The role of learning in risk-avoidance strategies during spider-ant interactions

Animal Cognition

Volumn 17, Issue 2, 2014, Pages 185-195

  Hénaut, Yann ^a   Machkour M'Rabet, Salima ^a   Lachaud, Jean Paul ^a,b  

^a EL COLEGIO DE LA FRONTERA SUR   (Mexico)

^b Université Paul Sabatier   (France)

Author keywords

Aversive learning; Evasive strategy; One trial learning; Predation risk; Predatory interaction; Prey avoidance

Indexed keywords

ARANEAE; ARTHROPODA; ECTATOMMA TUBERCULATUM; NEPHILA CLAVIPES;

ANIMAL; ANT; AVOIDANCE BEHAVIOR; FEMALE; PREDATION; RISK; SPIDER;

ANIMALS; ANTS; AVOIDANCE LEARNING; FEMALE; PREDATORY BEHAVIOR; RISK; SPIDERS;

EID: 84893727805     PISSN: 14359448     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10071-013-0651-x     Document Type: Article

References (106)

1. Balfour RA, Buddle CM, Rypstra AL, Walker SE, Marshall SD (2003) Ontogenetic shifts in competitive interactions and intra-guild predation between two wolf spider species. Ecol Entomol 28: 25-30.
2. Berenbaum MR, Miliczky E (1984) Mantids and milkweed bugs: efficacy of aposematic coloration against invertebrate predators. Am Midl Nat 111: 64-68.
3. Bernays EA (1993) Aversion learning and feeding. In: Papaj DR, Lewis AC (eds) Insect learning: ecological and evolutionary perspectives. Chapman and Hall, New York, pp 1-17.
4. Bjorkman-Chiswell BT, Kulinski MM, Muscat RL, Nguyen KA, Norton BA, Symonds MRE, Westhorpe GE, Elgar MA (2004) Web-building spiders attract prey by storing decaying matter. Naturwissenschaften 91: 245-248.
5. Bowdish TI, Bultman TL (1993) Visual cues used by mantids in learning aversion to aposematically colored prey. Am Midl Nat 129: 215-222.
6. Brodie ED III, Brodie ED Jr (1999) Predator-prey arms races: asymmetrical selection on predators and prey may be reduced when prey are dangerous. Bioscience 49: 557-568.
7. Brower JVZ, Brower LP (1965) Experimental studies of mimicry. 8. Further investigation of honeybees (Apis mellifera) and their dronefly mimics (Eristalis spp.). Am Nat 99: 173-187.
8. Burghardt GM, Wilcoxon HC, Czaplicki JA (1973) Conditioning in garter snakes: aversion to palatable prey induced by delayed illness. Anim Learn Behav 1: 317-320.
9. Caro TM (1994) Cheetahs of the Serengeti plains: group living in an asocial species. University of Chicago Press, Chicago.
10. Caro TM, Stoner C (2003) The potential for interspecific competition among African carnivores. Biol Conserv 110: 67-75.
11. Ceballos L, Hénaut Y, Legal L (2005) Foraging strategies of Eriophora edax (Aranae, Araneidae): a nocturnal orb-weaving spider. J Arachnol 33: 509-515.
12. Chameron S, Schatz B, Pastergue-Ruiz I, Beugnon G, Collett TS (1998) The learning of a sequence of visual patterns by the ant Cataglyphis cursor. Proc R Soc Lond B 265: 2309-2313.
13. Crossland MR (2001) Ability of predatory native Australian fishes to learn to avoid toxic larvae of the introduced toad Bufo marinus. J Fish Biol 59: 319-329.
14. Curio E (1976) The ethology of predation. Springer, Berlin.
15. Darmaillacq AS, Dickel L, Chichery MP, Agin V, Chichery R (2004) Rapid taste aversion learning in adult cuttlefish Sepia officinalis. Anim Behav 68: 1291-1298.
16. Davies NB, Krebs JR (1979) Predators and prey. In: Krebs JR, Davies NB (eds) Behavioural ecology: an evolutionary approach. Blackwell Scientific, Oxford, pp 21-151.
