Morphology, ultrastructure, and probable functions of the sense organs on the ovipositor stylets of the hymenoptran parasitoid, Venturia canescens (Gravenhorst)

Morphology, Ultrastructure, and Probable Functions of theSense Organs on the Ovipositor Stylets of the HymenoptranParasitoid, Venturia canescens (Gravenhorst)ZAHID ALI SHAH*Department of Biological and Medical Sciences, University of Dundee, Dundee, DD1 4HN, United Kingdom

KEY WORDS Venturia canescens; ovipositor stylets sensilla; SEM; TEM; host-discrimination;parasitoid; oviposition

ABSTRACT To help understand the mechanism of host discrimination during oviposition of aparasitoid wasp, Venturia canescens (Gravenhorst) (Hymenoptera: Ichneumonidae), the ultrastruc-ture and morphology of the sense organs on the dorsal and ventral stylets of the ovipositor wereexamined using scanning and transmission electron microscopy. Ovipositor stylets were scannedfor sense organs, because only unsheathed ovipositors are used for probing, stabbing, and host dis-crimination. Five types of sensilla and secretary pores were identified. Based on their pattern ofinnervation, the surface-dome and pitted-dome sensilla were thought to have a gustatory functionand, thus, are the best candidates for host-discrimination. The arrangements of dendrites of type Iand type II campaniform sensilla suggested that these acted as pressure- and mechano-receptors,respectively. Coeloconic sensilla might act as thermo-hygroreceptors, whilst secretary pores mightprovide lubrication during the process of stabbing for oviposition. Surface-dome sensilla were themost numerous type found followed by secretary pores, pitted-dome sensilla, and coeloconic sen-silla. Almost all the sensilla and secretary pores were more numerous on the dorsal than on theventral stylets, and the maximum number of these sensilla and secretary pores occurred on the dis-tal end of the ovipositor stylets and decreased toward the proximal end. The surface-dome sensillaand secretary pores occurred in alternate rows while the pitted-dome sensilla were scattered allover the surface of the ovipositor stylets, especially on the sides of the stylets. Microsc. Res. Tech.00:000–000, 2012. VVC 2012 Wiley Periodicals, Inc.

INTRODUCTION

Sense organs on the hymenopteran ovipositor styletsand sheath have been described by King and Fordy(1970), Ganesalingam (1972), van Lenteren (1972),Hawke et al. (1973), Greany et al. (1977), Le Ralec andWagnberg (1990), Nenon et al. (1997), Brown andAnderson (1998), Shah (1998), Consoli et al. (1999),Quicke et al. (1999), van Lenteren et al. (2007), Dwecket al. (2008), Boring and Sharkey (2009), Nacro andNenon (2009), and Obonyo et al. (2011) using electronmicroscopy.

Parasitoids are able to discriminate parasitized hostsfrom unparasitized ones (Arthur, 1971; Bakker et al.,1967; Brown and Anderson, 1998; Chiappini and Soli-nas, 2002; Consoli et al., 1999; Dweck et al., 2008;Fisher and Ganesalingam, 1970; Ganesalingam, 1969,1974; Guillot et al., 1974; Holler et al., 1993; Nacro andNenon, 2009; Nelson and Roitberg, 1993; Price, 1970,1972; Quicke et al., 1999; van Lentern, 1972; van Len-teren et al., 2007; Vinson and Guillot, 1972; Wylie,1970, 1971). So, there is a need to identify the organson the body of these parasitoids that are capable ofhost-discrimination. Venturia canescens (Gravenhorst)(Hymenoptera: Ichneumonidae) is also capable of hostdiscrimination by perceiving cues from the host hemo-lymph (Fisher and Ganesalingman, 1970; Ganesalin-gam, 1974; Harrison et al., 1985; Hubbard et al., 1987;Mudd et al., 1982; Rogers, 1972; Waage, 1979). It is

also known that V. canescens uses an unsheathed ovi-positor for probing, stabbing, discrimination, and ovi-position (Ozkan and Gurkan, 2001). Therefore, itwould be useful to identify the sense organs on oviposi-tor stylets that are capable of host discrimination.

