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

In: Tijdschrift voor Entomologie
Author:
J.C. Roskam Department of Evolutionary Biology, Institute of Biology, University of Leiden, Sylvius Laboratory, Sylviusweg 72, 2333 BE Leiden, The Netherlands. j.c.roskam@biology.leidenuniv.nl

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Fully grown larvae have been described of chalcidoids belonging to four genera, viz., Torymus 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.

Introduction

Insects living in female birch catkins are all centred upon galls in fruit gall caused by representatives of the gall midge genus Semudobia Kieffer, 1913 (Diptera: Cecidomyiidae). This genus consists of five species, viz., the fruit gall inducing Palaearctic S. betulae (Winnertz, 1853), together with its Nearctic geographic vicariants S. brevipalpis Roskam, 1977 and S. steenisii Roskam, 1977; S. tarda Roskam, 1977 is exclusively Palaearctic and also induces fruit galls; it has no Nearctic vicariants. Finally the circumboreal midge S. skuhravae Roskam, 1977 induces galls in the bracts (fruit scales) of the catkins (Roskam 1977, part I of the series on the entomofauna of female birch catkins).

Related publications on this entomofauna dealt with host preferences of the gall inducing midges (Roskam & van Uffelen 1981; part III). Apart from gall inducers, some inquiline, saprophagous and predaceous gall midges are frequently found in female birch catkins (Roskam 1979; part II). Part IV (Roskam 1986) was devoted to the egg-larval platygastrid endoparasitoids. The question why three closely related gall midges can co-occur in the same niche can be made understandable from a historical-ecological perspective. Inquiline gall midges and platygastrid parasitoids make clear how specialised representatives of these guilds may track their hosts.

Apart from some incidental chalcidoid parasitoids, Semudobia gall midges are the target for at least eight regular chalcidoid ectoparasitoid species belonging to three genera in three different families. Two torymid parasitoids, now placed in the large genus Torymus (with 191 described Palaearctic species), viz., T. fuscicornis (Walker, 1833) and T. nitidulus (Walker, 1833), were earlier assigned to Lioterphus Thomson, 1876 – L. fuscicornis and L. pallidicornis Boheman, 1834, respectively – a genus with only two species exclusively attacking Semudobia gall midges. The pteromalid genus Psilonotus contains three species in the Palaearctic, viz., P. adamas Walker, 1834, P. achaeus Walker, 1848 and P. hortensia Walker, 1846, all species being specialised on Semudobia. Finally, three eulophid parasitoids belonging to the large genus Aprostocetus (with 258 Palaearctic species), viz., A. clavicornis (Zetterstedt, 1838), A. pallipes (Dalman, 1820) and A. constrictus Graham, 1987, are exclusively known as Palaearctic parasitoids of Semudobia.

Hodges (1969) was first in analyzing the food web in female birch catkin galls and treating the life-history of the parasitoids. Because the present differentiation into several species of the gall inducing host Semudobia was not known in those days, she was unable to determine the precise food web associations between gall midge hosts and parasitoids. Because of (1) the present knowledge of gall inducing midges inhabiting female birch catkins, (2) the occurrence of so many parasitoids in female birch catkins, (3) the conclusions of highly specialised associations in the earlier studies on inquiline gall midges and platygastrids in female birch catkins, and, last but not least (4) the many examples of other highly specialised associations given in, e.g., Redfern (2011), it became intriguing to further explore host-parasitoid associations in such a small arena represented by a birch catkin: can we explain the occurrence of so many parasitoid species exclusively specialised on birch female catkins as a consequence of differentiation of niches presented by host gall midges, c.q. of host speciation?

Materials and methods

If gall inducing midge characteristics are the primary cue in explaining the occurrence of the parasitoids, galls caused by Semudobia betulae, S. tarda and S. skuhravae have to be sorted in order to discriminate the substrates of the parasitoids involved. The galls caused by the different Semudobia species are morphologically distinct (Roskam 1977).

Nine samples were collected in the central part of The Netherlands, N 52.13 E 5.32, alt. 10 m, December 2011; and 12 samples in Germany, Winterberg, Hoch Sauerland Kreis (HSK), N 51.11 E 8.31, alt. 760 m, January 2012. All samples, each containing ten birch fruit catkins, of Dutch and of German origin were from Betula pubescens in moderately dry habitat, the Dutch and German localities mainly differing in altitude. The catkins were dissected and galls were sorted for the three gall makers according to characters in the identification key to galls. Galls were first stored for about one month in a refrigerator at a temperature of 4°C, allowing the insects to pass diapause. Then they were kept at room temperature, except the samples used for the determination of phenology. The latter were kept outdoors in Leiden, The Netherlands, with a temperature/humidity regime similar to that of the locality where they were taken.

Despite the high numbers of galls, the numbers of emerged parasitoids were relatively low; therefore also data were used from a rearing experiment during December 1971. In those days, S. tarda, as well as S. skuhravae, were still undescribed, but it was already apparent that galls in bracts and in fruits were caused by different Semudobia midges. For this experiment bract and fruit galls of 100 fruit catkins, all from western Netherlands localities, were reared separately at room temperature.

