Leucoptera malifoliella (pear leaf blister moth)
- Summary of Invasiveness
- Taxonomic Tree
- Notes on Taxonomy and Nomenclature
- Distribution Table
- Risk of Introduction
- Hosts/Species Affected
- Host Plants and Other Plants Affected
- List of Symptoms/Signs
- Biology and Ecology
- Natural enemies
- Notes on Natural Enemies
- Means of Movement and Dispersal
- Plant Trade
- Similarities to Other Species/Conditions
- Prevention and Control
- Links to Websites
- Distribution Maps
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PicturesTop of page
IdentityTop of page
Preferred Scientific Name
- Leucoptera malifoliella Costa (1836)
Preferred Common Name
- pear leaf blister moth
Other Scientific Names
- Cemiostoma scitella Zeller (1848)
- Elachista malifoliella Costa
- Leucoptera scitella Zeller (1839)
- Opostega scitella Zeller (1839)
International Common Names
- English: apple leaf miner; pear leaf miner; pear leaf, blister moth; ribbed apple leaf miner
- Spanish: minadora; minadora de hojas
- French: cémiostome du pommier; mineuse cerclée; mineuse des feuilles du poirier; mineuse des feuilles du pommier
- Russian: boiariishnikovaia kruzkovaia mol; mol plodovaia krugominiruiushaia
- Portuguese: cemiostoma da macieira
Local Common Names
- Belgium: damschijfmineermot
- Bulgaria: kruglominirast molec
- Czech Republic: podkopnícek spirálový
- Denmark: cirkelminermol
- Germany: Fleckenminiermotte; Glattkopfmotte; Glattkopfmotte, Kernobst-; Kernobstminiermotte; Miniermotte, Flecken-; Miniermotte, Obstbaum-; Miniermotte, Pfennig-; Münzenminiermotte; Obstbaumminiermotte; Pfennigminiermotte
- Hungary: lombosfa fehérmoly
- Italy: cemiostoma o minatrice concentrica del melo; Minatrice delle foglie del melo; Minatrice delle foglie del pero
- Netherlands: Appeldamschijfmot; Damschijfmineerrups
- Norway: sirkelminermoll
- Slovenia: sadni listni duplinar
- Sweden: cirkelminerarmal
- LEUCSC (Leucoptera malifoliella)
Summary of InvasivenessTop of page L. malifoliella has many hosts and is capable of successful spread in new regions such as North and South America, Australia and even southern Africa.
Taxonomic TreeTop of page
- Domain: Eukaryota
- Kingdom: Metazoa
- Phylum: Arthropoda
- Subphylum: Uniramia
- Class: Insecta
- Order: Lepidoptera
- Family: Lyonetiidae
- Genus: Leucoptera
- Species: Leucoptera malifoliella
Notes on Taxonomy and NomenclatureTop of page Hübner described the genus Leucoptera in 1825. Costa (1836) named this leaf-mining moth Leucoptera malifoliella because it attacked mainly the leaves (foliage) of apple, but Zeller (1839) introduced the name Leucoptera scitella. Both names are popular, but the former is the current preferred scientific name. In 1848 Zeller described the genus Cemiostoma (subfamily Cemiostomatinae) and proposed the name Cemiostoma scitella.
Of the three English common names for L. malifoliella, 'pear leaf blister moth' is the most popular, but the name 'ribbed apple leaf miner' is probably more appropriate, as the pest prefers apple to pear.
The Russian name 'boiariishnikovaia kruzkovaia mol' is connected with an important wild host, hawthorn (Crataegus) (Gulii and Pamuzak, 1992). Another Russian name 'mol plodovaia krugominiruiushaia' and the Bulgarian name 'kruglominirast molec' mean 'circular leaf-miner' because the caterpillars make large, circular galleries in the leaves (Argiropulo et al., 1948; Grigorov, 1976).
DescriptionTop of page The moths are small. The adults have a wingspan of 6-7 mm. The forewings are lanceolate, greyish-white, and shiny with a brownish stripe. The brownish stripe is surrounded by coppery zones intermixed with black and white. The hind wings are pale grey and fringed (CFIA, 2005a). The body is about 3 mm long, covered with greyish-white, shiny scales. Both sexes have thread-like antennae with 27 segments. The antennae and legs are clothed with greyish-white scales. The hind legs are largest with two pairs of spurs on the tibia. The forelegs are smallest, and are without spurs. The middle tibias have one pair of spurs. The abdomen has 10 segments, and is larger in the female (Ivanov, 1976).
The eggs are oval, with an average size of 0.30 x 0.23 mm. Newly laid eggs are white, but before hatching they are a shiny grey (Ivanov, 1976).
