Int. J. Insect Morphol. & Ernbrvol., Vol. 17. No. 3, pp. 185 195. 1988 0020 7322/88 $3.00 + .00 Printed in Great Britain Pergamon Press plc

ORGANIZATION OF THE ANTENNAL LOBE IN THE QUEEN HONEY BEE, APIS M E L L I F E R A L.

(HYMENOPTERA • APIDAE)

GERARD ARNOLD, SATI BUDHARUGSA a n d CLAUDINE MASSON

Laboratoire de Neurobiologie Comparge des Invert6brgs, I .N .R .A . -C .N .R .S . UA 1190, 91440 Bures sur Yvette, France

(Accepted 5 November 1987)

A b s t r a c t - - A n t e n n a l afferent pathway topography was studied in the queen honey bee, Apis mellifera L. (Hymenoptera : Apidae) by staining with cobalt chloride applied directly to the cut antennal axons. Antennal lobe organization in the queen was compared with those in worker and drone bees. The organization is similar in queen and worker bees. For the first time in a female insect the possible existence of a macroglomerulus is shown, which may be involved in the processing of species-specific information. A comparative quantitative neuromorphological study of the glomeruli was performed between young queens (8-day old) and l-yr-old queens. The mean volume of the glomeruli is 46% greater in the older queens.

Index descriptors (in addition to those in title): Aging, antennal lobe, glomeruli, macroglomerulus,

I N T R O D U C T I O N INSECT antennae carry sensilla innervated by sensory cells that are specialized to detect different sensory modalities (Altner et al., 1977). In the workers and drones, more than 95% of the sensilla serve an olfactory function (Esslen and Kaissling, 1976). Most of the sensory axons project into the antennal lobe glomeruli. There, they connect with the dendrites of antennal lobe neurons in the glomeruli where the olfactory messages undergo an important integration before being transmitted to higher centers in the brain (Masson, 1972, 1977; Ernst and Boeckh, 1983; Masson and Mustaparta, 1988).

Olfaction is very important in all castes of the honey bee. For the queen, it is particularly important during swarming and mating (Morse and Boch, 1971). Knowledge of the anatomical organization of the olfactory system is indispensable for an adequate understanding of olfactory signal processing. The system is well known in the drone and worker bee (Jawlowski, 1948; Pareto, 1972; Suzuki, 1975; Mobbs, 1982; Arnold et al., 1985).

An important sexual dimorphism is demonstrated by the drone in that at the level of the antennal lobe there are 4 large and easily identifiable glomerular complexes (Arnold et al., 1985).

In this paper, we describe the antennal afferent topography in the central nervous system (CNS) of the queen honey bee. A comparative study of antennal afferent

185

186 G. ARNOLD et al.

t o p o g r a p h y in 8 - d a y - o l d q u e e n s ( y o u n g q u e e n s , y .q . ) and in 1-yr-old q u e e n s (o ld q u e e n s ,

o . q . ) was also u n d e r t a k e n .

M E T H O D S

Twenty-one 8-day-old virgin and 10 1-yr-old fertile Apis mellifera queens were used in this study. Each test subject had 5 segments of one antenna amputated, a 5% solution of cobalt chloride was then applied to the cut end. This technique has previously been employed to map the antennal afferent projections in the drone and worker bee ('Arnold et al., 1983, 1984, 1985). Seven micrometre serial sections were cut from the brain of the 31 queens. All of these were examined by light microscope.

Nine y.q. and 8 o.q. were used for detailed analysis. Measurements were made of their antennal lobes and of some distinctive glomeruli. The central body, a brain structure outside the antennal afferent system, was selected for control measurements.

In 2 y.q., the dimensions of all glomeruli were measured, and in 3 y.q. the total number of glomeruli was determined. Because the cobalt chloride technique allows the identification of all glomeruli, a specific number was assigned to each one. This enabled identification of the same glomerulus in consecutive sections.

All measurements were made with a Leitz ASM 68 K image analyzer. The serial sections were imaged using a video camera (Varioscan V 16) coupled to a microscope (Fluovert Leitz). The outlines of the glomeruli and of the complete antennal lobe were drawn with a cursor on to a digitizer. Their volume and size were then computed by the image analyzer.

Error estimation

Number ofglomeruli . On the images of antennal lobe sections, the precise boundaries of 2 or 3 glomeruli were somet imes difficult to determine. This may have led to one glomerulus being counted when there were, in fact, 2. The max imum error which may have been introduced in the process was, however, very small (less than 2%).

Volume. The method employed allowed volumes to be determined with a precision greater than 95%.

