Cameraria ohridella (horsechestnut leafminer)
- Summary of Invasiveness
- Taxonomic Tree
- Notes on Taxonomy and Nomenclature
- Distribution Table
- History of Introduction and Spread
- Habitat List
- Hosts/Species Affected
- Host Plants and Other Plants Affected
- List of Symptoms/Signs
- Biology and Ecology
- Latitude/Altitude Ranges
- Air Temperature
- Natural enemies
- Notes on Natural Enemies
- Means of Movement and Dispersal
- Pathway Causes
- Pathway Vectors
- Plant Trade
- Impact Summary
- Economic Impact
- Environmental Impact
- Threatened Species
- Social Impact
- Risk and Impact Factors
- Detection and Inspection
- 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
- Cameraria ohridella Deschka & Dimic
Preferred Common Name
- horsechestnut leafminer
International Common Names
- English: horse chestnut leaf miner; horse-chestnut leafminer
- French: mineuse du marronnier
Local Common Names
- Austria: Rosskastanienminiermotte
- Czech Republic: Klínenka jírovcová
- Germany: Rosskastanienminiermotte
- Hungary: vadgesztenyelevél
- Italy: minatore fogliare dell'ippocastano
- Netherlands: paardenkkastanjemineermot
- Poland: szrotowek kasztanowiaczek
- Slovakia: ploskacik pagastanovy
- Switzerland: Rosskastanienminiermotte
- LITHOD (Cameraria ohridella)
Summary of InvasivenessTop of page
Cameraria ohridella probably originates from remote natural stands of the European horse-chestnut, Aesculus hioppocastanum in Greece, Albania and Macedonia. It was first observed attacking ornamental horse-chestnut trees in Macedonia in the 1970s, then in Serbia in 1987 and Austria in 1989, from where it spread to most of Europe. Since then, in all invaded regions, outbreaks have continued unabated, causing aesthetic damage to horse-chestnut, one of the favourite ornamental trees in European cities. The fast dispersal of the moth in Europe is attributed mainly to human transport. Cars, lorries, trains and other vehicles may carry adults and overwintering pupae in dead leaves. The moth is listed in the 100 worse invasive species in Europe in the DAISIE database (DAISIE, 2009).
Taxonomic TreeTop of page
- Domain: Eukaryota
- Kingdom: Metazoa
- Phylum: Arthropoda
- Subphylum: Uniramia
- Class: Insecta
- Order: Lepidoptera
- Family: Gracillariidae
- Genus: Cameraria
- Species: Cameraria ohridella
Notes on Taxonomy and NomenclatureTop of page
Cameraria ohridella was described based on material collected at the Ohrid Lake in Macedonia (hence its specific name).
DescriptionTop of page
The morphology of all developmental stages of C. ohridella has been studied mainly by Deschka and Dimic (1986), Skuhravý (1998) and Sefrová and Skuhravý (2000).
The eggs are white and 0.2-0.4 mm.
There are four, occasionally five, instars of feeding larvae and two instars of spinning larvae. Instars of feeding larvae differ by length and by width of the head capsule (Sefrova and Skuhravy, 2000).
First-instar larvae are 0.5 mm long; head capsule is 0.1-0.17 mm wide.
Second-instar larvae are 1.2 mm long; head capsule is 0.2-0.3 mm wide.
Third-instar larvae are 2.1 mm long; head capsule is 0.36-0.46 mm wide.
Fourth-instar larvae are 3.5 mm long; head capsule is 0.5-0.66 mm wide.
Larval morphology of C. ohridella corresponds to that of the subfamily Lithocolletinae (Kumata, 1963). The body is distinctly constricted between the segments which appear to be convex laterally. Tergites and sternites are formed from extensively sclerotized plates, which enable the caterpillars to move within the mine. The mouthparts, the labrum and labium, are massive, shield-shaped; the flat sickle-shaped mandibles move horizontally. The thoracic legs and the ventral and anal prolegs are completely reduced. The width of the head capsule of the two spinning instar larvae does not change from the fourth feeding instar larva. Mouthparts are complete and the antennae, maxillae and maxillar palpi and spineret are present (Sefrova and Skuhravy, 2000).
The pupa is brown and is 2.9-4.5 mm long (3.7 mm on average). Freise and Heitland (1999) describes a method to distinguish between male and female pupae.
The body is 4-5 mm long. The moth is a rich brown colour with bright white chevrons edged with black.
