(ertle and davis) (hymenoptera : trichogrammatidae) - Science Direct

Inf. J. Insecr Morphol 4 Embryo/., Printed in Great Bntairt

Vol. 22. No. 5. pp. 507-520,

1993 0

0020-7322193 $6.00+ .oO 1993 Pergamon Press Ltd

ANTENNAL SENSILLA OF FEMALE TRICHOGRAMMA NUBILALE (ERTLE AND DAVIS) (HYMENOPTERA : TRICHOGRAMMATIDAE) AND COMPARISONS WITH OTHER PARASITIC HYMENOPTERA

D. M. OLSON and D. A. ANDOW Department

of Entomology,

University

of Minnesota,

(Accepted

1980 Fowell Avenue, St. Paul. MN 55108, U.S.A.

18 December

1992)

Abstract-We describe the external morphology and relative positions of antenna1 sensilla of female Trichgramma nubilale (Hymenoptera : Trichogrammatidae) by scanning electron microscopy (SEM), and compared the results with 11 similar studies representing 15 species and 8 families within the parasitic Hymenoptera. There are 6 morphologically and structurally distinct structures on female T. nubilale antennae, which are probably sensilla, and one seta and one campaniform-like structure that may have a sensory function. Sensilla pore numbers and positions suggests that the multiporous grooved basiconica (MPG) C, multiporous pitted (MPP) trichodea A and the MPP placodea A have an olfactory function, whereas the MPP trichodea C have a gustatory function. The lack of pores and the presence of a basal socket suggests a mechanoreceptor function for aporous (AP) trichodea B, and the uniporous pitted (UPP) trichodea D, although, the latter also have a minute pore or dimple at the sensillar apex. Positions and numbers of these sensilla, setae and campaniform-like structures were consistent in all the specimens examined. These analyses suggest that antenna1 sensilla types and relative positions are highly conserved within the genus Trichogramma, and there are broad similarities within the pamsitic Hymenoptera. Index descriptors

(in addition

to those in title):

Scanning

electron

microscopy.

INTRODUCTION

are minute endoparasitoids of eggs of insects, primarily Lepidoptera, and are used worldwide for biological control of pests in various crops (Stinner, 1977). Trichogramma nubilde was first discovered in Delaware (Ertle and Davis, 1975), and is a relatively efficient parasitoid of the European corn borer, Ostrinia nubildis (Htibner), egg masses (Hintz and Andow, 1990; Prokrym et al., 1992). Trichogrammatids examine host eggs by rapidly drumming their antennae on the egg or egg mass surface, a behavior found in many other parasitoids within the parasitic Hymenoptera, and individuals deposit one to over 30 eggs in each host egg, depending on the size and shape of the egg (Klomp and Teerink, 1962; Schmidt and Smith, 1985). The mechanisms behind host examination .snd resulting oviposition behavior are not completely clear, but some elucidation may be possible by descriptive and comparative analyses of the antenna1 sensilla of each species. TRICHOGRAMMATIDS

507

ANALYSIS

x(3)

x

X

X

x(3) x

x

x

AP trichodea

X

X

x(l)

x

41)

x

UPP trichodea

X

MPP trichodea C

1972

and Vinson, 1974a et al., 1978a

1987

Norton and Vinson, 1974a, b Norton and Vinson, 1974a Nasasero and Elzen, 1991 Richardson et al., 1972

Norton Borden

Cave and Gaylor,

Miller, 1972 Miller, 1972 Wibel et al.. 1984

Weseloh,

Barlin et al., 1981 Dahms. 1984

VoegelC et al., 1975 Schmidt and Smith. 1987

Source

Reported presence is designated with an ‘x’ and indicates that the sensillum is similar in morphology and external surface structure as those of T. nubilule. (1) = presence of pores is determined by wall porosity studies, (2) = presence of pores determined by TEM, and (3) = presence of pores determined by SEM and TEM. For others, we inferred pore presence based on sensillar morphology. AP = aporous, MPG = multiporous grooved, MPP = multiporous pitted, UPP = uniporous pit pore.

