Ultrastructure of the contact chemoreceptors of Apis mellifera L. (Hymenoptera : Apidae)

Int. J. Insect Morphol. & Embryol. 514/5): 301-315. 1976. Pergamon Press. Printed in Great Britain.

U L T R A S T R U C T U R E OF THE CONTACT CHEMORECEPTORS OF APIS MELLIFERA L. (HYMENOPTERA • APIDAE) A. T. WHITEHEAD* and J. R. LARSEN Department of Entomology, University of Illinois, Urbana, IL 61801, U.S.A. (Accepted 19 March 1976)

Abstract--Seasilla chaetica of different sizes were found by scanning electron microscopy on the glossa, labial palps, galeae, antennae and tarsi of the worker honey bee. Sensilla basiconica also were found on these structures, except the antennae and glossa. With the exception of the mandibles, whose sensilla are all innervated by on~ sensory neuron, transmission electron microscope studies showed these receptors are similar in ultrastructure to taste receptors previously described in other insects. It was determined that sensilla on the mouthparts and tarsi possess 5 sensory neurons, one of which ends at the sensilla base as a mechanoreceptor, the other 4 extending up the lumen of a two-chambered hair. Many of the sensilla are tipped with either a pore or a papilla. About half of the sensilla observed on the antennae are innervated by 6 sensory neurons. A peculiarly shaped sensillum trichodeum occurs on the mandible which breaks off at pupal eclosion. A spatulate peg on the tarsal claw is also present. Index descriptors (in addition to those in the title): Scanning electron microscopy, transmission electron microscopy, sensilla chaetica, sensilla basiconica, taste receptors, honey bee.

INTRODUCTION SOME EARLY investigators (Briant, 1884; Breithaupt, 1886; and M c l n d o o , 1916) assigned a strictly tactile function to the blunt hairs they found on the mouthparts o f the honey bee. Will (1885) considered those f o u n d on the tongue (glossa), and Briant (1884) regarded only those f o u n d on the antennae to be taste receptors. The discovery that certain hairs on the tarsi o f butterflies and the proboscis o f the blow fly initiated feeding responses when touched by sugar solutions (Minnich, 1921 ; 1926) led to n u m e r o u s investigations o f contact chemoreceptors in a n u m b e r o f insects (reviewed by Frings and Frings, 1949). The honey bee was used extensively in some o f these investigations at a behavioral level. Kunze (1932) and Minnich (1932) behavior_ally determined that taste receptors were not only on the antennae but on the front tarsr as well. Frings and Frings (1949) confirmed the presence o f front-tarsal receptors. The most elaborate series o f behavioral experiments (von Frisch, 1934) reported the bees' reactions to various sugar and chemical solutionswithout regard to chemoreceptor location. The elaboration o f the structure and function o f insect contact chemoreceptors using electron microscopy (reviewed by Slifer, 1970) and electrophysiology (reviewed by H o d g s o n , 1968) is well known. Morphological studies on honey bee contact chemoreceptors is limited. Dostal (1958) described the distribution o f chemoreceptors on the bee antennae, and Slifer and Sekhon (1961) investigated these chemoreceptors at the ultrastructural level. Galic * Permanent Address: Department of Zoology, Brigham Young University, Provo, UT 84602, U.S.A. 301