DistributionTop of page
C. ohridella was first observed attacking Aesculus hippocastanum in Macedonia in the 1970s, and described as a new species in 1986 (Simova-Tosic and Filev, 1985; Deschka and Dimic, 1986). In 1987 it was found in Serbia (Petkovic, 1989) and in 1989 in Austria, from where it spread to most of Europe. Its origin has been a matter of debate. It was first suggested to be a relict species that has survived the Ice Age with its host in south-eastern Europe (Deschka and Dimic, 1986; Grabenweger and Grill, 2000), whereas, according to Holzschuh (1997) and Kenis et al. (2005) it was more likely a non-European species only recently introduced in the Balkans. Hellrigl (2001) suggested that the moth may have shifted from another host tree (e.g. an Acer species) in the Balkans or the Near East. Recent molecular studies and observations of ancient herbarium collections now suggest that the moth originates from some remote natural horse-chestnut stands in the Balkan mountains of Macedonia, Albania and Greece and that it has moved to urban areas in these countries in the second half of the 20th century (Valade et al., 2009; Lees et al., 2011).
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.
|Continent/Country/Region||Distribution||Last Reported||Origin||First Reported||Invasive||Reference||Notes|
|Turkey||Restricted distribution||Introduced||Invasive||Cebeci and Acer, 2007; Cebeci et al., 2011; Gözel and Gözel, 2014||First observed in 2004.|
|Albania||Widespread||Native||Invasive||Simova-Tosic and Filev, 1985; CABI/EPPO, 2003; EPPO, 2014||Probably originates from some native horse chestnut stands but invasive in urban trees.|
|Austria||Widespread||Introduced||1989||Invasive||Puchberger, 1990; Tomiczek, 1997; CABI/EPPO, 2003; EPPO, 2014|
|Belarus||Present||Introduced||2003||Invasive||Gninenko and Orlinski, 2004; EPPO, 2014|
|Belgium||Widespread||Introduced||2000||Invasive||Prins and Puplesiene, 2000; CABI/EPPO, 2003; EPPO, 2014|
|Bosnia-Hercegovina||Widespread||Introduced||Invasive||Dautbasic and Dimic, 1999; CABI/EPPO, 2003; EPPO, 2014||First observed in 1993.|
|Bulgaria||Widespread||Introduced||Invasive||Pelov et al., 1993; CABI/EPPO, 2003; EPPO, 2014||First observed in 1989.|
|Croatia||Widespread||Introduced||1995||Invasive||Maceljski and Bertic, 1996; CABI/EPPO, 2003; EPPO, 2014|
|Czech Republic||Widespread||Introduced||1997||Invasive||Liska, 1997; Skuhravý, 1998; CABI/EPPO, 2003; EPPO, 2014|
|Denmark||Widespread||Introduced||Invasive||CABI/EPPO, 2003; Karsholt and Kristensen, 2003; EPPO, 2014||First observed in 2002.|
|Finland||Restricted distribution||Introduced||Invasive||Buszko, 2006||First observed in 2006.|
|France||Widespread||Introduced||2000||Invasive||Guichard and Augustin, 2002; CABI/EPPO, 2003; Augustin et al., 2004; EPPO, 2014|
|Germany||Widespread||Introduced||1994||Invasive||Freise, 2001; CABI/EPPO, 2003; EPPO, 2014|
|Greece||Widespread||Introduced||1996||Invasive||Skuhravý, 1998; Avtzis and Avtzis, 2003; CABI/EPPO, 2003; EPPO, 2014||Probably originates from some native horse chestnut stands but invasive in urban areas.|
|Hungary||Widespread||Introduced||1994||Invasive||Szaboky, 1997; CABI/EPPO, 2003; Bodor, 2011; EPPO, 2014|
|Italy||Widespread||Introduced||1992||Invasive||Hellrigl, 1998a; Hellrigl, 2001; CABI/EPPO, 2003; EPPO, 2014|
|Latvia||Present||Metla et al., 2013; EPPO, 2014|
|Lithuania||Widespread||Introduced||2002||Invasive||Ivinskis and Rim?aite, 2006; Peciulyte and Kacergius, 2012; EPPO, 2014|
|Macedonia||Widespread||Native||Invasive||Deschka and Dimic, 1986; CABI/EPPO, 2003; EPPO, 2014||Probably originates from some native horse chestnut stands but invasive in urban areas.|
|Moldova||Present||Introduced||Invasive||Timus and Mihailov, 2005; EPPO, 2014||First observed in 2003.|
|Netherlands||Widespread||Introduced||1999||Invasive||Stigter et al., 2000; CABI/EPPO, 2003; EPPO, 2014|
|Poland||Widespread||Introduced||1998||Invasive||Skuhravý, 1998; CABI/EPPO, 2003; EPPO, 2014|
|Romania||Widespread||Introduced||Invasive||Sefrová and Lastuvka, 2001; CABI/EPPO, 2003; EPPO, 2014; Olenici and Duduman, 2016||First observed in 1998.|
|Russian Federation||Restricted distribution||Introduced||2003||Invasive||Gninenko and Orlinski, 2004; EPPO, 2014|
|-Central Russia||Present||EPPO, 2014|
|-Southern Russia||Restricted distribution||EPPO, 2014|
|Serbia||Widespread||Introduced||Invasive||Petkovic, 1989; EPPO, 2014||First observed in 1987.|
|Slovakia||Widespread||Introduced||1996||Invasive||Sivicek et al., 1997; CABI/EPPO, 2003; EPPO, 2014|
|Slovenia||Widespread||Introduced||1995||Invasive||Milevoj and Macek, 1997; CABI/EPPO, 2003; EPPO, 2014|
|Spain||Restricted distribution||Introduced||2002||Invasive||Villalva and Del Estal, 2003; EPPO, 2014|
