Odonatologica38(4): 329-340 December I, 2009

A comparative investigation of the antennal

sensilla in adult Anisoptera

M. Rebora*, S. Piersanti and E. Gaino

Dipartimentodi BiologiaCellulare e Ambientale,Università di Perugia,

Via Elce di Sotto, I-06123 Perugia, Italy

Received May 4, 2009 / Revised and Accepted July 9, 2009

A fine structural overview of the flagellar sensilla of forcipatus

(), Aeshna cyanea (Aeshnidae),Somatochlora metallica (Cordulidae)and

boltonii Cordulegaster (Cordulegastridae) revealed the presence of pits containing

sensilla located the latero-ventral typically on side of the first flagellar segments in

all four species. These sensilla are represented by coeloconic single-walled olfactory

sensilla and sunken sensilla deeply styloconica (type-1 and type-2) sharing common

features typicalof thermo-hygroreceptors. Sensilla styloconica arelocated inside deep

convoluted cavities. It is suggested that olfactory and thermo-hygrosensory sensilla

the main are sensilla on the antennae of all anisopteran families. The attribution of

the coeloconic sensilla of dragonfliesto single-walledolfactory sensilla (confirmed by

the finding of pore tubules in O. forcipatus), together with their common occurrence

in the suborder Anisoptera, are relevant for phylogenetic studies.

INTRODUCTION

“The face of is a practically nothing but eyes!”, as a Japanese haiku states. Indeed, are remarkable in their powers of vision (CORBET,

this the 1999). In regard, sensilla located on the antennae of Odonatahave been

An overview the antennal poorly investigated. early on flagellum of some Ani-

and & soptera Zygoptera species (SLIFER SEKHON, 1972) reports the pres- ence of coeloconic sensilla located in simple and compound cavities. Some behav- ioural studies on Orthetrum cancellatum (GEWECKE et ah, 1974; GEWECKE

& consider the and sites for ODENDAHL, 2004) scape pedicel as important air speed perception and flight control.

Recently, a finestructural investigation of the adults of the dragonfly Libellula

* Corresponding Author: e-mail [email protected]; - tel. ++390755855729; - fax ++390755855733 330 M. Rebora, S. Piersanti & E. Gaino

depressa (Libellulidae) performed by REBORA et al. revealed the (2008) pres- of sensilla located in ence pits on the latero-ventralside of the antennalflagellum.

sensilla These are represented by sensilla coeloconica and by deeply sunken sen-

silla styloconica. The structure of the sensilla coeloconica is coherent with that

for reported single-walled chemoreceptors. The deeply sunken sensilla are

kinds of sensilla represented by two styloconica sharing common features typi- cal of thermo-hygroreceptors.

The aims present paper to investigate whether the putative olfactory sensilla

and the two kinds of putative thermo-hygrosensory sensilla described in L. de-

in pressa are widespread Anisoptera. Thus, the sensilla located on the antennal

flagellum of adults belonging to Onychogomphus forcipatus (Gomphidae), Aesh- na cyanea (Aeshnidae), Somatochlora metallica(Cordulidae) and Cordulegaster boltonii (Cordulegastridae) are analyzed using scanning electron microscopy

(SEM), These four species, together with L. depressa (Libellulidae) (REBORA et al., 2008), represent the five Anisoptera familiesfound in Italy.

In order add information to on the internal structure of the above reported

sensilla, already described in L. depressa (REBORA et al., 2008), transmission electron microscopy (TEM) has been carried out on the antennae of O. forcipa-

tus, a common species in southern Europe (DIJKSTRA & LEW1NGTON, 2006)

belonging to the superfamily Aeshnoidea.

The results here of presented are part a programme on the fine structure of antennal sensilla in well Studies the zygopterans as as anisopterans. on sensory of in consideration biology , of their belonging to Paleoptera, are also useful for phylogenetic studies.

