JOURNAL OF MORPHOLOGY 213:85-103 (1992)

Morphology of the Antennae of Two Species of Biting Midge: Culicoides impunctatus (Goetghebuer) and Culicoides nubeculosus (Meigen) (Diptera, Ceratopogonidae) ALISON BLACKWELL, A. JENNIFER MORDUE (LUNTZ), AND WILLIAM MORDUE Department of Zoology, University of Aberdeen, Aberdeen AB9 ZTN, Scotland

ABSTRACT Scanning and transmission electron microscopy of the antennae of Culicoides impunctatus and Culicoides nubeculosus show that males and females share five sensillum types. Sensilla chaetica resemble mechanoreceptors, each innervated by a single neurone whose dendrite terminates distally in a tubular body: the arrangement of sensilla on male antennae suggests that females are located by sound. The antennae have both sharp- and blunt-tipped sensilla trichodea, sharp-tipped sensilla on only the distal third and blunttipped sensilla on all subsegments. These sensilla are typical of olfactory receptors, having multiporous walls and being innervated by a number of neurones with bifurcating dendrites ascending the hair shafts. Sensilla basiconica occur on the distal five subsegments of the female antenna and the distal three subsegments of the male antenna. Sensilla coeloconica always occur on subsegment one and sometimes on a number of other subsegments, depending on sex and species. Both basiconic and coeloconic sensilla have double walls and unbranched dendrites and may be either olfactory or thermo- and/or hygroreceptors. All antennae except those of male C. impunctatus antennae have sensilla ampullacea, apparently deep-seated olfactory or thermoreceptors. Small peg sensilla fitting the description of contact chemoreceptors occur only at the tip of the male antenna. D 1992 Wiley-Liss, Inc. Biting midges of the genus Culicoides are widely distributed throughout the world. The blood-sucking behavior of the females, in addition to being an irritation) can cause severe problems and several species are major pests. Culicoides spp. bite mammals and birds and are vectors of a number of animal and some human pathogens, both viral and non-viral (Braverman and Galum, '73; Linley et al., '83; Linley, '85). Despite the importance of biting midges as pests and vectors of disease, no effective defense strategy has yet been achieved. Crucial to the development of nontoxic, behavior-modifying chemicals to control midges is a greater understanding of their life history, behavior) and sensory biology. Olfactory cues are of prime importance in host location but to date there are few detailed studies of the antennal sensilla, or investigations into the roles of the individual sensilla. Chu-Wang et al. ('75) have used


scanning and transmission electron microscopy to look at the sensilla of C. furens, but only in the female midge. In addition, there is a brief morphological study of the antennal sensilla of female C. paraensis (FelippeBauer et al., '89). This study is a comprehensive and comparative account of the sensory structures on the antennae of males and females of two species of biting midge endemic to the United Kingdom, C. impunctatus and C. nubeculosus. C. impunctatus is the infamous "Scottish biting midge." It is the commonest biting midge in the United Kingdom and the scourge of the Highlands of Scotland during the summer months, having a particular impact on tourism and outdoor industry, especially forestry (Hendry, '86; Hendry and Godwin, '88). C. nubeculosus is also widespread in the United Kingdom, being mainly associated with farms where it bites cattle.




Insects Living Culicoides impunctatus (Goetghebuer) midges were collected from field sites in Argyllshire, Scotland. Culicoides nubeculosus (Meigen) midges were reared in the laboratory, from a colony provided by P. Mellor (I.A.H., Pirbright, Surrey, UK), according to the method of Boorman (’74). Scanning electron microscopy Entire midges or isolated midge heads were mounted on specimen stubs with doublesided tape and gold-coated in a n Emscope SC 500A sputter coater. The coating process was repeated three times, tilting and rotating the stub between each run to maximize coating and reduce subsequent charging. To avoid tissue collapse, specimens were often freezedried overnight before coating (Edwards, Modulyo drier). For both species, between 6 and 15 antennae of each sex were examined in detail with a Cambridge Instruments S600 microscope a t an accelerating voltage of 15 kV. Transmission electron microscopy Two different fixation regimes were employed, The first was the fixation of whole midge heads for 1 hr in a solution of 10% acrolein and 2.5% glutaraldehyde, buffered in 0.1 M sodium cacodylate. The heads were then washed overnight in buffer, post-fixed in aqueous 1% Os04for 2 hr, dehydrated in a series of alcohols, and embedded in L.R. White resin, hard grade (Agar Sci. Ltd., Stansted, Essex, U.K.). In the second regime some antennae were fixed in Karnovsky’s (’65) fixative: 5% glutaraldehyde and 2.5% paraformaldehyde, buffered in 0.1 M sodium cacodylate. The slower penetration of this fixative necessitated the fixation of only small sections of the antennae: cut up under a binocular microscope while the antennae were immersed in fixative. The antennal pieces were grouped according to the antennal subsegments they included, fixed for 1 hr, and then, to ease subsequent handling of the tissue, the pieces were embedded in agar blocks (1.5% solution of low-gelling-temperature agarose; Sigma, St. Louis, MO) which were fixed for a further 2 h r and then post-fixed, dehydrated, and embedded as above. Silver sections were cut with a diamond knife (Micro Star, Taab Labs, Reading, Berks, U.K.), picked up on Formvar-coated grids,

stained with uranyl acetate and lead citrate, and examined with a Philips 301 microscope. RESULTS

