The leaf and stem mines of British flies and other insects
 

(Coleoptera, Diptera, Hymenoptera and Lepidoptera)

by Brian Pitkin, Willem Ellis, Colin Plant and Rob Edmunds

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TRIFOLIUM. Clovers and Hop Trefoil. [Fabaceae]


Seventy species of Trifolium are recorded in Britain. These include Hop Trefoil (T. campestre), Strawberry Clover (T. frageriferum), Alsike Clover (T. hybridum), Crimson Clover (T. incarnatum), Sulphur Clover (T. ochroleucon), Hungarian Clover (T. pannonicum), Red Clover (T. pratense) and White Clover (T. repens). The BSBI provide a downloadable plant crib for vegetative widespread species of Trifolium.

Sixteen British miners are recorded on Trifolium.

White clover - Trifolium repens. Image: © Brian Pitkin
White clover
Trifolium repens



Key for the identification of the known mines of British
Diptera recorded on Trifolium


Note: Diptera larvae may live in a corridor mine, a corridor-blotch mine, or a blotch mine, but never in a case, a rolled or folded leaf, a tentiform mine or sandwiched between two more or less circular leaf sections in later instars. Pupation never in a cocoon. All mining Diptera larvae are leg-less maggots without a head capsule (see examples). They never have thoracic or abdominal legs. They do not have chewing mouthparts, although they do have a characteristic cephalo-pharyngeal skeleton (see examples), usually visible internally through the body wall. The larvae lie on their sides within the mine and use their pick-like mouthparts to feed on plant tissue. In some corridor miners frass may lie in two rows on alternate sides of the mine. In order to vacate the mine the fully grown larva cuts an exit slit, which is usually semi-circular (see Liriomyza huidobrensis video). The pupa is formed within the hardened last larval skin or puparium and as a result sheaths enclosing head appendages, wings and legs are not visible externally (see examples).

See Key to non-Diptera.


1a > Leaf-miner: Linear mine in sepals and leaves. Puparium orange-brown

On Anthyllis, but not yet on Trifoloium,in Britain and this and other Fabaceae elsewhere. Known only from Devon in Britain and continental Europe.

Phytomyza brischkei Hendel, 1922 [Diptera: Agromyzidae].

1b > Leaf-miner: A distinctive mine primarily above mid-rib, with irregular short lateral offshoots into leaf blade. Pupation external (Spencer, 1972: 51 (fig. 172), 55; Spencer, 1976: 270, 271 (fig. 486)).

Branched, whitish, upper-surface corridor; main axis overlying the midrib; side branches overlying the main lateral veins. (In Campanula and Phyteuma the mine is much less branched, sometimes nothing more than a corridor on top of the midrib). Frass in rather long strings. Usually the mines begins as a long and narrow, shallow, tortuous lower-surface corridor that ends upon the midrib but otherwise is not associated with the leaf venation. Often this initial corridor is filled with callus, and then even less conspicuous. Pupation outside the mine (Bladmineerders van Europa).

A linear mine on the upper surface, usually following the midrib and showing side branches along the veins. The frass is in strings (British leafminers).

Polyphagous. On more than 40 host genera in 15 families, but not yet on Trifolium, in Britain,. Widespread throughout Britain. Also recorded in the Republic of Ireland. Widespread in continental Europe.

Liriomyza strigata (Meigen, 1830) [Diptera: Agromyzidae].

1c > Leaf-miner: Initially a linear mine running towards apex of leaf which then turns back and develops into a blotch in the area of the mid-rib (Spencer, 1972b: 37, fig. 114A; Spencer, 1976: 110, fig. 177).

Upper-surface corridor along the leaf margin, running from the leaf base to the tip. Once at the tip the corridor goes down over the midrib, widening considerably. Frass in the corridor part in a broad green central band, with minute black particles at either side. In the final, blotchy part frass in coarse black grains that may sometimes stick together. Pupation outside the mine (Bladmineerders van Europa).

Puparium reddish brown.

Agromyza frontella on Medicago sativa
Mines of Agromyza frontella on Medicago sativa
Image: © Whitney Cranshaw (Bladmineerders van Europa)

On Medicago, Melilotus and Trifolium in Britain and elsewhere. Widespread in Britain and continental Europe.

Agromyza frontella (Rondani, 1875) [Diptera: Agromyzidae].

1d > Leaf-miner: Larva producing a short narrow linear mine not associated with the margin, which then develops into a conspicuous white blotch centred on the mid-rib. At the end of feeding the larva lies for one or two days along the mid-rib. Pupation external (Spencer, 1972b: 37 (fig. 114b); Spencer, 1976: 126, fig. 213A).