17. De Cock R, Matthysen E (2003) Glow-worm larvae bioluminescence (Coleoptera: Lampyridae) operates as an aposematic signal upon toads (Bufo bufo). Behav Ecol 14: 103-108.
18. De la Mora A, Pérez-Lachaud G, Lachaud J-P (2008) Mandible strike: the lethal weapon of Odontomachus opaciventris against small prey. Behav Process 78: 64-75.
19. Dejean A (1988) Memory effect on predatory behaviour of Odontomachus troglodytes (Formicidae-Ponerinae). Behaviour 107: 131-137.
20. Dejean A, Lachaud J-P (1992) Growth-related changes in predation behavior in incipient colonies of the ponerine ant Ectatomma tuberculatum (Olivier). Insect Soc 39: 129143.
21. Dejean A, Corbara B, Oliva-Rivera J (1990) Mise en évidence d'une forme d'apprentissage dans le comportement de capture des proies chez Pachycondyla (= Neoponera) villosa (Formicidae, Ponerinae). Behaviour 115: 175-187.
22. Dejean A, Lachaud J-P, Beugnon G (1993) Efficiency in the exploitation of patchy environments by the ponerine ant Paltothyreus tarsatus: an ecological consequence of the flexibility of prey capture behavior. J Ethol 11: 43-53.
23. Donadio E, Buskirk SW (2006) Diet, morphology, and interspecific killing in carnivora. Am Nat 167: 524-536.
24. Drummond H, Macías Garcia C (1995) Congenital responsiveness of garter snakes to a dangerous prey abolished by learning. Anim Behav 49: 891-900.
25. Eberhard WG (1988) Memory of distances and directions moved as cues during temporary construction in the spider Leucauge mariana (Araneae: Araneidae). J Insect Behav 1: 51-66.
26. Edwards GB, Jackson RR (1994) The role of experience in the development of predatory behaviour in Phidippus regius, a jumping spider (Araneae, Salticidae) from Florida. N Z J Zool 21: 269-277.
27. Eisner T (1965) Defensive spray of a phasmid insect. Science 148: 966-968.
28. Eisner T, Meinwald J (1966) Defensive secretions of arthropods. Science 153: 1341-1350.
29. Estes WK, Skinner BF (1941) Some quantitative properties of anxiety. J Exp Psychol 29: 390-400.
30. Godzinska EJ (1989) Rapid learning of a new prey type in the ants. Abstracts 21st international ethological conference, Utrecht, pp 69.
31. Gosselink TE, van Deelen TR, Joselyn MG, Warner RE (2003) Temporal habitat partitioning and spatial use of coyotes and red foxes in east-central Illinois. J Wildl Manage 67: 90-103.
32. Grober MS (1988) Brittle-star bioluminescence functions as an aposematic signal to deter crustacean predators. Anim Behav 36: 493-501.
33. Gustavson CR, Garcia J, Hankins WG, Rusiniak KW (1974) Coyote predation control by aversive conditioning. Science 184: 581-583.
34. Hadfield JD (2010) MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package. J Stat Softw 33: 1-22.
35. Hall CS (1934) Emotional behavior in the rat. I. Defecation and urination as measures of individual differences in emotionality. J Comp Psychol 18: 385-403.
36. Hasegawa M, Taniguchi Y (1996) Behavioral discrimination of prey with various defense mechanisms by the lizard Eumeces okadae. J Ethol 14: 89-97.
37. Hayward MW, Slotow R (2009) Temporal partitioning of activity in large African carnivores: tests of multiple hypotheses. South Afr J Wildl Res 39: 109-125.
38. Heiling AM, Herberstein ME (1999) The role of experience in web-building spiders (Araneidae). Anim Cogn 2: 171-177.
39. Hénaut Y, Machkour-M'Rabet S (2010) Interspecific aggregation around the web of the orb spider Nephila clavipes: consequences for the web architecture of Leucauge venusta. Ethol Ecol Evol 22: 203-209.
