Pergamon In: J. Inse~~r Morphul. & b'mhrwl Vol. 26. No I. pp. 27-34, 1997

1’5 1997 Elsevier Science Ltd

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ULTRASTRUCTURE OF THE ANTENNAL SENSILLA OF QUEENSLAND FRUIT FLY, BACTROCERA TRYONI (FROGGATT) (DIPTERA: TEPHRITIDAE).

Craig D. Hull and Bronwen W. Cribb

Department of Entomology and the Centre for Microscopy and Microanalysis, The University of Queensland, 4072, Brisbane, Australia

(Received25 November 1996; accepted 17 January 1997)

Abstract-Antenna1 sensilla of the Queensland fruit fly, Bactrocera tryoni (Froggatt) (Diptera: Tephritidae) were examined using transmission electron microscopy. Six sensillar types were recognised: a multiporous double-walled type (Mp-dw), multiporous single-walled types (Mp-SW) (4 subtypes) and no-pore sensilla with inflexible sockets (Np-is). The Mp-SW sensilla were categorised on the basis of wall thickness and differences in wall, pore and dendrite structure. The Mp-dw sensilla are innervated by 2 or 3 unbranched dendrites. The Mp-SW thick-walled sensilla have 1 or 2 sensory cells, whose dendrites show limited branching within the shaft. The Mp-SW thin-walled sensilla are innervated by 2 or 3 sensory cells with dendrites that branch extensively within the shaft. The Np-is sensilla have not previously been described from tephritid antennae, and are found only in the antenna1 sensory pit. They have a granular appearance to the exterior walls and are innervated by 3 sensory cells, only 2 of which project dendrites into the hair lumen. The proposed functions of the sensilla are discussed. (CY 1997 Elsevier Science Ltd

Index descriptors (in addition to those in the title): Olfactory; thermoreceptor; hygroreceptor; multiporous; double-walled; single-walled; thick-walled; thin-walled; no-pore sensilla.

INTRODUCTION

The antennae are the primary olfactory organs for most

insects. For the Queensland fruit fly, Bactrocera tryoni, the sense of olfaction plays a role in many orientation behaviours, including oviposition and feeding (Fletcher

and Watson, 1974; Bateman and Morton, 198 1; Eise-

mann and Rice, 1992). Furthermore, many of the moni-

toring and control techniques for tephritid flies use

olfactory based behavioural manipulation (see Bateman,

1982; Drew, 1982). However, despite extensive research

on the techniques of behavioural manipulation, little is

known of the physiology of the antenna1 sensory appar- atus of B. tryoni. This paucity of information may impede

the development of new control strategies (Rice, 1989).

A knowledge of the morphology of the olfactory struc- tures is seen as a basis from which further research, such

as single-sensillum electrophysiology, can be conducted.

The external morphology of the antenna1 sensilla of B. tryoni has been characterised using scanning electron

microscopy (Giannakakis and Fletcher, 1985). The ante-

nna has numerous curved and tapering microtrichia that

are not innervated. The innervated sensilla are classified

into 6 types: sensilla chaetica, trichoid types I and II, basiconic, clavate and styloconic types. These are dis- tributed among the microtrichial hairs. However, the sen- silla chaetica were found only on the scape and pedicel, whereas the remaining types were found only on the funiculus (the 3rd antenna1 segment). The sensilla chae- tica are similar in external appearance to those in other species of Tephritidae, which have been shown to func-

tion as mechanoreceptors (Dickens et af., 1988). The external morphology of the funicular sensilla is similar to that found for other tephritid species, including B. dorsalis, B. oleae, B. cucurbitae, Ceratitis capitata and Anastrepha ludens (Dickens et al., 1988; Crnjar et al., 1989; Bigiani et al., 1989); however, various authors have

used differing terminologies. Among the Tephritidae, the internal ultrastructure of

the antenna1 sensilla of only B. dorsalis (Lee et al., 1995),

C. capitata (Mayo et al., 1987) and A. ludens (Dickens et al., 1988) has been reported. No work has been published on the internal ultrastructure of the antenna1 sensilla of B. tryoni. Furthermore, no studies, either external or

internal, have been published that examine the sensory pit of tephritid antennae. Studies on other Dipterans suggest that the sensory pit contains numerous sensilla (DuBose and Axtell, 1968; Itoh et al., 1991; Ross and

Anderson, 1991; Shanbhag et al., 1995), including no- pore sensilla with inflexible sockets (Np-is). The purpose of the present work is to determine the innervation and

wall structures of the funicular sensilla of B. tryoni in

preparation for electrophysiological studies.

