Plant Parasites of Europe

leafminers, galls and fungi

gallers on Trifolium

Dichotomous table for gallers on Trifolium

by Hans Roskam

1a On above ground organs => 4

1b On roots => 2

2a Roots with lateral nodules, or swellings situated on all sides in the root body => 3

2b Roots externally hardly changed, temporarily bearing about poppy-seed sized egg capsules (cysts), at first white, soon brown, which drop at maturity. Giant cells develop at the infestation site. Plant atrophied, with “starvation roots”. Trifolium spp.: Heterodera trifolii

3a Roots with nodular or slender spindle-shaped swellings on all sides, up to 6 mm long, bearing several lateral roots. T. alexandrinum, hybridum, incarnatum, pannonicum, pratense, repens, etc.: Meloidogyne hapla

3b Rotund-oval to slender cylindrical or forked nodules, also coralloid branched, up to 5 mm long, laterally inserted on main- or adventitious roots. Trifolium spp.: Rhizobium trifolii

4a On inflorescences, flowers or fruits => 25

4b On vegetative organs => 5

5a Localised malformations on stems, buds, leaves or more expanded malformations on single shoots => 6

5b Complete plant stunted, often excessively leafy. Shoots, also leaf- and inflorescence stalk stunted, usually spongy thickened at base; organs clustered, often distorted. Leaf blades reduced, swollen, sometimes extensively twisted, undulate or brittle. T. arvense, campestre, dubium, hybridum, incarnatum, medium, pratense, repens: Ditylenchus dipsaci

= Witches’ broom-like malformations lacking spongy thickenings on T. repens have been described as virus disease

6a Malformations on stems or leaves, caused by fungi, which develop their distinctive fruiting bodies at the surface of the host organs => 17

6b Galls caused by animals or by fungi, which fruit inside the host tissue => 7

7a Galls on leaf blades or -stalks, sometimes additionally also on stems => 12

7b Pronounced stem galls or malformations on buds => 8

8a Bud galls => 11

8b Stem galls => 9

9a Galls always on higher situated stem parts => 10

9b Stem with spindle-shaped swellings, up to 6 x 2.5 mm, on root collar or on higher situated parts. Containing a single larva. T. arvense, aureum, campestre, dubium, hybridum, pratense, spadiceum: Catapion pubescens

= Catapion curtisii has been recorded from oval swellings (6 x 3 mm) in root collar or root. T. fragiferum, repens

= Conspicuous proliferations on root collar by the polyphagous wood cancer Agrobacterium tumefaciens have also been reported for Trifolium

10a Galls spindle-shaped to ± cylindrical; sometimes developing to twice the stem diameter. T. hybridum, medium, pratense, etc.: Catapion seniculus

10b Stem often with several one-sided, almost hemispherical galls, sometimes clustered or coalescing. Each containing a single larva. T. arvense, pratense: Protapion varipes

11a End- or lateral buds transformed into a usually flattened egg-shaped gall, up to 8 mm long and 5 mm thick, succulent, one-chambered, yellowish-green, sometimes reddish at tip and ± enveloped by the associated enlarged stipules. Containing a rugose yellow larva with distinct brown head capsule. T. alpestre, arvense, aureum, campestre, medium, pratense, striatum, subterraneum, etc.:
Tychius polylineatus

11b Similar galls in lateral buds of T. medium and also T. fragiferum, purpureum, scabrum. Containing a single red midge larva. Dasineura axillaris

12a Single galls about 1 mm across, golden-yellow translucent, sometimes coalescing into crusts or ridges or hyaline to brown, 0.5–3 mm long. Caused by fungus => 16

12b Malformations larger => 13

13a Leaves ± folded and simultaneously variously twisted or curled => 15

13b Leaflets without particular curling, folded upwards over the midrib. Galls especially at midrib; their wall conspicuously or hardly thickened => 14

14a Galls bilge-like swollen; their wall conspicuously ± succulent to cartilaginous thickened, glabrous or slightly rugose, pale-green or reddened. Gall body on many hosts with ± broad, not thickened margin. Larvae at first white, later on orange- to reddish-yellow. Trifolium spp.: Dasineura trifolii

14b Galls restricted to the central part of the leaf blade, always surrounded by a broad margin of not thickened leaf blade tissue. Wall only slightly thickened, sometimes pale-green, also red discoloured, browned if mature. Containing 1–2 (3) pale yellow to pale orange-red larvae. T. pratense: Tricholaba trifolii

15a Leaf blade of leaflet folded together upwards or loosely rolled inwards; not or slightly thickened, twisted and ± undulately curled. Trifolium spp.: Aceria trifolii

= he gall mite Aculops eximius causes rust on mediterranean T. ochroleucon, pratense

15b Malformations of clustered leaves on locally stunted shoots caused by a froth-covered nymph. T. pratense: Philaenus spumarius

