Morphological Structure of the Body Setae as Mechanoreceptor on the Mesonotum of Telenomus remus Nixon (Hymenoptera, Platygastridae)

ABSTRACT


Introduction
Telenomus remus Nixon, 1937, is a native species of Peninsular Malaysia and Papua New Guinea (Hernández et al., 1989).Telenomus remus from India was firstly introduced to Israel to control the armyworm Spodoptera litturalis, the sister species of Spodoptera litura (Gerling, 1972;Li et al., 2021).The following successful introduction of T. remus was in Tapa la lucha, Venezuela, in July 1987 to control Spodoptera frugiperda in cornfield (Hernández et al., 1989).However, not all the T. remus release were succesfull.In Florida, the two years establishment of T. remus in 1975-1977 had failed to control S. frugiperda due to climate differences with the tropical countries (Van Waddill & Whitcomb, 1982).
The female of T. remus starts the host recognition by drumming the eggs with her antennae and smearing the eggs with her ovipositor before laying her own eggs into the host (Gerling & Schwartz, 1974).The older the female, the time for her to lay the eggs took longer time (Schwartz & Gerling, 1974).The sex pheromones of S. frugiperda could also act as kairomones, by which the parasitization of T. remus to S. frugiperda eggs was increased (Nordlund et al., 1983).Thus, the orientation of T. remus oviposition is mediated by the function of the sensory organs located on the ovipositor and antennae as tactile and air-born chemical sensors.
As a potential parasitoid, however, the exploration of the sensory organs of T. remus were very limited at this time.Some sensory receptors were recorded from the antennae of T. dendrolimusi and T. reynoldsi, such as basiconic, chaetica, trichoid, trichoid curvata, multiparous gustatory, campaniform, and stylonica sensilla (Cave & Gaylor, 1987;S. Zhang et al., 2015).The diversity of sensory receptors on the antennae of T. dendrolimusi was higher compared to the other organs such as mouthparts, thoracic legs, eyes, mesonotum, wings, and external genitalia (S.Zhang et al., 2015).Vol. 3, No. 1, June 2023, pp. 24-29 Wikantyoso & Putra (Morphology Structure of The Body Setae) Although the antennae are important as multimodal sensory organs, the other body parts bear other sensory receptors that the putative function has not yet to be understood.
On insect body, the sensory receptors are often called as setae (singular: seta) when they are innervated.The putative function of the setae can also be inferred from the outer morphology and the characteristic of the cuticle.For example, mechanoreceptors on the wings or body of terrestrial and flying insect are important to receive input from the surrounding situation, such as a direct mechanical input, wind speed, wing load, or other airborne vibration (Aiello et al., 2021;Dinges et al., 2021;Fuller et al., 2014;Hengstenberg, 1988;Müller & Wehner, 2007;Wikantyoso et al., 2023;Wolf & Wehner, 2005).In this study we observed setae from the mesonotum part of Telenomus remus Nixon and analyze the microstructure to infer the putative function.

Specimen collection
Samples were collected within August 2022 -February 2023 in Bantul, Yogyakarta.Stratified random sampling method was applied for the collection.The selection of the corn plantation area was carried out by purposive sampling with the availability of the S. frugiperda infestation as the main criterion.The eggs of S. frugiperda were collected and labelled.In the laboratory, the eggs were transferred to the plastic cup and kept until the parasitoid emerge.The parasitoid was preserved in 70% alcohol for further identification and electron microscopy analysis.

Specimen preparation for electron microscopy
Collected samples were soaked into cacodylate buffer and cleaned by using ultrasonic cleaner for 5 min.Cleaned samples were subjected to prefixation, fixation, and dehydration process.Prefixation was started by adding 2.5 % glutaraldehyde in a vial with samples inside for overnight at 4ºC.Samples were subjected further to fixation process by soaking them in 2% tannic acid solution for 6 hoursovernight.Fixed samples were washed with cacodylate buffer four times (5 min each time).Dehydration process was carried out by soaking the samples in the serial aqueous alcohol solution (70%, 85%, 98%, and absolute).Samples were dried by using tert-butanol and frozen in the refrigerator for overnight.The freezed samples were put into the vacuum drier and kept in the desiccator.Dried samples were attached on the sample's stubs with carbon adhesive tape.Finally, samples were coated with sputter gold target and subjected into electron microscopy analysis.