C. impunctatus is smaller than C. nubeculosus; females of the two species have wing lengths of 1.3 and 2.4 mm, respectively (Campbell and Pelham-Clinton, ’60). Their antennae only differ from each other in size. C. impunctatus has the smaller antennae, its mean antennal length being 539.0 36.9 pm (n = 15) for the female and 553.4 t 25.1 pm (n = 10) for the male. By comparison, C. nubeculosus females have a mean antennal length of 821.0 2 18.6 pm (n = 6) and the males have a mean length of 832.5 25.1 pm (n = 8). The following account of the antennal morphology, unless stated otherwise, applies to both of the species studied. The antennal segments each have a dense covering of microtrichia, minute, hair-like non-innervated cuticular structures; they also have additional sensory structures in patterns which vary between the sexes (Fig. 1A,B). There are three main segments, with segment 3 (the “antennal flagellum”) having 13 subsegments. Segment 1,attached to the head, is the scape; a small, flattened ring with a triangular apex, from which segment 2 arises; the globular, cup-shaped pedicel, having a diameter of approximately 60 pm on the antenna of female C. impunctatus and 70 pm on the antenna of female C. nubeculosus. The enlarged pedicel of the male antenna measures some 100 km in diameter in C. impunctatus and 130 pm in C. nubeculosus, accommodating a well-developed Johnston’s organ (Fig. 1C). I n female midges, subsegments 1-8 inclusive of the flagellum are all widest at the base, of similar lengths (e.g., range 26-42 pm in C. impunctatus),and have similar morphology. Subsegments 9-13 inclusive have a more uniform, extended shape, with their lengths increasing toward the distal end (range 50-70 pm for C. impunctatus). The subsegment lengths allow calculation of the antennal ratio (a species-specific character for females). This ratio is the sum of the lengths of subsegments 9-13 to the sum of the lengths of subsegments 1-8 (Campbell and PelhamClinton, ’60). The present data show it to be 0.88 and 0.81 pm for females of C. impunctatus and C. nubeculosus, respectively. There are a number of sexually dimorphic characteristics in the Culicoides antennae, including the difference in length and the noticeably different pedicel. Both sexes have




Fig. 1. C. impunctutus. Scanning electron micrographs of the antennae (antennae of C. nubeculosus differ only in length, being slightly longer). A: Montage of whole female antenna. Scale bar = 20 pm. B: Montage of whole male antenna. Scale bar = 20 pm. C: Johnston’s


organ contained within the pedicel of the male’s antenna; note the large number of radial scolopidia.Scale bar = 40 pm. P, pedicel; S, scape; SB, sensilla basiconica; SC, sensilla chaetica; ST(bt), blunt-tipped sensilla trichodea; ST(st),sharp-tipped sensilta trichodea.



the same number of subsegments but in the male only the final three subsegments are elongated in the same way as the distal five subsegments of the female flagellum. For example, the distal three subsegments of the male flagellum extend to 90 km in C. impunctatus, whereas the distal five subsegments of the female antenna measure 70 pm. The remaining male subsegments (i.e., 1-10) are more or less fused, whereas subsegments 1-8 in the female are more clearly defined. In addition, the numbers of sensilla on the antennae of the different sexes vary as described below. At least five sensillum types occur on both the male and female antennae: sensilla chaetica, sharp- and blunt- tipped sensilla trichodea, sensilla basiconica, and sensilla coeloconica (terminology of Wirth and Navai, ’78). In addition, the male antenna bears terminal sensory pegs and antennae of both sexes occasionally have sensilla ampullacea (Fig. 2). The flagellum of male and female C. impunctatus bears a maximum of 313 and 241 sensilla, respectively, and that of male and female C. nubeculosus bears 332 and 254, respectively. Each hair type has a characteristic ultrastructure. The distributions and



Fig. 2. Culicoides. Scale drawings of the different sensillum types on the antennae. With the exception of type F, female sensilla are represented. A Sensilla chaetica. B: Blunt-tipped sensilla trichodea (proximal antennal subsegment). C: Sharp-tipped sensilla trichodea (distal antenna1 subsegment). D: Sensilla basiconica. E: Sensilla coeloconica. F Terminal sensory pegs (male only). G: Sensilla ampullaceae. Scale bar = 5 pm.

mean lengths of these sensilla are represented in Tables 1 and 2.

Aporous (mechanoreceptor) sensilla: Sensilla chaetica One type of aporous hair occurs on the Culicoides antenna, namely the sensilla chaetica. On the female antenna, the sensilla chaetica occur in whorls a t the proximal ends of subsegments 1-8 inclusive (Fig. 3A). In addition, one or two sensilla chaetica, ofsimilar length, lie within proximal whorls of another hair type (trichoid sensilla) on each of the distal subsegments. The tip of subsegment 13 of the female flagellum of both species bears a single, shorter sensilla chaetica, 30-40 pm in length. Wherever sensilla chaetica were lost in processing, the sockets are clearly revealed and measure approximately 1.8 km long and 1.3 km wide (Fig. 3B). The total number of sensilla chaetica on the female antenna is about 60. On the male antenna, sensilla chaetica occur proximally on all of the flagellar subsegments, with the exception of the final subsegment on which there is, as on the female antenna, a shorter, distal sensilla chaetica. The sensilla chaetica of males number about 175 and the majority extend at least twothirds of the length of the flagellum. It is these long sensilla chaetica on subsegments 2-10 that give the male antenna its characteristic appearance, completely enveloping the antenna when not erect (Fig. 1B). The base of each subsegment is ringed by a deep groove in which the sensilla chaetica are held, in two groups of six to eight (Fig. 3C). The groove is most obvious after the hairs have been removed (Fig. 3D). The sensilla chaetica on the distal, elongated subsegments of the flagellum are shorter, occurring in basal whorls in sockets, as on the female antenna. In section, sensilla chaetica have a nonperforated wall and a single bipolar sensory neurone, the dendrite of which terminates a t the base of the hair shaft (Fig. 4A). In cross section, the ten grooves of the thick sensillum wall are clearly visible, as is the hair lumen, which would be fluid-filled in life (Fig. 5A). A tubular body, a mass of parallel microtubules (in the region of 200-300) set into an electron-dense material, represents the end of the dendrite and interacts with the inner portion of the socket (Fig. 5B). The microtubules emerge independently from the proximal side of the tubular body and travel through the fine granular ground substance



