Sensilla on the antennae, mouthparts, and body of the larva of the alfalfa weevil, hypera postica (gyllenhal) (Coleoptera : Curculionidae)

Int. J. Insect Morphol. & Embrvol., Vol. 12, No. 5/6, pp. 261 Io 272, 1983. Printed in Great Britain.

SENSILLA

ON THE ANTENNAE,

MOUTHPARTS,

THE LARVA OF THE ALFALFA (GYLLENHAL)

0 0 2 0 - 7322/83 $3.00 + .00 1983 Pergamon Press 1 td.

AND BODY OF

WEEVIL, HYPERA POSTICA

(COLEOPTERA

• CURCULIONIDAE)

R. G. BLAND Biology Department, Central Michigan University, Mt. Pleasant, MI 48859, U.S.A. (Accepted 14 March 1983)

Abstract--The morphology of the antennal complex, major mouthpart sensilla and body sensilla of alfalfa weevil larvae, Hyperapostica (Gyllenhal) (Coleoptera : Curculionidae), is described. All instars have a short l-segmented antenna with a large, multiporous sensillum basiconicum (s.b.) on its apex. Surrounding the s.b. are 2 unusual sensilla auricularia, and 3 small s.b., 2 of which are uniporous. The galea of the maxilla contains 11 s.b. and the apex of the palpus bears 12 thick-walled, uniporous s.b. The labial palpus has I0 similar s.b. apically. First-instar larvae have long, rodlike sensilla with a large, thick-walled bulbous apex; they are probably mechanoreceptors. The other 3 instars bear unusual nodulated and ridged sensilla with thin walls and a fragment-filled lumen. Sensilla on the apex of the thoracic legs and prolegs are also illustrated. Index descriptors (in addition to those in title): Chemoreceptors, contact chemoreceptors, labium, maxilla, mechanoreceptors, morphology, olfactory chemoreceptors, sensilla, sensilla auricularia, sensilla basiconica, sensilla trichodea. INTRODUCTION

THE ADULT alfalfa weevil, Hypera postica, is able to locate alfalfa, alfalfa volatiles and water vapor through olfactory and gustatory senses and long-wavelength photoreceptors (Byrne and Steinhauer, 1966; Springer and Pienkowski, 1969; Meyer and Raffensperger, 1974 a,b; Meyer, 1977; Bland, 1979). The adult's antennae consist of a variety of chemoand mechanoreceptors involved in food detection (Bland, 1981). However, similar morphological information on the antennae of alfalfa weevil larvae is not available, nor is any literature on the morphology of larval mouthpart and body sensilla relative to feeding behavior. The lack of work with receptors on alfalfa weevil larvae might be partly attributed to the minimal searching necessary for larvae to locate food. First-instar larvae hatch from eggs deposited in the pith of an alfalfa stem and exit the stem's interior to move toward the expanding buds at the stem apex. The larvae feed concealed under developing vegetative or floral parts of the buds. Second-instars generally feed externally on more developed leaflets, although some remain inside the buds. The 3rd and 4th instars feed externally on developing and mature leaflets. This study describes the external and internal morphology of the antennal complex and the major mouthpart sensilla that alfalfa weevil larvae use to detect suitable food sources. Several types of body and leg sensilla are also described. MATERIALS

AND

METHODS

Larvae for scanning electron microscopy were fixed by 3 different procedures: (I) boiling water (30 sec) - 4°/o glutaraldehyde (4 h r ) - 10°70 boiling KOH (30 sec) (Petralia el al., 1979); (2) D M P - e t h a n o l (I : 3 for 3 hr) 261

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(Bjerke et al., 1979); and (3) 4°//o glutaraldehyde (4 hr). Graded ethanol was used for dehydration and all specimens were critical-point dried in CO: and sputter-coated with 20 nm of gold-palladium. An AMR-1200 SEM was used for observations. None of the 3 fixation procedures produced consistently superior results over another. Specimens for transmission electron microscopy were fixed in 5% glutaraldehyde buffered in 0.2 M sodium cacodylate, postfixed in 1% OsO~ in 0.2 M sodium cacodylate and dehydrated in graded acetone. Specimens were embedded in Spurr's low viscosity medium (Spurr, 1969) with propylene oxide as the solvent. Sections were double-stained in uranyl acetate and lead citrate and examined with a Philips-300 TEM. Measurements of sensillar length were made by orienting sensilla lengthwise to reduce foreshortening errors, and averaging values from 10 or more sensilla of each type. All measurements are from the last (4th) instar unless otherwise noted. RESULTS

