Skip to main content

Neuromodulators and the Control of Aggression in Crickets

  • Chapter
  • First Online:
The Cricket as a Model Organism

Abstract

Crickets have emerged as ideal model systems for investigating the mechanisms controlling intraspecific aggressive behaviour. As in many animals, male aggression in crickets is shaped by numerous experiences including physical exertion, past wins and defeats and the acquisition of resources. This chapter reviews work revealing that neuromodulators, primarily octopamine and nitric oxide, mediate such experience-dependent plasticity by modulating the relative behavioural thresholds to fight and to flee. Octopamine, the invertebrate analogue of noradrenaline, promotes the tendency to fight by mediating the effects of flying, winning and shelter occupancy and thus represents the motivational component of aggression. The gaseous neuromodulator nitric oxide, on the other hand, mediates the decision to flee and induces a period of prolonged submissiveness, which is characteristic for social defeat in many animals. Accumulating evidence also suggests a role for serotonin, dopamine and selected peptides in controlling insect aggression. The roles for neuromodulators in insect aggression are in essence similar to those emerging for corresponding signalling molecules in mammals, where their specific behavioural functions are less clear.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 149.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 199.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 199.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Adamo SA, Baker JL (2011) Conserved features of chronic stress across phyla: the effects of long-term stress on behavior and the concentration of the neurohormone octopamine in the cricket, Gryllus texensis. Horm Behav 60:478–483

    Article  CAS  PubMed  Google Scholar 

  • Adamo SA, Hoy RR (1995) Agonistic behavior in male and female field crickets, Gryllus bimaculatus, and how behavioural context influences its expression. Anim Behav 49:1491–1501

    Article  Google Scholar 

  • Adamo SA, Linn CE, Hoy RR (1995) The role of neurohormonal octopamine during ‘fight or flight’ behaviour in the field cricket Gryllus bimaculatus. J Exp Biol 198:1691–1700

    CAS  PubMed  Google Scholar 

  • Albert D, Walsh M, Jonik R (1993) Aggression in humans: what is its biological foundation? Neurosci Biobehav Rev 17:405–425

    Article  CAS  PubMed  Google Scholar 

  • Alekseyenko OV, Kravitz EA (2015) Serotonin and the search for the anatomical substrate of aggression. Fly 8(4):1–6

    Google Scholar 

  • Alekseyenko OV, Lee C, Kravitz EA (2010) Targeted manipulation of serotonergic neurotransmission affects the escalation of aggression in adult male Drosophila melanogaster. PLoS One 5:e10806

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Alexander RD (1961) Aggressiveness, territoriality, and sexual behaviour in field crickets (Orthoptera: Gryllidae). Behavior 17:130–223

    Article  Google Scholar 

  • Anstey ML, Rogers SM, Ott SR, Burrows M, Simpson SJ (2009) Serotonin mediates behavioral gregarization underlying swarm formation in desert locusts. Science 323:627–630

    Article  CAS  PubMed  Google Scholar 

  • Aonuma H, Watanabe T (2012) Octopaminergic system in the brain controls aggressive motivation in the ant. Formica Jpn Acta Biol Hung 63(Suppl 2):63–68

    Article  Google Scholar 

  • Archer J (1988) The behavioural biology of aggression. Cambridge University Press, Cambridge

    Google Scholar 

  • Baier A, Wittek B, Brembs B (2002) Drosophila as a new model organism for the neurobiology of aggression? J Exp Biol 205:1233–1240

    PubMed  Google Scholar 

  • Barron AB, Sovik E, Cornish J (2010) The roles of dopamine and related compounds in reward-seeking behavior across animals phyla. Front Behav Neurosci 4:1–9

    Article  CAS  Google Scholar 

  • Bertram SM, Rook VLM, Fitzsimmons JM, Fitzsimmons LP (2011) Fine- and broad-scale approaches to understanding the evolution of aggression in crickets. Ethology 117:1067–1080

    Article  Google Scholar 

  • Bhatia N, Maiti PP, Choudhary A, Tuli A, Masih D, Khan MMU et al (2011) Animal models in the study of stress: a review. NSHM J Pharm Healthc Manag 2:42–50

    Google Scholar 

  • Bidaye SS, Machacek C, Wu Y, Dickson BJ (2014) Neuronal control of Drosophila walking direction. Science 344:97–101

