Role of visual information and learning in habitat selection by a generalist parasitoid foraging for concealed hosts

Animal Behaviour

Volumn 74, Issue 1, 2007, Pages 131-142

  Segura, Diego F ^a   Viscarret, Mariana M ^a   Carabajal Paladino, Leonela Z ^a   Ovruski, Sergio M ^b   Cladera, Jorge L ^a  

^a INSTITUTO NACIONAL DE TECNOLOGÍA AGROPECUARIA INTA   (Argentina)

^b PLANTA PILOTO DE PROCESOS INDUSTRIALES MICROBIOLÓGICOS PROIMI CONICET   (Argentina)

Author keywords

associative learning; Diachasmimorpha longicaudata; host foraging behaviour; parasitoid wasp; sensitization; visual cues

Indexed keywords

GENERALIST; HABITAT SELECTION; HOST SELECTION; HOST-PARASITOID INTERACTION; LEARNING; PARASITOID; VISUAL CUE; WASP;

DIACHASMIMORPHA LONGICAUDATA;

EID: 34347218258     PISSN: 00033472     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.anbehav.2006.12.005     Document Type: Article

References (81)

1. Aguiar-Menezes E.L., and Menezes E.B. Natural occurrence of parasitoids of Anastrepha spp. Schiner, 1868 (Diptera: Tephritidae) in different host plants, in Itaguai (RJ) Brasil. Biological Control 8 (1997) 1-6 10.1006/bcon.1996.0485
2. van Alphen J.J.M., and Vet L.E.M. An evolutionary approach to host finding and selection. In: Waage J.K., and Greathead D. (Eds). Insect Parasitoids (1986), Academic Press, London 23-61
3. van Alphen J.J.M., Nordlander G., and Eijs I. Host habitat finding and host selection of the Drosophila parasitoid Leptopilina australis (Hymenoptera, Eucoilidae), with a comparison of the niches of European Leptopilina species. Oecologia 87 (1991) 324-329 10.1007/BF00634586
4. Aluja M., Rull J., Sivinski J., Norrbom A.L., Wharton R.A., Macías-Ordóñez R., Díaz-Fleischer F., and López M. Fruit flies of the genus Anastrepha (Diptera: Tephritidae) and associated native parasitoids (Hymenoptera) in the tropical rainforest biosphere reserve of Montes Azules, Chiapas, México. Environmental Entomology 32 (2003) 1377-1385 10.1603/0046-225X(2003)032[1377:FFOTGA]2.0.CO;2
5. Baker M.B. Experience influences settling behaviour in desert isopods, Hemilepistus reaumuri. Animal Behaviour 69 (2005) 1131-1138 10.1016/j.anbehav.2004.07.017
6. Bautista R.C., and Harris E.J. Effect of insectary rearing on host preference and oviposition behaviour of the fruit fly parasitoid Diachasmimorpha longicaudata. Entomologia Experimentalis et Applicata 83 (1997) 213-218 10.1023/A:1002926624071
7. Brown P.E., Frank C.P., Groves H.L., and Anderson M. Spectral sensitivity and visual conditioning in the parasitoid wasp Trybliographa rapae (Hymenoptera: Cynipidae). Bulletin of Entomological Research 88 (1998) 239-245
8. Cancino Díaz J.L., and Yoc M.O. Methods proposed to apply quality control in the mass rearing of Diachasmimorpha longicaudata. In: Nicoli G., Benuzzi M., and Leppla N.C. (Eds). Proceedings of the 7th Workshop of the Global IOBC Working Group: Quality Control of Mass Reared Arthropods (1993), IOBC/OILB, Rimini, Italy 37-47
9. Carrejo N.S., and González R. Parasitoids reared from species of Anastrepha (Diptera: Tephritidae) in Valle de Cauca, Colombia. Florida Entomologist 82 (1999) 113-118
10. Chinajariyawong A., Clarke A.R., Jirasurat M., Kritsaneepiboon S., Lahey H.A., Vijaysegaran S., and Walter G.H. Survey of opiine parasitoids of fruit flies in Thailand and Malaysia. Raffles Bulletin of Zoology 48 (2000) 71-101
11. Cornelius M.L., Duan J.J., and Messing R.H. Visual stimuli and the response of female oriental fruit flies (Diptera: Tephritidae) to fruit-mimicking traps. Journal of Economic Entomology 92 (1999) 121-129