|Sweden||Restricted distribution||Introduced||2002||Invasive||Svensson, 2003; EPPO, 2014|
|Switzerland||Widespread||Introduced||1999||Invasive||Kenis and Forster, 1998; CABI/EPPO, 2003; EPPO, 2014|
|UK||Restricted distribution||Introduced||Invasive||RHS, 2002; CABI/EPPO, 2003; Tilbury et al., 2004; EPPO, 2014||First observed in 2002.|
|-England and Wales||Restricted distribution||EPPO, 2014|
|Ukraine||Present, few occurrences||Introduced||Invasive||Akimov et al., 2003; CABI/EPPO, 2003; EPPO, 2014|
|Yugoslavia (Serbia and Montenegro)||Widespread||Introduced||Invasive||Deschka and Dimic, 1986; Petkovic, 1989; CABI/EPPO, 2003||First observed in 1987.|
History of Introduction and SpreadTop of page
C. ohridella was first observed attacking ornamental horse-chestnut trees in Macedonia in the 1970s, and described as a new species in 1986 (Simova-Tosic and Filev, 1985; Deschka and Dimic, 1986). In 1987 it was found in Serbia (Petkovic, 1989) and in 1989 in Austria, from where it spread to most of Europe. Its origin has been a matter of debate. It was first suggested to be a relict species that has survived the Ice Age with its host in south-eastern Europe (Deschka and Dimic, 1986; Grabenweger and Grill, 2000) whereas, according to Holzschuh (1997) and Kenis et al. (2005) it was more likely a non-European species only recently introduced in the Balkans. Hellrigl (2001) suggested that the moth may have shifted from another host tree (e.g. an Acer species) in the Balkans or the Near East. Recent molecular studies and observations of ancient herbarium collections now suggest that the moth originates from some remote natural horse-chestnut stands in the Balkan mountains of Macedonia, Albania and Greece and that it has moved to urban areas in these countries in the second half of the 20th century (Valade et al., 2009; Lees et al., 2011).
IntroductionsTop of page
|Introduced to||Introduced from||Year||Reason||Introduced by||Established in wild through||References||Notes|
|Natural reproduction||Continuous restocking|
|Belarus||2003||Yes||Gninenko and Orlinski (2004)|
|Belgium||2000||Yes||Prins and Puplesiene (2000)|
|Bosnia-Hercegovina||1993||Yes||Dautbasic and Dimic (1999)|
|Bulgaria||1993||Yes||Pelov et al. (1993)|
|Croatia||1995||Yes||Maceljski and Bertic (1996)|
|Czech Republic||1997||Yes||Liska (1997)|
|Denmark||2002||Yes||Karsholt and Kristensen (2003)|
|England and Wales||2002||Yes||Tilbury et al. (2004)|
|France||2000||Yes||Guichard and Augustin (2002)|
|Lithuania||2003||Yes||Gninenko and Orlinski (2004)|
|Moldova||2003||Yes||Timus and Mihailov (2005)|
|Netherlands||1999||Yes||Stigter et al. (2000)|
|Romania||1998||Yes||Sefrová and Lastuvka (2001)|
|Russian Federation||2003||Yes||Gninenko and Orlinski (2004)|
|Serbia||1987||Yes||Petkovic (1989); Sivicek et al. (1997)|
|Slovakia||1996||Yes||Sivicek et al. (1997)|
|Slovenia||1995||Yes||Milevoj and Macek (1997)|
|Spain||2002||Yes||Villalva and Del Estal (2003)|
|Switzerland||1999||Yes||Kenis and Forster (1998)|
|Turkey||2004||Yes||Cebeci and Acer (2007)|
|UK||2002||Yes||Tilbury et al. (2004)|
|Ukraine||2002||Yes||Akimov et al. (2003)|
Habitat ListTop of page
|Terrestrial – Managed||Managed forests, plantations and orchards||Secondary/tolerated habitat||Harmful (pest or invasive)|
|Rail / roadsides||Principal habitat||Harmful (pest or invasive)|
|Urban / peri-urban areas||Principal habitat||Harmful (pest or invasive)|
|Terrestrial ‑ Natural / Semi-natural||Natural forests||Principal habitat||Harmful (pest or invasive)|
|Natural forests||Principal habitat||Natural|
Hosts/Species AffectedTop of page
C. ohridella lives primarily on the leaves of Aesculus hippocastanum, but successful development is also occasionally observed on Acer pseudoplatanus and Acer platanoides. It also develops on some species of the genus Aesculus, but not on others (Skuhravý, 1998; Hellrigl, 2001; Freise, 2001). Freise et al. (2003a) and Kenis et al. (2005) carried out screening tests on most of the world Aesculus spp. and several Acer spp. to assess the present or potential host range of C. ohridella. The two most suitable hosts were A. hippocastanum and the Japanese horse-chestnut A. turbinata, whereas successful development also occurred on the American species A. glabra, A. sylvatica and A. flava (= A. octandra). In contrast, it did not develop successfully on the Asian A. chinensis, A. assamica and A. indica and on the American A. pavia, A. californica and A. parviflora. Larvae also developed successfully, but often failed to pupate, in the North American A. circinatum and, occasionally, in the European A. pseudoplatanus, A. tataricum and A. heldreichii, and the Asian A. japonicum.
