Comparison of auditory sense organs in parasitoid Tachinidae (Diptera) hosted by Tettigoniidae (Orthoptera) and homologous structures in a non-hearing Phoridae (Diptera)

The dipteran parasitoids Therobia leonidei and Homotrixa alleni (Tachinidae) use acoustic cues to locate their calling tettigoniid (Ensifera, Orthoptera) hosts. The sexually dimorphic tympanal organs of both fly species are located at the prosternum. For comparison a homologous chordotonal organ in the non-hearing fly Phormia regina, Meigen (Phoridae) is also described. The scolopidial sense organs of the ears have approximately 180 sensory cells in Th. leonidei and 250 cells in H. alleni. Interspecific analysis indicates that the cell number and arrangement might be genus specific in Tachinidae. The mononematic scolopidia, each with one sensory cell, are of different sizes and insert at the tympanal membrane. Large scolopidial units (diameter of sensory cells up to 50 μm) extend longitudinally from the centre of the sensory organ towards the ligament, whereas small units (sensory cell diameter up to 10 μm) are arranged sequentially within the sensory organ. This arrangement is discussed to be a possible basis for frequency discrimination. The ultrastructure of the scolopidia is similar in the hearing and non-hearing flies. In both groups, the majority of scolopales has a diameter from 2 to 2.9 μm, although hearing species have additionally wider scolopales. The homologous chordotonal organ of Ph. regina consists of approximately 55 sensory cells of uniform direction. The data are discussed in comparison to the ears of other Diptera.     

Evolution of the metathoracic tympanal ear and its mesothoracic homologue in the Macrolepidoptera (Insecta)

Two independent methods of comparison, serial homology and phylogenetic character mapping, are employed to investigate the evolutionary origin of the noctuoid moth (Noctuoidea) ear sensory organ. First, neurobiotin and Janus green B staining techniques are used to describe a novel mesothoracic chordotonal organ in the hawkmoth, Manduca sexta, which is shown to be serially homologous to the noctuoid metathoracic tympanal organ. This chordotonal organ comprises a proximal scolopidial region with three bipolar sensory cells, and a long flexible strand (composed of attachment cells) that connects peripherally to an unspecialized membrane ventral to the axillary cord of the fore-wing. Homology to the tympanal chordotonal organ in the Noctuoidea is proposed from anatomical comparisons of the meso- and metathoracic nerve branches and their corresponding peripheral attachment sites. Second, the general structure (noting sensory cell numbers, gross anatomy, and location of peripheral attachment sites) of both meso- and metathoracic organs is surveyed in 23 species representing seven superfamilies of the Lepidoptera. The structure of the wing-hinge chordotonal organ in both thoracic segments was found to be remarkably conserved in all superfamilies of the Macrolepidoptera examined except the Noctuoidea, where fewer than three cells occur in the metathoracic ear (one cell in representatives of the Notodontidae and two cells in those of other families examined), and at the mesothoracic wing-hinge (two cells) in the Notodontidae only. By mapping cell numbers onto current phylogenies of the Macrolepidoptera, we demonstrate that the three-celled wing-hinge chordotonal organ, believed to be a wing proprioceptor, represents the plesiomorphic state from which the tympanal organ in the Noctuoidea evolved. This ’trend toward simplicity’ in the noctuoid ear contrasts an apparent ’trend toward complexity’ in several other insect hearing organs where atympanate homologues have been studied. The advantages to having fewer rather than more cells in the moth ear, which functions primarily to detect the echolocation calls of bats, is discussed. Accepted: 18 June 1999     

Bimodal innervation of the infrared organ of Merimna atrata (Coleoptera,Buprestidae) by thermo- and mechanosensory units