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(1971) did a light microscope study on the chemosensory structures on the glossa, epip h a r y n x a n d h y p o p h a r y n x o f the bee. Dietz a n d H u m p h r e y s (1971) did a scanning elec t r o n microscope study on bee a n t e n n a e b u t did n o t identify contact chemoreceptors. The purpose of the present study is to report the ultrastructure of possible c o n t a c t chemoreceptors f o u n d on the mouthparts, tarsi, a n d a n t e n n a e of the honey bee a n d to l a y a morphological f o u n d a t i o n for electrophysiological studies now being conducted in our laboratory. MATERIALS AND METHODS Adult worker honey bees emerged from the pupal stage within 2~ hr were obtained from the University of Illinois apiary. Whole mounts for light microscopy were made by conventional methods. A filar micrometer was used for measuring sensilla lengths. Material for scanning electron microscopy (SEM) was prepared from live bees, dehydrated in an ethanolicFreon 113 series, critical-point dried in Freon 13, mounted on stubs, and subsequently coated with carbon and gold-palladium alloy. Tissue for transmission electron microscopy (TEM) was processed after the method of Harbach and Larsen (1976) almost exclusively under vacuum and cold conditions (approx. 4°C) and using pieces no longer than ½ mm in length. The material was dissected in 2.5 ~ glutaraldehyde (pH 7.0), placed under vacuum for 2-3 hr, washed in cacodylate buffer and left overnight under light vacuum. The material was post-fixed in 1 ~ osmium tetroxide for 2-3 hr, dehydrated in ethanol, followed by propylene oxide and embedded in Luft's (hard mixture) Epon (Pease, 1964). After sectioning, the grids were stained in ethanolic uranyl acetate (1 ~) for 1 hr. OBSERVATIONS The areas of the honey bee examined were the a n t e n n a e (Figs. 32, 36), tarsi (Figs. 37-39), a n d m o u t h p a r t s (Fig. 2). The structure a n d location of the contact chemoreceptors o c c u r r i n g on each of these areas will be reported separately. T o avoid ambiguity in n a m i n g s e n s o r y structures a modification of the system employed by C a l l a h a n (1975) will be used. The contact sensilla of the honey bee are grouped into 2 classifications (Table l). (1) Sensilla TABLE 1.

LOCATION, NUMBERS AND LENGTHS OF HONEY BEE CONTACT CHEMORECEPTORS

Sensilla chaetica Sensilla location Glossal tip Glossa (distal 9, not includingtip) Labial palp segment 1 Labial palp segment 2 Labial palp segment 3 Labial palp segment 4 Galea (distal t) Galea (maxillary-palp area) Antennal segments (10) Fore tarsus: Pre-tarsus 5th Tarsomere 4th Tarsomere 3rd Tarsomere 2 nd Tarsomere 1st Tarsomere (basitarsus) * from Galic (1971) from Dostal (1958)

Sensilla basiconica

No.

Range of lengths (/~m)

No.

Range of lengths (t~m)

12 66-78* 0 4-6 10 7-9 12-16 0 318t

60-70 41-59 -I 1-61 13-45 11-36 44-59 -14-44

0 0 0 8-13 l 1-15 9-12 10-16 43-47 0

---4-8 4-8 3-7 10-16 6-10 --

10-14 15-16 12-16 12-17 12-15 21 +

24-64 17-82 39-78 17-60 29-72 49-82

0 1-6 l 1 1 0

-8 10 8 10 --

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303

basiconica: straight, smooth-walled, blunt-tipped, with or without terminal papilla, and usually less than 10-p.m long. (2) Sensilla chaetica (a term used by Galic, 1971): same general description, but they are usually slightly curved and their length exceeds 10/~m. Glossal receptors Galic (1971) reported that an average of 72 s. chaetica (41-59 t~m), occur on the distal 2/3 of the glossa, and none is present on the proximal 1/3. Twelve longer (60-70/zm) s. chaetica are present on the glossal tip arranged compactly in 2 rows of 5 sensilla each on the ventral side bordering the median groove (Fig. 4), and the other 2 occur opposite to these on the dorsal side (Fig. 3). The glossal-tip sensilla point distally and slightly lateral to the midline. The shorter sensilla are randomly interspersed between the bases of the non-innervated branched hairs (called pseudohairs by Galic, 1971) that densely cover the surface of the glossa in successive rows. The shorter sensilla occupy both ventral and dorsal surfaces with a few being found on the lateral margins. The sensilla are oval in cross-section and usually bear a terminal papilla (Fig. 1). No terminal pores were observed. Galic (1971) reports that each glossal sensillum contains 5 bipolar neurons whose axons enter 1 of 2 glossal nerves that terminate via the labial nerves in the subesophageal ganglion. We determined that these axons are 0.5-0.8/~m in diameter. The sensory-cell bodies are oval measuring 8-13/zm in diameter containing relatively large nuclei 6/~m in diameter. Their cytoplasm has large numbers of mitochondria, golgi apparatus, and extensive rough endoplasmic reticulum. Both flat and round onion bodies (Cook, 1972) were observed. Each of the perikarya sends out dendrites that pass extracellularly through the trichogen cell. At this point the tormogen cell surrounds the trichogen cell and dendrites forming a concentric structure (Fig. 5). The dendrites taper after leaving their perikarya and average 1 /~m in diameter. Prior to entering the extracellular vacuole of the trichogen cell they are held tightly in a glial complex (Fig. 7) which, when observed under higher magnifications, is bound by septate desmosomes. After entrance into the vacuole the dendrites are abruptly reduced in diameter to 0.4/zm where the ciliary region lies distal to the basal bodies. The dendrites then enter the fragmented base (Fig. 9) of the dendritic sheath (Hansen and Heumann, 1971). The sheath becomes consolidated distally (Figs. 6, 8). As the dendrites progress up the sheath they enlarge again to a diameter of about 0.9/,m (Fig. 8). In the region of the socket the mechanoreceptor dendrite contains a tubular body (Thurm, 1963) and is segregated within a chamber of the sheath (Fig. 6). The socket is elevated above the surrounding cuticle (Fig. 10) on the glossal-tip sensillum, and those more proximal glossal sensilla have even more elevated sockets. The glossal-tip hairs have thick walls without lateral pores and contain 4 dendrites moderately filling the dendritic lumen (Fig. 11). The dendrites are in what appears to be an extension of the dendritic sheath forming an irregular tube that extends to the approximate tip of the hair. Occasionally, we encountered seemingly empty vesicles (Fig. 11) that might be degenerating mitochondria or empty nutritive vesicles (Slifer, 1970). In young bees, a p~ortion of the trichogen cell could still be seen in the non-dendritic lumen of the hair in the region of the socket. The number of dendrites stayed constant even toward the hair tip where the non-dendritic chamber ends. No sections were obtained through the tips of the hairs. The proximal sensilla on the glossa have the same subepidermal cellular complex (SECC) described above, but the dendrites completely fill the dendritic-chamber lumen (Fig. 12).