Host Plants and Other Plants AffectedTop of page
|Acer platanoides (Norway maple)||Aceraceae||Other|
|Acer pseudoplatanus (sycamore)||Aceraceae||Other|
|Aesculus flava (yellow buckeye)||Hippocastanaceae||Other|
|Aesculus glabra (Texas buckeye)||Hippocastanaceae||Other|
|Aesculus hippocastanum (horse chestnut)||Hippocastanaceae||Main|
|Aesculus sylvatica (Painted buckeye)||Hippocastanaceae||Other|
|Aesculus turbinata (Japanese horse-chestnut)||Hippocastanaceae||Main|
SymptomsTop of page
Larvae of C. ohridella form blotch mines and develop in the parenchyma tissue of leaves of Aesculus hippocastanum. The mines start off small and yellow, later turning brown. Eventually the mines may cover the entire surface of the leaflets, especially from July on, when the second and third generations develop. At sites where dead leaves containing overwintering pupae are not removed in the autumn, trees are usually totally defoliated, year after year.
List of Symptoms/SignsTop of page
|Leaves / internal feeding|
|Leaves / yellowed or dead|
Biology and EcologyTop of page
C. ohridella overwinters in the pupal stage in a cocoon in dead leaves. The emergence of C. ohridella adults in spring occurs between the beginning of April and the second half of May, depending on climatic conditions (Pschorn-Walcher, 1994; Freise, 2001; Hellrigl, 2001; Girardoz et al., 2007a; Ivanov et al., 2007). Male eclosion starts 2-5 days earlier than for females. At this time both males and females regularly sit on the trunks or on the lower branches of Aesculus. They usually fly from 06:00 h to 12:30 h with a peak at 08:00-09:30 h.
After mating, each female may lay up to 180 eggs (Girardoz et al., 2007a); each egg is laid singly on the upper part of the leaflets, mostly near the veins. Females of the second and third generations lay eggs on all leaflet surfaces.
Larval development lasts 25-35 days with the larva developing through four, occasionally five, feeding instars and two spinning instars (Deschka, 1995; Skuhravý, 1998; Freise and Heitland, 2004). First-instar larvae make only a small gallery. The second- and third-instar larvae develop a round mine of 4-7 mm in average diameter. Special adaptations of the mouth parts enable the caterpillars to cut or scrape the leaf parenchyma inside the mines. The mine of the fourth instar increases to 4-7 cm². The larva digests liquid or pappy food. The larva then goes through two spinning instars (see Images), which may or may not build a true cocoon in the mine. The percentage of larvae which spin true cocoons increases in each of the subsequent generations. In the first generation, only 5-13% of larvae spin cocoons, in the second 20-35% and in the third generation nearly all larvae spin cocoons. Pupae of C. ohridella may survive low temperatures from -19.5-23°C (Kovacz and Lakatos, 1999).
Adults of the first generation emerge from mid-June to late-July. C. ohridella has two to four generations a year, depending on the temperature conditions. There will only be two generations in higher altitudes and colder conditions whereas, in warmer areas, up to four generations may develop (Pschorn-Walcher, 1994; Hellrigl, 2001; Freise and Heitland, 2004; Girardoz et al., 2007a; Ivanov et al., 2007). During the summer and autumn, the eggs, larvae, pupae and adults occur simultaneously.
Larvae of C. ohridella damage leaves by feeding between the upper and lower parenchyma. The mine starts to turn yellow and later brown. At this time the damage is very visible. Trees with a low number of attacked leaves are not greatly affected, but when the entire surface of leaves is covered with mines, the leaves start to dry out and fall off. However, total defoliation does not seem to affect the growth of mature trees (Salleo et al., 2003).