The pyrophilous Australian “fire-beetle” Merimna atrata approaches forest fires and possesses abdominal infrared (IR) organs. Each round IR organ is centrally innervated by a sensory complex showing two different units: one thermoreceptive multipolar neuron and one mechanosensitive chordotonal organ (CO) consisting of two scolopidia. We investigated the CO and found that the scolopidia are mononematic (the scolopale cap remains below the cuticle) and monodynal (one sensory cell per scolopidium). The dendrites of the scolopidia extend anteriorly and are attached by their caps to the cuticle about in the middle of the absorbing area. Structural features at the site of innervation suggest that the CO measures minute thermal deformations caused by IR absorption. Therefore, an additional photomechanic component which has been described for the IR receptors of pyrophilous jewel beetles of the genus Melanophila can be proposed for the IR organ of Merimna. Because scolopidia can measure displacements in the subnanometer range, the CO may enhance the sensitivity of the IR organ. The sensory complex of the Merimna IR organ shows the same units and similar cuticular modifications as the tympanal organs of some noctuid moths. Therefore, a parallel evolution of insect ears and the Merimna IR organ is discussed.     

The tympanal hearing organ of the parasitoid fly Ormia ochracea (Diptera, Tachinidae, Ormiini)

Tympanate hearing has evolved in at least 6 different orders of insects, but had not been reported until recently in the Diptera. This study presents a newly discovered tympanal hearing organ, in the parasitoid tachinid fly, Ormia ochracea. The hearing organ is described in terms of external and internal morphology, cellular organization of the sensory organ and preliminary neuroanatomy of the primary auditory afferents. The ear is located on the frontal face of the prothorax, directly behind the head capsule. Conspicuously visible are a pair of thin cuticular membranes specialized for audition, the prosternal tympanal membranes. Directly attached to these membranes, within the enlarged prosternal chamber, are a pair of auditory sensory organs, the bulbae acusticae. These sensory organs are unique among all auditory organs known so far because both are contained within an unpartitioned acoustic chamber. The prosternal chamber is connected to the outside by a pair of tracheae. The cellular anatomy of the fly's scolopophorous organ was investigated by light and electron microscopy. The bulba acustica is a typical chordotonal organ and it contains approximately 70 receptor cells. It is similar to other insect sensory organs associated with tympanal ears. The similarity of the cellular organization and tympanal morphology of the ormiine ear to the ears of other tympanate insects suggests that there are potent constraints in the design features of tympanal hearing organs, which must function to detect high frequency auditory signals over long distances. Each sensory organ is innervated by a branch of the frontal nerve of the fused thoracic ganglia. The primary auditory afferents project to each of the pro-, meso-, and metathoracic neuropils. The fly's hearing organ is sexually dimorphic, whereby the tympanal membranes are larger in females and the spiracles larger in males. The dimorphism presumably reflects differences in the acoustic behavior in the two sexes.     

The tympanal hearing organ of the parasitoid fly Ormia ochracea (Diptera,Tachinidae, Ormiini)

Tympanate hearing has evolved in at least 6 different orders of insects, but had not been reported until recently in the Diptera. This study presents a newly discovered tympanal hearing organ, in the parasitoid tachinid fly, Ormia ochracea. The hearing organ is described in terms of external and internal morphology, cellular organization of the sensory organ and preliminary neuroanatomy of the primary auditory afferents. The ear is located on the frontal face of the prothorax, directly behind the head capsule. Conspicuously visible are a pair of thin cuticular membranes specialized for audition, the prosternal tympanal membranes. Directly attached to these membranes, within the enlarged prosternal chamber, are a pair of auditory sensory organs, the bulbae acusticae. These sensory organs are unique among all auditory organs known so far because both are contained within an unpartitioned acoustic chamber. The prosternal chamber is connected to the outside by a pair of tracheae. The cellular anatomy of the fly's scolopophorous organ was investigated by light and electron microscopy. The bulba acustica is a typical chordotonal organ and it contains approximately 70 receptor cells. It is similar to other insect sensory organs associated with tympanal ears.The similarity of the cellular organization and tympanal morphology of the ormiine ear to the ears of other tympanate insects suggests that there are potent constraints in the design features of tympanal hearing organs, which must function to detect high frequency auditory signals over long distances. Each sensory organ is innervated by a branch of the frontal nerve of the fused thoracic ganglia. The primary auditory afferents project to each of the pro-, meso-, and metathoracic neuropils. The fly's hearing organ is sexually dimorphic, whereby the tympanal membranes are larger in females and the spiracles larger in males. The dimorphism presumably reflects differences in the acoustic behavior in the two sexes.     

