Preferred name: Nemorimyza maculosa
Authority: (Malloch)
Taxonomic position: Animalia: Arthropoda: Hexapoda: Insecta: Diptera: Agromyzidae
Other scientific names: Agromyza guaranitica Brethes, Agromyza maculosa Malloch, Amauromyza maculosa (Malloch), Dizygomyza maculosa Blanchard, Phytobia maculosa (Malloch)
Common names in English: burdock leaf miner, chrysanthemum leaf miner
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Notes on taxonomy and nomenclature EPPO Categorization: A1 list
EU Categorization: A1 Quarantine pest (Annex II A)
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EPPO Code: AMAZMA

Feeding widely on Asteraceae, N. maculosa has been recorded on more than 30 genera of host plants in this family. In the EPPO region the potential host range would include ornamental plants such as Aster spp., chrysanthemums, Dahlia spp., as well as vegetable crops such as lettuce (Lactuca sativa), sunflower (Helianthus annuus) and artichoke (Cynara cardunculus) (Spencer, 1990; Benavent-Corai et al., 2005; Eisman & Lonsdale, 2019; Monteiro et al., 2019). Isolated reports on Brassicaceae, Solanaceae and Convolvulaceae (Sanabria de Arevalo, 1994; Spencer et al., 1992) are considered doubtful and require further confirmation (EFSA, 2020).

Host list: Acanthospermum sp., Ageratum conyzoides, Arctium lappa, Arctotis sp., Argyranthemum frutescens, Artemisia vulgaris, Aster sp., Baccharis douglasii, Baccharis halimifolia, Bellis sp., Bidens alba, Bidens pilosa, Calendula officinalis, Chromolaena odorata, Chrysanthemum indicum, Chrysanthemum x morifolium, Chrysanthemum, Conyza apurensis, Conyza sp., Cynara cardunculus, Dahlia pinnata, Emilia coccinea, Emilia fosbergii, Emilia sonchifolia, Erechtites hieraciifolius, Erechtites valerianifolius, Erigeron canadensis, Eupatorium sp., Gaillardia aristata, Gamochaeta pensylvanica, Gerbera jamesonii, Gnaphalium sp., Grindelia squarrosa, Helenium sp., Helianthus annuus, Lactuca sativa, Lagascea mollis, Leucanthemum vulgare, Leucanthemum x superbum, Melanthera aspera, Melanthera nivea, Mikania micrantha, Packera glabella, Pericallis x hybrida, Solidago sp., Sonchus asper, Symphyotrichum novi-belgii, Synedrella nodiflora, Tagetes erecta, Tagetes patula, Tagetes sp., Tagetes tenuifolia, Tanacetum parthenium, Tanacetum vulgare, Taraxacum sp., Tithonia rotundifolia, Zinnia elegans

Originally described from the United States, N. maculosa probably originated from tropical or subtropical areas of South America, as suggested by its current distribution. Supporting this hypothesis, the leaf miner is found outdoors in warmer eastern USA states, while in the most northern states and in Canada, it occurs in greenhouses (EFSA, 2020). This species is widely distributed in the Americas, particularly in the Neotropical area (Spencer, 1990; Martinez & Etienne, 2002; Valladares et al., 2011; Valenzuela-Escoboza et al., 2017; Lonsdale, 2021; Monteiro et al., 2019. The first records of N. maculosa for the Old World and specifically the EPPO Region are relatively recent and restricted to isolated areas (Madeira and Canary Islands) (Černý et al., 2018). Given the considerable touristic movement between the Atlantic islands and Continental Europe, it might be only a question of time until the leaf miner becomes transferred to plant hosts on the continent (Černý et al., 2018).