In the non-overwintering generations, mortality is usually low, which allows populations to grow fast. The main mortality factors occur in the last generation of the year. Firstly, when populations are high, larvae may die from intra-specific competition and leaf senescence that occurs earlier than normal (Pschorn-Walcher, 1994; Freise and Heitland, 2004; Girardoz et al., 2007a). Secondly, synchronization between larval development and leaf fall is often not perfect and, some years, many larvae die because they cannot complete their development before leaf senescence (Girardoz et al., 2007b). Finally, overwintering mortality of pupae in dead leaves is usually very high, because most leaves are destroyed, blown away or eaten by detritivores (Girardoz et al., 2007a).
ClimateTop of page
|C - Temperate/Mesothermal climate||Tolerated||Average temp. of coldest month > 0°C and < 18°C, mean warmest month > 10°C|
|Cf - Warm temperate climate, wet all year||Tolerated||Warm average temp. > 10°C, Cold average temp. > 0°C, wet all year|
|Cs - Warm temperate climate with dry summer||Tolerated||Warm average temp. > 10°C, Cold average temp. > 0°C, dry summers|
|D - Continental/Microthermal climate||Preferred||Continental/Microthermal climate (Average temp. of coldest month < 0°C, mean warmest month > 10°C)|
|Df - Continental climate, wet all year||Preferred||Continental climate, wet all year (Warm average temp. > 10°C, coldest month < 0°C, wet all year)|
Latitude/Altitude RangesTop of page
|Latitude North (°N)||Latitude South (°S)||Altitude Lower (m)||Altitude Upper (m)|
Air TemperatureTop of page
|Parameter||Lower limit||Upper limit|
|Absolute minimum temperature (ºC)||-34|
|Mean annual temperature (ºC)||6||18|
|Mean maximum temperature of hottest month (ºC)||21||33|
|Mean minimum temperature of coldest month (ºC)||-8||6|
RainfallTop of page
|Parameter||Lower limit||Upper limit||Description|
|Dry season duration||0||6||number of consecutive months with <40 mm rainfall|
|Mean annual rainfall||400||1500||mm; lower/upper limits|
Natural enemiesTop of page
|Natural enemy||Type||Life stages||Specificity||References||Biological control in||Biological control on|
|Lecanicillium aphanocladii||Pathogen||Larvae||Peciulyte and Kacergius, 2012|
Notes on Natural EnemiesTop of page
Among natural enemies, parasitoids have been by far the most widely studied (e.g. Hellrigl and Ambrosi, 2000; Freise et al., 2002; Grabenweger, 2003; Grabenweger et al., 2005a; Girardoz et al., 2006; Grabenweger et al., 2010). Over 30 indigenous leaf miner parasitoid species have already been reared from C. ohridella in Europe. The majority are polyphagous species of the family Eulophidae (Chalcidoidea) but Eupelmidae, Pteromalidae, Braconidae and Ichneumonidea are also occasionally recorded. In Western and Central Europe, the main parasitoids are the ectoparasitoid eulophids Minotetrastichus frontalis, Pnigalio agraules and, to a lesser extent, the endoparasitoids Chrysocharis nephereus, Closterocerus trifasciatus and Pediobius saulius. In Eastern Europe and the Balkans, the same species are present, but there the parasitoid complex is usually dominated by the pupal endoparasitoid P. saulius. All these parasitoids are polyphagous parasitoids of leaf miners in Europe, attacking a wide range of hosts in various insect orders, although host-specific biotypes or sibling species cannot be excluded (Girardoz et al., 2007c). Details on the biology of the parasitoids of C. ohridella may be found in various publications, e.g. Freise et al. (2002), Grabenweger (2003, 2004), Grabenweger et al. (2005a), Girardoz et al. (2006) and Volter and Kenis (2006). A key to the parasitoids of C. ohridella in Europe is provided by Grabenweger et al. (2003).
Several methods have been used to calculate parasitism rates of C. ohridella (Volter and Kenis, 2006). However, no matter the method, parasitism rates are usually very low compared to other leaf miners. Total parasitism rates typically vary between 1 and 20% (e.g.Hellrigl, 2001; Freise et al., 2002; Grabenweger, 2003; Freise and Heitland, 2004; Grabenweger et al., 2005a; Girardoz et al., 2006; Volter and Kenis, 2006; Girardoz et al., 2007a, b; Grabenweger et al., 2010). Parasitism is usually higher on spinning stages and pupae than on feeding larvae and does not vary significantly from one generation to another. Girardoz et al. (2006) found no difference in parasitism rate and the composition of the parasitoid complex between forest and urban sites and, in the Balkans, Grabenweger et al. (2005a; 2010) showed that parasitism is similar in natural horse-chestnut stands and on urban trees.
