Biosystematics of Insects Living in Female Birch Catkins. V. Chalcidoid Ectoparasitoids of the Genera Torymus Dalman, Aprostocet

Tijdschrift voor Entomologie 156 (2013) 21–34 brill.com/tve

Biosystematics of insects living in female birch catkins. V. Chalcidoid ectoparasitoids of the genera Tor ymus Dalman, Aprostocetus Westwood, Psilonotus Walker and Eupelmus Dalman (Hymenoptera, Chalcidoidea) J.C. Roskam

Fully grown larvae have been described of chalcidoids belonging to four genera, viz., Tor ymus Dalman (Torymidae), Aprostocetus Westwood (Eulophidae), Psilonotus Walker (Pteromalidae) and Eupelmus Dalman (Eupelmidae), all parasitoids of gall midges of the genus Semudobia Kieffer (Diptera: Cecidomyiidae), associated with fruit catkins of birch, Betula. Identiﬁcation keys are provided for mature larvae as well as adults. Phenology and host-parasitoid associations have been analysed from samples collected in The Netherlands at about sea level and from western Germany at an altitude of 760 m. Finally, possible patterns of co-speciation have been discussed for gall midge hosts and parasitoids. J.C. Roskam, Department of Evolutionary Biology, Institute of Biology, University of Leiden, Sylvius Laboratory, Sylviusweg 72, 2333 BE Leiden, The Netherlands. [email protected]

Introduction from gall inducers, some inquiline, saprophagous Insects living in female birch catkins are all cen- and predaceous gall midges are frequently found in tred upon galls in fruit gall caused by representa- female birch catkins (Roskam 1979; part II). Part tives of the gall midge genus Semudobia Kieffer, 1913 IV (Roskam 1986) was devoted to the egg-larval (Diptera: Cecidomyiidae). This genus consists of ﬁve platygastrid endoparasitoids. The question why three species, viz., the fruit gall inducing Palaearctic S. be- closely related gall midges can co-occur in the same tulae (Winnertz, 1853), together with its Nearctic niche can be made understandable from a historical- geographic vicariants S. brevipalpis Roskam, 1977 ecological perspective. Inquiline gall midges and and S. steenisii Roskam, 1977; S. tarda Roskam, platygastrid parasitoids make clear how specialised 1977 is exclusively Palaearctic and also induces fruit representatives of these guilds may track their hosts. galls; it has no Nearctic vicariants. Finally the cir- Apart from some incidental chalcidoid para- cumboreal midge S. skuhravae Roskam, 1977 in- sitoids, Semudobia gall midges are the target for at duces galls in the bracts (fruit scales) of the catkins least eight regular chalcidoid ectoparasitoid species (Roskam 1977, part I of the series on the entomo- belonging to three genera in three different fam- fauna of female birch catkins). ilies. Two torymid parasitoids, now placed in the Related publications on this entomofauna dealt large genus Tor ymus (with 191 described Palaearc- with host preferences of the gall inducing midges tic species), viz., T. fuscicornis (Walker, 1833) and (Roskam & van Uffelen 1981; part III). Apart T. nitidulus (Walker, 1833), were earlier assigned to

Tijdschrift voor Entomologie 156: 21–34, Tables 1–5. Figs 1–22. [ISSN 0040-7496]. brill.com/tve © Nederlandse Entomologische Vereniging. Published by Koninklijke Brill NV, Leiden. Published 15 July 2013. DOI 10.1163/22119434-00002020

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Lioterphus Thomson, 1876 – L. fuscicornis and L. tor at a temperature of 4°C, allowing the insects to pallidicornis Boheman, 1834, respectively – a genus pass diapause. Then they were kept at room temper- with only two species exclusively attacking Semu- ature, except the samples used for the determination dobia gall midges. The pteromalid genus Psilono- of phenology. The latter were kept outdoors in Lei- tus contains three species in the Palaearctic, viz., P. den, The Netherlands, with a temperature/humidity adamas Walker, 1834, P.achaeus Walker, 1848 and P. regime similar to that of the locality where they were hortensia Walker, 1846, all species being specialised taken. on Semudobia. Finally, three eulophid parasitoids be- Despite the high numbers of galls, the numbers longing to the large genus Aprostocetus (with 258 of emerged parasitoids were relatively low; therefore Palaearctic species), viz., A. clavicornis (Zetterstedt, also data were used from a rearing experiment during 1838), A. pallipes (Dalman, 1820) and A. constrictus December 1971. In those days, S. tarda,aswellasS. Graham, 1987, are exclusively known as Palaearctic skuhravae, were still undescribed, but it was already parasitoids of Semudobia. apparent that galls in bracts and in fruits were caused Hodges (1969) was first in analyzing the food web by different Semudobia midges. For this experiment in female birch catkin galls and treating the life- bract and fruit galls of 100 fruit catkins, all from history of the parasitoids. Because the present differ- western Netherlands localities, were reared separately entiation into several species of the gall inducing host at room temperature. Semudobia was not known in those days, she was un- Foranalysisoflarvalcharactersthelarvaewere able to determine the precise food web associations macerated in warm lactic acid (80%, 80°C), body between gall midge hosts and parasitoids. Because of content was removed and skins were mounted in (1) the present knowledge of gall inducing midges in- polyvinyl-lactophenol on microscopic slides. Mea- habiting female birch catkins, (2) the occurrence of surements of larvae were taken from material on mi- so many parasitoids in female birch catkins, (3) the croscopic slides using an ocular measuring reticule. conclusions of highly specialised associations in the Phase-contrast microscopy was used to study low earlier studies on inquiline gall midges and platy- contrast structures like larval sensilla. Descriptions gastrids in female birch catkins, and, last but not least and keys for galls, adult parasitoids and their fully (4) the many examples of other highly specialised as- grown larvae are given below. Results of rearings and sociations given in, e.g., Redfern (2011), it became dissections are presented in the sections on morphol- intriguing to further explore host-parasitoid associ- ogy and host-parasitoid associations. ations in such a small arena represented by a birch The number of specimens examined in the de- catkin: can we explain the occurrence of so many par- scriptions are given in Tables 1–3. The terminology asitoid species exclusively specialised on birch female follows Roskam (1982); for the description of platy- catkins as a consequence of differentiation of niches gastrid larvae see Roskam (1986). presented by host gall midges, c.q. of host speciation? Identification keys Materials and methods Key to galls If gall inducing midge characteristics are the primary 1. Malformation of fruit, ovary swollen and cue in explaining the occurrence of the parasitoids, contentaborted...... 2 galls caused by Semudobia betulae, S. tarda and S. – Gall restricted to the slightly thickened base skuhravae have to be sorted in order to discriminate of the fruit scales, which are firmly con- the substrates of the parasitoids involved. The galls nected with the spindle of the catkin . . . . . caused by the different Semudobia species are mor- ...... Semudobia skuhravae Roskam phologically distinct (Roskam 1977). 2. Fruit more or less egg-shaped, swollen, dull, Nine samples were collected in the central part of more or less pubescent; wings distinctly The Netherlands, N 52.13 E 5.32, alt. 10 m, De- smaller than those of healthy fruits, but usu- cember 2011; and 12 samples in Germany, Winter- ally distinctly developed; exit hole distinct, berg, Hoch Sauerland Kreis (HSK), N 51.11 E 8.31, still closed by a membrane or window . . . . alt. 760 m, January 2012. All samples, each contain- ...... Semudobia betulae (Winnertz) ing ten birch fruit catkins, of Dutch and of Ger- – Fruit globularly swollen, glossy, glabrous; man origin were from Betula pubescens in moderately wings often almost completely reduced; exit dry habitat, the Dutch and German localities mainly hole present but visible as an indistinctly differing in altitude. The catkins were dissected and translucent ‘weak spot’ on gall surface . . . . galls were sorted for the three gall makers according ...... Semudobia tarda Roskam to characters in the identification key to galls. Galls Galls may be strongly flattened due to feeding activ- were first stored for about one month in a refrigera- ities of inquiline gall midges Dasineura interbracta,