Coeloides brunneri

x

x(3) x

E(3) 43) x

x

:(l)

Braconidae Cardiochiles nigriceps Microplitus croceipes

x(2)

i(l)

41)

x

43) x

x

MPP placodea

Aphidiidae Aphidius smithi

Ichneumonoidea Ichneumonidae Campoletis sonorensis Itoplectis conquisitor

Proctotmpoidea Scelionidae Telenomus reynoldsi

x x x

Pteromalidae Nasonia vitripennis Peridesmia discus Nasonia vitripennis

41)

x

Encrytidae Cheiloneurous noxius

x

MPG basiconica

43) x

x

A

Trichogramma nubilale S~NSILLA WITHTHOSE REPORTED FROM 15 SPECIESRE~H~S~NTING 8 FAMILIESAND 3 SuPERFAh~ILIEs OF THE PARASITIC HYMENOPTERA

MPP trichodea

OF

Eulophidae Tetrastichus hagenowii Melittobia australica

Chalcidoidea Trichogrammatidae Trichogramma evanescens Trichogramma minutum

Species

TABLE 1. A COMPARA~VE

2

6

9

P ?

I? a

g co

Antenna1

Sensilla of Female

Trichogramma

nubilale

509

An insect sensillum consists of cuticular components, sensory neuron(s), and sheath cells (McIver, 1975). Insect sensilla have been identified and classified within the limits of resolution of light microscopy by gross external shape and mode of insertion on or in the body wall (Snodgrass, 1935; Schneider, 1964) and histological studies of the relative thickness and porosity of the cuticular walls (Slifer, 1969). More recently, pore structure and position using scanning electron microscopy (SEM) and transmision electron microscopy (TEM) has been proposed as criteria for sensillar classification, because in many cases these characteristics have been correlated with sensillar function (Altner, 1977). There are a few SEM studies of antenna1 sensilla of parasitic Hymenoptera (Table l), but comparisons among species is difficult, because not all of these are sufficiently detailed or complete. We describe the surface morphology and relative positions of sensilla on the antenna of T. nubilale to provide a basis for comparative analyses and insights into the roles these structures play in insect behavior. Such information would also facilitate studies using histological and electrophysiological techniques.

MATERIALS

AND

METHODS

Trichgramma mAilale were reared on eggs of European corn borer, Ostrinia nubilalis, at the University Minnesota Agricultural Experiment Station. The T. nubilale culture originated from field collections Delaware during 1987. The external surface structure of the female antenna was examined by SEM.

of in

Preparation for gros external antenna1 viewing Intact insects were chilled in a refrigerator for c. 15 min, then fixed by placing a drop of 2% osmium tetroxide in their container for c. 24 hr until vapor infiltration was evident by the black appearance of the insects. Examinations were made with a Philips 500 SEM at -160°C between 3.0 and 6.0 kV. Preparation for higher magnification viewing of the antenna1 sensilla and other cuticular structures (a) Insects were chilled and the antennae or heads were removed, while immersed in a drop of 3% glutaraldehyde. They were subsequently fixed in 3% glutaraldehyde in 0.1 M sodium cacodylate buffer. pH 7.2, with 5% sucrose for 1 hr, and post-fixed in 0.2 M sodium cacodylate buffer (pH 7.2) and 2% osmium tetroxide for 1 hr. Saecimens were dehydrated with CO* from absolute ethanol, sputter-coated with c. 6 nm of platinum and viewesd with a Hitachi S-900 field emission SEM between 1.0 and 3.5 kV. (b) Several specimens were prepared as in the intact insect method and dehydrated with CO* from absolute ethanol. After sputter-coating with c. 6 nm of platinum, they were viewed with a Hitachi S-900 field emission SEM between 1.0 and 3.5 kV or a Hitachi S-4000 field emission SEM between 1.0 and 5.0 kV. (c) The heads or antennae were removed from chilled insects, air-dried and sputter-coated with c. 2.5 nm of gold and viewed unsder an ISI-DS 130 Akashi SEM at 5.0 kV. Examinations were made of dorsal, lateral or ventral antenna1 surfaces by positioning specimens on the stub so that the desired surface was exposed. The total number and position of each structure were verified by observations on approximately 10 antennae at magnifications between 350 and 30,000 X. Verification of the similarity of structures at different positions was made by examination of the structures at higher magnifications (ranging from 30,000 x to 150,000 x). Approximately 40 antennae were examined in this manner and a representative photomicrograph was taken of each structure. The terminology of Snodgrass (1935) and the criteria proposed by Altner (1977) and elaborated upon for SEM by Zacharuk (1980) were used in combination for the sensillar descriptions; each one by itself does not distinguish variation in sensilla sufficiently to be used on its own in a descriptive and comparative analysis with SEM. Specimen preparation Specimen preparation and viewing techniques have profound effects on the images resolved, often causing similar structures to appear very different. The appearance of a socket at a sensillar base that is really nonsocketed may be apparent simply because this area “sinks”, probably due to shrinkage during air or vacuum drying, and a depr’ession resembling a socket results. The morphology of sensillar insertions can also be distorted because of partial structural collapse. In this case, sensilla appear elevated at the base although the base is actually flush with the antenna1 surface. Both of these preparational artifacts were observed during this

