Dichotomous table for gallers on Populus

by Hans Roskam

1a On inflorescences or fruits => 76

1b On vegetative plant parts => 2

2a Gall development restricted to particular organs or their parts => 4

2b More or less witches’ broom-like malformation of complete shoot systems => 3

3a Malformation of all terminal shoots. Usually several galled shoots shortened, somewhat thickened, ± pubescent; apical shoots sometimes slightly elongated. Leaves smaller, margin curled, thickened, yellowish or reddish. Stipules often leafy and ± coalesced with the associated leaf. P. tremula, ? alba: Aceria dispar

3b Expanded erect witches’ broom on side branches; on P. alba, nigra often emerging from the axils of twigs that are still herbaceous: Inducer unknown

4a On leaves, shoot tips or buds => 20

4b On shoot axial parts, sometimes encroaching into the buds, or on roots => 5

5a On young twigs that are one to several years old => 13

5b On older twigs, branches, stems and roots => 6

6a On shoot parts distant from the ground => 7

6b More or less tuber-shaped proliferations, initially soft, soon woody and browned on root collars or on basal stem parts. “Root cancer”. Populus spp.: Agrobacterium tumefaciens

6c Nodule-shaped swellings on young roots of P. alba, nigra: Meloidogyne sp

7a Closed galls inhabited by insect larvae; or malformations induced by mistletoes => 9

7b Conspicuous tuberous proliferations or ± rimmed open cancers; caused by bacteria or fungi => 8

8a Galls laterally protruding from the younger stems and branches, irregular tuberous, soon with cracked surface. “Tubercles”. Populus spp.: cf. Bacillus populi

8b Younger twigs, also older branches and stems with cancer-like wounds, which are surrounded by rim-like ± irregular proliferations of the bark. Populus spp.

a Wounds usually with slime secretions. “Bacterium cancer”: Xanthomonas populi

b Wounds without slimy excretions. During later stages, an open woody area is surrounded by sometimes several ± concentric and fissured rims. “Nectria cancer”: Neonectria ditissima

= From similar cancers have been isolated Botryodiplodia penzigii, which species is likewise able to induce cancers.

= On the other hand, Dothichiza populea, a bark smut, does not cause gall-like cancers

9a Galls only a few cm long => 10

9b Older branches, also stems with expanded spindle-shaped to tuberous swellings from which develop: Viscum album

10a Swellings on ± thumb size thickened parts of branches and twigs. Pith containing larvae with distinct head capsule => 12

10b Similarly situated galls caused by larvae without conspicuous head capsule, living in bark or sapwood => 11

11a Spindle-shaped to oblong swellings several cm long which usually do not envelop the stem; bark initially glabrous, heavily perforated after emergence of the gall midges. Several to many slender larvae, with a sternal spatula, lacking conspicuous mouth parts; in inner bark and outer wood. P. alba, tremula: Rabdophaga giraudiana

11b Swelling due to proliferation of bark and sapwood. Bark of the galls glabrous; with single exit hole later on. Each gall containing in a depression of the sapwood a compact, rotund, greenish-white maggot, provided with vertical, hooked mandibles. Galls one-sided, up to about 1 cm long, ± bean-shaped. P. alba, nigra, incl. var. italica, tremula: Hexomyza schineri

12a Locally raised bumps, usually swelling on all sides. Caterpillar biennial, white-yellow with black-brown head capsule, in pith. Populus spp.: Paranthrene tabaniformis

12b Compact swelling, usually on all sides, up to 25 mm long. Larvae yellowish, in pith. Populus spp.: Saperda populnea

= From GB has also been recorded Saperda carcharias causing swelling and deformation of the stem in older trees of P. tremula

= The caterpillar of Cydia corollana may also induce similar galls

13a Galls contain animals => 14

13b Bark of young twigs with irregular, rimmed depressions, which contain the flat froth-covered nymph, covered by a pear-shaped scale up to 2.5 mm long. P. tremula, nigra etc.: Chionaspis salicis

= The polyphagous “Oyster shell scale” Diaspidiotus ostreaeformis (living under a rotund, ± dark grey scale, exceptionally causes similar but much less conspicuous malformations on P. alba, nigra, tremula