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FIG. 1. Terminal papilla on a glossal-tip s. chaeticum. Marker indicates 1.1 p.m. FIG. 2. Dorsal aspect of mouthparts of honey bee showing mandibles, maxillary galea, labial palps, glossa and labellum (abbreviations after Snodgrass, 1956). FIG. 3. Dorsal aspect of glossal tip. Labellum on dorsal side is covered with branched pseudohairs. Only 2 s. chaetica (arrows) occupy dorsal side of tip. FIG. 4. Ventral aspect of giossal tip. Labellum is smooth and without hairs. S. chaetica and pseudohairs fan out over proximal surface of labeilum while very fine pseudohairs (arrow) mark opening of median groove.

Labial-palp receptors The labial palps are elongate, having 4 segments, each segment b e c o m i n g p r o gressively shorter distally (Snodgrass, 1956). O n l y the 3 distal segments b e a r either s. b a s i c o n i c a o r chaetica (Table 1). T h e lengths o f the s. chaetica generally decrease on each s u c c e e d i n g segment distally.

305

FIG. 5. Cross section of a glossal-tip s. chaeticum showing tormogen cell, trichogen cell, and 5 dendrites (1-5). FIG. 6. Cross section of a glossal-tip sensillum in socket area. Dendritic sheath encloses tubular body of a mechanoreceptor (5). Note vacuole present between dendrites (1-4). F t 6 . 7 . Cross section of a giossal-tip s. chaeticum showing glial wrappings surrounding dendrites (1-5). At higher magnifications septate desmosomes are seen at junction (arrow) between glial wrappings. FIG. 8. Dendritic sheath and dendrites of a glossal-tip sensillum distal to ciliary region. Sheath is more consolidated and begins to enclose mechanoreceptor dendrite. F1G. 9. Ciliary region of dendrites of a glossal-tip sensillum. Dendritic sheath is fragmented in this area.

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FIG. 10. Tangential section through socket of a glossal-tip sensillum. Hair emerges from socket and contains dendritic chamber. Termination of mechanoreceptor (arrow) occurs at hair base. FIG. 11. Cross-section of giossal-tip sensillum hair showing 4 dendrites. Note vacuole within electron-dense dendritic-sheath extension (arrow). FIG. 12. Cross-section of a more proximal glossal sensillum with dendrites filling lumen of hair. FIG. 13. Distal-lateral margin of 2ad segment of labial palp. Five s. chaetica and 3 s. basiconica are visible. Other hairs are s. trichodea. FIG. 14. Cross-section of tarsal-claw s. chaeticum hair showing extra-cellular space in dendritic lumen.

