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The apple leaf curling midge, Dasineura mali, is a species of gall midge belonging to the family Cecidomyiidae within the order Diptera. It is known as the Apple Leaf Curling Midge, Apple leaf midge [English] , Cécidomyie du pommier [French] , Appelbladgalmug [Dutch] , and Apfelblattgallen [German].

As a member of the family Cecidomyiidae, D. mali is grouped with other gall midges, a diverse selection of very small flies of which some are known for their ability to induce gall formation on host plants.

Description
D. mali is a minute and delicate species of dipteran, belonging to the family Cecidomyiidae. Adults measure between 2 to 3 millimetres in length. Identifying features include the long moniliform antennae with whorls of fine hairs, used for sensory perception and navigation in their environment. They have small simple eyes (ocelli) aiding in light detection and orientation. Wings appear fringed with fine hairs, displaying few longitudinal veins and lacking obvious cross veins, contributing to their fragile appearance.

Coxae are not elongated, and their tibiae lack spurs, distinguishing them from related species. Tibiae provide support and stability during movement. Larvae with red or orange hues are characteristic of D. mali, though differentiation from other species can be challenging, as larvae may also exhibit a yellow or white colour. To identify D. mali larvae, the length of setose papillae on the first thoracic segment and the shape of the sternal spatula are measured. Larval characteristics include small heads with pigment spots but no eyes. The body has thirteen visible trunk segments and nine pairs of spiracles on the prothorax and first eight abdominal segments, facilitating respiration during development. The sternal spatula, a mid-ventral structure on the thorax, is a distinguishing feature of D. mali larvae within the Cecidomyiidae family.

Natural global range
D. mali originated in the Palaearctic region, where it evolved alongside its primary host, the apple (Malus domestica). Accidental introductions to new regions expanded its distribution, reaching North America and New Zealand. These introductions provided opportunities for D. mali to establish populations beyond its native range.

Spreading into three specific areas of the world: Europe, America, and New Zealand, D. mali prefers host plants belonging to the Rosaceae family, which includes apples, peaches, pears and cherries. In North America, insects that initially fed on wild relatives of these host plants, such as native roses, may have gradually adapted to cultivated apple trees. The historical association between D. mali and the wild species within the Rosaceae family, facilitates its transition to cultivated apple trees as its primary host.

New Zealand range
The introduction of the Apple leaf curling midge into New Zealand occurred in 1950, marking its establishment as a secondary pest primarily controlled by broad-spectrum insecticides targeted at key pests. Regions for apple production, such as Hawke's Bay, serve as significant habitats for this species with high levels of apple and pear cultivation. Hawke's Bay, often referred to as the fruit bowl of New Zealand, offers a diverse range of apple varieties, stone fruits, and soft fruits. Nelson is New Zealand's oldest apple-growing region. The establishment of Apple leaf curling midge in Nelson would present significant challenges for the industry, as this invasive pest induces the formation of galls on host leaves. Otago serves as the southern most apple-growing area in New Zealand. With a rich history in orcharding, Otago contributes significantly to the country's export crop production. Although current inaturalist observations may not fully support the presence of Apple leaf curling midge in New Zealand's apple orchards, the species' close affinity with these environments suggests the potential for its establishment.

Habitat
Apples (Malus domestica) have a rich botanical and cultural history, with archaeological evidence suggesting their cultivation dates back thousands of years. As one of the most widely cultivated fruit species, apples have undergone centuries of selective breeding, resulting in a diverse array of cultivars. Apple orchards are the ideal habitat for D. mali, given their close association with cultivated apple trees. D. mali, is an established pest of apple trees in New Zealand. Apple trees offer ample food resources for D. mali larvae, while the managed nature of orchards provides shelter and protection from natural predators and adverse environmental conditions. The larval feeding gall inducing behaviour leads to the characteristic symptom of rolled or twisted leaves on apple trees. Mature larvae seeking pupation sites may contaminate fruit with pupal cocoons, posing concerns for fresh fruit quality and quarantine.

Life cycle and phenology
D. mali undergoes four generations yearly in most of New Zealand from early spring to mid-autumn. In Central Otago, there are typically three or four generations based on summer temperatures. Adults emerge from soil litter, immediately mate, and lay eggs on growing shoots. Larvae develop within tightly rolled leaves for 2–3 weeks, protected from insecticides. Mature larvae pupate in the ground and sheltered locations. Overwintering as mature larvae in the soil is common among successive generations.