MATERIALS AND METHODS Flies were cultured within the Department of Entomology, University

of Queensland. The culture was originally obtained from the Depart- ment of Primary Industries and the flies have been cultured for more than 20 generations. For scanning electron microscopy, antennae were removed from live flies using fine-point tweezers. The antennae were attached to stubs using double-sided sticky-tape. The antennae were vacuum dried over silica gel for 2 days. and then fixed overnight by

27

28 C. D. Hull and B. W. Cribb

exposing them to osmium tetroxide vapour above a 5% solution. The stubs were then sputter-coated with gold and examined in a Jeol6400F scanning electron microscope at 5 kV.

For transmission electron microscopy, the flies were immersed in a solution of 3% glutaraldehyde in 0.1 M cacodylate buffer. The antennae were then removed and each was cut into approximately 3 sections and left for 4 h at 4°C. The antenna1 sections were then washed in 0.1 M cacodylate buffer and post-fixed in 1% osmium tetroxide in 0.1 M cacodylate buffer, dehydrated through a graded series of acetone rang- ing from 30% to absolute, and then embedded in hard Spurr’s resin @purr, 1969). Thin sections were cut using a diamond knife and picked up with formvar-coated copper grids. Sections were stained with lead citrate and uranyl acetate. The preparations were viewed on a Jeol 1010 or 1210 transmission electron microscope using an 80 kV accelerating voltage. Measurements were taken from ten sensilla of each type and comprise the mean + 1 standard error.

RESULTS

The antenna is 3-segmented with an arista arising from the 3rd segment. The chemosensory hairs are found only on the 3rd segment (Fig. la). The hairs on the 3rd segment can be divided into 4 main types, based on their ultra- structure: non-innervated microtrichia, multiporous dou- ble-walled sensilla (Mp-dw), multiporous ‘single-walled sensilla (Mp-SW) and no-pore sensilla with inflexible sock- ets (Np-is). The Mp-SW sensilla can be divided into thick- walled and thin-walled types, and the thin walled sensilla can further be classified into 3 subtypes. The non-innerv- ated microtrichia have a curved and tapering exterior

Fig. 1. Sensilla from the external surface of the funiculus of Bactrocera tryoni showing multiporous double-walled sensilla (MD), multiporous single-walled thick-walled sensilla (T), 3 subtypes of multiporous single-walled thin-walled sensilla (Sl, S2 and S3) and non-innervated microtrichia (MT). A=antennal cuticle. Bar= 10pm. (b). Opening of the sensory pit on the 3rd antenna1 segment (arrowhead). Bar = 10 pm. (c). Antenna of B. tryoni showing scape (S), pedicel (PE), funiculus (F) (3rd antenna1 segment), arista (A) and sensory pit (arrowhead). Bar = 100 pm. (d). Transverse section of multiporous double-walled sensillum showing longitudinal ridges (L), inner wall (I), pore (arrowhead) and 3 dendrites (D). Bar = 100 nm. (e). Section proximal to a multiporous double-walled sensillum, near the ciliary region, showing 3 innervating dendrites (D). ISC = inner sheath cell, Bar = 200 nm. (f). Section through a multiporous

double-walled sensillum proximal to the base of the hair shaft. Note the electron-dense dendritic sheath (DS). Bar = 500 nm.

Ultrastructure of Antenna1 Sensilla of Queensland Fruit Fly 29

form, and show an obvious external grooving (Fig. la).

Also, there is a single sensory pit on the external lateral

surface of the 3rd segment (Fig. 1 b, lc). The sensory pit contains only Mp-dw and Np-is sensilla.

Mp-dw sensilla

Eight to 12 longitudinal ridges, arranged around the outside of the sensilla, form the characteristic grooved

peg shape of the Mp-dw sensilla (Fig. Id). Pores of these

sensilla are 27 + 2 nm wide at the narrowest point and lie between longitudinal ridges. The diameter of the longi-

tudinal ridges is 15Ok40 nm, and the inner walls are

58 f 3 nm thick (Fig. Id). Mp-dw sensilla are innervated by 2 or 3 dendrites proximal to the shaft base (Fig. le),

that become surrounded by an electron-dense dendritic sheath distally (Fig. If). No branching of the dendrites occurs in these sensilla.