Ultrastructure of the Contact Chemoreceptors

307

The 2nd segment usually has 4 s. chaetica (20-61/~m long) along its distal-lateral margin, and I or 2 s. chaetica (about 18/~m long) occur more proximal on the lateral margin (Fig. 13). Eight to 13 s. basiconica (4-8/zm long) are found scattered along the lateral margin. The measurements and locations of these hairs vary. The 3rd segment has 10 s. chaetica (13-45 tzm long) arranged in a broken circle around its distal lip (Fig. 22) together with 11-15 s. basiconica (4-8 tzm long) which are scattered over the distal 2/3 of the segment. The 4th or terminal segment has 7-9 s. chaetica (11-36 t,m long) interspersed with s. basiconica (3-7 t~m long) (Fig. 20). Four or 5 of the basiconics are found on the apex of this segment with the s. chaetica making an irregular circle about them. Both types of hairs on the labial-palp segments have been observed with or without terminal papilla (Figs. 15-18). The SECC of these sensilla is similar to the receptors on the glossa. Five bipolar neurons innervate each sensillum. The dendritic sheath also contains a tubular body, and the hair has 4 dendrites moderately filling the dendritic lumen. A pore or depression 0.2 t~m in diameter was found at the tip of 1 s. chaeticum.

Maxillary receptors S. chaetica and basiconica are present on each galea (Table 1). About 12 s. chaetica (44-59 /~m long) are arranged in a straight row on the distal 1/3 of the lateral galeal margin (Fig. 21). A total of 10-16 s. basiconica (10-16/zm long) alternate between the chaetica (Fig. 19). A group of over 40 s. basiconica (6-10 t~m long) are on the galeal surface near the maxillary palp (Fig. 29). They are more conical at the tip than s. basiconica described above and have a well-defined pore (Fig. 28). The SECC of the galeal s. chaetica is also similar to those on the glossa in that they are innervated by 5 neurons. A mechanoreceptor is in the base, and 4 dendrites are in the lumen of a two-chambered hair.

Mandibular receptors The distal-lateral edge of the mandible bears a row of small basiconic pegs (6-tzm long) (Fig. 26), that are unlike any described above. They are more blunt (Fig. 24), and are innervated by only 1 neuron. Another group of basiconics are on the proximal-lateral face of the mandible near the exit of the mandibular gland (Nedel, 1960). No sections were made through these receptors. The median surface of the mandible has a long transverse ridge along which lie 12 large blunt setae which are bent toward the front edge (Fig. 30). Some smaller sharply pointed setae (9/~m long) occur at the distal end of this ridge (Fig. 27). They were not examined by TEM. The large setae (Fig. 31) may have been broken off during emergence of the bee from its pupal cell; therefore, pharate bees were examined and their mandibles did indeed show unbroken, long, bent, sharp hairs (Fig. 25). All of the sensilla examined along the distal edges of the mandible showed only 1 neuron and appear to be mechanoreceptors.

Antennal receptors Dostal (1958) counted 318 s. chaetica (her Type II s. trichodea) on all 10 antennal segments. We observed no s. basiconica on the antennae. Most of the s. chaetica are found on the distal segments and are most numerous on the anterior surfaces. The 10th or terminal segment has the largest number of s. chaetica; they are especially numerous around the ~MVA 5 4 / 5 - - F

308

A . T . WHITEHEAD and J. R. LARSEN

FIGS. 15-18. S. basiconica from 3rd labial-palp segment showing presence and absence of terminal papilla. Fig. 16 shows tip of s. chaeticum with possible pore in tip; most sensiila had terminal papilla. Marker indicates 4 t~m except Fig. 16 which indicates 0.8 tLm. FIG. 19. S. chaeticum and basiconica on galen tip (region of top arrow in Fig. 21). Hairs are partially hidden behind galeal surface. Sharp hair is s. trichodeum. FJG. 20. Distal end of 4th segment of labial palp showing basiconica of varying length (arrows) amid s. chaetica. FIG. 21. Distal end of maxillary galea (frontal aspect) showing row ofs. chaetica (between arrows) along lateral edge. FIG. 22. Distal end of 3rd segment of labial palp. FIG. 23. Longitudinal section through dendritic sheath and socket of an s. chaeticurn from 5th tarsomere. Note round vesicles (arrow).