R E S U L T S

Deutocerebral afferents T h e a n t e n n a l s e n s o r y a x o n s o f t he q u e e n b e e c o u l d be s e p a r a t e d in to 3 m a i n g r o u p s o f

ips i l a te ra l t r ac t s as t h e y e n t e r t he bra in . T h e t rac t s T1 to T4 p r o j e c t to the a n t e n n a l lobe .

T r a c t T5 p r o j e c t s to t he do r sa l l obe . T r a c t T6 cou ld be s u b d i v i d e d in to 3 s u b b r a n c h e s .

B r a n c h e s T6-1 a n d T6-3 p r o j e c t to the p r o t o c e r e b r u m , whi l e the b r a n c h T6-2 p r o j e c t s to

the s u b e s o p h a g e a l gang l i a .

The antennal lobe T h e a n t e n n a l l o b e has a n e u r o p i l a r c o r e and a ce l lu l a r p e r i p h e r y , wh ich is c o m p o s e d of

gl ial cel ls and n e u r o n s o m a . T h e n e u r o n s in t he q u e e n b e e , as in the o t h e r cas tes , a re

o r g a n i z e d in to i n t e r n a l , do r sa l , and e x t e r n a l g roups . T h e e x t e r n a l g r o u p is t he la rges t . T h e g l o m e r u l a r n e u r o p i l is l o c a t e d in t he o u t e r n e u r o p i l a r r e g i o n s u r r o u n d i n g the cen t r a l

c o a r s e n e u r o p i l .

1. Neuropilar organization T h e c o m p a r a t i v e d i m e n s i o n s o f t he a n t e n n a l l obe b e t w e e n y o u n g q u e e n s and o ld

q u e e n s a r e d e s c r i b e d in T a b l e 1. T h e o . q . s h o w e d a 4 7 % g r e a t e r v o l u m e t h a n y .q . , wh ich

was s ign i f i can t ( P < 0 . 0 2 , M a n n - W h i t n e y U test) .

T h e v o l u m e of t he cen t r a l b o d y was s imi la r in b o t h the y .q . (1851 + 94 x 10 ~ i, zm 3 (n = 9)) a n d in t he o . q . (2014 + 220 × 103 ixm 3 (n = 7)) , a v o l u m e d i f f e r e n c e p r o v i n g

Antennal Lobe of the Queen Honeybee

TABLE 1. DIMENSIONS OF THE ANTENNAL LOBE

187

Young queen Old queen (8-day-old) (1-yr-old)

(n = 9) (n = 8)

Antero posterior diameter 246 _+ 25 l~m 274 +_ 27 ~m

Mediolateral diameter 237 _+ 8 p~m 285 _+ 18 ~m

Dorsoventral diameter 233 _+ 9 ~m 263 _+ 25 p~m

Volume 7170 _+ 599 x 10 ~ gm -~ 10554 _+ 1530 x 103 ~m 3

insignificant with a Mann-Whitney U test. In the queen, as in the worker and drone, 4 main regions of the glomerular neuropil

were distinguished according to corresponding afferent bundles (Fig. 1): the anterior and dorsal region (tract T1), the intermediate region (tract T2), the ventral region (tract T3), and the posterior region (tract T4).

As in the worker, some of the ventral glomeruli formed a "lobule" which was recessed slightly from the main mass of glomeruli (Fig. 2).

The diameters of the main afferent bundles, T1 and T2, were identical in both the y.q. and the o.q. ('Fable 2).

2. Glomeruli

2.1. Structure. The intrinsic structure of the glomeruli in the queen is very similar to that previously described in the worker. The majority of glomeruli show a characteristic intensely staining cortical layer (Fig. 2). However, the seven giomeruli in the posterior region lack a cortical layer (Fig. 3).

2.2. Dimensions. Two aspects of the glomerular dimensions were considered: (i) the dimensions (diameter, volume) of each glomerulus of the antennal lobe in

2 y.q.; (ii) the volume of the total glomerular neuropil in 15 queens (8 y.q. and 7 o.q.). (i) The dimensions of all the glomeruli, e.g. their largest diameter and their volume,

varied little from one insect to the next (Fig. 4a, b). The glomeruli in the ventral region had a mean volume, which was 29.8% less than

those in the dorsal region. A similar percentage (29.0) is expressed in the worker (Table 3).

The 7 glomeruli in the posterior region, appear to be less intensely stained by cobalt than the other glomeruli. They were, however, among the most voluminous glomeruli of the antennal lobe. As in the worker bee, their mean volume was twice that of the dorsal glomeruli, and 3 times that of the ventral glomeruli.