This study was conducted to understand the basisfor this discrimination by identifying host discriminat-ing sense organs on the ovipositor stylets of Venturiacanescens (Gravenhorst) and relating the morphologyand ultrastructure of these sense organs to their proba-ble function.

MATERIALS ANDMETHODSParasitoid Rearing

The parasitoid wasp, Venturia canescens (Grave-nhorst) (Hymenoptera: Ichneumonidae), was reared onthe Indian meal moth, Plodia interpunctella Hubner(Lepidoptera: Pyralidae), in 4-L sterilized jars kept in a

Present address of Zahid Ali Shah: Department of Zoology, Government Post-graduate College, Gojra, Toba Tek Singh, Pakistan*Correspondence to: Zahid Ali Shah, Department of Biological and Medical

Sciences, University of Dundee, Dundee, DD1 4HN, United Kingdom. E-mail:[email protected]

Received 29 September 2011; accepted in revised form 22 November 2011

Contract grant sponsor: Federal Ministry of Education, Government ofPakistan, Islamabad

DOI 10.1002/jemt.22007

Published online inWiley Online Library (wileyonlinelibrary.com).

VVC 2012 WILEY PERIODICALS, INC.

MICROSCOPY RESEARCH AND TECHNIQUE 00:000–000 (2012)

constant temperature room maintained at 268C 6 18C,65% 6 4% relative humidity, and a 16:8 light–darkphotoperiod. The wasps were fed with a 50% honey so-lution.

Scanning Electron Microscopy

Freshly enclosed parasitoids were anaesthetizedwith CO2 after which the ovipositor stylets wereexcised, dehydrated in a graded ethyl alcohol series,and mounted on aluminum stubs using double-sidedsticky tape. The ovipositor stylets were shadow-coatedin a sputter coater (Polaron SEM Coating Unit E 5100Series II’Cool’ Sputter Coater) with a thin film of gold–palladium alloy for 5 min and viewed using a scanningelectron microscope (JEOL JSM-35) at an acceleratingvoltage of 15 kV. Structures present on the stylets werephotographed.

Transmission Electron Microscopy

Parasitoids were anaesthetized with CO2 and placedin 2.5% glutaraldehyde in 0.1 M cacodylate buffer (pH5 7.2), following which the ovipositor stylets were cutwhile still under the solution and fixed in 25% glutaral-dehyde and 10% acrolein in 0.1 M cacodylate buffer(pH 5 7.2) over night. Then the specimens were rinsedtwo times in the same buffer and postfixed in 1% OsO4

in 0.1 M cacodylate buffer (pH 5 7.2) for 90 min, em-bedded in 2% agar, dehydrated in ethanol, treated withpropylene oxide, and infiltrated for 3 days with mix-tures of variable composition (1:1, 3:1, and full) ofSpurr’s resin and propylene oxide. Specimens werethen transferred to embedding molds with Spur’s resinand polymerized in an oven set at 608C for 24 h. Ultra-thin sections were cut with a ultramicrotome (Reichert,OMU-3) using a diamond knife and mounted on 50-mesh pioloform-coated grids. Sections were stained

with uranyl acetate and Reynolds lead citrate, exam-ined, and photographed using a transmission electronmicroscope (JEOL-1200 EX) at an accelerating voltageof 80 kV.

RESULTS

Five types of sense organs and secretary pores wereidentified using SEM and TEM on the dorsal and ven-tral stylets of the ovipositor of Venturia canescens(Gravenhorst). The sense organs discovered usingSEM were surface-dome sensilla (Figs. 1 and 2 SD),pitted-dome sensilla (Figs. 1 and 2 PD), and coeloconic

Fig. 1. Lower magnification SEM micrograph of the tip of the dorsal stylet showing the distributionand relative abundance of different types of sense organs present on the ovipositor stylets of Venturiacanescens. Scale bar 5 10 lm. PD, Pitted dome; SD, surface dome; SP, secretary pore.

