Structure of the Principal Groups of Microinsects. VI. Trichogrammatid Wasps (Hymenoptera: Trichogrammatidae)

Abstract

Studies on the morphology of Trichogrammatidae are briefly reviewed. The external and internal morphology of Trichogramma and Megaphragma are described in detail. It is shown that in spite of minute size, external structures of adult Trichogrammatidae remain complex. Such internal structures of these wasps as the intestine and tracheal and circulatory systems are considerably simplified; the number of Malpighian tubules is reduced; some muscles are lost. It is shown that the nervous system of adult M. mymaripenne is almost anucleate, because in more than 95 % of cells of the central nervous system, cell bodies and nuclei undergo lysis at later stages of pupal development.

8.1 Introduction

Trichogrammatids are small insects distributed worldwide; their larvae develop in eggs of other insects. Trichogrammatids of the genus Megaphragma include some of the smallest insects and some of the smallest metazoans. Unique almost anucleate nervous system was recently described in M. mymaripenne (Polilov 2012), making this species especially interesting for studies of miniaturization in insects and miniaturization of the nervous system in animals in general. Since some trichogrammatids are widely used in biological methods of pest control, their biology and taxonomy are intensively studied (Nagarkatti and Nagaraja 1977). Much fewer studies treat the morphology of Trichogrammatidae. The external morphology of adults of many genera has been described in rather much detail (Chumakova 1966; Sorokina 1993; Pinto 2006). A separate large set of studies treats the sensillar armature of Trichogrammatidae (Voegelt et al. 1975; Schmidt and Smith 1985; Olson and Andow 1993; Amornsak et al. 1998; Ruschioni et al. 2012; Zhang et al. 2012). Only one detailed study treats the internal morphology of adult trichogrammatids, the species Trichogramma evanescens (Polilov 2016). Other available publications on the structure of trichogrammatids include studies on the anatomy of different Trichogramma species (Flanders 1937; Chumakova 1968; Boivin 2010) and of Prestwichia aquatica (Ivanova-Kazas 1952), descriptions of the structure of the cerebrum in Megaphragma mymaripenne (Polilov 2012) and Trichogramma evanescens (Makarova and Polilov 2013) and structure of the eyes (Fischer et al. 2011; Makarova et al. 2015), and ultrastructure of spermatozoa (Lino-Neto et al. 2000; Lino-Neto and Dolder 2001). Many studies are available on the development and external and internal morphology of trichogrammatid larvae (Flanders 1937; Ivanova-Kazas 1952, 1954, 1961; Chumakova 1966; Kochetova 1969; Dahlan and Gordh, 1996; Hawlitzky and Boulay 1982; Volkoff et al. 1995; Jarjees et al. 1998; Cônsoli et al. 1999; Wu et al. 2000; Jarjees and Merritt 2002, 2004; Boivin 2010).

Literature on the structure of related groups of Hymenoptera is reviewed in the previous chapter of this book (Chap. 7).

8.2 Brief Description of the Structure of Trichogrammatidae

Small hymenopterans 0.17–2 mm long (usually 0.4–0.8 mm long). Body compact (Fig. 8.1). Coloration monotonous, from yellow to black, without metallic sheen. Integument without complex microsculpture or dense pubescence. Head hypognathous. Compound eyes lateral, consisting of 30–200 ommatidia; number of ocelli 3. In some representatives eyes and ocelli absent. Antennae 5–9-segmented, clavate, attached between eyes. Mesosoma consisting of fused pro-, meso-, metathorax, and abdominal segment 1. Two pairs of wings usually present; hindwings sometimes strongly reduced; in some cases wings absent. Wing venation strongly depleted; perimeter of wings with fringe of long setae. Legs divided into coxa, trochanter, femur, tibia, and tarsus, typical of insects. Trochanter in most representatives of this family 2-segmented. Tarsi 3-segmented. Number of visible segments of metasoma 5–7, because of abdominal segment 1 included in mesosoma, segment 2 forming petiole, and distal segments modified; number of visible tergites and sternites often different in males and females of one species. Petiole usually weakly pronounced. External male genitalia represented by phallobase, bearing parameres, and simple aedeagus. Females with ovipositor, often long, consisting of external and internal sheaths and pair of stylets.

Fig. 8.1

External morphology of Trichogrammatidae, SEM: a, c, e Trichogramma evanescens; b, d, f Megaphragma mymaripenne; a, d dorsal view, b, c lateral view; e, f ventral view

Males and females different in size, proportions, number of visible sclerites of abdomen, number of antennomeres, and armature of antennae and legs. Some species include both winged and and wingless forms.

