Wasp uses venom cocktail to manipulate the behavior of its cockroach prey

Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology

Volumn 189, Issue 7, 2003, Pages 497-508

  Libersat, F ^a  

^a BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

Author keywords

Ampulex compressa; Grooming; Neurotoxins; Paralysis; Periplaneta americana

Indexed keywords

DOPAMINE; NICOTINIC RECEPTOR; WASP VENOM;

ANIMAL; CHEMICALLY INDUCED DISORDER; COCKROACH; DRUG EFFECT; GROOMING; HYPOKINESIA; NERVOUS SYSTEM; PARAPLEGIA; PHYSIOLOGY; PREDATION; REVIEW; SYNAPSE; THORAX; WASP;

ANIMALS; COCKROACHES; DOPAMINE; GROOMING; HYPOKINESIA; NERVOUS SYSTEM; PARAPLEGIA; PREDATORY BEHAVIOR; RECEPTORS, NICOTINIC; SYNAPSES; THORAX; WASP VENOMS; WASPS;

EID: 0042976462     PISSN: 03407594     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00359-003-0432-0     Document Type: Review

References (82)

1. Adams ME (1996) Neurotoxins, 2nd edn. TINS [Suppl], pp 1-36
2. Adams ME, Oliviera B (1994) Neurotoxins: overview of an emerging research technology. Trends Neurosci 17:151-155
3. Ali DW, Orchard I (1994) Characterization of DA and serotonin receptors on the salivary glands of the locust, Locusta migratoria. Biogenic Amines 10:195-212
4. Beckage NE (2002) Parasite- and pathogen-mediated manipulation of host hormones and behavior. In: (eds) Hormones, brain and behavior, vol 3. Elsevier Sciences, USA, pp 281-316
5. Bettini S (1978) Arthropods venoms, vol 48. Handbook of experimental pharmacology. Springer, Berlin Heidelberg New York
6. Bjorklund A, Lindvall O (1986) Catecholaminergic brain stem regulatory systems. In: Mountcastle VB, Bloom FE, Geiger SR (eds) Handbook of physiology. American Physiological Society, Bethesda, Maryland, pp 155-235
7. Blagburn JM, Sattelle DB (1987) Presynaptic depolarization mediates presynaptic inhibition at a synapse between an identified mechanosensory neurone and giant interneurone 3 in the first instar cockroach, Periplaneta americana. J Exp Biol 127:135-157
8. Blum MS (1981) Chemical defenses of arthropods. Academic Press, New York
9. Callec JJ, Sattelle DB (1973) A simple technique for monitoring the synaptic actions of pharmacological agents. J Exp Biol 59:725-738
10. Camhi JM (1984) A case study in neuroethology: the escape system of the cockroach. In: Camhi JM (ed) Neuroethology. Sinauer, Sunderland, Massachusetts, pp 79-105
11. Camhi JM, Levy A (1989) The code for stimulus direction in a cell assembly in the cockroach. J Comp Physiol A 165:83-97
12. Camhi JM, Nolen TG (1981) Properties of the escape system of cockroaches during walking. J Comp Physiol A 142:339-346
13. Casagrand JL, Ritzmann RE (1992) Biogenic amines modulate synaptic transmission between identified giant interneurons and thoracic interneurons in the escape system of the cockroach. J Neurobiol 23:644-655
14. Claasen DE, Kammer AE (1986) Effects of octopamine, dopamine, and serotonin on production of flight motor output by thoracic ganglia of Manduca sexta. J Neurobiol 17:1-14
15. Comer CM, Dowd JP (1993) Multisensory processing for movement: antennal and cercal mediation of escape turning in the cockroach. In: Beer RD, Ritzmann RE, McKenna T (eds) Biological neural networks in invertebrate neuroethology and robotics. Academic Press, Boston, pp 89-112
16. 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
17. Dorce VA, Sandoval MR (1994) Effects of Tityus serrulatus crude venom on the GABAergic and dopaminergic systems of the rat brain. Toxicon 32:1641-1647
18. Eberhard W (2000) Spider manipulation by a wasp larva. Nature 406:255-256
19. Eldefrawi AT, Eldefrawi ME, Konno K, Mansour NA, Nakanishi K, Oltz E, Usherwood PNR (1988) Structure and synthesis of a potent glutamate receptor antagonist in wasp venom. Proc Natl Acad Sci USA 85:4910-4913
20. Fabre JH (1879) Souvenirs entomologiques, vol 1. Delagrave, Paris (1945 edn), pp 108-112
21. Ferton C (1902) Notes detachees sur l' instinct des hymenoptères mellifères et ravisseurs II. Ann Soc Entomol Fr 71:499-531
22. Fouad K, Libersat F, Rathmayer W (1994) The venom of the cockroach-hunting wasp Ampulex compressa changes motor thresholds: a novel tool for studying the neural control of arousal? Zoology 98:23-34
23. Fouad K, Libersat F, Rathmayer W (1996) Neuromodulation of the escape behavior of the cockroach Periplaneta americana by the venom of the parasitic wasp Ampulex compressa. J Comp Physiol A 178:91-100