The structure and properties of an abdominal chordotonal organ in Carausius morosus and Blaberus discoidalis

Each side of the abdominal segments of the stick insect Carausius morosus contains a chordotonal organ lying longitudinally in a ventro-lateral position. These ventro-lateral chordotonal organs each possess two nerve cell bodies and two scolopales. There is a single attachment strand to the cuticle.Electrical recordings from the receptors show that they respond in a highly phasic manner to both stretching and subsequent relaxation of the attachment strand. They are sensitive to substrate vibration but are activated by ventilatory movements. The effects of ramp and square wave stimulation are examined. The rôle of the ventro-lateral chordotonal organs as ventilatory receptors is discussed and abdominal chordotonal organs of insects in general are reviewed.The ‘ventral phasic receptors’ of the cockroach are re-examined and shown to be chordotonal organs. They are re-named ‘mid-ventral’ chordotonal organs.     

The tympanal hearing organ of a fly: phylogenetic analysis of its morphological origins

A key adaptation for any parasitoid insect is the sensory modality that it uses to locate its host insect. All members of the speciose family Tachinidae (Diptera) are parasitoids, but only flies of the tribe Orminini use acoustic cues to find their hosts. Ormiine flies are parasitoids of various genera of crickets and katydids. Gravid females of one ormiine species, Ormia ochracea, hear the reproductive calling song of male field crickets and home in on those calls to locate their hosts. While many flies possess various kinds of ears to detect airborne sounds, only ormiine flies have been reported to possess true tympanal hearing organs. Such organs are wellknown to occur in their cricket and katydid hosts. The ormiine ear is an evolutionary innovation within Diptera. Our objective was to trace the phylogenetic origins of the tympanal hearing organ among higher flies. Since the ormiine hearing organ is a complex organ within the prothorax, we examined possible precursor structures in the prothoraces of selected Diptera. We have uncovered a suite of characters that define the ormiine ear. These characters in the prothorax include a pair of prosternal tympanal membranes, a pair of chordotonal sensory organs, and modifications of the tracheal system. We have been able to identify and trace the presumptive homologs of these ormiine characters through selected species of related Diptera, using the method of outgroup comparison.Dedicated to the memory of Dr. Edmund A. ArbasThis work was supported by grants from NIH (5RO1 DC 00103), NIMH (IKOS MH01148-01), NSF (240-1879A) and Hatch (NYC-191403) to R.R.H. and the Swiss Science Foundation and the Janggen-Pöhn Foundation to D.R.     

The metathoracic wing-hinge chordotonal organ of an atympanate moth,Actias luna (Lepidoptera,Saturniidae): a light- and electron-microscopic study

Summary The structure of a simple chordotonal organ, the presumed homologue of the noctuoid moth tympanal organ, is described in the atympanate moth, Actias luna. The organ consists of a proximal scolopidial region and a distal strand, which attaches peripherally to the membranous cuticle ventral to the hindwing alula. The strand is composed of elongate, microtubule-rich cells encased in an extracellular connective tissue sheath. The scolopidial region houses three mononematic, monodynal scolopidia, each comprised of a sensory cell, scolopale cell, and attachment cell. The dendritic apex is octagonally shaped in transverse section, its inner membrane lined by a laminated structure reminiscent of the noctuoid tympanal organ collar. A 9+0-type cilium emerges from the dendritic apex, passes through both the scolopale lumen and cap, and terminates in an extracellular space distal to the latter. Proximal extensions of the attachment cell and distal prolongations of the scolopale cell surrounding the cap are joined by an elaborate desmosome, with which is associated an extensive electron-dense fibrillar plaque. Within the scolopale cell, this plaque constitutes the scolopale rod material. The data are discussed in terms of both the organ's potential function, and its significance as the evolutionary proto-type of the noctuoid moth ear.     