The relative positions of the antennae, ocelli, mouthparts, and numerous sensilla trichodea on the head capsule are shown in Fig. 1. Antenna Each antenna is a short, bulbous protuberance (Fig. 1) with a complex of 6 sense receptors on its blunt apex. The largest receptor is a broad-based, non-socketed sensillum basiconicum that ranges from 22 ram (lst-instar) to 45 ram (4th-instar) in length (Fig. 2). The surface is faintly pockmarked with pores (Fig. 3). The basal ½ is thick-walled with up to 10 wall layers visible. Distally, the inner wall region changes into fingerlike projections of varying widths which radiate inwardly (Fig. 4). Pores are visible along the periphery of the wall and indicate that this large s. basiconicum is a multiporous, olfactory receptor. Partially surrounding the large basiconic sensillum dorsolaterally are 5 (rarely 6) short, satellite sensilla (Fig. 2). Sensilla 1 and 2 present an unusual auriculate shape. Sensillum 1 (Fig. 5) is ca. 14 ram long and a very broad, shallow channel extends along the distal j of the sensillum's length. Sensillum 2 is ca. 12 ram long and has a very similar shape. The sensilla do not insert into a socket. The wall lacks pores and averages 0.7 ram in width near the middle region of the sensilla. The lumen is filled with a relatively homogeneous, electron-dense material containing dark, scattered granules. Sensilla 3 and 5 (Fig. 2) are similar thick-walled, basiconic pegs that taper apically to a blunt point. Sensillum 3, including its broad and raised base, is 7 lam long and sensillum 5 is 5 ram long; both contain an apical pore and at least 2 dendritic branches. Sensillum 4 (Fig. 2) is a 4 lam long basiconic receptor that is greatly tapered above its broad base. No apical pore was observed and the lumen contained electron-dense, flocculent material with no evidence of dendrites. A rare 6th sensillum was very similar to sensillum 5 and occurred adjacent to it. Maxilla The elongated stipes with 3 long sensiila trichodea narrows to a 2-segmented palpus and a stout galea, the latter with 11 sensilla basiconica ranging from 5 to 25 ram in length (Fig. 6). These sensilla are either relatively slender and gradually taper to a sharp point, or stout and taper apically to a blunt or trifurcate point. They are inserted into sockets, which suggests that some movement is likely. The sensilla of each galea are transversely oriented to the anterior face of the head indicating that they probably act as mechanoreceptors and chemoreceptors as they contact food moving toward the mouth cavity. The apex of the maxillary palpus bears 12 stout sensilla basiconica ranging from 2.5 to 5 ~tm in length (Fig. 7). Eleven sensilla form an irregular ring around the slightly broader central peg. A terminal pore was faintly resolved in a few sensilla and dendritic branches were observed in most sensilla.

Sensilla on the A n t e n n a e , M o u t h p a r t s , a n d Body o f the L a r v a o f the A l f a l f a Weevil

Ft(;. 1. F r o n t a l view o f head o f a l f a l f a weevil larva, a - a n t e n n a ; I - l a b i u m ; lb - l a b r u m ; m = maxilla; m d = m a n d i b l e ; o - ocellus. Fl(;. 2. A n t e n n a l c o m p l e x , a - large sensillum b a s i c o n i c u m ; 1 and 2 = a u r i c u l a t e sensilla; 3, 4 and 5 = sensilla basiconica. FIG. 3. S u r f a c e o f large m u h i p o r o u s s. b a s i c o n i c u m .

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~i i! ¸ !! iii iii¸ iii ii

FIG. 4. Transverse section of large s. basiconicum that forms part of antennal complex. Note fingerlike wall (w) and numerous pores (p). L = lumen. Fl~;. 5. Auriculate sensillum No. 1 in antennal complex.

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FIG. 6. Galea of maxilla with sensilla of various shapes and sizes. Note central trifurcate sensillum. g = galea. Fl6. 7. S. basiconica on apex of maxillary palpus.