Fig. 2. Higher magnification SEM micrograph of different types ofsense organs present on the ovipositor stylets of Venturia canescens.Scale bar5 10 lm. SD, surface dome; P, pore; PD, pitted dome.

Microscopy Research and Technique

2 Z.A. SHAH

sensilla (Fig. 3). TEM revealed two types of surface-dome sensilla: taste receptors (Figs. 4, 6, and 7) andtype II campaniform sensilla (Figs. 5 and 11). The tastereceptors consisted of two or three chemoreceptor den-drites and one mechanoreceptor dendrite. Pitted-domesensilla (Figs. 8 and 9) comprised four chemoreceptorsand one mechanoreceptor. A second type of campani-form sensillum, type I (Fig. 10), not detected using

SEM, was observed in ultrathin sections. Secretarypores (Figs. 1 and 2 SP) did not show any innervationwhen viewed using TEM. Therefore, a TEM micro-graph for secretary pores has not been presented. Themorphology of these sensilla was related to their histol-ogy in the following two ways: (1) serial sections of theexternal structures of the sensilla were examined andfollowed deep inside the ovipositor stylets; (2) theexternal morphology of pitted-dome sensilla or surface-dome sensilla was related to the structures found byTEM. The morphology and ultrastructure of five kindsof sensilla and secretary pores were discovered usingSEM and TEM on the ovipositor stylets of Venturiacanescens (Gravenhorst) and will each be addressedindividually.

Surface-Dome Sensilla

Surface-dome sensilla (Figs. 1, 2 SD, and 4), as thename indicates, were dome-shaped and occurred on thesurface of the dorsal and ventral stylets of the oviposi-tor. These sensilla were present in rows on the oviposi-tor stylets and were more numerous on the dorsal thanon the ventral stylets. The density of these sensilla washighest near the stylet tip and decreased toward theproximal end. Surface-dome sensilla were 1 lm in di-ameter and 1–1.4 lm in length. These sensilla were oftwo types: (i) taste receptors and (ii) type II campani-form sensilla. However, these types were indistinguish-able externally.

Taste Receptors

The transmission electron micrograph of the firsttype indicated that these were innervated by groups oftwo to four neurons represented by their respectivedendrites in the lumen of the stylets (Figs. 4, 6, and 7).One dendrite in almost every group was a mechanore-ceptor while the rest were chemoreceptors. Each den-

Fig. 3. SEM micrograph of the coeloconic sensillum (indicated byblack arrow) found on the ovipositor stylets of Venturia canescens.Scale bar5 1 lm.

Fig. 4. TEM micrograph of the longitudinal section of a surface-dome sensillum (taste receptor) found on the ovipositor stylets of Ven-turia canescens. Scale bar 5 0.1 lm. CD, chemoreceptor dendrite; p,pore (expected).

Fig. 5. TEM micrograph of the cross section of campaniform sen-silla type II (mechanoreceptor dendrite) found on the ovipositorstylets of Venturia canescens. Scale bar 5 0.1 lm. CS, cuticularsheath; DM, dendritic membrane; MD, mechanoreceptor dendrite;MT, microtubule.


3MORPHOLOGY ULTRASTRUCTURE OF THE SENSE ORGANS

drite of these sensory cells was surrounded by a dendri-tic membrane, and each group of dendrites wasenclosed by a cuticular sheath. The domes of these sen-silla seemed to possess a solitary pore where chemore-ceptor dendrites might end (Fig. 4).

Type II campaniform sensilla are discussed later.

Pitted-Dome Sensilla

Pitted-dome sensilla (Figs. 1 and 2) were present allover the surface of the ovipositor stylets especially onthe sides including the tip of the stylets and were the