MATERIAL AND METHODS

Adult and Aeshna Onychogomphusforcipatus cyanea were collected in Umbria (central Italy) dur-

2007. Somatochlora metallica ing summer Dry and Cordulegasterboltonii specimens were investigated after a procedure of rehydration (ALBA-TERCEDOR, 1987).

In the laboratory, antennal flagella were dissected from anaesthetised specimens and fixed for 12 hours in 2.5% glutaraldehydein cacodylate buffer, pH 7,2.

For scanning electron microscopy (SEM) analysis, the fixed material was rinsed for three times in the same buffer, dehydratedusing a graded ethanol series and critical-point dryed in a CPD 030 Bal-

Tec critical-point dryer (Bal-Tec Union Ltd, Balzers, Liechtenstein). Specimens were mounted on stubs with silver with in Emitech K550X conducting paint, sputter-coated gold-palladium an sput- terer (Emitech, Ashford, England), and observed with a Philips XL30 SEM (Philips, Eindhoven, The

of 18kV. Netherlands), at anaccelerating voltage For observations of the inner cuticular wall of the antenna, the flagella were sectioned longitudinally with a razor blade and cleaned with KOH-solu- tion. These then in flagellawere dehydrated a graded ethanol series, dried in an oven and gluedonto the SEM specimen supports in order to allow the observation of the inner side of the antenna.

For transmission electron microscopy (TEM), the fixed antennal flagella were rinsed three times in buffer cacodylate and post-fixed for 1 hour at 4°C in 1% osmium tetroxide in cacodylate buffer.

Afterward the material was washed three times in the same buffer, dehydrated using a graded etha- nol series and embedded in an Epon-Aralditeresin mixture. Ultrathin sections, cut on a Leica EM Antennal sensilla in adult Anisoptera 331

UC6 ultracut (Leica Microsystem GmbH, Wien, Austria), were collected on formvar-coated cop-

stained with uranyl acetate per grids, and lead citrate, and examined with a Philips EM 208 (Philips, Eindhoven,The Netherlands).

RESULTS

OBSERVATIONS UNDER SEM

- The antenna consists of Onychogomphus forcipatus (Gomphidae). a scape, The a pedicel and a two-segmented flagellum. proximal flagellar segment is well

terms of its in developed (in sensory structures) comparison with the distal one and bears sensilla located in numerous pits on its latero-ventral side (Fig. la).

Most of these sensilla coeloconicawhile few pits (about 40) host a of them (about

2) are widerand represent the openings of large cavities inside the antenna (Figs

The sensilla coeloconica visible the la-c). are on antennal surface as pegs locat- ed in pits (Figs la, c, d). The cuticle of the peg bears pore-like structures clearly evident under the SEM (Fig. The cavities each measure about 40 Id). large pm in width and about 20 in The is convoluted and hosts pm depth. cavity very nu- merous type-1 and type-2 deeply sunken sensilla styloconica (Fig. 1c), bothchar-

wide acterized by a stylus bearing an apical cone (Fig. le). Type-1 sensilla have a cone with cuticular ‘fingers’ in its distal portion (Fig. le). Type-2 sensilla have

with cuticular surface a cone a rugged (Fig. le). No pore is visible on the cuticle of either type-1 or type-2 sensilla (Fig. le).

Aeshna — The consists of cyanea (Aeshnidae). antenna a scape, a pedicel and antennal an flagellum of four segments. The first (proximal) and the second flag- ellar show segments wide pits on their latero-ventral sides (Fig. If), with about 6

the first and on segment 3 on the second. Images of the inner cuticular wall re- veal that these wide the of pits are openings convoluted cavities, which measure about20 in width and 30-50 in pm pm depth (Fig. Ig). Longitudinally fractured cavities show coeloconic located the pegs on edge of the pits (Figs 1 h, i) and type-

1 and type-2 deeply sunken sensilla styloconica located inside the cavities (Fig.

The sensilla coeloconica bear their Ij). pore-like structures on surface (Fig. li).

Type-1 sensilla have a cone with cuticular ‘fingers’ in their distalportion (Fig. Ij).

sensilla have with cuticular surface No is Type-2 a cone a rugged (Fig. Ij). pore visible the on cuticle of either type-1 or type-2 sensilla (Fig. Ij).

