International Journal of Zoological Investigations Vol. 4, No. 1, 73-80 (2018) ______

International Journal of Zoological Investigations

Contents available at Journals Home Page: www.ijzi.net

ISSN: 2454-3055

Comparative Scanning Electron Microscopic Study of Antennae and Hearing Organ of Two Indian Mantids religiosa and Gongylus gongylodes

Kavya M. K., Raghunandan K. S., Padmanabha B. and Channaveerappa H.*

P.G. Department of Applied Zoology, Maharani Science College for Women, University of Mysore, Mysuru – 570 005, India

*Corresponding Author

Received: 30th April 2018 Accepted: 29th May 2018 ______

Abstract: Antennae of Mantis religiosa and Gongylus gongylodes exhibit sexual dimorphism. In G. gongylodes the male has pectinate antennae with terminal filiform structure but female has filiform antennae.The antennae of male M. religiosa are longer than the female and filiform in both. Antennae of these two species posed for SEM studies showed differences in the distribution of sensillae at basal, middle and terminal flagellomeres in both tsexes of these species. In G. gongylodes the terminal segments had more number of sensilla chaetica and sensilla trichodea than sensilla basiconica and coeloconica. In M. religiosa sensilla coeloconica were more in terminal segments of both the sexes.Tip of antennae was flat, depressed and enclosed sensilla coeloconica in both the sexes. Single hearing organ found in meso-metathoracic region on ventral side. In both species the structure of hearing organ was of DK type in both sexes. Keywords: Sexual dimorphism, Flagellomeres, Sensillae, Terminal segments, Hearing organ , DK type ______

Introduction Mantids have evolved sensory structures to scanning electron microscopic studies have locate different signals which are adapted been carried out by several workers (Fauchex, specifically to perform certain functions. Two 2006; Holwell et al., 2007; Fauchex, 2009; such structures are antennae and hearing Greven and Brenner, 2009) but such an organs. So far, the antennae have been utilized analysis in Indian mantids is wanting. as tool to describe or discriminate species of Mantids have single ventral hearing organ mantids at taxonomic level and to assess commonly referred to Mantid ear. The sexual dimorphism (Mukherjee et al., 1995; auditory system is unique (Yager, 1999). Vyjayandi, 2005; Sureshan, 2009). The first These organs can trace ultrasonic sounds morphological description of antenna was generated by flying bats (Triblehorn and done by Slifer (1968). Recent works on Yoger, 2005). Few workers have utilized the

73 auditory systems of mantids to trace pressed EVAC button. The sound of rotatory phylogeny (Yager and Svenson, 2008) and pump is heard and then wait for more than 20 described six different kinds of hearing minutes to achieve high vacuum. organs, of these four are found to be most commonly distributed among mantid fauna. Then the SEM is turned on by pressing ‘on’ The present study performed the scanning button. Then select magnification on the electron microscopic structures of antennae of screen obtaining from 10X made to high two Indian mantids, M. religiosa and G. desired magnification. For this the key of Z gongylodes to observe whether there is axis were used and adjusted the images using geographical variation existing in the antennal key on the SEM table board. structures already described in other species Results from different parts of the world. Also, SEM analysis of antenna Gongylus gongylodes description of hearing organs of two mantids G. gongylodes and M. religiosa are presented. The antenna (Figs. 1-4) of both the sexes scanned for the detailed study revealed Materials and Methods similar types of sensilla with difference in Hearing organs of both the species are located distribution on the antennal segments. The on the ventral meso-metathoracic region pectinate section of male antenna had more viewed by lateral stretching of the meso- members of sensilla basiconica, sensilla metathoracic segments. Hearing organs were coeloconica, as well sensilla trichodeum photographed using NIKON D7000 DSLR (Table 1). The sensillae were found to be camera. located in a round depression irrespective of the type, sensilla coeloconica and trichodeum Scanning Electron Microscopy had straight stem and surrounded by cuticular The procedure by Doug Kim and Chunmin wall. The terminal part of the antenna of male Fung (2005) was followed for SEM imaging. and female had more number of sensilla Scanning electron microscope studies were trichodea, sensilla basiconica and sensilla done using Carl Zeiss Electron Microscope at coeloconica. In the non-pectinate region of the IOE University of Mysore, Mysore. The parts male antenna large sized trichodium was to be imaged were obtained from the freshly recorded. In female the long trichodial sensilla prepared specimens of mantids of both sexes. and large trichodial sensilla were present in The samples of antennae or parts of leg were all the segments but the number was more separated and critically dried and mounted on compared to the male terminal structures. to carbon sticky tapes, the position of each Their number in the flagellar segments was sample noted. The values of the nitrogen gas more than 25 in each terminal as well mid tank (less than 100 psi) kept open, vent segments of female. Even the small button on the microscope table pressed. After coeloconica and basiconica sensilla were the click sound the chamber door is opened by found scattered in each antennal segment and pulling the lever up. The sample mounting their number was equally high compared to stage moved down by operating the Z axis key. male antennal terminal segment. All types of The sample holder stubs are placed into the sensilla were present in circular cuticular mounting holes. Closed the door and then depression in female antennal segment like