= Also the “Poplar armoured scale”, Diaspidiotus gigas occasionally causes similar damage to woody twigs of poplar and aspen

14a Oblong or pouch-shaped galls => 15

14b Bark of young shoots with a double row of egg capsules (procecidia: oviposition scars, not true galls): Nematus miliaris

15a Galls elongated; ± spindle-shaped and predominantly on all sides. Larvae with distinct head capsule => 18

15b Galls rotund to pouch-shaped, one-sided => 16

16a Galls caused by aphids => 17

16b Swelling on the petiole of the leaf, rotund, with short conical tip, which opens at maturity; occasionally with several, coalescing to varied extents and causing bending of the leaf blade. Each chamber containing a red-yellow larva. P. tremula, rarer canescens, alba: Contarinia petioli

17a Gall at the base of present-year shoots, up to 20 mm long, oblong pouch-like, laterally somewhat compressed, initially green, later on ± lignified. Opening at the gradually tapering tip, bent downwards halfway or laterally. P. nigra, as well as var. italica. Ornamental poplars have also been recorded as primary hosts: Pemphigus borealis

17b Galls similar, usually slightly larger, always more strongly bent. Exit hole almost reaching the place of attachment. P. nigra and var. italica, robusta: Pemphigus immunis

18a Galls caused by sawflies; gall usually not completely enveloping the twig => 19

18b Gall shape different, slender to bulging spindle-shaped; usually enveloping the twig. In the pith is a several cm long cavity, which opens by a circular hole into a projecting cigar-like, frass-covered, silken tube. Containing a brownish caterpillar with dark- to black-brown head and neck shield. Populus spp,: Gypsonoma aceriana

18c Similar galls. P. nigra, x canadensis: Gypsonoma dealbana

19a Swellings slightly prominent. The pith containing a single larva. P. tremula: Inducer unknown

19b Pronounced, short oval, blister-like swellings; solitary or several coalescing into tubercular bulges. Larval chamber oblong, in pith. P. nigra, tremula: Inducer unknown

19c Less pronounced malformations caused by egg batches: Stictocephala bisonia

20a On leaf blades or petioles => 28

20b On shoots or buds => 21

21a On shoots => 25

21b On buds => 22

22a Pouch-shaped galls, ± curved, initially green, later on lignified and browned, which open at their apex. Caused by aphids. Sometimes with several together.

22b Galls caused by other inducers => 23

23a Galls caused by gall midges or mites => 24

23b All parts of the opening bud severely stunted, disfigured, up to about 3 cm long. Stem parts sometimes slightly swollen and densely covered on the underside with orange-yellow uredinia, like the leaf rudiments. P. alba, tremula: Melampsora populnea

24a Buds weakly disfigured; more compact, not opening. Containing a single red larva. P. alba: Dasineura populnea

24b Buds are changed into a large mass which is similar to ‘bedeguar’ on rose; inside a chamber containing yellow-white midge larvae. P. tremula: Macrolabis bedeguariformis

24c The dormant buds of lignified shoots, especially on coppice close to ground, or of young, and more rarely also the ± higher situated buds on older stem parts, grow up to about 20 (35) mm long, initially succulent, cauliflower-like accumulations, ± finely partitioned, yellowish or often reddened and sometimes pubescent proliferations. Aceria populi

25a Tuft-like accumulation of several disfigured leaves on the markedly stunted shoot tips; caused by aphids => 26

25b Looser accumulations of curled and curved terminal leaves; larvae on underside. P. alba, canescens: Sthenarus rotermundi

26a Up to fist-size tufts of paler, broadly-bulging swollen shoots often with thickened stalk; on P. alba and forms => 27

26b On P. tremula, x canescens. Petiole bent backwards; leaf blades deflected, ± overlapping: Pachypappa tremulae

26c Large pale green, yellowish to slightly reddish blister-like galls, open to the underside, on leaves of P. tremula: Pachypappa populi

27a Leaf blades ± bladder-like swollen and often bleached: Pachypappa vesicalis

27b Malformations similar to those caused by the previous aphid: Pachypappa warshavensis