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Roskam, 1979 and D. fastidioda Roskam, 1979, – Lateral aspect of thorax in both sexes rather which larvae may be present on the outside of the slender and triangular, anterior part of gall. Moreover, larvae of the phytosaprophagous gall pronotum ± gradually declining towards midge Clinodiplosis cilicrus (Kieffer, 1889) and of head...... A. clavicornis (Zetterstedt) the predaceous gall midge Lestodiplosis vorax (Rüb- (Graham 1987: 257) saamen, 1892) may often live on the fruit scales 6. Mesopleuron in female always impressed; (Roskam 1979). mesoscutum with parapsidal grooves complete or merely anteriorly indicated, immo- Key to adults, reared material bileagainstscutellum...... 7 1. Insect wasp-like, two pairs of wings, anten- – Mesopleuron in females convex, not im- nae elbowed and abdomen constricted dif- pressed; scuto-scutellar suture in female ferentiating a propodeum and gaster ...... 2 straight, allowing movement of dorsal scle- – Insect midge-like, only one pair of wings, rites; antenna with only one ring segment antennae straight and abdomen not con- and seven funicular segments; male with stricted but conspicuously red-orange parapsidal grooves deep and pleuron shal- coloured . . . . . Gall midge host Semudobia lowlyimpressed...... For morpholo- . . . . Eupelmidae, Eupelmus urozonus Dalman gical and biological details see Roskam (1977). 7. Hind coxa usually at least three times 2. Parasitoid wasp minute, less than 2 mm larger than front coxa; pronotum large long, glossy black; wing venation absent or and rounded; parapsidal grooves complete; with medial vein (but no marginal vein) . . gaster ovate and ovipositor prominent, long ...... Platygastridendoparasitoid ...... Torymidae,Tor ymus –8 Sclerotised wing – Hind coxa only little larger than front coxa; venation is absent from Platygaster; basal, pronotum small, rounded or carinate; gaster medial; and subcostal veins are distinct elongate and either ovoid or laterally com- in Metaclisis phragmitis Debauche, 1947. pressed;ovipositorlargelyhidden...... The latter species is occasionally present ...... Pteromalidae,Psilonotus –9 in birch catkin galls but was not encoun- 8. Head, thorax and gaster bright green metal- tered during this study. For morpholo- lic; legs excepting coxae, fifth tarsal seg- gical and biological details see Roskam (1986). ments and hind femora pale yellow. An- – Parasitoid wasp larger, longer than 2 mm; tennae in female with frontal part of scape wing venation reduced, but always with bright yellow; antennae in male completely distinctmarginalvein...... 3 bright yellow ...... T. nitidulus (Walker) 3. Parasitoid glossy, bright green metallic; (Walker 1833: 138 [Callimome]; tarsi five-segmented, antennae at least 11- Grissell 1976: 58) segmented...... 6 – Head, thorax and gaster bluish-green metal- – Parasitoid black but with slight blue metallic; legs excepting coxae, fifth tarsal seg- lic shine and some yellow marks on head ments and all femora fuscous yellow. An- and thorax; tarsi four-segmented, antennae tennae in female metallic brown; antennae each with at most nine distinct segments, in male completely brown, sometimes with postmarginal vein reduced. Eulophidae . . . very narrow frontal lighter stripe on scape ...... Aprostocetus –4 ...... T. fuscicornis (Walker) 4. Gaster in females oblong, at least three (Walker 1833: 138 [Callimome]) times as long as wide; antennae in males 9. Both sexes: antennae inserted below level of without conspicuous long, sturdy bristles . . . . 5 ventral edge of eyes; pronotum either car- – Gaster in females ovoid, about 1.5 times as inate or rounded; scutellum distinctly flat- long as wide; antennae in male with con- tened. Gaster in females oblong, distinctly spicuous long, sturdy bristles. . .A. pallipes compressedbilaterally...... 10 (Dalman) – Antennae in both sexes inserted above (Graham 1987: 332) level of ventral edge of eyes; pronotum al- 5. Lateral aspect of thorax in both sexes rather ways carinate; scutellum moderately con- globular, anterior part of pronotum steeply vex, slightly longer than broad. Gaster in fe- decliningtowardshead...... males ovoid, not compressed bilaterally ...... A. constrictus Graham ...... P. h o r t e n s i a Walker (Graham 1987: 304) (Graham 1969: 628)