Somatochlora metallica(Corduliidae). — The antenna consists of a scape, a and antennal of four pedicel an flagellum segments. The first (proximal) and the second their flagellar segments show, on latero-ventral sides, a number of pits

with about 40 the first and (Fig. 2a), on segment 3 on the second. The pits are isolated or in groups of two or three (Figs 2a, b) and most of them host sensilla coeloconica (Figs 2a, b, d), while some represent the openings of deep cavities

(Figs The sensilla coeloconica are evident on the antennal surface 2a-c). as pegs with pore-like structures on the cuticle (Fig. 2d). Each deep cavity is parallel to 332 M. Rebora, S. Piersanti & E. Gaino

Fig. 1. Longitudinallyfractured antennal flagella of Onychogomphusforcipatus(a-e) and Aeshna cya- nea (f-j) under SEM; (a) outercuticular wall of the first flagellar segment showing pits, on its latero-

ventral side, containingsensilla coeloconica; arrows point to the openings of large cavities bearing

deeply sunken sensilla styloconica. Scale bar 50 pm; — (b) inner cuticular wall showing the shape of

the cavities Scale bar — view of fractured large (arrows). 50 pm; (c) enlarged a cavity showing type-

sensilla bar - detail of sensillum I and type-2 deeply sunken styloconica. Scale 10 pm; (d) a coelo- Antennal sensilla in adult Anisoptera 333

the longitudinal axis of the antenna and measures about 15 jam in width and 70 in It is |am depth. very convolutedand hosts numerous type-1 and type-2 deeply sunken sensilla sensilla have styloconica (Fig. 2c). Type-1 a cone with cuticular

in its distal sensilla have with ‘fingers’ portion (Fig. 2e). Type-2 a cone a fairly

cuticular surface No is visible the of rugged (Fig. 20. pore on cuticle either type-

1 or type-2 sensilla (Figs 2e, f).

Cordulegaster boltonii - The (Cordulegastridae). antenna consists of a scape, and a pedicel an antennal flagellum of four segments. The first and the second flagellar segments show wide pits on their latero-ventral sides (Fig. 2g), with 9 and about on the first segment 3 on the second. Images of the inner cuticular wall reveal that the wide the pits are openings of convoluted cavities measuring about 20 in widthand 20-30 in pm pm depth (Fig. 2h). Longitudinally fractured cavities show located the of sensilla coeloconica on edge the pits (Fig. 2h, i), and and type-1 type-2 deeply sunken sensilla styloconica inside the cavities (Figs 2j-

The sensilla coeloconica bear k). pore-like structures on their surface (Fig. 2i). sensilla have Type-1 a cone with cuticular ‘fingers’ in its distal portion (Fig. 2j). sensilla with Type-2 have a cone a cuticular surface is rugged (Fig. 2k). No pore visible the cuticle of either on type-1 or type-2 sensilla (Figs 2j, k).

OBSERVATIONS UNDER TEM

Onichogomphus forcipatus (Gomphidae). - Longitudinal sections of one of the cavities reveal the large presence of type-1 and type-2 deeply sunken sensilla

the and styloconica inside cavity sensilla coeloconica on its edge (Fig. 3a).

SENSILLA COELOCONICA. The sensilla coeloconica are innervated by three unbranched whose neurons (Figs 3c-e), outer dendritic segments enter the

The three the peg (Fig. 3e). dendrites are enveloped by tormogen, the trichogen and the this last the dendrite and thecogen cell, secreting sheath containing a scolopale-like structure The dendritesheathends the (Fig. 3c). at base of the peg and the dendrites (Fig. 3b), are in contact with the sensillum lymph of medium