510

D. M. OLSON and D. A.

ANDOW

b

f

t d

Fro. 1. Right antenna of female. Trichogramma nubilale. A. Dorsal view; B. lateral (interior) view: C. ventral view. Fl = first fiagellomere; F2 = 2nd flagellomere; F3 = 3rd flagellomere; F4 = 4th flagellomere; F5 = 5th flagellomere; P = pedicel; SC = scape. a = Campaniform-like structure: b = MPG basiconica A: c = UPP trichodea D: d = MPP trichodea C; e = AP trichodea B; f = MPP trichodea A; g = MPP placodea A. A-C = x 625; a-f = x 5000.

study (unpublished data), and the first type of artifact may be present for most of the multiporous grooved basiconica reviewed (Weseloh, 1972: Norton and Vinson, 1974a and b; Cave and Gaylor. 1987). The sensillar structures are also affected; for example, the multiporous pitted (MPP) placodea can appear blunt tipped with ridges along the sides that are not very apparent (Fig. 10). or pointed at the tip with deep ridges along the sides (Fig. 11). Differential dehydration or fixative infiltration levels may be responsible. Results of viewing several sensilla at various angles using standardized preparation techniques indicated that the MPP placoidea sensilla of T. nubdale are not superficially different. The first method for relatively lower magnifications and the first method for higher magnifications proved to be the most effective methods for viewing and describing the antenna1 structures.

Antenna1

Sensilla of Female

Trichogramma

nubilule

511

FIG 2. Type A and type B basal insertions. Scale bar = x 1.08 pm, x 7780. FIG. 3 Type C basal insertion of MPP trichodea C. Scale bar = 2.20 pm, X 5850. FIG. 4. Type D basal insertion of UPP trichodea D located at the antenna1 apex. Scale bar = 0.90 km, x 25,000. FIG. 5. External surface structure of AP trichodea A. Scale bar = 660nm, X 46,000. FIG. 6. Apex and external surface structure of UPP trichodea D. Scale bar = 600 nm, x 50,000.

RESULTS

AND

DISCUSSION

Antenna The antenna of female Trichogramma nubilale is 7-segmented, and comprised of a scape, pedicel and 5 flagellomeres (Fig. 1). The first flagellomere (Fl) is very short and cylindrical. The closely joined F2 is triangular and overlaps F3 when viewed from a lateral perspective; it is not visible from a ventral perspective, and is longer than Fl when viewed dorsally. F3 and F4 are cylindrical and about as long as they are wide. F5 is the clava and tapers apically. VoegelC et al. (1975) refer to Fl and F2 and F3 and F4 as “funicles” in their description of the antenna of female as “anneli”, T. evanescens.