    Article  CAS  PubMed  Google Scholar 

  • Blenau W, Baumann A (2001) Molecular and pharmacological properties of insect biogenic amine receptors: lessons from Drosophila melanogaster and Apis mellifera. Arch Insect Biochem Physiol 48:13–38

    Article  CAS  PubMed  Google Scholar 

  • Böhm H, Schildberger K (1992) Brain neurones involved in the control of walking in the cricket Gryllus bimaculatus. J Exp Biol 166:113–130

    Google Scholar 

  • Brace RC, Purvey J (1978) Size-dependant dominance hierarchy in the anemone Actinia equina. Nature 273:752–753

    Article  Google Scholar 

  • Bräunig P (1991) Suboesophageal DUM neurons innervate the principal neuropiles of the locust brain. Philos Trans R Soc Lond B 332:221–240

    Article  Google Scholar 

  • Braunig P, Pflüger HJ (2001) The unpaired median neurons of insects. Adv Insect Physiol 28:185–266

    Article  Google Scholar 

  • Bräunig P, Allgäuer C, Honegger HW (1990) Suboesophageal DUM neurones are part of the antennal motor system of locusts and crickets. Experientia 46:259–261

    Article  Google Scholar 

  • Briffa M (2008) Decisions during fights in the house cricket, Acheta domesticus: mutual or self assessment of energy, weapons and size? Anim Behav 75:1053–1062

    Article  Google Scholar 

  • Brown WD, Smith AT, Moskalik B, Gabriel J (2006) Aggressive contests in house crickets: size, motivation and the information content of aggressive songs. Anim Behav 72:225–233

    Article  Google Scholar 

  • Brown WD, Chimenti AJ, Siebert JR (2007) The payoff of fighting in house crickets: motivational asymmetry increases male aggression and mating success. Ethology 113:457–465

    Article  Google Scholar 

  • Bubak AN, Grace JL, Watt MJ, Renner KJ, Swallow JG (2014) Neurochemistry as a bridge between morphology and behavior: perspectives on aggression in insects. Curr Zool 60:778–790

    Article  Google Scholar 

  • Buhl E, Schildberger K, Stevenson PA (2008) A muscarinic cholinergic mechanism underlies activation of the central pattern generator for locust flight. J Exp Biol 211:2346–2357

    Article  CAS  PubMed  Google Scholar 

  • Bullerjahn A, Mentel T, Pflüger HJ, Stevenson PA (2006) Nitric oxide: a co-modulator of efferent peptidergic neurosecretory cells including a unique octopaminergic neurone innervating locust heart. Cell Tissue Res 325:345–360

    Article  CAS  PubMed  Google Scholar 

  • Busch S, Tanimoto H (2010) Cellular configuration of single octopamine neurons in Drosophila. J Comp Neurol 518:2355–2364

    Article  CAS  PubMed  Google Scholar 

  • Cacioppo JT, Hawkley LC (2009) Perceived social isolation and cognition. Trends Cogn Sci 13:447–454

    Article  PubMed  PubMed Central  Google Scholar 

  • Cannon WB (1915) Bodily changes in pain, hunger, fear and rage: an account of recent researches into the function of emotional excitement. Appleton, New York

    Book  Google Scholar 

  • Carre JM, Putnam SK (2010) Watching a previous victory produces an increase in testosterone among elite hockey players. Psychoneuroendocrinology 35:475–479

    Article  CAS  PubMed  Google Scholar 

  • Cattaert D, Delbecque JP, Edwards DH, Issa FA (2010) Social interactions determine postural network sensitivity to 5-HT. J Neurosci 30:5603–5616

    Article  CAS  PubMed  Google Scholar 

  • Certel SJ, Savella MG, Schlegel DC, Kravitz EA (2007) Modulation of Drosophila male behavioral choice. Proc Natl Acad Sci U S A 104:4706–4711

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Certel SJ, Leung A, Lin CY, Perez P, Chiang AS, Kravitz EA (2010) Octopamine neuromodulatory effects on a social behavior decision-making network in Drosophila males. PLoS One 5:e13248

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chan YB, Kravitz E (2007) Specific subgroups of FruM neurons control sexually dimorphic patterns of aggression in Drosophila melanogaster. Proc Natl Acad Sci U S A 104:9577–9582

