Possible effects of inter-specific competition on the coexistence of two parasitoid species: Trichogramma brassicae Bezdenko and Chelonus oculator (F.) (Hymenoptera: Trichogrammatidae, Braconidae)

Community Ecology

Volumn 12, Issue 1, 2011, Pages 78-88

  Cabello, T ^a   Gamez M ^a   Torres, A ^a   Garay, J ^b  

^a UNIVERSITY OF ALMERÍA   (Spain)

^b EÖTVÖS LORÁND UNIVERSITY   (Hungary)

Author keywords

Extrinsic competition; Functional response; Handling time; Hymenoptera; Idiobiont; Intrinsic competition; Koinobiont; Larvaphogous; Lepidoptera; Mother effects; Oophagous; Parasitoid; Polydnavirus; Wolbachia

Indexed keywords

BACTERIUM; COEXISTENCE; EGG PARASITOID; FUNCTIONAL RESPONSE; INTERSPECIFIC COMPETITION; NUMERICAL MODEL; VIRUS; WASP;

BRACONIDAE; CHELONUS; HEXAPODA; HYMENOPTERA; LEPIDOPTERA; TRICHOGRAMMA BRASSICAE; TRICHOGRAMMATIDAE; WOLBACHIA;

EID: 79958812618     PISSN: 15858553     EISSN: 15882756     Source Type: Journal    
DOI: 10.1556/ComEc.12.2011.1.10     Document Type: Article

References (99)