Labium Four stout sensilla trichodea ca. 70 ~tm in length occur between the paipi (Fig. 1). Below the palpi are 2 ventrally directed sensilla trichodea ca. 100 txm in length (Figs 1, 9). The "l-segmented labial palpus bears 10 stout sensilla basiconica 2 - 4 ~m long (Fig. 8). As with the maxillary palpi, the broader central sensillum is irregularly ringed by the other sensilla. This thick-walled sensillum has dendritic branches and wall pores in the medial and distal regions indicating that it may have an olfactory function. Most of the remaining thick-walled sensilla have 2 or more dendrites each and are probably uniporous although apical pores could not be resolved.

Body The major difference in body sensilla occurs between the 1st instar and the subsequent 3 instars. The 1st instar is the only stage that bears very long, slender, cylindrical hairs that have a distinct bulbous apex (Figs 1 0 - 1 2 ) . The enlarged tip is thick-walled with an amorphous, electron-dense lumen; no pores were observed. These rodlike sensilla range from 80 p.m in the thoracic region to 180 ~m in the caudal area. They are distributed dorsally, laterally and ventrolaterally on all regions except the head so that approx. 7 sensilla partially encircle each segment. Shorter, tapered sensilla basiconica occur ventrolaterally on the posterior 5 abdominal segments (Fig. 10(a)). Instars 2 - 4 have unusual receptors that enlarge distally into a cluster of longitudinal ridges, nodules and elongated, overlapping plates (Fig. 13). There was no evidence of wall pores or dendrites. The interior generally consists of a thin wall c f fragmented and fibrous material and a large electron-lucent or fragment-filled lumen. These receptors occur primarily on the dorsum and secondarily on the lateral regions of all segments except the head. The sensilla on the 4th instar range in length from 60 to 120 ~m with the majority

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FIG. 8. S. basiconica on apex of labial palpus. FIG. 9. S. trichodeum on labium between palps. 6 0 - 7 0 Ixm. The longest are slender and not greatly enlarged distally. They occur primarily on the anterior ½ of the prothorax (ca. 8) and the posterior 3 abdominal regions ( 2 - 3 per segment). These long receptors are ca. the same length on all instars. The shortest sensilla (60 lam) have the greatest apical expansion (Fig. 13) and the overlapping plates are rounded apically in contrast to the bluntly pointed plates of the intermediatelength sensilla. An average of 16 combined short- and intermediate-length sensilla occur per segment. Other types of body receptors are found on instars 1 - 4 . (1) Trichoid sensilla 1 0 0 - 120 I,tm long occur in low numbers on the lateral areas of the body (Fig. 14) and the head contains ca. 18 trichoid sensilla up to 260 ~tm in length. (2) One or 2 basiconic sensilla ca. 120 ~m in length occur on the pleural region just above each proleg and thoracic leg (Fig. 15). A similar sensillum occurs on each dorsolateral region of the prothorax on instars 2 - 4. (3) Approximately 18 sensilla basiconica averaging 35 Ixm in length are scattered on the dorsal and lateral surfaces of the prothorax of instars 2 - 4.

Legs The smooth tip of the thoracic legs of instars 2 - 4 contains 4 sensilla (Fig. 16). The longest (220 Bm) is a trichoid type and the 3 remaining sensilla basiconica range from 20 to 100 I.tm in length. Two adjacent basiconic receptors are on the spinulated cuticle. There are no similar sensilla on the prolegs. Sensilla do not occur on the thoracic legs of the 1st instar but, on the prolegs, 1 sensillum basiconicum 6 - 8 lam in length is located in a socket on the anterior edge of the rounded proleg apex (Fig. 17(a)). Approximately 20 tapered papillae 2 - 4 Ixm long and with flat, broad bases also occur on the anterior edge of the apex and continue partway down the anterior face of the proleg. DISCUSSION The antennae of alfalfa weevil larvae are shorter and bear fewer sensilla than most larvae of other orders reported in the literature (Schneider, 1964; Schoonhoven, 1968;

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FIG. 10. Rodlike hairs on posterior region of a lst-instar larva, a = s. basiconicum. FiG. 11. Rodlike hair with bulbous apex. FtG. 12. Surface of bulbous apex. FIG. 13. Nodulated body sensillum on a 2nd-instar.