15c Leaves stunted; leaf blades of leaflets constricted, upwards ± folded together. T. dubium: Unidentified thrips

16a Galls consist of several cells, hemispherical, greenish-yellow, ± golden-yellow translucent, the depressed nutritive cell containing an overwintering sporangium about 160 (‒180) μm large; usually in large numbers mainly on the leaf blades of basal leaves, on their ± distorted stalks and sometimes on their lower stem parts. T. dubium. pratense, repens: Synchytrium aureum

16b Warts hyaline, 0.5–1 mm across, with sporangia and perennial spores. Galls unopened for a long period; later on rupturing in the middle; usually many on leaves as well as on the additionally disfigured stems, leaf- and inflorescence stalks. T. hybridum, incarnatum, montanum, repens: Physoderma trifolii

16c In similar galls on ± distorted leaves, leaf- and inflorescence stalks. T. hybridum, montanum, repens: Olpidium trifolii

16d Petioles and leaf veins, also inflorescence stalks, with several, usually elongate-oval, 2–3 mm long, soon discoloured black-brown, occasionally coalescing swellings; the bearing organs ± arched, bulging. T. fragiferum: Physoderma vagans

= Enatia on leaf undersides on T. incarnatum and other Trifolium species are caused by the Pisum-Virus I

17a The usually bulging galls bear yellowish aecia or dark coloured sori. Galls caused by rust fungi => 18

17b Leaf blades of developing leaves with inconspicuous weak archings, usually expanded, pale-green, bearing a down of branched conidiophores on leaf undersides. “False mildew”. The fungi which are ± frequent on several clover species are very specialised and may be assigned according to biometrical characters to the following micro-species:

a On T. alpestre: Peronospora trifolii-alpestris. – Minor swellings have sporadically been recorded

b On T. arvense: Peronospora trifoliorum. – Galls not observed

c On T. campestre, dubium, spadiceum: Peronospora trifolii-minoris. – Galls not observed.

d On T. hybridum, strictum: Peronospora trifoliorum. – This fungus exceptionally causes minor bulgings; especially on T. hybridum

e On T. medium, incarnatum: Peronospora trifoliorum. – Gall-like arching of leaf only rarely observed. Fungus especially distributed on the often conspicuously etiolated T. medium

f On T. pratense: Peronospora trifoliorum. – Fungus usually only in small pale-green spots on undersides of leaves that are not disfigured.

g On T. repens: Peronospora trifoliorum. – Occasionally the mycelium causes minor archings

18a Malformations bearing aecia, usually also other spore forms present => 22

18b Malformations bearing uredinia, or telia, no spermogonia or aecia => 19

19a Sori contain uredinia as well as telia => 20

19b Oblong swellings, sometimes associated with conspicuous distortions on underside of leaf veins or on petioles; bearing only telia. Mainly occurring on T. fragiferum, repens; also recorded from T. alpestre, arvense, aureum, dubium, etc.: Uromyces trifolii

19c Similar malformations are sometimes caused on T. repens: Uromyces trifolii-repentis

20a In addition to aecia, fungi also develop on sometimes distinctly different malformations, in some species also facultatively cecidogenic, spore forms on Trifolium species. Parasites not positively distinguished according to the malformations => 22

20b Fungi host alternating; develops only on the veins or stems on Trifolium, sometimes facultatively weakly cecidogenic uredinia and telia => 21

21a Sori usually mainly on leaf underside, scattered over the leaf blade, only causing minor swellings and sometimes distinct archings if developing on the venation. T. arvense, aureum, campestre, dubium, micranthum, striatum and close relatives: Uromyces striatus

21b Similar, minor malformations, facultatively on venation T. campestre, dubium, scabrum: Uromyces jaapianus

22a Fungi; all spore forms develop on Trifolium species. Telia only with warts, solitary or arranged loosely in rows => 24

22b Fungi do not develop uredinia => 23

23a Fungus mainly on T. montanum. Aecia often densely arranged in slightly swollen pads, especially on venation, up to 10 mm long. Also recorded from T. angustifolium: Uromyces minor

23b Fungus living on T. repens. Aecia on leaf veins and -stalks usually on distinct longitudinal swellings and malformations, occurring on leaf blades in small, circularly arranged groups: Uromyces trifolii

= Stems and leaflets bearing aecia, telia and uredinia on T. pratense, medium, incarnatum have been assigned to Uromyces fallens

24a Aecia only in spring, usually rare. Aecia mainly in elongated groups on underside of ± swollen and curved leaf veins, more rarely on bulges on petioles and stems; spermogonia usually on leaf upperside. Cups with whitish lacerate margin. Trifolium spp.: Uromyces trifolii