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10. Antennae with combined length of pedi- – Median conical elevation on head absent; cellus and flagellum slightly longer than clypeus conspicuous and comb-like due to breadth of head with all funicle segments arowofteeth(Fig.18)...... subquadrate; scutellum weakly convex, as Eupelmidae, Eupelmus urozonus Dalman broad as long. Pronotum short, carinate, Occasional polyphagous ectoparasitoid, steeply declining towards head. Propodeum during this study only once collected as larva. ratherdull,plicaecomplete...... 4. Nose accompanied by a lateral pair of con- ...... P. a c h a e u s Walker spicuously sclerotic plates each with three (Graham 1969: 627) blunt-conical elevations (Fig. 6)...... – Antenna with combined length of pedicel- ...... T. fuscicornis (Walker) lus and flagellum shorter than breadth of – Pair lateral plates weakly sclerotised and head; distal segments of funicle strongly usuallyindistinct...... T. nitidulus (Walker) transverse. Pronotum longer, dorso-ven- 5. Antennae protruding, situated on blunt trally flattened, the collar longer medially, bell-shaped elevations. All sensilla, except- not distinctly margined in front, but almost ing some in mouth region, bear minute rounded off into the pronotal neck, which setae. Mandibles triangular, lacking sclero- does not slope ventrally. Propodeum shiny, tised ventral plate in flattened condition plicaeincompleteorabsent...... (Fig. 11) . . . Pteromalidae, Psilonotus spec...... P. adamas Walker Further identification on qual- (Graham 1969: 627) itative characters to species level not possible. – Antennae not protruding, flattened bell- Key to immature stages present inside gall shaped pedestal bearing antennae absent. 1. Larva cream-coloured, pale yellowish or Body sensilla without minute setae. Mandi- whitish. Biting mouth parts distinct, dark bles, if flattened, with conspicuous ventral brown coloured . . . . . Chalcidoid parasitoid – 2 plate. (Figs 16–17) ...... – Larva bright orange-red coloured; scle- ...... Eulophidae–Aprostocetus spec. rotised plate, so called spatula sternalis, Further identification on qualitative on ventral side of first thoracic segment. characters to species level only partially pos- Mouthpartsinconspicuous...... sible, see remark under descriptions of larvae...... GallmidgehostSemudobia Gall midge larvae may be inert Description of fully grown chalcidoid and show black punctures due to host feeding usually of adult parasitoids of Psilonotus. parasitoid larvae = Gall contains black parasitoid enveloped by Tor ymus Dalman, 1920 gallmidgelarvalskin...... Head (Figs 1–6) ...... Platygastridendoparasitoid Cranium (Figs 4, 6). The torymid larvae associ- Host larval skin is dis- ated with Semudobia are distinguished by a con- coloured, enclosing Platygaster wasps; very spicuous conical medio-frontal sclerotic protruding, occasionally orange tinted host skins enclos- ‘nose’. Antennae simple and usually well developed. ing Metaclisis phragmitis Debauche may be Origin of frontal muscle indicated in cranial wall found (Roskam 1986). The latter species (dfm, Short 1952, 1959). Demarcation of clypeus was not encountered during this study. indistinct. Anterior tentorial pits (at) distinct, situ- Platygastrids develop in au- ated ventrally of antennae. Seven pairs of long setae, tumn into inert adults which overwinter in viz., two pairs of superior frontal setae (Fs), two pairs the gall in diapause and become active and of inferior frontal setae (Fi), two pairs of genal setae emerge in following spring. For morpholo- (Ge), situated laterally to antennae and anterior ten- gical and biological details, see Roskam (1986). torial pits. Two pairs of setae of intermediate length 2. Body surface glabrous, lacking conspicuous are inserted, respectively, on dorsal and ventral blunt- bristles(setae)...... 5 conical sclerotised elevations, leaving the submedian – Conspicuous bristles present on head as elevations without setae. Elevations are well sclero- wellasoneachbodysegment...... 3 tised in T. fuscicornis, less distinct or absent in T. ni- 3. Head with ‘nose’, median sclerotic brown tidulus. One pair of short setae on labrum, accompa- conical elevation. Clypeus indistinct, not nied by five pairs of sensilla. sclerotic...... Torymidae,Tor ymus –4 Under-lipcomplex(Fig.6,ul).Thiscomplex consists of the united hypopharynx, maxillae and

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Figs 1–6. Torymus fuscicornis, final instar larva. 1, spiracle and pleural seta on 2nd thoracic segment; 2, spiracle on 7th abdominal segment; 3, larva, lateral view; 4, head, lateral view; 5, 9th abdominal segment and anal segment, lateral view; 6, head, frontal view. a1, 8, 1st and 9th abdominal segment, respectively; an, antenna; at, anterior tentorial pit; dfm, mark on cranial wall at place of origin of frontal muscles; Fi, Fs, inferior and superior frontal seta, respectively; h, head; La, labral seta; man, mandible; ma se, maxillary sensilla; no, ‘nose’, conical medio-frontal sclerotic protruding; pol se, postlabial sensilla; prl se, prelabial sensilla; pr ms, median prelabial sensilla; s, spiracle; sp, sclerotised plate; th1, 3, 1st and 3rd thoracic segment, respectively; ul, under lip complex. 1–2, 63 × 18; 3, 6.3 × 18; 4–5, 40 × 18; 6, 25 × 18. labium. Although the demarcation of membranes is to spiracles on spiraculate thoracic and abdominal usually indistinct, regions can be distinguished by segments, three to four rows of medium to short presence of particular setae and sensilla. Three pairs length ventrally situated to spiracles, not arranged of maxillary sensilla (max se), the most ventrally ones in a definite pattern. Sensilla in dorsal, pleural and compound. Four pairs of lateral prelabial sensilla, ventral areas absent. Anal segment (Fig. 5) with two one pair of short median prelabial setae and one pair pairs of short setae dorsal to anal slit, and two pairs of short postlabial setae. ventrally. Tentorium. Mandibles triangular, well sclerotised, one-toothed, articulating with anterior and posterior Psilonotus Walker, 1834 processes of pleurostomae. Epistomal bridge usually No qualitative differences could be detected between weakly sclerotised, often indistinct. P. adamas and P. achaeus; size of spiracles of P. hortensia, especially on A7, may exceed those of the Body (Figs 1–3, 5, Table 1) other two species. [Distribution of sizes of head and body segments is expected to be binominal due to size difference Head between larger females and smaller males.] Cranium (Fig. 11). Antennae situated on distinct Segmentation. As in all chalcidoids, body consists semiglobose elevations. Antennae simple, blunt con- of thirteen segments, viz., three thoracic (Th 1– ical, well developed. Origin of frontal muscle indi- 3) and ten abdominal segments, the ultimate of cated in cranial wall (dfm, Short 1952). Demarcation which is the anal segment (A 1–9, AS, respectively). of clypeus usually distinct. Anterior tentorial pits (at) Respiration peripneustic; spiracles absent from Th 1, distinct, situated ventrally to antennae. Sensilla usu- A8 and 9, and AS. ally with very short setae; viz., one pair of superior Setae and sensilla. Proximally five paired rows of frontal setae (Fs) situated above antennae, one pair setae of large to medium length dorsally situated of inferior frontal setae (Fi) situated medially to an-

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Table 1. Tor ymus, characters of mature larvae, measurements in μm, N = 10 per cohort. a, abdominal segment; as, anal segment; fr, frons; th, thoracic segment, Ø sp, diameter of spiracle; measurements of longest setae close to spiracles (Th, A) or longest ones on AS.

