Research Article |
Corresponding author: Michael Csader ( m.csader@web.de ) Academic editor: Jose Fernandez-Triana
© 2021 Michael Csader, Karin Mayer, Oliver Betz, Stefan Fischer, Benjamin Eggs.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Csader M, Mayer K, Betz O, Fischer S, Eggs B (2021) Ovipositor of the braconid wasp Habrobracon hebetor: structural and functional aspects. Journal of Hymenoptera Research 83: 73-99. https://doi.org/10.3897/jhr.83.64018
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The Braconidae are a megadiverse and ecologically highly important group of insects. The vast majority of braconid wasps are parasitoids of other insects, usually attacking the egg or larval stages of their hosts. The ovipositor plays a crucial role in the assessment of the potential host and precise egg laying. We used light- and electron-microscopic techniques to investigate all inherent cuticular elements of the ovipositor (the female 9th abdominal tergum, two pairs of valvifers, and three pairs of valvulae) of the braconid Habrobracon hebetor (Say, 1836) in detail with respect to their morphological structure and microsculpture. Based on serial sections, we reconstructed the terebra in 3D with all its inherent structures and the ligaments connecting it to the 2nd valvifers. We examined the exact position of the paired valvilli, which are bilateral concave structures that protrude into the egg canal. In H. hebetor, these structures putatively divert the egg ventrally between the 1st valvulae for oviposition. We discuss further mechanical and functional aspects of the ovipositor in order to increase the understanding of this putative key feature in the evolution of braconids and of parasitoid wasps in general.
3D reconstruction, Braconidae, functional morphology, Hymenoptera, parasitoid, SEM, serial sectioning, terebra
Most hymenopteran species belong to the guild of parasitoids of other insects (
The hymenopteran ovipositor is an anatomical and functional cluster that consists of the following elements: the paired 1st valvulae (8th gonapophyses), the 2nd valvula (fused 9th gonapophyses), the paired 3rd valvulae (9th gonostyli), the paired 1st valvifers (fusion of the 8th gonocoxites and gonangula (
Despite many comparative studies on the terebra of hymenopterans (
However, knowledge about structural and functional aspects of the ovipositor system of the ecologically and morphologically extremely diverse and species-rich Braconidae remains limited.
Habrobracon hebetor (Say, 1836) (Fig.
The H. hebetor (Fig.
For whole mount samples, female H. hebetor were killed in 70 % ethanol at 45 °C. The metasoma was cut off and macerated in 10% aqueous potassium hydroxide for up to 24 h at room temperature to remove tissues, cleaned in distilled water on a mini-shaker, and dehydrated stepwise in ethanol. We then dissected the ovipositor out of the metasoma by using thin tungsten needles, mounted the specimen onto a microscope slide, and embedded it in Entellan® (Merck KGaA, Darmstadt, Deutschland).
For semithin serial sections, we anaesthetized female H. hebetor with carbon dioxide. The metasomas were removed and, in order to avoid autolysis, immediately submersed in a primary fixative containing 2.5% glutaraldehyde and 5% sucrose, buffered with 0.1 M cacodylate to pH 7.4. During this fixation, the samples were held in an ice bath at approximately 4 °C for 4 h. Samples were rinsed three times for 10 min in pre-chilled 0.1 M cacodylate buffer (pH 7.4) and post-fixed by using a solution of 1% osmium tetroxide in 0.1 M cacodylate buffer at 4 °C for 4 h. After being further rinsed in the same buffer, the samples were dehydrated through a graded series of ethanol with steps of 30% for 15 min and 50% for 10 min at 4 °C, three times per step, and of 70% for 10 min, three times at room temperature. The following steps were performed at room temperature. En bloc staining was conducted using a saturated solution of 70% ethanolic uranyl acetate for 12 h on a rotatory shaker. Afterwards, dehydration was continued in 5% steps, three times for 10 min each. The fully dehydrated samples were washed in 100% propylene oxide twice for 1 h , and subsequently infiltrated in Spurr low-viscosity embedding resin (Polysciences Inc., Warrington, PA, USA) via a propylene oxide:resin mixture at ratios of 1:1, 1:3, and 1:7 for 1 h per step and then in pure resin for 17 h on a rotatory shaker. As a last incubation step, the samples were placed in fresh pure resin, embedded in silicon molds, and polymerized at 70 °C for 8 h.