Mp-SW thick-walled sensilla

The average thickness of the wall of the Mp-SW thick- walled sensilla is 255 f25 nm. The pores are lo+ 1 nm

wide and connect to the sensillar cavity through a gradu-

ally widening gap in the sensillar wall (Fig. 2a). Pore tubules are present near the constriction of the pore. The Mp-SW thick-walled sensilla have 1 or 2 sensory cells leading to 1 or 2 dendrites, respectively, in the sensillum (Fig. 2b). However, apical branching of the dendrites was

found in some Mp-SW thick-walled sensilla, producing up to 10 dendritic segments (Fig. 2~).

Mp-SW thin-walled sensilla

We can identify 3 subtypes of the Mp-SW sensilla, based

on differences in the wall, pore, and dendritic structures. Subtype 1. The walls of the subtype 1 Mp-SW thin-

walled sensilla are 115 + 3 nm, and also show a slight “pimpling” of the outer surface (Fig. 2d). The pores are 13 &- 1 nm wide at the narrowest point and often have a

distinct pore kettle, leading into several pore tubules. They are innervated by 2 or 3 sensory cells (Fig. 2e), and the dendrites are extensively branched within the shaft

(Fig. 2d). Subtype 2. Subtype 2 Mp-SW thin-walled sensilla have

thinner walls, which are 91+ 6 nm. The pores are

32+2 nm wide and have a pore kettle structure with

associated pore tubules (Fig. 20. They are innervated by 2 or 3 sensory cells (Fig. 2g), and the dendrites are

extensively branched (Fig. 20. Subtype 3. Subtype 3 Mp-SW thin-walled sensilla are

innervated by 3 sensory cells (Fig. 3a), and are charac- terised by a large dendrite that shows lamellar folding within the apical section (Fig. 3b, 3~). The dendrites of the other 2 sensory cells are extensively branched. The walls are 137 f 10 nm thick. The pores are 27 ) 2 nm wide and often show a pore kettle arrangement, with associ- ated pore tubules.

No-pore sensilla with inflexible sockets

The Np-is sensilla are found only within the sensory

pit. The sensory pit is multi-chambered, and expands

beneath the opening such that the sensory hairs at the base are not easily seen from the exterior. The opening of the pit is up to 17 pm wide (Fig. 3d), and the pit enlarges to 37pm inside. The Np-is sensilla are peg-shaped, and are characterised by the granular nature of their external

cuticle (Fig. 3e, 3g). The walls are 163 + 15 nm thick. No pores are present at the tip of the hair (Fig. 3f). An

electron-dense dendritic sheath is present. The sheath

starts just above the ciliary region, and ends at the base

of the hair (Fig. 3g). The sensilla are innervated by 3 sensory cells (Fig. 3h, 3i). Only 2 of the dendrites project

up into the lumen of the peg (Fig. 3g), and they do not branch. In cross-section, the dendrites fill up the entire hair lumen, and are in close contact with the cuticle of the sensillum (Fig. 3e). The inner surface of the wall,

around the dendrites, also shows distinct layering and the outer wall has numerous irregular channels. Occasionally, the irregular channels form small cavities

in the outer wall, but there is no connection to the outside.

DISCUSSION

Mp-dw sensilla

The Mp-dw sensilla correspond to the styloconic sen- silla found by Giannakakis and Fletcher (1985). Mp-dw sensilla have also been found on C. capitata (Levinson et

al., 1987) B. dorsalis (Lee et al., 1995) Simulium arcticum

(Sutcliffe et al., 1990), Drosophila melanogaster (Ven- katesh and Singh, 1984) Aedes aegypti (Diptera: Cul- icidae) (McIver, 1974; Cribb and Jones, 1995) and Delia

radicum (Ross and Anderson, 1987). Functional inves-

tigations of Mp-dw sensilla from Diptera are limited in number. The Mp-dw sensilla of Ae. aegypti have been

shown to contain both excitatory and inhibitory neurons responding to lactic acid (a known host attractant), and to have neurons responding to various other environ- mental volatiles (Davis and Sokolove, 1976). Some of the sensory cells within Mp-dw sensilla from other insect groups have been found to respond to odours emanating