The cuticleof the shows wide electron-density (Fig. 3f). peg pore-like structures,

conicum with structures 2 pore-like the surface. Scale bar - (arrows) on peg pm; (e) detail of type-1 and type-2 sunken sensilla deeply styloconica showing the stylus and the cone; arrow points to the

cuticular fingersof the type-1 cone. Scale bar - 2.5 pm; (1) outercuticular wall of the first (proximal)

wide its latero-ventral - flagellar segment showing pits (arrows) on side. Scale bar 20 pm; (g) inner cuticular wall the of the cavities the Scale bar 50 showing shape (arrows) corresponding to pits. pm;

- (h) fractured sunken sensilla cavity showing deeply styloconica (arrow); sensilla coeloconica are located the — on edge of the pit. Scale bar 10 pm; (i) enlarged view showing the pore-like structures

(arrows) visible on the cuticle of sensilla - coeloconica. Scale bar 5 pm; (j) fractured cavity showing type-1 and type-2 sunken sensilla deeply styloconica; arrow points to the cuticular fingers oftype-1.

— — Scale bar 5 pm. [Co: cone; CS: coeloconic sensillum; — St: stylus; — Tl: type-1 deeply sunken — sensillum styloconicum; T2: type-2 deeply sunken sensillum styloconicum] 334 M. Rebora, S. Piersanti & E. Gaino

Fig. 2. Antennal flagella of Somatochlora metallica (a-f) and Cordulegaster boltonii (g-k) under SEM:

(a)outer cuticular wall ofthe first flagellar segmentshowing pits on its latero-ventral side containing sensilla the of cavities coeloconica; somepits are openings (arrows) deep hosting deeply sunken sen-

Scale — view silla styloconica. bar 50 pm; (b) enlarged showing sensilla coeloconica and the opening

(arrow) of a 10 — deep cavity. Scale bar pm; (c) longitudinallyfractured cavity showing type-1 and

sunken — type-2 deeply sensilla styloconica. Scale bar 20 pm; (d) detail of a sensillum coeloconicum Antennal sensilla in adult Anisoptera 335

at the base of which the continuity of the dense cuticulin layer is interrupted by actual In the sensillum pores (Fig. 31). lymph, between the pores and the den-

tubules about 20 in drites, pore measuring nm diameter, are clearly evident (Fig. 31).

SENSILLA STYLOCONICA. — sensilla Type-1 styloconica are innervated

four unbranched the cells by neurons enveloped by accessory (Figs 3g, h). The dendritic outer segments are enveloped by the dendrite sheath (Figs 3g-i), which

in disappears the apical portion of the cone (Figs 3j, k). Three dendrites enter the cone of the sensillum while the fourth one ends before (Figs 3h-j). The ac-

and cessory cells enter the stylus produce an enormous numberof electron-lucid vesicles strictly adhering to the dendrite sheath surrounding the outer dendritic

At the of the segments (Figs 3g-i). apex cone, the cuticle forms cuticular fingers

(Figs 3g, i-k). A cap-like structure, consisting of amorphous material, covers the

of the dendrites apex (Figs 3g, j, k). The cuticular fingers surround the cap-like structure at the tip of the cone No socket and (Figs 3g, k). no pores connecting the dendriteswith the outside are visible.

innervated Type-2 sensilla styloconica are by threeunbranched neurons envel-

the cells oped by accessory (Figs 31, m), the latter producing an electron-dense secretion interspersed amongthe microvilli of the labyrinth (Figs 31, m). One (in

sensilla of the dendrites before some two) three stops entering the cone. Thus two dendrites in sensilla (Fig. 3p), (but some only a single one. Figs 3n, o), enter the

where adherentdendrite cone, they are enveloped by atightly sheath in close con- tact with the surrounding cuticle. The cuticle of the cone is solid in its proximal portion (Fig. 3n) while it shows round holes in its distal portion (Figs 3o-p). The

of the cuticular apex cone shows a rough surface and a central, plugged molting

No socket and pore (Fig. 3q). no connection of the dendrites with the outside are visible.