28a On leaf blades => 41

28b On petioles => 29

29a Swelling on the basal part of the petiole as well as on the leaf pad, or laterally compressed galls immediately below the leaf blade base, up to about 8 mm long, slender. In the latter case the larvae produce short, spot-like mines with frass arranged in two rows in the immediately adjacent leaf blade => 36

29b Malformation of undefined condition or many small egg capsules next to each other on the side of the petiole => 30

30a Bag- to pouch-like or oval to almost globular, ± smooth-walled galls => 33

30b Gall wall twisted screw-like or swellings arranged like string of pearls on the sides of the petiole => 31

31a Petiole broadened; the bands in loose coils tightly coalesced into a wide spindle-shaped gall; sometimes reddened => 32

31b Minute semi-oval swellings on the upper side, soon developing a slit, in tight series arranged next to each other, usually on both sides of the stalk, often over its complete length and remaining recognizable as swellings after the larvae have eclosed. “Procecidia”: oviposition scars, not true galls. Especially on P. tacamahacca, tremula, also on P. alba, canadensis, candicans, nigra etc.: Cladius grandis

31c Similar swellings: Pristiphora compressicornis

31d Swollen egg capsules, usually in a low number, containing several eggs in spring on petioles as well as on young shoots of poplars: Rhytidodus decimusquartus

32a Gall is green, reddish or yellowish, smooth, formed by thickening, flattening and spiral twisting of petiole with the number of twists not exceeding 5 (usually 3–4), 10‒25 x 7‒10 mm. P. berolinensis, nigra and var. italica, rarer on ornamental forms, hybrids: Pemphigus spyrothecae

32b Galls smooth, shiny, green mottled with red, caused by swelling. Flattening and spiral twisting of the leaf petiole, similar to those of P. spyrothecae but usually thinner and with more and smaller twists (more than 5), about 30 mm long. P. nigra and more often on var. italica: Pemphigus protospirae

33a Galls less than 1.5 (2.0) cm long, wall ± glabrous => 34

33b Galls more than 3 cm long, sometimes at the base of the present year shoot up to hen egg size, provided with many, irregular, ± tubular proliferations, especially towards the top. P. nigra, suaveolens: Pemphigus vesicarius

34a Galls longer than broad, ± pouch- or pear-shaped; induced by aphids => 35

34b Almost globular, up to 5 (8) mm across, sometimes slightly pubescent and reddened, one-chambered gall, which is occasionally narrowed at both ends and laterally with a conical appendage. At maturity with round opening. Sometimes with several ± largely coalesced. Each chamber containing an orange-coloured larva. P. alba, canescens, tremula: Contarinia petioli

35a Galls ± oblong, pouch-shaped, especially apically increasingly narrowing, not or slightly curved; on upper or lower part of the petiole; up to 15 mm long, reddish and lignified. Exit hole on top, surrounded by a somewhat thickened rim. P. berolinensis, canadensis, deltoides, nigra (especially var. italica), robusta, simonii, tacamahacca, etc.: Pemphigus bursarius

35b Globular galls at the base of a green shoot, green, red around the exit opening. The gall is up to 2.5 cm large, and invariably solitary. P. nigra incl. var. italica: Pemphigus trehernei

= Closely related aphids are Pemphigus borealis and Pemphigus immunis

36a Galls on the upper part of the petiole; from 8 onwards => 37

36b Basal part of petiole and bud pad swollen, exit hole later on the base of the leaf pad. P. tremula: Cause unknown – ? gall midge

37a In autumn the mature larvae in the laterally compressed gall make a short, compact, mine on both sides tunneling into the leaf blade base. Each mine containing a single larva. Infected leaf blade segments remain :green islands” of chlorophyll in the otherwise yellowing leaf => 38

37b The older caterpillar encroaches by scraping from the usually cylindrical gall into the base of the leaf blade between two veins on the underside. Feeding sites net-like; on P. alba usually ± covered by the remains of the felt-like pubescence. No preservation of chlorophyll in the infected leaf: Gypsonoma oppressana

38a On P. alba and tremula. Nepticulid larvae living initially in slightly disfigured petioles; transfer to leaf mining when almost mature => 39

38b On P. canadensis, nigra and var. italica: Ectoedemia hannoverella

39a On P. alba, canadensis => 40

39b On P. tremula: Ectoedemia argyropeza

40a The larva constructs its later mine in the axil between two leaf veins. Ectoedemia turbidella