    Google Scholar 

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

    Article  Google Scholar 

  • Craft LL, Perna FM (2004) The benefits of exercise for the clinically depressed. J Clin Psychiatry 6:104–111

    Google Scholar 

  • Davenport AP, Evans PD (1984) Changes in haemolymph octopamine levels associated with food deprivation in the locust Schistocerca gregaria. Physiol Entomol 9:269–274

    Article  CAS  Google Scholar 

  • de Boer SF, Koolhaas JM (2005) 5-HT1A and 5-HT1B receptor agonists and aggression: a pharmacological challenge of the serotonin deficiency hypothesis. Eur J Pharmacol 526:125–139

    Article  PubMed  CAS  Google Scholar 

  • Dierick HA, Greenspan RJ (2007) Serotonin and neuropeptide F have opposite modulatory effects on fly aggression. Nat Genet 39:678–682

    Article  CAS  PubMed  Google Scholar 

  • DiRienzo N, Pruitt JN, Hedrick AV (2012) Juvenile exposure to acoustic sexual signals from conspecifics alters growth trajectory and an adult personality trait. Anim Behav 84:861–868

    Article  Google Scholar 

  • Dixon KA, Cade WH (1986) Some factors influencing male-male aggression in the field Cricket Gryllus integer (time of day, age, weight and sexual maturity). Anim Behav 34:340–346

    Article  Google Scholar 

  • Duch C, Mentel T, Pflüger HJ (1999) Distribution and activation of different types of octopaminergic DUM neurons in the locust. J Comput Neurol 403:119–134

    Article  CAS  Google Scholar 

  • Dyakonova VE, Krushinkskii AL (2006) Effects of an NO synthase inhibitor on aggressive and sexual behavior in male crickets. Neurosci Behav Physiol 36:565–571

    Article  CAS  Google Scholar 

  • Dyakonova VE, Krushinkskii AL (2013) Serotonin precursor (5-hydroxytryptophan) causes substantial changes in the fighting behavior of male crickets, Gryllus bimaculatus. J Comp Physiol A 199:601–609

    Article  CAS  Google Scholar 

  • Dyakonova VE, Krushinskii AL (2008) Previous motor experience enhances courtship behaviour in male cricket Gryllus bimaculatus. J Insect Behav 21:172–180

    Article  Google Scholar 

  • Dyakonova VE, Schurmann F, Sakharov DA (1999) Effects of serotonergic and opioidergic drugs on escape behaviors and social status of male crickets. Naturwissenschaften 86:435–437

    Article  CAS  PubMed  Google Scholar 

  • Dyakonova VE, Schurmann FW, Sakharov DA (2002) Effects of opiate ligands on intraspecific aggression in crickets. Peptides 23:835–841

    Article  CAS  PubMed  Google Scholar 

  • Edwards AC, Zwarts L, Yamamoto A, Callaerts P, Mackay TF (2009) Mutations in many genes affect aggressive behavior in Drosophila melanogaster. BMC Biol 7:29

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Elwood RW, Arnott G (2012) Understanding how animals fight with Lloyd Morgan’s canon. Anim Behav 84:1095–1102

    Article  Google Scholar 

  • Erber J, Kloppenburg P, Scheidler A (1993) Neuromodulation by serotonin and octopamine in the honeybee: behaviour, neuroanatomy and electrophysiology. Experientia 49:1073–1083

    Article  CAS  Google Scholar 

  • Evans PD (1985) Octopamine. In: Kerkut GA, Gilbert LI (eds) Comprehensive insect physiology biochemistry and pharmacology. Pergamon, Oxford, pp 499–530

    Google Scholar 

  • Fernandez MP, Chan YB, Yew JY, Billeter JC, Dreisewerd K, Levine JD et al (2010) Pheromonal and behavioral cues trigger male-to-female aggression in Drosophila. PLoS Biol 8:e1000541

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Fuxjager MJ, Marler CA (2010) How and why the winner effect forms: influences of contest environment and species differences. Behav Ecol 21:37–45

    Article  Google Scholar 

  • Getting PA, Dekin MA (1985) Tritonia swimming. A model system for integration within rhythmic motor systems. In: Selverston AI (ed) Model networks and behavior. Plenum Press, New York, pp 3–20