EPPO Region: Portugal (Madeira), Spain (Islas Canárias)
North America: Canada (Ontario), Mexico, United States of America (California, Connecticut, Florida, Georgia, Hawaii, Indiana, Kentucky, Massachusetts, New York, North Carolina, Ohio, Oklahoma, Wisconsin)
Central America and Caribbean: Bahamas, Barbados, Bermuda, Cayman Islands, Costa Rica, Cuba, Dominican Republic, Guadeloupe, Jamaica, Martinique, St Kitts-Nevis, Trinidad and Tobago
South America: Argentina, Bolivia, Brazil (Para), Chile (Easter Island), Colombia, French Guiana, Guyana, Peru, Uruguay, Venezuela

Nemorimyza maculosa is multivoltine, completing several generations in one year. Ota & Nishida (1966) recorded a development time of 22 to 28 days at about 26°C (3–4 days for eggs, 6–8 days for larvae and 13–16 days for pupae). Duration of the life cycle varies with temperature and host plants, e.g. on artichoke (at 24 - 26°C) the life cycle of N. maculosa lasted 22.6 days (eggs hatched in 2 days; first and second larval instars lasted 2 days each, third instar took 3 days, and the pupa lasted 11 to 14 days) whereas on sunflower the life cycle took 19.8 days in total (egg, first and second larval instars lasted 1-2 days each one; third larval instar 2.5 - 3 days, and pupa 10 - 12 days) (Enriquez et al., 2014). Sex ratio (M: F) was 1: 1.5.

Oviposition begins at sunrise, peaks between mid-morning and noon, then decreases towards sunset. Females insert usually 2 – 4 eggs close to each other under the leaf epidermis and near the leaf margins. Total number of eggs and length of the oviposition period varied with individual flies and with the host plant (Ota & Nishida 1966). In young leaves, egg extrusion might lead to increased mortality if eggs are ejected by the growing tissue and thus exposed to the external environment (Enriquez et al., 2014; Videla & Valladares, 2007). After hatching, larvae feed within the leaf, consuming the mesophyll and creating a large communal blotch mine (i.e. a mine where several larvae are developing). Third instar larvae cut semicircular exit slits in the leaf epidermis and drop to the ground where they pupate under debris or up to 3 cm into the soil.

Adults emerge from pupariae mostly between 6 and 11 a.m.; they are diurnal, most active during the morning. Adult females live longer than males. Otta & Nishida (1966) recorded a lifespan of 14 days for females and 7 days for males, but much longer adult lifespans (females: 36 – 41 days, males: 21 – 32 days) and significant host plant effects on longevity were found by Enriquez et al. (2014). Female flies use their ovipositor to puncture host plant leaves, causing wounds which serve as sites for oviposition but also for feeding on the sap exudates. This causes whitish or brown stipples on the leaves, with feeding punctures destroying more cells and being more clearly visible than oviposition punctures. Males are unable to puncture leaves but they feed at the punctures produced by females. In the laboratory, both males and females feed on dilute honey (Ota & Nishida, 1966; Enriquez et al., 2014).

Symptoms

The first symptom of leaf miner attack on plants is leaf stippling, caused by feeding and oviposition punctures which appear as white (sometimes becoming brown) speckles, about 0.15 mm in diameter. Oviposition punctures tend to be smaller and more uniformly round.

Feeding by N. maculosa larvae produces a conspicuous blotch mine, which is more noticeable on the upper side of the leaves. The mine is initially whitish and soon becomes predominantly brown with dampened black areas. Most of the mesophyll (upper as well as lower parenchyma) is consumed, leading to necrosis of the affected area. Several larvae (frequently 2 - 8) are found within a wide communal mine, which usually lacks the initial linear tract seen in blotch mines of other species such as N. posticata (Eiseman & Lonsdale, 2018).

A positive identification requires examination of the adult flies. Nemorimyza maculosa is easily differentiated from the other species in the genus by having a distinctive dark spot on the otherwise white halteres; whitish squamae and fringe; dorsocentral presutural seta present; black abdomen and curved, divergent tubules of the bifid distiphallus (Monteiro et al., 2019; Sousa & Couri, 2021). The combination of presence of prescutellar bristles and Phytomyzinae-like wing vein pattern also help the identification (Dempewolf, 2004).

Morphology

Eggs

Oval, 0.20-0.37 mm x 0.10-0.20 mm, off-white and slightly translucent (Ota & Nishida, 1966; EFSA, 2020).

