Antennal Development in the Praying Mantis (Tenodera aridifolia) Highlights Multitudinous Processes in Hemimetabolous Insect Species

Abstract

Insects possess antennae equipped with a large number of segments (flagellomeres) on which sensory organs (sensilla) are located. Hemimetabolous insects grow by molting until they reach adulthood. In these species, the sensory structures develop and mature during each stage of development; new flagellomeres are generated at each molt elongating the antennae, and new sensilla appear. The praying mantis (Tenodera aridifolia) is a hemimetabolous insect with 7 different instars before it reaches adulthood. Because their antennae are provided with an atypical sensillar distribution, we previously suggested that their antennae develop with a different mechanism to other hemimetaboulous insect species. In the present study, we measured the number, length and width of flagellomeres along the antennae in nymph and adult mantis Tenodera aridifolia. For this study, we developed a new and innovative methodology to reconstruct the antennal development based on the length of flagellomeres. We observed and confirmed that the antennae of mantises develop with the addition of new segments at two distinct sites. In addition, we constructed a complete database of the features of the flagellum for each stage of development. From our data, we found that sexual dimorphism appears from the 6 instar (larger number and wider flagellomeres in males) in accordance with the appearance of their genital apparatus. The antennal sexual dimorphism completes at adulthood with longer flagellomeres and the emergence of a huge number of grooved peg sensilla in males during the last molting, which suggests once again their function as sex-pheromone receptive sensilla.

Two types of sensory proliferation patterns underlie the formation of spatially tuned olfactory receptive fields in the cockroach Periplaneta americana

“…New flagellomeres are added into the proximal part of the antenna in the cockroach and the grasshopper by dividing the meriston and meristal segments (Chapman, ; Minelli, ). In contrast, in the mantis (Carle et al, ) and mantophasmatodea (Hockman, Picker, Klass, & Pretorius, ), in addition to the proximal part, new flagellomeres appear in the middle part of the antenna via binary division of each of the flagellomeres. In basal insects, bristletails, new flagellomeres are likely to be added evenly across the whole antenna at every molt (Fröhlich & Lu, ).…”

“…In previous cockroach studies, topographic organization of OSNs in the glomeruli has been proposed to reflect the postembryonic development of the antenna (Nishino & Mizunami, ; Nishino et al, , ). In hemimetabolous insects, including the cockroach, new flagellomeres are added in the proximal region of the flagellum at each molt (Carle, Yamawaki, Watanabe, & Yokohari, ; Chapman, ; Minelli, ; Schafer & Sanchez, ). Olfactory sensilla and OSNs emerge concomitantly with the addition of new flagellomeres to the proximal end of the flagellum (Schafer & Sanchez, ).…”

Decision‐making and motor control in predatory insects: a review of the praying mantis

“…Some behaviours are evoked by visual stimuli and others by auditory stimuli. However, it is possible that olfactory stimuli modify predatory and defensive behaviours because the mantis has an unexpectedly well‐developed olfactory system (Carle et al ., ,b, ). For example, Wilder and Rypstra () reported that T. sinensis tended to prefer the site with chemical cues from crickets.…”

Organization of the antennal lobes in the praying mantis (Tenodera aridifolia)

“…Furthermore, they can eat pieces of banana and associate this food reward with the odor of banana (Prete, Lum, & Grossman, ). Although the morphological features of antennae have been investigated in several species of mantises (Holwell, Barry, & Herberstein, ; Allen, Barry, & Holwell, ; Carle, Toh, Yamawaki, Watanabe, & Yokohari, , ), little is known about their olfactory system. In fact, little is known about the olfactory capabilities of insect predators that heavily depend on their visual system to obtain food.…”

“…Briefly, the proximal parts are equipped with only mechanosensory and hygro‐/thermoreceptive sensilla, whereas the distal parts additionally possess olfactory sensilla in females. Moreover, a large number of grooved peg sensilla are present mostly on the proximal parts of male antennae, which are speculated to be their sex‐pheromone sensilla (Holwell et al, ; Allen et al, ; Carle et al, , ). In the present study, the anatomical organization of ALs in the praying mantis T. aridifolia was investigated to increase our understanding of olfactory processes in predators having a well‐developed visual system.…”