    Chapter  Google Scholar 

  • Ghosal K, Gupta M, Killian KA (2009) Agonistic behavior enhances adult neurogenesis in male Acheta domesticus crickets. J Exp Biol 212:2045–2056

    Article  PubMed  PubMed Central  Google Scholar 

  • Ghosal K, Naples SP, Rabe AR, Killian KA (2010) Agonistic behavior and electrical stimulation of the antennae induces Fos-like protein expression in the male cricket brain. Arch Insect Biochem Physiol 74:38–51

    Article  CAS  PubMed  Google Scholar 

  • Giurfa M (2012) Social learning in insects: a higher-order capacity? Front Behav Neurosci 6:57

    Article  PubMed  PubMed Central  Google Scholar 

  • Goldstein RS, Camhi JM (1991) Different effects of the biogenic amines dopamine, serotonin and octopamine on the thoracic and abdominal portions of the escape circuit in the cockroach. J Comp Physiol A 168:103–112

    Article  CAS  PubMed  Google Scholar 

  • Gras H, Hörner M, Runge L, Schürmann FW (1990) Prothoracic DUM neurons of the cricket Gryllus bimaculatus respond to natural stimuli activity in walking behaviour. J Comp Physiol A 166:901–914

    Article  Google Scholar 

  • Haden SC, Scarpa A (2007) The noradrenergic system and its involvement in aggressive behaviors. Aggress Violent Behav 12:1–15

    Article  Google Scholar 

  • Hall MD, McLaren L, Brooks RC, Lailvaux SP (2010) Interactions among performance capacities predict male combat outcomes in the field cricket. Funct Ecol 24:159–164

    Article  Google Scholar 

  • Hammer M (1993) An identified neurone mediates the unconditioned stimulus in associative olfactory learning in honeybees. Nature 366:59–63

    Article  CAS  PubMed  Google Scholar 

  • Hammer M, Menzel R (1995) Learning and memory in the honey bee (Review). J Neurosci 15:1617–1630

    CAS  PubMed  Google Scholar 

  • Hauser F, Cazzamali G, Williamson M, Blenau W, Grimmelikhuijzen CJP (2006) A review of neurohormone GPCRs present in the fruitfly Drosophila melanogaster and the honey bee Apis mellifera. Prog Neurobiol 80:1–19

    Article  CAS  PubMed  Google Scholar 

  • Henry J, Scherman D (1989) Radioligands of the vesicular monoamine transporter and their use as markers of monoamine storage vesicles. Biochem Pharmacol 28:2395–2404

    Article  Google Scholar 

  • Hofmann HA (1996) The cultural history of Chinese fighting crickets: a contribution not only to the history of biology. [German]. Biologisches Zbl 115:206–213

    Google Scholar 

  • Hofmann HA, Schildberger K (2001) Assessment of strength and willingness to fight during aggressive encounters in crickets. Anim Behav 62:337–348

    Article  Google Scholar 

  • Hofmann HA, Stevenson PA (2000) Flight restores fight in crickets. Nature 403:613

    Article  CAS  PubMed  Google Scholar 

  • Homberg U (2002) Neurotransmitters and neuropeptides in the brain of the locust. Microsc Res Tech 56:189–209

    Article  CAS  PubMed  Google Scholar 

  • Hoyer SC, Eckart A, Herrel A, Zars T, Fischer SA, Hardie SL et al (2008) Octopamine in male aggression of Drosophila. Curr Biol 18:159–167

    Article  CAS  PubMed  Google Scholar 

  • Hsu Y, Earley RL, Wolf LL (2005) Modulation of aggressive behaviour by fighting experience: mechanisms and contest outcomes. Biol Rev Camb Philos Soc 81:33–74

    Article  Google Scholar 

  • Huber F (1955) Sitz und Bedeutung nervöser Zentren für Instinkthandlungen beim Männchen von Gryllus campestris. Z Tierpsychol 12:12–48

    Article  Google Scholar 

  • Huber F (1960) Untersuchungen über die Funktion des Zentralnervensystems und insbesondere des Gehirnes bei der Fortbewegung und der Lauterzeugung der Grillen. Z Vergleichende Tierphysiologie 44:60–132

    Article  Google Scholar 

  • Huber F, Moore TE, Loher W (1989) Cricket behavior and neurobiology. Cornell University, New York