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that of male antennae. The length of antenna Hearing organ in male was 18.05 mm and of female was 6.86 Hearing organ (Figs. 8a, b) is located in mm. between meta and mesothoracic legs on the SEM analysis of antenna of Mantis religiosa ventral surface in Gongylus gongylodes and Mantis religiosa and were of DK form (deep Antennae of both the sexes in Mantis religiosa groove and prominent knobs). The ultrasound (Figs. 5-7) are filiform and exhibited variation sensitive chambers were separated at its in between male and female. The antennal anterior end by two well defined thick length of male was 24.51 mm and had 99 cuticular lobes. At right angle to the long axis of the thorax, the rostral border of the knob segments whereas in females the length was was present. The two lateral walls of the 10.61 mm and had 62 antennomeres. Each chamber almost touch the rostral region at antenna irrespective of the sex is formed of a 1/3 of the length and progressively the wall scape, a pedicel and flagellomeres. The scape are widely separated in the posterior region. is long compared to other segments of the Two furcal pits lie deep in the chamber near antenna and cylindrical in shape. The pedicel the caudal end which were not visible from is bulbus and articulates with flagellum. The outside. The lateral wall of the auditory chamber faces medially and include three first flagellomere is twice longer than the distinctive structure—(i) cuticle ridge (ii) other mid anteomeric segments. 2-5 basal tympanal depression and (iii) the bifid flagellomeres are referred to and could be sensillum. The cuticle ridge or ventral rod recognized easily by their short length and runs from rostral to caudal direction in the carry few sensilla. After 10th/11th segment middle of the wall. Dorsal to this wall is a tear only the flagellomere acquire regular size, drop shape tympanal depression, it is the real whereas the distal flagellomere is three times tympanum. At the extreme point to the ends of the ventral rod and the tympanum is longer than normal segments. The SEM present a conical sensory structure -- the bifid studies have revealed that the flagellum bears sensillum which is encircled by a thin cuticle. different types of sensilla coeloconica and In Gongylus gongylodes, a dark brown sensilla basiconica (Table 1) which are expanded structure (Fig. 8 b) was present on present in both sexes of this species. The basal abdomen in between the 6th--8th abdominal segments showed a plain structure without segments which was strongly represented in any sensilla whereas the last few segments males whereas in female it was present had different type of sensilla-- sensilla between 6th-7th segments and feebly basiconica, sensilla coeloconica, sensilla represented. This patch has velvet like trichodium (a long hair-like structure covering and its significance is not scattered in each of the terminal segments, understood. The butterfly like brown 50-60 flagellomres) and sensilla chactica (5-6 structure expanded in the corner angles scattered in each of the terminal segments). appeared as bright dark brown marks. In On the basal flagellomere and on scape Mantis religiosa this marking was totally bohm’s sensilla and sensilla chaetica were absent in both sexes. found.