1. Ables, J.R., Vinson S.B. and Ellis J.S. 1981. Host discrimination by Chelonus insularis, Telenomus Heliothidis, and Trichogramma pretiosum. BioControl 26: 149â156.
2. Alphen, J.J.M. van and Jervis M.A. 1996. Foraging behaviour. In: Jervis, M.A., Kidd, N. (Eds.). Insect Natural Enemies: Practical Approaches to their Study and Evaluation. Chapman & Hall, London, pp. 1â62.
3. Amarasekare, P. 2000. Coexistence of competing parasitoids on a patchily distributed host: local vs. spatial mechanisms. Ecology 81: 1286â1296.
4. Askew, R.R. and Shaw, M.R. 1986. Parasitoid communities: their size, structure and development. In: Waage, J. and Greathead, D. (eds.), Insect Parasitoids. Academic Press. London, pp. 225â264.
5. Baaren, J., Boivin, G. and Nenon, J.P. 1994. Intra- and interspecific host discrimination in two closely related egg parasitoid. Oecologia 100: 325â330.
6. Belda, J., Justicia, L., Pascual, F. and Cabello, T. 1994. Distribuciãn espacial de Spodoptera exigua en cultivo de pimiento en invernadero. Bol. San. Veg. Plagas 20: 287â301.
7. Benoit, M. and Voelege, J. 1979. Choix de lâhote et comportement trophique des larves de Trichogramma evanescens en fonction du dãvelopment embryonnaire de Ephestia kuehniella et Ostrinia nubilali. BioControl 24: 199â207.
8. Berryman, A.A., Stenseth, N.C. and Isaev, A.S. 1987. Natural regulation of herbivorous forest insect populations. Oecologia 71:174â184.
9. Beserra, E.B., Parra, J.R.P. 2005. Impact of the number of Spodoptera frugiperda egg layers on parasitism by Trichogramma atopovirilia. Sci. agric. 62: 190â193.
10. Boivin, G. and Brodeur J. 2006. Intra- and Interspecific interactions among parasitoids: Mechanisms, outcomes and biological control. In: Brodeur, J. and Boivin, G. (eds.), Trophic and Guild in Biological Interactions Control. Springer, Berlin, pp. 123â144.
11. Bonsall, M.B., Hassell, M.P. and Asefa, G. 2002. Ecological tradeoffs, resource partitioning, and coexistence in a host-parasitoid assemblage. Ecology 83: 925â934.
12. Cabello, T. 1985. Biologã-a de dos especies de Trichogramma parasitas de Heliothis spp. en algodonero: posibilidades de su empleo como agentes de control. PhD Diss, Universidad de Cordoba.
13. Cabello, T. 1989. Natural enemies of noctuid pests in alfalfa, corn, cotton and soybean crops in southern Spain. J. Appl. Entomol. 108: 80â88.
14. Cabello, T. and Vargas, P. 1985. Estudio con olfactãmetro de la influencia de la planta y del insecto huãsped en la actividad de bãsqueda de Trichogrmma cordubensis y T. sp.p. buesi. Bol. San. Veg. Plagas 11: 237â241.
15. Cabello, T. and Vargas, P. 1988. Response of Trichogramma cordubensis and T. pintoi to different densities of alternative host eggs. Les Colloques de lâINRA, 9: 165â172.
16. Cabello, T., Gamez, M. and Varga, Z. 2007. An improvement of the Holling type III functional response in entomophagous species model. J. Biol. Syst. 15: 515â524.
17. Cabello, T., Pino, M. del, Torres, A., Lara, L., and Blom, J. van der. 2005. Control biolãgico de Spodoptera exigua en cultivos hortã-colas en invernaderos: crã-a del parasitoide. I Jornadas de Control Biorracional de Plagas. C.S.I.C. Barcelona: 19.
18. Cave, R.D. 2000. Biology, ecology and use in pest management of Telenomus remus. Biocontrol News Inf. 21: 21â26.
19. Chapman, A.V., Kuhar, T.P., Schultz, P.B. and Brewster, C.C. 2009. Dispersal of Trichogramma ostriniae in potato fields. Environ. Entomol. 38: 677â685.
20. Chiri, A.A. and Legner, E.F. 1982. Host-searching kairomones alter behavior of Chelonus sp. nr. curvimaculatus, a hymenopterous parasite of the pink bollworm, Pectinophora gossypiella. Environ. Entomol. 11: 452â455.
21. Chiri, A.A. and Legner, E.F. 1986. Response of three Chelonus species to kairomones in scales of six Lepidoptera. Can. Entomol. 118: 329â333.
22. Clausen, C.P. 1976. Phoresy among entomophagous insects. Annu. Rev. Entomol. 21:343â368.
23. Colazza, S., Peri, E., Salerno, G. and Conti, E. 2010. Host searching by egg parasitoid: Exploitation of host chemical cues. In: Conzoli, F.L, Parra, J.R.P. and Zucchi, R.A. (eds.). Egg parasitoids in agroecosystems with emphasis on Trichogramma. Prog. Biol. Control 9: 149â165.
24. Consoli, F.L., Kitajima, E.W. and Parra, J.R.P. 1999. Ultrastructure of the natural and factitious host eggs of Trichogramma galloi and Trichogramma pretiosum. Int. J. Insect Morphol. Embryol. 28: 211â229.