most numerous of all the sensilla found. They weremost numerous near the distal end and decreased innumber toward the proximal end of the ovipositorstylets. They occurred in rows on the dorsal as well ason the ventral stylets, but were more numerous on thedorsal than on the ventral stylets. The pitted-domesensilla were present in oval pits and did not extendbeyond the surface of the ovipositor stylets. The ovalpits had maximum and minimum diameters of 1.74and 1.04 lm, respectively. The diameter of the externalprocess was 0.87 and 0.52 lm high. TEM revealed thatpitted-domes (Figs. 8 and 9) were innervated byapproximately five bipolar neurons represented bytheir respective dendrites in the lumen of the stylets.Each group of five dendrites comprised four chemo-receptors and one mechanoreceptor. Both types ofthese receptor dendrites possessed microtubules.Microtubules of the mechanoreceptor dendrites werearranged in a 9 1 0 pattern, while microtubules of thechemoreceptor dendrites were arranged irregularly.Each dendrite possessed its own dendritic membrane,and each group of dendrites was enclosed by a cuticularsheath. This cuticular sheath, in turn, was surroundedby supporting cells. The domes of these sensilla wereformed of thick cuticular walls consisting of darkspongy tissue over the dendrites of the neurons. Thewhole sensillum was present in a depression in such away that it did not protrude from the surface of the ovi-positor wall. The tubular body of the mechanoreceptordendrite could not be seen near the wall of the oviposi-tor stylets. Similarly, it was not possible in the presentstudy to detect any expected pore in the dome for prob-able taste reception using TEM.

Fig. 6. TEM micrograph of the cross section of groups of variablenumber of dendrites or taste receptors (surface-dome sensilla) foundon the ovipositor stylets of Venturia canescens. Scale bar 5 0.2 lm.CD, chemoreceptor dendrite; CS, cuticular sheath; DM, dendriticmembrane; MT, microtubule.

Fig. 7. TEM micrograph of the cross section of a group of twodendrites or taste receptors (surface-dome sensilla) found on the ovi-positor stylets of Venturia canescens. Scale bar 5 0.2 lm. CD, chemo-receptor dendrite; CS, cuticular sheath; DM, dendritic membrane;MT, microtubule.

Fig. 8. TEM micrograph of longitudinal section of the pitted-domesensilla seated on the ovipositor stylets of Venturia canescens. Scalebar 5 0.2 lm. CD, chemoreceptor dendrite; CS, cuticular sheath; D,dome; DM, dendritic membrane.


4 Z.A. SHAH

Coeloconic Sensilla

Coeloconic sensilla (Fig. 3) were least numerous ofall the sensilla present on the stylets of the ovipositorusually with only one occurring per ovipositor stylet.These occurred in deep pits and did not protrudebeyond the surface of the stylets. The pit consisted ofan outer circle with a maximum diameter of 3.53 lmand a minimum diameter of 2.47 lm and an innercircle with a maximum diameter of 1.41 lm and a mini-mum diameter of 1.06 lm. The external process ofthese sensilla possessed a smooth surface, roundedbody, and blunt tip. Pores could not be identified in theexternal process of these sensilla using SEM. Thesesensilla exhibited a uniform diameter (0.94 lm)throughout the length (1.18 lm) of their external pro-cess. These sensilla could not be detected in ultrathinsections.

Secretory Pores

Secretory pores (Figs. 1 and 2 SP) fell numerically inbetween the surface-dome sensilla and the pitted domesensilla and were more abundant on the dorsal than onthe lateral stylets of the ovipositor. Secretory poreswere oval in shape having a longitudinal slit (1.26 lm)in the center, which was either rectilinear or zigzag inappearance. Each secretory pore was surrounded bythree circles of depression relative to the surface of ovi-positor stylets. At their widest points, the diameters ofthese circles from outer to inner were 3.13, 2.61, and2.26 lm. The secretary pores occurred in rows on allthe stylets of the ovipositor. The rows of secretory poresalternated with the rows of surface-dome sensilla.These were found in highest density at the tip of thestylets and became less and less in number toward theproximal end.

Type I Campaniform Sensilla

Two types of campaniform sensillum were present inthe ovipositor wall of Venturia canescens (Grave-nhorst). The type I campaniform sensillum (Fig. 10)possessed a long and narrow tubular body and was�0.10 lm in diameter and 0.73 lm in length. A smallamount of spongy tissue was present around the tip inthe form of a thin band. This type of sensillum was in-nervated singly and was not discernible externally. Thedendrite of this sensillum seemed to possess a 9 1 0arrangement of microtubules and was surrounded by adendritic membrane. The membrane, in turn, wasenclosed by a cuticular sheath.