The young larvae are pale green, legless, and up to 2 mm long. Older larvae are yellow to pale brown, with legs, and can reach 3-4 mm long. The head is brown, very small, bevelled, and sunk into the thorax. Sutura coronalis is not available. The body segments are well separated. There are four pairs of lateral tentacles placed on the mesothorax, metathorax and first two segments of the abdomen, which are used for movement in early instars (Ivanov, 1976; CFIA, 2005a; HYPP, 2005).
The pupae are yellow to light brown, 3-4 mm long, in a white, spindle-shaped cocoon (Andreev, 2005; CFIA, 2005a).
DistributionTop of page L. malifoliella occurs in temperate zones of Eurasia, the whole of Europe, even in the most northern countries, Turkey, the former USSR, the area around the Caspian Sea, the Middle East, central Asia, western Siberia and east through northern China (Ivanov, 1976; Gulii and Pamuzak, 1992; CERIS, 2004; CFIA, 2005a; EPPO, 2005; Jonko, 2005).
Distribution TableTop of page
The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.Last updated: 23 Apr 2020
|Continent/Country/Region||Distribution||Last Reported||Origin||First Reported||Invasive||Reference||Notes|
|China||Present, Localized||Native||Invasive||APPPC (1987); CERIS (2004); EPPO (2020)|
|Iran||Present||Native||Invasive||CERIS (2004); EPPO (2020)|
|Israel||Present, Localized||EPPO (2020)|
|Kazakhstan||Present, Widespread||Native||Invasive||CERIS (2004)|
|Turkey||Present||Native||Invasive||CERIS (2004); EPPO (2020)|
|Turkmenistan||Present||Native||Invasive||CERIS (2004); EPPO (2020)|
|Uzbekistan||Present||Native||Invasive||Rakhmatullaev and Urmieva (1993)|
|Albania||Present||Native||Invasive||Isufi and Myrta (1996); EPPO (2020)|
|Austria||Present, Widespread||Native||Invasive||Ivanov (1976)|
|Bulgaria||Present||Native||Invasive||Ivanov (1976); EPPO (2020)|
|Croatia||Present, Widespread||Native||Invasive||Ciglar and Schmidt (1983)|
|Czechia||Present, Widespread||Native||Invasive||Ciglar et al. (1999); Jonko (2005); EPPO (2020)|
|Federal Republic of Yugoslavia||Present, Widespread||Native||Invasive||Ciglar and Schmidt (1983); Stamenković et al. (1990)|
|Denmark||Present||Native||Jonko (2005); EPPO (2020)|
|France||Present, Widespread||Native||Invasive||Chambon (1981); Blanc (1983); Bouron (1988)|
|Germany||Present||Native||Mey (1988); EPPO (2020)|
|Netherlands||Present||Native||Ellis (2005); EPPO (2020)|
|Poland||Present||EPPO (2020); CABI (Undated)|
|Romania||Present, Widespread||Native||Invasive||Drosu (2001)|
|Russia||Present||Native||Invasive||CABI (Undated a)|
|-Central Russia||Present, Widespread||Native||Invasive||Gulii and Pamuzak (1992)|
|-Southern Russia||Present, Widespread||Native||Invasive||Gulii and Pamuzak (1992)|
|-Western Siberia||Present||Native||Gulii and Pamuzak (1992)|
|Serbia||Present||Nikolic et al. (2006); EPPO (2020)|
|Serbia and Montenegro||Present||EPPO (2020)|
|Slovakia||Present, Widespread||Native||Jonko (2005)|
|Slovenia||Present, Widespread||Native||Fito-Info (2005)|
|Sweden||Present, Localized||Native||Coppola et al. (2005)|
|United Kingdom||Present, Localized||EPPO (2020)|
|-England||Present, Localized||EPPO (2020)|
|-Scotland||Present, Localized||EPPO (2020)|
Risk of IntroductionTop of page The most likely pathway for the introduction of L. malifoliella is through commercial shipment of apples from Europe and Asia. Inspections are difficult due to the small size (3 mm) of the pest and its location, usually within the calyx. Other potential pathways include nursery stock or scion material (CERIS, 2004).
L. malifoliella is a quarantine pest for Canada (CFIA, 2005b) and the USA (USDA, 2005).
Hosts/Species AffectedTop of page L. malifoliella has many hosts, but prefers apple. Other important primary hosts are pear, quince and sweet cherry. It also feeds on the leaves of other fruit trees including morello cherry (Prunus cerasus), plum, peach, apricot, medlar (Mespilus germanica) and pistachio. It also attacks species in deciduous forests and shade trees such as flowering quinces (Chaenomeles sp.), Cotoneaster sp., birch, wild apple (Malus sylvestris), blackthorn, wild pear (Pyrus communis) and fragrant pear (Pyrus sp. nr. communis), Chinese white pear (Pyrus bretschneideri), witch-wood (Sorbus aucuparia) and alder. The most important wild host is hawthorn, Crataegus sp. (Grigorov, 1976; Gulii and Pamuzak, 1992; Garland, 1995; Tomov and Trenchev, 2001; Andreev, 2005; HYPP, 2005; Ellis, 2005; CFIA, 2005a).