Parasitoids most probably play a minor role in the population dynamics of the moth, including in the probable area of origin in the Balkans (Freise et al., 2002; Grabenweger et al., 2005a; 2010). One reason for the low parasitism in C. ohridella is poor synchronization between parasitoid emergence in spring and the phenology of C. ohridella. The bulk of parasitoids emerge from dead leaves 6-8 weeks before suitable larvae and pupae of C. ohridella are available (Grabenweger, 2004; Girardoz et al., 2006). However, there must be other factors limiting parasitism in C. ohridella. There is no other Cameraria species occurring in Europe, nor any other leaf miner on horse-chestnut. Therefore, there may be physiological or chemical barriers that hamper the full adoption of C. ohridella by native parasitoids. Girardoz et al. (2007c) did not find higher parasitism or more parasitoid species on C. ohridella populations attacking maple, suggesting that host plant is not the major cause for low parasitism.
Predation was investigated by Grabenweger et al. (2005b) and Girardoz et al. (2007a, b) in Austria, Switzerland and Bulgaria. Blue tits (Parus caeruleus), great tits (P. major) and marsh tits (P. palustris) preyed on mature larvae and pupae of C. ohridella. Mines were also commonly opened by invertebrate predators. Various species were found on infested trees, but only the southern oak bushcricket (Meconema meridionale) and the lacewing (Chrysopa carnea) were observed preying on C. ohridella. The bushcricket is probably the most important invertebrate predator of C. ohridella in Austria. In laboratory tests, third- and fourth-instar larvae suffered heavy attacks whereas young larvae, spinning stages and pupae were neglected. In northern Italy, Radeghieri et al. (2004) observed workers of the acrobat ant (Crematogaster scutellaris) preying on larvae and pupae of C. ohridella. Predation rates may vary significantly between studies and countries. Birds caused 2-4% mortality in Austria (Grabenweger et al., 2005b) and 3% in Bulgaria (Girardoz et al., 2007b), but 16% in Switzerland, with up to 41% in some generations (Girardoz et al., 2007b). In contrast, predation by invertebrates was responsible for an average of 10% mortality in Bulgaria and 2% in Switzerland (Girardoz et al., 2007b).
Means of Movement and DispersalTop of page
The fast dispersal of the moth, which spread from Macedonia to most of Europe in less than 20 years, is attributed mainly to human transport. Cars, lorries, trains and other vehicles may carry adults and overwintering pupae in dead leaves (Augustin et al., 2009). Some long-distance jumps have also been attributed to the transportation of infested seedlings (Gilbert et al., 2005). The natural dispersal capacity of adults is poorly known. Long-distance dispersal by wind cannot be excluded although the fact that it has taken so long for the moth to move from natural horse-chestnut stands in the Balkans to planted trees in urban areas in the same region suggests that it does not migrate very easily by itself (Valade et al., 2009). The regional spread of C. ohridella has been analysed in detail in Germany by Gilbert et al. (2004) and in France by Augustin et al. (2004) and Gilbert et al. (2005). They compared the performances of several invasion models and found that the best model to describe the spread of C. ohridella was a stratified dispersal model taking into account the effect of human population density on the probability of long-distance dispersal events. Within cities, the moth probably disperses by flight and in dead leaves that are blown away (Gilbert et al., 2003).
The natural dispersal capacity of adults is poorly known. Long-distance passive dispersal cannot be excluded although the fact that it has taken so long for the moth to migrate from natural horse-chestnut stands in the Balkans to planted trees in urban areas in the same region suggest that it does not migrate very easily by itself (Valade et al., 2009). Locally, the moth disperses by flight, in dead leaves that are blown away (Gilbert et al., 2003) and probably also by garden waste disposal.
The fast dispersal of the moth, which spread from Macedonia to most of Europe in less than 20 years, is attributed mainly to human transport. Cars, lorries, trains and other vehicles may carry adults and overwintering pupae in dead leaves. Some long-distance jumps have also been attributed to the transportation of infested seedlings. The regional spread of C. ohridella has been analysed in detail in Germany by Gilbert et al. (2004) and in France by Augustin et al. (2004) and Gilbert et al. (2005). They compared the performances of several invasion models and found that the best model to describe the spread of C. ohridella was a stratified dispersal model taking into account the effect of human population density on the probability of long-distance dispersal events.
