lasts approximately 4 days at 32 °C or 4-6 days at 28 °C. At 32 °C, pupae were detected as early as 8-11 days after egg laying in the body of the hosts.

Imago: Adults appear through an irregular exit hole, which they gnaw through at the rear end of the body of a mummified mealybug. Already 12 days after laying eggs, you can expect the appearance of an imago. The development time of Anagyrus pseudococci females ranges from 14 to 18 days, and the development time of males ranges from 12 to 27 days.

Anagyrus pseudococci is characterized by a form of parthenogenesis. Females lay unfertilized eggs that develop into males and fertilized eggs that develop into females. Females do not need to mate to lay eggs. Females begin laying eggs 48 hours after emergence and continue until death. Adult females that lay fertilized eggs have higher fertility than females that lay unfertilized ones. The number of offspring and the proportion of females depends on the age and size of the host. Females appear from adult and large victims, and males from small ones.

The average life expectancy of the imago ranges from 6.9 ± 1.2 days to 8.2 ± 1.3 days. Adults feed on nectar and carrion. The imago mortality rate does not depend on the humidity level.

The hosts are victims

The registered hosts of Anagyrus pseudococci include numerous mealybugs — Pseudococcus citriculus, Planococcus citri, long-tailed mealybug (Pseudococcus longispinus), Comstock mealybug (Pseudococcus comstocki (Kuwana)), pink (hibiscus) mealybug (Maconellicoccus hirsutus), cassava mealybug (Phenacoccus manihoti), Phenacoccus herreni, Pseudococcus mealybugs.

Larvae developing in the nymphs of the citrus mealybug of the third instar demonstrated a development time comparable to larvae developing in adult hosts. However, adult mealybugs are the best host for potential fertility and produce significantly more adult female parasitoid wasps.

Economic significance

Anagyrus pseudococci is economically important as a means of biological control of mealybugs, pests of agriculture in closed ground, as well as for the control of citrus mealybug in its native range in Italy and Israel. This entomophage is usually used against grape and citrus mealybug. The grape mealybug is of high economic importance because it infects wine grapes and uses various weeds as alternative hosts. Citrus mealybugs are the main pests of citrus fruits, but their host range includes at least 27 different plant families, including economically significant ornamental plants, vegetables, and fruits.

Anagyrus pseudococci are the most effective parasitoids against the mealybug of grapes. The development is faster than that of other parasitoids used to fight mealybugs at all temperatures.

The timing of the parasitoid wasp’s release is very critical for improving the effectiveness of biological control programs against mealybug. It is necessary to calculate the entomophage release time so that it coincides with the preferred temperatures for the best control. The presence of ants will reduce the effectiveness of the bioagent, therefore, in order to achieve the best results, their population should be monitored.

It is recommended to use the parasitoid wasp in orchards, vineyards and protected crops in combination with the ladybird Cryptolaemus montrouzieri for the most effective control.