Otoacoustic emissions in bushcricket ears: general characteristics and the influence of the neuroactive insecticide pymetrozine

The tympanal organ of the bushcricket Mecopoda elongata emits pronounced distortion-product otoacoustic emissions (DPOAEs). Their characteristics are comparable to those measured in other insects, such as locusts and moths, with the 2f1–f2 emission being the most prominent one. Yet the site of their generation is still unclear. The spatial separation between the sound receiving spiracle and the hearing organ in this species allows manipulations of the sensory cells without interfering with the acoustical measurements. We tried to interfere with the DPOAE generation by pharmacologically influencing the tympanal organ using the insecticide pymetrozine. The compound appears to act selectively on scolopidia, i.e., the mechanosensor type characteristically constituting tympanal organs. Pymetrozine solutions were applied as closely as possible to the scolopidia via a cuticle opening in the tibia, distally to the organ. Applications of pymetrozine at concentrations between 10⁻³ and 10⁻⁷ M to the tympanal organ led to a pronounced and irreversible decrease of the DPOAE amplitudes.     

The morphology and physiology of CAP organs in Jasus novaehollandiae (crustacea,decapoda, reptantia,macrura)

The location and external anatomy of the CAP organs of Jasus novaehollandiae were examined and found to be similar to those in Homarus gammarus (Laverack, 1978a). Histological examination of the organs showed threads or filaments arising from the internal surface of the spines to run through canals in the cuticle and join with dendrites of CAP sensory cells in the region of the hypodermis. The CAP neuron cell bodies lie in the nearby chordotonal organ strand. It is demonstrated that flexion of the limb causes the articulating membrane to deflect the spines of the sensillae distally. A variety of experimental techniques used to investigate the physiology of the organs reveals why previously reported attempts to record from the receptors failed. Direct stimulation of the sensillae with an analogue of the membrane and summation of many traces revealed phase constant responses at points corresponding to the covering and uncovering of the sensillae.     

The accessory organ,a scolopidial sensory organ,in the cave cricket Troglophilus neglectus (Orthoptera: Ensifera: Rhaphidophoridae)

Mechanoreceptor organs occur in great diversity in insect legs. This study investigates sensory organs in the leg of atympanate cave crickets (Troglophilus neglectus KRAUSS, 1879) by neuronal tracing. Previously, the subgenual and the intermediate organs were recognised in the subgenual organ complex, lacking the tympanal membranes present for example in the tibial hearing organs of Gryllidae and Tettigoniidae. We document the presence of the accessory organ in T. neglectus. This scolopidial organ is located in the posterior tibia close to the subgenual organ and can be identified by position, innervation and orientation of the dendrites of sensory neurons. The main motor nerve in the leg innervates a part of the subgenual organ and the accessory organ. The dendrites of sensory neurons in the accessory organ are characteristically bent in proximo‐dorsal direction, while the subgenual organ dendrites run distally along the longitudinal axis of the leg. The accessory organ contains 6–10 scolopidial sensilla, and no differences in neuroanatomy occur between the three thoracic leg pairs. Hence, the subgenual organ complex in cave crickets is more complex than previously known. The wider taxonomic distribution of the accessory scolopidial organ among orthopteroid insects is inconsistent, indicating its repeated losses or convergent evolution.     