Semithin sections of 600 nm were cut perpendicularly to the terebra of H. hebetor by using an ultramicrotome Leica Ultracut UTC (Leica Microsystems GmbH, Wetzlar, Germany) equipped with a diamond knife (45° knife angle; DuPont Instruments, Wilmington, DE, USA); a series was obtained with 1920 sections. Semithin sections were then mounted on a microscopic slide by using a ‘Perfect Loop for Light Microscopy’ (Electron Microscopy Sciences, Hatfield, PA, USA), stained with Stevenel’s blue (del Cerro et al. 1980) for 40 min at 60 °C, and subsequently washed in distilled water twice for 5 min each. After being dried, the stained sections were embedded in ‘Xylolfreies Eindeckmittel’ (Engelbrecht Medizin- und Labortechnik GmbH, Edermüde, Germany).
The image stack for the 3D reconstruction was generated using a Zeiss Axioplan (Carl Zeiss Microscopy GmbH, Jena, Deutschland) light microscope, equipped with a Nikon D7100 single-lens reflex digital camera (Nikon K.K., Tokio, Japan) and Helicon Remote software version 3.6.2.w (Helicon Soft Ltd, Kharkiv, Ukraine). Flawed images (missing or folded structures and staining problems) were replaced by a copy of the previous or the following image (this was the case for fewer than 3% of the images) for reconstruction purposes. Adobe Photoshop Lightroom version 6.0 (Adobe Systems, San José, CA, USA) was used for initial image processing (white balancing, color contrasting, black and white conversion), whereas Fiji (
Schematic drawings of the cross-sections of the terebra were generated in Inkscape version 0.92.4 (Inkscape Community; available online at http://www.inkscape.org/) based on the original light-microscopic images of the semithin sections.
For lateral and ventral habitus images, female wasps were imaged with a Keyence VHX-7000 Digital Microscope (Keyence Corporation, Osaka, Japan) using focus stacking.
For scanning electron microscopy (SEM), the specimens were air-dried in a desiccator with Silica gel blue (Carl Roth GmbH & Co. KG, Karlsruhe, Deutschland) for at least four days before being mounted with double-sided adhesive tabs onto stubs and sputter-coated with 19 nm pure gold by using an Emitech K550X (Quorum Technologies Ltd, West Sussex, UK). Images were taken with a scanning electron microscope of the type EVO LS 10 (Carl Zeiss Microscopy GmbH, Jena, Germany) and SmartSEM version V05.04.05.00 software (Carl Zeiss Microscopy GmbH, Jena Germany).
As in all hymenopterans, the ovipositor of H. hebetor consists of three pairs of valvulae, two pairs of valvifers, and the female T9 (Fig.
Habitus images of female Habrobracon hebetor: lateral (a) and ventral (b) ascpect. Schematic drawing of the ovipositor of H. hebetor (lateral view) based on the light microscopic and SEM images (c). Abbreviations: 1vf = 1st valvifer; 1vv = 1st valvula; 2vf = 2nd valvifer; 2vv = 2nd valvula; 3vv = 3rd valvula; ar9 = anterior ridge of T9; ba = basal articulation; blb = bulb; dr1 = dorsal ramus of the 1st valvula; hsl = hook-shaped lobe of the 2nd valvifer; iva = intervalvifer articulation; mb2 = median bridge of 2nd valvifers; sr = sensillar row of the 2nd valvifer, sp = sensillar patch of the 2nd valvifer; T9 = female T9; tva = tergo-valvifer articulation.