40b The mine is located on a vein instead of in the axil between two veins and protrudes laterally into the leaf blade: Ectoedemia klimeschi

41a Leaf blade folded over the midrib on both sides without distinct thickening, or leaf blade with conspicuous folds or rolls of the margin => 66

41b Malformations different => 42

42a Globular to oval smaller to conspicuous pocket-, pouch-, sac-shaped galls, provided with narrow entry, of defined form, and different size => 55

42b Leaves either with small warts, or humped proliferations at the base of the leaf blade; these with erinea, or bulge- to bladder-like swellings of various sizes on sometimes ± nest-like accumulations of leaves => 43

43a Nest-like accumulation of leaves; variously shaped and curled; moderately pubescent flat bulges or wide opened bladders; additionally associated with curving of the leaf blade => 49

43b Warts, grooves, erinea on the normally unfolded leaf blade or proliferations at the base of the leaf blade => 44

44a Whitish, reddish to brownish or creamy white to yellow erinea => 47

44b Grooves, warts or pustules in the free part of the leaf blade or bumpy bulges on the base of the leaf blade => 45

45a Grooves, warts or pustules on the leaf blade => 46

45b Glands of base of the leaf blade transformed into irregular, rotund to long oval proliferations, up to 4 mm long, bumpy, ± reddened. P. tremula: Eriophyes diversipunctatus

46a Small, 1–1.5 mm broad, flat upward protuberances on the usually normally coloured leaf blade. P. nigra and var. italica: Trioza sp.

46b Many ± golden-yellow warts, less than 1 mm across, on the underside of only the basal leaves: Synchytrium aureum

= On higher leaves, occasionally occur inconspicuous small, oval, two-sided, old pustules, the egg batches especially of sawflies. More conspicuous are the “procecidia”, oviposition scars, not true galls, of the sawfly Pristiphora conjugata, which occur isolated, often many, between the teeth on the leaf margin. Mature caterpillars are green with black-brown head capsule; first- and last segments with clearly defined red or yellow colouration. On willows as well as poplars.

47a Felt-like, white, red to brown erinea of many-celled, hair-like protrusions => 48

47b Leaf blade with one, or several protrusions, up to about 5 (10) mm broad, flat bladder-shaped, pale- to yellow-green upwardly, exceptionally downwardly, projected. Arching at ripening of spores, with extended erinea consisting of densely arranged, almost cylindrical, golden-yellow asci: Taphrina populina

48a Erinea whitish, greenish or yellowish, only rarely reddish, black-brown when old; often arched on the upperside (occasionally also on underside), ± discoloured, on the underside about 5–6 mm broad, rotund grooves, on both leaf surfaces; sometimes clustered and additionally disfiguring the leaf blade. Outgrowths multi-cellular, on top ± widened. P. tremula, much rarer on P. alba, canescens, nigra var. italica: Phyllocoptes populi

= And the probable inquilines Aculus reticulatus and A. aegirinus

48b Initially red, brownish felt masses later developing from short-stalked, abundantly tree-like branching, haired tufts, mainly on the underside, but also on the upperside of the leaves. Erinea sometimes ± depressed. P. tremula: Aceria varia

49a Curling, arching or bladder-like swelling of the leaf blade => 50

49b Leaves on young shoots in spring slightly changed, or the leaf blade over its length ± folded upwards and clustered, nest-like, due to severe bending of the hardly swollen petioles. P. tremula, occasionally x canescens: Pachypappa tremulae

49c Similarly, on P. alba, canescens, euphratica: Pachypappa warshavensis

50a Leaf blade with localised curls, or expanded, flat bulge-like, swellings => 54

50b Leaf blade completely, or partially with conspicuous strongly bladder-like arched swellings wide open on the underside. Contain waxy aphids 5–7, often spilling out of gall, which is not closed => 51

51a On P. alba, tremula => 52

51b On P. nigra and var. italica. Conspicuous broad bladder-shaped wide open swellings, on the underside on both sides of the midrib, on the basal leaf blade, apically and marginally decaying: Pachypappa marsupialis