Larva

A headless maggot, yellowish white, up to 4.6 mm long when fully grown; posterior spiracles of larva (and puparium) paired, each with three pores. The puparium is oval, slightly flattened ventrally, 2.2-2.8 mm long, turning from creamy yellow to dark brown (Ota & Nishida, 1966; Enriquez et al., 2014).

Adult

Small, shiny black, compact-bodied flies, about 2.2 to 2.7 mm in body length. Wing length 2.2-2.3 mm (males), 2.2-3.1 mm (females). Head, mesonotum, pleura and legs entirely black; squamae and fringe silvery white; halteres mostly white, but knob with a conspicuous dark spot above (Spencer, 1973; Lonsdale, 2021). Females are larger than males and body size varies depending on larval host plant (Enriquez et al., 2014). Distinctive male genitalia: distiphallus with broad, dark, basal section apically ending in a pair of pale diverging and curved tubules almost as long as basal section (Monteiro et al., 2019; Lonsdale, 2021).

Detection and inspection methods

Visual inspection of leaves searching for blotch leaf mines and feeding / oviposition punctures, should allow detection of infested plant material. Mined leaves should then be incubated to obtain adults for a more reliable identification, which might need to be referred to a specialist. Morphological keys for adults are available to identify the species (e.g. Spencer, 1963; Spencer & Steyskal, 1986; De Sousa & Couri, 2021).

Inspection of crops can also be carried out in situ, again by visual inspection of leaves followed by adult rearing. Adult leaf miner flies can be monitored by sweeping with gauze nets over Asteraceae crops or associated vegetation (e.g. Černý et al., 2018); by using Malaise or water traps (Scheirs et al., 1997), or by placing yellow sticky traps in fields and, for protected crops, using traps in greenhouses (Monica et al., 2021).

Adult flies are capable of limited flight, although they may be carried passively by wind currents (Yoshimoto & Gressitt, 1964). Dispersal over long distance is mediated by transportation of host plant material. Even cut flowers can present a risk as a means of dispersal considering, for example, that the vase life of chrysanthemums is sufficient to allow completion of the life cycle of the pest (Spencer, 1973).

Economic impact

The large blotch mines of N. maculosa cause considerable damage to chrysanthemums and other glasshouse ornamentals (Weigel, 1923; Weigel & Sasser, 1923; Stegmaier, 1967). Although there are few reports of serious outbreaks, even slight damage to plants in the flower industry can cause economic losses. In California, USA, regular low-level damage to young plants calls for constant vigilance (EFSA, 2020). Severe damage to lettuce crops has also been reported (Spencer, 1973).

Damage is caused by females puncturing leaves for feeding and oviposition and by subsequent larval mining within leaves. The photosynthetic ability of the plants is often greatly reduced as the chlorophyll-containing cells are destroyed, reducing plant metabolism and vigour (Spencer, 1973). Severely infested leaves may fall, consequently exposing plant stems to wind action, whereas flower buds and developing fruit could be damaged by excessive sunlight exposure (Musgrave et al., 1975). Aesthetic damage resulting from the presence of unsightly larval mines and adult punctures in edible leaves (e.g. lettuce) or ornamental plants can further reduce the value of crops or even render them unmarketable (Smith et al., 1962; Musgrave et al., 1975; Dempewolf, 2004). In young plants and seedlings, mining may cause considerable delay in plant development leading to plant loss. Leaf miner damage may also facilitate penetration of bacterial and fungal pathogens into the leaves via female feeding punctures (Dempewolf, 2004).

Control

Some insecticides, particularly pyrethroids, are effective but leaf miner resistance can make control difficult (Parrella et al., 1984). Translaminar insecticides such as abamectin, cyromazine, spinosyns and azadirachtine (Reitz et al., 2013) have shown efficacy against leaf miner larvae while being compatible with biological control (Kaspi & Parrella, 2002; Salvo & Valladares, 2007; Mani, 2022).