Length Height Height Length Height Length Ø sp Length Ø sp Length Ø sp Length body body head seta fr as seta as th2 seta th2 a1 seta a1 a7 seta a7

T. nitidulus on Semudobia tarda mean 1265 807 383 64.3 128 10.014.749.112.325.711.529.3 sd 186 134 41 18.7162.42.012.11.57.81.79.3 max 1563 947 446 101.4 151 12.517.265.514.042.114.049.9 min 932 568 318 34.3936.210.928.19.412.59.520.3

T. fuscicornis on Semudobia betulae mean 1527 884 401 65.2 134 10.116.54 47.614.022.612.524.0 sd 224 129 42 14.7231.51.97 12.21.66.81.54.7 max 1816 1042 446 96.7 159 12.520.28 70.215.632.815.629.6 min 1153 663 310 48.4 101 7.814.04 32.710.915.610.917.2 tennae, one pair of genal setae (Ge), situated later- Body (Figs 8–10, Table 2) ally to epistomal arch; hypostomal setae absent. Two [Distribution of sizes of head and body segments, pairs of short setae on labrum. One pair of sensilla segmentation and arrangement of spiracles see Tor y- on labrum situated between the labral setae. mus.] Under-lip complex (Fig. 11). Four pairs of lateral Sensilla. All abdominal segments with one pair prelabial sensilla (prls) are present, two pairs with of dorsal sensilla, one pair of pleural sensilla. First setae; three pairs of median prelabial sensilla (prms), thoracic segment and ninth abdominal segment with two pairs setose and one pair of postlabial setose one pair of ventral sensilla. Anal segment (Fig. 7) sensilla (pos). with two pairs of sensilla dorsally of anal slit, and Tentorium. Mandibles triangular, well sclerotised, one pair ventrally. All sensilla bear short setae. one-toothed, articulate with anterior and posterior processes of pleurostomae. Epistomal bridge usually Aprostocetus Westwood, 1822 weakly sclerotised. Head Cranium (Fig. 17). Distinguished by all sensilla lacking distinct setae (Aprostocetus clavicornis, A. constric-

Figs 7–11. Psilonotus cf. adamas (dissected from galls of both Semudobia betulae and S. tarda) ﬁnal instar larva. 7, 8th,9th abdominal segment and anal segment, terminal view; 8, larva, lateral view; 9–10, spiracles on 2nd thoracic and 7th abdominal segment, respectively; 11, head, frontal view. Abbreviations as in Figs 1–6; max se, maxillary setae; prel se, prelabial setae; pol se, postlabial seta. 7, 11, 25 × 18; 8, 6.3 × 18; 9–10, 63 × 18.

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Table 2. Psilonotus, characters of mature larvae, measurements in μm, N = 10 per cohort, P. h o r t e n s i a excepted, N = 1. a, abdominal segment; as, anal segment; th, thoracic segment, Ø sp, diameter of spiracle.

length body height body height head height as Ø sp th2 Ø sp a1 Ø sp a7

P. adamas on Semudobia tarda mean 1360 837 330 133 14.712.99.4 sd 219 98 33 12 2.00.81.5 max 1737 947 392 159 17.214.012.5 min 979 647 301 124 10.912.57.8

P. adamas on Semudobia betulae mean 1309 846 334 126 15.313.19.7 sd 94 71 17 8 10.71.11.2 max 1484 963 361 136 15.614.010.9 min 1200 742 316 116 14.010.97.8

P. a c h a e u s on Semudobia skuhravae mean 1462 943 355 137 14.514.010.5 sd 140 106 33 16 2.21.01.3 max 1658 1074 391 167 17.215.612.5 min 1311 726 316 116 9.412.59.4

P. hortensia on Semudobia skuhravae (only one reared specimen) μm 1311 711 313 128 17.215.614.0 tus) or minute setae (A. pallipes). Antennae simple, Eupelmus urozonus Dalman, 1920 blunt conical, well developed. Origin of frontal mus- [Only one larva collected, ectoparasitic on Semudo- cleindicatedincranialwallinvisible,aswellasan- bia skuhravae on Betula pubescens, Figs 18–20.] terior tentorial pits. Demarcation of clypeus usually distinct, not sclerotised. Superior frontal sen- Head silla (Fs) absent, one pair of inferior frontal sensilla Mouth region (Fig. 18). Eupelmus urozonus larvae are (Fi) situated medially of antennae present, three pairs distinct by a conspicuously sclerotised six-toothed of genal setae (Ge), situated laterally to epistomal clypeus with 5 other teeth situated ventral to the arch, hypostomal sensilla absent, two pairs of sensilla stoma. Setae on head as well as on body long, ﬂexible on labrum, the lateral pair often accompanied by a and long tapering. One pair of setae of intermediate darker sensilla-like structure. length on labrum. Under-lip complex (Figs 16–17). Three pairs of Under-lip complex. Three pairs of maxillary sen- maxillary sensilla (max se) are present, one pair large, silla (max se) are present, one pair of prelabial sensilla the other two pairs small and often distinct; two pairs (prl se), one pair of postlabial sensilla (pol se). of prelabial sensilla (prl se), one pair large, one pair Tentorium. Mandibles triangular, well sclerotised, small and often indistinct. one-toothed, articulate with anterior and posterior Tentorium. Mandibles pointed with large distal processes of pleurostomae. Epistomal bridge weakly plate, visible in ventral aspect, well sclerotised, one- sclerotised, indistinct. toothed, articulate with anterior and posterior processes of pleurostomae. Epistomal bridge not visible. Body Segmentation and spiracular arrangement, see Tor y- Body (Figs 13–15, Table 2) mus. [Distribution of sizes of head and body segments, Setae and sensilla. Two rows of setae situated dor- segmentation and spiracular arrangement, see Tor y- sally to spiracles, one pair in pleural region close to mus.] spiracles and two rows situated ventrally to spiracles. Sensilla. Abdominal segments, seventh excepted, All setae long and gradually tapering. Sensilla in dor- with one pair of dorsal sensilla, all abdominal seg- sal, pleural and in ventral areas absent. Anal segment ments with one pair of pleural sensilla. First thoracic with two pairs of short setae dorsal to anal slit, and segment and ninth abdominal segment with one pair four pairs ventrally of medium length. of ventral sensilla. Anal segment (Fig. 12) with two pairs of sensilla dorsally of anal slit, and one pair ven- = trally. Measurements (in μm, n 1) Length of body 1500, width of body 980; width head 430, width anal segment 220 μm.