Broad and short hook-like upper-surface corridor, ending in a little blotch in the centre of a leaflet. The blotch is upper-surface as well, but has some deep spots, giving the mine a mottled appearance when hold against the light. Frass in the blotch in a few large lumps. Pupation outside the mine (Bladmineerders van Europa).

A short, broad gallery leading to a conspicuous, roundish white blotch in the centre of the leaf. The blotch is upper surface with full depth spots - comprising of large clumps of frass (British leafminers).

. Puparium reddish

On Medicago, Melilotus and Trifolium in Britain and in addition other genera of Fabaceae elsewhere. Common and widely distributed in England. Also recorded in the Republic of Ireland. Widespread and common throughout Europe.

Agromyza nana Meigen, 1830 [Diptera: Agromyzidae].

1e > Leaf-miner: Mine linear, whitish, both upper and lower surface. Pupation internal, at the end of the mine with the anterior spiracles projecting through the epidermis (Spencer, 1976: 433).

Upper-surface, less often lower-surface corridor. Frass in isolated grains. Pupation within the mine, usually in a lower-surface puparial chamber (Bladmineerders van Europa).

A long whitish upper surface corridor, which eventually goes lower surface (British leafminers).

Two highly polyphagous species of Chromatomyia, with indistinguishable mines, have been recorded in Britain. These are syngenesiae (Hardy) and horticola (Goureau) which can only be distinguished by the male genitalia. Both species are widespread in Britain and elsewhere, although syngenesiae is almost entirely restricted to Asteraceae. Records on Asteraceae not based on examination of male genitalia are treated in this account as Chromatomyia 'atricornis'.

Chromatomyia horticola is recorded on 160 plant genera in 31 families, of which 55 plant genera in 19 families, but not yet on Trifolium, in Britain. On Trifolium elsewhere.

Chromatomyia horticola (Goureau, 1851) [Diptera: Agromyzidae].

1f > Leaf-miner: An upper surface linear mine with frass in conspicuous greenish strips, largely alternating at each side of the channel. Puparium yellow

Liriomyza congesta puparium
Liriomyza congesta puparium
Image: © Willem Ellis (Bladmineerders van Europa)

Polyphagous. On numerous genera of Fabaceae, including Trifolium, in Britain and elsewhere. Widespread in Britain. Also recorded in the Republic of Ireland and widespread and common throughout most of Europe

Liriomyza congesta (Becker, 1903) [Diptera: Agromyzidae].

1g > Leaf-miner: The mine starts as a long, narrow, winding corridor running towards the midrib, widening to a blotch. Usually upper-surface, but in small leaves also full-depth parts may occur. The blotch has broad lobes; in their ends most frass is accumulated in the form of green patches or clouds. Sometimes several larvae share mine. Pupation usually in the soil, less often in the leaf (and then generally not in the mine itself but in a small separated mine, that may even be made in the petiole) (Bladmineerders van Europa).

Scaptomyza graminum on
Mine of Scaptomyza graminum on Cerastium glomeratum
Image: © Jean-Yves Baugnée (Bladmineerders van Europa)

On ? Amaranthus, Cerastium, Lychnis, Myosoton, Nasturtium, Silene, Stellaria, Atriplex, ? Anthyllis, ? Lupinus, ? Medicago, ? Montia and ? Antirrhinum, but not yet on Trifolium, in Britain.

On Amaranthus, Lepidium, Moricandia, ? Rorippa, Agrostemma, Arenaria, Cerastium, Corrigiola, Cucubalus, Dianthus, Gypsophila, Lychnis, Moehringia, Myosoton, Polycarpon, Saponaria, Silene, Spergularia, Stellaria, Vaccaria, Viscaria, Atriplex, Beta, Chenopodium, Obione, Salicornia, Spinacia, Anthyllis, Lupinus, Medicago, Allium, Montia, Portulaca and Antirrhinum elsewhere. Widespread in Britain and continental Europe.

Scaptomyza graminum (Fallén, 1823) [Diptera: Drosophilidae].

1h > Leaf-miner: Corridor-blotch mine, normally dorsal; usually whitish; in small leaves it lies characteristically in the centre of the leaf often touching the petiole; in larger leaves it lies to one side of the mid-rib. Frass deposited in green clumps near the leaf margin. Pupation usually external, sometimes in a separate pupation mine.