Host Plants and Other Plants AffectedTop of page
|Chaenomeles (flowering quinces)||Rosaceae||Other|
|Cydonia oblonga (quince)||Rosaceae||Main|
|Frangula alnus (alder buckthorn)||Rhamnaceae||Other|
|Malus domestica (apple)||Rosaceae||Main|
|Malus sylvestris (crab-apple tree)||Rosaceae||Other|
|Mespilus germanica (medlar)||Rosaceae||Other|
|Pistacia vera (pistachio)||Anacardiaceae||Other|
|Prunus armeniaca (apricot)||Rosaceae||Other|
|Prunus avium (sweet cherry)||Rosaceae||Main|
|Prunus cerasus (sour cherry)||Rosaceae||Other|
|Prunus domestica (plum)||Rosaceae||Other|
|Prunus persica (peach)||Rosaceae||Other|
|Prunus salicina (Japanese plum)||Rosaceae||Other|
|Prunus spinosa (blackthorn)||Rosaceae||Other|
|Pyrus bretschneideri (yali pear)||Rosaceae||Other|
|Pyrus communis (European pear)||Rosaceae||Main|
|Sorbus aucuparia (mountain ash)||Rosaceae||Other|
SymptomsTop of page The larvae are solitary miners on the upper surface of the leaves; the fruits are not affected (CFIA, 2005a). They live in concentric galleries, which can reach a diameter of 5-6 mm. The mines change size and colour over time from small and whitish to large with brown spots. Frass may be visible, grouped in dark, concentric circles. In the event of heavy infestation, the leaf surface is severely damaged by the presence of mines and photosynthesis is reduced (HYPP, 2005).
Heavy infestations lead to premature leaf drop (Ivanov, 1976).
List of Symptoms/SignsTop of page
|Leaves / abnormal leaf fall|
|Leaves / internal feeding|
|Leaves / necrotic areas|
Biology and EcologyTop of page Physiology and phenology
Francke et al. (1987) identified the sex pheromone of L. malifoliella as 5,9-dimethylheptadecane. Some minor components, dimethylheptadecane, 5,9- and dimethyloctadecane,5,9-, were later found by Riba et al. (1990).
At 18 and 23°C, the photoperiod in the larval stage primarily determines diapause. The close correlation between the critical time of illumination and temperature determines the annual number of generations for a given geographical location (Saringer and Csontos, 1998).
L. malifoliella is a multivoltine, lyonetiid species, with between one and five generations per growing season in Europe, depending on geographical location. In Bulgaria, Hungary and southern parts of Russia, there are three to four generations per year; in Italy and France, two to four generations; in Poland and Germany, two generations; and in Austria, Belgium and Holland, only one generation is reported. The last generation is often partial (Ivanov, 1976; Dulinafka, 1983; Mey, 1988a; Gulii and Pamuzak, 1992; Maciesiak, 1999; CFIA, 2005a; HYPP, 2005). Four generations per year have been reported in Iran (Beheshti, 1989). One generation took an average of 26 days at 28°C, 36 days at 23°C and 50 days at 18°C (Saringer et al., 1985).
L. malifoliella overwinters as a diapausing pupa in tiny, white cocoons in sheltered places such as bark crevices, on dead leaves or debris on the ground, and around the base of the host plant. Cocoons have been found at the stem and calyx ends of imported apples and pears (CFIA, 2005a).
Adults emerge in the spring, at the 'pink bud' stage of apples, when average temperatures are up to 12°C. In southern Europe this occurs from the end of March to mid-April. The flight can continue to the end of September. The moths are active during the day between 09.00 h and 17.00 h at temperatures above 15-16°C. The second and third generations appear in the second week of June and the second week of July, respectively. Mating and oviposition of overwintering moths begins 50-60 hours after eclosion. The adults of the next generations are mature and can copulate immediately after emerging. Copulation occurs on tree leaves, branches and stems, and takes 15-45 minutes. Polyandry is available (Ivanov, 1976; Koutinkova et al., 1999; Andreev and Koutinkova, 2001; CERIS, 2004).
In Iran the adults of the overwintering generation begin to emerge at the end of March. The second, third and fourth generations peak in mid-June, late July and mid-September, respectively (Beheshti, 1989).