8.3 Morphology of Adult Trichogrammatidae

8.3.1 External Morphology

Body length of adult 370–420 (M = 390, n = 10) in Trichogramma evanescens, 220–255 (M = 235, n = 10) in Megaphragma mymaripenne. In smallest representative of family, Megaphragma caribea, body length only 170 μm (Delvare 1993).

Structure of head

Head hypognathous (Fig. 8.2). Cranium with only one weakly discernible postoccipital suture and several folds of unclear homology around base of antennae. Hypostome and clypeus not distinguished. Tentorium, as in other chalcidoids, with anterior and posterior arms, dorsal arms reduced. Occipital area with numerous folds; because of these folds, volume of cranium decreasing from pupae to adults.

Fig. 8.2

Structure of head in Trichogramma evanescens, SEM: a dorsal view; b lateral view; c frontal view; d posterior view; a, b male; c, d female; ant antenna, cuf cuticular folds, lb labium, md mandible, mx maxilla, oc eye, ocl ocellus

Compound eyes lateral, consisting of 30–200 ommatidia, much fewer than in most other hymenopterans. Number of ocelli usually 3.

Antennae 5–9-segmented with 1–3-segmented club, consisting of scape, pedicel, anellus, funicle, and club. In males of some species segments of flagellum fused with club. Each antenna of Trichogramma bearing about 260 sensilla of 14 types (Amornsak et al. 1998). Antenna of Megaphragma mymaripenne bearing 38 sensilla of six types: 3 chaetoid on scape; 5 chaetoid on pedicel; 1 chaetoid and 5 trichoid (type 1) on flagellum; 14 trichoid (type 1), 2 trichoid (type 2), and 1 clavate on segment 1 of club; and 2 trichoid (type 1), 4 placoid, and 1 styloconic on segment 2 of club.

Mouthparts of structure typical of chalcidoids, consisting of well developed mandibles, maxillae, and labium (Figs. 8.3 and 8.4). Labrum weakly developed and represented by rather small triangular membranous plate. Mandibles with undulate margin and spines on internal surface. Maxillae connected with labium by membranous septum into labiomaxillary complex. Maxillae consisting of cardo, stipes, fused galea and lacinia, and maxillary palp. Maxillary palp 1-segmented, strongly reduced. Galea bearing large setae and spines, lacinia fused with galea and appearing as brush of setae. Labium consisting of mentum, bearing 1-segmented palps, ligulae, and paraglossae.

Fig. 8.3

Trichogramma evanescens, SEM: a male antennae; b–d mouthparts; b dorsal view; c lateral view; d ventral view; ca cardo, ga galea, lbp labial palp, li ligula, md mandible, mnt mentum, mxp maxillary palp, sti stipes

Fig. 8.4

Structure of head in Megaphragma mymaripenne, SEM: a–c head; a dorsal view; b lateral view; c frontal view; d antennae; e mouthparts, posterior view; f mouthparts, ventral view; ant antenna, ca cardo, cuf cuticular folds, ga galea, lbp labial palp, li ligula, md mandible, mnt mentum, mxp maxillary palp, oc eye, ocl ocellus, sr sensory ridge, sti stipes

Structure of mesosoma

Prothorax narrow, consisting of semicircular pronotum and propectus, formed by sternite and pleurites of prothorax (Fig. 8.5a–c). Anterior part of propectus bearing paired cervical processes; head attached to these processes. Profurca Y-shaped with flattened arms. Pleurite bearing well developed apodeme.

Fig. 8.5

Structure meso- and of metasoma in Trichogramma evanescens, SEM: a–c mesosoma; d metasoma; e leg; f male copulatory apparatus; a dorsal view; b, d, e lateral view; c, f ventral view; aed aedeagus, aest2 mesepisternum, aest3 metepisternum, ax axillary sclerite, cx1.2.3 pro-, meso-, and metacoxae, ep2 mesepimeron, ll scapulae, nt1.3 pro- and metanotum, par parameres, pl1 propleurite, pre prepectus, pro propodeum, sc scutum, scl scutellum, st1 prosternite, ter tergite

Mesothorax more developed than other segments of metasoma (Figs. 8.5a–c and 8.6a–c). Mesonotum consisting of two parts, divided by scuto-scutellar suture. Anterior part divided by longitudinal parapsidal striae into scutum and scapulae. Posterior part divided into scutellum and axillary sclerites. Lateral part of mesothorax divided into episternum and epimeron by weakly discernible suture. Prepectus (secondary formation found in all chalcidoids) present in Trichogrammatidae between pro- and mesothorax. Mesofurca typical of Chalcidoidea, lateral arms well developed. Posterior margin of mesonotum forming mesophargma reaching middle of abdomen (Trichogramma) or almost reaching apex of abdomen (Megaphragma). The part of the mesophragma reaching into the metasoma is termed as postphragma by some authors (Sorokina 1993). Pair of spiracles present between pro- and mesothorax.