Ultrastructure of the Contact Chemoreceptors

FIG. 24. Basiconic pegs on lateral mandibular edge at bases of large s. trichodea. FIG. 25. Median surface of right mandible of pharate bee showing unbroken hairs on ridge. FIG. 26. Posterior aspect of distal end of mandible showing large s. trichodea with row of short basiconic pegs on edge (arrow). FIG. 27. Sharp-tipped sensilla from distal end of ridge (Fig. 30). Marker indicates 9/~m. FiG. 28. Tip of galeal sensillum (from area of maxillary palp) showing pore. Marker indicates 1.5 p,m.

FtG. 29. Lateral view of maxillary-palp area of galea showing maxillary palp at left and group of s. basiconica (arrow). Maxillary palp has no contact chemoreceptor. FIO. 30. Median surface of left mandible showing blunt, bent hairs (double arrow) along a transverse ridge. They point to front edge of mandible. Four sharp-tipped sensilla (single arrow) occur at distal end of ridge. FIG. 31. Large, blunt hair from transverse lidge of mandible showing broken tip. Marker indicates 18 ~m.

309

310

A . T . WHITEHEAD and J. R. LARSEN

FIG. 32. Frontal aspect of apex of 10th antennal segment showing s. trichodea (bent tips) and s. chaetica (SCI), a possible contact chemoreceptor; and SC2, a thin-walled possible olfactory receptor. FIG. 33. Terminal papilla on tip of s. chaeticum (SC~ of Fig. 32) on antenna. Marker indicates 2 p.m. FIG. 34. Tip of thin-walled s. chaeticum (SC2 of Fig. 32) showing dimpled surface (arrows). Indentation in tip is not a pore. Fic. 35. Tip of a thin-walled s. chaeticum (SCa) from antenna. FIG. 36. Apical end of 10th left antennal segment showing flattened ventral disc bearing s. trichodea and a few s. chaetica. Disc is ringed by s. chaetica (arrows) interspersed among many s. trichodea.

Ultrastructure of the Contact Chemoreceptors

311

flattened ventral area (Fig. 36). The s. chaetica (14-44/~m long) each bear a terminal papilla (Fig. 33). The longest sensilla (35-44 t~m long) are found randomly distributed over the surfaces of the more proximal segments. A number of round-tipped s. chaetica (15 t~m long) (Fig. 35) is found on the antenna, and are similar to the slender, thin-walled hairs of Slifer and Sekhon (1961) and the Type III s. trichodea of Dietz and Humphreys (1971). An additional group of thicker, blunt s. chaetica (about 15/zm long) (Fig. 32) similar to the large, thin-walled hairs of Slifer and Sekhon (1961) and the s. basiconica of Dietz and Humphreys (1971) is found on the 6 distal segments. These show slight indentations on their surfaces and have no terminal papillae (Fig. 34). All s. chaetica observed on the antennae have a similar SECC compared to those of the glossa. However, about half of the antennal s. chaetica are innervated by 6 neurons (Fig. 40). The other half have 5. All of these hairs have a mechanoreceptor.