Slifer, 1970; Chapman, 1982). Antennae of lepidopterous larvae are typically 3-segmented and bear sensilla (s.) basiconica and styioconica for olfaction and temperature sensing (Schoonhoven, 1967, 1973). Antennae of dipterous larvae are typically segmented and discrete structures in the Nematocera, whereas the Cyclorrhapha have an antennomaxillary complex of fused sensory structures or structures separated into 2 or 3 groups (dorsal, terminal, and ventral organs). The sensilla include dome-shaped, styloconic and campaniform receptors. C h a p m a n (1982) and Frederick and Denell (1982) list salient studies on this order. Antennae of coleopterous larvae range from 1 to 3 segments that contain various combinations of contact and olfactory chemoreceptors in the form of styloconic, basiconic, coeloconic, and placoid sensilla, and campaniform and trichoid mechanoreceptors (Crombie, 1944; Chin, 1950; Zacharuk, 1962; Corbi~re-Tichan~ and Bermond, 1971; Ryan and Behan, 1973b; White et al., 1974). Suspected infrared detectors (Corbi~re-Tichan~ and Bermond, 1972), hygrodetectors (Roth and Willis, 1951) and CO~, receptors (Klingler, 1966) have also been reported on antennae of beetle larvae. The type of antennal complex described in this study has not been reported for other insect larvae. The multiporous nature of the large basiconic sensilla indicates that this recep'tor is the major olfactory organ. This sensiilum, with its thick wall and fingerlike projections, is an exception to the typical characterization of olfactory sensilla as having

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©

Fl(;. 14. S. t r i c h o d e u m on lateral area o f a larva. FIG. 15. S. b a s i c o n i c u m a b o v e a proleg. FtG. 16. Apex of a 2 n d - i n s t a r ' s thoracic leg with s. b a s i c o n i c a and trichodea. FJc. 17. Apex of a proleg on a l s t - i n s t a r s h o w i n g single s. b a s i c o n i c u m (a) and p a p i l l a e on a n t e r i o r face.

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thin walls. A similar cone organ occurs on the 1-segmented antennae of the mosquito larva, Aedes aegypti, along with a large peg, several trichoid sensilla and a campaniform sensillum (Zacharuk et al., 1971). However, the cone changes proximally to a tubular organ, and functions as a probable gustatory receptor. Sensilla basiconica 3 and 5 of alfalfa weevil larvae are uniporous receptors and probably function as contact chemoreceptors. The role of s. basiconicum 4 is unknown. Sensilla similar in appearance to antennal auriculate receptors l and 2 of alfalfa weevil larvae were described from the antennae of an adult tortricid moth (Den Otter et al., 1978). They were approx. 20 ~m long and 6 occurred on each of 3 antennal segments. However, unlike those of the alfalfa weevil larva, the sensilla contained many wall perforations with electron-dense material and a large number of dendrites. The authors postulated that these sensilla were olfactory receptors, but this same function for the poreless auriculate sensilla on alfalfa weevil larvae is not likely. Callahan (1969, 1973) described auricular sensilla on the antennae of 2 species of adult moths, the corn earworm, Heliothis zea, and a pyralid, Hypsipyla grandella. He speculated that the sensilla may resonate by shape to certain infrared spectral lines (along with probable thermal pyroelectric - dielectric arrays of sensilla on the antennae) from attractant or host plant scents. Although the auriculate sensilla on the alfalfa weevil larvae appear very similar externally, there is no internal evidence to support this speculation. They may, in fact, simply be flattened hairs that function as mechanoreceptors. The maxillary sensilla of the alfalfa weevil larva are grouped into 2 main regions, the galea and the apex of the palpus. The variety of s. basiconica on the galea as compared with those on the palp apex indicates a more diverse receptive ability and probably a more important role in food rejection or acceptance. The galea on the few species of lepidopterous larvae studied have 2 gustatory s. styloconica and several gustatory and olfactory s. basiconica (Schoonhoven, 1973; Reese and Carlson, 1974). The galea of the red turnip beetle larva, Entomoscelis americana, has a large uniporous sensillum and short associated poreless sensilla, and responds to sucrose, certain amino acids and several deterrents (Mitchell, 1978). The Colorado potato beetle larva, Leptinotarsa decemlineata, has a galea with 2 peg-shaped sensilla that taper apically to a terminal pore (Mitchell and Schoonhoven, 1974). The sensilla respond to sucrose, NaCl, amino acids and other chemicals. Other setae are present but are not chemoreceptive. The maxillary palpi of insect larvae typically have s. basiconica a n d / o r styloconica on their apices. Two unique subterminal, multiporous plate sensilla occur on a cutworm species, Euxoa messoria (Devitt and Smith, 1982). The palp sensilla of lepidopterous larvae are uniporous and are known or presumed contact chemoreceptors (Schoonhoven, 1968; Slifer, 1970; Devitt and Smith, 1982). In addition, a few of the sensilla on the tobacco hornworm, Manduca sexta, and the imported cabbageworm, Pieris rapae, have an olfactory function (Schoonhoven, 1973; Hanson and Dethier, 1973; St~dler and Hanson, 1975). In nematocerous dipteran larvae, the shape, number and arrangement of palp sensilla vary considerably and examples of sensillar morphology and a review of relevant work are found in Craig and Borkent (1980) and McIver and Siemicki (1982). Further modifications are seen in the antenno-maxillary complex of cyclorrhaphous dipteran larvae (Ryan and Behan, 1973a; Frederick and Denell, 1982). Contact chemoreceptors on the maxillary palpi of coleopterous larvae include a central ampullaceous sensillum with surrounding basiconic and protrusible styloconic sensilla in Tribolium (Ryan and Behan, 1973b), a variety in number and arrangement of basiconic