24. Gnatzy W (2001) Digger wasp versus cricket: (neuro-)biology of a predator-prey-interaction. Zoology 103:125-139
25. 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
26. Gundelfinger ED (1992). How complex is the nicotinic receptor system of insects? TINS 15:206-211
27. Harvey A (1993) Natural and synthetic neurotoxins. Neuroscience perspectives. Academic Press, London
28. Haspel G, Libersat F (1997) Biochemistry of wasp's neurotoxin and its physiological effect on insect's neurons. Neurosci Lett 48:S24
29. Haspel G, Libersat F (2003) Wasp venom blocks central cholinergic synapses to induce transient paralysis in cockroach prey. J Neurobiol 54:628-637
30. Haspel G, Rosenberg LA, Libersat F (2003) Direct injection of venom by a predatory wasp into cockroach brain. J Neurobiol (in press)
31. Heinrich R, Wenzel B, Elsner N (2001) A role for muscarinic excitation: Control of specific singing behavior by activation of the adenylate cyclase pathway in the brain of grasshoppers. PNAS 98:9919-9923
32. Hogan-Warburg AJ, Hogan JA, Ashton MC (1995) Locomotion and grooming in crickets: competition or time sharing? Anim Behav 49:531-533
33. Hofmann HA, Stevenson PA (2000) Flight restores fight in crickets. Nature 403:613
34. Kien J, Altman JS (1992) Decision-making in the insect nervous system: a model for selection and maintenance of motor programmes. In: Kien J, McCrohan CR, Winlow W (eds) Neurobiology of motor programme selection. Pergamon studies in neuroscience, no 4. Pergamon Press, Oxford, UK, pp 147-169
35. Kravitz EA (1988) Hormonal control of behavior: amines and the biasing of behavioral output in lobsters. Science 241:1775-1781
36. Kravitz EA (2000). Serotonin and aggression: insights gained from a lobster model system and speculations on the role of amine neurons in a complex behavior. J Comp Physiol A 186:221-38
37. Lent CM, Dickinson MH, Marshall CG (1989) Serotonin and leech feeding behavior: obligatory neuromodulation. Am Zool 29:1241-1254
38. Libersat F, Moore J (2000) The parasite Moniliformis moniliformis alters the escape response of its cockroach host Periplaneta americana. J Insect Behav 13:103-110
39. Libersat F, Haspel G, Casagrand J, Fouad K (1999) Localization of the site of effect of a wasp's venom in the cockroach escape circuitry. J Comp Physiol A 184:333-345
40. Liebenthal E, Uhlman O, Camhi JM (1994) Critical parameters of the spike trains in a cell assembly: coding of turn direction by the giant interneurons of the cockroach. J Comp Physiol A 174:281-296
41. Martin J, Ernst R, Heisenberg M (1998) Mushroom bodies suppress locomotor activity in Drosophila melanogaster. Learn Mem 5:179-191
42. Mello LE, Cavalheiro EA (1989) Behavioural, electroencephalographic and neuropathological effects of the intrahippocampal injection of the venom of the South American rattlesnake (Crotalus durissus terrificus). Toxicon 27:189-199
43. Molloy AG, Waddington JL (1984) Dopaminergic behaviour stereospecifically promoted by the D-1 agonist R-SK&F 38393 and selectively blocked by the D-1 antagonist SCH 23390. Psychopharmacology 82:409-410
44. Moore J (2002) Parasites and the behavior of animals. Oxford series in ecology and evolution. Oxford University Press, New York
45. 3H]pifluthixol, a dopamine antagonist, in the brain of the American cockroach, Periplaneta americana. Insect Biochem 17:587-590
46. Nye SW, Ritzmann RE (1992) Motion analysis of leg joints associated with escape turns of the cockroach, Periplaneta americana. J Comp Physiol A 171:183-194
47. Ocker W, Hedwig B, Elsner N (1995) Pharmacological induction and modulation of stridulation in two species of acridid grasshoppers. J Exp Biol 198:1701-1710
48. Olivera BM (1999) Conus venom peptides: correlating chemistry and behavior. J Comp Physiol A 185:353-359
49. Olivera BM, Cruz LJ, Yoshikami D (1999) Effects of Conus peptides on the behavior of mice. Curr Opin Neurobiol 9:772-777
50. Orr N, Orr GL, Hollingworth RM (1992) The Sf9 cell line as a model for studying insect octopamine-receptors. Insect Biochem Mol Biol 22:591-597
51. Piek T (1990) Neurotoxins from venoms of the Hymenoptera - 25 years of research in Amsterdam. Comp Biochem Physiol C 96:223-233
52. Piek T, Spanjer W (1986) Chemistry and pharmacology of solitary wasp venoms. In: Piek T (ed) Venoms of the Hymenoptera. Academic Press, London, pp 161-307