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Table 1: Measurements of different types of sensilla present in antenna

Types of sensilla M. religiosa G. gongylodes Sensilla basiconica 4.5 ± 0.4µm 4.01 0.4µm Sensilla coeloconica 1. 1.2 ± 0.2µm 1. 3.04 0.4µm 2. 3.01 ± 0.2µm 2. 6.6 ± 0.01µm 3. 6.2± 0.1µm Sensilla trichodia 21.01 to 35.6 ± o.2µm 20.09 to 37.56 o.1µm Sensilla chaetica 1. 33.1 ± 3.0µm 1. 30.2 8.0µm 2. 109 9.5µm 2. 110.1 8.5µm

Fig. 1: Gongylus gongylodes male antenna: A = Fig. 2: Gongylus gongylodes male antenna: Enlarged Pectinate and B = Terminal part portion of Pectinate region showing sensillae B- Basiconica C- Coeloconica

Fig. 3: Gongylus gongylodes Female antenna Fig. 4: Gongylus gongylodes Female antenna Terminal part : C = Chaetica; T = Trichodia

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Fig. 5: Mantis religiosa Male antenna: Middle Fig. 6: Mantis religiosa Female antenna: Middle segment—C—Coeloconica; B—Basiconica segment—C- Coeloconica; B—Basiconica; T- Trichodia

Fig. 7: Mantis religiosa Female antenna: Terminal Fig. 8: Hearing organ a-- Gongylus gongylodes and segment Terminal depression b-- Mantis religiosa

Discussion related functions (Faucheux, 2009). These Antenna structures are found to have a role in reception of sex pheromones. Many workers In both the species of mantids there was clear performed scanning electron microscopic sexual dimorphism in the morphological (SEM) studies of antennal structures in features of antennae. Sexual dimorphism was different species of mantids such as also recorded in other studies (Hurd et al., Oxyothespis moroccana, Mantis religiosa 2004). The antennae possess large number of (Faucheux, 2008), Pseudomantis albofimbriata sensory and glandular structures showing and Ciulfina biseriata (Holwell et al., 2007), sexual dimorphism and many physiological Gongylus gongylodes (Greven and Brenner,

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2009), Iris oratoria (Faucheux, 2009). As far and female of the species. The meriston the Indian mantids are concerned majority of formed 5-6 short segments and hardly had the work has been done only on any type of sensillae in both sexes of Mantis morphological description of antennae but no religiosa and Gongylus gongylodes. The SEM related work has been carried out. In this terminal part of filiform antennae of Mantis regard we have tried to review and analyze religiosa had depression bearing sensilla the nature of ultra-morphological structures coeloconica and one or two sensilla chaetica, of antennae in the two species Mantis religiosa whereas the terminal segment of female and Gongylus gongylodes. Mantis religiosa had large number of coeloconica surrounded by a saucer-like The ultra-morphology of antennae of structure enclosed with in the flaked Gongylus gongylodes and Mantis religiosa elongation of the walls, compared to antennal revealed one common structure that the organization of Gongylus gongylodes female. In sensillae were present in a round depression female, antennal segment had blunt irrespective of the type of sensilla. In both appearance with least number of sensilla these species sensilla basiconica, sensilla coeloconica (i) 1.2 µ (ii) 3.01 µ (iii) 6.2 µ, coeloconica, sensilla trichodeum and sensilla sensilla trichodea 21.01 to 35.6 µ or sensilla chaetica were present. The sensilla chaetica 33.1µ to 109 µ. coeloconica and sensilla trichodium had straight stem with grooved ridges running Thus in both these species there was from base towards tip in both Mantis religiosa comparable differences in the arrangement or and Gongylus gongylodes. In male of Gongylus distribution of different types of sensillae in gongylodes the pectinate region had least both the sexes. The present study also has number of sensilla trichodea or even missing identified a few differences from the earlier in some of the pectinate segment but non- works of Faucheux (2008) on Mantis religiosa pectinate terminal part of male antenna had and of Greven and Breuner (2009) on long sensilla trichodea ranging from 5-6 in Gongylus gongylodes. Major variation in both number in each of the segment but in female species presents striking differences in the of this species the long sensilla coelconica, basal segments and terminal segments sensilla chaetica and sensilla trichodea were particularly in possessing more sensilla present in all the segments. In both male and chaetica and sensilla trichodium. The median female Mantis religiosa, sensilla coeloconica, segments also have revealed difference with were abundant in each flagellar after the 15th sensilla basiconica numbers. flagellar segment of antenna. The basal Hearing organ segment did not bear any type of sensillae and were like pealed bark in appearance. Up to The auditory system of mantids is interesting 15th antennal segment only a few very short which consists of single ear (Yager, 1999), peg-like sensillae which were often referred though the ear anatomically a single structure to antennal glands were present. The five comprises of two tympana in a deep cuticular terminal segments had long sensilla trichodea, chamber. In this study, the ear in both species sensilla chaetica ranging between 5-6 of mantids was in the ventral mid- line of the numbers in each of the segments, in both male metathorax, similar to the reports of several