Structure and sensory physiology of the leg scolopidial organs in Mantophasmatodea and their role in vibrational communication

Individuals of the insect order Mantophasmatodea use species-specific substrate vibration signals for mate recognition and location. In insects, substrate vibration is detected by mechanoreceptors in the legs, the scolopidial organs. In this study we give a first detailed overview of the structure, sensory sensitivity, and function of the leg scolopidial organs in two species of Mantophasmatodea and discuss their significance for vibrational communication. The structure and number of the organs are documented using light microscopy, SEM, and x-ray microtomography. Five scolopidial organs were found in each leg of male and female Mantophasmatodea: a femoral chordotonal organ, subgenual organ, tibial distal organ, tibio-tarsal scolopidial organ, and tarso-pretarsal scolopidial organ. The femoral chordotonal organ, consisting of two separate scoloparia, corresponds anatomically to the organ of a stonefly (Nemoura variegata) while the subgenual organ complex resembles the very sensitive organs of the cockroach Periplatena americana (Blattodea). Extracellular recordings from the leg nerve revealed that the leg scolopidial organs of Mantophasmatodea are very sensitive vibration receptors, especially for low-frequency vibrations. The dominant frequencies of the vibratory communication signals of Mantophasmatodea, acquired from an individual drumming on eight different substrates, fall in the frequency range where the scolopidial organs are most sensitive.     

Development of leg chordotonal sensory organs in normal and heat shocked embryos of the cricket Teleogryllus commodus (Walker)

This paper describes the embryonic development of some parts of the sensory peripheral nervous system in the leg anlagen of the cricket Teleogryllus commodus in normal and heat shocked embryos. The first peripheral neurons appear at the 30% stage of embryogenesis. These tibial pioneer neurons grow on a stereotyped path to the central nervous system and form a nerve which is joined by the growth cones of axons that arise later, including those from the femoral chordotonal organ, subgenual organ and tympanal organ. The development of these organs is described with respect to the increase in number of sensory receptor cells and the shape and position of the organs. At the 100% stage of embryogenesis all three organs have completed their development in terms of the number of sense cells and have achieved an adult shape. To study the function of the tibial pioneer neurons during embryogenesis a heat shock was used to prevent their development. Absence of these neurons has no effect on the development of other neurons and organs proximal to them. However, the development of distal neurons and organs guided by them is impaired. The tibial pioneer neurons grow across the segmental boundary between femur and tibia early in development, and the path they form seems to be essential for establishing the correct connections of the distal sense organs with the central nervous system.     

Ultrastructural investigations on the nuchal organ of the protandric polychaete,Ophryotrocha puerilis (Polychaeta,Dorvilleidae)

Summary The nuchal organs of the protandric hermaphrodite Ophryotrocha puerilis were studied by electron microscopy. Ophryotrocha puerilis is the first species hitherto described which possesses four instead of two nuchal organs. These sensory structures are located as ciliary pits at the posterior margin of the prostomium. Histologically, the nuchal organs are composed of supporting cells with long motile cilia and bipolar sensory cells, the perikarya of which form four distinct nuchal ganglia adjoining the brain. These structural components are concentrically arranged around the central sensory area. This area is covered by a modified cuticle, whereas the cuticle above the peripheral region of the sense organ exhibits the appearance typical for polychaetes. Two types of vesicular material are produced in the basal supporting cells, a dense-cored one within the central supporting cells only and a clear irregular-shaped one in all of these cells. The first type is considered to be responsible for the formation of the modified cuticle. The significance of these most probably long-distance chemoreceptory organs and their possible role in reproductive behaviour is discussed.     

Fine structure of the tibiotarsal and pretarsal sensory organs in Monobella grassei banyulensis Deharveng (Collembola : Neanuridae)

The fine structure of the tibiotarsal and pretarsal sensory organs of Monobella grassei banyulensis Deharveng (Collembola : Neanuridae) has been examined by electron microscopy.Three types of sensory organs have been observed. (1) the most numerous setae of the tibiotarsus are classic mechanosensitive setae with one bipolar sensory cell, whose distal outer segment ends in a tubular body. (2) Two small setae are arranged on each side of the basal part of the claw; they show 3 sensory cells, 2 of which are mechanosensitive cells of the scolopidial type; the outer segments of the 2 mechanosensitive cells end at the base of the sensory hair. The dendrite of the 3rd sensory cell extends into the hair shaft. (3) Two similar chordotonal sensilla link the tibiotarsus and the pretarsus; each sensillum is composed of 2 bipolar sensory cells enveloped in sheath cells. The first type of sensory organ shows the characteristics of insect exteroceptive mechanosensitive hairs. The mechanosensitive cells of the 2nd and 3rd tibiotarsus sensory organs are probably proprioceptive and control the movements of the pretarsus in relation to the tibiotarsus. Two features are noteworthy: (1) the association of the scolopidial cells with a chemosensitive one has never been observed in other insect sensory organs, except in the Collembola; and (2) there is an important morphological diversity in the ciliary roots of the various scolopidial cells, which are in other respects very similar.     