52a On P. tremula => 53

52b On P. alba, x canescens. Nest-like clustered leaves with bladder-like leaf blades on the short shoots of usually tree-like hosts: Pachypappa vesicalis

53a On saplings. Bladder-like swelling and upward arching of the leaf blade, in cross section up to 7 cm long; venation conspicuously protruding on the discoloured gall: Pachypappa populi

53b Leaves of older trees sometimes disfigured into a large pouch-shaped gall, up to 10 cm long, often situated rather high up in old trees and therefore hard to find. The gall is formed from a longitudinally folded leaf which is paler than the normal leaves and becomes much enlarged with a thickened petiole: Gootiella tremulae

53c Conical leaf-galls. P. alba: Gootiella alba

53d Leaf blade folded down over its length to form a cone, discoloured bright red-orange. P tremula: Pachypappella lactea

54a Leaf blade, slightly arched upwards or downwards, depending on the position of the insects. P. nigra and related species, also P. balsamifera: Chaitophorus leucomelas

54b Leaf blade locally strongly curled; often darker green where the aphid feeds. The respective venation variously bent downwards with the adjacent margin less disfigured leaf blades. P. tremula: Philaenus spumarius

55a Globular, rotund, rarely ± bulge-like galls, less than 8 mm long. Caused by gall midges => 58

55b Sac- or pouch-like galls, often more than 1 cm long of ± defined shape but different size; caused by aphids => 56

= The eggs of the Cerura virula are usually laid in pairs on the upper surface of the leaves of willow and poplar and resemble small galls

56a Galls longer than wide => 57

56b Egg-shaped- or irregularly bulging, smooth-walled galls, distinctly narrowed at their base on the upperside of the leaf, predominantly at the base of the leaf base; opening on the upperside. P. nigra and var. italica, trichocarpa: Pemphigus populi

57a Pouch-shaped gall, about 20 mm long and the upper half up to about 10 mm wide, yellowish or usually reddened on, or immediately next to the midrib. Slit-shaped opening on the underside. P. nigra and var. italica, occasionally P. deltoides, tacamahacca: Pemphigus populinigrae

57b Galls and hosts similar to the above. Aphid differs by its migration to the roots of Apiaceae:

a Alternating on Daucus species: Pemphigus phenax

b Alternating on Carum carvi, exceptionally on Aegopodium and Daucus: Pemphigus passeki

c Alternating on Aethusa cynapium: Pemphigus gairi

58a Galls on one side of leaf only, usually distinctly developed on the upper side; on the opposite side not protruding or, with slightly rimmed exit hole => 64

58b Galls distinct on both sides of leaf => 59

59a The gall opens by a slit when mature; a separate inner gall is absent => 62

59b Ripe gall with a round opening; usually with distinct inner gall => 60

60a Galls relatively thick-walled, about 4–5 mm across, protruding on both sides of leaf. Inside is an oval inner gall, with its longitudinal axis along the longitudinal axis of the leaf blade => 61

60b Galls thin-walled, nodular or flat bladder-like, rotund, up to ± 3 mm across, surrounded by a narrow, ± acute wall; often next to a main vein, which is somewhat thickened and bent. Large cavity with an oval inner gall in the centre, orientated perpendicular to the leaf blade. Containing a single sulfur-yellow, later on red larva. Exit hole usually on the upper side. P. tremula: Harmandiola pustulans

61a Galls greenish to reddish; ± hemispherical on the underside. Larva pale yellow to orange-coloured, sometimes migrating outside the inner gall before maturity. P. alba, tremula: Contarinia populi

61b Galls similar, slightly smaller, usually protruding on the upperside, centrally with slight blunt-conical projection; more rarely protruding on the underside. Larva orange. P. alba, x canescens, tremula: Lasioptera populnea

62a Galls thin-walled, usually only 2‒3 (4) mm across, slightly protruding on the underside => 63

62b Galls thick-walled, oblong-rotund; usually up to about 5 mm across, pale green or ± reddened, single-chambered; only a third of its dimension protruding on the upperside; usually situated next to a vein. Exit hole parallel to the vein; on the upperside ± lip-like surrounded by a circular wall. Larva orange-coloured to pale yellowish-brown. P. alba, x canescens, tremula: Harmandiola cavernosa