The eggs are deposited singly on the undersides of leaves. Over 350 eggs can be found on a single leaf when the population density is very high. Females from overwintered (April-May) and late-summer (August-September) generations lay an average of 25-30 eggs, whereas females from summer generations (June-July-August) lay 45-50 eggs. The adults live for 4-7 days (Ivanov, 1976).
Embryonic development may exceed 1 month at low temperatures; at 15-17°C, it takes 13-17 days; at 23-24°C, 8-10 days; and above 24°C, 7-8 days. More than 95% of the eggs laid on fresh leaves hatch, but only 5-11% hatch on dry leaves (Ivanov, 1976; CFIA, 2005a; HYPP, 2005).
Newly hatched larvae bore through the egg directly into the leaf tissue. They make round, blister-like mines in the upper leaf layers (CFIA, 2005a). The caterpillars take four larval instars to complete their development. Development is dependent on temperature: in Bulgaria it takes 17-21 days for the first (Spring) and last (Autumn) generations and 11-14 days for the summer generations. In Germany, larval development takes 39 days for the first and up to 45 days for the second generation (Ivanov, 1976; Mey, 1988a).
Some authors (Saringer et al., 1985; Oltean et al., 1995) have reported that the larvae of L. malifoliella pass through six instar stages.
In France, the larvae of successive generations are present from early May, early July, mid-August and early October; those of the last generation were unable to complete their development before winter (Blanc, 1983).
Egg and larval development required 50 days to complete at 15°C, 35 days at 18°C and 29 days at 20°C (CERIS, 2004).
Fully-grown larvae emerge from the mines through the upper surface of the leaf and begin to search for pupation sites. They often climb down on silk fibre. The caterpillars spin white cocoons in which they pupate. The larvae of the first generation pupate mainly on leaves, whereas the later generations pupate in bark crevices or on the fruit. The pupae are often found in groups (Ivanov, 1976; CERIS, 2004; HYPP, 2005).
The pupa is formed after 2 days. Development takes 7-13 days for the summer generations, but sometimes longer, depending on temperature: 12-13 days at 23°C and 28 days at 15°C (Ivanov, 1976; CERIS, 2004; HYPP, 2005).
A long, warm autumn prolongs the presence of vegetation on the host plants, and all caterpillars are able to complete their development. L. malifoliella overwinters more successfully in warmer winters. The population density increases when the second and third (summer) generations lay their eggs and hatch in dry conditions with limited rainfall. Some adults can appear when the temperature increases in February-March, but if the weather turns cold, 100% will die without ovipositing, thus reducing the population density of overwintering adults and damaging the first generation (Ivanov, 1976).
Natural enemiesTop of page
|Natural enemy||Type||Life stages||Specificity||References||Biological control in||Biological control on|
Notes on Natural EnemiesTop of page A list of natural enemies of L. malifoliella on apple, pear and peach in the Saluzzo area of Italy included 10 parasitic species (one braconid (Rhysipolis decorator) and nine eulophids) and three predators (two mirids and one vespid). Comparison of chemically treated and untreated orchards showed that these natural enemies could keep Leucoptera populations under control only if left undisturbed by chemical intervention. Chrysocharis nitetis was the most widespread species and the last to disappear from sprayed orchards, but it could not control L. malifoliella alone, as it only became abundant late in the year (Santoro and Arzone, 1983).
A rate of 35-53% parasitism was found on overwintering pupae of L. malifoliella. However, more detailed examination, including dissection of the pupae, showed that only 13-18% of the total winter mortality of L. malifoliella was attributable to parasitism, the rest being due to fungi, bacteria and unknown causes (Celli et al., 1985).
A total of 28 parasitic insects and five hymenopteran hyperparasites were found on the larvae and pupae of L. malifoliella in Plovdiv and Assenovgrad regions in southern central Bulgaria. The most important were the larval parasitoids Closterocerus trifasciatus, Chrysocharis pentheus, Chrysocharis assis and Achrisocharella formosa, which could parasitize more than 45% of the caterpillars. The parasitoids mainly attack the final larval instars, when the mines exceed 6 mm. Young caterpillars are rarely parasitized. Pediobius pyrgo is the most important parasitoid of the pupae. The flight of the parasites is synchronized with that of the host. They emerge a few days later than the host, but follow its development and oviposit in the most susceptible stages (Ivanov, 1976; Koutinkova and Andreev, 2001).