For analysis of larval characters the larvae were macerated in warm lactic acid (80%, 80°C), body content was removed and skins were mounted in polyvinyl-lactophenol on microscopic slides. Measurements of larvae were taken from material on microscopic slides using an ocular measuring reticule. Phase-contrast microscopy was used to study low contrast structures like larval sensilla. Descriptions and keys for galls, adult parasitoids and their fully grown larvae are given below. Results of rearings and dissections are presented in the sections on morphology and host-parasitoid associations.

The number of specimens examined in the descriptions are given in Tables 1–3. The terminology follows Roskam (1982); for the description of platygastrid larvae see Roskam (1986).

Identification keys

Key to galls

  1. 1. Malformation of fruit, ovary swollen and content aborted .................. 2
  2. Gall restricted to the slightly thickened base of the fruit scales, which are firmly connected with the spindle of the catkin .................. Semudobia skuhravae Roskam
  3. 2. Fruit more or less egg-shaped, swollen, dull, more or less pubescent; wings distinctly smaller than those of healthy fruits, but usually distinctly developed; exit hole distinct, still closed by a membrane or window .................. Semudobia betulae (Winnertz)
  4. Fruit globularly swollen, glossy, glabrous; wings often almost completely reduced; exit hole present but visible as an indistinctly translucent ‘weak spot’ on gall surface .................. Semudobia tarda Roskam

Galls may be strongly flattened due to feeding activities of inquiline gall midges Dasineura interbracta, Roskam, 1979 and D. fastidioda Roskam, 1979, which larvae may be present on the outside of the gall. Moreover, larvae of the phytosaprophagous gall midge Clinodiplosis cilicrus (Kieffer, 1889) and of the predaceous gall midge Lestodiplosis vorax (Rübsaamen, 1892) may often live on the fruit scales (Roskam 1979).

Key to adults, reared material

  1. 1. Insect wasp-like, two pairs of wings, antennae elbowed and abdomen constricted differentiating a propodeum and gaster .................. 2
  2. Insect midge-like, only one pair of wings, antennae straight and abdomen not constricted but conspicuously red-orange coloured .................. Gall midge host Semudobia For morphological and biological details see Roskam (1977).
  3. 2. Parasitoid wasp minute, less than 2 mm long, glossy black; wing venation absent or with medial vein (but no marginal vein) .................. Platygastrid endoparasitoid Sclerotised wing venation is absent from Platygaster; basal, medial; and subcostal veins are distinct in Metaclisis phragmitis Debauche, 1947. The latter species is occasionally present in birch catkin galls but was not encountered during this study. For morphological and biological details see Roskam (1986).
  4. Parasitoid wasp larger, longer than 2 mm; wing venation reduced, but always with distinct marginal vein .................. 3
  5. 3. Parasitoid glossy, bright green metallic; tarsi five-segmented, antennae at least 11-segmented .................. 6
  6. Parasitoid black but with slight blue metallic shine and some yellow marks on head and thorax; tarsi four-segmented, antennae each with at most nine distinct segments, postmarginal vein reduced. Eulophidae .................. Aprostocetus – 4
  7. 4. Gaster in females oblong, at least three times as long as wide; antennae in males without conspicuous long, sturdy bristles .................. 5
  8. Gaster in females ovoid, about 1.5 times as long as wide; antennae in male with conspicuous long, sturdy bristles .................. A. pallipes (Dalman) (Graham 1987: 332)
  9. 5. Lateral aspect of thorax in both sexes rather globular, anterior part of pronotum steeply declining towards head .................. A. constrictus Graham (Graham 1987: 304)
  10. Lateral aspect of thorax in both sexes rather slender and triangular, anterior part of pronotum ± gradually declining towards head .................. A. clavicornis (Zetterstedt) (Graham 1987: 257)
  11. 6. Mesopleuron in female always impressed; mesoscutum with parapsidal grooves complete or merely anteriorly indicated, immobile against scutellum .................. 7
  12. Mesopleuron in females convex, not impressed; scuto-scutellar suture in female straight, allowing movement of dorsal sclerites; antenna with only one ring segment and seven funicular segments; male with parapsidal grooves deep and pleuron shallowly impressed .................. Eupelmidae, Eupelmus urozonus Dalman
  13. 7. Hind coxa usually at least three times larger than front coxa; pronotum large and rounded; parapsidal grooves complete; gaster ovate and ovipositor prominent, long .................. Torymidae, Torymus – 8
  14. Hind coxa only little larger than front coxa; pronotum small, rounded or carinate; gaster elongate and either ovoid or laterally compressed; ovipositor largely hidden .................. Pteromalidae, Psilonotus – 9
  15. 8. Head, thorax and gaster bright green metallic; legs excepting coxae, fifth tarsal segments and hind femora pale yellow. Antennae in female with frontal part of scape bright yellow; antennae in male completely bright yellow .................. T. nitidulus (Walker) (Walker 1833: 138 [Callimome]; Grissell 1976: 58)
  16. Head, thorax and gaster bluish-green metallic; legs excepting coxae, fifth tarsal segments and all femora fuscous yellow. Antennae in female metallic brown; antennae in male completely brown, sometimes with very narrow frontal lighter stripe on scape .................. T. fuscicornis (Walker) (Walker 1833: 138 [Callimome])
  17. 9. Both sexes: antennae inserted below level of ventral edge of eyes; pronotum either carinate or rounded; scutellum distinctly flattened. Gaster in females oblong, distinctly compressed bilaterally .................. 10
  18. Antennae in both sexes inserted above level of ventral edge of eyes; pronotum always carinate; scutellum moderately convex, slightly longer than broad. Gaster in females ovoid, not compressed bilaterally .................. P. hortensia Walker (Graham 1969: 628)
  19. 10. Antennae with combined length of pedicellus and flagellum slightly longer than breadth of head with all funicle segments subquadrate; scutellum weakly convex, as broad as long. Pronotum short, carinate, steeply declining towards head. Propodeum rather dull, plicae complete .................. P. achaeus Walker (Graham 1969: 627)
  20. Antenna with combined length of pedicellus and flagellum shorter than breadth of head; distal segments of funicle strongly transverse. Pronotum longer, dorso-ventrally flattened, the collar longer medially, not distinctly margined in front, but almost rounded off into the pronotal neck, which does not slope ventrally. Propodeum shiny, plicae incomplete or absent .................. P. adamas Walker (Graham 1969: 627)