TABLE 1. Distribution and numbers (range) of the sensilla on the 13 antennal flagellum subsegments of C . imuunctatus and C. nubeculosus’ Sharp-tipped sensilla trichodea2

Sensilla chaetica Subsegment




1 2 3 4 5 6 7 8 9 10 11 12 13

8-15 12-16 12-16 12-16 12-16 12-16 12-16 12-16 12-16 12-16 3-8 2-8 1

4-6 P 6 4-6 4-6 4-6 4-6 4-6 P 6 1-2 1-2 1-2 1-2 1-3

0 0 0 0 0 0 0 0 0 0 7-18 11-26 3648

Blunt-tipped sensilla trichodea

Sensilla hasiconica

Sensi11a coeloconica






1-3 1-4 2-4 1-4 2 4 2 4 1-3 1-4 1-2 1-3 1-3 1-4 2-7

0 0 0 0 0 0 0 0 0 0 14 2-6 5-12

0 0 n

0 0 9-16 10-19 10-22 11-27 2642

2 4 2-3 2-3 2-3 2-3 2-3 2-3 2-3 2-3 2-3 1-2 1-2 1-3

Sensilla ampullacea




1-3 0 0

1 1 0

0 1-2 2 2-3 0

1 0 0 0 0 0 0 0 0



0 1-2 0

0 0 0


0 d


0 0 0 1-2 1-3 1-4 1-6 4-10

1 1-2 2-3 0 0 1-2 1-2


0 0 0 0 0 0

0 0 0

’These are common to male and female C. irnpunctatus (n = 10 for males; n = 15 for females) and C. nubeculosus (n = 8 for males; n = 6 for females), and hence numbers for the two species have been combined. Subsegment 1is proximal. 2Tbenumbers ofthe different sensillum types are similar for both species, with the exception of sharp-tipped sensilla trichodea which are more abundant on C. nubeculosus antennae (2-5 extra sensilla per subsegment).

of the proximal dendritic segment toward the ciliary structure. It is difficult to tell whether the microtubules are continuous with the ring-like ciliary structure, which has a “9 + 0” arrangement of microtubule doublets (Fig. 5C), from which the inner distal nerve process expands in diameter.

Each sensory neurone is accompanied by three accessory (or sheath) cells which wrap around the neuronal processes (Fig. 4A). Their primary functions are those of secreting the hair shaft and accompanying structures and this is reflected in their cellular organelles (Fig. 5C). The innermost thecogen

TABLE 2. Mean lengths ( p m ) f S.E. (ni of the differentsensillum types on the antennae of C . impunctatus and C. nubeculosus’

Sensilla chaetica

C. impunctatus 8 6

C. impzinctatus P 0



= 414.3 f

15.9 (45) D = 90.2 t 6.1 (24)

+ D = 57.2 & 1.1 (118)

C. nubeculosus 6 6

C. nubeculosus P P

P = 506.0 t 10.3 (44) D = 93.3 t 4.5 (25) P

+ D = 63.4 f 0.4 (95)

Sharp-tipped sensi11a trichodea’ W1&2 = 45.3 f 1.1 (97) W3 = 29.7 f 1.1 (54) W4-7 = 24.6 t 1.0 (79) W1&2 = 43.8 f 0.7 (176) W3 = 33.0 f 1.0 (71) W4-7 = 25.1 t 1.0 (73) W1&2 = 49.0 t 0.7 (84) ,~~, W3 = 37.4 t 0.7 (53) W4-7 = 26.8 2 1.0 (69) W1&2 = 45.6 f 0.5 (192) W3 = 31.1 f 0.6 (85) W4-7 = 26.7 f 0.6 (48)

Blunt-tipped sensilla trichodea


Sensi11a basiconica

32.5 f 1.6 (40) D = 15.0 f 0.8



1.2 (109) D = 18.8 -t 0.6 (77)

D = 6.5 t- 0.1







55.2 t 0.1 (59) D = 20.3 f 0.8 (26) =



f 0.1




’P = proximal antennal subsegments 11-8 (female), 1-10 (male)]and D = distal subsegments [9-13 (female), 11-13 (male)]. *Measurements are given for different whorls (maximum of 7 whorls per subsegment).Whorl 1 is proximal.