512

D. M. OLSONand D. A. ANDOW

Sensillar structure For this study, a total of 6 types of sensilla plus a seta and a campaniform-like structure, each possibly having a sensory function, were found on the antenna of female T. nubilale. For the comparative analysis, similar studies of antenna1 sensilla for other members of the parasitic Hymenoptera were reviewed for external surface structure and positional similarities with those of T. nubilale. The reviewed sensilla were grouped (Table 1) based largely on our inference from the published photomicrographs. The fine external surface structure of sensilla could not be discerned from the published photomicrographs; however, for 11 sensilla from 7 species (Table l), the presence and positions of a pore(s) was determined by histological studies using light microscopy (Slifer, 1969), TEM (Norton and Vinson, 1974a and b; Barlin and Vinson, 1981) or a combination of TEM and SEM analyses (Richardson et al., 1972; Norton and Vinson, 1974a and b; Borden et al., 1978a; Barlin et al., 1981) and was used as a basis for comparison. The sensillar positions were considered similar to T. nubilale, if they were restricted to the same antenna1 surfaces (i.e. dorsal, ventral and lateral) because antenna1 segmentation varied greatly, ranging from 3 to 36 flagellomeres. The trichodea subtypes, described below by their basal areas, could not be distinguished in the previous published studies, because in most cases the basal areas were not discernible; the comparative analysis was based only on those similarities that could be found in sensillar morphology, surface structure, and relative position. Aporous (AP) sensillar trichodea B. Snodgrass (1935) designated sensilla trichodea as setiform or “hairlike”. We distinguished sensilla trichodea as having a ratio of the diameter (at the widest point along the sensillar length) to the length (measured from the base to the tip of the sensillum) of less than 0.30. A ratio greater than or equal to 0.30 describes a sensilla basiconica. We further distinguished sensilla trichodea subtypes by their type of insertion on the antenna1 surface which may reflect their range of articulation. The AP sensilla trichodea of T. nubifale have a type B basal insertion and can be found on the scape, pedicel and all flagellomeres (Fig. lA, lB, lC, le). Type B basal insertions (Fig. 2B) are sockets with the top ridge of the socket not elevated from the body wall, and they have a ratio of the diameter of the sensillum at the base to the diameter of the socket opening (measured from the interior edges of the opening) of greater than or equal to 0.50 (sensilla trichodea B). They are dispersed along the length of the scape where their number varied between 18 and 24. The pedicel has a total of 6 of these hairs, 3 located on the dorsal, one on the ventral, and one each on the 2 lateral surfaces of this segment. There is one hair on the interior lateral surface of Fl, one on the interior lateral surface of F3 and one on the dorsal surface of F4. F5 has 2 located on the proximoventral half of the flagellomere interspersed with many nonsocketed setae, and there are 2 more located dorsally near the apex. Along the interior lateral surface of F.5, is a linear arrangement of 4 sensilla with the most apical being more slender and curved than the others. There are variations in the size and curvature of these sensilla, but the surface structure for both types is the same as the nonsocketed seta shown in Fig. 5; there are grooves along the longitudinal axis of each structure and both lack pores. This is the only type of sensilla found on the scape and pedicel. All other studies of the parasitic Hymenoptera report the presence of AP sensilla trichodea, except those in the Pteromalidae (Miller, 1972; Wibel et al., 1984), and the