The 1st and 2nd valvulae form the terebra and enclose the egg canal (cf. Figs
(next page) Cross sections through the terebra of Habrobracon hebetor (from proximal to distal); schematic drawings of the 1st and 2nd valvula (a–i) based on the light microscopic images of the presented semithin sections (a’–i’ 600 nm; stained with Stevenel’s blue). The drawings are of the same size ratio. The 2nd valvulae possesses, in the proximal region, two lumina that merge into one in the most distal region (h–i). The bulbs (b) and the valvilli (g) are visible. The orange lines (in e, f) mark the position of the distally pointing ctenoid structures on the dorsal surfaces of the 1st valvulae, which are in close contact with the ventral surface of the 2nd valvula. The genital membrane connects the dorsal margins of the 2nd valvifers (b’–h’) c fine cuticular structures arise from the dorsal and ventral parts of the 2nd valvula and define the lumina of the bulbs (arrow) h1 olistheter-like interlocking system connecting the medial surfaces of the apices of the paired 1st valvulae (arrow). Final segmented 3D reconstruction based on a semithin section series (600 nm thickness) a*–i* position of each single section marked on the final 3D reconstruction of the terebra. Abbreviations: 1vv = 1st valvula; 2vv = 2nd valvula; 3vv = 3rd valvula; au = aulax; blb = bulb; cr = longitudinal crack of 2nd valvula; ec = egg canal; fl1 = longitudinal flap of the 1st valvula; gm = genital membrane; igs = internal guiding structure; l1 = lumen of 1st valvula; l2 = lumen of 2nd valvula; lb = lumen of the bulb; lg = ligament; oth = olistheter; rh = rhachis; vd = duct of the venom gland; vl = valvillus.
3D reconstruction of the basal part of the terebra of Habrobracon hebetor composed of the 2nd valvulae and the paired 1st valvulae, based on a semithin section series (600 nm thickness a lateroventral aspect b lateral aspect c dorsal aspect d ventral aspect). The duct of the venom gland enters dorsoproximally on the left side only. The two ligaments connect the 2nd valvula to the anterior parts of the 2nd valvifers (not visible in these images). The black circle (b) indicates the rotation axis of the basal articulation. The lines of the processus articularis and processus musculares (b) point to their presumed position according to the results of
SEM images of the 1st valvulae of Habrobracon hebetor a–c apex of 1st valvula with sawteeth (a lateral aspect b–c dorsal aspect). The aulaces are visible (b) d–e valvillus of 1st valvula (distal is right) f distally oriented scale-like structures on the lateral walls of the aulax g leaf-like ctenidia on the medial side of 1st valvula h 1st valvula with distally oriented ctenoid structures on its dorsal side (contact surface with the 2nd valvula) and ctenidia on its medial side (contact surface with the opposing 1st valvula building the egg canal in the distal part of the terebra). Abbreviations: 1vv = 1st valvula; au = aulax; ct = ctenidium; rcs = row of ctenoid structures; sc = scales; st = sawtooth; vl = valvillus.
In H. hebetor, the cross sections of the terebra differ notably along its length (Fig.
The paired 1st valvulae of H. hebetor form the ventral half of the terebra (1vv; Figs
At their apices, the 1st valvulae of H. hebetor possess several sawteeth, which decrease in size apically (st; Fig.
A single valvillus situated on the inner surface of each 1st valvulae protrudes inside the egg canal (vl; Figs
Each 1st valvula contains a lumen (l1, Fig.
In H. hebetor, the 2nd valvula (2vv; Figs
The apex of the 2nd valvula is not serrated but is slightly enlarged before it narrows towards the tip (Figs
SEM images of the 2nd valvula of Habrobracon hebetor a overview of the 2nd valvula (ventral aspect with the interlocked 1st valvulae removed) b proximal part of 2nd valvula featuring the bulbs c apex of 2nd valvula with the ending of the rhachises (arrow) and campaniform sensillae (medioventral aspect) d–e middle part of the 2nd valvula showing the rhachises and distally oriented ctenidia f sensilla at the apex of the 2nd valvula (detail image of c). Abbreviations: 2vv = 2nd valvula; blb = bulb; cs = campaniform sensilla; ct = ctenidia; rh = rhachis.
Proximally, the 2nd valvula features a distinct longitudinal crack at the ventral side along the middle, which is clearly visible in cross-section (cr; Fig.
The paired 3rd valvulae of H. hebetor originate at the distal end of the 2nd valvifers and extend far beyond the posterior tip of the metasoma towards the tip of the terebra (Figs
SEM images of 3rd valvulae of Habrobracon hebetor a the terebra is partially embraced by the 3rd valvulae b inner proximal surface of the 3rd valvulae with fine trichomes distally c outer surface of the 3rd valvulae, proximally exhibiting annulation caused by fine transverse furrows (arrow) d outer surface of the 3rd valvulae at the transition zone (arrow) between the distal longitudinal ridge to the proximal vertically folded surface at the region in which the 3rd valvulae expand e inner surface of the apex of a 3rd valvula covered by trichomes. Abbreviations: 3vv = 3rd valvula; trb = terebra; t = trichome.
