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Behavioral response to antennal tactile stimulation in the field cricket Gryllus bimaculatus

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Abstract

We examined behavioral responses of the field cricket Gryllus bimaculatus to tactile stimuli to the antennae. Three stimulants of similar shape and size but different textures were used: a tibia from the hunting spider Heteropoda venatoria (potential predator), a tibia from the orb-web spider Argiope bruennichi (less likely predator), and a glass rod. Each stimulus session comprised a first gentle contact and a second strong contact. The evoked behavioral responses were classified into four categories: aversion, aggression, antennal search, and no response. Regardless of the stimulants, the crickets exhibited antennal search and aversion most frequently in response to the first and second stimuli, respectively. The frequency of aversion was significantly higher to the tibia of H. venatoria than to other stimulants. The most striking observation was that aggressive responses were exclusive to the H. venatoria tibia. To specify the hair type that induced aggression, we manipulated two types of common hairs (bristle and fine) on the tibia of the predatory spider. When bristle hairs were removed from the H. venatoria tibia, aggression was significantly reduced. These results suggest that antennae can discriminate the tactile texture of external objects and elicit adaptive behavioral responses.

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References

  • Altner H, Prillinger L (1980) Ultrastructure of invertebrate chemo-, thermo, and hygroreceptors and its functional significance. Int Rev Cytol 67:69–139

    Article  Google Scholar 

  • Baba Y, Tsukada A, Comer CM (2010) Collision avoidance by running insects: antennal guidance in cockroaches. J Exp Biol 213:2294–2302

    Article  PubMed  Google Scholar 

  • Balakrishnan R, Pollack GS (1997) The role of antennal sensory cues in female responses to courting males in the cricket Teleogryllus oceanicus. J Exp Biol 200:511–522

    PubMed  Google Scholar 

  • Barth FG (2002) A spider’s world: senses and behavior. Springer, Berlin

    Google Scholar 

  • Bartos M, Honegger H-W (1997) Impact of motor activity and antennal mechanosensory input on the intensity of proctolin-like immunoreactivity in antennal motoneurons of crickets (Gryllus bimaculatus). J Comp Physiol A 181:59–70

    Article  Google Scholar 

  • Burdohan JA, Comer CM (1996) Cellular organization of an antennal mechanosensory pathway in the cockroach Periplaneta americana. J Neurosci 16:5830–5843

    PubMed  CAS  Google Scholar 

  • Camhi JM, Johnson EN (1999) High-frequency steering maneuvers mediated by tactile cues: antennal wall-following in the cockroach. J Exp Biol 202:631–643

    PubMed  CAS  Google Scholar 

  • Chapman RF (1982) Chemoreception: the significance of receptor numbers. Adv Insect Physiol 16:247–356

    Article  CAS  Google Scholar 

  • Comer CM, Baba Y (2011) Active touch in orthopteriod insects: behaviours, multisensory substrates and evolution. Philos Trans R Soc B 366:3006–3015

    Article  Google Scholar 

  • Comer CM, Mara E, Murphy KA, Getman M, Mungy MC (1994) Multisensory control of escape in the cockroach Periplaneta americana. II. Patterns of touch-evoked behavior. J Comp Physiol A 174:13–26

    Article  Google Scholar 

  • Comer CM, Parks L, Halvorsen MB, Breese-Terteling A (2003) The antennal system and cockroach evasive behavior. II. Stimulus identification and localization are separable antennal functions. J Comp Physiol A 189:97–103

    CAS  Google Scholar 

  • Dicke M, Grostal P (2001) Chemical detection of natural enemies by arthropods: an ecological perspective. Annu Rev Ecol Syst 32:1–23

    Article  Google Scholar 

  • Dumpert K, Gnatzy W (1977) Cricket combined mechanoreceptors and kicking response. J Comp Physiol 122:9–25

    Article  Google Scholar 

  • Erber J, Kierzek S, Sander E, Grandy K (1998) Tactile learning in the honeybee. J Comp Physiol A 183:737–744

    Article  Google Scholar 

  • Foelix RF (1985) Mechano- and chemoreceptive sensilla. In: Barth FG (ed) Neurobiology of arachnids. Springer, Berlin, pp 118–137

    Chapter  Google Scholar 

  • Foelix RF, Chu-Wang I-W (1973) The morphology of spider sensilla. I. Mechanoreceptors. Tissue Cell 5:451–460

    Article  PubMed  CAS  Google Scholar 

  • Fudalewicz-Niemczyk W, Rosciszewska M (1973) The peripheric nervous system of the larva of Gryllus domesticus L. (Orthoptera). Part I. Antenna. Acta Biol Cracov Zoo 16:209–217

    Google Scholar 

  • Gebhardt M, Honegger H-W (2001) Physiological characterisation of antennal mechanosensory descending interneurons in an insect (Gryllus bimaculatus, Gryllus campestris) brain. J Exp Biol 204:2265–2275

    PubMed  CAS  Google Scholar 

  • Gnatzy W, Heußlein R (1986) Digger wasp against crickets. Naturwissenschaften 73:212–215

    Article  Google Scholar 

  • Hardy TN, Shaw KC (1983) The role of chemoreception in sex recognition by male crickets: Acheta domesticus and Teleogryllus oceanicus. Physiol Entomol 8:151–166

    Article  Google Scholar 

  • Harley CM, English BA, Ritzmann RE (2009) Characterization of obstacle negotiation behaviors in the cockroach, Blaberus discoidalis. J Exp Biol 212:1463–1476

