The complex tibial organ of the New Zealand ground weta: sensory adaptations for vibrational signal detection.

In orthopteran insects, a complex tibial organ has evolved to detect substrate vibrations and/or airborne sound. Species of New Zealand weta (Anostostomatidae) with tympanal ears on the foreleg tibia use this organ to communicate by sound, while in atympanate species (which communicate by substrate drumming) the organ is unstudied. We investigated the complex tibial organ of the atympanate ground weta, Hemiandrus pallitarsis, for vibration detection adaptations. This system contains four sensory components (subgenual organ, intermediate organ, crista acustica homolog, accessory organ) in all legs, together with up to 90 scolopidial sensilla. Microcomputed tomography shows that the subgenual organ spans the hemolymph channel, with attachments suggesting that hemolymph oscillations displace the organ in a hinged-plate fashion. Subgenual sensilla are likely excited by substrate oscillations transmitted within the leg. Instead of the usual suspension within the middle of the tibial cavity, we show that the intermediate organ and crista acustica homolog comprise a cellular mass broadly attached to the anterior tibial wall. They likely detect cuticular vibrations, and not airborne sound. This atympanate complex tibial organ shows elaborate structural changes suggesting detection of vibrational stimuli by parallel input pathways, thus correlating well with the burrowing lifestyle and communication by substrate-transmitted vibration.

Neuromodulatory unpaired median neurons in the New Zealand tree weta, Hemideina femorata.

Wetas are ancient Gondwanan orthopterans (Anostostomatidae) with many species endemic to New Zealand. Like all Orthoptera they possess efferent neuromodulatory dorsal unpaired median (DUM) neurons, with bilaterally symmetrical axons, that are important components of motor networks. These neurons produce overshooting action potentials and are easily stimulated by a variety of external mechanosensory stimuli delivered to the body and appendages. In particular, stimulation of the antennae, mouth parts, tarsi and femora of the legs, abdomen, cerci and ovipositor is very effective in activating DUM neurons in the metathoracic ganglion of wetas. In addition, looming visual stimuli or light on-, light off-stimuli excite many metathoracic DUM neurons. These DUM sensory reflex pathways remain viable after the prothoracic to subesophageal connective is cut, whereas in locusts such reflex pathways are interrupted by the ablation. This suggests that, in wetas, sensory reflex pathways for DUM activation are organized in a less centralized fashion than in locusts, and may therefore reflect a plesiomorphic evolutionary state in the weta. In addition, many weta DUM neurons exhibit slow rhythmic bursting which also persists following the connective ablation.

Responses of efferent octopaminergic thoracic unpaired median neurons in the locust to visual and mechanosensory signals.

Insect thoracic ganglia contain efferent octopaminergic unpaired median neurons (UM neurons) located in the midline, projecting bilaterally and modulating neuromuscular transmission, muscle contraction kinetics, sensory sensitivity and muscle metabolism. In locusts, these neurons are located dorsally or ventrally (DUM- or VUM-neurons) and divided into functionally different sub-populations activated during different motor tasks. This study addresses the responsiveness of locust thoracic DUM neurons to various sensory stimuli. Two classes of sense organs, cuticular exteroreceptor mechanosensilla (tactile hairs and campaniform sensilla), and photoreceptors (compound eyes and ocelli) elicited excitatory reflex responses. Chordotonal organ joint receptors caused no responses. The tympanal organ (Müller's organ) elicited weak excitatory responses most likely via generally increased network activity due to increased arousal. Vibratory stimuli to the hind leg subgenual organ never elicited responses. Whereas DUM neurons innervating wing muscles are not very responsive to sensory stimulation, those innervating leg and other muscles are very responsive to stimulation of exteroreceptors and hardly responsive to stimulation of proprioceptors. After cutting both cervical connectives all mechanosensory excitation is lost, even for sensory inputs from the abdomen. This suggests that, in contrast to motor neurons, the sensory inputs to octopaminergic efferent neuromodulatory cells are pre-processed in the suboesophageal ganglion.

Somatotopic mapping of chordotonal organ neurons in a primitive ensiferan, the New Zealand tree weta Hemideina femorata: II. complex tibial organ.

Most ensiferan insects possess sets of highly specialized chordotonal organs in the proximal tibiae to detect conspecific auditory/vibratory signals or approach of predators. To date, most auditory/vibratory afferents have been classified according to their physiological properties and axonal projection morphology, but not to somatotopic origins. Hence, the functional specialization of identified receptor cells in the tibial organs remains uncertain. To address this question from an anatomical aspect, we investigated the structure of the weta, Hemideina femorata, tibial organs (the most elaborated tibial chordotonal organs among ensiferans) and their central projections by staining small numbers of receptor afferents from identified tibial organs. These organs comprise the "complex tibial organ," including the subgenual organ (primary vibration detector) and its posterior complement, the accessory organ, and the crista acustica (primary auditory organ) and its proximal complement, the intermediate organ. Unlike reports of a membranous organ structure for homologs in other ensiferans, weta tibial organs contain receptor cells embedded in thick solid masses. Primary afferents project ipsilaterally to the medial ventral association center of thoracic ganglia, where axon terminals are arrayed topographically in different areas specific to each organ, except for almost complete overlap of afferents originating from the distal part of the crista acustica and from the intermediate organ. In contrast to somatotopic reflection of sensilla position on limbs, as known for mechanoreceptor hairs, the somatotopic projection map of the insect ear reveals topographic association with acoustic tracheae or tibial cuticular attachment sites, which in turn must reflect determinants of response sensitivity (e.g., frequency or threshold).

Novel use of hair sensilla in acoustic stridulation by New Zealand giant wetas (Orthoptera: Anostostomatidae).

Sound production in New Zealand giant wetas (Orthoptera: Anostostomatidae) includes a femoro-abdominal mechanism, a ticking sound when alarmed (mechanism unknown) and, in two species (Deinacrida rugosa and Deinacrida parva), a tergo-tergal mechanism on the dorsal overlapping surfaces of abdominal tergites. The tergo-tergal mechanism consists of bilaterally paired patches of short curved spines on the dorsal anterior margins of tergites II-V, rubbed by opposing patches of articulated hair sensilla on the underside of each overlapping tergite. The latter are extremely robust, modified mechanoreceptors inserted at an acute angle onto raised bases which greatly restrict movement. They rub sideways against the underlying spines and produce sound during telescopic abdominal contraction which accompanies defence leg kicking stridulation. Movement analysis showed that the abdominal tergites contract asynchronously during stridulation. Sound is produced during both phases of telescoping. Femoro-abdominal sound comprises loud clicks of broadband sound principally below 10 kHz; tergo-tergal sound is a softer hiss spreading broadly from 10 kHz to the ultrasonic above 20 kHz. We propose that the tergo-tergal mechanism may have evolved under predation pressure by the ground gleaning short tailed bat endemic to New Zealand. The use of mechanosensory hair sensilla for sound production is rare in arthropods.