12. Cunningham J.P., Moore C.J., Zalucki M.P., and West S.A. Learning, odour preference and flower foraging in moths. Journal of Experimental Biology 207 (2004) 87-94 10.1242/jeb.00733
13. Dalesman S., Rundle S., Coleman R.A., and Cotton P.A. Cue association and antipredator behaviour in a pulmonate snail, Lymnaea stagnalis. Animal Behaviour 71 (2006) 789-797 10.1016/anbehav.2005.05.028
14. Davis J.M., and Stamps J.A. The effect of natal experience on habitat preferences. Trends in Ecology and Evolution 19 (2004) 411-416 10.1016/j.tree.2004.04.006
15. Dukas R., and Duan J.J. Potential fitness consequences of associative learning in a parasitoid wasp. Behavioral Ecology 11 (2000) 536-543
16. Eben A., Benrey B., Sivinski J., and Aluja M. Host species and host plant effects on performance of Diachasmimorpha longicaudata (Hymenoptera: Braconidae). Environmental Entomology 29 (2000) 87-94 10.1603/0046-225X(2000)029[0087:HSAHPE]2.0.CO;2
17. Fischer S., Samietz J., Wäckers F.L., and Dorn S. Interaction of vibrational and visual cues in parasitoid host location. Journal of Comparative Physiology A 187 (2001) 785-791 10.1007/s00359-001-0249-7
18. Fischer S., Samietz J., Wäckers F.L., and Dorn S. Perception of achromatic cues during host location of a pupal parasitoid. Entomologia Experimentalis et Applicata 106 (2003) 63-66 10.1046/j.1570-7458.2003.00004.x
19. Geervliet J.B.F., Vreugdenhil A.I., Dicke M., and Vet E.M. Learning to discriminate between infochemicals from different plant-host complexes by the parasitoids Cotesia glomerata and C. rubecula. Entomologia Experimentalis et Applicata 86 (1998) 241-252 10.1023/A:1003186706517
20. Godfray H.C.J. Parasitoids Behavioural and Evolutionary Ecology. 1st edn (1994), Princeton University Press, Princeton, New Jersey
21. Greany P.D., Ashley T.S., Baranowski R.M., and Chambers D.L. Rearing and life history studies on Biosteres (Opius) longicaudatus (Hym.: Braconidae). Entomophaga 21 (1976) 207-215
22. Henneman M.L. Maximization of host encounters by parasitoids foraging in the field: females can use a simple rule. Oecologia 116 (1998) 467-474
23. Hernández-Ortíz V., Perez-Alonso R., and Wharton R.A. Native parasitoids associated with the genus Anastrepha (Dip.: Tephritidae) in Los Tuxtlas, Veracruz, Mexico. Entomophaga 39 (1994) 171-178 10.1007/BF02372355
24. Hoffmeister T.S., Lachlan R.F., and Roitberg B.D. Do larger fruits provide a partial refuge for rose-hipe flies against parasitoids?. Journal of Insect Behavior 12 (1999) 451-460 10.1023/A:1020906521745
25. Iizuka T., and Takasu K. Olfactory associative learning of the pupal parasitoid Pimpla luctuosa Smith (Hymenoptera: Ichneumonidae). Journal of Insect Behavior 11 (1998) 743-760 10.1023/A:1022355127628
26. Jang E.B., Messing R.H., Klungness L.M., and Carvalho L.A. Flight tunnel response of Diachasmimorpha longicaudata (Ashmead) (Hymenoptera: Braconidae) to olfactory and visual stimuli. Journal of Insect Behavior 13 (2000) 525-538 10.1023/A:1007811602140
27. de Jong R., and Kaiser L. Odor learning by Leptopilina boulardi, a specialist parasitoid (Hymenoptera: Eucoilidae). Journal of Insect Behavior 4 (1991) 743-750 10.1007/BF01052228
28. Kaiser L., Pérez-Maluf R., Sandoz J.C., and Pham-Delégue M.H. Dynamics of odour learning in Leptopilina boulardi, a hymenopterous parasitoid. Animal Behaviour 66 (2003) 1077-1084 10.1006/anbe.2003.2302
29. Keasar T., Ney-Nifle M., Mantel M., and Swezey S. Early oviposition experience affects patch residence time in a foraging parasitoid. Entomologia Experimentalis et Applicata 98 (2001) 123-132 10.1023/A:1018770802124
30. Law E., Nuttley W.M., and van der Kooy D. Contextual taste cues modulate olfactory learning in C. elegans by an occasion-setting mechanism. Current Biology 14 (2004) 1303-1308 10.1016/j.cub.2004.06.066