Key to immature stages present inside gall

  1. 1. Larva cream-coloured, pale yellowish or whitish. Biting mouth parts distinct, dark brown coloured .................. Chalcidoid parasitoid – 2
  2. Larva bright orange-red coloured; sclerotised plate, so called spatula sternalis, on ventral side of first thoracic segment. Mouth parts inconspicuous .................. Gall midge host Semudobia Gall midge larvae may be inert and show black punctures due to host feeding usually of adult parasitoids of Psilonotus.
  3. = Gall contains black parasitoid enveloped by gall midge larval skin .................. Platygastrid endoparasitoid Host larval skin is discoloured, enclosing Platygaster wasps; very occasionally orange tinted host skins enclosing Metaclisis phragmitis Debauche may be found (Roskam 1986). The latter species was not encountered during this study. Platygastrids develop in autumn into inert adults which overwinter in the gall in diapause and become active and emerge in following spring. For morphological and biological details, see Roskam (1986).
  4. 2. Body surface glabrous, lacking conspicuous bristles (setae) .................. 5
  5. Conspicuous bristles present on head as well as on each body segment .................. 3
  6. 3. Head with ‘nose’, median sclerotic brown conical elevation. Clypeus indistinct, not sclerotic .................. Torymidae, Torymus – 4
  7. Median conical elevation on head absent; clypeus conspicuous and comb-like due to a row of teeth (Fig. 18) .................. Eupelmidae, Eupelmus urozonus Dalman Occasional polyphagous ectoparasitoid, during this study only once collected as larva.
  8. 4. Nose accompanied by a lateral pair of conspicuously sclerotic plates each with three blunt-conical elevations (Fig. 6) .................. T. fuscicornis (Walker)
  9. Pair lateral plates weakly sclerotised and usually indistinct .................. T. nitidulus (Walker)
  10. 5. Antennae protruding, situated on blunt bell-shaped elevations. All sensilla, excepting some in mouth region, bear minute setae. Mandibles triangular, lacking sclerotised ventral plate in flattened condition (Fig. 11) .................. Pteromalidae, Psilonotus spec. Further identification on qualitative characters to species level not possible.
  11. Antennae not protruding, flattened bell-shaped pedestal bearing antennae absent. Body sensilla without minute setae. Mandibles, if flattened, with conspicuous ventral plate. (Figs 16–17) .................. Eulophidae – Aprostocetus spec. Further identification on qualitative characters to species level only partially possible, see remark under descriptions of larvae.
Figs 1–6.
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.

Citation: Tijdschrift voor Entomologie 156, 1 (2013) ; 10.1163/22119434-00002020

Description of fully grown chalcidoid parasitoid larvae

Torymus Dalman, 1920 Head (Figs 1–6)

Cranium (Figs 4, 6). The torymid larvae associated with Semudobia are distinguished by a conspicuous conical medio-frontal sclerotic protruding, ‘nose’. Antennae simple and usually well developed. Origin of frontal muscle indicated in cranial wall (dfm, Short 1952, 1959). Demarcation of clypeus indistinct. Anterior tentorial pits (at) distinct, situated ventrally of antennae. Seven pairs of long setae, viz., two pairs of superior frontal setae (Fs), two pairs of inferior frontal setae (Fi), two pairs of genal setae (Ge), situated laterally to antennae and anterior tentorial pits. Two pairs of setae of intermediate length are inserted, respectively, on dorsal and ventral blunt-conical sclerotised elevations, leaving the submedian elevations without setae. Elevations are well sclerotised in T. fuscicornis, less distinct or absent in T. nitidulus. One pair of short setae on labrum, accompanied by five pairs of sensilla.