No difference in the number and morphology of the described sensilla has been found in males and females of the four observed species.

with structures Scale bar 2 - pore-like (arrows). pm; (e) detail of a type-1 deeply sunken sensillum

styloconicum with cone and cuticular Scale 5 - stylus, apical fingers. bar pm; (0 detail of two type-

2 deeply sunken sensilla styloconica with stylus, cone and apical Scale bar 5 - moltingpore. pm; (g) longitudinallyfractured first flagellar article showingwide pits (arrows) on its latero-ventral side. Scale

bar 200 — pm; (h) enlarged view showing the shape of a cavity located in correspondence of one of the wide sensilla pits; coeloconica located the of the Scale bar 10 - are on edge pit. pm; (i) detail of

a sensillum coeloconicum with structures Scale bar 5 - detail pore-like (arrows). pm; (j) of a type- 1 deeply sunken sensillum styloconicum with stylus, cone and apical cuticular fingers (arrow). Scale bar 2 - (k) detail of a type-2 pm; deeply sunken sensillum styloconicum with stylus, cone and the

- molting Scale bar 2 - - — pore. pm. [CF; cuticular fingers; Co: cone; CS: coeloconic sensillum;

— — MP: St: Tl: sunken — moltingpore; stylus; type-1 deeply sensillum styloconicum; T2: type-2 deeply sunken sensillum styloconicum] 336 M. Rebora, S. Piersanti & E. Gaino

Fig. 3. Antennal flagellumof Onychogomphusforcipatus under TEM [a: cross section ofthe antennal flagellumat the level of a large cavity, — b-f; sensilla coeloconica, — g-k: type-1 deeply sunken stylo- conic sensillum, 1-q: type-2 deeply sunken styloconic sensillum]: (a) note the coeloconic sensillum (cir-

cle) in longitudinalsection on the antennal surface and the deeplysunken sensilla styloconica, type-1 - (double square) and type-2 (square) in cross section. Scale bar 5 pm; (b) sensillum coeloconicum Antennal sensilla in adult Anisoptera 337

DISCUSSION

The fine present structural investigation of the flagellar sensilla of Onychogom-

Aeshna phus forcipatus, cyanea, Somatochlora metallicaand Cordulegaster bolto-

nii, revealed that sensilla are located in pits on the latero-ventral side of the first

in all four These sensilla flagellar segments species. are represented by porous

coeloconic sensilla and deeply sunken sensilla styloconica (type-1 and type-2),

very similarto those described in Libellula depressa (REBORA et ah, 2008).

The porous coeloconic sensilla are always visible on the antennal surface but

their distribution differs in the different species. In the species belonging to the

superfamily Libelluloidea(S. metallicaand L. depressa ) most of the pits contain-

the coeloconic sensilla isolated. ing are In the superfamily Aeshnoidea, two of

the three analysed species (C. boltonii and A. cyanea) show coeloconic sensilla

on the edge of the opening of the convoluted cavities, while in the third species,

in section the dendrite at longitudinal showing sheath opening the base of the peg and the dendrites

entering the Scale bar 2 - cross at peg. pm; (c) section the level of the outer dendritic segments sur-

rounded the and the cell by thecogen, trichogen tormogen cells; thecogen contains a scolopale-like

Scale bar 2 — section the level of the dendritic structure. pm; (d) cross at outer segments surrounded

the dendrite sheath. Scale bar 1 - section by pm; (e) cross at the level of the peg; note the dendrites

without a dendrite sheath and the pore-like structures (arrows). Scale bar 1 pm; — (f) cross section at

the of level the peg showing that the continuity of the cuticulin layer at the base of the wide pore-like

structures is interruptedby actual the of tubules in the sensillum pores; note presence pore lymph.

Scale bar 500 — longitudinal nm; (g) section showing the dendrites entering the cone, surrounded

the dendrite sheath. In the contact by sensory cone the dendrites are in with a cap-like structure sur-

rounded by cuticular fingers; note the number of electron-lucid vesicles in the cells. large accessory

Scale bar 2 - section of the four dendrites the level of the pm; (h)cross at outer dendritic segments.