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Figs 12–17. Aprostocetus clavicornis. 12, anal segment, terminal view; 13, larva, lateral view; 14–15, spiracles on 2nd thoracic and 7th abdominal segment, respectively; 16, mouth parts and under lip complex (mandibles are rotated 90° downwards relative to normal position); 17, head, frontal view. Abbreviations as in Fig. 1–6; max se, maxillary sensilla; prl se, prelabial sensilla. 12, 17, 25 × 18; 13, 6.3 × 18; 14–15, 63 × 18; 16, 40 × 18.

Diameter spiracles on A2 29, on Th1 24, on A7 Although it is rather difﬁcult to pass diapause un- 24 μm. der artiﬁcial conditions of a refrigerator and mor- Length of frontal setae 200, of pleural setae (near- tality is considerable therefore, midges as well as est to spiracle) on Th2 245, on A1 185, on A7 95 parasitoids emerged in substantial numbers, ranging and on AS 30 μm. from 9.5 up to 37.8% of the reared galls. Parasitism varied from 6.8 up to 68.6%. Remarkable were the Host-parasitoid associations large numbers of S. skuhravae, especially in the HSK Results of samples reared during 2011 and 2012 samples: in Roskam (1977) this species, although in The Netherlands (NL) and in Germany, Hoch numbers per locality differed substantially, was often Sauerland Kreis (HSK) are presented in Table 4; less abundant. Numbers of collected galls as well as those collected in December 1971, only Dutch sam- of reared insects do not allow drawing conclusions ples, in Table 5. about differences between NL and HSK. Chance

Table 3. Aprostocetus, characters of mature larvae, statistics measurements in μm, N = 10 per cohort. a, abdominal segment; as, anal segment; th, thoracic segment, Ø sp, diameter of spiracle.

length body height body height head height as Ø sp th2 Ø sp a1 Ø sp a7

A. clavicornis on Semudobia tarda mean 1210 633 238 157 10.69.08.0 sd 171 83 17 34 1.20.70.5 max 1547 742 256 210 12.59.49.4 min 979 505 210 116 7.87.87.8

A. clavicornis on Semudobia betulae mean 1140 614 227 154 10.68.98.1 sd 125 115 32 33 1.41.71.0 max 1279 758 260 202 12.512.59.4 min 868 426 155 105 7.86.26.2

A. pallipes/constrictus on Semudobia skuhravae mean 1350 786 263 168 15.913.613.4 sd 84 66 13 22 1.01.31.1 max 1500 868 279 202 17.215.614.0 min 1216 663 233 136 14.010.910.9

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Figs 18–20. Eupelmus urozonus. 18, clypeus, mandibles and under lip complex, frontal view; 19, antenna, lateral view; 20, spiracle 2nd thoracic segment. Abbreviations as in Figs 12–17, cl, clypeus. 18, 40 × 18; 19–20, 63 × 18. may explain the absence of a particular species in a bract galling S. skuhravae. Apparent ecological differ- particular locality. ences between A. pallipes and constrictus could not be Associations between gall midges and platygastrid found. egg-larval parasitoids are analysed in Roskam (1986). All three species of Psilonotus are exclusively as- Remarkable host specificity was found in that sociated with Semudobia and are ectoparasitoids of study, indicating Platygaster betularia preferred S. mature larvae. Both P. achaeus and P. hortensia were skuhravae,andonlyS. betulae of the fruit galling frequently reared from S. skuhravae at both localities; midges. P. betularia was only infrequently reared all three species were reared from S. betulae,NLonly; from S. tarda. Metaclisis phragmitis was earlier found and P.achaeus was absent from S. tarda at both local- in Semudobia betulae and S. tarda and was absent ities. P. adamas was rarely reared from S. skuhravae, from S. skuhravae (Roskam 1986). Absolute host HSK only; and emerged in low numbers from both specificity was not found for chalcidoid parasitoids fruit galling midges S. betulae and S. tarda,inNL. during the present study but distinct preferences The 1971 rearing results corroborate those of were present. 2012 but show stricter host preferences. In Aprosto- Both Tor ymus species are ectoparasitoids of imma- cetus, A. pallipes and only one specimen of A. con- ture Semudobia gall midges. Substantial numbers of strictus emerged from bract galls (caused by Semu- T. fuscicornis were reared on S. skuhravae,inNLas dobia skuhravae); A. clavicornis was abundant, but well as in HSK and on S. betulae in NL. T. nitidulus, only in seed galls (caused by S. betulae and S. tarda). on the other hand, was present in substantial num- In Psilonotus, P. achaeus was common in bract galls, bers only on S. tarda at both localities. Single records, whereas P. adamas preferred fruit galls and P. h o r t e n - of T. fuscicornis and of T. nitidulus may be due to sia numbers were too low to draw conclusions. Fi- identification errors by parasitoids or the investiga- nally, in Tor ymus the 2012 results were also corrobo- tor. It may be concluded that T. fuscicornis preferred rated: T. nitidulus preferred fruit galls and T. fuscicor- S. skuhravae and S. betulae,butnotS. tarda, the latter nis wasrearedfrombract-aswellasfruitgalls. being the preferred host for T. nitidulus. Parasitoid-host associations are summarised in Three species of Aprostocetus are regular ectopar- Fig. 21. A particular phenomenon must be reported asitoids of Semudobia, viz., A. clavicornis, constrictus here. Platygastrids usually and chalcidoids belonging and pallipes. A. clavicornis was reared in substantial to Aprostocetus and Psilonotus always deposit only one numbers on S. tarda at both localities and S. betu- egg per host. Both Tor ymus species, however, lay sys- lae in NL only. A. pallipes and A. constrictus were tematically two eggs per still very small host larva. relatively frequent on S. skuhravae at both localities After hatching of these two eggs one larva first feeds but absent from the two other gall midge species. on its sibling allowing the gall midge larva to grow. Hence a different preference exists, on the one hand Only after consuming of its sibling it starts feeding of A. clavicornis for seed galling S. betulae and tarda, on the gall midge host. This might be an adaptation: and on the other of A. pallipes and constrictus for the in this early phase of parasitisation the host is first al-