(ii) The glomerular neuropil comprised 54.7% of the total volume of the neuropil of the antennal lobe in the y.q. and 54.3% in the o.q. This proportion was smaller, 44% in the worker bee (Arnold et al., 1985).

The total volume of the glomerular neuropil was 3923 + 371 x 10 3 p~m 3 (n = 8) for the

88 G. ARNOLD et al.

I

~ M G ; ~ L_ . . . .

~. ~ T1 ~ ~ ¢-~-:~

I

_,~'MG L_ . . . .

dorsal region ventral region intermediate region posterior region

FIG. 1. Schematic frontal drawing of antennal lobe of queen. Four main regions of glomerular neuropil have been distinguished according to corresponding afferent bundles: anterior and dorsal region; ventral region; intermediate region; posterior region. MG = Macroglomerulus; T1, T2, T3,

T4, = T1, T2, T3, T4 bundles.

TABLE 2. C O M P A R A T I V E S T U D Y OF T H E D I M E N S I O N S OF THE MEAN DIAMETER OF THE

T1 A N D T2 B U N D L E S BE T W E E N Y O U N G Q U E E N S A N D OLD Q U E E N S

Mean diameter of the T1 and T2 bundles

Young queen Old queen (8-day-old) (1-yr-old)

(n = 9) (n = 8)

T1 28.5 _+ 1.2 txm 30.4 _+ 0.9 txm

T2 10.5 _+ 0.8 txm 10.6 _+ 0.4 ixm

Antennal Lobe of the Queen Honeybee 189

Fw. 2. Comparative frontal sections of left antennal lobe of a queen (a, b) a worker (c) and a drone (d). Cellular staining with cobalt chloride. Organization of glomeruli (G) is very similar for queen and worker bees, except for a glomerulus (MG), which is relatively more developed in queen and could be a macroglomerulus. This is located in dorsal region, in a position similar to that of glomerulus D44 of worker (arrow-head) and glomerular complexes of drone (GC). Tracts TI and T 2 innervating dorsal and intermediate regions are respectively in a similar position in worker, drone, and queen. However, their cross-sectioned area varies, being largest in drone and smallest in queen, suggesting that number of sensory cells is lower in queen. Scale bar = 50 p,m. DTN =

deutoneurons; Lb = lobule: UN = central coarse neuropil. (c and d, from Arnold et al., 1985).

y.q. a n d 5730 + 754 x 103 tx 3 (n = 7) for the o .q . , r e p r e s e n t i n g an inc rease of 4 6 % for

the la t te r . T h e d i f f e r ence was s ign i f ican t ( P < 0 . 0 0 2 , M a n n - W h i t n e y U test) . Th i s i nc r ea se was i den t i c a l to the i nc r ea se of the to ta l v o l u m e of the n e u r o p i l ( i nc lud ing the n o n - g l o m e r u l a r n e u r o p i l ) , i .e. 4 7 % (see ab o v e ) .

2.3. Macrog lomeru lus . T h e v isual i den t i f i c a t i on of o n e very charac te r i s t i c bu lky g l o m e r u l u s , w/aich a lways o c c u p i e d the s a m e pos i t i on in the dorsa l b r a in r eg ion of the 31 q u e e n s s t u d i e d , l ed us to h y p o t h e s i z e tha t it cou ld be a m a c r o g l o m e r u l u s ( M G ) . Its v o l u m e in the ,_¢.q. a n d the o .q . was r e spec t ive ly 94069 + 8003 ~ m 3 (n -- 9) a n d 153453 +

90 G. ARNOLD et al.

FIG. 3. Frontal section of antennal lobe of queen honeybee showing posterior glomeruli (PG). Their structure is different from that of other glomeruli. C.L. = c6rtical layer; DTN = deutoneurones; G

= glomerulus.

Nb.(l.(%) 50

30

! i I

lO 30 50

Nb.gl.(~) D Queen No 2 ,L

~.~.,,, [Z]Queen No 4

• ~ ; ~ : ~

® ® 30 ~

• t i ~ ® ~

~gN/:

V.(.10 pm )

FIG. 4. Comparat ive distribution and frequency of glomerular diameter (a) and glomerular volume (b) in 2 g-day-old queens. Dimensions of all glomeruli vary little from insect to insect.