Fig. 8.6

Structure of meso- and of metasoma in Megaphragma, SEM: a–f, h M. mymaripenne; g M. amalphitanum; a–c mesosoma; d apex tarsi; e–g metasoma; h wing setae; a, h dorsal view; b, d ventral view; c, d, f, g lateral view; aed aedeagus, aest2 mesepisternum, aest3 metepisternum, aro arolium, ax axillary sclerite, cl claw, cx1.2.3 pro-, meso-, and metacoxae, ep2 mesepimeron, exv external valves of ovipositor, inv internal valves of ovipositor, ll scapulae, nt1.3 pro- and metanotum, par parameres, pl1 pleurite of prothorax, pre prepectus, pro propodeum, prp propectus, sc scutum, scl scutellum, sp spiracle, stl stylet of ovipositor, ter tergite, wi wing

Metathorax represented by narrow semicircle of metanotum; other sclerites of metathorax fused with abdominal segment 1, forming propodeum. Propodeum bearing pair of abdominal spiracles. Metepisterna separated from propodeum by weakly pronounced suture. Epimera fused with propodeum. Pleural apodeme well developed, shaped as high longitudinal ridge with flattened top. Metafurca represented by two short, widely set arms (Trichogramma) or absent (Megaphragma).

Wings with strongly depleted venation (Fig. 8.7). In some representatives wings reduced or absent. Three veins preserved in forewing: submarginal (Pinto 2006: subcostal and premarginal), marginal, and stigmal (Sorokina 1993: radial), usually fused into one arch near anterior wing margin. These veins formed by fusion of subcostal and radius; homology of particular parts is discussed in earlier studies (Burks 1938; Brandley 1955). Hindwings narrower than forewing. In contrast to other chalcidoids, postmarginal, medial, and cubital veins and parastigma absent. Forewings of Trichogramma rather wide, covered with small hairs, with longer hairs forming fringe on perimeter of wing. Hindwings of Trichogramma bearing fringe of long setae along posterior margin. Hindwing with only one short vein of unknown homology. Forewings of Megaphragma represented by narrow wing blade with fringe of long setae on perimeter.

Fig. 8.7

Wings of Trichogrammatidae: a, b Trichogramma evanescens; c, d Megaphragma mymaripenne; a, c forewing, b, d hindwing

Legs slender, ambulatorial, consisting of coxa, 1–2-segmented trochanter, femur, tibia, and 3-segmented tarsus. Tibiae of legs apically bearing well developed, often branched spurs. Apical tarsomere bearing two claws and well developed arolium.

Structure of metasoma

Abdomen in Trichogrammatidae 10-segmented, as in other hymenopterans. Segment 1 included in propodeum, segment 1 forming petiole, distal segments usually modified and sunk into metasoma. In trichogrammatids petiole not pronounced, mesosoma and metasoma broadly joined. Metasoma consisting of six of seven visible tergites and six visible sternites (Trichogramma), or sternites weakly discernible (Megaphragma) (Figs. 8.5d and 8.6e–g).

Ovipositor consisting of outer ovipositor plates (derivates of tergite 9), inner ovipositor plates (Val3), sheath (fused Val2), and stylets (Val1). Spermatheca rather small, rounded or pear-shaped.

External male genitalia represented by simple aedeagus, phallobase, and parameres.

8.3.2 Internal Morphology

General plan of internal structure: most of head occupied by supraoesophageal and suboesophageal ganglia; considerable part of metasoma occupied by musculature; very large muscle (IIdlm1) occupying much of meso- and metasoma; reproductive system occupying most of metasoma (Figs. 8.8 and 8.9).