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Table 4. Host parasitoid associations, determined from Table 5. Rearing results of chalcidoid parasitoids, sepa- reared insects during the year 2012. NL, The Nether- rated for bract- and fruit galls during December 1971. lands; HSK, Germany, Hoch Sauerland Kreis. chalcidoids Bract Fruit NL HSK Aprostocetus constrictus 1 0 S. skuhravae (bract galls) pallipes 9 0 altitude (m) 10 760 clavicornis 0 47 galls 653 1536 Torymus fuscicornis 71 78 reared midges 84 503 nitidulus 0 40 parasitoids reared wasps 51 78 Platygaster spec 29Psilonotus achaeus 28 1 Aprostocetus constrictus 412 hortensia 14 Aprostocetus pallipes 713 adamas 250 Aprostocetus clavicornis 0 1 Torymus fuscicornis 22 23 Torymus nitidulus 11 Psilonotus achaeus 710 Psilonotus hortensia 77with records of specimens swept from birch. As ex- Psilonotus adamas 0 2 pected, emerging of gall midges overlaps completely Eupelmus urozonus 10that of platygastrid egg parasitoids. Aprostocetus and all reared total (nr) 135 581 Psilonotus emerged simultaneously after the flight pe- reared total (%) 20.737.8 parasitised (%) 37.813.4 riod of Semudobia during the new generation second S. betulae (fruit galls) and third instar larvae, whereas early emergence of altitude (m) 10 760 Tor ymus waspsoverlapswithemergenceofmidges galls 596 353 as well as of platygastrid parasitoids; and late emerg- reared midges 43 69 parasitoids reared wasps 53 5 ing wasps are partially simultaneous with Aprostoce- Platygaster spec 33tus and Psilonotus, indicating attacking of first and Aprostocetus constrictus 00second instars of host larvae – for host phenology, pallipes 00see Roskam (1977, Table 4). The emergence of T. clavicornis 13 1 Torymus fuscicornis 23 1 nitidulus reflects the association with S. tarda,be- nitidulus 00ing the latest of the host species. As is indicated in Psilonotus achaeus 3 0 Fig. 22, adults of Aprostocetus and Psilonotus are still hortensia 8 0 active at the end of October. The large time-span, adamas 3 0 Eupelmus urozonus 00end of May until the end of October, in which the all reared total (nr) 96 74 adults of Aprostocetus and Psilonotus occur may sug- reared total (%) 16.121.0 gest a multivoltine life style with overlapping genera- parasitised (%) 55.26.8 S. tarda (fruit galls) altitude (m) 10 760 galls 399 189 reared midges 13 11 parasitoids reared wasps 25 24 Platygaster spec 0 1 Aprostocetus constrictus 00 pallipes 00 clavicornis 10 5 Torymus fuscicornis 10 nitidulus 616 Psilonotus achaeus 00 hortensia 41 adamas 41 Eupelmus urozonus 00 all reared total (nr) 38 35 reared total (%) 9.518.5 parasitised (%) 65.868.6 lowed to grow before becoming a sufficient resource for complete parasitoid development. Fig. 21. Parasitoid and inquiline host Semudobia preferences. Data for inquilines are from Roskam, 1979; for Phenology egg-larval parasitoids from Roskam, 1986. All arrows Figure 22 summarises results of Semudobia galls indicate regular associations, the incidental ones are, for reared under natural outdoor conditions, combined sake of clarity, not given.

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Fig. 22. Phenology insects in birch catkins. Time blocks represent weeks. Filled (X) blocks regard to specimens reared under outdoor conditions as well as to specimens swept from birch; empty blocks refer to specimens swept from birch only. tions, in contrast with a univoltine life style of Platy- conspicuous yellow coloured antennae in males as gaster and Tor ymus. well as the more abundant yellow marks all over body and legs in both sexes might be considered as autapo- Patterns of co-speciation morphies for T. nitidulus. This corroborates the spe- Phylogeny of gall midge Semudobia and co-speciation pattern in Semudobia,becauseT. nitidulus, ciation pattern with host plant Betula was hypoth- with a number of autapomorphies is associated with esised in Roskam (1979): the fruit gall inducing S. S. tarda, the midge species with most apomorphies betulae, together with its Nearctic geographic vicari- of the hosts, whereas T. fuscicornis is associated with ants S. brevipalpis and S. steenisii, are considered as both other Semudobia midges. asistergroupofS. tarda; all fruit galling midges in Aprostocetus is a large genus of Eulophidae and their turn are considered as a sister group of circum- is represented with three species in the Palaearctic boreal S. skuhravae, which induces galls in bracts of birch catkins biocoenosis. A. pallipes is similar to fruit catkins. the usual eulophid habitus having an ovoid gaster. Of Platygaster egg parasitoids only two repre- A. constrictus and A. clavicornis share elongate fe- sentatives are associated with three Semudobia host male gasters. The rigid antennal bristles in A. pal- species, viz., P.betularia Kieffer, 1916 is strictly asso- lipes males could be considered as an apomorphy; the ciated with S. skuhravae,aswellasS. betulae,whereas setose larval papillae and female ovoid gaster, how- P. betulae (Kieffer, 1916) was only found in S. tarda ever, as a plesiomorphic state. The elongate gaster (Roskam, 1986). Both Platygaster species belong to a is shared with other species assigned to Aprostocetus large genus of mainly gall midge parasitoids. Because which parasitize other gall midges (Graham 1987). P. betularia is associated with two gall midge hosts, Hence, within the birch catkin system associations viz., S. skuhravae and S. betulae which are not sister of all three Aprostocetus species should be regarded species, we must conclude an independent colonisa- as independent colonisations. It is peculiar that A. tion of, at one hand P. betularia on S. skuhravae and pallipes with plesiomorphic character states, viz.,the S. betulae, and, on the other hand, of P. betulae of S. ovoid female gaster of and setose larval sensilla is de- tarda. Metaclisis phragmitis Debauche, 1947, rarely limited to S. skuhravae, the midge which is hypoth- found in birch catkins and not in this study, only esised as basal in the midge phylogeny. A. clavicornis emerged from fruit galls caused by Semudobia betu- is specialised on both seed galling midges, whereas lae and S. tarda. Because its adults appeared relatively A. constrictus and A. clavicornis are both well adapted late, its absence from the early emerging S. skuhravae to ovipositing in the birch catkin by their elongated was suggested to be a mismatch between parasitoid female gaster. and host phenology (Roskam 1986). Representatives of the small pteromalid genus Tor ymus larval ectoparasitoids are, like Platygaster, Psilonotus are exclusively associated with Semudobia. represented by only two species. Although both Psilonotus adamas has a rounded pronotum. Clos- species belong to the large torymid genus Tor ymus, est relative is P. achaeus, sharing on the one hand they were earlier assigned to Lioterphus Thomson, the apomorphic bilaterally compressed female gaster, exclusively associated with Semudobia. It is therefore an adaptation to ovipositing in the birch catkin, as acceptable to regard them as sister species, with the well as the ﬂattened head and lower placed antennae, specialisation on Semudobia as a synapomorphy. The but sharing on the other hand a carinate pronotum reduced sclerotic frontal elevations in larvae and the with P. hortensia, considered as plesiomorhic, which