Pathway CausesTop of page
Pathway VectorsTop of page
|Bulk freight or cargo||Yes||Gilbert et al., 2004; Gilbert et al., 2005|
|Debris and waste associated with human activities||Yes||Kehrli and Bacher, 2004|
|Land vehicles||Railway wagons, TIR (international road transport) vehicles||Yes|
|Plants or parts of plants||Yes||Yes||Gilbert et al., 2005|
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|
|Leaves||eggs; larvae; pupae||Yes||Yes||Pest or symptoms not visible to the naked eye but usually visible under light microscope|
|Seedlings/Micropropagated plants||eggs; larvae; pupae||Yes||Yes||Pest or symptoms not visible to the naked eye but usually visible under light microscope|
Impact SummaryTop of page
ImpactTop of page
Although outbreaks usually continue unabated, causing severe aesthetic damage to horse-chestnut, studies in Italy showed that there is little or no impact on tree survival and tree growth in urban areas (Salleo et al., 2003). Furthermore, in Macedonia, trees still survive after 30 years of heavy outbreak. This would suggest that there is no immediate danger for the tree. However, in Germany, C. ohridella is suspected to cause the decline of horse-chestnut because defoliation induces a second flowering, decreasing frost hardness (Balder et al., 2004). Social, cultural and economic impacts of C. ohridella are difficult to assess. Despite a low risk for the survival of the trees in urban areas, the aesthetic damage is so severe that many municipalities are replacing this highly valuable tree by other species. In Germany, Reinhardt et al. (2003) estimated that the additional leaf removal caused by C. ohridella costs about 8 million Euro per year. The replacement costs for the all horse-chestnut trees in Germany would be as high as 10.7 billion Euro.
Economic ImpactTop of page
Studies in Italy showed that there is little or no impact on tree survival and tree growth in urban areas (Salleo et al., 2003). Furthermore, in the Balkans trees still survive after more than 20 years of heavy outbreak. This would suggest that there is no immediate danger for the tree. However, in Germany, C. ohridella is suspected to cause the decline of horse-chestnut because defoliation induces a second flowering, decreasing frost hardness (Balder et al., 2004). In Germany, Reinhardt et al. (2003) estimated that the additional leaf removal caused by C. ohridella costs about 8 million Euro per year. Despite a low risk for the survival of the trees in urban areas, the aesthetic damage is so severe that many municipalities are replacing this highly valuable tree by other species. The replacement costs for the all horse-chestnut trees in Germany would be as high as 10.7 billion.
Environmental ImpactTop of page
The horse-chestnut is endemic to the Balkans. Valade et al. (2009) recently showed, using molecular tools, that C. ohridella probably originates from natural horse-chestnut stands in Macedonia, Albania and Greece. In these stands, damage is often less severe (Ivanov et al., 2007; Tomov et al., 2007). In contrast, the moth is most probably invasive in the only natural stand in Bulgaria, where damage is as severe as in other invaded regions (Girardoz et al., 2007b). In natural forests heavy defoliation may hamper the regeneration process, causing concern for the survival of this rare tree species (Thalmann, 2003; Thalmann et al., 2003). In addition, C. ohridella is occasionally found attacking and developing on maple trees (Acer pseudoplatanus and A. platanoides), on which damage levels may be as high as on horse-chestnut (Hellrigl, 2001; Freise et al., 2003a; Péré et al., 2010a). It cannot be ruled out that the damage on maple will increase with time, considering the constant pressure on the moth to find suitable new host trees when horse-chestnut trees are totally defoliated. Péré et al. (2010b) also found that some native leaf miners are less abundant in the vicinity of heavily infested horse-chestnut trees, but the mechanisms underlying this effect are still unclear (Péré et al., 2011).
Threatened SpeciesTop of page
Social ImpactTop of page
Horse-chestnut is a highly valued ornamental tree in Central European cities. It is often a key element in urban parks and historical areas, including in touristic areas. It is also often used as shade tree in outdoor restaurants and bars. Because of the spectacular damage caused to horse-chestnut in cities, C. ohridella has become one of the best known invasive species in Europe.
Risk and Impact FactorsTop of page Invasiveness
- Invasive in its native range
- Proved invasive outside its native range
- Abundant in its native range
- Tolerates, or benefits from, cultivation, browsing pressure, mutilation, fire etc
- Highly mobile locally
- Benefits from human association (i.e. it is a human commensal)
- Fast growing
- Has high reproductive potential
- Host damage
- Negatively impacts tourism
- Reduced amenity values
- Highly likely to be transported internationally accidentally
- Difficult/costly to control
Detection and InspectionTop of page
In spring, adults emerging from overwintering pupae can be detected by pheromone trapping or by inspecting the trunks of Aesculus hippocastanum for moths. Later in the season, mines are usually very numerous and easily detected on the leaves.
Similarities to Other Species/ConditionsTop of page
In Europe C. ohridella is the only leaf miner on Aesculus hippocastanum but may be confused with other Gracillariidae, especially Phyllonorycter spp., feeding on Acer spp. The most important differences between the caterpilllars of C. ohridella and those of Phyllonorycter, are presented in Sefrova and Skuhravy (2000).