Under-lip complex (Fig. 6, ul). This complex consists of the united hypopharynx, maxillae and labium. Although the demarcation of membranes is usually indistinct, regions can be distinguished by presence of particular setae and sensilla. Three pairs of maxillary sensilla (max se), the most ventrally ones compound. Four pairs of lateral prelabial sensilla, one pair of short median prelabial setae and one pair of short postlabial setae.

Tentorium. Mandibles triangular, well sclerotised, one-toothed, articulating with anterior and posterior processes of pleurostomae. Epistomal bridge usually weakly sclerotised, often indistinct.

Body (Figs 1–3, 5, Table 1)

[Distribution of sizes of head and body segments is expected to be binominal due to size difference between larger females and smaller males.]

Segmentation. As in all chalcidoids, body consists of thirteen segments, viz., three thoracic (Th 1–3) and ten abdominal segments, the ultimate of which is the anal segment (A 1–9, AS, respectively). Respiration peripneustic; spiracles absent from Th 1, A8 and 9, and AS.

Setae and sensilla. Proximally five paired rows of setae of large to medium length dorsally situated to spiracles on spiraculate thoracic and abdominal segments, three to four rows of medium to short length ventrally situated to spiracles, not arranged in a definite pattern. Sensilla in dorsal, pleural and ventral areas absent. Anal segment (Fig. 5) with two pairs of short setae dorsal to anal slit, and two pairs ventrally.

Table 1.

Torymus, 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.

Table 1.
Figs 7–11.
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.

Citation: Tijdschrift voor Entomologie 156, 1 (2013) ; 10.1163/22119434-00002020

Psilonotus Walker, 1834

No qualitative differences could be detected between P. adamas and P. achaeus; size of spiracles of P. hortensia, especially on A7, may exceed those of the other two species.

Head

Cranium (Fig. 11). Antennae situated on distinct semiglobose elevations. Antennae simple, blunt conical, well developed. Origin of frontal muscle indicated in cranial wall (dfm, Short 1952). Demarcation of clypeus usually distinct. Anterior tentorial pits (at) distinct, situated ventrally to antennae. Sensilla usually with very short setae; viz., one pair of superior frontal setae (Fs) situated above antennae, one pair of inferior frontal setae (Fi) situated medially to antennae, one pair of genal setae (Ge), situated laterally to epistomal arch; hypostomal setae absent. Two pairs of short setae on labrum. One pair of sensilla on labrum situated between the labral setae.

Under-lip complex (Fig. 11). Four pairs of lateral prelabial sensilla (prls) are present, two pairs with setae; three pairs of median prelabial sensilla (prms), two pairs setose and one pair of postlabial setose sensilla (pos).

Tentorium. Mandibles triangular, well sclerotised, one-toothed, articulate with anterior and posterior processes of pleurostomae. Epistomal bridge usually weakly sclerotised.

Body (Figs 8–10, Table 2)

[Distribution of sizes of head and body segments, segmentation and arrangement of spiracles see Torymus.]

Sensilla. All abdominal segments with one pair of dorsal sensilla, one pair of pleural sensilla. First thoracic segment and ninth abdominal segment with one pair of ventral sensilla. Anal segment (Fig. 7) with two pairs of sensilla dorsally of anal slit, and one pair ventrally. All sensilla bear short setae.

Table 2.

Psilonotus, characters of mature larvae, measurements in μm, N = 10 per cohort, P. hortensia excepted, N = 1. a, abdominal segment; as, anal segment; th, thoracic segment, Ø sp, diameter of spiracle.

Table 2.

Aprostocetus Westwood, 1822 Head

Cranium (Fig. 17). Distinguished by all sensilla lacking distinct setae (Aprostocetus clavicornis, A. constrictus) or minute setae (A. pallipes). Antennae simple, blunt conical, well developed. Origin of frontal muscle indicated in cranial wall invisible, as well as anterior tentorial pits. Demarcation of clypeus usually distinct, not sclerotised. Superior frontal sensilla (Fs) absent, one pair of inferior frontal sensilla (Fi) situated medially of antennae present, three pairs of genal setae (Ge), situated laterally to epistomal arch, hypostomal sensilla absent, two pairs of sensilla on labrum, the lateral pair often accompanied by a darker sensilla-like structure.

Figs 12–17.
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.

Citation: Tijdschrift voor Entomologie 156, 1 (2013) ; 10.1163/22119434-00002020

Under-lip complex (Figs 16–17). Three pairs of maxillary sensilla (max se) are present, one pair large, the other two pairs small and often distinct; two pairs of prelabial sensilla (prl se), one pair large, one pair small and often indistinct.

Tentorium. Mandibles pointed with large distal plate, visible in ventral aspect, well sclerotised, one-toothed, articulate with anterior and posterior processes of pleurostomae. Epistomal bridge not visible.

Body (Figs 13–15, Table 2)

[Distribution of sizes of head and body segments, segmentation and spiracular arrangement, see Torymus.]