7.5 t 0.2 (30)



Fig. 3. C. impunctatus. Scanning electron micrographs of sensilla chaetica. A Montage showing proximal whorls of sensilla chaetica on subsegments 1-8 of the female flagellum. Scale bar = 10 pm. B: Characteristic sensilla chaetica socket on the female flagellum (sensillum removed). Note: This micrograph was obtained with a JEOL 200EX microscope. Scale bar = 1 pm. C: Twelve

to 16 long (400-500 pm) sensilla chaetica at the proximal end of each of subsegments 2-10 of the male flagellum. Scale bar = 5 pm. D: The deep groove at the base of each of subsegments 2-10 of the male flagellum in which the sensilla chaetica (removed) are inserted. Scale bar = 2 km. SC, sensillachaetica.

cell envelops the proximal dendritic segment and the sensory cell body, forming a thin, continuous layer around the nerve. It is usually possible to see parallel microtubules associated with septate desmosomes where the thecogen cell interacts with the outer accessory cells. The intermediate accessory cell, the trichogen cell, and the outermost and

largest accessory cell, the tormogen cell, partly envelop the distal dendritic segment. They contain the majority of the secretory apparatus: granular endoplasmic reticulum, Golgi apparatus, secretory granules and vesicles, multilamellar bodies, and numerous large mitochondria. The tormogen cell is characterized by a large polyploid nucleus; the

Fig. 4. Culicoides. Diagrammatic representations of the ultrastructural components of the different sensilla located on the antennae of both C. impunctatus and C. nubeculosus. A. Sensilla chaetica; note the non-perforated wall and the single sensory neurone whose dendrites terminate in a tubular body at the base of the hair shaft. Also note the three accessory cells wrapped around the neurone. B: Multiporous, single-walled sensilla trichodea with three sensory neurones with branching dendrites (sharp-tipped hairs, 3-4 neurones; blunt-tipped, a maximum of 12 neurones). C : Multiporous, double-walled

sensilla basiconica and sensilla coeloconica with sensory neurones having non-branching dendrites (basiconic hairs, 3 4 neurones; coeloconic, 5 neurones). D: Uniporous terminal sensory pegs of the male antenna. Five dendrites, four ascendingto the hair tip and one terminating at the base of the hair in a tubular body. BL, basal lamina; C, cuticle; CR, ciliary region; CT, cuticular tube; D, dendrite; DB, dendritic branch; EC, epidermal cell; GR, groove; JM, joint membrane; N, nerve cell; OS, outer dendritic segment; P, wall pore; TB, tubular body; TH, thecogen cell; TO, tormogen cell; TR, tricogen cell.

Fig. 5. Culicoides. Transmission electron micrographs of sensilla chaetica in C. impunctatus female (A), fixed in Karnovsky’s fixative, and C. nubeculosus (B,C), fixed in 10% acrolein/2.5% paraformaldehyde. A: Cross section showing the 10 grooves in the thick wall, each with a number of smaller scallops within it. Note the lack of dendritic material within the lumen. Scale bar = 400 nm. B: Longitudinal section of the tubular body, showing the mass of parallel microtubules (male).Scale bar = 300 nm. C: Transverse section showing both the tubular body and ciliary region of the sensory cell (female). See text for details of accessory cells. The extracellular space forms by the retraction of the trichogen and tormogen

cells on completion of the formation of the cuticularparts. Where the plasma membrane remains bound to the extracellular space an extensive system of microlamellae is produced. Scale bar = 1 pm. Insert: The ciliary region, with “9 + 0” microtubule doublets connected to the outer dendritic wall by fine fibrils. Scale bar = 300 nm. CB, ciliary body; CS, ciliary sinus; DS, dendritic sheath; ECS, extracellular space; GR, groove; HS, hair shaft; M, mitochondria; ML, microlamellae; MLB, multilamellar body; MT, microtubules; NU, nucleus; RER, rough endoplasmic reticulum; S, socket; SDe, septate desmosomes; SL, shaft lumen; TB, tubular body; TO, tormogen cell; TR, trichogen cell.


nuclear envelope is associated with a network of rough endoplasmic reticulum which spreads throughout the cell (Fig. 5C). The ultrastructure of the male and female sensilla chaetica is similar, with the exception that the sensilla of the male have a n expanded exocuticle of dense, amorphous material forming the groove in which the hair shafts are embedded; perhaps the groove helps to restrict the direction of the sensilla. Multiporous (olfactory chemoreceptor) sensilla There are three types of multiporous sensilla on the midge antenna: one is singlewalled and two are double-walled. Single-walled: Sensilla trichodea Both sharp- and blunt-tipped trichoid sensilla are found on the antenna. They have thin, almost smooth walls and are not articulated. The sharp-tipped sensilla are approximately two-thirds of the width of the blunttipped ones. Sharp-tipped sensilla trichodea occur only on the distal antennal subsegments. A maximum of 125 occur on a female antenna and 90 on male ones, the number being equivalent in both species. Each subsegment bears a single whorl of sharp-tipped sensilla trichodea at the proximal end. The female flagellum usually bears one to two sensilla chaetica within these proximal whorls (Fig. 6A). More distally lie varying numbers of additional whorls of sharp-tipped sensilla trichodea. Their numbers increase toward the tip, with a maximum of seven whorls on the final subsegment, the exact number being difficult to determine because the sensilla are densely spaced around the tip (Fig. 6B). In both sexes each whorl consists of u p to eight sensilla. The sharp-tipped trichoid hairs have a curved base and become longer and thinner toward the tip. They vary in length within the different whorls, decreasing in size from the proximal to the distal end of each subsegment (Table 2). The blunt-tipped sensilla trichodea are more uniform in length than are the sharptipped ones. On the proximal subsegments of both male and female antennae the blunttipped ones are unmistakable; three to four whorls of thick sensilla arise from midway up each subsegment (Fig. 6C). Totals of between 37 and 47 have been observed on all of t h e midges examined (male and female). On both