Scale bar 2 pm; - (i)cross section of the proximal portion ofthe coneshowing three dendrites enter-

the surrounded the dendrite sheath the ing cone, by (arrowhead); note accessory cell. Scale bar 1 pm;

— (j) cross section of the coneat a more distal level showing the dendrites, without dendrite sheath,

surrounded by amorphous material (arrow head). Scale bar 1 pm; - (k) apical cross section of the

the structure 1 - coneshowing cap-like surrounded by cuticular fingers. Scale bar pm; (1) longitudi-

nal section the dendrites the cone surrounded the dendrite sheath. In the showing entering by sensory

the dendrites in close contact with the cone are cuticle; arrow points to the clefts in the cuticle; arrow

head tothe electron-dense secretion in the cells. 2 - points accessory Scale bar pm; (m) cross section

of the three dendrites at the level of the outer dendritic segments surrounded by the dendrite sheath;

arrow head the electron dense secretion in the cells. Scale bar 1 - points to accessory pm; (n) cross

section of the cone showing one dendrite with the dendrite sheath strictly adheringto the surround-

cuticle. Scale bar — ing 500 nm; (o/p) subapical cross sections of the cone of two different sensilla

showing one and two dendrites surrounded the dendrite sheath in the (o) (p) by sensory cone; note

the round clefts in the cuticle. Scale bar 500 — nm; (q) apical cross section of the cone showing the - central pluggedmolting Scale bar 500 nm. — — C: Ca: - pore. [AC: accessory cell; cuticle; cap; - - - Cav: cavity; CF: cuticular fingers; CL: cuticulin layer; D: dendrites; - DS: dendrite sheath;

— MP: - MV; — Nu: nucleus of the — moltingpore; microvilli; accessory cell; OD: outer dendritic

— - PT: - segments; P: pores; pore tubules; Sc: scolopale-like structure; — SL: sensillum lymph;

— — Th: thecogen cell; To: tormogen cell; — Tr: trichogencell; — V: vesicles] 338 M. Rebora, S. Piersanti & E. Gaino

O. sensilla tend be forcipatus, coeloconic to isolated, in pairs or associated with the very large cavities. This last species differs from the others also in considera-

tion of the reduced number of the instead flagellomeres (two of four). In this re- it is worth gard, stressing that a molecular phylogenetic analysis of Anisoptera

(MISOF et al., 2001), reports that all the morphologically recognized families

and the are monophyletic Gomphidae are well differentiated from the others.

In all the analysed species the convoluted cavities always include the two kinds

of sensilla The cavities variable in styloconica. are number and shape and are

in O. where host particularly developed forcipatus they a high numberof sensilla styloconica.

The internal of the sensilla O. structure of forcipatus, as a representative of

Aeshnoidea, confirmed the fine structural characteristics already shown in L.

depressa (REBORA et al., 2008) and revealed some additional details. Its po-

rous coeloconicpegs are innervated by three unbranched dendrites, which enter

the the dendritesheath the base of the The has socket peg, ending at peg. peg no

and its cuticle shows wide pore-like structures at the base of which the cuticulin

layer is interrupted rise to actual Pore tubules giving pores. measuring 20 nm in diameter are clearly visible and closely resemble those described in the olfactory of other receptors (see review in STEINBRECHT, 1997). This confirms

the attribution of the coeloconic sensilla dragonfly to single-walled olfactory sen-

silla. In of no preparation L. was it to determinewhether depressa possible pore

tubules were actually present in the sensillum lymph (REBORA et al„ 2008).

The sunken sensilla of deeply styloconica O. forcipatus have no pores, an in-

flexible socket and unbrancheddendrites in close association with the cone wall,

showing features typical of thermo/hygroreceptors (reviews in ALTNER & LOF-

TUS, 1985,TICHY&FOETUS, 1996,STE1NBRECHT, 1998 and YOKOHAR1.

1999). Likewise in L. depressa et the (REBORA al., 2008), accessory cells show

secretory activity and contain electron-lucid vesicles in type-1 sensilla and elec-

tron-densematerial in type-2 sensilla. In the type-1 sensilla of O. forcipatus there

is alarge number of electron-lucid vesicles tightly adherentto the dendritesheath.