Cojocaru (2000) found 19 species of hymenopteran parasitoids of L. malifoliella collected from apple tree orchards in the eastern and central part of Romania, between 1992 and 1996. The most efficient parasitoid species in this complex were Chrysocharis pentheus, Chrysocharis orchestis, Chrysonotomyia lanassa, Neochrysocharis formosa, Chrysocharis sp., Minotetrastichus frontalis, Chrysonotomyia sp., Cirrospilus variegatus and Sympiesis sericeicornis. Chrysocharis and Chrysonotomyia genera were the most important parasitoids, regardless of the collection site. Experimental results showed that total parasitization of L. malifoliella larvae was between 2.4 and 32.5%, whereas previous literature for Romania indicated it was 19-63% for larvae and 13-65% for pupae.
Sixty-seven parasitoid species were reared from L. malifoliella and three other leaf miners and leaf rollers collected from apple orchards in Hungary. The lowest number of parasitoid species occurred in conventionally managed orchards, whereas the highest number was found in integrated and untreated orchards. The most important parasitoid species were Sympiesis sericeicornis, Pnigalio pectinicornis, P. soemius, Chrysocharis pentheus, Pediobius pyrgo, Minotetrastichus frontalis and Neochrysocharis chlorogaster. The larvae and pupae of leaf miners were parasitized by up to 35-45%, occasionally to 80% (Balazs, 1997).
A total of 16 parasitoid species was reared from the larvae and pupae of L. malifoliella in Germany. Chrysocharis nitetis was the most frequent parasitoid of the larvae. All of the identified species were polyphagous parasitoids, and thus not restricted to single habitats. Percentage parasitism was very low at all sites in the first generation, but parasitoid-induced mortality was high in the second generation, often exceeding 50%. Parasitism was generally low throughout the study period in sprayed orchards (Mey 1988b, 1993).
In Tabriz, Iran, the percentage mortality of overwintering pupae was 7.17%, of which 1.83% was due to parasitism, whereas the other control agents caused 5.34% mortality. Approximately 2.64 and 1.73% egg mortalities were calculated for the two generations. Mortality rates due to natural control agents at four larval instar stages and the pupal stage during the first generation were 7.4, 1.58, 13.74, 22.2 and 12.16%, respectively, whereas estimates of such mortality rates during the second generation were 6.7, 11.29, 42.59, 32.16 and 2.60%, respectively. The highest mortality rates within the two generations were associated with parasitism and the main parasitoids collected from different developmental stages belonged to the genus Baryscapus in the family Eulophidae (Rahnemoon et al., 2003).
The most important predatory insect is Anthocoris nemoralis, which matures in the second half of the summer and can kill 5-18% of the leaf-miner larvae. Many other polyphagous predatory insects were found to destroy the eggs and larvae of miner moths in the orchards, but could not effectively control the population density of these pests. Predatory ladybirds were of highest density and importance (Ivanov, 1976; Koutinkova and Andreev, 2001).
The mirids, Deraeocoris flavilinea and Pilophorus perplexus, and the vespid, Polistes gallicus, are reported as predators on larvae of L. malifoliella in Italy (Santoro and Arzone, 1983).
Chaffinches (Fringulla coelebs) and wrens (Troglodytes parvulus) eat caterpillars in the mines and when they leave the leaves before pupating (Ivanov, 1976).
Means of Movement and DispersalTop of page The most likely pathway forintroduction of L. malifoliella is through international trade of apples and pears from Europe and Asia. Inspections are difficult due to the small size of the pest (3 mm) and its covert location, usually within the calyx. Other potential pathways of introduction include nursery stock or scion material.
Plant TradeTop of page
|Plant parts liable to carry the pest in trade/transport||Pest stages||Borne internally||Borne externally||Visibility of pest or symptoms|
|Fruits (inc. pods)||pupae||Yes||Pest or symptoms usually visible to the naked eye|
ImpactTop of page Extremely high populations of L. malifoliella can be dangerous, for example, in regions with large apple, pear or quince orchards where abiotic (climatic), biotic (natural regulators) and human factors (unskillful use of insecticides) favour the build-up of the pest. Outbreaks of L. malifoliella are thought to be caused by the application of insecticides against other pests (Ivanov, 1976), as happened in Slovenia during the periods 1968-1978, 1981-1988, 1992-1995 and since 2000 (Matis, 2004).
Heavier leaf loss leads to a decrease in fruit size, quality and total yield by causing a reduction in the number of fruits. Insufficient nutrient supply due to a reduced leaf area and a consequently smaller leaf:fruit ratio leads to a decrease in mean fruit size and total yield. Heavy leaf loss also has an adverse effect on fruit quality components (dry matter substance, viscosity, total sugar and acid content of fruit juice), which is reflected in sensory evaluation criteria. Heavy leaf losses also influence blossom bud differentiation in the blossom set of the following year. Both the number of inflorescences and the number of blossoms per inflorescence are reduced. For L. malifoliella, a mean mine size of 0.96 cm² was recorded, which corresponds to a 4.2% loss of leaf area (Baufeld and Freier, 1991, 1992).