The scolopidial accessory organ in the Jerusalem cricket (Orthoptera: Stenopelmatidae)

Multiple mechanosensory organs form the subgenual organ complex in orthopteroid insects, located in the proximal tibia. In several Ensifera (Orthoptera), a small chordotonal organ, the so-called accessory organ, is the most posterior part of this sensory complex. In order to document the presence of this accessory organ among the Ensifera, the chordotonal sensilla and their innervation in the posterior tibia of two species of Jerusalem crickets (Stenopelmatidae: Stenopelmatus) is described. The sensory structures were stained by axonal tracing. Scolopidial sensilla occur in the posterior subgenual organ and the accessory organ in all leg pairs. The accessory organ contains 10–17 scolopidial sensilla. Both groups of sensilla are commonly spatially separated. However, in few cases neuronal fibres occurred between both organs. The two sensillum groups are considered as separate organs by the general spatial separation and innervation by different nerve branches. A functional role for mechanoreception is considered: since the accessory organ is located closely under the cuticle, sensilla may be suited to detect vibrations transferred over the leg's surface. This study extends the known taxa with an accessory organ, which occurs in several taxa of Ensifera. Comparative neuroanatomy thus suggests that the accessory organ may be conserved at least in Tettigoniidea.     

Discovery of a Lipid Synthesising Organ in the Auditory System of an Insect

Weta possess typical Ensifera ears. Each ear comprises three functional parts: two equally sized tympanal membranes, an underlying system of modified tracheal chambers, and the auditory sensory organ, the crista acustica. This organ sits within an enclosed fluid-filled channel–previously presumed to be hemolymph. The role this channel plays in insect hearing is unknown. We discovered that the fluid within the channel is not actually hemolymph, but a medium composed principally of lipid from a new class. Three-dimensional imaging of this lipid channel revealed a previously undescribed tissue structure within the channel, which we refer to as the olivarius organ. Investigations into the function of the olivarius reveal de novo lipid synthesis indicating that it is producing these lipids in situ from acetate. The auditory role of this lipid channel was investigated using Laser Doppler vibrometry of the tympanal membrane, which shows that the displacement of the membrane is significantly increased when the lipid is removed from the auditory system. Neural sensitivity of the system, however, decreased upon removal of the lipid–a surprising result considering that in a typical auditory system both the mechanical and auditory sensitivity are positively correlated. These two results coupled with 3D modelling of the auditory system lead us to hypothesize a model for weta audition, relying strongly on the presence of the lipid channel. This is the first instance of lipids being associated with an auditory system outside of the Odentocete cetaceans, demonstrating convergence for the use of lipids in hearing.     

Range fractionation in the locust metathoracic femoral chordotonal organ

Summary Insect femoral chordotonal organs are internal proprioceptors which monitor the position and movements of the femur-tibia joint of the leg. The locust (Locusta migratoria) metathoracic femoral chordotonal organ is composed of approximately 100 neurones with a variety of response properties. In this study intracellular recordings were used to examine the range fractionation of phasic and tonic responses to tibial movements. Some neurones responded across the full range of leg angles, while others had restricted response ranges, and could therefore act as labeled lines. Neurones with maximal firing at mid-angles are described for the first time in a locust femoral chordotonal organ. Responses are discussed in terms of underlying structural constraints on signal transduction.Abbreviation (mt) FCO (metathoracic) femoral chordotonal organ