Fig. 8.8

Internal morphology of Trichogramma evanescens, 3D: a lateral internal view; b lateral external view; c dorsal view; d ventral view; cer cerebrum, gg1.2.3 pro-, meso-, and metathoracic ganglia, exv external valves of ovipositor, fr2 mesophragma; mg midgut, mt Malpighian tubules, ova ovary, rc rectum, soeg suboesophageal ganglion, stl stylet of ovipositor. Colors: blue cuticle, green digestive system, yellow central nervous system, brown musculature, purple reproductive system. Musculature see text

Fig. 8.9

Internal morphology of Megaphragma mymaripenne, 3D: a lateral internal view; b lateral external view; c dorsal view; d ventral view; acg acid gland, ag abdominal ganglion, cer cerebrum, cx1.2 meso- and metacoxae, exv external valves of ovipositor, gg1.2.3 pro-, meso-, and metathoracic ganglia, fr2 mesophragma; mg midgut, mt Malpighian tubules, oc eye, oes oesophagus, ova ovary, rc rectum, soeg suboesophageal ganglion, stl stylet of ovipositor. Colors: blue cuticle, green digestive system, yellow central nervous system, brown musculature, purple reproductive system. Musculature see text

Integument

Integument consisting of cuticle, hypoderm, and basal membrane. Cuticle thickness 0.8–3 μm (M = 1.7, n = 80) in Trichogramma, 0.7–2.4 (M = 1.2, n = 80) in Megaphragma. Cuticle consisting of epicuticle and procuticle. Procuticle homogeneous (Fig. 8.10a–c). Hypoderm represented by strongly flattened cells up to 1.5 μm thick. Many areas of hypoderm, especially in head, with numerous electron transparent vacuoles.

Fig. 8.10

Ultrastructure of Megaphragma mymaripenne, TEM, cross-sections: a, b integument, head, c musculature and fat body, head; d ovary, e midgut, f attachment site of muscles to cuticle, head; cut cuticle, fbc cell of fat body, mf muscle fiber, mit mitochondrion, mv microfibers, nu nucleus, vac vacuole

Digestive and excretory systems

Digestive system complying with general plan typical of insects. Digestive canal divided into fore-, mid-, and hindgut (Figs. 8.11a, b and 8.12a, b). Fore- and hindgut with thin cuticular lining. Midgut without cuticular lining. Intestinal canal somewhat longer than body, forming loop in metasoma. Digestive glands not found.

Fig. 8.11

Internal morphology of Trichogramma evanescens, 3D: a, b intestine and Malpighian tubules; c, d central nervous system; a, c dorsal view; b, d lateral view; ag abdominal ganglion, cer cerebrum, cr crop, gg1.2.3 pro-, meso-, and metathoracic ganglia, hg hindgut, mg midgut, mt Malpighian tubules, oes oesophagus, rc rectum, soeg suboesophageal ganglion

Fig. 8.12

Internal morphology of Megaphragma mymaripenne, 3D: a, b intestine and Malpighian tubules; c, d central nervous system; a, c dorsal view; b, d lateral view; ag abdominal ganglion, cer cerebrum, gg1.2.3 pro-, meso-, and metathoracic ganglia, mg midgut, mt Malpighian tubules, oes oesophagus, rc rectum, soeg suboesophageal ganglion

Foregut divided into pharynx, oesophagus, and crop. Oesophagus straight, running through entire thorax. Muscles of oesophagus absent. Crop situated in metasoma.

Midgut short, wide. Walls of midgut formed by strongly flattened cells. Muscles of midgut not found, distinguishing trichogrammatids from other chalcidoids; layer of circular muscles present. Peritrophic membrane not found.

Hindgut short, divided into small intestine and rectum.

Boundary between mid- and hindgut bearing three Malpighian tubules, shaped as short tubes.

Circulatory system and fat body

Circulatory system strongly reduced. Heart and blood vessels absent, probably because of diffusion sufficing for transport of molecules in organisms of such small sizes. Fat body occupying almost all cavities between organs in metasoma and to a smaller degree in mesosoma.

Tracheal system

Tracheal system strongly simplified. Only few weakly branching tracheae present, connected to mesosomal and metasomal spiracles. Transverse stems and air sacs absent, probably because of diffusion sufficing for oxygen transport in organisms of such small sizes. Tracheae with structure typical of insects, consisting of hypoderm and intima, intima with helical thickenings—taenidia.

Nervous system

Cerebrum and suboesophageal ganglion fused into one synganglion and localized entirely in cranium. Ganglia of thoracic neural chain in Trichogramma separated, in Megaphragma mesothoracic and metathoracic ganglion fused (Figs. 8.11c, d and 8.12c, d). Trichogramma with pair of small abdominal ganglia, in Megaphragma abdominal ganglia fused into one synganglion.