Leaf fresh weight and dry matter contents progressively decline with an increase in the number of leaf miners. Chlorophyll content and assimilation also decrease, thus reducing the crop yield. The reduction in apple production caused by leaf-mining moths was calculated as 4.6-23.4% (Ivanov, 1975).
The most intense leaf drop in apple, caused by L. malifoliella, resulted in a damage rate of 7-9 mines/leaf (Celli and Burchi, 1984).
More than 50% of the foliage dropped prematurely as a result of damage caused by L. malifoliella larvae in large apple orchards in the Bacs-Kiskun department of Hungary in 1982 (Dulinafka, 1983).
However, only a small decrease in production parameters was observed in Italy, despite heavy infestation (up to 70% leaf drop, nearly 100% of mined leaves and more than 12 mines/leaf) (Cravedi et al., 1992).
The pupation of larvae on the fruits and the presence of cocoons reduces the commercial value of apples and creates export quarantine problems (Blanc, 1983).
Similarities to Other Species/ConditionsTop of page The adult moth is difficult to mistake for another species. The closely related moth, Leucoptera susinella, makes similar circular (but larger), mines on poplar and aspen; L. malifoliella does not affect these plants (Argiropulo et al., 1948).
Small mines (up to 3 mm) on apple, caused by L. malifoliella, are similar to the circular mines of Rhamphus oxyacanthae, but the larvae of this species concentrate frass in the middle of the mines (Tomov and Trenchev, 2001).
Prevention and ControlTop of page
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.
Leaf-mining moths on fruit trees are difficult to control for various reasons, including their covert way of life, which makes them difficult to reach with sprays. The population density of L. malifoliella increases in orchards when chemical pesticides (organophosphates, carbamates, etc.) are applied without skill, as the pesticides can kill almost all of the natural regulators of the pest. In Bulgaria, more than 75% of larvae are parasitized in nontreated orchards, whereas in treated orchards, between 2 and 28% of caterpillars are affected by parasites (Ivanov, 1976; Ivanov et al., 1982). Similar results were obtained in Germany (Vogt, 1997) and in Hungary (Balazs, 1997).
Observations in Hungarian apple orchards with L. malifoliella and Panonychus ulmi found that weak pruning techniques were correlated with a higher level of pest damage than strong pruning techniques, especially in organic growing systems. Techniques should be carefully chosen because shoots grow faster and more vigorously after strong pruning, and this supports better preservation of trees, because of the reduced susceptibility to pests and diseases (Holb et al., 2001).
The population density of the overwintered generation can be reduced by scraping and removing old, loose bark, along with the cocoons of the pupae (Ivanov, 1976).
For successful chemical control against L. malifoliella, the phenological development of the pest must be followed and sensitive stages identified. These sensitive stages depend on the life cycle of the pest and on the mode of action of the applied pesticides. The most appropriate times for chemical control are the period of active flight and egg laying, until the beginning of egg hatching; and the period of hatching and larval injury, until the formation of small mines. Insect growth regulators (chitin-synthesis inhibitors, juvenoids, ecdisoids) are used during the first period and contact insecticides from different groups can be used during the second period (Ivanov et al., 1982; Andreev et al., 2001). Winter spraying against pupae is possible in March, but this is not sufficient to reduce summer treatment. Mineral oils, applied alone or in combination with organophosphates, are 25-60% effective (Ivanov, 1976). Control of adult moths is not satisfactory because they fly for long periods of time (Ivanov, 1976). Several sprays with highly persistent insecticides are required, which can kill natural regulators of the pest. However, treatment of adults with compounds containing pyrethroids gave good results when applied at the beginning of mass swarming and at peak swarming in apple and cherry orchards in Hungary (Penzes, 1985). The larvae have to be controlled by sprays applied immediately after hatching and before they have entered the leaves. Some insecticides, which penetrate the leaf tissue, are efficient against young larvae, when the mines are up to 3 mm, but chemical control is not effective when the mines are larger than 5-6 mm. A long list of organophosphates, pyrethroids, carbamates, etc. are reported to control L. malifoliella. The list contains trichlorphon, tetrachlorvinphos, phosalone, methomil, chlorpyrifos, dimetoate, deltamethrin, cypermethrin, etc. (many of these insecticides are still in use) and ends with the new generation of neonicotinoid insecticides such as acetamiprid, imidacloprid, thiacloprid and thiamethoxam. Pesticides with high toxicity and long persistence are no longer permitted. Single spraying is not effective as the first generation of L. malifoliella has a long flight period. At least two treatments are required in cases of heavy infestation (Ivanov, 1976, 1978, 1980; Maciesiak, 1999; Maciesiak and Olszak, 2002; Miklavc, 2003; NSPP, 2005). Insect growth regulators have a good ovicidal effect on 1-day-old eggs and the most effective chemical control against L. malifoliella is achieved with treatment at the start of oviposition. Juvenoids, ecdisoids, inhibitors of premature drop and chitin synthesis inhibitors such as triflumuron, teflubenzuron, tebufenozide, spinosad, methoxyfenozide and hexaflumuron may be used (Velcheva, 1986; Vogt, 1997; Maciesiak, 1999; Maciesiak and Olszak, 2002; Miklavc, 2003; Enzsoly and Kuroli, 2003). A loss in efficacy of diflubenzuron against L. malifoliella was reported in 11 apple orchards in the province of Bologna, Italy (Faccioli et al., 1990). Temperatures above 26°C and air humidity below 50% reduced the effectiveness of preparations based on active ingredients including trichlorfon, diflubenzuron and cypermethrin by 20-40%, when used against L. malifoliella (Marinkov, 1986). The population dynamics of L. malifoliella were influenced by insecticides used against the European cherry fruit fly (Rhagoletis cerasi), San Jose scale (Diaspidiotus perniciosus) and cherry bark tortrix moth (Enarmonia formosana) in Hungarian sour cherry orchards (Balazs and Jenser, 2004).