40. Hénaut Y, Alauzet C, Dargagnon D, Lambin M (1999) Visual learning in larval Orius majusculus a polyphagous predator. Entomol Exp Appl 90: 103-107.
41. Hénaut Y, Alauzet C, Ferran A, Williams T (2000) Effect of nymphal diet on adult predation behavior in Orius majusculus (Heteroptera: Anthocoridae). J Econ Entomol 93: 252-255.
42. Hénaut Y, Pablo J, Ibarra-Nuñez G, Williams T (2001) Retention, capture and consumption of experimental prey by orb-web weaving spiders in coffee plantations of Southern Mexico. Entomol Exp Appl 98: 1-8.
43. Hénaut Y, Delme J, Legal L, Williams T (2005) Host selection by a kleptobiotic spider. Naturwissenschaften 92: 95-99.
44. Hénaut Y, Machkour-M'Rabet S, Winterton P, Calmé S (2010) Insect attraction by webs of Nephila clavipes (Araneae: Nephilidae). J Arachnol 38: 135-138.
45. Herberstein ME, Gaskett AC, Glencross D, Hart S, Jeansch S, Elgar MA (2000) Does the presence of potential prey affect web design in Argiope keyserlingi (Araneae, Araneidae)? J Arachnol 28: 346-350.
46. Higgins L (2007) Juveniles Nephila (Araneae, Nephilidae) use various attack strategies for novel prey. J Arachnol 35: 530-534.
47. Hoback WW, Higley LG, Stanley DW (2001) Tigers eating tigers: evidence of intraguild predation operating in an assemblage of tiger beetles. Ecol Entomol 26: 367-375.
48. Hölldobler B (1980) Canopy orientation: a new kind of orientation in ants. Science 210: 86-88.
49. Holway DA, Case TJ (2000) Mechanisms of dispersed central-place foraging in polydomous colonies of the Argentine ant. Anim Behav 59: 433-441.
50. Ibarra-Núñez G, García JA, López JA, Lachaud J-P (2001) Prey analysis in the diet of some ponerine ants (Hymenoptera: Formicidae) and web-building spiders (Araneae) in coffee plantations in Chiapas, Mexico. Sociobiology 37: 723-755.
51. Jackson RR, Li D (2004) One-encounter search-image formation by araneophagic spiders. Anim Cogn 7: 247-254.
52. Jackson RR, Pollard SD (1996) Predatory behavior of jumping spiders. Annu Rev Entomol 41: 287-308.
53. Jackson RR, Pollard S, Cerveira AM (2002a) Opportunistic use of cognitive smokescreens by araneophagic jumping spiders. Anim Cogn 5: 147-157.
54. Jackson RR, Pollard SD, Li D, Fijn N (2002b) Interpopulation variation in the risk-related decisions of Portia labiata, an araneophagic jumping spider (Araneae, Salticidae), during predatory sequences with spitting spiders. Anim Cogn 5: 215-223.
55. Jaffé K, Ramos C, Lagalla C, Parra L (1990) Orientation cues used by ants. Insect Soc 37: 101-115.
56. Janetos AC (1986) Web-site selection: are we asking the right questions? In: Shear WA (ed) Spiders-webs, behavior, and evolution. Stanford University Press, Stanford, pp 9-22.
57. Johnson RA (1991) Learning, memory, and foraging efficiency in two species of desert seed-harvester ants. Ecology 72: 1408-1419.
58. Kamler JF, Ballard WB, Gilliland RL, Lemons PR, Mote K (2003) Impacts of coyotes on swift foxes in northwestern Texas. J Wildl Manage 67: 317-323.
59. Kruse KC, Stone BM (1984) Largemouth bass (Micropterus salmoides) learn to avoid feeding on toad (Bufo) tadpoles. Anim Behav 32: 1035-1039.
60. Lachaud J-P, López Méndez JA, Schatz B, de Carli P, Beugnon G (1996) Comparaison de l'impact de prédation de deux ponérines du genre Ectatomma dans un agroécosystème néotropical. Actes Coll Insect Soc 10: 67-74.