from food or oviposition sites, with most sensilla also containing a thermosensory cell (Altner and Loftus, 1985). Owing to the similarity in structure, these sensilla

in B. tryoni may respond to odours and temperature changes. The channel-like structure of the pore and

absence of pore tubules found for the Mp-dw sensilla of

B. tryoni are typical features of double-walled sensilla (Altner and Prillinger, 1980).

Mp-SW thick-walled sensilla Mp-SW thick-walled sensilla, corresponding to the

trichoid type I sensilla of Giannakakis and Fletcher (1985) are common across a wide variety of insect groups, and are known to respond to environmental odours (such as the short-chain alcohols, esters and aldehydes arising

30 C. D. Hull and B. W. Cribb

d

PK

Fig. 2. Transverse section through a multiporous single-walled thick-walled sensillum with 2 dendrites (D). P=pore; PT= pore tubules. Bar = 100 nm. (b). Section proximal to the base of a multiporous single-walled thick-walled sensillum, near the ciliary region, showing 2 inner dendritic segments (Cl, C2). Bar=200 nm. (c). Transverse section through the apical region of a multiporous single-walled thick-walled sensillum. Note the multiple dendrites (D) indicating branching within the shaft. Bar = 100 nm. (d). Transverse section of a multiporous single-walled thin-walled subtype 1 sensillum. Note the texture of the external cuticle with its numerous raised “pimples” (PM). D=dendrite; P=pore; PK=pore kettle, with associated pore tubules. Bar= 100 nm. (e). Section proximal to the base of a multiporous single-walled thin-walled subtype 1 sensillum, at the level of the ciliary region, showing 2 innervating dendrites (D) surrounded by an inner sheath cell (ISC). Bar = 200 nm. (f). Transverse section through a multiporous single-walled thin-walled subtype 2 sensillum. D = dendrite; P = pore; PK = pore kettle, with associated pore tubules. Bar = 100 nm. (g). Section proximal to the base of a multiporous single-walled thin-walled subtype 2 sensilhun at the level of the ciliary region. Two dendrites (D) are surrounded by an

inner sheath cell (ISC). Bar = 200 nm.

from plant material) and to pheromones (Altner and distal region of Mp-SW thick-walled sensilla of A. Zudens Prillinger, 1980; Steinbrecht, 1987). The branching of the (Dickens et al., 1988). The functional significance of the dendrites in the Mp-SW thick-walled sensilla of B. tryoni dendritic branching in the Mp-SW thick-walled sensilla of contrasts with both B. dorsalis (Lee et al., 1995) and C. B. tryoni and A. ludens is yet to be determined. However, capitata (Mayo et al., 1987) where no branching was Mellor and Anderson (1995) suggest that the increased found. However, dendritic branching was found in the surface area of branched dendrites may be an adaptation

Ultrastructure of Antenna1 Sensilla of Queensland Fruit Fly 31

e

Fig. 3. Oblique section near the ciliary region, proximal to a multiporous single-walled thin-walled subtype 3 sensillum, showing 3 inner dendritic segments (Cl, C2 and C3). ISC = inner sheath cell. Bar = 500 nm. (b). Transverse section of a multiporous single-walled thin-walled subtype 3 sensillum through the basal region of the hair shaft. Note the large, unbranched dendrite (D) surrounded by branched dendrites. P = pore; PK = pore kettle, with associated pore tubules. Bar = 200 nm. (c). Transverse section of a multiporous single-walled thin-walled subtype 3 sensillum through the apical region of the hair shaft. Note that the largest dendrite has numerous lamellar foldings (LM). Bar = 200 nm. (d). Section through the 3rd antenna1 segment showing the sensory pit. The pit is arranged into distinct chambers (CH) that open into one large cavity (not shown). OP=opening of pit. Bar=5 pm. (e). Section through a no-pore sensillum with an inflexible socket. The external cuticle has a granular surface structure(G). In the shaft are 2 dendrites(D), surrounded by distinct layering of the cuticle (arrowhead). Within the cuticular wall are irregular channels (CL). Bar= 100 nm. (f). Section through the tip of a no-pore sensillum with an inflexible socket (arrowhead), showing the lack of a terminal pore. Bar = 100 nm. (g). Oblique section through a no-pore sensillum with an inflexible socket. The dendritic sheath (DS) ends at the base of the hair shaft. D=dendrites; G=granular external cuticle. Bar= SOOnm. (h). Section of a no-pore sensillum with an inflexible socket proximal to the base of the dendritic sheath (DS), showing the dendrites of 3 sensory cells (D). ISC = inner sheath cell. Bar = 200 nm. (i). Section proximal to a no- pore sensillum with an inflexible socket through the dendritic sheath (DS) showing the arrangement of the 3 dendrites (D) within.