The leaves of A. hippocastanum may also be attacked by the fungus Guignardia aesculi. Attack by this fungus is characterized by irregular brown blotches with yellow haloes on leaflets (Buczacki and Harris, 2000). The leaflets turn red and brown from the margins and no mines are detected (see Images). Attack by G. aesculi may occur at the same time as attack by C. ohridella.
Prevention and ControlTop of page
C. ohridella can be controlled by aerial spraying of diflubenzuron. It is commonly used in some countries, such as Austria or the Czech Republic, but not registered in others (e.g. Germany, Switzerland). It is especially used on high value trees and touristic and scenic areas. When properly applied on eggs in the first generation, the trees remain green until the end of the summer. The timing can be defined using pheromone traps. However, spraying chemicals on large urban trees is rather expensive and not liked by a significant part of the public. It probably affects other invertebrates, including beneficials. Furthermore, technical problems arise with the treatment of high trees, which require platforms or high pressure spraying machines. Therefore, the spray of diflubenzuron or other chemicals should be restricted to nurseries and highly valuable trees, especially at sites where leaves cannot be not fully removed in autumn; sprays should be always limited to the first generation.
Trees can also be protected by injecting a systemic insecticide in the stem. Stem injection has been tested in many countries, using various equipments and insecticides, but it is not widely registered and not commonly used. Costs are higher than for other control methods and injections tend to injure the trees, through necrosis and secondly infections.
Leaf removal is the most widely used control method. Dead leaves containing overwintering pupae can be removed in autumn, or even until early spring, and burned or composted (Kehrli and Bacher, 2003, 2004). In favourable conditions (i.e. when all trees are cleaned and all leaves are removed in the near neighbourhood), this method provides a sufficient level of control by itself, and trees may remain green at least until late summer. When possible, bushes at the bottom of the tree should be removed to facilitate leaf removal.
In many regions, city gardeners have already started to replace horse-chestnut by other ornamental trees. It is not always feasible because of the high value of mature urban trees. However, it should be considered for trees that are of little ornamental interest, where leaves are not removed and which can act as reservoir for C. ohridella.
Sex pheromones are sensitive and a highly specific monitoring tool (Svatos et al., 1999a, b; Kalinova et al., 2003). However, for the moment, pheromone-based methods by themselves are not likely to provide satisfying control. Mass-trapping (attract-and-kill) methods are hampered by the very high densities of C. ohridella. Sexual confusion methods have been tested (Siekmann et al., 2009) but are hindered by technological problems and the characteristics of urban plantations.
C. ohridella has been adopted by a whole complex of polyphagous parasitoid and predator species (e.g. Hellrigl, 2001; Freise et al., 2002; Grabenweger, 2003; Grabenweger et al., 2005a, b; Girardoz et al., 2007a, b; Grabenweger et al., 2010). Nevertheless, parasitism and predation remain low, even at the type location 30 years after its arrival (Grabenweger et al., 2005a, b; Girardoz et al., 2007b; Grabenweger et al., 2010). Kehrli et al. (2005) have developed a system to augment parasitism at the local scale. They stored dead leaves with overwintering moths in containers that, at emergence, allow the parasitoids to escape without their host. They observed increased parasitism rates at the experimental plots, but no effect on moth populations. Similarly, Klug et al. (2008) could increase parasitism rates by the release of Pnigalio agraules, but no long term effect was observed. In the long run, unless a native European natural enemy suddenly improves its capability of controlling the moth, the only sustainable solution to the C. ohridella problem would be the introduction of an exotic natural enemy. Classical biological control against C. ohridella has long been constrained by the fact that the region of origin of the moth was unknown (Kenis et al., 2005). The recent discovery that the moth originates from remote horse-chestnut stands in the Balkans should encourage the search for new natural enemies in these areas (Valade et al., 2009).
ReferencesTop of page
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OrganizationsTop of page
France: INRA, Station de Zoologie Forestière, CS 40001 Ardon 45075, Orléans Cedex 2, http://www.orleans.inra.fr/
Switzerland: CABI Europe - Switzerland, 1 Rue des Grillons, 2800 Delémont, www.cabi.org
UK: Forest Research, Alice Holt Lodge, Farnham Surrey GU10 4LH, http://www.forestresearch.gov.uk
ContributorsTop of page
20/10/2011 Updated by:
Marc Kenis, CABI Europe - Switzerland, 1 Chemin des Grillons, CH-2800 Delémont, Switzerland
12/05/2009 Updated by:
Marc Kenis, CABI Europe - Switzerland, 1 Chemin des Grillons, CH-2800 Delémont, Switzerland
Distribution MapsTop of page
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