of the species studied, the blunt-tipped sensilla trichodea are about 10 pm longer on the proximal subsegments of the female antennae than on those of the male. On the distal flagellar subsegments of both sexes, blunttipped trichoid hairs are far less conspicuous, being smaller and randomly positioned. Maximal numbers occur on the distal-most subsegment. In section, the single-walled trichoid sensilla have a number of dendritic branches ascending the hair lumen (Fig. 4B). Sharpand blunt-tipped trichoid sensilla are similar, but differ in the numbers of sensory neurones and in the hair dimensions. Sharptipped trichoid hairs have a narrower diameter than blunt-tipped ones (mean = 1.14 pm compared with 1.78 pm in C. nubeculosus female) but have relatively thicker walls (onefifth of the total hair diameter compared with one-ninth that of the blunt-tipped hairs). In addition, blunt-tipped hairs have 5.4 times more pores than sharp-tipped ones (Fig. 7A,B). The pores have a narrow opening (pore channel: 15 nm in diameter) leading into a wider chamber (120 nm in diameter) filled with the same dense material as the inner lumen in which the free dendritic branches are located. Pore tubules leading from the pore to the inner hair lumen have been identified in sharp-tipped hairs (Fig. 7 0 , but not in blunt-tipped hairs. The numbers of dendritic branches within the lumens of blunt-tipped hairs vary between 12 and 24 for both species and sexes in this study, depending on the shaft diameter: larger hairs usually contain more dendritic branches. The dendrites of each sensillum appear to branch only once before they begin ascending the hair shaft; thus, a maximum of 12 sensory neurones have been found in the vicinity of each blunt-tipped trichoid hair (i.e., correlating with 24 dendritic branches in the hair lumen). In such hairs, the outer dendritic segments are often grouped into two sets of six within a common sensory sinus, surrounded by cellular organelles characteristic of the accessory cells (Fig. 7D). With so many different sensilla close to each other, it is difficult to ascertain whether or not each group of dendrites, or “neuronal unit” (Solinas et al., ’831, has a separate set of three accessory cells. Sharp-tipped trichoid sensilla are innervated by either three or a maximum of four sensory neurones (Fig. 7E). A maximum of



Fig. 6 . Culicoides. Scanning electron micrographs of sensilla trichodea of female C. impunctatus (A,C) and C. nubeculosus (B). A: Montage showing whorls of sharptipped sensilla trichodea at the proximal ends of subsegments 9-13. Note the one or two sensilla chaetica within these whorls. Scale bar = 20 km. B: Montage showing sharp-tipped sensilla trichodea (6-7 whorls) on the dis-

tal most subsegment of the flagellum. Scale bar = 20 pm. C: Montage showing blunt-tipped trichoid sensilla arising from midway up subsegments 1-8 in whorls of 3-4. Scale bar = 10 km. SC, sensilla chaetica; ST(btj, blunttipped sensilla trichodea; ST(stj, sharp-tipped sensilla trichodea.



eight dendritic branches have been counted in the shaft lumens. Double-walled: Sensilla basiconica and sensilla coeloconica There are two types of double-walled, multiporous sensilla on the antennae of both sexes of both species. These have similar ultrastructure (Fig. 4C), but different morphological appearance (Fig. 8A,B), distributions (Table 11, and perhaps functions. The grooved-walled sensilla basiconica are thorn-shaped, terminating in a rounded tip (Fig. 8A). They occur on only the distal flagellar subsegments (Table 11,and range between 6 and 7 pm in length (Table 2). The sensilla are not articulated but instead are attached by shallow basal structures. The grooves extend from just above the base right up to the tip: each sensillum has 10-11 grooves. In both sexes and species, basiconic sensilla are most numerous on subsegment 13, occurring in four whorls. The numbers of basiconic sensilla decrease proximally on the antenna. Total numbers range between 19 and 25 on all of the antennae examined. The second double-walled hair type, sensilla coeloconica (Fig. 8B), occurs in only small numbers. Sensilla coeloconica always occur on the distal end of subsegment 1 of both male and female C. impunctatus and C. nubeculosus. Additional sensilla lie on the other subsegments depending on sex and species; the total number of sensilla never exceeds seven for these two species. Further coeloconic sensilla lie on subsegments 6 and 12 of female C. impunctatus antennae, subsegments 12 and 13 of male C. impunctatus antennae, subsegments 6-8 of female C. nubeculosus antennae, and subsegments 7-9 of male C. nubeculosus antennae. In each case the number of coeloconic sensilla varies between one and three in a row. Coeloconic sensilla consist of a short, grooved-walled peg (2.5-4 pm in length) on the floor of a small depression in the cuticle, 3.3-3.6 pm in diameter. Only the proximal third of the peg wall is grooved, having 10-12 grooves. A ring of between 5 and 12 microtrichia surrounds the pit. Basiconic and coeloconic sensilla are similar in section; both are multiporous, with unbranched dendrites ascending the hairshaft lumens (Fig. 4C). The dendrites of both hair types are enclosed in a thick cuticular sheath or tube which ascends from the ciliary region in the sensory sinus to the hair tip (Fig. 9A,B). The cuticular tube, or inner wall, connects to the small pores a t the ends of the

wall grooves by radial channels within narrow spokes (12-24 nm in diameter). The spoke channels are continuous with the inner lumen and thus are filled with granular material equivalent to that which surrounds the dendrites (Fig. 9C,D). There are no pore tubules. Basiconic sensilla of both C. impunctatus and C. nubeculosus are innervated by three or four sensory neurons (Fig. 9C), whereas serial sections of coeloconic sensilla consistently show five dendrites in both species (Fig. 9D). The floor of the coeloconic sensillum pit seems to lack pores (Fig. 9B).