ISC = inner sheath cell. Bar = 200 nm.

32 C. D. Hull and B. W. Cribb

to increase the sensitivity of the sensory cell. In C. capitata the Mp-SW thick-walled sensilla have been found to respond to trimedlure (a known attractant) (Dickens et al., 1988), and on female flies they respond to the male sex pheromones (Levinson et al., 1990). It is likely that the Mp-SW thick-walled sensilla of B. tryoni respond to pheromones, and maybe also to odours emanating from the environment.

Mp-SW thick-walled sensilla in insects generally, do not have pore kettle structures, and if pore tubules are visible they generally end at the apex of the opening in the cuticular wall (Zacharuk, 1980). The poor resolution of the pore tubules in this paper is likely to be due to the fixation technique used. Pore tubules were more evident in the trichoid sensilla of Ae. aegypti (Diptera: Culicidae) when fixed with Dalton’s fixative, freeze drying or nega- tive staining compared with glutaraldehyde fixation or cryo-prepared specimens (Muir and Cribb, 1994). However, it was not the main objective of this paper to determine the stimulus conducting mechanisms of the sensilla; therefore, further preparations using different fixation techniques were not conducted.

Mp-SW thin-walled sensilla Subtype 1. The distinction between the subtype 1 and

subtype 2 Mp-SW thin-walled sensilla is based on the pore size, pore density, and the pimpled outer wall of the subtype 1 sensilla. The subtype 1 Mp-SW thin-walled sen- silla correspond to trichoid type 2 sensilla of Giannakakis and Fletcher (1985). However, the pimpled outer wall was not mentioned in the scanning work of Giannakakis and Fletcher (1985). The comparative sizes for the pores of the Mp-SW thin-walled sensilla correspond roughly with the figures obtained by Giannakakis and Fletcher (1985) but are slightly smaller (e.g., 12.0nm versus 2& 25 nm for subtype 1 sensilla). The discrepancy is probably due to the use of transmission microscopy, which allowed us to see the pores at their narrowest point. The pore kettle structures and pore tubules evident in the subtype 1 Mp-SW thin-walled sensilla most likely have a role in conducting odour molecules towards the dendrites (Kaissling, 1986; Steinbrecht, 1987; Popov et al., 1994).

Subtype 2. The subtype 2 Mp-SW sensilla correspond to the basiconic sensilla of Giannakakis and Fletcher (1985). Among other Dipterans, sensilla corresponding to the subtype 2 Mp-SW thin-walled sensilla, in terms of external and internal morphology, are also found on the face fly, Musca autumnalis (Bay and Pitts, 1976), De. radicum (Ross and Anderson, 1987), D. melanogaster (Venkatesh and Singh, 1984).

The term basiconica has also been used to describe a variety of sensilla types based solely on external mor- phology. However, such nomenclature is unrep- resentative of wall structure, making comparisons across sensilla basiconica from such studies inaccurate. Some sensilla basiconica are double-walled, whereas others are single-walled. Using a nomenclature based on func-

tionally relevant ultrastructural characters should allevi- ate much of the confusion (Altner and Prillinger, 1980).

Owing to the multiple pores in the walls, and putative- stimulus conducting structures, the subtype 2 Mp-SW thin-walled sensilla are also likely to be olfactory sensilla. However, the exact function of these sensilla in the higher Dipterans is yet to be determined.