Type II Campaniform Sensilla

The type II campaniform sensillum (Fig. 11) was visi-ble externally in the form of raised domes that had asmooth surface. This smooth surface possessed a nar-row, deep depression at the central point of the tubularbody of the solitary mechanoreceptor dendrite. Campa-niform sensilla of this type possessed a thick cap of darkspongy tissue over the short, much expanded tubularbody �0.25 lm in diameter and 0.65 lm in length. Thecuticular wall of the dendrite of this type of sensillumpossessed infoldings that were not detected in the cam-paniform sensilla of the type I. This type of sensillumwas also innervated singly. The dendrites of these sen-silla possessed a 9 1 0 arrangement of microtubulesand were surrounded by dendritic membrane that, inturn, was enclosed by a cuticular sheath (Fig. 5).

DISCUSSIONSurface-Dome Sensilla

This is the first report of surface-dome sensilla inVenturia canescens (Gravenhorst). These sensilla pos-sessed one to four dendrites, and almost all these sen-silla exhibited one mechanoreceptor dendrite. Any

Fig. 9. TEM micrograph of cross section of the pitted-dome sen-silla seated on the ovipositor stylets of Venturia canescens. Scale bar5 0.2 lm. CD, chemoreceptor dendrite; CS, cuticular sheath; D,dome; DM, dendritic membrane; MD, mechanoreceptor dendrite.

Fig. 10. TEM micrograph of longitudinal section of campaniformsensillum type I found on the ovipositor stylets of Venturia canescens.Scale bar 5 0.2 lm. CS, cuticular sheath; DM, dendritic membrane;MD, mechanoreceptor dendrite; TB, tubular body.



additional dendrites of surface-domes were chemo-receptors, and the surface-dome sensilla with chemore-ceptor dendrites possessed a terminal pore. Thus, thesesensilla can be divided into two categories according totheir function. The first type is mechanoreceptors thatoccur with one, two, or three chemoreceptors endingnear a terminal pore that can be categorized as tastereceptors. Thus, these sensilla could be involved inhost-discrimination during oviposition. This type ofsurface-dome sensillum has not been described previ-ously for parasitoid wasps. The second type of surface-dome sensilla, a solitary mechanoreceptor neuron, canbe designated as a type II campaniform sensillum andwill be discussed later.

Pitted-Dome Sensilla

Pitted-dome sensilla are the most intensively studiedsensillum type found on the ovipositor stylets of parasi-toid wasps. This type of sensillum has been describedby King and Fordy (1970) in Cotesia glomerata L., Ves-pula vulgaris L., and Apis mellifera L. These authorsfound a depression in the center of the dome and sug-gested that, as these sensilla do not protrude out of thesurface of the ovipositor stylet, they were protectedfrom physical damage during stabbing. van Lenteren(1972) detected pitted-domes on the ovipositor of Pseu-deucoila bochei Weld using SEM and proposed a dis-criminatory function for them. Hawke et al. (1973) pre-sented details of the structure of pitted-dome sensillaon the ovipositor of Orgilus iepidus Muesebeck andstated that these sensilla were innervated by onemechanoreceptor cell and four chemoreceptor cells onthe dorsal stylets and five chemoreceptor cells on thelateral stylets: a terminal-pore was also present.Greany et al. (1977) also studied these sensilla usingSEM and TEM on the ovipositor of Biosteres (Opius)longicaudatus Ashmead and reported that these sen-silla possessed one chemoreceptor dendrite and onemechanoreceptor dendrite along with a terminal pore.Nenon et al. (1995) detected this type of dome on theovipositor of Apechthis compunctor Linnaeus. van Lan-teren (2007) reported similar types of sensilla on theovipositor of Leptoplina heterotoma (Thomson) possess-ing six dendrites, one of which was always a mechanor-