Sensilla. Abdominal segments, seventh excepted, with one pair of dorsal sensilla, all abdominal segments with one pair of pleural sensilla. First thoracic segment and ninth abdominal segment with one pair of ventral sensilla. Anal segment (Fig. 12) with two pairs of sensilla dorsally of anal slit, and one pair ventrally.

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.

Table 3.

Eupelmus urozonus Dalman, 1920

[Only one larva collected, ectoparasitic on Semudobia skuhravae on Betula pubescens, Figs 18–20.]

Figs 18–20.
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.

Citation: Tijdschrift voor Entomologie 156, 1 (2013) ; 10.1163/22119434-00002020

Head

Mouth region (Fig. 18). Eupelmus urozonus larvae are distinct by a conspicuously sclerotised six-toothed clypeus with 5 other teeth situated ventral to the stoma. Setae on head as well as on body long, flexible and long tapering. One pair of setae of intermediate length on labrum.

Under-lip complex. Three pairs of maxillary sensilla (max se) are present, one pair of prelabial sensilla (prl se), one pair of postlabial sensilla (pol se).

Tentorium. Mandibles triangular, well sclerotised, one-toothed, articulate with anterior and posterior processes of pleurostomae. Epistomal bridge weakly sclerotised, indistinct.

Body

Segmentation and spiracular arrangement, see Torymus.

Setae and sensilla. Two rows of setae situated dorsally to spiracles, one pair in pleural region close to spiracles and two rows situated ventrally to spiracles. All setae long and gradually tapering. Sensilla in dorsal, pleural and in ventral areas absent. Anal segment with two pairs of short setae dorsal to anal slit, and four pairs ventrally of medium length.

Measurements (in μm, n = 1)

Length of body 1500, width of body 980; width head 430, width anal segment 220 μm.

Diameter spiracles on A2 29, on Th1 24, on A7 24 μm.

Length of frontal setae 200, of pleural setae (nearest to spiracle) on Th2 245, on A1 185, on A7 95 and on AS 30 μm.

Host-parasitoid associations

Results of samples reared during 2011 and 2012 in The Netherlands (NL) and in Germany, Hoch Sauerland Kreis (HSK) are presented in Table 4; those collected in December 1971, only Dutch samples, in Table 5.

Table 4.

Host parasitoid associations, determined from reared insects during the year 2012. NL, The Netherlands; HSK, Germany, Hoch Sauerland Kreis.

Table 4.
Table 5.

Rearing results of chalcidoid parasitoids, separated for bract- and fruit galls during December 1971.

Table 5.

Although it is rather difficult to pass diapause under artificial conditions of a refrigerator and mortality is considerable therefore, midges as well as parasitoids emerged in substantial numbers, ranging from 9.5 up to 37.8% of the reared galls. Parasitism varied from 6.8 up to 68.6%. Remarkable were the large numbers of S. skuhravae, especially in the HSK samples: in Roskam (1977) this species, although numbers per locality differed substantially, was often less abundant. Numbers of collected galls as well as of reared insects do not allow drawing conclusions about differences between NL and HSK. Chance may explain the absence of a particular species in a particular locality.

Associations between gall midges and platygastrid egg-larval parasitoids are analysed in Roskam (1986). Remarkable host specificity was found in that study, indicating Platygaster betularia preferred S. skuhravae, and only S. betulae of the fruit galling midges. P. betularia was only infrequently reared from S. tarda. Metaclisis phragmitis was earlier found in Semudobia betulae and S. tarda and was absent from S. skuhravae (Roskam 1986). Absolute host specificity was not found for chalcidoid parasitoids during the present study but distinct preferences were present.

Both Torymus species are ectoparasitoids of immature Semudobia gall midges. Substantial numbers of T. fuscicornis were reared on S. skuhravae, in NL as well as in HSK and on S. betulae in NL. T. nitidulus, on the other hand, was present in substantial numbers only on S. tarda at both localities. Single records, of T. fuscicornis and of T. nitidulus may be due to identification errors by parasitoids or the investigator. It may be concluded that T. fuscicornis preferred S. skuhravae and S. betulae, but not S. tarda, the latter being the preferred host for T. nitidulus.

Three species of Aprostocetus are regular ectoparasitoids of Semudobia, viz., A. clavicornis, constrictus and pallipes. A. clavicornis was reared in substantial numbers on S. tarda at both localities and S. betulae in NL only. A. pallipes and A. constrictus were relatively frequent on S. skuhravae at both localities but absent from the two other gall midge species. Hence a different preference exists, on the one hand of A. clavicornis for seed galling S. betulae and tarda, and on the other of A. pallipes and constrictus for the bract galling S. skuhravae. Apparent ecological differences between A. pallipes and constrictus could not be found.

All three species of Psilonotus are exclusively associated with Semudobia and are ectoparasitoids of mature larvae. Both P. achaeus and P. hortensia were frequently reared from S. skuhravae at both localities; all three species were reared from S. betulae, NL only; and P. achaeus was absent from S. tarda at both localities. P. adamas was rarely reared from S. skuhravae, HSK only; and emerged in low numbers from both fruit galling midges S. betulae and S. tarda, in NL.