    Article  PubMed  CAS  Google Scholar 

  • Harris DJ, Mill PJ (1977) Observation on the leg receptors of Ciniflo (Araneida: Disctynidae). I. External mechanoreceptors. J Comp Phyiol 119:37–54

    Article  Google Scholar 

  • Honegger H-W (1981) A preliminary note on a new optomotor response in crickets: antennal tracking of moving targets. J Comp Physiol 142:419–421

    Article  Google Scholar 

  • Honegger H-W, Allgäuer C, Klepsch U, Welker J (1990) Morphology of antennal motoneurons in the brains of two crickets, Gryllus bimaculatus and Gryllus campestris. J Comp Neurol 291:256–268

    Article  PubMed  CAS  Google Scholar 

  • Iwasaki M, Katagiri C (2008) Cuticular lipids and odors induce sex-specific behaviors in the male cricket Gryllus bimaculatus. Comp Biochem Phys A 149:306–313

    Article  Google Scholar 

  • Kevan P, Lane MA (1985) Flower petal microtexture is a tactile cue for bees. Proc Natl Acad Sci USA 82:4750–4752

    Article  PubMed  CAS  Google Scholar 

  • Kortet R, Hedrick A (2004) Detection of the spider predator, Hololena nedra by naïve juvenile field crickets (Gryllus integer) using indirect cues. Behaviour 141:1189–1196

    Article  Google Scholar 

  • Loher W, Rence B (1978) The mating behavior of Teleogryllus commodus (Walker) and its central and peripheral control. Z Tierpsychol 46:225–259

    Article  Google Scholar 

  • Martin H (1965) Leistungen des topochemischen Sinnes bei der Honigbiene. Z Vergl Physiol 50:254–292

    Google Scholar 

  • Miyashita T, Shinkai A (1995) Design and prey capture ability of webs of the spiders Nephila clavata and Argiope bruennichii. Acta Arachnol 44:3–10

    Article  Google Scholar 

  • Okada J, Toh Y (2000) The role of antennal hair plates in object-guided tactile orientation of the cockroach (Periplaneta americana). J Comp Physiol A 186:849–857

    Article  PubMed  CAS  Google Scholar 

  • Okada J, Toh Y (2004) Spatio-temporal patterns of antennal movements in the searching cockroach. J Exp Biol 207:3693–3706

    Article  PubMed  Google Scholar 

  • Okada J, Toh Y (2006) Active tactile sensing for localization of objects by the cockroach antenna. J Comp Physiol A 192:715–726

    Article  Google Scholar 

  • Rence B, Loher W (1977) Contact chemoreceptive sex recognition in the male cricket, Teleogryllus commodus. Physiol Entomol 2:225–236

    Article  Google Scholar 

  • Schneider D (1964) Insect antennae. Annu Rev Entomol 8:103–122

    Article  Google Scholar 

  • Schöneich S, Schildberger K, Stevenson PA (2011) Neuronal organization of a fast-mediating cephalothoracic pathway for antennal-tactile information in the cricket (Gryllus bimaculatus DeGeer). J Comp Neurol 519:1677–1690

    Article  PubMed  Google Scholar 

  • Schütz C, Dürr V (2011) Active tactile exploration for adaptive locomotion in the stick insect. Philos Trans R Soc B 366:2996–3005

    Article  Google Scholar 

  • Staudacher E, Schildberger K (1999) A newly described neuropile in the deutocerebrum of the cricket: antennal afferents and descending interneurons. Zoology 102:212–226

    Google Scholar 

  • Staudacher E, Gebhardt MJ, Dürr V (2005) Antennal movements and mechanoreception: neurobiology of active tactile sensors. Adv Insect Physiol 32:49–205

    Article  CAS  Google Scholar 

  • Steinbrecht RA (1984) Chemo-, hygro-, and thermoreceptors. In: Bereiter-Hahn J, Matoltsy AG, Richards KS (eds) Biology of the integument, vol 1. Springer, Berlin, pp 523–553

    Google Scholar 

  • Tregenza T, Wedell N (1997) Definitive evidence for cuticular pheromones in a cricket. Anim Behav 54:979–984

    Article  PubMed  Google Scholar 

  • Ye S, Comer CM (1996) Correspondence of escape-turning behavior with activity of descending mechanosensory interneurons in the cockroach, Periplaneta americana. J Neurosci 16:5844–5853

    PubMed  CAS  Google Scholar 

  • Zacharuk RY (1985) Antennae and sensilla. In: Kerkut GA, Gilbert LI (eds) Comprehensive insect physiology, biochemistry and pharmacology vol 6. Pergamon Press, Oxford, pp 1–69

    Google Scholar 

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Acknowledgments

The authors are grateful to Drs. Fumio Yokohari (Fukuoka University), Hiroyuki Nakagawa (Fukuoka University), Toshio Ichikawa (Kyushu University), and Yoshihiro Toh (Professor Emeritus at Kyushu University) for technical assistance in the SEM study. This study was supported in part by Grant-in-Aid for Scientific Research (C) from the Japan Society for the Promotion of Science (19570070), the Yamada Science Foundation, and Launch-up support from Nagasaki University.

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  1. Graduate School of Fisheries Science and Environmental Studies, Nagasaki University, Nagasaki, 852-8521, Japan

    Jiro Okada & Seiryo Akamine

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  1. Jiro Okada
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  2. Seiryo Akamine
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Correspondence to Jiro Okada.

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Okada, J., Akamine, S. Behavioral response to antennal tactile stimulation in the field cricket Gryllus bimaculatus . J Comp Physiol A 198, 557–565 (2012). https://doi.org/10.1007/s00359-012-0729-y

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  • DOI: https://doi.org/10.1007/s00359-012-0729-y

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