    Google Scholar 

  • Huhman K (2006) Social conflict models: can they inform us about human psychopathology? Horm Behav 50:640–646

    Article  PubMed  Google Scholar 

  • Hurd PL (2006) Resource holding potential, subjective resource value, and game theoretical models of aggressiveness signalling. J Theor Biol 241:639–648

    Article  PubMed  Google Scholar 

  • Iba M, Nagao T, Urano A (1995) Effects of population density on growth, behavior and levels of biogenic amines in the cricket, Gryllus bimaculatus. Zool Sci 12:695–702

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Iwasaki M, Delago A, Nishino H, Aonuma H (2006) Effects of previous experience on the agonistic behaviour of male crickets, Gryllus bimaculatus. Zool Sci 23:863–872

    Article  PubMed  Google Scholar 

  • Iwasaki M, Nishino H, Delago A, Aonuma H (2007) Effects of NO/cGMP signaling on behavioral changes in subordinate male crickets, Gryllus bimaculatus. Zool Sci 24:860–868

    Article  CAS  PubMed  Google Scholar 

  • Johnson O, Becnel J, Nichols CD (2009) Serotonin 5-HT(2) and 5-HT(1A)-like receptors differentially modulate aggressive behaviors in Drosophila melanogaster. Neuroscience 158:1292–1300

    Article  CAS  PubMed  Google Scholar 

  • Judge KA, Bonanno VL (2008) Male weaponry in a fighting cricket. PLoS One 3:e3980

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Judge KA, Ting JJ, Schneider J, Fitzpatrick MJ (2010) A lover, not a fighter: mating causes male crickets to lose fights. Behav Ecol Sociobiol 64:1971–1979

    Article  Google Scholar 

  • Jung SN, Borst A, Haag J (2011) Flight activity alters velocity tuning of fly motion-sensitive neurons. J Neurosci 31:9231–9237

    Article  CAS  PubMed  Google Scholar 

  • Kemp DJ, Wiklund C (2004) Residency effects in animal contests. Proc R Soc Lond 271:1707–1711

    Article  Google Scholar 

  • Khazraie K, Campan M (1999) The role of prior agonistic experience in dominance relationships in male crickets Gryllus bimaculatus (Orthoptera: Gryllidae). Behav Processes 44:341–348

    Article  CAS  PubMed  Google Scholar 

  • Killian KA, Allen JR (2008) Mating resets male cricket aggression. J Insect Behav 21:535–548

    Article  Google Scholar 

  • Kravitz E, Huber R (2003) Aggression in invertebrates. Curr Opin Neurobiol 13:736–743

    Article  CAS  PubMed  Google Scholar 

  • Lihoreau M, Brepson L, Rivault C (2009) The weight of the clan: even in insects, social isolation can induce a behavioural syndrome. Behav Processes 82:81–84

    Article  PubMed  Google Scholar 

  • Marder E (2012) Neuromodulation of neuronal circuits: back to the future. Neuron 76:1–11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maynard Smith J, Price GR (1973) The logic of animal conflict. Nature 246:15–18

    Article  Google Scholar 

  • McFarland DJ, Sibly RM (1975) The behavioural final common path. Philos Trans R Soc B 270:265–293

    Article  CAS  Google Scholar 

  • Mendl M, Paul ES, Chittka L (2011) Animal behaviour: emotions in invertebrates? Curr Biol 21:R463–R465

    Article  CAS  PubMed  Google Scholar 

  • Miczek KA, Nikulina EM, Takahashi A, Covington HE III, Yap JJ, Boyson CO et al (2011) Gene expression in aminergic and peptidergic cells during aggression and defeat: relevance to violence, depression and drug abuse. Behav Genet 41:787–802

    Article  PubMed  Google Scholar 

  • Mizunami M, Unoki S, Mori Y, Hirashima D, Hatano A, Matsumoto Y (2009) Roles of octopaminergic and dopaminergic neurons in appetitive and aversive memory recall in an insect. BMC Biol 7:46

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Morris OT, Duch C, Stevenson PA (1999) Differential activation of octopaminergic (DUM) neurones via proprioceptors responding to flight muscle contractions in the locust. J Exp Biol 202:3555–3564