53. Piek T, Visser JH, Veenendaal RL (1984) Change in behaviour of the cockroach, Periplaneta americana, after being stung by the sphecid wasp Ampulex compressa. Entomol Exp Appl 195:195-203
54. Ramirez JM, Pearson KG (1988) Generation of motor patterns for walking and flight in motoneurons supplying bifunctional muscles in the locust. J Neurobiol 19:257-282
55. Rappuoli R, Montecucco C (1997) Guidebook to protein toxins and their use in cell biology. Oxford University Press, Oxford
56. Rathmayer W (1962) Paralysis caused by the digger wasp Philanthus. Nature 196:1148-1151
57. Rathmayer W (1978) Venoms of Sphecidae, Pompilidae, Mutillidae and Bethylidae. In: Bettini S (ed) Handbook of experimental pharmacology, vol 48. Arthropod venoms. Springer, Berlin Heidelberg New York, pp 661-690
58. Reale V Hannan F, Hall LM, Evans PD (1997) Agonist-specific coupling of a cloned Drosophila melanogaster D1-like dopamine receptor to multiple second-messenger pathways by synthetic agonists. J Neurosci 17:6545-6553
59. Ritzmann RE (1993) The neural organization of cockroach escape and its role in context-dependent orientation. In: Beer RD, Ritzmann RE, McKenna T (eds) Biological neural networks in invertebrate neuroethology and robotics. Academic Press, Boston, pp 113-137
60. Ritzmann RE, Pollack AJ (1986) Identification of thoracic interneurons that mediate giant interneurons-to-motor pathways in the cockroach. J Comp Physiol A 159:639-654
61. Ritzmann RE, Pollack AJ (1994) Responses of thoracic interneurons to tactile stimulation in the cockroach, Periplaneta americana. J Neurobiol 25:1113-1128
62. Ritzmann RE, Pollack AJ, Hudson SE, Hyonen A (1991) Convergence of multi-modal sensory signals at the thoracic interneurons of the escape system of the cockroach, Periplaneta americana. Brain Res 563:175-183
63. 3) receptor. Life Sci 50:21-28
64. Roubaud E (1917) Le venin et l' evolution paralysante chez les hymenoptères predateurs. Bull Biol Fr Belg 51:391-419
65. Rosenberg LA, Libersat F (2002) Wasp venom injected into prey's brain affects the activity of bioaminergic neurons to regulate the expression of specific motor patterns. Neural Plast 9:108
66. Schaefer PL, Kondagunta GV, Ritzmann RE (1994) Motion analysis of escape movements evoked by tactile stimulation in the cockroach, Periplaneta americana. J Exp Biol 190:287-294
67. Schaefer PL, Ritzmann RE (2001) Descending influences on escape behavior and motor pattern in the cockroach. J Neurobiol 5:9-28
68. Silveira R, Siciliano J, Abo V, Viera L, Dajas F (1988) Intrastriatal dendrotoxin injection: behavioral and neurochemical effects. Toxicon 26:1009-1015
69. 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
70. Steiner AL (1986) Stinging behaviour of solitary wasps. In: Piek T (ed) Venoms of the Hymenoptera. Academic Press, London, pp 63-160
71. Stevenson PA, Kutsch W (1987) A reconsideration of the central pattern generator concept for locust flight. J Comp Physiol A 161:115-130
72. 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
73. Strauss R (2002) The central complex and the genetic dissection of locomotor behavior. Curr Opin Neurobiol 120:633-638
74. Tipton KF, Dajas F (1994) Neurotoxins in neurobiology: their actions and applications. Ellis Horwood series in neuroscience. Ellis Horwood, New York
75. Treherne JE, Schofield PK (1979) Ionic homeostasis of the brain microenvironment in insects. Trends Neurosci 2:227-230
76. Van Marle J, Piek T (1986) Morphology of the venom apparatus. In: Piek T (ed) Venoms of the Hymenoptera. Academic Press, London, pp 17-44
77. Weisel-Eichler A, Libersat F (1996) Neuromodulation of flight initiation by octopamine in the cockroach. J Comp Physiol A 179:103-112
78. Weisel-Eichler A, Libersat F (2002) Are monoaminergic systems involved in the lethargy induced by a parasitoid wasp in the cockroach prey? J Comp Physiol A 188:315-324
79. Weisel-Eichler A, Haspel G, Libersat F (1999) Venom of a parasitoid wasp induces prolonged grooming in the cockroach. J Exp Biol 202:957-964
80. Williams FX (1942) Ampulex compressa (Fabr.), a cockroach-hunting wasp introduced from New Caledonia into Hawaii. Proc Haw Entomol Soc 11:221-233
81. Yellman C, Tao HHeB, Hirsh J (1997) Conserved and sexually dimorphic behavioral responses to biogenic amines in decapitated Drosophila. Proc Natl Acad Sci 94:4131-4136
82. Zars T (2002) Behavioral functions of the insect mushroom bodies. Curr Opin Neurobiol 10:790-5