25. Doutt, R.L. 1984. Caracterã-sticas bio1ãgicas de los adultos entomãfagos. In: DeBach, P. (ed.). Control biolãgico de las plagas de insectos y malas hierbas. C.E.C.S.A., Mãxico, pp. 179â204.
26. Earl, S.L. and Graham, H.M. 1984. Interaction between Chelonus insularis and Telenomus remus, parasitoids of Spodoptera frugiperda. Southwest. Entomol. 9: 326â333.
27. Faria, C.A., Torres, J.B. and Farias, A.F. 2000. Resposta funcional de Trichogramma pretiosum Riley parasitando ovos de Tuta absoluta: Efeito da idade do hospedeiro. An. Soc. Entomol. Bras. 29: 85â93.
28. Fatouros, N.E., Huigens, M.E., Van Loon, J.J.A., Dicke, M., and Hilker, M. 2005. Butterfly anti-aphrodisiac lures parasitic wasps. Nature 433:704.
29. Fatouros, N.E., Dicke, M., Mumm, R., Meiners, T. and Hilker, M. 2008. Foraging behavior of egg parasitoids exploiting chemical information. Behav. Ecol. 19: 677â689
30. Garay, J. and Mori, T.F. 2010. When is predatorâs opportunism remunerative? Community Ecol. 11: 160â170.
31. Garcia-Martin, M., Gamez, M. and Cabello, T. 2005. Estudio de respuesta funcional en sistemas parasitoide-huãsped: aplicaciãn en lucha biolãgica contra plagas. Ed. Universidad de Almeria. Almeria.
32. Garcia-Martin, M., Gãmez, M. and Cabello, T. 2008. Functional response of Chelonus oculator according to temperature. Community Ecol. 9:45â51.
33. Gauld, I. and Bolton, B. 1996. The Hymenoptera. Oxford University Press, Oxford.
34. Godfray, H.C.J. and Mãller, C.B., 1998. Host parasitoid dynamics. In: Dempster, J.P. and McLean, I.F.G. (Eds.). Insect Populations: In Theory and in Practice. Kluwer Academic Publ. Dordrecht, pp. 135â165.
35. Gordh, G., Legner, E.F. and Caltagirone, L.E., 1999. Biology of parasitic Hymenoptera. In: Bellows, T.S., Fisher, T.W., Caltagirone, L.E., Dahlsten, D.L., Gordh, G. and Huffaker, C.B. (Eds.). Handbook of Biological Control: Principles and Applications of Biological Control. Elsevier, Amsterdam, pp. 355â381.
36. Grossniklaus-Bãrgin, C., Pfister-Wilhelm, R., Meyer, V., Treiblmayr, K. and Lanzrein, B. 1998. Physiological and endocrine changes associated with polydnavirus/venom in the parasitoidhost system Chelonus inanitus-Spodoptera littoralis. J. Insect Physiol. 44, 305â321.
37. Hassell, M.P. 1978. Arthropod Predator-prey Systems. Princeton University Press, Princeton.
38. Hawkins, B.A. and Cornell, H.V. 1994. Maximum parasitism rates and successful biological control. Science 266: 1886.
39. Hawkins, B.A., Mills, N.J., Jervis, M.A. and Price, P.W. 1999. Is the biological control of insects a natural phenomenon? Oikos 86: 493â506.
40. Hawlitzky, N. and Boulay, C. 1982. Rãgimes a1imentaires et developement chez Trichogramma maidis dans 1âoeuf dâ Anagasta kuehiniella. Les Trichogrammes. Les Colloques de lâINRA 9: 101â106.
41. Headrick, D.H. and Goeden, R.D. 2001. Biological control as a tool for ecosystem management. Biol. Control 21: 249â257.
42. Hoddle M.S. 2004. Biological control in support of conservation: friend or foe. In: Gordon, M.S. and Bartol, S.M. (eds.). Experimental Approaches to Conservation Biology. Univ. California Press. Berkeley, pp. 202â240
43. Hohmann, C.L., Luck, R.F., Oatman, E.R. and Platner, G.R. 1988. Oviposition behavior of Trichogramma platneri. An. Soc. ent. Bras. 17: 185â195.
44. Houseweart, M.V, Southard, G. and Jennings D.T. 1982. Availability and acceptability of spruce budworm eggs to parasitism by the egg parasitoid, Trichogramma minutum. Entomophaga 25: 95â103.
45. Hunter, M.D. and Price, P.W. 1992. Playing chutes and ladders: heterogeneity and the relative roles of bottom-up and top-down forces in natural communities. Ecology 73: 724â732.
46. Jandel Scientific, 1994. Table Curve 2D-Userâs manual. Version 2.0. Jandel Scientific. San Rafael.
47. Jarjees, E.A. and Merritt D.J. 2002. Development of Trichogramma australicum in Helicoverpa host eggs. Austral. J. Entomol. 41: 310â315.
48. Jarjees, E., Merritt, D.J. and Gordh G. 1998. Anatomy of the mouthparts and digestive tract during feeding in larvae of the parasitoid wasp Trichogramma australicum. Int. J. Insect Morphol. Embryol. 27: 103â110.
49. Jones, D, 1996. Biochemical interaction between Cheloninae wasps and their Lepidopteran hosts: after a decade of research â' the parasite in control. Insect Biochem. Mol. Biol. 26: 981â996.
50. Juliano, S.A. 1982. Influence of host age on host acceptability and suitability for a species of Trichogramma attacking aquatic Diptera. Can. Entomol. 114: 713â720.