Setae as mechanoreceptor
The observation on T. remus showed that the setae on the mesonotum were not only usual hair.The structure of the hair showed several biological structures that has potential to be functional as a sensory receptor.The all setae on the mesonotum had long peg ended with tapered tip.The base of the peg were smooth and longitudinal grooves prolonged to the tip of the peg.Setae with respective characteristics were also observed in other insects' body, such as antennae, mouthpart, and legs.It is usually called as chaetica or trichoid sensilla (Yanagawa et al., 2009;S. Zhang et al., 2015;Zhang et al., 2016).those setae function might be related to the mechanoreceptor or chemo-tactile receptor (Wikantyoso et al., 2022; Y.-R.Zhang et al., 2015).However, the seta peg was surrounded by a prominent structure called as socket (Figure 1).It may confirm one putative function of the setae on the mesonotum of T. remus were related to the mechanoreceptive function.Socket on the base of the peg give the setae peg flexible movement when it receives a certain amount of vibration or distortion on surrounding cuticle (McIver, 1975;Thurm, 1965).The distortion of the cuticle will be received by the nerve system attached to the base of the peg under the socket.Eventually, the distortion is converted as a signal (Iwasaki et al., 1999) (Figure 2).A future study including the analysis of internal anatomy of the setae by transmission electron microscopy technique to understand further about the outer dendritic nervous system characteristics of the mesonotum setae.The mechanoreception is mediated by long tapered peg, socket, gap, and a tubular body as the nervous system.When input comes, the gap provide flexibility to the peg to move to a certain direction.The movement of the peg may create cuticle distortion on the whole level of the peg and socket.The distortion serves as an input and will be converted to a chemical signaling by the tubular body as the peripheral nervous system.

Biological and behavioral aspects
The study of T. remus morphology is important to assess the deformity in the mass rearing process for the application of parasitoid as natural control agent, especially morphology related to wing size reduction related to the parasitoid flying ability (Pomari-Fernandes et al., 2016).However, the study related to the T. remus body setae that act as sensory organs important to support the orientation ability are limited.This study observed the existence of setae as mechanoreceptors on the mesonotum of T. remus that might be related to the ability to understand the air particle movement to control their flight.On the locust head, the setae on the head have the ability to respond the heavy air current (Camhi, 1969a).The wind stimulation to the locust facial setae also influences their behavior to open their wings as they are ready to fly (Camhi, 1969b).The position and direction of the dangling setae pegs might also show their importance to detect the air current from the anterior and control flying speed (Figure 2), as the deflection of the seta toward their dangling direction elicit massive action potential until the stimulus ends.But the deflection against their dangling direction did not significantly produce action potential (Corfas & Dudai, 1990).The setae might be important for the parasitoid mechanical sensitivity to a direct touch from the natural predator or surrounding obstacle such as leaves and twigs.Since the Spodoptera mostly lays the eggs under the leaves (EPPO, 2015), the long flexibly dangled setae pegs and their dense distribution may also help the orientation of the upside-down maneuver from T. remus during the oviposition.

Conclusion
The setae on the mesonotum of T. remus had the characteristics of mechanoreceptor.The characteristics of long peg, socket, and the gap between the base of the peg and the socket demonstrated the important structure to sense tactile or airborne mechanical stimuli.

Figure 1 .
Figure 1.Setae as mechanoreceptor on the mesonotum of T. remus.a: dorsal view of mesonotum (Msn) located on the posterior side of the head (H), b: lateral view of the thorax showed pronotum (Prn), mesonotum, and metanotum (Mtn), c: closer look of mesonotum with the setae scattered on mesoscutum (MsSct) and mesoscutellum (MsScl) parts, d: setae socket located on the posterior side of each cuticle scale on mesoscutum (arrow), e: each setae has a clear prominent structure as a socket (Soc).There was a gap between the socket and the base of the setae peg that enable the setae flexibly move, f: the characteristics of the setae peg's cuticle showed longitudinal grooves (Lgv) appeared from the base to the tapered tip (dotted square) of the peg.

Figure 2 .
Figure2.Schematic drawings of a seta as mechanoreceptor.The mechanoreception is mediated by long tapered peg, socket, gap, and a tubular body as the nervous system.When input comes, the gap provide flexibility to the peg to move to a certain direction.The movement of the peg may create cuticle distortion on the whole level of the peg and socket.The distortion serves as an input and will be converted to a chemical signaling by the tubular body as the peripheral nervous system.