Oviposition whitin the leaf, at the lower surface. The first part of the mine is a long, sometimes very long, corridor, that mostly will be overrun by the later developments. Generally this corridor is directed, frequently guided by a thick vein, to the midrib. The next section of the mine is large, irregular blotch overlying the basal section of the midrib. Locally large chunks of midrib tissue are consumed. From this central blotch excursions are made into the leaf blade: generally upper-surface, less often lower-surface and locally full-depth. In plants with narrow leaves, like Diplotaxis, the mine may occupy the entire width of the leaf. Often several larvae together in a mine. Frass blackish green, powdery, in clouds, sometimes along the sides of the corridors, later more in the periphery of the mine and in the end of extensions of the blotch, sometimes seemingly absent. (Often the frass can only be seen after the mine has been opened). Pupation generally in the ground, rarely within he leaf, in a short mine without frass. Hendel (1928a) described the biology, larva and puparium (Bladmineerders van Europa).

An initial narrow gallery then leads to a blotch on the midrib of the leaf (British leafminers).

Watch a video of a scaptomyzid fly larva on Arabidopsis on YouTube by mash92587.

Polyphagous. On numerous genera of Brassicaceae, Asteraceae, Papaveraceae, Resedaceae, Tropaeolaceae and Violaceae, including Alliaria, Barbarea, Brassica, Cheiranthus, Cochlearia, Coincyia, Conringia, Diplotaxis, ? Eruca, Erysimum, ? Hesperis. Lepidium, Matthiola, Raphanus, ? Rorippa and Sinapis, but not yet on Trifolium, in Britain. On additional genera of these families and Fabaceae elsewhere. Widespread, from Caithness in the north to Cornwall in the south of Britain. Also recorded in the Republic of Ireland, Europe, the East Palaearctic, Near East and Neartic Region.

Scaptomyza flava (Fallén, 1823) [Diptera: Drosophilidae].

1i > Leaf-miner: A short, irregular, linear upper surface mine on any part of the leaf. Also recorded from young pods (Bland, 1997a).

Long corridor mine. As a rule the first part of the mine is lower-surface, the later part upper-surface. Often the loops are so dense that a secondary blotch is the result. Because upper- and lower-surface corridor segments often cross, the mine obtains a strange array of transparant patches. There is no association with the midrib. Frass in strings and thread fragments. Pupation outside the mine; exit slit in upper epidermis (Bladmineerders van Europa).

Mine not associated with the veins or midrib of the leaf (It is this character which enables distinction from another Agromyzid pest species - Liriomyza huidobriensis). The larvae may leave one leaf (if not large enough) and enter another leaf, via the petiole). It exits the leaf to pupate through a semi-circular slit in the upper surface of the leaf (British leafminers).

Polyphagous. On 119 plant genera in 31 plant families of which only 4 plant genera in 2 plant families, but not yet on Trifolium, in Britain. On Alisma elsewhere. Local, probably introduced to Britain. Widespread in continental Europe particularly in Botanical Gardens and glasshouses. Also recorded in Egypt.

Liriomyza bryoniae (Kaltenbach, 1858) [Diptera: Agromyzidae].



Key for the identification of the known mines of British
non-Diptera recorded on Trifolium


Note: The larvae of mining Coleoptera, Hymenoptera and Lepidoptera may live in a corridor mine, a corridor-blotch mine, a blotch mine, a case, a rolled or folded leaf, a tentiform mine or sandwiched between two more or less circular leaf sections in later instars. Larva may pupate in a silk cocoon. The larva may have six legs (although they may be reduced or absent), a head capsule and chewing mouthparts with opposable mandibles (see video of a gracillarid larva feeding). Larvae of Hymenoptera and Lepidoptera usually also have abdominal legs (see examples). Frass, if present, never in two rows. Unless feeding externally from within a case the larva usually vacates the mine by chewing an exit hole. Pupa with visible head appendages, wings and legs which lie in sheaths (see examples).


1a > Leaf-miner and leaf-spinner: The larvae feed between spun leaves and often mine them. The mine is illustrated in British leafminers.

On Genista, but not yet on Trifolium, in Britain. On Genista, Medicago and Trifoloium elsewhere. West and East Sussex and I. of Wight (British leafminers).

Syncopacma vinella (Bankes, 1898) [Lepidoptera: Gelechiidae].

1b > Leaf-miner: Small full depth blotch; older larvae free among spun leaves (Robbins, 1991a).