Uniporous (chemoreceptor)sensilla No previous description reports sensory structures lying at the tip of the male antenna of Culicoides. The tips of male antennae studied (both Culicoides impunctatus and C. nubeculosus),but not those of the female antennae, bear a group of two or three stubby, smooth-walled pegs, set into flexible sockets. The pegs are 1-2 pm long. The sensilla are commonly bifurcated (Fig. 10A,B). Each sensillum has a single narrow pore at the apex, approximately 60 nm in diameter, with dendritic material immediately below it (Fig. 1OC). Midway along the hair shaft there are four dendrites, within an inner cuticular tube (Fig. 10D). In the sensory sinus below the sensillum are groups of five sensory neurones (Fig. lOE), one of which terminates with a tubular body a t the base of the hair shaft (Fig. 10F). Sensilla ampullacea Opposite sensilla coeloconica, on the distal ends of subsegments 1and 2 of the flagellum of female C. impunctatus and in a similar position on subsegment 1of female and male C. nubeculosus antennal flagella, are small protuberances (approximately 1.5 pm high), with a single narrow (0.2 pm) opening a t the top (Fig. 111, identical to the sensilla ampullacea described by Felippe-Bauer and Bauer ('90) for C. paraensis. The ultrastructure of these tiny sensilla has not been investigated. DISCUSSION

This is the first detailed report of the morphology and fine structure of the antennal sense organs of both sexes of two species of Culicoides: C. impunctatus and C. nubeculosus. The present observations confirm the array of sense organs for Culicoides previously identified in light microscopy studies (Campbell and Pelham-Clinton, '60) and by electron microscopy (Chu-Wang et al., '75; Felippe-Bauer et al., '89) and have identified



a new sensillum type on the male antenna. The general function or functions of the sensilla are inferred from their ultrastructure, although verification will require behavioral and electrophysiological studies.

Aporous (mechanoreceptor) sensilla The sensilla chaetica are conspicuous and may serve to protect the underlying more delicate structures on both the male and female antennae; these sensilla have the typical appearance of mechanoreceptors which is confirmed by their fine structure. A single bipolar neurone terminating in a tubular body at the base of the strong, thick-walled hair is highly characteristic of a mechanoreceptor, with compression of the tubular body acting as the stimulus at the cellular level (Thurm, '64; Rice et al., '73). In addition to a tactile and protective function, the presence of large numbers of sensilla chaetica on the male antennae, together with the Johnston's organ, should enable the male to orient to sound. Such orientation is common in male mosquitoes in which the highly specialized Johnston's organ is tuned to the flight sound of the female (Slifer and Sekhon, '62; McIver and Hudson, '72). In fully mature Aedes aegypti, the tactile hairs stand out nearly at right angles to the long axis of the flagellum, which is moved as a whole by sound waves. Flagellar movement is detected by Johnston's organ (Slifer and Sekhon, '62). The single sensilla chaetica at the tip of both male and female Culicoides antennae is likely to have a general tactile capacity and to permit investigation of various substrates and textures. Such sensilla are common in insects, including the mosquito A. aegypti (Slifer and Sekhon, '62). The additional sensilla chaetica on the distal elongated subsegments of female antennae of C. impunctatus and C. nubeculosus, within whorls of sharptipped sensilla trichodea, do not occur on antennae of C. furens (Chu-Wang et al., '75). However, the distal antennal regions of other Culicoides species, such as C. similis, do bear small numbers of sensilla chaetica (Wirth and Navai, '78). Multiporous (olfactory chemoreceptor) sensilla A porous cuticle facilitates olfactory function and does not exclude the capacity to detect humidity and/or serve as a thermoreceptor (Zacharuk, '80; Altner and Loftus, '85). The differing morphology of the three types of multiporous hairs on the antennae probably reflects their sampling efficiency and posi-

Fig. 7. Culicoides. Transmission electron micrographs of sensilla trichodea on the antennal flagellum of female C. nubeculosus (A,C, Karnovsky's fixative; D,E, 10% acrolein/2.5%glutaraldehyde) and male C. zmpunctutus (B, 10% acrolein/2.5% glutaraldehyde). A Cross section of blunt-tipped hair, with 24 dendritic branches. Scale bar = 200 nm. B: Cross section of sharp-tipped hair, with three large dendritic branches and a number of smaller ones. Scale bar = 200 nm. C: Longitudinal section of sharp-tipped hair, showing the pore tubules coming from the wall pores into the dendritic lumen. Scale bar = 200 nm.

Fig. 7. (continued) D: Montage showing longitudinal section of blunt-tipped hair, with its 12 dendrites divided into two bundles of six: one cut at the basal body level on the right-hand side (together with five surrounding distal/ inner dendritic segments) and six cut through the ciliary regions on the left (three distaliinner dendritic segments shown). Note how the accessory cells penetrate the hair shaft with numerous microlamellae. Scale bar = 3 km. E: Longitudinal section of four sensory neurones innervating a sharp-tipped trichoid sensillum (hair shaft not

shown). Three have been cut through the ciliary region. The fourth distal dendritic segment lies behind the other three. The striated ciliary rootlets are visible in the right-hand distal segment. Scale bar = 1 km. AN, antennal nerve; BB, basal body; CR, ciliary rootlets; D, dendrite; DB, dendritic branch; HS, hair shaft; M, mitochondria; ML, microlamellae; NT, neurotubules; NU, nucleus; P, wall pore; PT, pore tubules; TH, thecogen cell; TO, tormogen cell; TR, tricogen cell.