Cravedi and Roversi (1985) investigated the relative susceptibility of 15 varieties of apple tree to L. malifoliella in Cremona, Italy. The number of eggs per leaf was in inverse ratio to the hairiness of the lower surface of the leaves. However, yield did not differ significantly between varieties that were more or less heavily affected.
Draganova and Tomov (1998) investigated the virulence of a strain of Beauveria bassiana against larvae of L. malifoliella. Twenty percent of larvae treated with conidia and 26.67% of larvae treated with blastospores died by mycosis before making a cocoon, whereas 56.67 and 50%, respectively, died by mycosis after making a cocoon. Rovesti and Deseo (1991) reported that seed kernel extract of Neem (Azadirachta indica) was most effective at a low dose (1.25 g/L) producing 80-100% mortality of L. malifoliella larvae. The growth of hatched larvae was disrupted and no pupation occurred. Neem leaf extract gave 80% mortality. However, these results were not confirmed in another investigation in Italy (Pasqualini et al., 1998), where the author established a low efficiency of Neem extract against L. malifoliella.
Integrated Crop Management
L. malifoliella is an important pest in apple IPM systems (Briolini, 1975; Pelov et al., 1996; Jenser et al., 1999) and the population density of the pest must be considered. Chemical control is only used when the population density exceeds the economic threshold (Ivanov et al., 1982). According to the principles of IPM, the pesticides used must be the least hazardous to humans, livestock and beneficial entomofauna whilst providing effective control of the pests; for example, insect growth regulators and some contact insecticides (Dulic and Injac, 1982; Pelov et al., 1996; Vogt, 1997). The number of parasitoids (predominantly Chrysocharis pentheus, Neochrysocharis formosa, Pholetesor bicolor, Sympiesis sericeicornis, S. gordius and Pnigalio pectinicornis) and parasitized leaf miner larvae were higher on an apple IPM farm than in a conventionally managed farm in Hungary. The leaf miner population increased by 13.0-25.6% due to the suspension of IPM (Balazs and Jenser, 1999). In Hungary, Fekete et al. (2004) investigated the importance of flowering herbaceous plants in IPM of apple. In a comparison of different IPM plots, the population of L. malifoliella was lower in a plot of sowed herbaceous plants, and more parasites were found in the larvae. L. malifoliella was found in IPM systems for sour cherry orchards in Hungary (Jenser et al., 2001).