51. Kainoh, Y. and Brown, J.J. 1994. Amino acids as oviposition stimulants for the egg-larval parasitoide, Chelonus sp. near curvimaculatus. Biol. Control 4: 22â25.
52. Kaeslin, M., Wehrle, I., Grossniklaus-Burgin, C., Wyler, T., Guggisberg, U., Schittny, J.C. and Lanzrein B. 2005. Stage-dependent strategies of host invasion in the egg-larval parasitoid Chelonus inanitus. J. Insect Physiol. 51: 287â296.
53. Kalyebia, A., Overholtb, W.A., Schulthessa, F., Muekec, J.M., Hassan, S.A. and Sithananthama, S. 2005. Functional response of six indigenous trichogrammatid egg parasitoids in Kenya: influence of temperature and relative humidity. Biol. Control 32: 164â171.
54. Klomp, H. and Teerink, B.J. 1962. Host selection and number of eggs per oviposition in the egg-parasite Trichogramma embryophagum. Nature 195: 1020â1021.
55. Laurenne, N. 2008. Phylogeny of a taxonomically difficult group and evolution of host location mechanism. PhD thesis. Faculty of the Biosciences of the University of Helsinki, Helsinki.
56. Lewis, W., Jones, R.L. and Sparks, A.N. 1972. Ahost-seeking stimulant for the egg parasite, Trichogramma evanescens. Its source and demonstration of its laboratory and field activity. Ann. Entomol. Soc. Am. 65:1087â1089.
57. Lewis, W.J., Nordlund, D.A., Gueldner, R.C., Teal, P.E.A. and Tumlinson, J.H. 1982. Kairomones and their use for management of entomophagous insects. XIII. Kairomonal Activity for Trichogramma spp. of abdominal tips, excretion, and a synthetic sex pheromone blend of Heliothis zea moths. J. Chem. Ecol. 8: 1323â1331.
58. Mackauer, M. 1990. Host discrimination and larval competitions in solitary endoparasitoids. In: Mackauer, M., Ehler, L.E. and Roland, J. (eds.). Critical Issues in Biological Control. Entercept Ltd., Andover, pp. 41â62.
59. Mahmoud, A.M.L. and Lim, U.T. 2008. Host discrimination and interspecific competition of Trissolcus nigripedius and Telenomus gifuensis, sympatric parasitoid of Dolycoris baccarum. Biol. Control 45: 337â343.
60. Makeea, H. 2006. Effect of host egg viability on reproduction and development of Trichogramma cacoeciae and T. principium. Biocontrol Sci. Tech. 16: 195â204.
61. McGregor, R. and Henderson, D. 1998. The influence of oviposition experience on response to host pheromone in Trichogramma sibericum. J. Insect Behav. 11: 621â632.
62. Miller, J.C., 1977. Ecological relationships among parasites of Spodoptera praefica. Environ. Entomol. 6: 581â585.
63. Mills, N. 2006. Interspecific competition among natural enemies and single versus multiple introductions in biological control. In: Brodeur, J. and Boivin, G. (Eds.). Trophic and Guild Interactions in Biological Control. Springer. Dordrecht. pp. 191â220.
64. Mills, N.J. and Lacan, I. 2004. Ratio dependence in the functional response of insect parasitoides: evidence from Trichogramma minutum foraging for eggs in small host patches. Ecol. Entomol. 29: 208â216.
65. Morrison, G. and Lewis, W. J. 1981. The allocation of searching time by Trichogramma pretiosum in host-containing patches. Entomol. Exp. Appl. 30: 31â39.
66. Motulsky, H. and Christopoulos, A. 2003. Fitting Models to Biological Data Using Linear and Nonlinear Regression: A Practical Guide to Curve Fitting. GraphPad Software Inc. San Diego.
67. Nagarkatti, S. and Nagaraja, H. 1977. Biosystematics of Trichogramma and Trichograrnmatoidea species. Annu. Rev. Entomo1. 22: 157â176.
68. Neher, D.A. 1999. Soil community composition and ecosystem processes: comparing agricultural ecosystems with natural ecosystems. Agroforest. Syst. 45: 159â185.
69. Noldus, L.P.J.J., Lenteren, J.C. van and Lewis, W.J. 1991. How Trichogramma parasitoids use moth sex pheromones as kairomones: orientation behaviour in a wind tunnel. Physiol. Entomol. 16: 313â327.
70. Ozder, N. and Saglam, O. 2005. Overwintering of the egg parasitoids Trichogramma brassicae and T. cacoeciae in the Thrace region of Turkey. J. Pest Sci. 78: 129â132.
71. Pak, G.A. and Oatman, E.R. 1982. Biology of Trichogramma brevicapillum. Ent. Exp. App1. 32: 61â67.
72. Pennacchio, F. and Strand, M.R. 2006. Evolution of developmental strategies in parasitic Hymenoptera. Annu. Rev. Entomol. 51: 233â258.
73. Polaszek A. 2010. Species diversity and host associations of Trichogramma in Eurasia. In: Cã nsoli, F.L., Parra, J.R.P. and Zucchi, R.A. (Eds.). Egg Parasitoids in Agroecosystems with Emphasis on Trichogramma. Springer. Dordrecht, pp. 237â266.
74. Quicke, D.L.J., 1997. Parasitic Wasps. Chapman & Hall, London.