This material, probably lipoid in nature, has been noted in other insect sensilla

(ALTNERet al„ 1977; BARTLETetal., 1999;BINetal„ 1989;McIVER, 1974).

The location of inside cavities thermo/hygroreceptors deep on dragonfly anten-

nae mechanical and probably guarantees protection acts as a buffering system from the outside the air, protecting sensilla against exposure to random changes in humidity and temperature.

The above the reported data, together with observations on the antenna of L.

allow forward depressa (REBORA et al., 2008), us to the following considera- tions:

(1) Olfactory and thermo-hygrosensory sensilla are the main sensilla on the an-

tennae of Anisoptera. Thus, the small antennae of dragonflies could play an

important role in the biology of these insects. This role needs to be investi- Antennal sensilla in adult Anisoptera 339

gated with behaviouraland electrophysiological studies.

The of (2) in awide of presence thermo-hygroreceptors range anisopterans is im- that portant, considering dragonflies are typically heliothermic insects (MAY,

1976). The ability to perceive the microclimate conditions concerning tem-

perature and humidity is probably crucial in regulating basking behavior. The

structural differences of type-1 and type-2 deeply sunken sensilla, observed both in L. depressa and O. forcipatus, probably correspond to functional dif- ferences.

(3) The attributionof the coeloconic sensilla of dragonflies to single-walled ol-

sensilla the factory (confirmed by finding of pore tubules in O. forcipatus),

with their in together common presence the suborder Anisoptera, is rele-

vant for phylogenetic studies. Neuroanatomical studies on the insect brain

have allowed researchers that to hypothesize paleopteran insects, such as

and all Ephemeroptera Odonata, are probably anosmic with respect to air- borne odors, because they lack glomerular antennal lobes, typically receiv-

ing olfactory receptor neurons in Neoptera, and mushroom body calyces,

probably important for processing olfactory information (FARRIS, 2005;

STRAUSFELD et Recent studies the al, 1998). neuroanatomical on ground plan of the insect mushroom bodies claim that Odonatapossess a remnant

calyx equipped with microglomeruli receiving inputs from visual neurons

that reflect the of vision in the of may great importance ecology this group & (SVIDERSKY PLOTNIKOVA, 2004; STRAUSFELD et al., 2009). On

the other hand, the protocerebrum lateral lobe of these insects is connected

with the antennal nerve and could play an olfactory function according to

PLOTNIKOVA & ISAVNINA (2006). Further physiological, behavioural and

studies shed anatomical are necessary to light on this controversial field of

research to ascertain the supposed ability of dragonflies to perceive odors.

ACKNOWLEDGEMENTS

We aregratefulto Dr FABIO TERZANI for sending us specimens ofSomatochlora metalica and

Cordulegaster boltonii from his collection. Thanks to Dr ANGELO SPEZIALE for helping us to collect specimens of Onychogomphus forcipatus. This research was partially supported by FISR MI-

CENA funds.

REFERENCES

ALBA-TERCEDOR 1987. Une methode rammollir les J., simple pour etrehydrater Ephemeropteres

de collection piques a sec. Annls S.S.N.A. T. V. 39: 65-66.

ALTNER, H., H. SASS & I. ALTNER, between structure and function of 1977, Relationship an-

tennal chemo-, hygro-, and thermoreceptive sensilla in Periplaneta americana. Cell Tissue

Res. 176: 389-405.

ALTNER, H. & R. LOFTUS, 1985. Ultrastructure and function of insect thermo- and hygrorecep-

tors. Amu. Rev. Em. 30: 273-295. 340 M. Rebora, S. Piersanti & E. Gaino

BARTLET, E., R. ROMANI, I.H. WILLIAMS & N. ISIDORO, 1999. Functional anatomy of sen-

sory structures on the antennaeof Psylliodes chrysocephala L. (Coleoptera:Chrysomelidae).

Int. J. Insect Morphol. 28: 291-300.