Antenna1 Sensilla of Female Trichogramma nubilale

513

Ichneumonid, Itoplectis conquisitor (Borden et al., 1978a) (Table 1). For the latter groups, these sensilla may have been present but not reported. In the other species, these sensilla are found on all flagellomeres, including the scape and pedicel, and are much more numerous than they are in T. nubilale. T. minutum has a total of 5 of these hairs on the pedicel and 17 hairs on the scape (Schmidt and Smith, 1987). The morphology, external surface structure and relative positions are similar for T. evanescens (VoegelC et al., 1975) and ir. nubilale. The AP sensilla trichodea B are likely mechano-hair sensilla, which are usually tactile receptors, but they may also perceive air-borne vibrations (McIver, 1975). The several hairs that are somewhat linearly arranged along the interior lateral surface of the antenna on all flagellomares in T. nubilale, are not located on the lateral exterior surface of these flagellomeres, which suggests that they may have a function related to their position. The contact of these sensilla from each antenna could provide the wasp with information about the relative position of their antennae which may be important in their searching behavior. It is not known if a similar arrangement is present elsewhere in the parasitic Hymenoptera. Hairplates on the scape-head and pedicel-scape joints of T. minutum are likely to be involved in detection of antenna1 depression and extension, respectively (Schmidt and Smith, 1986). VoegelC et al. (1975) distinguished the relatively slender and somewhat curled sensilla trichodea at the antenna1 apex as a unique sensilla type. We do not make that distinction, because the morphology and external surface structure of these sensilla are the same in other respects to AP sensilla trichodea B, and curvature sometimes occurs during preparation and/or drying where the sensilla may otherwise be straight in the living state. Uniporous pit pore (UPP) sensilla trichodea D. Zacharuk (1980) distinguished 2 types of uniporous (‘UP) sensilla; those with a simple pit pore (UPP) and those with a sculptured porous point (UPS). The latter have several cuticular ridges or finger-like projections visible at the pore. This UPP type of sensillum was found at the apex of the antenna (Fig. lA, lB, lC, lc). The single pore or dimple is located at the ventroposteriorly directed apex of the sensillum (Fig. 6). The wall of the sensillum has ridges and no pores are evident. This sensillum has a Type D basal insertion that appears membranous and is segmented ventrally, is continuous with the antenna1 wall dorsally, and has a ratio of the diameter of the sensillum at the base to the basal insertion diameter (as measured from the edges of the apparently membranous ventral area) between 0.35 and 0.40 (Fig. 4). A total of 6 studies reports the UPP sensilla trichodea D (Table l), but variations in the structure of basal insertions and sensillar locations are apparent. Some basal areas appear variably elevated (Miller, 1972; VoegelC et al., 1975), and others appear less elevated but have a distinct ring-like socket around the sensillar base (Norton and Vinson, 1974a, b). All of these sensilla have longitudinal ridges, and all have relatively blunt tips that project posteriorly. It was not possible to determine from the photomicrographs of the respective studies whether these structures are of the UPP or UPS type as described by Zacharuk (1980), or aporous. These sensilla in the Ichneumonoidea project perpendicularly from the antenna1 surface. They are found on all flagellomeres of males and females and are relatively numerous especially at the distal area of these segments. For female T. evanescens and the males and females of Pteromalidae, they are located at the apex and ventrally on the distal flagellomeres

514

D. M. OLSON and D. A. ANDOW

FIG. 7. Lateroventral view of MPP trichodea C. Scale bar = 860 nm, x 35,000. FIG. 8. Apex and external surface structure of MPP trichodea A. Scale bar = 660 nm, x 45,000. FIG. 9. Apex and external surface structure of MPP placodea A. Scale bar = 1.00 pm, x 30,000. FIG. 10. Apex and external surface structure of MPP placodea A. Scale bar = 1.50 p,m, x 20,000. FIG. 11. Lateral view of MPG basiconica C. Scale bar = 1.20 urn, x 25,000. FIG. 12. A campaniform-like structure found on F2, F4 and F5. Scale bar = 1.65 km, x 20,000.

(Miller, 1972; Voegele et al., 1975; Wibel et al., 1984). This sensillum is not present at the apex of male Trichogramma although it could be elsewhere on their antennae. The UPP sensilla D are probably mechanoreceptors and possibly contact chemoreceptors. The pore at the sensillar apex is very small (approximately 57 nm diameter) and could be a dimple in the cuticle arising from the molting of the insect. The socket appears to restrict the lateral and dorsal movement of the hair, which may maintain the hair in important positions for substrate examination. Multiporous pitted (MPP) sensilla trichodea C. Multiporous sensilla are distinguished by the position of the pores along the sensillar wall (Zacharuk, 1980); multiporous pitted (MPP) types have pores distributed relatively uniformly along the walls of the sensillum, whereas multiporous grooved (MPG) sensilla have pores located within longitudinal grooves present along the length of the sensillum. The MPP hairs of T. nubilale occur on the ventral surface of F.5 where they are distributed throughout approximately half of the