The 1971 rearing results corroborate those of 2012 but show stricter host preferences. In Aprostocetus, A. pallipes and only one specimen of A. constrictus emerged from bract galls (caused by Semudobia skuhravae); A. clavicornis was abundant, but only in seed galls (caused by S. betulae and S. tarda). In Psilonotus, P. achaeus was common in bract galls, whereas P. adamas preferred fruit galls and P. hortensia numbers were too low to draw conclusions. Finally, in Torymus the 2012 results were also corroborated: T. nitidulus preferred fruit galls and T. fuscicornis was reared from bract- as well as fruit galls.

Parasitoid-host associations are summarised in Fig. 21. A particular phenomenon must be reported here. Platygastrids usually and chalcidoids belonging to Aprostocetus and Psilonotus always deposit only one egg per host. Both Torymus species, however, lay systematically two eggs per still very small host larva. After hatching of these two eggs one larva first feeds on its sibling allowing the gall midge larva to grow. Only after consuming of its sibling it starts feeding on the gall midge host. This might be an adaptation: in this early phase of parasitisation the host is first allowed to grow before becoming a sufficient resource for complete parasitoid development.

Fig. 21.
Fig. 21.

Parasitoid and inquiline host Semudobia preferences. Data for inquilines are from Roskam, 1979; for egg-larval parasitoids from Roskam, 1986. All arrows indicate regular associations, the incidental ones are, for sake of clarity, not given.

Citation: Tijdschrift voor Entomologie 156, 1 (2013) ; 10.1163/22119434-00002020

Phenology

Figure 22 summarises results of Semudobia galls reared under natural outdoor conditions, combined with records of specimens swept from birch. As expected, emerging of gall midges overlaps completely that of platygastrid egg parasitoids. Aprostocetus and Psilonotus emerged simultaneously after the flight period of Semudobia during the new generation second and third instar larvae, whereas early emergence of Torymus wasps overlaps with emergence of midges as well as of platygastrid parasitoids; and late emerging wasps are partially simultaneous with Aprostocetus and Psilonotus, indicating attacking of first and second instars of host larvae – for host phenology, see Roskam (1977, Table 4). The emergence of T. nitidulus reflects the association with S. tarda, being the latest of the host species. As is indicated in Fig. 22, adults of Aprostocetus and Psilonotus are still active at the end of October. The large time-span, end of May until the end of October, in which the adults of Aprostocetus and Psilonotus occur may suggest a multivoltine life style with overlapping generations, in contrast with a univoltine life style of Platygaster and Torymus.

Fig. 22.
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.

Citation: Tijdschrift voor Entomologie 156, 1 (2013) ; 10.1163/22119434-00002020

Patterns of co-speciation

Phylogeny of gall midge Semudobia and co-speciation pattern with host plant Betula was hypothesised in Roskam (1979): the fruit gall inducing S. betulae, together with its Nearctic geographic vicariants S. brevipalpis and S. steenisii, are considered as a sister group of S. tarda; all fruit galling midges in their turn are considered as a sister group of circumboreal S. skuhravae, which induces galls in bracts of fruit catkins.

Of Platygaster egg parasitoids only two representatives are associated with three Semudobia host species, viz., P. betularia Kieffer, 1916 is strictly associated with S. skuhravae, as well as S. betulae, whereas P. betulae (Kieffer, 1916) was only found in S. tarda (Roskam, 1986). Both Platygaster species belong to a large genus of mainly gall midge parasitoids. Because P. betularia is associated with two gall midge hosts, viz., S. skuhravae and S. betulae which are not sister species, we must conclude an independent colonisation of, at one hand P. betularia on S. skuhravae and S. betulae, and, on the other hand, of P. betulae of S. tarda. Metaclisis phragmitis Debauche, 1947, rarely found in birch catkins and not in this study, only emerged from fruit galls caused by Semudobia betulae and S. tarda. Because its adults appeared relatively late, its absence from the early emerging S. skuhravae was suggested to be a mismatch between parasitoid and host phenology (Roskam 1986).

Torymus larval ectoparasitoids are, like Platygaster, represented by only two species. Although both species belong to the large torymid genus Torymus, they were earlier assigned to Lioterphus Thomson, exclusively associated with Semudobia. It is therefore acceptable to regard them as sister species, with the specialisation on Semudobia as a synapomorphy. The reduced sclerotic frontal elevations in larvae and the conspicuous yellow coloured antennae in males as well as the more abundant yellow marks all over body and legs in both sexes might be considered as autapomorphies for T. nitidulus. This corroborates the speciation pattern in Semudobia, because T. nitidulus, with a number of autapomorphies is associated with S. tarda, the midge species with most apomorphies of the hosts, whereas T. fuscicornis is associated with both other Semudobia midges.