    PubMed  Google Scholar 

  • Müller U (1997) The nitric oxide system in insects. Prog Neurobiol 51:363–381

    Article  PubMed  Google Scholar 

  • Murakami S, Itoh MT (2001) Effects of aggression and wing removal on brain serotonin levels in male crickets, Gryllus bimaculatus. J Insect Physiol 47:1309–1312

    Article  CAS  PubMed  Google Scholar 

  • Murakami S, Itoh MT (2003) Removal of both antennae influences the courtship and aggressive behaviors in male crickets. J Neurobiol 57:110–118

    Article  PubMed  Google Scholar 

  • Nagao T, Tanimura T (1993) Distribution of biogenic amines in the cricket central nervous system. Anal Biochem 171:33–40

    Article  Google Scholar 

  • Nagao T, Tanimura T, Shimozawa T (1991) Neurohormonal control of the mating interval in the male cricket, Gryllus bimaculatus DeGeer. J Comp Physiol A 168:159–164

    Article  Google Scholar 

  • Nelson RJ, Trainor BC (2007) Neural mechanisms of aggression. Nature reviews. Neuroscience 8:536–546

    CAS  PubMed  Google Scholar 

  • Nilsen SP, Chan YB, Huber R, Kravitz EA (2004) Gender-selective patterns of aggressive behavior in Drosophila melanogaster. Proc Natl Acad Sci U S A 101:12342–12347

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nosil P (2002) Food fights in house crickets, Acheta domesticus, and the effects of body size and hunger level. Can J Zool 80:409–417

    Article  Google Scholar 

  • O’Connell LA, Hofmann HA (2011) The vertebrate mesolimbic reward system and social behavior network: a comparative synthesis. J Comp Neurol 519:3599–3639

    Article  PubMed  Google Scholar 

  • Passamonti L, Crockett MJ, Apergis-Schoute AM, Clark L, Rowe JB, Calder AJ et al (2012) Effects of acute tryptophan depletion on prefrontal-amygdala connectivity while viewing facial signals of aggression. Biol Psychiatry 71:36–43

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Payne RJH (1998) Gradually escalating fights and displays: the cumulative assessment model. Anim Behav 56:651–662

    Article  CAS  PubMed  Google Scholar 

  • Perry CJ, Barron AB (2013) Neural mechanisms of reward in insects. Annu Rev Entomol 58:543–562

    Article  CAS  PubMed  Google Scholar 

  • Pfennig DW, Reeve HK (1989) Neighbor recognition and context dependent aggression in a solitary wasp, Sphecius speciosus (Hymenoptera, sphecidae). Ethology 80:1–18

    Article  Google Scholar 

  • Pflüger H, Stevenson P (2005) Evolutionary aspects of octopaminergic systems with emphasis on arthropods. Arthropod Struct Dev 34:379–396

    Article  CAS  Google Scholar 

  • Raichlen DA, Foster AD, Gerdeman GL, Seillier A, Giuffrida A (2011) Wired to run: exercise-induced endocannabinoid signaling in humans and cursorial mammals with implications for the ‘runner’s high’. J Exp Biol 215:1331–1336

    Article  CAS  Google Scholar 

  • Rillich J, Stevenson PA (2011) Winning fights induces hyperaggression via the action of the biogenic amine octopamine in crickets. PLoS One 6:e28891

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rillich J, Stevenson PA (2014) A fighter’s comeback: dopamine is necessary for recovery of aggression after social defeat. Horm Behav 66:696–704

    Article  CAS  PubMed  Google Scholar 

  • Rillich J, Stevenson PA (2015) Releasing stimuli and aggression in crickets: octopamine promotes escalation and maintenance but not initiation. Front Behav Neurosci 9(95):1–11

    Google Scholar 

  • Rillich J, Schildberger K, Stevenson PA (2007) Assessment strategy of fighting crickets revealed by manipulating information exchange. Anim Behav 74:823–836

    Article  Google Scholar 

  • Rillich J, Buhl E, Schildberger K, Stevenson PA (2009) Female crickets are driven to fight by the male courting and calling songs. Anim Behav 77:737–742

    Article  Google Scholar 

  • Rillich J, Schildberger K, Stevenson PA (2011) Octopamine and occupancy – an aminergic mechanism for intruder-resident aggression in crickets. Proc R Soc Lond B 278:1873–1880

    Article  Google Scholar 

  • Rillich J, Stevenson PA, Pflüger HJ (2013) Flight and walking in locusts – cholinergic co-activation, temporal coupling and its modulation by biogenic amines. PLoS One 8(5):e62899