515

distal area of the segment (Fig. lC, Id). The hair is recurved and laterally flattened with oblique grooves but no pores are evident in these areas. Pores are located along the outer margin (Fig. 7) of the hair and come into contact with the substrate as the female exhibits drumming behavior. The hair at the base has a reduced diameter and inserts in a type C base, which is a shallow socket that appears membranous and has a ratio of the diameter of the sensilla at the base to the diameter of the apparently membranous area of less than or equal to 0.30 (Fig. 3). The morphology and locations of the MPP sensilla trichodea C correspond with those reported by Voegele et al. (1975) for T. evanescens. No other studies on the parasitic Hymenoptera report this sensillar type. The MPP sensilla trichodea C are likely to be both mechanoreceptors and contact chemoreceptors. The constriction at the base of the sensilla suggests increased flexibility (McIver, 1975) and may be involved in the detection of fine physical characteristics, such as discrimination between individual eggs within an egg cluster. The variation in the number of hairs is both size and species specific (unpublished data), and may help to explain differences in the ability of different Trichogrurnma species in handling hosts that are highly clustered. The large numbers of sensilla increase the spatial density of chemical reception and could be useful in detecting chemical marks present on hosts that have been parasitized. Multiporous pitted (MPP) sensilla trichodea A. A type A basal insertion (Fig. 2) is continuous with the body wall, and has a ratio of basal insertion diameter to the diameter of the sensilla at the base of 1.0. For T. nub&de, these MPP sensilla have a type A basal insertion (Fig. Z!) and have relatively few pores (approximately 3 per pm2), which are evident on the surface along the length of the sensillum (Fig. 8). There are 8 of these sensilla evenly dispersed on the dorsal surfaces of F5 (Fig. lA, lf). The morphology and antenna1 positions of the MPP sensilla trichodea A in T. nubilule are the same as those for T. evanescens (Voegele et al., 1975); the latter report that these sensilla are inserted into basal sockets, but these sockets are not apparent in their photomicrographs. The similarity in morphology and antenna1 position of this sensillar type to those of T. nubilule suggests that the basal area of these sensilla of T. evanescens may need to be reexamined. The MPP sensilla trichodea of the males and females of the Pteromalids are more numerous than those of T. nub&de and are found on all sides of the flagellomere. In the Ichneumonoidea, the MPP sensilla trichodea are few in number and are located dorsally on the antenna for females and they are more numerous and located on the entire surface of each flagellomere of the males. For Cardiochiles nigricepes, these sensilla insert in a socket with the edges of the socket flush with the antenna1 surface (Norton and Vinson, 1974a, b). This sensillum type may be similar to the relatively longer types found on all flagellomeres of male Trichogrumma (unpublished data). The presence of pores suggests that these hairs may function in olfaction. They are more numerous and have a wider distribution on male T. nubiZale antenna suggesting that the male is more sensitive to the chemical source. Possibly, these sensilla are involved in the identification and location of females. Multiporous pitted (MPP) sensilla placodea A. Placodeal or plate type sensilla vary in shape, elevation above the antenna1 surface and basal areas in the Hymenoptera (Snodgrass, 1935). They may also be attached to the antenna1 surface throughout their