Aprostocetus is a large genus of Eulophidae and is represented with three species in the Palaearctic birch catkins biocoenosis. A. pallipes is similar to the usual eulophid habitus having an ovoid gaster. A. constrictus and A. clavicornis share elongate female gasters. The rigid antennal bristles in A. pallipes males could be considered as an apomorphy; the setose larval papillae and female ovoid gaster, however, as a plesiomorphic state. The elongate gaster is shared with other species assigned to Aprostocetus which parasitize other gall midges (Graham 1987). Hence, within the birch catkin system associations of all three Aprostocetus species should be regarded as independent colonisations. It is peculiar that A. pallipes with plesiomorphic character states, viz., the ovoid female gaster of and setose larval sensilla is delimited to S. skuhravae, the midge which is hypothesised as basal in the midge phylogeny. A. clavicornis is specialised on both seed galling midges, whereas A. constrictus and A. clavicornis are both well adapted to ovipositing in the birch catkin by their elongated female gaster.

Representatives of the small pteromalid genus Psilonotus are exclusively associated with Semudobia. Psilonotus adamas has a rounded pronotum. Closest relative is P. achaeus, sharing on the one hand the apomorphic bilaterally compressed female gaster, an adaptation to ovipositing in the birch catkin, as well as the flattened head and lower placed antennae, but sharing on the other hand a carinate pronotum with P. hortensia, considered as plesiomorhic, which prefers as host S. skuhravae, with also plesiomorphic traits. Basal in the Psilonotus phylogeny is P. hortensia, lacking any Semudobia host preference in Palaearctic birch catkins. A possible scenario here might be an early colonisation by P. hortensia, which allowed the already existing association between Semudobia and Psilonotus to better exploit the seed galling Semudobia species by favouring wriggling between catkin scales, necessary to lay eggs. Nevertheless, specialist P. achaeus and P. adamas did not outcompete generalist P. hortensia, which is still a frequent parasitoid.

Discussion

Morphology

Gall midge host Semudobia species are distinct by their galls, as well as adult and larval morphology. In parasitoids, adults are distinct, but larvae could mainly be discriminated between genera. Within genera only a few larval characters allowed discrimination between species. Hence, differentiation of immature host stages is more distinct than that of parasitoids.

Chalcidoid parasitoids have several adaptations which favour especially the laying of eggs in compact inflorescences like fruit catkins of birch. Aprostocetus clavicornis and A. constrictus, for example, have elongate female gasters which allow them to wriggle better between the catkin scales to reach the midge galls.

Torymus fuscicornis and T. nitidulus have, like many Torymidae, long ovipositors which allow them to drill into hidden galls. T. fuscicornis and T. nitidulus differ mainly by the colour of the male antennae: metallic green in T. fuscicornis and bright yellow in T. nitidulus. This difference may have evolved during an episode of allopatry, an episode also hypothesised for Semudobia (Roskam, 1979). The difference became functional after secondary sympatry, avoiding hybridisation: during courtship females are able to recognize the right mates. Although Grissell (1976) placed Lioterphus in synonymy, there may be arguments to maintain it as an independent genus. The size of adults in both species is significantly smaller than that of species which belong to Torymus. Both species exclusively develop in female birch catkins. The larval character of a ‘sclerotised nose’ could well be an autapomorphy validating Lioterphus. A nose is present in Torymus but is all white like the rest of the face (Askew, in litt.). However, more study of Torymus larvae is needed before making taxonomic changes.

In Psilonotus apparently a trend evolved from a normal pteromalid body shape into a flattened one. The body shape in P. hortensia still matches the shape of related genera like Mesopolobus Westwood, 1833: a relatively globular head, a high thorax and an ovoid female gaster. The head (proximally-distally), thorax (dorsal-ventrally) and female gaster (bilaterally) of P. achaeus and P. adamas are distinctly flattened, again an adaptation allowing the females to wriggle better between the catkin scales. These traits are considered as a synapomorphy of the latter two (sister-) species. A rounded pronotum of P. adamas – carinate in P. achaeus and P. hortensia – is a further (autapomorphic) trait facilitating wriggling into birch fruit catkins.

Phenology and association

All four parasitoid genera are specialised on different developmental stages of their hosts. Only the egg-larval platygastrid parasitoids have an endoparasitic life style. The results of reared Semudobia parasitoids, especially during the 2012 experiment, may endorse Askew & Shaw (1986). These authors stipulated that late parasitoids – idiobionts in their terminology – are expected to be less fastidious than parasitoids of early host stages – koinobionts in their terminology – because synchronisation of koinobiont endo- as well as ectoparasitoids is more critical and the resources for idiobiont ectoparasitoids, already substantially diminished by early koinobiont parasitoids, are less abundant. Platygastrid endoparasitoid Platygaster and chalcidoid ectoparasitoid Torymus are typical koinobionts in terms of specialist host-parasitoid association. Representatives of these two genera have strict associations with their host species, as predicted by Askew & Shaw (1986). Specific associations in Psilonotus are present, but less strict. Also here Askew & Shaw (1986) is endorsed. The particular feeding on siblings in Torymus may be a further specialisation to parasitisation of early developmental phase of the host. The host-feeding habit in Psilonotus females is a particular adaptation to provide proteins for egg production. Host feeding has not been observed in Aprostocetus, but might not be excluded.

