The Subgenual Organ Complex in Stick Insects: Functional Morphology and Mechanical Coupling of a Complex Mechanosensory Organ

Abstract

Leg chordotonal organs in insects show different adaptations to detect body movements, substrate vibrations, or airborne sound. In the proximal tibia of stick insects occur two chordotonal organs: the subgenual organ, a highly sensitive vibration receptor organ, and the distal organ, of which the function is yet unknown. The distal organ consists of a linear set of scolopidial sensilla extending in the tibia in distal direction toward the tarsus. Similar organs occur in the elaborate hearing organs in crickets and bushcrickets, where the auditory sensilla are closely associated with thin tympanal membranes and auditory trachea in the leg. Here, we document the position and attachment points for the distal organ in three species of stick insects without auditory adaptations (Ramulus artemis, Sipyloidea sipylus, and Carausius morosus). The distal organ is located in the dorsal hemolymph channel and attaches at the proximal end to the dorsal and posterior leg cuticle by tissue strands. The central part of the distal organ is placed closer to the dorsal cuticle and is suspended by fine tissue strands. The anterior part is clearly separated from the tracheae, while the distal part of the organ is placed over the anterior trachea. The distal organ is not connected to a tendon or muscle, which would indicate a proprioceptive function. The sensilla in the distal organ have dendrites oriented in distal direction in the leg. This morphology does not reveal obvious auditory adaptations as in tympanal organs, while the position in the hemolymph channel and the direction of dendrites indicate responses to forces in longitudinal direction of the leg, likely vibrational stimuli transmitted in the leg’s hemolymph. The evolutionary convergence of complex chordotonal organs with linear sensilla sets between tympanal hearing organs and atympanate organs in stick insects is emphasized by the different functional morphologies and sensory specializations.

Morphological coupling of the distal organ in the Peruvian walking stick (Oreophoetes peruana): Structural and functional aspects

“…In this study, connecting structures of the chordotonal organs in the SGO complex of the Peruvian stick insect were studied to better understand its functional morphology. The overall organization of the chordotonal organs (SGO and DO) in O. peruana is identical to other stick insects in organization and numbers of the sensilla, the shape of the SGO, the distal extension of the SGO, and the connection to the DO (Strauß, Moritz, & Rühr, 2021). The present study documents a major tissue strand at the proximal DO to the cuticle and a thin membrane between the SGO and the DO.…”

“…These tissues, as well as the finer strands, may provide attachments to keep the organs in position but could also transfer vibration stimuli to the sensilla of the SGO and DO. The SGO is connected to the cuticle at the posterior side by a relatively strong tissue strand, while the DO is connected at its proximal end to the dorsal leg cuticle by a connective tissue strand (Jägers‐Röhr, 1968; Strauß, 2021; Strauß, Moritz, & Rühr, 2021) (Figure 1B). The latter strand is also associated with a group of campaniform sensilla (CS) placed in the cuticle (Strauß, Moritz, & Rühr, 2021).…”

“…The SGO is connected to the cuticle at the posterior side by a relatively strong tissue strand, while the DO is connected at its proximal end to the dorsal leg cuticle by a connective tissue strand (Jägers‐Röhr, 1968; Strauß, 2021; Strauß, Moritz, & Rühr, 2021) (Figure 1B). The latter strand is also associated with a group of campaniform sensilla (CS) placed in the cuticle (Strauß, Moritz, & Rühr, 2021). The CS are specialized mechanoreceptors that detect cuticular strain (Zill et al, 1999; Zill & Moran, 1981), and they can occur as single sensilla or in groups (Harris et al, 2020; Keil, 1997).…”

“…Previously, a fine membrane was documented between the SGO and DO in stick insects, forming a connection between the two chordotonal organs (Figure 1B–D). This membrane is placed between the anterior and posterior sides of the tibia (Strauß, Moritz, & Rühr, 2021) and runs between both organs in the horizontal longitudinal level (Ball & Field, 1981) of the tibia (Figure 1C). It contacts the DO on the dorsal side and eventually merges with the DO surface (Figure 1D).…”

“…(C, D) Transverse sections (shown as hatched lines in B) of the tibia showing the position of the membrane at the proximal DO. Anatomy of the subgenual organ complex adapted from Sipyloidea sipylus (Strauß, Moritz, & Rühr, 2021). Scale = 200 μm.…”