The inner surface of the 3rd valvulae facing the terebra is densely covered by trichomes (t; Fig.
In lateral view, the paired 1st valvifers of H. hebetor have a compact triangular shape with rounded edges (1vf; Figs
(previous page) SEM (a–d) and light microscopic (e–i) images of the ovipositor of Habrobracon hebetor a overview of the ovipositor (lateral aspect; visible pore-like structures are presumably artefacts of detached trichomes) c 1st valvifer exhibiting the interarticular ridge and the hook-shaped lobe of the 2nd valvifer. The 1st valvifer is continuous with the dorsal rami of the 1st valvula and is articulated with the 2nd valvifer and the female T9 via the intervalvifer articulation and the tergo-valvifer articulation, respectively d sensillar patch of the 2nd valvifer (made visible by partly removal of the 1st valvifer) b, f sensillar patch of the 2nd valvifer e overview of the 2nd valvifer and female T9. The arrow shows the dorsal hump of the T9 g tergo-valfiver articulation between the 1st valvifer and female T9 h detail image of e. The laterally placed bulbs of the most proximal part of the 2nd valvula are articulated with the paired 2nd valvifers via the basal articulation i sensilla in a row at the dorsal margin of the 2nd valvifer. Abbreviations: 1vf =1st valvifer; 1vv = 1st valvula; 2vf = 2nd valvifer; 2vv = 2nd valvula; 3vv = 3rd valvula; ar9 = anterior ridge of T9; ba = basal articulation; blb = bulb; df2 = dorsal flange of 2nd valvifer; dm2 = dorsal margin of the 2nd valvifer; dr1 = dorsal ramus of the 1st valvula; ds = dorsal spike of the 2nd valvifer; hsl = hook-shaped lobe of the 2nd valvifer; iar = interarticular ridge of the 1st valvifer; iva = intervalvifer articulation; sp = sensillar patch of the 2nd valvifer; sr = sensillar row of the 2nd valvifer; pa = processus articularis; pm = processus musculares; T9 = female T9; trb = terebra; tva = tergo-valvifer articulation.
The paired 2nd valvifers of H. hebetor are elongated in the longitudinal axis (2vf; Figs
At its anterodorsal corner, the 2nd valvifer extends upwards in a hook-shaped lobe (hsl; Fig.
Two main ridges are found on the 2nd valvifer, i.e. (1) the dorsal flange of the 2nd valvifer (df2; Fig.
Clusters of sensillae (“styloconic sensillae” according to
The female T9 is unpaired and elongated (T9; Figs
Functional models of the actuation and movement mechanisms based on thorough analyses of the musculoskeletal system of an ichneumonid and a braconid wasp have recently been described (Eggs et al. 2020,
The ovipositor movements are mainly actuated by two pairs of antagonistically working muscles (further described below), i.e. (1) the depression (i.e. downward rotation to the active position) and elevation (i.e. upward rotation back to the resting position) of the terebra, and (2) the pro- and retraction of the 1st valvulae. Smaller muscles, i.e. the 1st valvifer-genital membrane muscle or the posterior T9-2nd valvifer muscle, might predominantly serve to stabilize the ovipositor system during oviposition.
In the context of the described movements, the 1st valvifer acts as a one-armed class 3 lever (force arm smaller than load arm). In our lever model (Fig.
Functional lever model of 1st valvifer with both articulations and the beginning of the dorsal ramus of the 1st valvula (arrow) with the intervalvifer articulation acting as pivot point. c = anatomical inlever ; c’ = effective (= mechanical) inlever; d = anatomic outlever; d` = effective (= mechanical) outlever; F(in protraction), F(in retraction) = Force input at the 1st valvifer; F(out protraction), F(out retraction) = Force output at the 1st valvifer that is transferred to the dorsal ramus of the 1st valvula. c’ · F(in) = d’ · F(out). Abbreviations: 1vf = 1st valvifer; dr1 = dorsal ramus of the 1st valvula; iar = interarticular ridge of the 1st valvifer; iva = intervalvifer articulationtva = tergo-valvifer articulation.