Antennal Lobe of the Queen Honeybee 191

TABLE 3. COMPARATIVE STUDY OF THE DIMENSIONS OF THE GLOMERULI BETWEEN 2 QUEENS AND 2 WORKERS

Mean glomerular volume

Queen Worker*

Absolute value Relative value Absolute valuee ° Relative value

(X 10 3 la, m 3) VG ( % ) ( × 10 3 la, m 3) VG ( % )

= V G VAL = V G VAL

Dorsal region 23.1 + 2.4 0.268 30.2 + 3.2 0.305 (n = 131) (n = 144)

Intermediate and ventral 16.4 + 1.5 0.190 21.2 + 1.8 0.214 regions (n = 171) (n = 173)

Posterior region 45.0 + 9.2 0.552 65.7 + 15.9 0.663 (n = 14) (n = 14)

Mean glomerular volume 20.5 +_ 1.5 0.238 27.0 _+ 2.0 0.272 (n = 316) (n = 331)

* According to Arnold et al. (1985).

22820 &m 3 (n = 8). The significant increase was 63% for the o.q. (P <0.002, M a n n - W h i t n e y U test). This volume represented respectively 1.32 + 0.16% (y.q.) and 1.46 + 0.15% (o.q . ) of the total volume of the neuropil . This glomerulus was 3.7 times greater than the mean g lomerular volume in the y.q. and 4.1 times larger in the old queen.

Moreover , when the macrog lomeru lus was compared to o ther voluminous glomeruli , the volume of the biggest of these glomeruli was always smaller, 59060 + 11572 ixm 3 in the y.q. and 85480 + 14601 ixm 3 in the o .q . , i.e. 63% and 56% of the volume of the MG, respectively.

The M G was located in a similar region (dorsal region) to the glomerulus D44 of the worker and to 3 of the 4 g lomerular complexes of the drone (GC1, GC2, GC3).

2.4. Number o f glomeruli. In the 3 insects analyzed in this respect, the number of glomerul i was respectively 150, 157 and 158 (mean = 155.3; SD = 8.7).

Deutocerebral efferents The axons of the deu toneu rons were ga thered into 4 tracts, which leave the antennal

lobe and end in the p ro toce reb rum. Their trajectories were similar in both the queen and the worker bee. Their main targets were the calyces of the m u s h r o o m bodies, and the lateral lobe of tile p r o t o c e r e b r u m (Fig. 5).

D I S C U S S I O N The organizat ion o f the antennal afferent pa thway of the queen bee is similar to that of

the worker . All but the 7 glomeruli in the poster ior region have a characteristic intensely staining cortical layer. The synapses be tween the sensory axons and the central neurons are confined mainly to this area (Boeckh et al., 1970; Masson, 1972; Pareto , 1972). The 7

192 G. ARNOLD etal.

FIG. 5. Frontal section of right half of brain of worker bee. Axons of deutoneurones are gathered into 4 tracts, which leave antennal lobe and end in protocerebrum. Three tracts are seen on this photomicrograph = MT, AMLT, PMLT. They project into lip (L) of calyces of mushroom bodies and in lateral lobe of protocerebrum (× 200). AL = antennal lobe; AMLT = anterior mediolateral tract; G = glomerulus; L = lip; LC = lateral calyx; LPTC = lateral lobe of protocerebrum; MC =

median calyx; MT = median tract; OE = oesophagus; PMLT = posterior mediolateral tract.

characterist ic poster ior g lomerul i described in this study have also been identif ied in both the worker and the d rone (Arno ld et al . , 1985). Thei r s tructure differs from that of all o ther g lomerul i in that they lack a cortical layer; this suggests that these glomeruli may be funct ional ly different f rom the others.

The 4 groups of sensory axon tracts innerva t ing the an tenna l lobe of the queen are homologous to those in the worker and drone. The cross-sectional area of the main tract (T1) is, however , smal ler in the queen , this is p robably because the queen has fewer an tenna l sensilla (Schenk, 1903; Mac Indoo , 1922).

Imprecis ion in coun t ing cannot explain the difference in number s of glomerul i found in the 3 individual queens analyzed. The results suggest a 5 .3% variabil i ty among

Antennal Lobe of the Queen Honeybee 193

individuals. In 5 worker bees, the inter-individual variability was 5.4% (Arnold et al. , 1985). Considered in terms of number, the postembryonic development of the majority of glomeruli is probably fixed by genetic factors. The process might be more plastic for a small minority, where, for instance, fusion or splitting of glomerular primordia might occur.

No significant difference is found between the numbers of glomeruli in the queen (155.3 + 8.7, n = 3) and in the worker (167.4 + 4.3, n = 5). Nevertheless, the standard deviation observed suggests that this result is mainly due to the small sample size.

In both the worker and the drone, an overall invariance of glomerular organization has been shown (Arnold et al . , 1985). A systematic study of the glomerular variability in the queen has not yet been done. However, the existence of 4 groups of afferent bundles as in the worker bee and the drone, the similarity in the number of glomeruli among individuals and the visual identification of some characteristic glomeruli, lead us to suggest an overall invariance of glomerular organization in the queen.