Ensheathment in Trichogramma well developed and structured as in Anaphes. Neural lamella 0.05–0.3 μm thick; perineurium 1–1.5 μm thick. As in A. flavipes, almost entire volume of body of neuron occupied by nucleus. Heterochromatin represented by large spherical islets in center of nucleus, flattened on periphery. In spite of small volume of cytoplasm, cellular organelles of neurons clearly discernible at cellular level. Granular endoplasmic reticulum, ribosomes, mitochondria, Golgi apparatus, and lysosomes pronounced (Fig. 8.13). Neuropil containing synaptic contacts of different types, but mostly of polarized type. Vast majority of contacts represented by chemical synapses of asymmetrical type. Nonpolarized synaptic contacts occurring less often and characterized by absence of synaptic vesicles and condensation of membranes in contact areas. Axoplasm of axons and dendrites with discernible mitochondria, microtubules, neurofibrils. Neuropil with some cortical glia embedding neurons and their projections. Minimum diameter of projections in neuropil of cerebrum in Trichogramma 0.06 μm.

Fig. 8.13

Ultrastructure of cerebrum in Trichogramma evanescens, TEM: Ga Golgi apparatus; gEPR granular endoplasmic reticulum; gl cortical glia; ls lysosomes; mcf microfilaments; med granules of mediator; mt mitochondrion; nn nucleus; syn synaptic contact. c–f arrows indicate synaptic contacts

Cell bodies in nervous system of T. evanescens 1.53–3.36 μm in diameter (M = 2.4, n = 346). Cerebrum of T. evanescens containing only 18000 cells.

Protocerebrum larger than any other region of cerebrum in Trichogramma. Large central body complex occupying medial position and, as in Anaphes, differentiated into central body (dorsal region, consisting of dorsal arch, fan-shaped body, ventral region, and noduli) and protocerebral bridge (Fig. 8.14). Mushroom bodies well developed. Peduncles of mushroom bodies long and twisted. In dorsal distal part, near calyces, peduncles with geniculate curve. Calyces single (secondarily fused), of spherical shape and glomerular structure. Optic lobes represented by three neuropils. Lamina elongate and crescent-shaped, other optic neuropils elypsoid. Lobular complex differentiated into lobula and lobular plate. All three optic neuropils tightly adjoining each other, together forming angle, as in Anaphes. Well-developed ocellar ganglia present. Antennal lobes of spherical shape and glomerular structure. Tritocerebrum rather small, clearly discernible, appearing as dense elongate structure. Tritocerebral commissures completely sunk into common neuropilar mass of cerebrum.

Fig. 8.14

3D reconstructions of cerebrum in Trichogramma evanescens (modified from Makarova and Polilov 2013): a dorsal view; b lateral view; c frontal view; an antennal nerves; ant antennae; cnt connectives linking suboesophageal ganglion with prothoracic ganglion; oc compound eyes; ocl ocelli; ocn ocellar nerves; ptx prothorax; lmc mouthparts; sgn nerves of suboesophageal ganglion, innervating mouthparts; soeg suboesophageal ganglion; tcn paired nerves of tritocerebrum

Stomatogastric nervous system situated very close to head synganglion and indistinguishable.

The central nervous system of Megaphragma has a fundamentally different ultrastructure (Figs. 8.15 and 8.16). It was shown that in adults of M. mymaripenne the nervous system is almost anucleate, because over 95 % of cells in the central nervous system undergo lysis of bodies and nuclei at late stages of pupal development (Polilov 2012). All ganglia in the nervous system of adults are represented almost exclusively by neuropil, the structure of which is almost identical to that of Trichogramma. The neuropil of the supraesophageal ganglion contains discernible optic lobes, the central body complex, and antennal lobes. At the same time, the central nervous system contains only 339–372 (M = 360, n = 3) nuclei, 179–253 of them in cerebrum. The extraneural sheath is incomplete, consisting of separate scattered cells. The neural lamella is absent, distinguishing Megaphragma from other insects. The cytoplasm of neurons in M. mymaripenne contains organelles: mitochondria, granular endoplasmic reticulum, and many lysosomes.

Fig. 8.15

Structure of cerebrum in Megaphragma mymaripenne, 3D: a, c lateral view; b, d dorsal view. Colors: blue cuticle, yellow cerebrum, green intestine, white eyes and ocelli, red nuclei of cells of central nervous system

Fig. 8.16

Ultrastructure of cerebrum in Megaphragma, TEM: a M. mymaripenne; b–e M. amalphitanum, med granules of mediator, mt mitochondrion, nu nucleus, pn perineurium, arrows indicate synaptic contacts

Muscular system

Structure of muscular system in trichogrammatids, in spite of their small size, complying with general plan typical of insects. Musculature has been studied in Trichogramma evanescens and Megaphragma mymaripenne (Table 7.1). Most muscles of Megaphragma are connected with the skeleton via strongly shortened tonofibril apparatus, which morphologically resembling the desmosome; a similar structure has been described in four-legged mites (Silvere and Shtein-Margolina 1976).