Tarsal receptors The tarsus of the honey bee consists of 5 tarsomeres and a pretarsus which bears a pair of lateral bifid claws (Fig. 37) (Snodgrass, 1956). S. chaetica and basiconica were found on all parts of the tarsi except the pretarsi and 1st tarsomeres (basitarsi) which lacked s. basiconica (Table 1). SEM studies were performed only on the fore tarsi. Light microscope examination indicated that both the middle and hind tarsi have equivalent numbers of sensilla in the same locations as on the fore tarsi, except there are considerably fewer s. chaetica on the basitarsi of the middle and hind legs. The long stiff spines on the basitarsi made counts very difficult to make especially on the middle and hind legs. Five to 7 s. chaetica (24--64/zm long) occupy the proximal, dorsal margin of each inner point of the tarsal claws (Fig. 37). All hairs observed had a terminal papilla. Four fiat, spatulate pegs and 2 sharp-pointed trichoid sensilla were found on the outer margins of each tarsal claw (Fig. 41). The spatulate pegs are fiat, tongue-shaped (3/~m long by 2.5/zm wide) and set into deep sockets (Figs. 41,42). Four s. chaeti~a ('!.4 68 tzm long) occur on each of the dorsal-lateral and medial-lateral margins of the 5th tarsomere (Fig. 38) and are intermingled with relatively dense, sharp, s. trichodea. Seven to 9 s. chaetica (17-82 tzm long) are broadly distributed along the ventral midline of this tarsomere (Fig. 39). One to 6 s. basiconica (8/zm long) have been seen on this segment usually on the ventral side (Fig. 39). The 3rd through the 4th tarsomeres are the shortest segments of the tarsi (Snodgrass, 1956), and they have both s. chaetica and s. basiconica (Table 1) distributed on their ventrallateral surfaces. The s. basiconica and shorter s. chaetica are proximal, and the longer s. chaetica (up to 78/zm long) are distal. Both the basiconica and chaetica are intermingled with fairly dense s. trichodea. The basitarsus has over 20 s. chaetica (49-82 t~m long) distributed on the ventral-lateral surface of the fore tarsus. S. chaetica are also present on the basitarsi of the middle and hind legs, but they are only found on the ventral sides and in greatly reduced numbers (only 2 or 3 were observed on each of these segments). The s. chaetica of the tarsal claws and 5th tarsomere of the fore tarsus have 5 dendrites, one ending in a mechanoreceptor and the other 4 continuing into the hair shaft. The dendrites in the hair are more loosely arranged, having more extracellular space than any other s. chaetica that we examined (Fig. 14). The vesicles appearing in the dendrite lumina of the hairs (Fig. 11) are round or slightly oval and also appear in the dendritic-sheath area (Fig. 23).

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A . T . WIHTEHEAD and J. R. LARSEN

FIG. 37. Apex of fore tarsus showing rows of s. chaetica (arrows) on inner margins of claws. FIG. 38. Dorsal-lateral aspect showing s. chaetica (arrows) on 5th tarsomere. Pretarsus is visible at left. FIG. 39. Ventral-lateral aspect of 5th tarsomere showing s. chaetica (arrows). Tarsal claw is visible in lower right corner. FIG. 40. Cross section through dendritic sheath of antennal s. chaeticum showing 6 dendrites (1-6). Sheath has almost enclosed (arrow) mechanoreceptor dendrite. FIG. 41. Lateral aspect of dorsal margin of tarsal claw showing spatulate pegs. One of 2 sharptipped pegs is visible at left. FIG. 42. Spatulate peg showing tongue-like shape.