The life cycle of D. mali begins with females laying their eggs on growing shoot tips of the host plant. The eggs incubate for 3-5 days, which is influenced by the temperature. When larvae emerge they feed on the young leaves of the host plant. Feeding induces the formation of leaf galls on the outer edges of the leaves, providing a protective tent for larval development. As the larvae mature, they exit the leaf galls and descend to the soil, where they undergo pupation. D. mali exhibit distinct seasonal patterns, with larvae from the late third generation and all individuals in the fourth generation undergoing overwintering. During the winter months, these larvae persist in their larval stage, awaiting the onset of spring. It is during the early spring, typically in early September, that overwintering larvae undergo pupation.

Researchers examined egg-laying behaviour by randomly collecting D. mali eggs from different host trees during the oviposition peaks of the first, second, and third generations. These eggs were then transported to the laboratory for further examination. The investigation of D. mali's phenology revealed a seasonal pattern.

Over two consecutive years, researchers gathered mature larvae of D. mali to study developmental stages, representing multiple generations. As the season advanced, researchers noticed that changes in environmental factors, such as the availability of suitable egg-laying sites and dry weather, influenced the behaviour of egg-laying. .

The transition from eggs to the end of the white larval stage typically spans 6–27 days, with later generations of the apple leaf curling midge exhibiting quicker development. 80% of plants enclosed with D. mali displayed eggs within two days, followed by the appearance of leaf galls within 4–5 days.

Diet and foraging
Gall midges are the richest group of gall-inducing arthropods in Europe and in the world. Phytophagous larvae of gall midges cause galls on all organs of host plants: on stems or twigs, on terminal or axial leaf buds, flower buds, leaves, flowers, fruits and roots. Gall midges that include the D. mali represents one of the most diverse groups of gall-inducing arthropods worldwide. Members of the Rosaceae family, including apples, peaches, pears, and cherries, are preferred hosts for D. mali. In North America, insects originally feeding on wild relatives of these crops, like native roses, may have transitioned to cultivated apple trees over time.

Within the Rosaceae family, to which apple trees belong, D. mali larvae are known to be monophagous, meaning they exclusively feed on plants within this botanical family. Specifically, they target cultivated varieties like Malus domestica (domestic apple) as well as wild species such as Malus sylvestris (European crab apple). From stems and twigs to terminal or axial leaf buds, flower buds, leaves, flowers, fruits, and roots, gall midge larvae demonstrate an impressive ability to induce gall formation across all parts of their host plants.

Predators, parasites, and diseases
D. mali, inflicts damage upon apple trees by inducing the formation of leaf galls. The galls disrupt the normal growth and development of affected foliage, potentially leading to diminished fruit yields and compromised tree health. The discovery of a new species closely associated with D. mali has encouraged scientific interest. Macrolabis mali, has been observed across a geographical range extending from South Tyrol to southwestern Germany. Researchers hypothesise that M. mali may function as an inquiline insect within the nests of D. mali, suggesting a potential ecological relationship between the two species. . The predatory mirid bug, Sejanus albisignata is also a player in the ecological balance of apple orchards and has been observed feeding on eggs of the D. mali. This feeding activity is a natural biocontrol mechanism suppressing pest populations and reducing damage to apple crops.

Other information
The adult D. mali is a small fly, typically measuring only a few millimeters in length. The larvae, which are the stage responsible for causing damage to apple trees, are tiny and maggot-like. The recent identification of the sex pheromone of the D. mali opens the door to the development of innovative monitoring techniques aimed at detecting and controlling D. mali populations more effectively. By synthesising the sex pheromone, researchers can create specialised traps or attractants that target male D. mali individuals, allowing accurate monitoring of populations. Pheromone-based strategies holds promise for integrated pest management approaches, offering environmentally friendly alternatives to conventional insecticide treatments.

Figure 2. Apple production in China 2022



M. domestica is widely cultivated globally with China being the world's largest apple producer. Figure 2 illustrates the apple production in China for the year 2022. With extensive exports and significant acreage dedicated to apple cultivation around the world, the threat of disrupted export markets and heightened production costs could become a reality. California growers, for example, export apples to 27 countries and maintain over 14,000 acres dedicated to apple production, valued at over $105 million.

While mature orchard yields may not be significantly affected, reduced fruit size and bud formation could occur, impacting newly planted trees and nursery stock.