31. Lawrence P.O. Host vibration: a cue to host location by the parasite, Biosteres longicaudatus. Oecologia 48 (1981) 249-251 10.1007/BF00347971
32. Lecomte C., and Thibout E. Pre- and post-imaginal experience in a specialist parasitoid Diadromus pulchellus (Hym.: Ichneumonidae). BioControl 38 (1993) 175-184 10.1007/BF02372551
33. Leyva J.L., Browning H.W., and Gilstrap F.E. Effect of host fruit species, size, and colour on parasitization of Anastrepha ludens (Diptera: Tephritidae) by Diachasmimorpha longicaudata (Hymenoptera: Braconidae). Environmental Entomology 20 (1991) 1469-1474
34. Lobdell C.E., Tze-Hei Y., and Hoffmann M.P. Host color preferences and short-range searching behaviour of the egg parasitoid Trichogramma ostriniae. Entomologia Experimentalis et Applicata 116 (2005) 127-134 10.1111/j.1570-7458.2005.00306.x
35. López M., Aluja M., and Sivinski J. Hymenopterous larval-pupal and pupal parasitoids of Anastrepha flies (Diptera: Tephritidae) in Mexico. Biological Control 15 (1999) 119-129 10.1006/bcon.1999.0711
36. McGregor R., and Henderson D. The influence of oviposition experience on response to host pheromone in Trichogramma sibericum (Hymenoptera: Trichogrammatidae). Journal of Insect Behavior 11 (1998) 621-632 10.1023/A:1022390608064
37. Mahometa M.J., and Domjan M. Classical conditioning increases reproductive success in Japanese quail, Coturnix japonica. Animal Behaviour 69 (2005) 983-989 10.1016/j.anbehav.2004.06.023
38. Menzel R. Associative learning in honey bees. Apidologie 24 (1993) 157-168
39. Menzel R., and Bitterman M.E. Learning by honeybees in an unnatural situation. In: Huber F., and Marka H. (Eds). Neuroethology and Behavioral Physiology (1983), Springer-Verlag, New York 206-215
40. Messing R.H., and Jang E.B. Response of the fruit fly parasitoid Diachasmimorpha longicaudata (Hymenoptera: Braconidae) to host-fruit stimuli. Environmental Entomology 21 (1992) 1189-1195
41. Michaud J.P., and Mackauer M. The use of visual cues in host evaluation by aphidiid wasps I. Comparison between three Aphidius parasitoids of the pea aphid. Entomologia Experimentalis et Applicata 70 (1994) 273-283 10.1007/BF02380561
42. Montoya P., Benrey B., Barrera J.F., Zenil M., Ruiz L., and Liedo P. Oviposition behaviour and conspecific host discrimination in Diachasmimorpha longicaudata (Hymenoptera: Braconidae), a fruit fly parasitoid. Biocontrol Science and Technology 13 (2003) 683-690 10.1080/09583150310001606273
43. Mumm R., Tiemann T., Varama M., and Hilker M. Choosy egg parasitoids: specificity of oviposition-induced pine volatiles exploited by an egg parasitoid of pine sawflies. Entomologia Experimentalis et Applicata 115 (2005) 217-225 10.1111/j.1570-7458.2005.00262.x
44. Nuttley W.M., Atkinson-Leadbeater K.P., and van der Kooy D. Serotonin mediates food-odor associative learning in the nematode Caenorhabditis elegans. Proceedings of the National Academy of Sciences, U.S.A. 99 (2002) 12449-12454 10.1073/pnas.192101699
45. Oliai S.E., and King B.H. Associative learning in response to colour in the parasitoid wasp Nasonia vitripennis (Hymenoptera: Pteromalidae). Journal of Insect Behavior 13 (2000) 55-69 10.1023/A:1007763525685
46. Olson D.M., Hodges T.A., and Lewis W.J. Foraging efficacy of a larval parasitoid in a cotton patch: influence of chemical cues and learning. Journal of Insect Behavior 16 (2003) 613-624 10.1023/B:JOIR.0000007699.31659.14
47. Ovruski S.M., Colin C., Soria A., Oroño L., and Schliserman P. Introducción y establecimiento en laboratorio de Diachasmimorpha tryoni y Diachasmimorpha longicaudata Hymenoptera: Braconidae, Opiinae) para el control biológico de Ceratitis capitata (Diptera: Tephritidae, Dacinae) en la Argentina. Revista de la Sociedad Entomológica Argentina 62 (2003) 49-59