Ultrastructure of the Contact Chemoreceptors

313

No sections were made through the spatulate pegs on the tarsal claws. All of the s. trichodea examined on the tarsi are innervated by 1 dendrite. DISCUSSION Our investigation has shown that the ultrastructural details of contact chemoreceptors found in the honey bee are similar to those reported in other insects, and the locations of these sensilla on the bee are also not usual (Slifer, 1970). The papilla present on the tips of most of the s. chaetica and basiconica on honey bees needs further elucidation. Eltringham (1933) first reported it on tarsal sensilla of a butterfly. It is not present as such on the taste hairs of muscoid flies whose tips are lip-like and moveable (Stfirckow et al., 1973). Henning (1974) reports a papilla on the basiconic pegs of the katydid as did Mitchell and Schoonhoven (1974) on short pegs on the Colorado potato beetle. Our observation that not all sensilla on the bee have a papilla could be explained by the presence of an eversible membrane-like structure at the tip responding to the feeding status of the insect (Bernays et al., 1972); or it may be an exudate forming on the tip (Dethier, 1972). The presence of 4 dendrites in most insect taste hairs is supported by the findings of Larsen (1962) and Peters and Richter (1963) working on blow flies, Slifer et al. (1957) on the grasshopper, Mustaparta (1973) on the pine weevil, Schafer (1971) on the cockroach, and Slifer and Sekhon (1963) on a hemipteran. However, Sttirckow et al. (1973) support Larsen (1962) in his observation that this number may vary. Rice et al. (1973) found only 2 and 3 respectively in 2 different types of labial contact receptors in the tsetse fly and St~idler et al. (1974) found only 2 in s. styloconica on the proboscis of the female eastern spruce budworm. Our finding that some of the antennal s. chaetica have 6 sensory neurons is supported by Slifer et al. (1957) who found 6 in some of the antennal pegs of the grasshopper and Borg and Norris (1971) who found up to 8 in sensilla on the antennae of a scolytid beetle. Electrophysiological studies currently being performed in our laboratory may shed some light on the function of additional neurons. Galic (1971) reported s. chaetica on the glossa of the honey bee. Our findings confirm the presence of these receptors on the glossa as well as on the labial palps (Briant, 1884; Mclndoo, 1916; Beetsma and Schoonhoven, 1966), maxillae (Mclndoo, 1916), and antennae (Slifer and Sekhon, 1961). The presence of contact receptors on honey-bee tarsi has been inferred by behavioral studies (Minnich, 1932; Kunze, 1932; Marshall, 1935; and Frings and Frings, 1949). Our findings confirm their presence morphologically. They have also been found on the tarsi of Lepidoptera (Mitchell and Seabrook, 1972; Ma and Schoonhoven, 1973), Diptera (Hansen and Heumann, 1971), and even other arthropods (Chu-Wang and Axtell, 1973). The function of the spatulate pegs on the tarsal claws and long s. trichodea on the median face of the mandibles is unknown although they are probably mechanoreceptors. LeBerre et al. (1969) describes dendrites which infiltrate the tips of the mandibular teeth in the grasshopper and postulates that they are part of a mechanoreceptor. A mechanoreceptor is present in the base of bee contact chemoreceptors. This is supported by Thurm (1963) who worked on honey bee hair-plate sensilla and by Beetsma and Schoonhoven (1966) who in a brief electrophysiological investigation found that the s. chaetica on the labial palps were sensitive to sugar solutions and mechanical stimulation. Current electrophysiological investigations of these sensilla will determine more exactly their functional classification and modalities.