Fig. 8. Culicoides. Scanning electron micrographs of the two types of double-walled sensilla located on the male and female antennae. These micrographs were obtained with a JEOL 200EX microscope. A: Sensilla ba-

siconica (C. nubeculosus). Scale bar = 1 pm. B: Sensilla coeloconica (C. impunctatus). Scale bar = 1 pm. MTR, microtrichia.



Fig. 9. Culicoides. Transmission electron micrographs of double-walled sensilla from C. nubeculosus female (A,B,D, fixed in Karnovsky's fixative) and C. impunctatus male (C, fixed in 10%acrolein/2.5% paraformaldehyde). A Montage showing longitudinal section of basiconic sensillum. Scale bar = 2 pm. B: Longitudinal

section of coeloconic sensillum. Scale bar = 1 pm. C,D: Cross sections midway up a basiconic sensillum with four dendrites (C) and a coeloconic sensillurn (D) with five dendrites. Scale bars = 200 nm. D, dendrite; GR, groove; NL, non-innervated lumen; IW,inner wall; MTR, microtrichia; OW, outer wall; SC, spoke channel.

tion on the antenna rather than their function. As discussed by Lewis ('71), there is no reason for olfactory sense organs to differ at any Ievel above the molecular organization of the receptor sites. Sensilla in more exposed conditions (i.e., Culicoides trichoid hairs) are generally more robust and larger than those a t less exposed sites (i.e., basiconic and coeloconic). Olfaction will play a key role in the hostfinding behavior of Culicoides females; host odor products such as octenol are highly attractive to female midges, as are lactic acid and COz W i n e et al., '90).Body heat of the

potential host may also be attractive. The single-walled trichoid hairs are likely to be the primary olfactory sensilla, accounting for about 45% and 76%of the total sensory input of male and female antennae, respectively. The occurrence of two hair types (sharp- and blunt-tipped) in C. impunctatus and C. nubeculosus, their positions and innervation, agree with the findings of Chu-Wang et al. ('75) for C. furens. The occurrence of two different sizes of blunt-tipped trichoid sensilla correlates with the types I and TI blunt-tipped sensilla trichodea described from the antennae of female C. paraensis (Felippe-Bauer et



Fig. 10. C. impunctatus. Terminal sensory pegs of the male antenna.A,B: Scanning electron micrographs showing pegs (arrows), which are sometimes bifurcated (Bj. Scale bars = 2 pm (A) and 1 km (Bj. C-E: Transmission electron micrographs of specimens fixed in 10%acroleini 2.5% glutaraldehyde. C: Longitudinal section showing a single apical pore. Scale bar = 300 nm. D: Cross section showing the double wall and four dendrites in the central lumen. Scale bar = 300 nm. E: Cross section of five

dendrites innervating a sensory peg, three cut through the ciliary body and two through the basal body. Scale bar = 500 nm. F: Montage showing longitudinal section of the single neurone of the group of five which terminates in a tubular body without ascending the sensillum lumen. Scale bar = 400 nm. BB, basal body; CB, ciliary body; D, dendrite; MT, microtubules; P, wall pore; OS, outer dendritic segment; SDe, septate desmosomes; TB, tubular body.


Fig. 11. C. nubeculosus. Scanning electron micrograph of a sensillum ampullacea on subsegment 1of the female antennal flagellum. Scale bar = 1pm.

al., '89). Similarly, both sharp- and blunttipped sensilla trichodea occur on mosquito antennae. These sensilla are structurally similar to those on the antennae of Culicoides, and are suggested to be the principal olfactory sense organs (Slifer and Brescia, '60; McIver, '69, '71). The two different types of Culicoides trichoid hair cannot be explained fully at present, although the longer blunttipped hairs and sharp-tipped sensilla might provide an effective odor-trapping net for long-range host-derived odors. In contrast, the shorter blunt-tipped hairs might be more effective a t trapping short-range, more specific odors such as those associated with nectar sources and oviposition sites. Behavioral studies on mosquitoes have shown that blunttiooed trichoid sensilla mediate resoonses to


repellents, whde sharp-tipped hairs are involved in host location (Steward and Atwood, '63). I t is shown that the dendrites of the trichoid sensilla branch only once before they begin ascending the hair shaft. This situation is different from that in many other insects. For example, in male sawflies (Neodiprion sertifer) the trichoid sensilla are innervated by 8-12 cells, all the dendrites of each having two or three branches (Hannson et al.,,911, and in the sorghum midge Contarinia sorghicola the trichoid hairs are innervated by five neurones with dendrites that divide to form a maximum of 36 branches in the hair lumen (Slifer and Sekhon, '71). One exception to the similarities of the trichoid hairs of Culicoides impunctatus and C. nubeculosus with those of C. furens is that neither the blunt- nor the sharp-tipped trichoid hairs of the latter species have pore tubules that might permit the transduction of odor molecules (Chu-Wang et al., '75). The tubules of the sharp-tipped hairs of C. impunctatus and C. nubeculosus resemble the pore filaments of multiporous thin-walled pegs of the flesh fly Sarcophaga argyrostoma, thought to be extensions of the dendrites and the sites where odorous molecules contact the dendrites (Slifer and Sekhon, '64). However, further work is needed to test the present findings. It is not unusual for insect olfactory sensilla to lack pore tubules, as is the case in the antennal sensilla of larval Aedes aegypti (Zacharuk and Blue, '71). Thick-walled olfactory hairs always lack pore tubules (Zacharuk, '801, as do the doublewalled basiconic and coeloconic hairs of Culicoides. In these cases the sensilla possess a spoke channel system that permits the passage of volatiles to the sensory dendrites. Sensilla basiconica also occur on the antennae of mosquitoes, and as on the antennae of Culicoides, there are significantly more basiconic sensilla on the terminal segments than on the subterminal segments (McIver, '71). Despite morphological similarities, basiconic sensilla of mosquitoes and Culicoides differ in ultrastructure. Sensilla of female culicine mosquitoes have only one main pore at the tip and may be hygroreceptors (McIver, '69, '70); this function has been confirmed electrophysiologically in A. aegypti (Kellogg, '70). Similarly, "grooved pegs" on the antennae of the cecidomyiid Mycodiplosis erysiphes are uniporous and may be either thermo- or hygroreceptors (Solinas and Nuzzaci, '87). The sensilla coeloconica of Culicoides are analogous to the "olfactory pits" described bv CamDbell and Pelham-Clinton ('60) in