Musculature of head (Figs. 8.17 and 8.18). 0an1 (M. tentorioscapalis anterior): O, anterior tentorial arms; I, anterior margin of base of scape. 0an2 (M. tentorioscapalis posterior): O, anterior tentorial arms; I, posterior margin of base of scape. 0an3 (M. tentorioscapalis lateralis): O, anterior tentorial arms; I, lateral margin of base of scape. Muscle of unclear homology, possibly 0an4 (M. tentorioscapalis medialis), with atypical attachment site: O, anterolateral part of frons; I, anterior margin of base of scape. 0md1 (M. craniomandibularis internus), consisting of two subunits: O, first, lateral part of cranium; second, gular zone; I, adductor of mandible. 0md3 (M. craniomandibularis externus): O, lateral part of cranium; I, abductor of mandible. 0md4 (M. hypopharyngomandibularis): O, anterior tentorial arms; I, adductor of mandible. 0mx1 (M. craniocardinalis): O, posterior part of cranium; I, ventrolateral part of cardo. 0mx3 (M. tentoriocardinalis): O, anterior tentorial arms; I, cardo. 0mx4 (M. tentoriostipitalis anterior): O, anterior tentorial arms; I, base of stipes. 0la5 (M. tentoriopraementalis): O, anterior tentorial arms; I, posterior margin of prementum. 0la6 (M. tentorioparaglossalis): O, anterior tentorial arms; I, anterior margin of prementum. 0hy1 (M. frontooralis): O, frons; I, posterior margin of epipharynx. 0hy3 (M. craniohypopharyngealis): O, anterior tentorial arms; I, anterior margin of epipharynx. Circular muscles of hypopharynx absent. 0ci1 (M. clypeopalatalis): O, clypeus; I, dorsal part of epipharynx. 0bu2 (M. frontobuccalis anterior): O, frons; I, dorsolateral part of pharynx. 0bu3 (M. frontobuccalis posterior): O, frons; I, dorsal part of pharynx. 0st1 (M. annularis stomodaei): transverse musculature, developed only on dorsal surface of pharynx. Internal musculature of antennae and mouthparts not studied because of extremely small size.

Fig. 8.17

Musculature of head in Trichogramma evanescens, 3D: a–c lateral internal view; d lateral external view; e frontal view; f posterior view; ant antenna, ata anterior tentorial arms, lb labium, md mandible, mx maxilla, oc eye, ocl ocellus, ph pharynx. Musculature see text

Fig. 8.18

Musculature of head in Megaphragma mymaripenne, 3D: a–c lateral internal view; d lateral external view; e dorsal view; f frontal view; ant antenna, ata anterior tentorial arms, lb labium, md mandible, mx maxilla, oc eye, ocl ocellus, ph pharynx. Musculature see text

Musculature of mesosoma (Figs. 8.19 and 8.20). Prothorax. Idlm5 (M. pronoto-phragmalis anterior): O, prophragma; I, medial part of pronotum. Idvm2 (M. cervico-occipitalis medialis): O, cervical region; I, occipital region. Itpm3 (M. pronoto-pleuralis anterior): O, lateral part of notum; I, propleurite, could not be determined precisely. Idvm5 (M. pronoto-cervicalis anterior) and Idvm6 (M. pronoto-cervicalis medialis) fused: O, posterior part of pronotum and prophragma; I, cervical region. Idvm7 (M. pronoto-cervicalis posterior): O, pronotum; I, cervical region. Idvm9 (M. profurca-occipitalis): O, profurca; I, occipital region. Idvm18 (M. pronoto-coxalis lateralis): O, pronotum; I, lateral margin of base of coxa. Itpm2 (M. propleuro-occipitalis): O, occipital zone; I, pleurite (Trichogramma), pleural apodeme (Megaphragma). Itpm4-5 (M. pronoto-apodemalis): O, lateral part of pronotum; I, pleurite. Ipcm3 (M. propleuro-trochantinalis): O, pleural apodeme; I, trochantin. Ipcm4 (M. propleuro-coxalis superior): O, pleural apodeme; I, anterior margin of base of coxa. Ipcm8 (M. propleuro-trochanteralis): O, pleural apodeme; I, trochanter, via fine tendon. Ivlm1 (M. profurca-cervicalis): O, profurca; I, cervical region. Ivlm3 (M. profurca-tentorialis): O, profurca; I, postoccipital region. Ivlm7 (M. profurca-mesofurcalis): O, profurca; I, mesofurca. Iscm1 (M. profurca-coxalis anterior): O, profurca; I, anterior margin of base of coxa. Iscm2 (M. profurca-coxalis posterior): O, profurca; I, posterior margin of base of coxa. Iscm3 (M. profurca-coxalis medialis): O, profurca; I, medial margin of base of coxa. Iscm5 (M. prospina-coxalis): O, fold between pro- and metathorax; I, posterior margin of base of coxa. Internal muscles of legs not studied because of extremely small size.