BIN, F., S. COLAZZA, N. IS1DORO, M. SOLINAS & B. VINSON, 1989. Antennal chemosensilla

and glands and their possible meaning in the reproductive behaviour of Trissolcus basalis

(Woll.) (Hym., Scelionidae). Entomologica24: 33-97.

CORBET, P.S., 1999. Dragonflies: behaviour and ecology of Odonata. Harley Books, Colchester.

K.D.B. & R. DIJKSTRA, LEWINGTON, 2006. Field guideto the dragonfliesofBritain and Europe.

British Wildlife Publishing, Gillingham.

FARRIS, S.M., 2005. Evolution of insect mushroom bodies; old clues, new insights. ArthropodStruct.

Dev. 34:211-234.

GEWECKE, M. & A. ODENDAHL, 2004. The movement apparatus of the antennae of the drag-

onfly species Orthetrum cancellatum (Odonata: Libellulidae). Entomol. gen. 27(2): 73-85.

GEWECKE, M., H.G. HEINZEL & J. PHILIPPEN, 1974. Role of the antennae of the dragonfly

Orthetrum cancellatum in flight control. Nature 249: 584-585.

1976. and MAY, M.L., Thermoregulation adaptation to temperaturein dragonflies (Odonata: Ani-

soptera). Ecol. Monogr. 46: 1-32.

1974. Fine of the antennal McIVER, S.B., structure grooved pegs of the mosquito, Aedes aegypti.

Cell Tissue Res. 153: 37-337.

MISOF, B„ A.M. RICKERT, T.R. BUCKLEY, G. FLECK & K.P SAUER, 2001. Phylogenetic signals and its decay in mitochondrial SSU and LSU rRNA gene fragments of Anisoptera.

Mol. Biol. Evol. 18(1): 27-37.

PLOTNIKOVA, S.I. & I.L. ISAVNINA, 2006. Data in favor of possible olfactory function of the

antennal nerve and lateral lobe of protocerebrum of larva of the dragonfly Aeshna grandis.

J. evol. Biochem. Physiol 42: 338-341.

REBORA. M., S. PIERSANTI & E. GAINO, 2008. The antennal sensilla of the adult of Libellula

depressa (Odonata: Libellulidae). Struct. Dev. 37: 504-510.

SLIFER, E.H & S. SEKHON, 1972. Sense organs on the antennal flagella of damselflies and drag-

onflies (Odonata). Int. J. Insect Morphol. Embryol. 1: 289-300.

STEINBRECHT, R.A., 1997. Pore structures in insect olfactory sensilla: a review of data and con-

cepts. Int. J. Insect Morphol. Embryol. 26(3/4): 229-245.

STEINBRECHT, R.A., 1998. Bimodal thermo- and hygrosensitivesensilla. In: F.W. Harrison & M.

invertebrates 11B: Locke, [Eds], Microscopic anatomy of 405-422,

STRAUSFELD, N.J., L. HANSEN, Y. LI, R.S. GOMEZ& K. ITO, 1998. Evolution, discovery, and

interpretations of arthropod mushroom bodies. Learn Memory 5: 11-37.

STRAUSFELD, N.J., I. SINAKEVITCH, S. BROWN& S. FARRIS, 2009. Ground plan of the insect

J. mushroom body: functional and evolutionary implications. comp. Neurol. 513:265-291.

SVIDERSKY, V.L. & S.I. PLOTNIKOVA, 2004. On structural-functional organization of dragon-

mushroom bodies and considerations fly somegeneral about purpose of these formations. J.

evol Biochem. Physiol 40: 608-624.

TICHY, H. & R. LOFTUS, 1996. Hygroreceptors in insects and a spider: Humidity transduction models. Naturwissenschaften 83: 255-263.

YOKOHARI, E, 1999. Hygro- and thermoreceptors, /n: E. Eguchi & Y. Tominaga, [Eds], Atlas

of arthropodsensory receptors: dynamic morphology in relation tofunction, pp. 191-210, Springer, Berlin.