516


length, or they may be free from the antenna1 surface for as much as one half of the sensillar length (Barlin and Vinson, 1981). There is a total of 5 MPP plates on the distal half of the F5 segment of each antenna of T. nubilale, 2 on the interior and 2 on the exterior lateral surfaces, and one on the mid-dorsal surface (Fig. lA, lB, lg). The ventrolateral and the dorsal plates are located at the same relative position along the longitudinal axis of the flagellomere, and extend along the distal half of the flagellomere. The dorsolateral sensilla are located slightly more distally than the other 3 (Fig. 1A). There are numerous pores on the surface (approximately 28 per km2) that are present along the length of the sensilla (Figs 9, 10). There are also numerous ridges along the length, which are more evident proximally and whose resolution varies depending on preparation and viewing techniques (Fig. 10). Studies carried out using similar preparation techniques and comparing similar angles of view along the plate length, indicate that the surface structure of all 5 MPP placodea are the same. Our results indicate that there is only one type of sensillum placadeum present on the antenna of T. nubilale, and this type corresponds to the MPP type of Zacharuk (1980). Approximately the terminal 1/20th of the length of the plate is separated from the antenna1 surface. The MPP and MPG plate sensilla classified by SEM study (Zacharuk, 1980) could not be distinguished for the studies reviewed. However, Barlin and Vinson (1981) compared the wall thickness and pores of the multiporous plate (MP) sensilla of several species in the Chalcidoidea. They refer to type I and type II MP placodea, which, based on their descriptions from TEM analyses, correspond to variants of our observed MPP type. In their study, MP sensilla occurred on almost every flagellomere of the species studied, and the distal end of each sensillum was free in all species. They found that type I MPP have a relatively thin porous plate and many pores (approximately 10 per km2), and type II MPP have a thicker porous plate and fewer pores (approximately 4 per pm2). We found the density of pores on the MPP sensilla placodea of T. nubilale to be much higher (28 per pm2), and this density appeared conserved for this sensillum type. No explanation can be given for this difference in pore density between these MP sensilla. For most species in the study by Barlin and Vinson (1981), the MP sensilla are equidistant from each other, except those of Anagyrus pseudococci (Encrytidae), which are more numerous on the dorsal surface. Wibel et al. (1984) determined, by freeze fracture techniques, that female N. vitripennis have type I MP and type II MP placodeum as described by Barlin et al. (1981)) but they found the pore density of the former to be 20 per pm2 and the pore density of the latter to be 9 per Fm2. Males have a unique type III MP placodeum with a pore density of 15 per pm2. The MP sensilla of T. evanescens reported by Voegele et al. (197.5), are similar in morphology and location to the MPP sensilla placodea of T. nubilale. The Ichneumonoidea have multiporous plate sensilla, but they are attached to the antenna1 surface throughout their length (Table l), and they are numerous and distributed uniformly around the circumference on all the flagellomeres. The symmetrical distribution of the MPP sensilla placodea for all species analyzed suggests that they may be used to orient the wasp to a chemical source, possibly serving to detect long-range attractants from the host or host habitat as has been suggested by Doutt (1964). Multiporous grooved (MPG) sensilla basiconica C. These sensilla resemble bulbs on stalks. The basal area appears to be a type C and was measured as such (Figs 3, 11);

Antenna1

Sensilla of Female

Trichogramma

nubilale

517

however, there appears to be a narrow apparently membranous area closely surrounding the sensilla base (Fig. ll), which may determine the articulation range of this sensillar type. Pores occur within the longitudinal grooves on the bulbous portion of this structure (Fig. 11). Each sensillum has 10 grooves. There is a total of 7 such sensilla on each antenna (Fig. LA, lB, lC, lb). Four sensilla are located dorsally with one on F3 and F4, and 2 on F5. Two MPG sensilla basiconica C are located laterally; there is one sensillum located on the interior lateral surface of both F4 and F5. One sensillum is located on the ventral surface near the apex of F5. Both the dorsal set of 4 and the lateral set of 2 are arranged linearly along the longitudinal axis of the antenna. Similar structures were reported for all parasitoids in the studies reviewed, except for I. conquisitor (Elorden et al., 1978a) and Coeloides brunnei (Richardson et al., 1972) in which they may have been present but not reported (Table 1). The morphology and antenna1 positions of these structures in T. nubilale are the same as those of T. evanescens (Voegele et al., 1975). In other parasitoids, there is one such sensillum per flagellomere, and for Microplitus croceipes they are arranged linearly on the dorsal surface along the longitudinal axis of the antenna (Norton and Vinson, 1974a). In other species of parasitoids, the MPG sensilla basiconica are located dorsally (Weseloh, 1972; Norton and Vinson, 1974a), dorsolaterally (Norton and Vinson, 1974a, b; Dahms, 1984), laterally (Cave and Gaylor, 1987), or apicoventrally (Cave and Gaylor, 1987). The Pteromalidae are unique in that female N. vitripennis has several MPG basiconica per flagellomere and they are arranged in a single row along the lateroventral surface of each of F3-Fll, and the male has one MPG sensillum basiconicum on the lateroventral surface of F4-F10 (Miller, 1972), although, Wibel et al. (1984) did not find this sensillum type on F5. Males and females of Peridesmia discus have one MPG sensillum basiconicum per flagellomere beginning with one on the dorsal surface of F6, and successive sensilla spiral around the antenna and terminate on the ventral surface of the most distal flagellomere. The protectiv’e positions of these porous sensilla suggest that they are receptors of airborne chemicals. They may also function as thermo- and/or hygrosensitive sensilla, because temperature sensitive receptors have been observed with MPG chemical receptors, althcugh it is not possible to identify these types by their general external appearance (Abner and Loftus, 1985). Campaniform-Eike structures. There are 3 very small (680 nm diameter) mushroomshaped structures on the antenna. Each structure is inserted in a socket, and they appear to have a pore at the apex (Fig. 12). One of these structures is located medially on the lateral exterior surface of F2, one is located dorsolaterally on the distal surface of F4, and one is located on the proximoventral surface of F5 (Fig. lA, lC, la). Similar campaniform-like structures were reported for N. vitripennis and P. discus (Miller, 1972; Wibel et al., 1984) where they are closely associated with the MPG basiconica. Aporous (AP) setae A. Setae are “hair-like” or setiform structures that lack pores and a basal socket and are therefore not considered to have a sensory function. These setae have a type A insertion (Fig. 2), but otherwise in shape and surface structure they are the same as trichodea B illustrated in Fig. 5; the structures are sharply pointed at the tip, lack pores and are grooved longitudinally. AP sensilla trichodea B, however, are more subject to electrostatic charging, possibly because they are less dense internally. The