Fig. 8.19

Musculature of mesosoma in Trichogramma evanescens, 3D: a–c lateral internal view; d lateral external view; e dorsal view; f ventral view; pl1 pleurite of prothorax, pla3 pleural apodeme of metathorax, fr1.2 pro- and mesophragma, fu1.2.3 pro-, meso-, and metafurca, cx1.2.3 pro-, meso-, and metacoxae. Musculature see text

Fig. 8.20

Musculature of mesosoma in Megaphragma mymaripenne, 3D: a–c lateral internal view; d lateral external view; e dorsal view; f ventral view; pl1 pleurite of prothorax, pla3 pleural apodeme of metathorax, fr1.2 pro- and mesophragma, fu1.2 pro- and mesofurca, cx1.2.3 pro-, meso-, and metacoxae. Musculature see text

Mesothorax. IIdlm1 (M. prophragma-mesophragmalis) largest muscle: O, prophragma; I, mesophragma. IIdvm7 (M. mesonoto-trochanteralis): O, mesonotum; I, apodeme of trochanter. IIdvm8 (M. mesofurca-phragmalis): O, mesofurca; I, mesophragma. IItpm2 (M. mesopleura-praealaris): O, pleurite; I, prealar zone. IItpm4 (M. mesonoto-pleuralis anterior): fused with IItpm6, O, pleurite; I, margin of mesonotum. IItpm6 (M. mesonoto-pleuralis posterior) fused with IItpm4. IItpm9 (M. mesepimero-axillaris tertius): O, pleurite; I, third axillary plate. IItpm10 (M. mesepimero-subalaris) in Trichogramma present: O, pleurite; I, subalare; in Megaphragma absent. IItpm11 (M. mesopleura-subalaris) in Trichogramma present: O, pleurite; I, subalare; in Megaphragma absent. IIppm2 (M. mesobasalare-intersegmentalis): O, intersegmental juncture; I, basalare. IIspm1 (M. mesopleura-sternalis), in Trichogramma present: O, anterior part of pleurite; I, sternal region; in Megaphragma absent. IIspm2 (M. mesofurca-pleuralis): O, apex of mesofurca, I, pleurite. IIvlm3 (M. mesofurca-metafurcalis) in Trichogramma present: O, mesofurca; I, metafurca. in Megaphragma with muscle of unclear homology, possibly, IIvlm3 with atypical attachment site: O, mesofurca; I, fold between meso- and metasoma. IIscm1 (M. mesofurca-coxalis anterior): O, mesofurca; I, anterior margin of base of coxa. IIscm2 (M. mesofurca-coxalis posterior): O, mesofurca; I, posterolateral margin of base of coxa. IIscm3 (M. mesofurca-coxalis medialis): O, mesofurca; I, medial margin of base of coxa. Internal muscles of legs not studied because of extremely small size.