The shape of the 1st valvifer varies between the various hymenopteran superfamilies (
The two sensilla clusters found on the 2nd valvifer of H. hebetor (sp, sr; Fig.
All the cuticular elements of the ovipositor of Habrobracon hebetor play a crucial role for successful oviposition. The 2nd valvifer and the female T9 exhibit many muscle insertions, the 1st valvifer acts as a lever that transmits movements to the 1st valvulae, and the terebra serves as a device for precise venom injection, host assessment, and accurate egg laying. All the cuticular elements feature many distinct structures in addition to the microsculpture that is crucial for the performance of these tasks. Our work also has shown that a 3D reconstruction based on a histological section series preserves useful information about the exact morphology and position of inherent structures thereby enabling us to draw conclusions about their function. Future comparative examination of the inherent ovipositor elements, their morphological structure, and the underlying mechanical and functional aspects has the potential to increase our understanding of a putative key feature in the evolution of parasitoid hymenopterans, a feature that probably has significantly impacted the evolutionary success of braconid wasps (more than 18,000 described (
We thank Paavo Bergmann for valuable hints regarding histological techniques, Monika Meinert for assistance with SEM, Verena Pietzsch and James H. Nebelsick with the Keyence digital microscope, Theresa Jones for linguistic corrections of the manuscript, and Lars Vilhelmsen and Donald L. J. Quicke for their useful comments.
This work was funded by the German Research Foundation (DFG) as part of the Transregional Collaborative Research Centre (SFB-TRR) 141 ‘Biological design and integrative structures’ (project A03 ‘Inspired by plants and animals: actively actuated rod-shaped structures exhibiting adaptive stiffness and joint-free kinematics’). The article processing charge was covered by the DFG and the Open Access Publishing Fund of the University of Tübingen.
Morphological terms relevant to the hymenopteran ovipositor system. The terms (abbreviations used in this article in brackets) are used and defined according to the Hymenoptera Anatomy Ontology Portal (HAO) (
Anatomical term (abbreviation) | definition / concept | URI |
---|---|---|
1st valvifer (1vf) | The area of the 1st valvifer-1st valvulae complex that is proximal to the aulax, bears the 9th tergal condyle of the 1st valvifer and the 2nd valviferal condyle of the 1st valvifer and is connected to the genital membrane by muscle. | http://purl.obolibrary.org/obo/HAO_0000338 |
1st valvifer-genital membrane muscle | The ovipositor muscle that arises from the posterior part of the 1st valvifer and inserts anteriorly on the genital membrane anterior to the T9-genital membrane muscle. | http://purl.obolibrary.org/obo/HAO_0001746 |
1st valvula, 1st valvulae (1vv) | The area of the 1st valvifer-1st valvulae complex that is delimited by the proximal margin of the aulax. | http://purl.obolibrary.org/obo/HAO_0000339 |
2nd valvifer (2vf) | The area of the 2nd valvifer-2nd valvulae-3rd valvulae complex that is proximal to the basal articulation and to the processus musculares and articulates with the female T9. | http://purl.obolibrary.org/obo/HAO_0000927 |
2nd valvula (2vv) | The area of the 2nd valvifer-2nd valvulae-3rd valvulae complex that is distal to the basal articulation and to the processus musculares and is limited medially by the median body axis. | http://purl.obolibrary.org/obo/HAO_0000928 |
3rd valvula, 3rd valvulae (3vv) | The area of the 2nd valvifer-3rdvalvulae complex that is posterior to the distal vertical conjunctiva of the 2nd valvifer-3rd valvulae complex. | http://purl.obolibrary.org/obo/HAO_0001012 |
anterior 2nd valvifer-2nd valvula muscle | The ovipositor muscle that arises from the anterodorsal part of the 2nd valvifer and inserts subapically on the processus articularis. | http://purl.obolibrary.org/obo/HAO_0001166 |