Subtype 3. The lamellar membrane structure present in the dendrites of the subtype 3 Mp-SW thin-walled sen- silla is also present in B. dorsalis (Lee et al., 1995) and C. cupitata (Mayo et al., 1987). The lamellated dendrites are found in the Mp-SW thin-walled sensilla that have a clubbed or bulbous tip, in this case corresponding to the clavate type of Giannakakis and Fletcher (1985). Similar dendritic structures have also been found in antenna1 sensilla of the sand fly Cu.furens (Chu-Wang et al., 1975) Ae. aegypti (McIver, 1972) and S. arcticum (Sutcliffe et al., 1987). Because lamellated dendrites are the only com- mon sensory feature from a variety of insects that are known to respond to carbon dioxide, Sutcliffe (1994) suggests that carbon dioxide receptivity is the primary purpose of these dendrites. The position of the lamellated dendrites within multiporous sensilla, thus allowing easy access of the carbon dioxide molecules to the dendrites, also supports this hypothesis. However, the transduction mechanisms of the lamellate dendrites are not yet known. Furthermore, where lamellated dendrites are found in aporous sensilla they are usually considered to act as thermoreceptors (Altner and Loftus, 1985). The role of carbon dioxide sensitivity for B. tryoni may be to aid in plant location, as has been proposed for male S. arcticum (Sutcliffe et al., 1987) or to provide an escape reaction from vertebrate predators (Rice, 1989). Sensilla on the antennae of Ae. aegypti (Kellogg, 1970) and the tsetse fly Glossina palpalis (Bogner, 1992) that contain carbon dioxide sensitive neurons also contain sensory cells that respond to general environmental odours, such as octenol, butanone and p-cresol. Therefore, we suspect that the other dendrites in the subtype 3 Mp-SW thin- walled sensilla of B. tryoni respond to general environ- mental odours.

No-pore sensilla with inflexible sockets Np-is sensilla generally contain a combination of

thermo- and hygroreceptors. Based on the similarities in ultrastructure between the sensilla described by Altner and Loftus (1985) and the Np-is sensilla of B. tryoni, the dendrites of the 2 sensory cells that enter the lumen of the cuticular hair may be 2 hygroreceptive units, 1 responding to dry air and the other to moist air. Whilst no lamellate foldings of the 3rd sensory cell dendrite were obvious, it may act as a thermoreceptor. Such a combination of sensory cells is generally referred to as a “triad” (Altner and Prillinger, 1980). Among the Diptera, Np-is sensilla that have similar dendritic structure to those reported here have also been found on S. arcticum (Sutcliffe et al., 1990) Ae. aegypti (Davis and Sokolove, 1976; McIver and Siemicki, 1979) De. radicum (Ross and

Ultrastructure of Antenna1 Sensilla of Queensland Fruit Fly 33

Anderson, 1991) and D. melanogaster (Shanbhag et al., 1995).

The confinement of the Np-is sensilla to the sensory

pit suggests that their position is somehow related to their function. Perhaps the pit structure affects the flow of air into the pit, and thus acts as a buffering system from the

outside air. The sensilla would then be less exposed to random changes in humidity and temperature brought about by the movement of air currents over the hair

surface. The concentric layering of the inner cuticular wall and

the irregular channels and caverns within the outer

cuticular wall are often seen in these types of sensilla

(Altner et al., 1981; Haug, 1985; Steinbrecht, 1989; Ste- inbrecht and Miiller, 1991). The function of these struc-

tures is not clear, but it is likely that they are part of the

sensory transduction mechanism. The granular external surface is a rare feature of Np-

is sensilla. Generally, the exterior surface of Np-is sensilla is smooth, and if external grooves are present they are

very shallow (Zacharuk, 1985). Three species of Hip- prlates eye gnats (Diptera: Chloropidae) were also reported to have granular-walled Np-is sensilla located

in antenna1 sensory pits (DuBose and Axtell, 1968).

Irregular sculpturing of sensillum walls has also been

found in D. melanogaster (Itoh et al., 1991), Bombqlx mori (Steinbrecht and Miiller, 1991) and the butterfly, Troides rhadamanthus plateni (Schmitz and Wasserthal, 1993). The function of the granular walls is unknown. However, hygroreceptive dendrites are generally thought to func- tion like mechanoreceptors, responding to deformations in the cuticle brought on by changes in water content

(Altner and Loftus, 1985). Therefore, the granular walls

of the Np-is sensilla may act to increase the surface area for absorption or evaporation of water, thus increasing

the sensitivity of the transduction mechanism.

The determination of the innervation of the various sensillar types of B. tryoni provides us with the basis

for electrophysiological experiments, that we will use to define the functional significance of the sensory cells.

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