78 workers in other species of mantids. Extensive other species in arrangement of sensillae. study on the organization and functioning of Even differences were recorded with findings mantis auditory system by Yager and Svenson of earlier works that may be due to (2008) and Yager and Hoy (1989) revealed geographical variations. It warrants further the presence of six major auditory types in studies involving large number of individuals mantids, but only four of the six could be for confirmations. The hearing organs were of anatomically recognized. These authors DK type as recorded but to establish superimposed molecular data with auditory phylogenetic relationship more number of organs to trace evolutionary origin of mantid Indian mantids have to be analysed.. ear and showed that the ear of mantids Acknowledgements evolved about 120mya. The same authors have concluded that the mantid ear could Authors are thankful to Sri Chandrashekar, gather only ultrasounds in all the species of Principal Scientist and Mr. Yogesh, SEM In- mantids examined. Based on the anatomical charge, IOE, University of Mysore, Mysore for features four types of ears namely DK (deep providing SEM facilities for this study. groove and prominent knobs), DNK (deep References groove, no knob), DO (knobs absent) and MSMT (mesothoracic and metathoracic Doug K and Chunmin F. (2005) SEM Standard operating segments are similar) have been identified procedure. http://www.sci.cuny.edu and described by Yager and Svenson (2008). Faucheux MJ. (2006) La mante religieuse, Sphodromantis viridis occidentalis (Werner, 1906) The present study revealed that in Mantis (Dictyoptera: Mantodea: Mantidae): Prospections religiosa the groove was deeper and the ridges dans Je Sud Marocain, etude des sensilles were prominent extending in between antennaires de Ia femelle. Bulletin Societe Sciences Naturelles 'Ouest France 28:104-108. metathoracic and mesothoracic segments. At its both ends a small opening was present. Faucheux MJ. (2008) Antenna sensilla of the male praying mantid, Oxyothespis maroccana Bolivar, The hearing organ of Gongylus gongylodes 1908 (Insecta: Mantodea: Mantidae): distribution also revealed the same type of deep groove and functional implications. Entomologie 30:29-36. and ridges but comparatively ridges were Faucheux MJ. (2009) Sensilles antennaires de l'imago de Brachythemis leucosticta Brumeister, 1839 wide and at the lower end of the opening (Odonata, Anisoptera, Libellulidae). Martinia looks like honey drop but for that both the 25:40-48. species had same type of auditory structure Greven Hand Brenner M. (2009). Zur Morphologie und that could be categorized as DK type. zum Verhalten der „Wandelnden Geige Gongylus gongylodes (Linné, 1758) (Mantodea, ). Conclusion Entomologie heute 21:63-76. Antennal structure differed in both the species Holwell GI, Katherine LB and Herberstein M E. (2007) examined in the flagellomere-wise Mate location, antennal morphology, and ecology in two praying mantids (Insecta: Mantodea). Biological arrangement of all types of sensillae. Journal Linnean Society 91:307-313. G.gongylodes exhibited variation in between Hurd L E, Frederick RP, Tappey H J, Singh TB and sexes with regard to possession of trichodia Richard T P. (2004) First identification of a putative and chaetica sensillae. The basal segments of sex pheromone in a praying mantid. J. Chem. Ecol. M. religiosa differed to large extent from 30:155-166.

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