eceptor and the remaining five chemoreceptors. Theyassigned a dual function to these sensilla, that is,mechano- as well as chemoreceptive. Brown andAnderson (1998) and Quicke et al. (1999) found a simi-lar arrangement of dendrites in functionally similarbut morphologically different sensilla on the ovipositorof Trybliographa rapae (Westwood) and Aphelinusabdominalis (Dalman), respectively. Boring and Shar-key (2009) also noted these types of sense organs onthe ovipositor of Homolobus truncator (Say), but theyneither described any dendritic arrangement of thesesensilla nor assigned any function to them. Obonyoet al. (2011) observed this type of sensillum on the ovi-positor of Cotesia sesamiae (Cameron) and C. flavipes(Cameron) which were supposed to perform a similarfunction, but instead of having a single pore, a charac-teristic of gustatory sensilla, these sensilla possessedmany pores. Ganesalingam (1972) studied the pitted-domes of Venturia canescens (Gravenhost). He statedthat each sensillum possessed a group of three den-drites. On reaching the surface cuticle of the ovipositor,Ganesalingam (1972) proposed that the dendritesreduced in diameter by fusion of the surrounding mem-branes and that the terminal portion of the dendritescontained compactly arranged microtubules but didnot have a pore. This study suggests that the structureof pitted-domes described by Ganesalingam is actuallyderived from three types of sensilla: (1) the externalstructure shown in the SEM micrograph by Ganesalin-gam is that of pitted-dome sensilla described in thisstudy; (2) the internal structure comprising three den-drites described by Ganesalingam pertains to the sur-face-dome sensilla of this study; and (3) the compactarrangement of microtubules in the terminal part ofthe dendrite formed by fusion reported by Ganesalin-gam was actually part of the mechanoreceptor den-drites of campaniform sensilla. This study proposesthat the reduction in the terminal portion of the den-drites corresponds to single innervation of the campa-niform sensilla rather than the fusion of three den-drites. Thus, Ganesalingam’s structure of a pitted-dome sensillum seems to be synthesized from threesensillar types found on the ovipositor of V. canescens.Therefore, the theory put forward by Ganesalingam toexplain the mechanism of the function of pitted-domesensilla may be incorrect. It is suggested that thesesensilla act as taste receptors and are perhaps involvedin host-discrimination.

Coeloconic Sensilla

This is the first report of the occurrence of coeloconicsensilla on the ovipositor of Venturia canescens (Grave-nhorst). These sensilla also occurred on the ovipositorof Trybliographa rapae (Brown and Anderson, 1998)and Leptoplina heterotoma (van Lenteren et al., 2007);however, these were found in large numbers in theselatter two species but were few in number in this study.Nacro and Nenon (2009) observed these sensilla on theovipositor of Aprostocetus procerae (Risbec) on whichthey were also few number; the authors assigned nofunction to them. However, these sensilla do occur onthe antennae of a large number of hymenopteran para-sitoids (Miller, 1972; Norton and Vinson, 1974a,b;Lane et al., 1988; Navasero and Elzen, 1991; Butter-field and Anderson, 1994; Skilbeck and Anderson,

Fig. 11. TEM micrograph of longitudinal section of campaniformsensillum type II found on the ovipositor stylets of Venturia canescens.Scale bar 5 0.2 lm. CS, cuticular sheath; D, dome; DM, dendriticmembrane; DP, depression; MD, mechanoreceptor dendrite; TB, tubu-lar body.


6 Z.A. SHAH

1996; Meyhofer et al., 1997; Ochieng et al., 2000;Bleeker et al., 2004; Roux et al., 2005; Bourdais et al.,2006; Dweck and Gadallah, 2008). The coeloconic sen-silla found on the ovipositor of V. canescens fulfill thecriteria described for ‘‘poreless sensilla with inflexiblesockets’’ proposed by Altner et al. (1983) in that thesensilla are (i) low in numbers, (ii) recognized by thepresence of a peg, (iii) poreless, and (iv) surrounded byinflexible sockets. However, a fifth criterion that thesensilla are characterized by the presence of threetypes of sensory cells could not be fulfilled in this study,because these sensilla were not detected by TEM.These sensilla perhaps act as thermo-hygroreceptors.