Co-speciation patterns

It is unlikely that co-speciation in Betula host plants, Semudobia gall midges and parasitoids is a result of a strict co-evolutionary process in which reciprocal selection pressure shaped parallel traits in host plant-, gall midge- and parasitoid phylogenies. Merely, gall midges passively followed speciation of birches and parasitoids followed speciation of gall midges and/or host plants. Jermy (1976) coined for this less strict co-evolutionary process the concept of sequential evolution in explaining why phylogenies of associates may display congruencies.

Congruent patterns in host and parasite phylogeny could be shown in SemudobiaBetula association (Roskam 1979). Such patterns cannot be expected in parasitoid genera like Platygaster and Aprostocetus with species parasitising various, and unrelated hosts. In Torymus, however, with only two apparently sister species on Semudobia, indeed the species with several (aut)apomorphies, T. nitidulus, is associated with the gall midge with also most (aut)apomorhies, S. tarda. This may be an example of sequential evolution of one parasitoid species which followed gall midge speciation.

In Psilonotus with three species associated with three related hosts sequential evolution might be expected but is not always obvious: P. hortensia with many plesiomorphic traits displays a generalist pattern by parasitising all Semudobia species. P. achaeus and P. adamas have more specialist host preferences and adaptations for ovipositing in birch fruit catkins. P. achaeus sharing apomorphic traits with P. adamas but, on the other hand, sharing a plesiomorphic trait of the pronotum with P. hortensia, prefers bract galling S. skuhravae. P. adamas, showing a further (aut-) apomorphy prefers both fruit galling S. betulae and S. tarda. The differentation between P. adamas and P. achaeus might indeed be explained as an example of sequential evolution paralleling the differentiation of fruit galling midge hosts Semudobia betulae and S. tarda from bract galling S. skuhravae.

Acknowledgements

For their constructive criticism of this manuscript I am indebted to Dr. M. Redfern, Dr. R.R. Askew, Dr. K.M. Harris and some anonymous reviewers. Mr. M.J. Gijswijt identified the Aprostocetus species. Mrs. S. Kofman and Mr. D.M. Hallensleben were most helpful with the preparation of materials. For the loan of specimens in their care I thank Naturalis Biodiversity Center (RMNH), Leiden, The Netherlands.

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Appendix: Data of used materials

Slides of full-grown larvae used for data in Tables 1–3 are deposited in Naturalis Biodiversity Center (RMNH), Leiden, The Netherlands. All materials are collected in The Netherlands.

Torymus fuscicornis on Semudobia betulae, Betula pubescens 771202.09, Voorschoten, Duivenvoorde, Sept. 14, 1977; 800808.01–06, 801103.01, The Hague, Meijendel, Jan. 28, 1980; 820105.01 and 820921.04, The Hague, Meijendel, Sept. 23, 1981.

Torymus nitidulus on Semudobia tarda, Betula pubescens 821201.65 and -70, 821202.67–68, 821208.50, -52, 55–58, Voorschoten, Duivenvoorde, Feb. 9, 1978.

Psilonotus adamas on Semudobia betulae, Betula pubescens 800318.15–16, 800320.04–07, -10, The Hague, Meijendel, Jan. 28, 1980; 800324.01, 820105.02–03, The Hague, Meijendel, Nov. 23, 1981.

Psilonotus adamas on Semudobia tarda, Betula pubescens 791026.05–06, Voorschoten, Duivenvoorde, Mar. 1979; 800318.01, -03, -06–07, The Hague, Meijendel, Jan. 28, 1980; 800807.03, -05–07, The Hague, Meijendel, Apr. 18, 1979.

Psilonotus achaeus on Semudobia skuhravae, Betula pubescens 780615.08, Valkenswaard, Malpie; 800630.09, -13–15, The Hague, Meijendel, Jan. 28, 1980; 800702.34–35, -39–40, The Hague, Meijendel, Apr. 18, 1979; 820111.01, The Hague, Meijendel, Aug. 16, 1981.

Psilonotus hortensia on Semudobia skuhravae, Betula pendula The Hague, Meijendel, Dec. 21, 1972.

Aprostocetus clavicornis on Semudobia betulae, Betula pubescens 810205.53, -59, -61, -63–64, The Hague, Meijendel, Jan. 28, 1980; 820113.01, The Hague, Meijendel, Oct. 29, 1981; 820923.30, The Hague, Meijendel, Feb. 9, 1978; 821011.18, The Hague, Meijendel, Aug. 23, 1981; 821012.07–08, The Hague, Meijendel, Sept. 30, 1982.

Aprostocetus clavicornis on Semudobia tarda, Betula pubescens 771206.22–24, 771208.12, -14–15, Voorschoten, Duivenvoorde, Sept. 14, 1977; 800311.01–04, The Hague, Meijendel, Jan. 28, 1980.

Aprostocetus pallipes/constrictus on Semudobia skuhravae, Betula pubescens 780418.02, 780419.01, -03, -07, -09, 780420.01, Valkenswaard, Malpie, Dec. 20, 1977; 800318.08–10, -12, The Hague, Meijendel, Jan. 28, 1980.

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