61. Landolfa MA, Barth FG (1996) Vibrations in the orb web of the spider Nephila clavipes: cues for discrimination and orientation. J Comp Physiol A 179: 493-508.
62. Laska M, Metzker K (1998) Food avoidance learning in squirrel monkeys and common marmosets. Learn Mem 5: 193-203.
63. Laurenson MK (1995) Implications of high offspring mortality for cheetah population dynamics. In: Sinclair ARE, Arcese P (eds) Serengeti II: dynamics, management, and conservation of an ecosystem. University of Chicago Press, Chicago, pp 385-399.
64. Linnell JDC, Strand O (2000) Interference interactions, co-existence and conservation of mammalian carnivores. Divers Distrib 6: 169-176.
65. Lowe WC, O'Boyle M (1976) Suppression of cricket killing and eating in laboratory mice following lithium chloride injections. Physiol Behav 17: 427-430.
66. Macquart D, Latil G, Beugnon G (2008) Sensorimotor sequence learning in the ant Gigantiops destructor. Anim Behav 75: 1693-1701.
67. Manton SM, Harding JP (1964) Mandibular mechanisms and the evolution of arthropods. Philos Trans R Soc Lond Ser B Biol Sci 247: 1-183.
68. McGlynn TP, Hoover JR, Jasper GS, Kelly MS, Polis AM, Spangler CM, Watson BJ (2002) Resource heterogeneity affects demography of the Costa Rican ant Aphaenogaster araneoides. J Trop Ecol 18: 231-244.
69. Meyers JJ, Herrel A (2005) Prey capture kinematics of ant-eating lizards. J Exp Biol 208: 113-127.
70. Mitchell BD, Banks PB (2005) Do wild dogs exclude foxes? Evidence for competition from dietary and spatial overlaps. Austral Ecol 30: 581-591.
71. Nicolaus LK, Cassel JF, Carlson RB, Gustavson CR (1983) Taste-aversion conditioning of crows to control predation on eggs. Science 220: 212-214.
72. O'Donnell S (1996) Dragonflies (Gynacantha nervosa Rambur) avoid wasps (Polybia aequatorialis Zavattari and Myschocyttarus sp.) as prey. J Insect Behav 9: 159-162.
73. Okano S, Nagaya H, Inatomi N (2005) Novelty stress increases fecal pellet output in Mongolian gerbils: effects of several drugs. J Pharmacol Sci 98: 411-418.
74. Palomares F, Caro TM (1999) Interspecific killing among mammalian carnivores. Am Nat 153: 492-508.
75. Palomares F, Delibes M (1994) Spatio-temporal ecology and behavior of European genets in southwestern Spain. J Mammal 75: 714-724.
76. Pastergue-Ruiz I, Beugnon G, Lachaud J-P (1995) Can the ant Cataglyphis cursor (Hymenoptera: Formicidae) encode global landmark-landmark relationships in addition to isolated landmark-goal relationships? J Insect Behav 81: 15-132.
77. Pierce CL (1988) Predator avoidance, microhabitat shift, and risk-sensitive foraging in laval dragonflies. Oecologia 77: 81-90.
78. Pietrewicz AT, Kamil AC (1979) Search image formation in the blue jay (Cyanoccitta cristata). Science 204: 1332-1333.
79. Pietrewicz AT, Richards JB (1985) Learning to forage: an ecological perspective. In: Johnston TD, Pietrewicz AT (eds) Issues in the ecological study of learning. Lawrence Eribaum Association Incorporation, London, pp 99-118.
80. Polis GA, McCormick SJ (1987) Intraguild predation and competition among desert scorpions. Ecology 68: 332-343.
81. Polis GA, Myers CA, Holt RD (1989) The ecology and evolution of intraguild predation: potential competitors that eat each other. Annu Rev Ecol Syst 20: 297-330.
82. R Development Core Team (2009) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0. http://www. R-project. org/.