48. Ovruski S.M., Schliserman P., and Aluja M. Indigenous parasitoids (Hymenoptera) attacking Anastrepha fraterculus and Ceratitis capitata (Diptera: Tephritidae) in native and exotic host plants in Northwestern Argentina. Biological Control 29 (2004) 43-57 10.1016/S1049-9644(03)00127-0
49. Ovruski S.M., Wharton R.A., Schliserman P., and Aluja M. Abundance of Anastrepha fraterculus (Diptera: Tephritidae) and its associated native parasitoids (Hymenoptera) in 'feral' guavas growing in the endangered northernmost Yungas forest of Argentina with an update on the taxonomic status of opiine parasitoids previously reported in this country. Environmental Entomology 34 (2005) 807-818 10.1603/0046-225X(2005)034[0807:AOAFDT]2.0.CO;2
50. Papaj D.R. Conditioning of leaf-shape discrimination by chemical cues in the butterfly, Battus philenor. Animal Behaviour 34 (1986) 1281-1288
51. Papaj D.R., and Prokopy R.J. Ecological and evolutionary aspects of learning in phytophagous insects. Annual Review of Entomology 34 (1989) 315-350 10.1146/annurev.en.34.010189.001531
52. Parmesan C., Singer M.C., and Harris I. Absence of adaptive learning from the oviposition foraging behaviour of a checkerspot butterfly. Animal Behaviour 50 (1995) 161-175
53. Peitsch D., Fietz A., Hertel H., de Souza J., Ventura D.F., and Menzel R. The spectral input systems of hymenopteran insects and their receptor-based colour vision. Journal of Comparative Physiology A 170 (1992) 23-40 10.1007/BF00190398
54. Poolman Simons M.T.T., Suverkropp B.P., Vet L.E.M., and de Moed G. Comparison of learning in related generalist and specialist eucoilid parasitoids. Entomologia Experimentalis et Applicata 64 (1992) 117-124 10.1007/BF00162984
55. Rolstad J., Loken B., and Rolstad E. Habitat selection as a hierarchical spatial process: the green woodpecker at the northern edge of its distribution range. Oecologia 124 (2000) 116-129 10.1007/s004420050031
56. Sato M., and Takasu K. Food odor learning by both sexes of the pupal parasitoid Pimpla alboannulatus Uchida (Hymenoptera: Ichneumonidae). Journal of Insect Behavior 13 (2000) 263-272 10.1023/A:1007796400186
57. Shafir S. Color discrimination of the wasp, Polybia occidentalis (Hymenoptera: Vespidae). Biotropica 28 (1996) 243-251 10.2307/2389078
58. Sivinski J. The influence of host fruit morphology on parasitization rates in the Caribbean fruit fly, Anastrepha suspensa. Entomophaga 36 (1991) 447-454 10.1007/BF02377951
59. Sivinski J., Aluja M., and López M. The spatial and temporal distributions of parasitoids of Mexican Anastrepha species (Diptera: Tephritidae) within the canopies of fruit trees. Annals of the Entomological Society of America 90 (1997) 604-618
60. Sivinski J., Piñero J., and Aluja M. The distributions of parasitoids (Hymenoptera) of Anastrepha fruit flies (Diptera: Tephritidae) along an altitudinal gradient in Veracruz, Mexico. Biological Control 18 (2000) 258-269 10.1006/bcon.2000.0836
61. Sivinski J., Vulinec K., and Aluja M. Ovipositor length in a guild of parasitoids (Hymenoptera: Braconidae) attacking Anastrepha spp. fruit flies (Diptera: Tephritidae) in southern Mexico. Annals of the Entomological Society of America 94 (2001) 886-895 10.1603/0013-8746(2001)094[0886:OLIAGO]2.0.CO;2
62. Steidle J.M.L. Learning pays off: influence of experience on host finding and parasitism in Lariophagus distinguendus. Ecological Entomology 23 (1998) 451-456 10.1046/j.1365-2311.1998.00144.x