75. Reay-Jones, F.P.F., Rochat J., Goebel, R. and Tabone, E. 2006. Functional response of Trichogramma chilonis to Galleria mellonella and Chilo sacchariphagus eggs. Entomol. Exp. Appl. 118: 229â236
76. Rechav, Y. and Orion, T. 1975. The development of the immature stages of Chelonus inanitus. Ann. Entomol. Soc. Am. 68: 457â462.
77. Rodriguez, H., Cabello, T. and Vargas, P. 1988a. Influencia de la dieta en el desarrollo de Ephestia kuehniella. Bol. San. Veg. Plagas 14: 363â369.
78. Rodriguez, H., Cabello, T. and Vargas, P. 1988b. Influencia de la dieta e iluminaciãn en la longevidad, fecundidad y fertilidad de Ephestia kuehniella. Bol. San. Veg. Plagas 14: 561â566.
79. Rosenheim, J.A. 1998. Higher-order predators and the regulation of insect herbivore populations. Annu. Rev. Entomol. 43:421â47.
80. Royer, L., Fournet, S., Brunel, E. and Boivin, G. 1999. Intra- and interspecific host discrimination by host-seeking larvae of coleopteran parasitoids. Oecologia 118:59â68.
81. Scholz, D. and Hãller, C, 1992. Competition for host between two hyperparasitoids of aphids, Dentrocerus laticeps and Dendrocerus carpenter: The benefit of interspecific host discrimination. J. Insect Behav. 5: 289â300.
82. Shaw M.R., 1994. Parasitoid host ranges. In: Hawkins B.A. and Sheenhan W. (Eds.), Parasitoid Community Ecology. Oxford University Press, Oxford, pp. 111â144.
83. Shaw M.R. 2006. Habitat considerations for parasitic wasps (Hymenoptera). J. Insect Conserv. 10: 117â127.
84. Shaw, M.R. and Huddleston, T. 1991. Clasification and biology of Braconid waps. Handbooks for the Identification of British insect, vol. 7, part 11. Royal Entomological Society of London, London.
85. SPSS 2009. Pasw Statistics Base 18. SPSS Inc. Chicago.
86. Strand, M.R. 1986. The physiological interactions of parasitoids with their hosts and their influence on reproductive strategies. In: Waage J. and Greathead D. (eds.). Insect Parasitoid. Academic, London, pp. 97â136.
87. Tobias, V.I., 1975. A Review of the Braconidae (Hymenoptera) of the USSR. Publishing Co. PVT. LTD, New Delhi.
88. Tobias, V.I., 1997. Subfamily Cheloninae. En: Medvedv, G.S. Keys to the Insects of the European Part of the USSR. Vol. III, part IV. Science Publishers Inc. New Delhi, pp. 512â588.
89. Turlings, T.C.J., Baterburg, F.D.H. van and Strien-van Liempt W.T.F.H. van, 1985. Why is there no interspecific host discrimination in the two coexisting larval parasitoid of Drosophila species: Leptopilina heterotoma and Asorbara tabida. Oecologia 67: 352â359.
90. Uka, D., Hiraoka, T. and Iwabuchi K. 2006. Physiological suppression of the larval parasitoid Glyptapantles pallipes by the polyembryonic parasitoid Compidosoma floridanum. J. Insect Physiol. 52: 1137â1142.
91. van Driesche, R.G., Hoddle, M.S. and Center, T.D. 2007. Control de plagas y malezas por enemigos naturales. USDA-USFS, Washington.
92. van Nouhuys, S. and Hanski, I. 2002. Colonization rates and distances of a host butterfly and two specific parasitoids in a fragmented landscape. J. Anim. Ecol. 71: 639â650.
93. Vinson, S.B. 1976. Host selection by insect parasitoide. Annu. Rev. Entomol. 21: 109â133.
94. Vinson, S.B., 1998. The general host selection behavior of parasitoid Hymenoptera and a comparison of initial strategies utilized by larvaphagous and oophagous species. Biol. Control. 11: 79â96.
95. Voegele, J., Brun, P. and Daumal, J. 1974. Les Trichogrammes: 1.-Modalitãs de la prise de possession et de lâãlimination de lâhote chez le parasite embryonnaire Trichogramma brasiliensis. Ann. Soc. Entomol. Fr. 10: 737â761.
96. Volkoff, A.N., Daumal, J., Barry, P., Franãois, M.C., Hawlitzky, N. and Rossi, M.M. 1995. Development of Trichogramma cacoeciae: time table and evidence for a single larval instar. Int. J. Insect Morphol. Embryol. 24: 459â466.
97. Wajnberg, E., Bernstein, C. and van Alphen, J. (Eds.) 2008. Behavioral Ecology of Insect Parasitoids: From Theoretical Approaches to Field Applications. Blackwell, Malden.
98. Wang, B. and Ferro, D.N. 1998. Functional responses of Trichogramma ostriniae to Ostrinia nubilalis under laboratory and field conditions. Environ. Entomol. 27: 752â758.
99. Zwãlfer, H. 1971. The structure and effect of parasite complexes attacking phytophagous host insect. In: Dynamics of populations. Proceedings of the Advanced Study Institute on Dynamics of Numbers in Populations, Oosterbeek, 1970. Centre AgricPubl Document, Wageningen, pp. 405â416.