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rodriguez-Munoz R, Bretman A, Tregenza T (2011) Guarding males protect females from predation in a wild insect. Curr Biol 21:1716–1719

    Article  CAS  PubMed  Google Scholar 

  • Roeder T (1999) Octopamine in invertebrates. Prog Neurobiol 59:533–561

    Article  CAS  PubMed  Google Scholar 

  • Roeder T, Degen J, Gewecke M (1998) Epinastine, a highly specific antagonist of insect neuronal octopamine receptors. Eur J Pharmacol 349:171–177

    Article  CAS  PubMed  Google Scholar 

  • Rogers SM, Matheson T, Sasaki K, Kendrick K, Simpson SJ, Burrows M (2004) Substantial changes in central nervous system neurotransmitters and neuromodulators accompany phase change in the locust. J Exp Biol 207:3603–3617

    Article  CAS  PubMed  Google Scholar 

  • Rutte C, Taborsky M, Brinkhof MW (2006) What sets the odds of winning and losing? Trends Ecol Evol 21:16–21

    Article  PubMed  Google Scholar 

  • Sakura M, Aonuma H (2013) Aggressive behavior in the antennectomized male cricket Gryllus bimaculatus. J Exp Biol 216:2221–2228

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Schröter U, Malun D, Menzel R (2007) Innervation pattern of suboesophageal ventral unpaired median neurones in the honeybee brain. Cell Tissue Res 327:647–667

    Article  PubMed  Google Scholar 

  • Schwärzel M, Monastirioti M, Scholz H, Friggi-Grelin F, Birman S, Heisenberg M (2003) Dopamine and octopamine differentiate between aversive and appetitive olfactory memories in Drosophila. J Neurosci 23:10495–10502

    Google Scholar 

  • Simmons LW (1986) Inter-male competition and mating success in the field cricket, Gryllus bimaculatus (de Geer). Anim Behav 34:567–579

    Article  Google Scholar 

  • Simpson SJ, Stevenson PA (2015) Neuromodulation of social behaviour in insects. In: Canli T (ed) The Oxford handbook of molecular psychology. Oxford University Press, Oxford, pp 27–51

    Google Scholar 

  • Simpson JS, Sword GA (2009) Phase polyphenism in locusts: mechanisms, population consequences, adaptive significance and evolution. In: Whitman DW, Ananthakrishnan TN (eds) Phenotypic plasticity of insects, mechanisms and consequences. Science Publishers, Enfield, pp 147–189

    Google Scholar 

  • Sokolowski MB (2010) Social interactions in “simple” model systems. Neuron 65:780–794

    Article  CAS  PubMed  Google Scholar 

  • Sombati S, Hoyle G (1984) Generation of specific behaviors in a locust by local release into neuropil of the natural neuromodulator octopamine. J Neurobiol 15:481–506

    Article  CAS  PubMed  Google Scholar 

  • Spörhase-Eichmann U, Vullings HGB, Buijs RM, Hörner M (1992) Octopamine-immunoreactive neurones in the central nervous system of the cricket Gryllus bimaculatus. Cell Tissue Res 268:287–304

    Article  PubMed  Google Scholar 

  • Staudacher E, Schildberger K (1998) Gating of sensory responses of descending brain neurones during walking in crickets. J Exp Biol 201:559–572

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Stevenson PA, Kutsch W (1987) A reconsideration of the central pattern generator concept for locust flight. J Comp Physiol A 161:115–129

    Article  Google Scholar 

  • Stevenson PA, Rillich J (2012) The decision to fight or flee – insights into underlying mechanism in crickets. Front Neurosci 6(118):1–12

    Google Scholar 

  • Stevenson PA, Rillich J (2013) Isolation associated aggression in crickets is a result of recovery from social subjugation. Plos ONE 8(9):e74965

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stevenson PA, Rillich J (2015) Adding up the odds – nitric oxide underlies the decision to flee and post conflict depression. Sci Adv 1:e1500060

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Stevenson PA, Schildberger K (2013) Mechanisms of experience dependant control of aggression in crickets. Curr Opin Neurobiol 23:318–323