Although such a structure has never been reported in a female insect, the most voluminous glomerulus in the queen, could be a macroglomerulus. In other insects, such as moths and cockroaches, the hypertrophied glomerular structures, the glomerular complexes or macroglomeruli, receive only sexual information (Boeckh et al. , 1977; Hildebrand et al . , 1980; Ernst and Boeckh, 1983). A study using specific odours derived from drones as stimuli is necessary to determine the function of this large glomerulus in the queen honeybee.

It has been known for a long time that the queen is very attractive to drones during mating flights (Butler, 1971). However, it has never been demonstrated that a queen is attracted by drones nor that the drones emit sex pheromones.

In the worker bee, the most voluminous glomerulus (D 44) is also situated medially in the dorsal region (Arnold et al. , 1985). Because both the volume and the position of the most voluminous glomerulus in queens (the so-called macroglomerulus) and workers (the glomerulus D 44) are very similar, it seems probable that these glomeruli are homologous. Nevertheless the present data are not sufficient to confirm this suggestion.

In the worker bee, the volume of the giomerulus D 44 is bigger (103 + 25 x 103 i~m 3) than the volume of the MG of the young queen (94 + 8 x 103 i, zm 3, n = 9), but smaller than that of the old queen (153 + 23 x 103 i, tm 3, n -~ 8). However, when the relative value is expressed as the ratio of the giomerular volume to the total volume of the neuropil, the volume of this worker glomerulus D 44 (1.04 + 0.13%) is smaller than the queen MG both in the y.q. (1.31 + 0.16%) and the o.q. (1.46 _+ 0.15%).

However, as the life span is very different between the worker bee (4-5 weeks in summer and 4 months in winter) and the queen (4-5 yr), the comparisons of the volume of the antennal lobe are difficult.

The presence of the MG of the queen located in the same region of 3 glomerular complexes of the drone does not demonstrate their homology. Two other hypotheses should be considered: the MG of the queen could be homologous to another male glomerulus or the MG could be specific to the queen without a male homology.

The increase of the volume of the antennal lobe in the 1-yr-old queen ~s certainly not due to an overa]il growth of the central nervous structures, because the volume of the central body, used as a control, remains stable.

The increase of the glomerular neuropil (46%) is similar to the increase of the central coarse neuropil (47%). At the present time, it is not possible to assert if a particular class

194 G. ARNOLD et al.

of n e r v e cel ls is spec i f i ca l ly r e s p o n s i b l e fo r this i nc rease . T h e cen t r a l c o a r s e n e u r o p i l

cons is t s o f t h e a f f e r e n t axons ( t rac t s T t and T2), t he p r o c e s s e s o f a n t e n n a l l o b e n e u r o n s

and gl ial cel ls . A s t h e d i a m e t e r s o f t he T1 and T2 t rac ts a re s imi la r in y .q . and o . q . , it

s e e m s tha t t h e i n c r e a s e o f t he n e u r o p i l a r v o l u m e m a y be due to n e u r o n and glial cel l

p r o c e s s e s r a t h e r t h a n to a f f e r e n t axons .

T h e i n c r e a s e o f t he v o l u m e of t h e m a c r o g l o m e r u l u s is h i g h e r ( 6 3 % ) t h a n fo r t he m e a n

g l o m e r u l a r v o l u m e ( 4 6 % ) . I f t he M G is i m p l i c a t e d in t he spec i f ic p r o c e s s i n g r e l a t e d to

s exua l i n f o r m a t i o n , its i n c r e a s e a f t e r 1 yr is s o m e w h a t su rpr i s ing , b e c a u s e m a t i n g was

f in i shed a b o u t 1 yr p r e v i o u s l y . P e r h a p s t he m a c r o g l o m e r u l u s is a lso , o r m a i n l y , i n v o l v e d

in t he p r o c e s s i n g o f o t h e r b io log i ca l o l f a c t o r y s ignals , such as q u e e n o d o u r s o r c o l o n y

o d o u r s . It is ac tua l ly v e r y i m p o r t a n t fo r the (o ld) q u e e n to d e t e c t t he p r e s e n c e o f a n o t h e r

q u e e n , i n c l u d i n g h e r o w n d a u g h t e r s , to a v o i d an e n c o u n t e r , wh ich g e n e r a l l y ends in

f ights t ha t a r e o f t e n fa ta l . E x p e r i m e n t s are n o w in p r o g r e s s to tes t t h e s e d i f f e r e n t

a s se r t ions .

Acknowledgements--We thank Evelyne Leblond-Boughdad for technical assistance.

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