63. Stephens D.W. Learning and behavioral ecology: incomplete information and environmental predictability. In: Papaj D.R., and Lewis A.C. (Eds). Insect Learning: Ecological and Evolutionary Perspectives (1993), Chapman & Hall, New York 195-218
64. Stireman III J.O. Learning in the generalist tachinid parasitoid Exorista mella Walker (Diptera: Tachinidae). Journal of Insect Behavior 15 (2002) 689-706 10.1023/A:1020752024329
65. Turlings T.C.J., Wäckers F.L., Vet L.E.M., Lewis W.J., and Tumlinson J.H. Learning of host-finding cues by hymenopterous parasitoids. In: Papaj D.R., and Lewis A.C. (Eds). Insect Learning: Ecological and Evolutionary Perspectives (1993), Chapman & Hall, New York 51-78
66. Vargas R.I., Stark J.D., Prokopy R.J., and Green T.A. Response of oriental fruit fly (Diptera: Tephritidae) and associated parasitoids (Hymenoptera: Braconidae) to different-colour spheres. Journal of Economic Entomology 84 (1991) 1503-1507
67. Vet L.E.M., and Dicke M. Ecology of infochemical use by natural enemies in a tritrophic context. Annual Review of Entomology 37 (1992) 141-172 10.1146/annurev.en.37.010192.001041
68. Vet L.E.M., de Jong A.G., Franchi E., and Papaj D.R. The effect of complete versus incomplete information on odour discrimination in a parasitic wasp. Animal Behaviour 55 (1998) 1271-1279
69. Vijaysegaran S. The occurrence of oriental fruit fly on starfruit in Serdang and the status of its parasitoids. Journal of Plant Protection in the Tropics 1 (1984) 93-98
70. Vinson S.B. How parasitoids locate their hosts: a case of insect espionage. In: Lewis T. (Ed). Insect Communication (1984), Academic Press, London 325-348
71. Vinson S.B. The general host selection behavior of parasitoid Hymenoptera and a comparison of initial strategies utilized by larvaphagous and oophagous species. Biological Control 11 (1998) 79-96
72. Wäckers F.L., and Lewis W.J. Olfactory and visual learning and their combined influence on host site location by the parasitoid Microplitis croceipes (Cresson). Biological Control 4 (1994) 105-112 10.1006/bcon.1994.1018
73. Wäckers F.L., and Lewis W.J. A comparison of colour-, shape- and pattern-learning by the hymenopteran parasitoid Microplitis croceipes. Journal of Comparative Physiology A 184 (1999) 387-393 10.1007/s003590050337
74. Wardle A.R. Learning of host microhabitat colour by Exeristes roborator (F.) (Hymenoptera: Ichneumonidae). Animal Behaviour 39 (1990) 914-923
75. Wardle A.R., and Borden J.H. Learning of an olfactory stimulus associated with a host microhabitat by Exeristes roborator. Entomologia Experimentalis et Applicata 52 (1989) 271-279 10.1007/BF00414053
76. Wardle A.R., and Borden J.H. Learning of host microhabitat form by Exeristes roborator (F.) (Hymenoptera: Ichneumonidae). Journal of Insect Behavior 3 (1990) 251-263 10.1007/BF01417916
77. Wharton R.A., and Gilstrap F.E. Key to and status of Opiinae braconid (Hymenoptera) parasitoids used in biological control of Ceratitis and Dacus S.L. (Diptera: Tephritidae). Annals of the Entomological Society of America 76 (1983) 721-742
78. Weiss M.R., and Papaj D.R. Colour learning in two behavioural contexts: how much can a butterfly keep in mind?. Animal Behaviour 65 (2003) 425-434 10.1006/anbe.2003.2084
79. Wund M.A. Learning and the development of habitat-specific bat echolocation. Animal Behaviour 70 (2005) 441-450 10.1016/j.anbehav.2004.11.009
80. Zanen P.O., and Cardé R.T. Learning and the role of host-specific volatiles during in-flight host-finding in the specialist parasitoid Microplitis croceipes. Royal Entomological Society of London 16 (1991) 381-389
81. Zar J.H. Biostatistical Analysis. 3rd edn (1996), Prentice Hall, Upper Saddle River, New Jersey