anterior ridge of T9 (ar9) | The ridge that extends along the anterior margin of female T9 and receives the site of origin of the ventral and the dorsal T9-2nd valvifer muscles. | http://purl.obolibrary.org/obo/HAO_0002182 |
anterior section of dorsal flange of 2nd valvifer | The area of the dorsal flange of the 2nd valvifer that is anterior to the site of origin of the basal line. | http://purl.obolibrary.org/obo/HAO_0002173 |
apodeme | The process that is internal. | http://purl.obolibrary.org/obo/HAO_0000142 |
aulax (au) | The impression that is on the 1st valvifer-1st valvula complex accommodates the rhachis. | http://purl.obolibrary.org/obo/HAO_0000152 |
basal articulation (ba) | The articulation that is part of the 2nd valvifer-2nd valvula-3rd valvula complex and adjacent to the rhachis. | http://purl.obolibrary.org/obo/HAO_0001177 |
basal line of the 2nd valvifer | The line on the 2nd valvifer that extends between the pars articularis and the dorsal flange of 2nd valvifer. | http://purl.obolibrary.org/obo/HAO_0002171 |
bulb (blb) | The anterior area of the dorsal valve [composite structure of the fused 2nd valvulae] that is bulbous. | http://purl.obolibrary.org/obo/HAO_0002177 |
conjunctiva | The area of the cuticle that is more flexible than adjacent sclerites. | http://purl.obolibrary.org/obo/HAO_0000221 |
distal notch of the dorsal valve (no) | The notch that is distal on the dorsal valve [composite structure of the fused 2nd valvulae]. | http://purl.obolibrary.org/obo/HAO_0002179 |
dorsal flange of the 2nd valvifer (df2) | The flange that extends on the dorsal margin of the 2nd valvifer. Part of the ventral T9-2nd valvifer muscle attaches to the flange. | http://purl.obolibrary.org/obo/HAO_0001577 |
dorsal projection of the 2nd valvifer (dp2) | The projection that is located on the 2nd valvifer and corresponds to the proximal end of the rhachis. | http://purl.obolibrary.org/obo/HAO_0002172 |
dorsal ramus of the 1st valvula (dr1) | The region that extends along the dorsal margin of the 1st valvula and bears the aulax. | http://purl.obolibrary.org/obo/HAO_0001579 |
dorsal T9-2nd valvifer muscle | The ovipositor muscle that arises along the posterodorsal part of the anterior margin of female T9 and inserts on the anterior section of the dorsal flanges of the 2nd valvifer. | http://purl.obolibrary.org/obo/HAO_0001569 |
egg canal (ec) | The anatomical space that is between the left and right olistheters. | http://purl.obolibrary.org/obo/HAO_0002191 |
female T9 (T9) | The tergite that is articulated with the 1st valvifer and is connected to the 2nd valvifer via muscles. | http://purl.obolibrary.org/obo/HAO_0000075 |
flange | The projection that is lamella-like and is located on a rim, carina, apodeme or edge. | http://purl.obolibrary.org/obo/HAO_0000344 |
genital membrane (gm) | The conjunctiva that connects the ventral margins of the 2nd valvifers arching above the 2nd valvula. | http://purl.obolibrary.org/obo/HAO_0001757 |
interarticular ridge of the 1st valvifer (iar) | The ridge that extends along the posterior margin of the 1st valvifer between the intervalvifer and tergo-valvifer articulations. | http://purl.obolibrary.org/obo/HAO_0001562 |
intervalvifer articulation (iva) | The articulation between the 1st valvifer and 2nd valvifer. | http://purl.obolibrary.org/obo/HAO_0001558 |
median bridge of the 2nd valvifers (mb2) | The area that connects posterodorsally the 2nd valvifers and is the site of attachment for the posterior T9-2nd valvifer muscle. | http://purl.obolibrary.org/obo/HAO_0001780 |
notal membrane | The conjunctiva that connects the medial margins of the 2nd valvulae. | http://purl.obolibrary.org/obo/HAO_0001733 |
notch | The part of the margin of a sclerite that is concave. | http://purl.obolibrary.org/obo/HAO_0000648 |
olistheter (oth) | The anatomical cluster that is composed of the rhachis of the 2nd valvula and the aulax of the 1st valvula. | http://purl.obolibrary.org/obo/HAO_0001103 |
ovipositor | The anatomical cluster that is composed of the 1st valvulae, 2nd valvulae, 3rd valvulae, 1st valvifers, 2nd valvifers and female T9. | http://purl.obolibrary.org/obo/HAO_0000679 |