D. M. OLSONand D. A.

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ANDOW

setae are relatively and variously numerous around the circumference of F3 and F4 and the proximoventral and proximolateral surfaces of F5 where they extend along approximately half of the length of the flagellomere. It is not known if these structures are sensory receptors: no pores were observed by SEM even at 150,000 x magnification. The AP setae may have a protective function if they do not have a sensory function. Histological studies of these structures and the campaniform-like structures of unknown typology would aid in the elucidation of their function. The latter types may be stress receptors, dermal glands with an exuvial pore, or they may be vestigial MPG sensilla basiconica (an inference made because of their similarities in basal morphology and relative positions).

CONCLUSION For the species reviewed, many similarities in sensillar morphologies to those of T. nubilde have been found, and in most of these cases the sensilla are located at similar relative positions on the antenna and surfaces of the flagellomeres as those of T. nubilule. Exceptions to this are found for the reported locations of the UPP trichodea of the Ichneumonoidea, the placodea types, which varied even within the Chalcidoidea, and the antenna1 positions of the MPG sensilla basiconica of the Pteromalidae. The Trichogrammatids appear to vary little in the positions of their antenna1 sensilla (unpublished data); however, it is difficult to make extensive comparisons with this study. The parasitoids that have been studied vary in their pattern of host usage. The groups consist of endoparasitoids of eggs and larvae, ectoparasitoids of larvae and one is a primary hyperparasite. They further vary in oviposition behavior; some lay eggs singly, others lay many eggs in one host, some are host specialists, and others are more catholic in host acceptance. Most of the insects reviewed exhibit antenna1 drumming behavior. With knowledge of the biology of the insect, and a more thorough analysis of sensillar morphology, surface structure and positions in each species, it may be possible to use functional morphology to elucidate patterns that provide insights into the roles these sensilla play in the behavior of the insects similar to the work on host curvature measurement by T. minutum (Schmidt and Smith, 1986,1987,1989). T. nubilale sensilla, and their general pattern of similarity to other parasitic Hymenoptera suggest that additional studies and refinement of resolution of sensilla types could provide very useful information for descriptive and comparative analyses, especially for minute insects. Acknowledgements

- We thank Rod Kuehn, Electron Microscopy Laboratory, Department of Biology, University of Minnesota, for his instruction on the use of the SEM. We thank Gib Ahlstrand, Department of Plant Pathology, University of Minnesota, for the photomicrographs of the frozen specimens. We are very grateful to Chris Fretham, Department of Cell Biology and Neuroanatomy, University of Minnesota, for his invaluable advice and assistance in the employment of alternate specimen preparation and microscope techniques illustrations Funding Legislative Trust Fund.

for obtaining the electron micrographs. We also thank Atilano Contreras-Ramos for the and Roger Blanik and Catherine Reed for their comments on the manuscript. for this project has been approved by the Minnesota Legislature Subd. 6(a) as recommended by the Commission on Minnesota Resources from the Minnesota Environment and Natural Resources This is publication 19,958 of the Minnesota Agricultural Experiment Station.


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