their Culicoides key (i.e., “thin-walled papillae arising from a pit surrounded by a number of minute setulae”). Jamnback (’65) assigned a taxonomic value to these pits, suggesting that their numbers are correlated with host preference. This hypothesis appears correct; whereas the antennae of female C. impunctatus (mammalophilic) usually bear about seven coeloconic sensilla, those of the ornithophilic species C. circumscriptus bear 47 (Campbell and Pelham-Clinton, ’60). This observation has been confirmed in 12 different Culicoides species of southern Africa; species showing a preference for mammals have six or fewer “antennal pits” (i.e., sensilla coeloconica), whereas those f e d n g on birds have more (Braverman and Hulley, ’79). Sensilla coeloconica occur on the antennae of anopheline but not of culicine mosquitoes. They lie mainly at the base of the antennal flagellum where they may function as hygroreceptors (McIver, ’69). More generally, electrophysiological studies showed that the neurones associated with sensilla coeloconica of a variety of insect species respond to Cog, temperature, andlor humidity (Schneider and Steinbrecht, ’68).

0.2 wm long and arise from a wide cuticular base, not from a flexible socket as do those of male C. impunctatus and C. nubeculosus. No such “styloconic-type’’ sensilla were identified in the present study.

Sensilla ampullaceae The small sensilla ampullaceae are morphologically identical to the sensilla ampullacea described for C. paraensis, suggested as serving species recognition and likened to the thermoreceptors of a variety of mosquito species (Felippe-Bauer and Bauer, ’90). The sensilla consist of aporous, thick-walled pegs in deep tubes (Boo and McIver, ’75). The sensilla ampullaceae (or “sensory flasks”) of Hymenoptera have a similar fine structure (Schneider, ’64). Zachurak and Shields (’91) likened the sensilla ampullaceae of a variety of insects to coeloconic sensilla, either functioning as aporous thermoreceptors or as multiporous chemoreceptors. In conclusion, the antennae of C. impunctatus and C. nubeculosus bear a variety of receptors, including mechanoreceptors and several types of chemoreceptor. These clearly indicate the stimulus types which are most Uniporous (chemoreceptor)sensilla important in regulating midge behavior. FeMultiple innervation and a n apical pore males possess three times as many potential a r e typical characteristics of uniporous olfactory sensilla as tactile hairs, reflecting chemosensilla which are gustatory (Zacharuk, their dependence on odorous stimuli, prima’80). Although further work is required on rily for host finding. Trichoid, basiconic, and the sensory pegs a t the tip of the male Culi- coeloconic sensilla are all likely to be incoides antenna, there does appear to be a volved, responding to skin odors, warmth, basal mechanosensitive neurone (ending in a humidity, and COz. In contrast, the ratio of tubular body) associated with four other neu- olfactory to mechanoreceptors is closer to 1:1 rones, all of which ascend to the tip of the in the male. The greater number of sensilla peg. This configuration strongly suggests a chaetica on the male antenna is the main contact-chemosensory function for these sen- example of sexual dimorphism between the silla. Similar sensilla are found on the distal adults, indicating the importance of sound in nodes of the antennal subsegments of the mate finding for these two species, as opsorghum midge Contarinia sorghicola, al- posed to perhaps chemical means, as sugthough their function remains unknown (Sli- gested by the clear sexual difference in the fer and Sekhon, ’71). The terminal pegs ap- development of the elaborate multiporous pear similar to apical labial sensilla in the circumfilia of the cecidomyiid Mycodiplosis Aleyrodidae, some of which are contact erysiphes which are thought to be pherochemoreceptors and probably involved in mone receptors (Solinas and Nuzzaci, ’87). host-plant selection (Walker and Gordh, ’89). However, the stubby pegs found on the tip The lack of such structures on the female only of antennae of male Culicoides antenCulicoides antenna perhaps points toward nae do indicate that contact chemoreception an involvement of the male terminal sensilla may be involved in the mating of both C. in mate recognition and subsequent orientation impunctatus and C. nubeculosus. No contact of the male to the female during copulation. sex pheromones have been identified in eiThe peg sensilla at the tip of the male C. ther of these species, but one has been demonimpunctatus and C. nubeculosus antennae strated behaviorally in C. melleus; in this differ from the “styloconic-type’’ sensilla at insect the legs of the males, not the antenthe tip of the female C. paraensis antenna nae, are used for detection of the pheromone (Felippe-Bauer et al., ’89). The latter are just (Linley and Carlson, ’78).


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Morphology of the antennae of two species of biting midge: Culicoides impunctatus (Goetghebuer) and Culicoides nubeculosus (Meigen) (Diptera, Ceratopogonidae).

Scanning and transmission electron microscopy of the antennae of Culicoides impunctatus and Culicoides nubeculosus show that males and females share f...
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