Secretory Pores

Pores have been described by many authors on theovipositor of various hymenopterous parasitoids (Cop-land and King, 1971a in Chalcididae; Copland andKing, 1971b in Eulophidae and Tetracampidae; Cop-land and King, 1972a in Pteromalidae; Copland andKing, 1972b in Torymidae and Agaonidae). Fulton(1933) observed these pores on the ovipositor of Habro-cytus cerealellae Ashmead. King (1962) and King andRafai (1970) detected them on the ovipositor ofNasoniavitripennis Walker. These pores have also beendescribed by Ganesalingam (1972), but he did not sug-gest a possible function. The most probable function ofthese pores seems to be the one proposed by Lyngnes(1961) that these pores provide fluid to reduce frictionduring stabbing.

Type I and II Campaniform Sensilla

These types of sensilla have been described on theovipositor of Orgilus lepidus by Hawke et al. (1973)and Biosteres (Opius) iongicaudatus by Greany et al.(1977) and erroneously described on the ovipositor of V.canescens by Ganesalingam (1972) as a part of thestructure of pitted-dome sensilla. They were alsoobserved on the ovipositor of Trichogramma maidis(Pintureau and Voegel) (Le Relac and Wagnberg, 1990)and T. galloi (Zucchi) and T. pretiosum (Riley) (Consoliet al., 1999), where they act as mechanoreceptor dis-cerning the relative position of the ovipositor withinthe host. Chiappini and Solinas (2002) observed thesesensilla on the ovipositor of Anagrus breviphragma(Soyka), and Dweck et al. (2008) reported them on theovipositor of Hebrobracom hebitor (Say) to which theyassigned a tactile function. Nacro and Nenon (2009)described them on the ovipositor of Aprostocetus pro-cerae (Risbec) and Platygaster diplosisae (Risbec).Campaniform sensilla display a lot of variation in formand structure and can be detected on various parts ofan insect including the antennae (Dietz and Hum-phreys, 1971; Miller, 1972; Mclver, 1975; Alm andKurczewski, 1982; Lane et al., 1988; Navasero andElzen, 1991; Skilbeck and Anderson, 1996; Dweck andGadallah, 2008). In this study, two types of campani-form sensilla were found. Type I campaniform sensillawere not discernable externally and perhaps respondto pressure during stabbing, similar to the onesdescribed by Matushkina (2011) on the sting of Bembixrostrata (Fabricius). Type II campaniform sensillawere surface-domes, which may perform a mechanore-ceptor function when the ovipositor bends during ovi-position.

CONCLUSIONS

The morphology and ultrastructure of five types of sen-silla and secretary pores were described on the ovipositorof Venturia canescens (Gravenhorst) using SEM andTEM and possible functions proposed. Surface-dome sen-silla and pitted-dome sensilla were considered to performgustatory functions based on their innervation pattern.These two sense organs are the best candidates for host-discrimination. The arrangement of dendrites of type Iand II campaniform sensilla suggests that they act aspressure- and mechanoreceptors, respectively. The coelo-conic sensilla may act as thermo-hygroreceptors and sec-retary pores as lubricating structure during oviposition.

ACKNOWLEDGMENTS

Sincere thanks are due to A/Prof Paul Holford, Uni-versity of Western Sydney for reviewing the manu-script for language/grammatical and subject correc-tions, helpful suggestions, and advice. The author isthankful to the Pakistan High Commission, London forcontinued cooperation throughout the study period;and the Department of Higher Education, Governmentof Punjab for sanctioning study leave for the period ofthis work. The author is also thankful to Khurram Azizfor extending cooperation during the study period. Theauthor is also thankful to all those who remained help-ful during the period of this work. Any of the aforesaidsponsors did not have any role in study design; datacollection, analysis, and interpretation; or in the deci-sion to submit the article for publication. The author isalso thankful to the referees for their valuable com-ments and helpful advice due to which the manuscriptwas improved to a great extent.

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Documents

Morphology, ultrastructure, and probable functions of the sense organs on the ovipositor stylets of the hymenoptran parasitoid, Venturia canescens (Gravenhorst)