    Article  CAS  PubMed  Google Scholar 

  • Stevenson PA, Spörhase-Eichmann U (1995) Localization of octopaminergic neurons in insects. Comp Biochem Physiol B 11:203–215

    Article  Google Scholar 

  • Stevenson PA, Hofmann HA, Schoch K, Schildberger K (2000) The fight and flight responses of crickets depleted of biogenic amines. J Neurobiol 43:107–120

    Article  CAS  PubMed  Google Scholar 

  • Stevenson PA, Dyakonova VE, Rillich J, Schildberger K (2005) Octopamine and experience-dependent modulation of aggression in crickets. J Neurosci 25:1431–1441

    Article  CAS  PubMed  Google Scholar 

  • Tachon G, Murray A-M, Gray DA, Cade WH (1999) Agonistic displays and the benefits of fighting in the field cricket, Gryllus bimaculatus. J Insect Behav 12:533–543

    Article  Google Scholar 

  • Tops M, Russo S, Boksem MA, Tucker DM (2009) Serotonin: modulator of a drive to withdraw. Brain Cogn 71:427–436

    Article  PubMed  Google Scholar 

  • Vrontou E, Nilsen SP, Demir E, Kravitz EA, Dickson BJ (2006) Fruitless regulates aggression and dominance in Drosophila. Nat Neurosci 9:1469–1471

    Article  CAS  PubMed  Google Scholar 

  • Wada-Katsumata A, Yamaoka R, Aonuma H (2011) Social interactions influence dopamine and octopamine homeostasis in the brain of the ant Formica japonica. J Exp Biol 214:1707–1713

    Article  CAS  PubMed  Google Scholar 

  • Wang L, Anderson DJ (2010) Identification of an aggression-promoting pheromone and its receptor neurons in Drosophila. Nature 463:227–231

    Article  CAS  PubMed  Google Scholar 

  • Watanabe T, Aonuma H (2012) Identification and expression analyses of a novel serotonin receptor gene, 5-HT2β, in the field cricket, Gryllus bimaculatus. Acta Biol Hung 63:58–62

    Article  CAS  PubMed  Google Scholar 

  • Watanabe T, Sadamoto H, Aonuma H (2011) Identification and expression analysis of the genes involved in serotonin biosynthesis and transduction in the field cricket Gryllus bimaculatus. Insect Mol Biol 20:619–635

    Article  CAS  PubMed  Google Scholar 

  • Wingfield JC, Hegner RE, Dufty AM Jr, Ball GF (1990) The challenge hypothesis—theoretical implications for patterns of testosterone secretion, mating systems, and breeding strategies. Am Nat 136:829–846

    Article  Google Scholar 

  • Yano S, Ikemoto Y, Aonuma H, Asama H (2012) Forgetting curve of cricket, Gryllus bimaculatus, derived by using serotonin hypothesis. Robot Auton Syst 60:722–728

    Article  Google Scholar 

  • Yoritsune A, Aonuma H (2012) The anatomical pathways for antennal sensory information in the central nervous system of the cricket, Gryllus bimaculatus. Invert Neurosci. doi:10.1007/s10158-012-0137-6

    PubMed  Google Scholar 

  • Yurkovic A, Wang, Basu C, Kravitz EA (2006) Learning and memory associated with aggression in Drosophila melanogaster. Proc Natl Acad Sci U S A 103:17519–17524

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou C, Rao Y, Rao Y (2008) A subset of octopaminergic neurons are important for Drosophila aggression. Nat Neurosci 11:1059–1067

    Article  CAS  PubMed  Google Scholar 

  • Zorovic M, Hedwig B (2012) Descending brain neurons in the cricket Gryllus bimaculatus (de Geer): auditory responses and impact on walking. J Comp Physiol A 199:25–34

    Article  Google Scholar 

Download references

Acknowledgements

We thank the German Research Council (DFG) for generous funding (DFG Research Group, FOR 1363, grant STE 714/4-1).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Paul A. Stevenson .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer Japan KK

About this chapter

Cite this chapter

Stevenson, P.A., Rillich, J. (2017). Neuromodulators and the Control of Aggression in Crickets. In: Horch, H., Mito, T., Popadić, A., Ohuchi, H., Noji, S. (eds) The Cricket as a Model Organism. Springer, Tokyo. https://doi.org/10.1007/978-4-431-56478-2_12

Download citation

Publish with us

Policies and ethics