63a Galls similar, but thin-walled and less protruding on the upper side, about 3–4 mm across. Larvae yellowish-red to brownish. P. alba, tremula: Harmandiola populi

63b Galls almost perfectly globular, only up to 2 mm across, lacking circular wall, P. tremula: Unidentified gall midge

64a Galls distinctly constricted at base => 65

64b Base of galls only slightly narrowed, not constricted, rotund, up to 2.5 (3) mm across, thin-walled, usually dark red coloured, single-chambered. Exit hole on underside. slit-shaped, surrounded by a ridge. Often several per leaf blade. Larvae reddish-yellow. P. alba, x canescens, tremula: Harmandiola globuli

65a Galls about (3) 4–5 (6) mm across; globular, with distinctly narrowed base; thick-walled, often dark red, single-chambered. Exit hole on underside surrounded by a narrow rim. Containing a single pale to dark orange-red larva. P. alba, x canescens, tremula: Harmandiola tremulae

65b Smaller to larger galls on P. tremula, similar to those of both previous reported midges, but predominantly on the leaf underside; circular wall surrounding the exit hole often present, sometimes lacking. Unidentified gall midges

66a Leaf margin rolled over different, often extensive length => 69

66b Leaf blade with locally defined valve-like marginal folds, or halves on the midrib folded downwards => 67

67a Largely discoloured downward folds of the often yellowish or orange-coloured halves of the leaf blade => 68

67b Local, 10–20 mm long, often under 10 mm deep valve-like fold of the leaf margin on the lower leaves of a young shoot caused by the fundatrix of Thecabius affinis

= In similar, up to now not discriminated folds lives also the fundatrix of Thecabius lysimachiae

68a On a wide range of Populus spp.: Thecabius affinis

68b On P. tremula living in similar folds: Gootiella tremulae and/ or Chaitophorus populeti

69a Loose, thick rolls of the leaf margin, in cross section usually not much over 2.5 mm long. Caused by aphids or gall midges => 71

69b Narrow, slender, more compact leaf rolls => 70

70a Leaf margins without abnormal pubescence, rolled upwards.P. tremula: Aceria dispar

70b Leaf blades, especially of suckers, with narrow upward rolls, which show on both leaf sides a dense encroaching pubescence, occasionally also extending onto the petiole. P. tremula: Unidentified ? gall mite

71a Leaf margin rolled upwards => 73

71b Downward roll of leaf margin => 72

72a On leaves of the ± stunted apical shoot of P. tremula, x canescens: Chaitophorus populeti

72b Corresponding malformations on P. alba, caused by a similar looking aphid: Chaitophorus populialbae

73a Extended upward roll; caused by gall midges or aphids => 74

73b Margin rolled upwards; caused by psyllids. P. alba, canadensis, nigra and var. italica, tremula, etc.: Camarotoscena speciosa

= The psyllid Camarotoscena subrubescens, causing similar malformations on P. alba, nigra, has been recorded from warm regions

74a Curled rolls of the leaf margin, often involving both halves of the leaf blade over extended or complete length; however, at least in its lower part not reaching the midrib. Usually on terminal leaves of current year shoots. P. tremula, alba => 75

74b Mostly one-sided leaf roll which usually involves half of the leaf blade. P. nigra: Thecabius lysimachiae

75a Leaf rolls glabrous, glossy and not excessively pubescent; in various instances they are sickle-shaped. Larvae white, jumping. P. tremula: Contarinia tremulae

75b Roll ± distinctly pubescent; predominantly on leaves of suckers. Larvae white, gregarious, non-jumping. P. tremula, rarely P. alba, x canescens: Dasineura populeti

76a Single fruits of the inflorescence greatly enlarged, concave. Wall thickened, ± discoloured yellowish. P. tremula, occasionally also on P. x canescens, tremula subsp. grandidentata, sieboldii, tremuloides: Taphrina johansonii

76b Corresponding galls on P. alba. Asci usually distinctly larger than in the previous fungus. Taphrina rhizophora

= Variously shaped malformations of catkins are usually caused by lepidopteran or beetle larvae, which bore in the rachis. The catkins (preferably the female ones), become disfigured and drop prematurely.

mod 24.xii.2019