24b Aecia from spring to late autumn. Spermogonia occurring between aecia, often on same petiole. Cups circularly arranged in small dense groups; oblong on veins, leaf- and inflorescence stalks, often causing yellowish discoloured bulges and distortions. Peridium cup-shaped, with narrow, finely lacerate margin. T. repens, fragiferum, etc.: Uromyces trifolii-repentis

25a Localised malformations caused by fungi, gall midge larvae or snout beetles => 26

25b Extended malformation usually of many inflorescences. Flowers ± twisted; calyx teeth strongly developed; corolla stunted, disfigured, ± greened or also sometimes largely leafy, like the stamens and ovaries. T. arvense, aureum, campestre, dubium, hybridum incl. subsp. elegans, medium, montanum, pratense, repens, spadiceum, striatum: Aceria trifolii

= The flower thrips Frankliniella intonsa has also recorded from Trifolium.

= On several Trifolium species, especially T. repens, more rarely T. hybridum, incarnatum, pratense, occur conspicuously disfigured, greened, leafy inflorescences. These are caused by viruses, transmitted by cicadellids

26a Malformations contain larvae with distinct head capsule => 29

26b Malformations caused by midge larvae or fungi => 27

27a Galls inhabited by midge larvae => 28

27b Flowers unaltered externally. Ovary slightly stunted and swollen, sometimes covered with conidia. T. pratense: Thecaphora deformans

28a Flower buds in capitula where oviposition has been early are severely stunted. Corolla unopened and usually shorter than calyx teeth; like the calyx, distinctly swollen, especially at base. Sex organs atrophied. Inside at first white- to yellowish, at maturity pink-coloured larvae. T. pratense, medium, less frequently on T. hybridum and some other related species: Dasineura leguminicola

= In flowers of T. repens, more rarely T. hybridum, pratense lives the white clover midge Dasineura gentneri. Because this midge deposits eggs in already developed flowers, galls are not induced.

28b Similar malformation. The infected flowers are less swollen. Also these remain unopened, but the corolla surmounts the calyx teeth. Larvae orange- to ochre-yellow, jumping. T. pratense, occasionally also T. medium, hybridum, repens: Tricholaba trifolii

28c Yellow larvae in swollen flower buds. T. medium: Hadrobremia longiventris

29a Often only minor malformations mainly to parts of flowers; only secondarily sometimes also the midrib of the inflorescence => 32

29b Gall formation primarily affects the inflorescence axis => 30

29c Flowers greened, larvae living inside the stalk in a long corridor. T. repens, pratense: Hylastinus obscurus

30a Malformations of T. arvense, hybridum, ochroleucon, pratense, repens => 31

30b Inflorescence stalk terminally swollen to a small, asymmetrical gall. Containing a single larva. T. dubium: Protapion filirostre

31a Axis of inflorescence swollen. Calyx of affected flowers at first turgid. Containing single or several larvae. T. arvense, pratense, repens: Protapion dissimile

31b Similarly living on T. ochroleucum, pratense, more rarely on T. hybridum, repens, etc. are the larvae of Protapion dissimile

31c Infected inflorescences about a half times broader than normal ones; terminally truncated, otherwise looking normal, apart from the discoloured calyx which is often entirely pale-green. Containing 1 (2–3) larvae. T. arvense: Tychius pusillus

32a Inflorescences largely disfigured => 33

32b In often conspicuously damaged capitula, usually only single parts are galled. Gall-like malformations usually involving flowers on which eggs are deposited by snout beetles. Calyx often swollen, belly-like, on one side, the axis of inflorescence usually remains normal. Usually several larvae per inflorescence. Trifolium spp.: Apion div. species:

a Flower galls in disfigured inflorescences. Mainly on T. repens, also on T. aureum, hybridum, medium, pratense: Protapion fulvipes

b Flower malformations on T. repens, also on T. alpestre, medium, ochroleucon, pratense, rubens: Protapion trifolii

c In hardly disfigured flowers of T. repens, etc.: Protapion nigritarse

d In disfigured capitula with densely clustered flowers on T. medium, montanum, pratense might develop: Protapion varipes

e As inducer of bud galls on several Trifolium species has also been recorded: Holotrichapion pisi

= Larvae of the curculionid beetle Hypera nigrirostris may cause galls on clover

33a Young inflorescences, usually developing from axils or several flowers variously transformed into a uniform succulent gall. Infestation of larger, older flower buds results only in strong stunting of corolla and ± distinct bladder-like swelling of calyx. Containing a single yellow larva. Galls variable, depending on condition of host. On T. arvense mainly as bud gall; similarly also on T. subterraneum. Larvae also known from T. alpestre, aureum, campestre, medium, pratense, strictum. Tychius polylineatus

33b Inflorescence compact. The infected flowers soon transformed into a hardening, ± knobby mass. Containing several larvae. T. medium, montanum, pratense: Protapion apricans

Last modified 24.viii.2020