Downloaded from Brill.com09/26/2021 07:28:12AM via free access 32 Tijdschrift voor Entomologie, volume 156, 2013 prefers as host S. skuhravae, with also plesiomorphic female gaster. The head (proximally-distally), thorax traits. Basal in the Psilonotus phylogeny is P.hortensia, (dorsal-ventrally) and female gaster (bilaterally) of P. lacking any Semudobia host preference in Palaearc- achaeus and P. adamas are distinctly flattened, again tic birch catkins. A possible scenario here might be an adaptation allowing the females to wriggle bet- an early colonisation by P. hortensia, which allowed ter between the catkin scales. These traits are con- the already existing association between Semudobia sidered as a synapomorphy of the latter two (sister-) and Psilonotus to better exploit the seed galling Semu- species. A rounded pronotum of P.adamas – carinate dobia species by favouring wriggling between catkin in P. achaeus and P. hortensia – is a further (autapo- scales, necessary to lay eggs. Nevertheless, specialist P. morphic) trait facilitating wriggling into birch fruit achaeus and P.adamas did not outcompete generalist catkins. P. hortensia, which is still a frequent parasitoid. Phenology and association Discussion All four parasitoid genera are specialised on different developmental stages of their hosts. Only the egg- Morphology larval platygastrid parasitoids have an endoparasitic Gall midge host Semudobia species are distinct by life style. The results of reared Semudobia parasitoids, their galls, as well as adult and larval morphology. especially during the 2012 experiment, may endorse In parasitoids, adults are distinct, but larvae could Askew & Shaw (1986). These authors stipulated that mainly be discriminated between genera. Within ge- late parasitoids – idiobionts in their terminology – nera only a few larval characters allowed discrimina- are expected to be less fastidious than parasitoids of tion between species. Hence, differentiation of im- early host stages – koinobionts in their terminol- mature host stages is more distinct than that of para- ogy – because synchronisation of koinobiont endo- sitoids. as well as ectoparasitoids is more critical and the Chalcidoid parasitoids have several adaptations resources for idiobiont ectoparasitoids, already sub- which favour especially the laying of eggs in compact stantially diminished by early koinobiont parasitoids, inflorescences like fruit catkins of birch. Aprostocetus are less abundant. Platygastrid endoparasitoid Platy- clavicornis and A. constrictus, for example, have elon- gaster and chalcidoid ectoparasitoid Tor ymus are typ- gate female gasters which allow them to wriggle bet- ical koinobionts in terms of specialist host-parasitoid ter between the catkin scales to reach the midge galls. association. Representatives of these two genera have Torymus fuscicornis and T. nitidulus have, like strict associations with their host species, as predicted many Torymidae, long ovipositors which allow them by Askew & Shaw (1986). Specific associations in to drill into hidden galls. T. fuscicornis and T. nitidu- Psilonotus are present, but less strict. Also here Askew lus differ mainly by the colour of the male antennae: & Shaw (1986) is endorsed. The particular feeding metallic green in T. fuscicornis and bright yellow in on siblings in Tor ymus may be a further specialisa- T. nitidulus. This difference may have evolved during tion to parasitisation of early developmental phase of an episode of allopatry, an episode also hypothesised the host. The host-feeding habit in Psilonotus females for Semudobia (Roskam, 1979). The difference be- is a particular adaptation to provide proteins for egg came functional after secondary sympatry, avoiding production. Host feeding has not been observed in hybridisation: during courtship females are able to Aprostocetus, but might not be excluded. recognize the right mates. Although Grissell (1976) placed Lioterphus in synonymy, there may be argu- ments to maintain it as an independent genus. The Co-speciation patterns size of adults in both species is significantly smaller It is unlikely that co-speciation in Betula host plants, than that of species which belong to Tor ymus.Both Semudobia gall midges and parasitoids is a result of species exclusively develop in female birch catkins. a strict co-evolutionary process in which reciprocal The larval character of a ‘sclerotised nose’ could well selection pressure shaped parallel traits in host plant-, be an autapomorphy validating Lioterphus.Anoseis gall midge- and parasitoid phylogenies. Merely, gall present in Tor ymus but is all white like the rest of midges passively followed speciation of birches and the face (Askew, in litt.). However, more study of parasitoids followed speciation of gall midges and/or Tor ymus larvae is needed before making taxonomic host plants. Jermy (1976) coined for this less strict changes. co-evolutionary process the concept of sequential In Psilonotus apparently a trend evolved from a evolution in explaining why phylogenies of associates normal pteromalid body shape into a flattened one. may display congruencies. The body shape in P.hortensia still matches the shape Congruent patterns in host and parasite phy- of related genera like Mesopolobus Westwood, 1833: logeny could be shown in Semudobia–Betula associ- a relatively globular head, a high thorax and an ovoid ation (Roskam 1979). Such patterns cannot be ex-