On Lathyrus, Vicia and Trifolium in Britain and on Lathyrus, Melilotus and Trifolium elsewhere. Widespread in Britain. Also recorded in the Republic of Ireland. Widespread in continental Europe.

Ancylis badiana (Denis & Schiffermmüller, 1775) [Lepidoptera: Tortricidae].

1c > Leaf-miner: The first generation initially forms an unmistakable leaf-mine on Anthyllis vulneraria, but the second generation feeds on the flowers. Feeding signs on other plants vary in appearance. Larvae can move between sewn leaves, and more than one larva may be found together (UKMoths). Larvae in a small full depth blotch, often with extensions. Frass concentrated in one corner of the mine. The mining activities may cause the leaf to roll inwards. Older larvae live free among spun leaves, but still they may make then full depth mines by feeding on the leaf tissue from a small opening (Bladmineerders van Europa).
Aproaerema anthyllidella larva,  dorsal
Aproaerema anthyllidella larva, dorsal
Image: © Steve Wullaert (Bladmineerders van Europa)

On Anthyllis, Medicago, Onobrychis, Ononis and Trifolium in Britain and Anthyllis, Chamaecytisus, Coronilla, Cysisus, Dorycnium, Galega, Glycine, Hymenocarpus, Lathyrus, Lotus, Medicago, Melilotus, Onobrychis, Ononis, Ornithopus, Oxytropis, Phaseolus, Psoralea, Trifolium, Trigonella and Vicia elsewhere. Britain including the Channel Is. and Northern Ireland. Also recorded in the Republic of Ireland. Widespread in continental Europe.

Aproaerema anthyllidella (Hübner, 1813) [Lepidoptera: Gelechiidae].

1d > Leaf-miner: In the first instar the larva mines the leaves, forming short, irregular, blotch-like mines, but in later instars it lives externally, feeding in spun leaves and often twisting those of tender shoots. Larval head light-brown or yellowish brown, edged with black postero-laterally, ocellar area blackish; prothoracic plate black edged with whitish anteriorly; abdomen dull dark green; pinacula distinct, black, sometimes brownish but with black bases to setae; anal plate large, black (Bradley et al., 1973). Small, full depth mine without a definite shape; little frass. Some silk is deposited in the mine. The larva soon leaves the mine and continues feeding among spun leaves (Bladmineerders van Europa).

Polyphagous. On numerous genera and species of several plant families, but not yet on Trifolium, in Britain. On numerous genera and species of several plant families, including Trifolium, elsewhere. Widespread in Britain and continental Europe. Also recorded from the Channel Is.

Cnephasia incertana (Treitschke, 1835) [Lepidoptera: Tortricidae].

1e > Leaf-miner: The mine begins as a tiny, lower-surface epidermal corridor. Only after the first moult the larva starts feeding on the leaf parenchyma. The first result is a corridor overlying the midrib. From here branches enter the leaf disk; gradually they widen and merge, laeving in the end almost the entire leaf mined out. Almost all frass is ejected. The larva can leave its mine and make a new one elsewhere. Pupation witin the mine (Bladmineerders van Europa).

On Ononis and Trifolium in Britain and elsewhere. Britain including East Kent and North Hants. Widespread in Continental Europe.

Parectopa ononidis (Zeller, 1839) [Lepidoptera: Gracillariidae].

1f > Leaf-miner: Lower surface tentiform mine that occupies only part of a leaflet. In full grown leaves the mine is strongly inflated and is largely hidden by the leaf. Unlike other species the entire leaflet is not mined out (Bladmineerders van Europa).On Ononis and Trifolium and Lathyrus, Medicago, Ononis, Trifolium and Vicia elsewhere. North Ebudes. Also recorded in the Republic of Ireland. Widespread in continental Europe.

Phyllonorycter insignitella (Zeller, 1846) [Lepidoptera: Incurvariidae].

1g > Leaf-miner: The mine is underside, occupying the whole leaflet, which turns down at edges (British leafminers). Lower surface tentiform mine that occupies an entire leaflet; lower epidermis strongly folded. Fully developed mines are strongly inflated and the leaflet is so completely folded over the mine that the latter becomes practically invisible. In this stage the larva has consumed also all tissue in the roof of the mine, making the mine very conspicuous (Bladmineerders van Europa).

On Lathyrus, Medicago, Trifolium and Vicia in Britain and Lathyrus, Lotus, Medicago, Trifolium and Vicia elsewhere. England, Ireland and continental Europe.

Phyllonorycter nigrescentella (Logan, 1851) [Lepidoptera: Gracillariidae].



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