83. Robinson MH (1990) Predator-prey interactions, informational complexity, and the origins of intelligence. In: Evans DL, Schmidt JO (eds) Insect defenses: adaptive mechanisms and strategies of prey and predators. State University of New York Press, Albany, pp 129-150.
84. Roche-Labarbe N, Beugnon G, Lachaud J-P (2004) Apprentissage de routes et orientation spatiale chez un insecte sur un support en 3 dimensions. Actes Coll Insect Soc 16: 52-56.
85. Rodríguez RL, Gamboa E (2000) Memory of captured prey in three web spiders (Araneae, Araneidae, Linyphiidae, Tetragnathidae). Anim Cogn 3: 91-97.
86. Roper TJ, Redston S (1987) Conspicuousness of distasteful prey affects the strength and durability of one-trial avoidance learning. Anim Behav 35: 739-747.
87. Schatz B, Lachaud J-P (2008) Effect of high nest density on spatial relationships in two dominant ectatommine ants (Hymenoptera: Formicidae). Sociobiology 51: 623-643.
88. Schatz B, Beugnon G, Lachaud J-P (1994) Time-place learning by an invertebrate, the ant Ectatomma ruidum Roger. Anim Behav 48: 236-238.
89. Schatz B, Lachaud J-P, Beugnon G (1999) Spatio-temporal learning by the ant Ectatomma ruidum. J Exp Biol 202: 1897-1907.
90. Schmidt JO (1982) Biochemistry of insect venoms. Ann Rev Entomol 27: 339-368.
91. Schultheiss P, Cheng K (2013) Finding food: outbound searching behavior in the Australian desert ant Melophorus bagoti. Behav Ecol 24: 128-135.
92. Sergio F, Hiraldo F (2008) Intraguild predation in raptor assemblages: a review. Ibis 150: 132-145.
93. Skow CD, Jakob EM (2006) Jumping spiders attend to context during learned avoidance of aposematic prey. Behav Ecol 17: 34-40.
94. Snyder WE, Hurd LE (1995) Egg-hatch phenology and intraguild predation between two mantid species. Oecologia 104: 496-500.
95. Spiller DA (1984) Seasonal reversal of competitive advantage between two spider species. Oecologia 64: 322-331.
96. Tillmann JE (2009) An ethological perspective on defecation as an integral part of anti-predatory behaviour in the grey partridge (Perdix perdix L.) at night. J Ethol 27: 117-124.
97. Toft S, Wise DH (1999) Behavioral and ecophysiological responses of a generalist predator to single and mixed species diets of different quality. Oecologia 119: 198-207.
98. Vanak AT (2008) Intraguild interactions between native and domestic carnivores in Central India. Ph. D thesis, Faculty of Graduate School, University of Missouri.
99. Wehner R (2003) Desert ant navigation: how miniature brains solve complex tasks. J Comp Physiol A 189: 579-588.
100. Wehner R, Srinivasan MV (1981) Searching behaviour of desert ants, genus Cataglyphys (Formicidae, Hymenoptera). J Comp Physiol A 142: 315-338.
101. Weiss MR (2006) Defecation behaviour and ecology of insects. Ann Rev Entomol 51: 635-661.
102. Welzl H, D'Alamo P, Lipp HP (2001) Conditioned taste aversion as a learning and memory paradigm. Behav Brain Res 125: 205-213.
103. Whitman DW, Blum MS, Jones CG (1986) Olfactory mediated attack suppression in the southern grasshopper mouse toward an unpalatable prey. Behav Process 13: 77-83.
104. Wissinger S, McGrady J (1993) Intraguild predation and competition between larval dragonflies: direct and indirect effects on shared prey. Ecology 74: 207-218.
105. Zschokke S (1999) Nomenclature of the orb-web. J Arachnol 27: 542-546.
106. Zschokke S, Hénaut Y, Benjamin SP, García-Ballinas JA (2006) Prey-capture strategies in sympatric web-building spiders. Can J Zool 84: 964-973.