Downloaded from Brill.com09/26/2021 07:28:12AM via free access Roskam: Chalcidoid ectoparasitoids in birch catkins 33 pected in parasitoid genera like Platygaster and Apros- dae). – University of California Publications 79: 1–120 tocetus with species parasitising various, and unre- (p. 58). lated hosts. In Tor ymus, however, with only two Hodges, S., 1969. Gall midges (Diptera-Cecidomyiidae) apparently sister species on Semudobia, indeed the and their parasites (Hymenoptera) living in female species with several (aut)apomorphies, T. nitidulus, birch catkins. – Transactions of the Society of British is associated with the gall midge with also most Entomology 18: 195–226. (aut)apomorhies, S. tarda. This may be an exam- Jermy, T., 1976. Insect-host plant relationship: co- ple of sequential evolution of one parasitoid species evolution or sequential evolution? – Symposia Biolog- which followed gall midge speciation. ica Hungarica 16: 109–113. Redfern, M., 2011. Plant galls. – The New Naturalist In Psilonotus with three species associated with Library, No. 117. HarperCollins Publishers, London, three related hosts sequential evolution might be ex- 562 pp. pected but is not always obvious: P. hortensia with Roskam, J.C., 1977. Biosystematics of insects living in fe- many plesiomorphic traits displays a generalist pat- male birch catkins. I. Gall midges of the genus Semudo- tern by parasitising all Semudobia species. P. achaeus bia Kieffer (Diptera, Cecidomyiidae). – Tijdschrift voor and P. adamas have more specialist host preferences Entomologie 120: 153–197. and adaptations for ovipositing in birch fruit catkins. Roskam, J.C., 1979. Biosystematics of insects living in P. achaeus sharing apomorphic traits with P. adamas female birch catkins. II. Inquiline and predaceous gall but, on the other hand, sharing a plesiomorphic midges belonging to various genera. – Netherlands trait of the pronotum with P. hortensia,prefersbract Journal of Zoology 29: 283–351. galling S. skuhravae. P. adamas, showing a further Roskam, J.C., 1982. Larval characters of some eurytomid (aut-) apomorphy prefers both fruit galling S. betulae species (Hymenoptera, Chalcidoidea). – Proceedings and S. tarda. The differentation between P. adamas of the Koninklijke Nederlandse Akademie van Weten- and P.achaeus might indeed be explained as an exam- schappen Series C 82: 293–305. ple of sequential evolution paralleling the differenti- Roskam, J.C., 1986. Biosystematics of insects living in fe- ation of fruit galling midge hosts Semudobia betulae male birch catkins. IV. Egg-larval parasitoids of the genus Platygaster Latreille and Metaclisis Förster (Hy- and S. tarda from bract galling S. skuhravae. menoptera, Platygastridae). – Tijdschrift voor Ento- mologie 129: 125–140. Acknowledgements Roskam, J.C. & G.A. van Uffelen, 1981. Biosystematics of insects living in female birch catkins. III. Plant-insect For their constructive criticism of this manuscript I relation between white birches, Betula L., Section Ex- am indebted to Dr. M. Redfern, Dr. R.R. Askew, celsae (Koch) and gall midges of the genus Semudobia Dr. K.M. Harris and some anonymous reviewers. Kieffer (Diptera, Cecidomyiidae). – Netherlands Jour- Mr. M.J. Gijswijt identified the Aprostocetus species. nal of Zoology 31: 533–553. Mrs. S. Kofman and Mr. D.M. Hallensleben were Short, J.R.T., 1952. The morphology of the head of larval most helpful with the preparation of materials. For Hymenoptera with special reference to the head of the the loan of specimens in their care I thank Naturalis Ichneumonoidea, including a classification of the final Biodiversity Center (RMNH), Leiden, The Nether- instar larvae of the Braconidae. – Transactions of the lands. Royal Entomological Society, London 103: 27–66. Short, J.R.T., 1959. A description and classification of the final instar larvae of the Ichneumonidae (Insecta, References Hymenoptera). – Proceedings of the United States Askew, R.R. & M.R. Shaw, 1986. Parasitoid communities: National Museum 110: 391–511. their size, structure and development. – In: J. Waage & Walker, F., 1833. Monographia Chalciditum. – Entomo- D. Greathead (eds), Insect parasitoids. Academic Press, logical Magazine 1: 115–142 (p. 138). Oxford, pp. 225–264. Graham, M.W.R. de V., 1969. The Pteromalidae of Received: December 12, 2012 North-Western Europe (Hymenoptera: Chalcidoidea). Accepted: February 21, 2013 – Bulletin of the British Museum (Natural History), suppl. 16: 1–908 (pp. 627–628). Graham, M.W.R. de V., 1987. A reclassification of the European Tetrastichinae (Hymenoptera: Eulophidae) with a revision of certain genera. – Bulletin of the British Museum (Natural History, Entomology) 55: 1– 392. Grissell, E.E., 1976. A revision of western Nearctic species of Tor ymus Dalman (Hymenoptera: Torymi-

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Appendix: Data of used materials Psilonotus achaeus on Semudobia skuhravae, Betula pubescens Slides of full-grown larvae used for data in Tables 1–3 are 780615.08, Valkenswaard, Malpie; 800630.09, -13–15, The deposited in Naturalis Biodiversity Center (RMNH), Leiden, Hague, Meijendel, Jan. 28, 1980; 800702.34–35, -39–40, The The Netherlands. All materials are collected in The Nether- Hague, Meijendel, Apr. 18, 1979; 820111.01, The Hague, lands. Meijendel, Aug. 16, 1981. Torymus fuscicornis on Semudobia betulae, Betula pubescens Psilonotus hortensia on Semudobia skuhravae, Betula pendula 771202.09, Voorschoten, Duivenvoorde, Sept. 14, 1977; The Hague, Meijendel, Dec. 21, 1972. 800808.01–06, 801103.01, The Hague, Meijendel, Jan. 28, Aprostocetus clavicornis on Semudobia betulae, Betula pu- 1980; 820105.01 and 820921.04, The Hague, Meijendel, bescens 810205.53, -59, -61, -63–64, The Hague, Mei- Sept. 23, 1981. jendel, Jan. 28, 1980; 820113.01, The Hague, Meijendel, Torymus nitidulus on Semudobia tarda, Betula pubescens Oct. 29, 1981; 820923.30, The Hague, Meijendel, Feb. 9, 821201.65 and -70, 821202.67–68, 821208.50, -52, 55–58, 1978; 821011.18, The Hague, Meijendel, Aug. 23, 1981; Voorschoten, Duivenvoorde, Feb. 9, 1978. 821012.07–08, The Hague, Meijendel, Sept. 30, 1982. Psilonotus adamas on Semudobia betulae, Betula pubescens Aprostocetus clavicornis on Semudobia tarda, Betula pubescens 800318.15–16, 800320.04–07, -10, The Hague, Meijendel, 771206.22–24, 771208.12, -14–15, Voorschoten, Duivenvo- Jan. 28, 1980; 800324.01, 820105.02–03, The Hague, Meij- orde, Sept. 14, 1977; 800311.01–04, The Hague, Meijendel, endel, Nov. 23, 1981. Jan. 28, 1980. Psilonotus adamas on Semudobia tarda, Betula pubescens Aprostocetus pallipes/constrictus on Semudobia skuhravae, 791026.05–06, Voorschoten, Duivenvoorde, Mar. 1979; Betula pubescens 780418.02, 780419.01, -03, -07, -09, 800318.01, -03, -06–07, The Hague, Meijendel, Jan. 28, 780420.01, Valkenswaard, Malpie, Dec. 20, 1977; 1980; 800807.03, -05–07, The Hague, Meijendel, Apr. 18, 800318.08–10, -12, The Hague, Meijendel, Jan. 28, 1980. 1979.

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