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pegs in elaterids (Zacharuk, 1962) and peg-like sensilla with and without villi in L. decemlineata (Mitchell and Schoonhoven, 1974). CO2 receptors occur on the maxillary palps of a cerambycid (White et al., 1974) and curculionid species (Klingler, 1966). Contrary to most other larval insects, the s. basiconica on the maxillary palps of alfalfa weevil larvae appear to be quite similar in external structure. Probably all are uniporous and act as contact chemoreceptors. Relatively few studies have been made on the labial palpi. In 2 cutworm species they are quite different from the maxillary palpi (Reese and Carlson, 1974; Devitt and Smith, 1982) but often the maxillary and labial palpi are similar in sensillar number, appearance and function as shown with several kinds of beetles (Zacharuk, 1962; Klingler, 1966; Ryan and Behan, 1973b; Mitchell and Schoonhoven, 1974; White et al., 1974). The alfalfa weevil larva's labial palpi also follow this generalization in that the sensilla are all similar externally and, except for the possible olfactory nature of the central sensillum, they most likely are contact chemoreceptors. Descriptions of the structure or function of larval body sensilla are scarce. Hairs similar to the capitate, thick-walled sensilla of 1st-instar alfalfa weevil larvae were reported on the antennae of aphids in the subfamily Drepanosiphinae (Shambaugh et al., 1978). The authors assumed the hairs were mechanoreceptors and this is most likely the role of these sensilla in alfalfa weevil larvae, Since the lst-instar larvae seek out and feed beneath closely appressed, developing vegetative and floral alfalfa tissue, the continuous deflection of the long sensilla by the tissue in the close feeding quarters may serve to depress locomotion and retain the larvae in this microhabitat. Upon molting, the loss of these mechanoreceptors results in most 2nd-instar larvae leaving their concealment to feed on the outside of the plant parts. The ridged and nodulated receptors on instars 2 - 4, with their thin, non-porous walls, and particle-filled lumen, may also be mechanoreceptors. Chapman (1982) has reviewed past studies on the number of chemoreceptors on insects and presented new data relating these receptors to insect behavior and evolution. He noted that the more polyphagous plant-feeding insects have a greater number of chemoreceptors on their mouthparts than those that are host specific. A similar pattern for antennae is present but less conclusive. The number of contact and olfactory sensilla on the mouthparts and antennae of 4 groups of beetle larvae ranged from 45 to 188 (but generally less than 100) for the mouthparts and from 20 to 28 for the antennae. These larvae were phytophagous to omnivorous in feeding habits. The alfalfa weevil larva is an oligophagous insect, feeding primarily on alfalfa, although other plants in the genus Medicago and occasionally species in the genera Melilotus and Trifolium are utilized. Thus, the number of sensilla should be relatively small. The larva has a total of 66 sensilla on the mouthparts and 12 sensilla on the antennae. The number of mouthpart chemoreceptors is not greatly different from those of other beetle larvae, but the number of antennal sensilla is about half. Thus, the large, multiporous s. basiconicum on the antenna may help provide the sensitivity to specific odors from alfalfa and closely related species. Acknowledgement--This research was supported by the C.M.U. Faculty Research and Creative Endeavors Committee Grant No. 4-22759.

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