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Acknowledgements--We thank Dr. Elbert Jaycox and Mr. Stephen Parise for supplying the honey bees. Especial thanks to Mrs. Mary Fisher for her technical assistance and in helping proof the manuscript. This study was supported in part by funds for a Professional-Development Leave from Brigham Young University to ATW and by a Public Health Service Training G r a n t (No. GM-1076) to JRL. REFERENCES BEETS~, J. and L. M. SCHOONnOVEN. 1966. Some chemosensory aspects of the social relations between the queen and the worker in the honey bee (Apis mellifera L.). Proc. K. Ned. Akad. Wet. SeE. C. Biol Meal. Sci. 69: 645-47. BE~NAVS, E. A., W. M. BLANEY and R. F. CHAPMAN. 1972. Changes in chemoreceptor sensilla on the maxillary palos ofLocusta migratoria in relation to feeding. J. Exp. Biol. 57: 745-53. BORG, T. K. and D. M. NORRIS. 1971. Ultrastructure of sensory receptors on the antennae of Scolytus multistriatus (Marsh.). Z. Zellforsch. Mikrosk. Anat. 113: 13-28. BREITHAUPT, P. F. 1886. Ueber die Anatomie und die Funktionen der Bienenzunge. Arch. f. Naturgesch. 52 (Jahrg. 1): 47-112. BR1ANT, T. J. 1884. On the anatomy and functions of the tongue of the honey bee (worker). J. Linn. Soc. Lond. Zool. 17: 408-17. CALLAHAN,P. S. 1975. Insect antennae with special reference to the mechanism of scent detection and the evolution of the sensilla. Int. J. Insect Morphol. EmbryoL 4: 381-430. Carl-WANG, I-Wu and R. C. AXTELL. 1973. Comparative fine structure of the claw sensilla of a soft tick, Argas (Persicargas) arboreus Kaiser, Hoogstraal, and Kohls, and a hard tick, Amblyomma americanum (L.). J. Parasitol. 59: 545-55. COOK, A. G. 1972. The ultrastructure of the A1 sensilla on the posterior surface of the clypeo-labrum of Locusta migratoria migratorioides (R and F). Z. Zellforsch. Mikrosk. Anat. 134: 539-54. DETHIER, V. G. 1972. Sensitivity of the contact chemoreceptors of the blowfly to vapors. Proc. Nat. Acad. Sci. U.S.A. 69: 2189-92. DIETZ, A. and W. J. HUMPHREYS. 1971. Scanning electron microscopic studies of antennal receptors of the worker honey bee, including sensilla campaniformia. Ann. Entomol. Soc. Amer. 64: 919-25. DOSTAL,B. 1958. Riechf'~ihigkeit und Zahl der Riechsinneselemente bei der Honigbiene. Z. VergL Physiol. 41: 179-203. ELTRINGHAM,a . 1933. On the tarsal sense-organs of Lepidoptera. Trans. R. Entomol. Soc. Lond. 81: 33-6. FRINGS, H. and N. FRINGS. 1949. The loci of contact chemoreceptors in insects. A review with new evidence. Amer. Midl. Nat. 41: 602-58. FRISCH, K. YON. 1934. 13bet den Geschmackssinn der Biene. Z. Vergl. Physiol. 21: 1-156. GALtC, M. 1971. Die Sinnesorgane an der Glossa, dem Epipharynx und dem Hypopharynx der Arbeiterin von Apis mellifica L. (Insecta, Hymenoptera). Z. Morphol. Tiere 70: 201-28. HANSEN, K. and H. G. HEUMANN. 1971. Die Feinstruktur der tarsalen Schmeckhaare der Fliege Phormia terraenovae Rob.-Desv. Z. Zellforsch. 117: 419-42. HARBACr~, R. E. and J. R. LARSEN. 1976. Uitrastructure of sensilla on the distal antennal segment of adult Oncopeltus fasciatus (Dallas) (Hemiptera: Lygaeidae). lnt. J Insect MorphoL EmbryoL 5: 23-33. HErqNIrqG, B. 1974. Morphologie und Histologie der Tarsen von Tettigonia viridissima L. (Orthoptera Ensifera). Z. Morphol. Tiere. 79: 323-42. HODOSON, E. S. 1968. Taste receptors of arthropods, pp. 269-77. In J. D. CARTHY and G. E. NEWELL (eds.). Invertebrate Receptors. Syrup. Zool. Soc. Lond. No. 23. Academic Press, London. KU'NZE, G. 1932. Einige Versuche 0ber den Antennengeschmackssinn der Honigbiene. Zool. Jahrb. Abt. AUg. Zool. Physiol. Tiere. 52: 465-512. LARSEN, J. R. 1962. The fine structure of the labellar chemosensory hairs of the blowfly Phormia regina Meig. J. Insect PhysioL g: 683-91. LEBERRE, J. R. and A. LOUVEAUX. 1969. Equipement sensoriel des mandibules de la larve du premier stade de Locusta migratoria L. C.R. Hebd. Seances Acad. ScL Ser. D. Sci. Nat. (Paris) 268: 2907-10. MA, W. and L. M. SCHOONrlOVEN. 1973. Tarsal contact chemosensory hairs of the large white butterfly Pieris brassicae and their possible role in oviposition behaviour. EntomoL Exp. AppL 16: 343-57. MARSHALL,J. 1935. On the sensitivity of the chemoreceptors on the antenna and fore-tarsus of the honey bee, Apis mellifica L. J. Exp. Biol. 12: 17-26. MCINDOO, N. E. 1916. The sense organs of the mouthparts of the honey bee. Smithson. Misc. Collect. 65: 1-55. MIN~CH, D. E. 1921. An experimental study of the tarsal chemoreceptors of two nymphalid butterflies. J. Exp. Zool. 33" 173-203. MINNIC., D. E. 1926. The organs of taste on the proboscis of the blowfly, Phormia regina Meigen. Anat. Rec 34: 126. MIrqNICH, D. E. 1932. The contact chemoreceptors of the honey bee Apis mellifera Linn. J. Exp. Zool. 61: 375-93.

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IMAE

Ciliary region Dendrite Dendritic chamber Dendritic sheath Galea Glia Glossa Hair Labellum Labial palp Mandible Mechanoreceptor Pseudohair

5 4/5--G

USED S SB SC SECC SEM SP ST TB FEM ToC TrC V

IN FIGURES Socket Sensillum basiconicum Sensillum chaeticum Sub-epidermal cellular complex Scanning electron microscope Spatulate peg Sensillum trichodeum Tubular body Transmission electron microscope Tormogen cell Trichogen cell Vacuole