Natural enemies represent a strong mortality source for leaf miners and periodically suppress their populations (Spencer, 1973). Leaf miner predators include birds, spiders and insects (Coleoptera, Hemiptera), whereas parasitoids include Hymenoptera species within Eulophidae, Pteromalidae, Braconidae and Figitidae. Conservation biological control and inoculative releases, mainly of parasitoid insects, are being considered as relevant strategies for control of leaf miner pest species (Salvo & Valladares, 2007). Parasitoids of N. maculosa include Chrysocharis sp., Diaulinopsis callichroma, Derostenus variipes, Derostenus sp. in Florida (Stegmaier, 1967); Opius sp. (Hym: Braconidae), Halticoptera sp. (Hym: Pteromalidae), Ganaspidium sp. (Hym: Eucoilidae), Chrysocharis sp. (Hym: Eulophidae) in Peru (Enriquez et al., 2014), and Phaedrotoma mesoclypealis in Argentina, the latter causing 19% parasitism on N. maculosa (Valladares et al., 1999).

Phytosanitary risk

Nemorimyza maculosa has the potential to become a major pest of a wide variety of ornamental and vegetable crops grown under glass or as protected crops in the EPPO region. This species could also cause damage to crops grown in the open in the warmer parts of the region. Given its presence in relatively close island areas, it seems likely that the species could establish in the continental part of the EPPO region (Černý et al., 2018).

The different life stages of the leaf miner could use different pathways to enter the EPPO region. Eggs and larvae could be introduced either within plants for planting with foliage, or within fresh leafy hosts for consumption (e.g. lettuce) or within cut flowers and branches with foliage (e.g. chrysanthemums, dahlias). Pupae could be transported within soil and growing media, but the import of soil or growing medium as such from third countries is prohibited in most EPPO member countries, therefore the entry of N. maculosa pupae is prevented.

All stages are killed within a few weeks by cold storage at 0°C. Newly laid eggs are, however, the most resistant stage and therefore it is recommended that cuttings of infested ornamental plants be maintained under normal glasshouse conditions for 3-4 days after lifting, to allow eggs to hatch. Subsequent storage of the plants at 0°C for 1-2 weeks should then kill off the leaf miner larvae (Webb & Smith, 1970; CABI, 2022).

To avoid the introduction of N. maculosa (and other leaf miner pest species such as Liriomyza huidobrensis, L. trifolii and L. sativae), it could be recommended that plants for planting (except seeds) of host plants, such as chrysanthemums, Aster, Gerbera, Calendula, Cynara, lettuces, sunflower, from countries where the pest occurs must have been inspected at least every month during the previous 3 months and found free from the pest. General guidance on how to conduct inspections of places producing vegetable plants for planting under protected conditions can be found in the EPPO Standard PM 3/77 (EPPO, 2022). It could also be recommended that consignments of cut flowers and leafy vegetables should originate from a country free from N. maculosa or should have been inspected and found free from the pest immediately before export.

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This datasheet was extensively revised in 2023 by Graciela Valladares, Centro de Investigaciones Entomologicas de Cordoba, Universidad Nacional de Cordoba – CONICET) (Retired). Her valuable contribution is gratefully acknowledged.

EPPO (2024) Nemorimyza maculosa. EPPO datasheets on pests recommended for regulation. https://gd.eppo.int (accessed 2024-04-27)

This datasheet was first published in the EPPO Bulletin in 1984, as part of the datasheet on Liriomyza trifolii, and revised in the two editions of 'Quarantine Pests for Europe' in 1992 and 1997, as well as in 2023. It is now maintained in an electronic format in the EPPO Global Database. The sections on 'Identity', ‘Hosts’, and 'Geographical distribution' are automatically updated from the database. For other sections, the date of last revision is indicated on the right.

CABI/EPPO (1992/1997) Quarantine Pests for Europe (1^st and 2^nd edition). CABI, Wallingford (GB).

EPPO (1984) Data sheets on quarantine organisms No. 131 Liriomyza trifolii. EPPO Bulletin 14(1), 29-37. https://doi.org/10.1111/j.1365-2338.1984.tb01978.x