Metathorax and propodeum. IIIdlm1 (M. mesophragma-metaphragmalis): O, mesophragma; I, metaphragma. IIIdvm2 (M. metanoto-trochantinalis anterior): O, metanotum; I, trochanter. IIItpm5 (M. metanoto-pleuralis medialis) and IIItpm6 (M. metanoto-pleuralis posterior) fused: O, pleural apodeme of metathorax; I, lateral margin of metanotum. IIItpm9 (M. metepimero-axillaris tertius): O, pleural apodeme; I, third axillary plate. IIItpm7 (M. metanepisterno-axillaris): O, pleural apodeme; I, third axillary plate. IIItpm11 (M. metapleura-subalaris): O, pleural apodeme; I, subalare. IIIspm1 (M. metapleura-sternalis): O, ventral part of propodeum; I, basalare. IIIpcm3 (M. metanepisterno-coxalis anterior): O, pleural apodeme; I, anterolateral margin of base of coxa. IIIpcm4 (M. metanepisterno-coxalis posterior): O, pleural apodeme; I, posterolateral margin of base of coxa. IIIpcm6 (M. metapleura-trochanteralis): O, pleural apodeme; I, trochanter. IIIvlm2 (M. metafurca-abdominosternalis): in Trichogramma present: O, metafurca; I, abdominal sternite 2; in Megaphragma absent. IIIscm1 (M. metafurca-coxalis anterior) in Trichogramma: O, metafurca; I, anterior margin of base of coxa; in Megaphragma: O, fold between meso- and metathorax; I, anterior margin of base of coxa. IIIscm2 (M. metafurca-coxalis posterior) in Trichogramma present: O, metafurca; I, posterior margin of base of coxa; in Megaphragma absent. IIIscm5 (M. metaspina-coxalis) in Trichogramma present: O, fold between meso- and metasoma; I, posterior margin of base of coxa; in Megaphragma absent. IIIscm6 (M. metafurca-trochanteralis) in Trichogramma present: O, metafurca; I, trochanter, via fine tendon; in Megaphragma absent. Muscle V118, described only in hymenopterans (Vilhelmsen et al. 2010: no. 118, ph3–T2. M. metaphragma-second abdominal tergal): O, metaphragma; I, tergite of abdominal segment 2. in Megaphragma with additional muscle of unclear homology (mx): O, base of mesofurca; I, medial margin of base of metacoxae. Internal muscles of legs not studied because of extremely small size.

Musculature of metasoma. Dorsal longitudinal muscles (Mm. dorsales): O, anterior phragma; I, posterior phragma. Ventral longitudinal muscles (Mm. ventrales), several parallel fibers: O, anterior margin of segment; I, posterior margin of segment. Dorsoventral muscles, several of urotergosternal muscles, homology unknown. Ovipositor with group of strong retractors (Snodgrass 1942: no. 198, 199).

Reproductive system

Male reproductive system consisting of paired testes, spermiducts, accessory glands, and copulatory apparatus (Figs. 8.21c, d and 8.22c, d).

Fig. 8.21

Reproductive system of Trichogramma evanescens, 3D: a, b female; c, d male; a, c lateral view; b, d dorsal view; acg acid gland, aed aedeagus, agl accessory glands, alg alkaline gland, ova ovary, spt spermatheca, stl stylet of ovipositor, te testis, val valves of ovipositor

Fig. 8.22

Reproductive system of Megaphragma mymaripenne, 3D: a, b female; c, d male; a, c lateral view; b, d dorsal view; acg acid gland, aed aedeagus, agl accessory glands, alg alkaline gland, ova ovary, spt spermatheca, stl stylet of ovipositor, te testis, val valves of ovipositor

Female reproductive system consisting of paired ovaries and paired oviducts fused into unpaired oviduct connected to vagina (Figs. 8.21a, b and 8.22a, b). Spermatheca pear-shaped (Trichogramma) or rounded (Megaphragma). Well-developed acid gland, alkaline gland, and paired accessory glands present. Each ovary consisting of 2 polytrophic ovarioles. Ovipositor described in section on morphology of metasoma.

8.4 Morphology of Larvae

Larvae of Trichogrammatidae lack legs, mouthparts (except for mandibles), eyes, or antennae. First instar larva represented by two morphological types (Bakkendorf 1934; Boivin 2010): mymariform, typical of Ophioneurus and Poropoea (body C-shaped, segmented; with distinguished head and caudal process; with long setae); sacciform, typical of Trichogramma, Chaetostrichia, Oligosita, and Prestwichia (body sacciform, without pronounced segmentation, head not distinguished; setae absent). Some authors have described in some species of Trichogramma worm-like first instar larvae (Boivin 2010) and in some cases noted weakly pronounced segmentation (Chumakova 1966). Second instar larvae sacciform, without pronounced segmentation, integument without setae. Body length in larvae of Trichogramma 150–300 μm at hatching; during feeding they grow to 500 μm (Boivin 2010). Larval intestine differentiated into pharynx, oesophagus, and midgut (Jarjees et al. 1998) or stomodaeum, midgut, and hindgut (midgut and hindgut not connected, Wu et al. 2000), stomodeum with four dorsal muscles and one ventral muscles (Wu et al. 2000). Structures recorded in some larvae include primordia of the reproductive system (Chumakova 1966; Ivanova-Kazas 1961), anal vesicle (Jarjees et al. 1998; Jarjees and Merritt, 2002) and primordia of the nervous system (Ivanova-Kazas 1961); at later stages of larval development primordia of the tracheal system and cutaneous musculature appear (Ivanova-Kazas 1952).