Field Monitoring/Economic Threshold Levels
The following methods are used for field monitoring and forecasting of L. malifoliella in Bulgaria: cage method, visual method, pheromone traps, phenological forecasting and models (Andreev et al., 2001). The cage method is the most reliable method used to follow the phenological development of L. malifoliella, but it is rarely used because it is labour-intensive and cannot be used to assess the population density. Observations begin with the collection of pupae from the trunks of fruit trees, either manually or with dry hunting belts set up to the stems. A minimum number of 200-300 pupae are placed in net cages, located among the trees in the orchard. The dynamics of moth emergence from the overwintered generation are observed in the spring. Further development of the moths is followed using cages without bottoms, placed above the trees, or branch isolators made of cloth. A clear polyethylene stripe is stitched in the middle of the isolators to make observations easier. In each isolator, 8-10 couples of emerged moths are released in the cages. It is possible to observe the start of egg laying, hatching of the larvae, and the appearance of the first mines (Andreev et al., 2001). The visual method is used for prognosis and indicating the presence of L. malifoliella. It does not require any preliminary preparation and provides accurate information on the phenological development and population density of the pest. The orchards are visited diagonally or between the lines of the trees. The trunks of the trees are observed during the non-vegetative period to find any overwintering pupae. The crowns of the trees are examined during the vegetative period to find the eggs and any specific injuries on the leaves. Observations are made on 5-10 representative trees (depending on the size of the orchard) in damaged orchards. In the spring, observations begin immediately after the establishment of the first flight of the moths and are made at 1-2 day intervals. Fifty leaves are collected from each tree (10 leaves from each side: east, west, north and south, and 10 leaves from the middle) and checked in the laboratory. The start of oviposition and the number of eggs laid and mines per leaf can be determined (Andreev et al., 2001). Pheromone traps are increasing importance for monitoring seasonal flight dynamics. They provide the most accurate information on the seasonal flight dynamics of L. malifoliella. The sex pheromones used today are highly selective and non-target pests are rarely found in the traps. Pheromone traps with a sticky bottom (type 'delta') are mostly widely used. They are hung on trees in the orchard at a height of 1.5-2 m, 1-2 weeks before the expected start of the flight and are examined every 2-3 days. The pheromone capsules (dispensers) have to be changed every 40 days, and the sticky bottoms must be removed when they are dirty. The pheromone traps can indicate a suitable time to apply insect growth regulators, during the first definite maximum flight of the overwintered generation, as this coincides with mass egg laying, and the beginning of hatching. For other generations, egg laying starts 1 day after the beginning of the flight period and can also be easily identified. The risk of injury to the leaves can be foreseen by additional observations (Kutinkova et al., 1999; Andreev et al., 2001). Phenological forecasting is an easily used method with limited use in forecasting the full phenological development of the pest. There is synchrony between the phenological development of L. malifoliella and its host plants and control can be related to the phenophase of some apple or pear cultivars. This method is mainly used in spring when, for a comparatively short period of time, a few clearly delimited stages of phenological development can be observed. The flight of the overwintered generation of L. malifoliella usually begins in the phenophase 'pink bud' to 'first bloom' of the early cultivar Prim Rouge. Egg laying of the moths from this generation coincides with the same phenophase of the late cultivar Granny Smith. If observations are made on other cultivars, with different times of blossoming, fruit growing and ripening, a system can be developed with accurate reference points (Andreev et al., 2001). A phenological model based on temperature accumulation (degree-days) is easy to use and offers the opportunity for prognosis of the full phenological development of L. malifoliella. However, the precision of this method can be unsatisfactory and this prevents its widespread use. In Bulgaria, calculations showed that the lower developmental threshold for L. malifoliella was 5.5°C and the following temperature sums were estimated: egg stage, 155-172 degree-days; larval stage, 284-328 degree-days; pupal stage, 212-246 degree-days; from egg to imago, 651-746 degree-days; the beginning of flight of the overwintered generation, 122-177 degree-days; and beginning of egg laying of the overwintered generation, 153-185 degree-days (Andreev et al., 2001). A similar model based on degree-hours has been developed in the Czech Republic (Kneifl and Knourkova, 1999). The authors report that the appropriate time for ovicidal treatment against the pest is when the temperature sum is in the range of 3000-3300 hour-degrees (10°C is the low temperature threshold). Sums of 5100-5400 hour-degrees indicate the best time for larvicidal treatment. In Bulgaria, the economic threshold for L. malifoliella is 2-4 eggs or mines per leaf (Zaharieva et al., 1997). The leaf:fruit ratio is particularly important for evaluating the extent of damage caused by leaf-damaging pests and has to be used to derive injury threshold ranges for L. malifoliella. Investigations on L. malifoliella in Hungary enabled the determination of preliminary flexible injury thresholds. The thresholds vary between 0.1-2.5 eggs and mines per leaf for the first generation and 0.3-3.5 eggs and mines/leaf for the second generation, depending on leaf:fruit ratio, yield level and leaf-miner generation (Baufeld and Freier, 1991, 1992). The economic damage threshold for L. malifoliella on apple in former Yugoslavia was found to be 50 mines/100 leaves, but the action thresholds for insecticide applications were 10 eggs/100 leaves for diflubenzuron (applied at the beginning of the oviposition period) and 50 eggs/100 leaves for deltamethrin (applied just before hatching) (Injac et al., 1987). In Russia the economic injury level in apple blossom is 8-10 moths per 100 shaken branches. After blossom, the EIL is 0.5-1 mines per leaf (Gulii and Pamuzak, 1992).
ReferencesTop of page
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Distribution MapsTop of page
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