ovipositor apparatus | The anatomical cluster that is composed of the ovipositor, abdominal terga 8-10, abdominal sternum 7 and muscles connecting them. | http://purl.obolibrary.org/obo/HAO_0001600 |
ovipositor muscle | The abdominal muscle that inserts on the ovipositor. | http://purl.obolibrary.org/obo/HAO_0001290 |
pars articularis / pars articulares | The articular surface that is situated anteriorly on the ventral margin of the 2nd valvifer and forms the lateral part of the basal articulation. | http://purl.obolibrary.org/obo/HAO_0001606 |
posterior 2nd valvifer-2nd valvula muscle | The ovipositor muscle that arises posteroventrally from the 2nd valvifer and inserts on the processus musculares of the 2nd valvula. | http://purl.obolibrary.org/obo/HAO_0001815 |
processus articularis / processus articulares | The process that extends laterally from the proximal part of the 2nd valvula and forms the median part of the basal articulation, and corresponds to the site of attachment for the anterior 2nd valvifer-2nd valvula muscle. The processus articularis is part of the sclerite. | http://purl.obolibrary.org/obo/HAO_0001704 |
processus musculares / processus muscularis | The apodeme that extends dorsally from the proximal part of the 2nd valvula to the genital membrane and receives the site of attachment of the posterior 2nd valvifer-2nd valvula muscle. | http://purl.obolibrary.org/obo/HAO_0001703 |
rhachis (rh) | The ridge that extends along the ventral surface of the 2nd valvula that is partially enclosed by the aulax. | http://purl.obolibrary.org/obo/HAO_0000898 |
ridge | The apodeme that is elongate. | http://purl.obolibrary.org/obo/HAO_0000899 |
sawtooth (st) | The process that is located along the ventral margin of the 1st valvula of the dorsal margin of the 2nd valvula. | http://purl.obolibrary.org/obo/HAO_0001681 |
sclerite | The area of the cuticle that is less flexible than adjacent conjunctivae. | http://purl.obolibrary.org/obo/HAO_0000909 |
sensillar patch of the 2nd valvifer (sp) | The patch that is composed of placoid sensilla adjacent to the intervalvifer articulation. | http://purl.obolibrary.org/obo/HAO_0001671 |
sensillum | A sense organ embedded in the integument and consisting of one or a cluster of sensory neurons and associated sensory structures, support cells and glial cells forming a single organized unit with a largely bona fide boundary. | http://purl.obolibrary.org/obo/HAO_0000933 |
terebra (trb) | The anatomical cluster that is composed of the 1st and 2nd valulae. | http://purl.obolibrary.org/obo/HAO_0001004 |
tergite | The sclerite that is located on the tergum. | http://purl.obolibrary.org/obo/HAO_0001005 |
tergo-valvifer articulation (tva) | The articulation that is located between the female T9 and the 1st valvifer and is composed of the 9th tergal condyle of the 1st valvifer and the 1st valviferal fossa of the 9th tergite. | http://purl.obolibrary.org/obo/HAO_0001636 |
valvillus (vlv) | The sclerite that articulates on the 1st valvula and projects into the egg/poison canal. | http://purl.obolibrary.org/obo/HAO_0001619 |
venom gland reservoir of the 2nd valvifer (vd) | The gland reservoir that is between the 2nd valvifers. | http://purl.obolibrary.org/obo/HAO_0002176 |
ventral ramus of the 2nd valvula | The area of the 2nd valvifer-2nd valvula-3rd valvula complex that bears the rhachis. | http://purl.obolibrary.org/obo/HAO_0001107 |
ventral T9-2nd valvifer muscle | The ovipositor muscle that arises from the lateral region of female T9 and inserts along the posterior part of the dorsal flange of the 2nd valvifer. | http://purl.obolibrary.org/obo/HAO_0001616 |
Video S1
Data type: Video file (mp4)
Explanation note: Animation of the rotated segmented 3D reconstruction of the terebra of Habrobracon hebetor.
Video S2
Data type: Video file (mp4)
Explanation note: Animation of the rotated segmented 3D reconstruction of the proximal region of the terebra of Habrobracon hebetor (cf. Fig.