View More View Less
  • 1 Almeria University Center for Agribusiness Biotechnology Research Ctra. Sacramento s/n ES-04120 Almeria Spain
  • 2 L. Eötvös University Research Group of Theoretical Biology and Ecology, Hungarian Academy of Sciences and Department of Plant Taxonomy and Ecology Pázmány Péter sétány1/c H-1117 Budapest Hungary
Restricted access

Insect parasitoids have been widely studied, particularly due to their ecological implications through the study of the special relationships observed among this kind of species, as well as to their expression in mathematical models. However, there are still scarce studies on parasitoid relationships and their expression in more realistic mathematical models. The present work is aimed at deepening into competition relationships among parasitoids. Bearing this purpose in mind, the system shaped by two parasitoids was chosen: Trichogramma brassicae (idiobiont egg parasitoid) and Chelonus oculator (koinobiont egg-larval parasitoid). Both species compete against each other for the same host species (Lepidoptera). The results obtained in the laboratory point out that T. brassicae may be considered a better competitor than Ch. oculator. This is the result of the extrinsic competition due to the substances injected by the female during parasitization. However, our results show this classification into better and worse competitors inaccurate. Thus, these interspecific competition influences are detrimental to both parasitoid species. This is the first time that the effect of this competition is mentioned regarding parasitoid functional response. Our results and their ecological implications are reported and discussed.

  • Ables, J.R., Vinson S.B. and Ellis J.S. 1981. Host discrimination by Chelonus insularis, Telenomus Heliothidis, and Trichogramma pretiosum. BioControl 26: 149–156.

    Ellis J.S. , 'Host discrimination by Chelonus insularis, Telenomus Heliothidis, and Trichogramma pretiosum ' (1981 ) 26 BioControl : 149 -156.

    • Search Google Scholar
  • 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. 1–62.

    Jervis M.A. , '', in Insect Natural Enemies: Practical Approaches to their Study and Evaluation , (1996 ) -.

  • Amarasekare, P. 2000. Coexistence of competing parasitoids on a patchily distributed host: local vs. spatial mechanisms. Ecology 81: 1286–1296.

    Amarasekare P. , 'Coexistence of competing parasitoids on a patchily distributed host: local vs. spatial mechanisms ' (2000 ) 81 Ecology : 1286 -1296.

    • Search Google Scholar
  • 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. 225–264.

    Shaw M.R. , '', in Insect Parasitoids , (1986 ) -.

  • Baaren, J., Boivin, G. and Nenon, J.P. 1994. Intra- and interspecific host discrimination in two closely related egg parasitoid. Oecologia 100: 325–330.

    Nenon J.P. , 'Intra- and interspecific host discrimination in two closely related egg parasitoid ' (1994 ) 100 Oecologia : 325 -330.

    • Search Google Scholar
  • Belda, J., Justicia, L., Pascual, F. and Cabello, T. 1994. Distribución espacial de Spodoptera exigua en cultivo de pimiento en invernadero. Bol. San. Veg. Plagas 20: 287–301.

    Cabello T. , 'Distribución espacial de Spodoptera exigua en cultivo de pimiento en invernadero ' (1994 ) 20 Bol. San. Veg. Plagas : 287 -301.

    • Search Google Scholar
  • Benoit, M. and Voelege, J. 1979. Choix de l’hote et comportement trophique des larves de Trichogramma evanescens en fonction du dévelopment embryonnaire de Ephestia kuehniella et Ostrinia nubilali. BioControl 24: 199–207.

    Voelege J. , 'Choix de l’hote et comportement trophique des larves de Trichogramma evanescens en fonction du dévelopment embryonnaire de Ephestia kuehniella et Ostrinia nubilali ' (1979 ) 24 BioControl : 199 -207.

    • Search Google Scholar
  • Berryman, A.A., Stenseth, N.C. and Isaev, A.S. 1987. Natural regulation of herbivorous forest insect populations. Oecologia 71:174–184.

    Isaev A.S. , 'Natural regulation of herbivorous forest insect populations ' (1987 ) 71 Oecologia : 174 -184.

    • Search Google Scholar
  • 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: 190–193.

    Parra J.R.P. , 'Impact of the number of Spodoptera frugiperda egg layers on parasitism by Trichogramma atopovirilia ' (2005 ) 62 Sci. agric. : 190 -193.

    • Search Google Scholar
  • 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. 123–144.

    Brodeur J. , '', in Trophic and Guild in Biological Interactions Control , (2006 ) -.

  • Bonsall, M.B., Hassell, M.P. and Asefa, G. 2002. Ecological tradeoffs, resource partitioning, and coexistence in a host-parasitoid assemblage. Ecology 83: 925–934.

    Asefa G. , 'Ecological tradeoffs, resource partitioning, and coexistence in a host-parasitoid assemblage ' (2002 ) 83 Ecology : 925 -934.

    • Search Google Scholar
  • Cabello, T. 1985. Biología de dos especies de Trichogramma parasitas de Heliothis spp. en algodonero: posibilidades de su empleo como agentes de control. PhD Diss, Universidad de Cordoba.

  • Cabello, T. 1989. Natural enemies of noctuid pests in alfalfa, corn, cotton and soybean crops in southern Spain. J. Appl. Entomol. 108: 80–88.

    Cabello T. , 'Natural enemies of noctuid pests in alfalfa, corn, cotton and soybean crops in southern Spain ' (1989 ) 108 J. Appl. Entomol. : 80 -88.

    • Search Google Scholar
  • Cabello, T. and Vargas, P. 1985. Estudio con olfactómetro de la influencia de la planta y del insecto huésped en la actividad de búsqueda de Trichogrmma cordubensis y T. sp.p. buesi. Bol. San. Veg. Plagas 11: 237–241.

    Vargas P. , 'Estudio con olfactómetro de la influencia de la planta y del insecto huésped en la actividad de búsqueda de Trichogrmma cordubensis y T. sp.p. buesi ' (1985 ) 11 Bol. San. Veg. Plagas : 237 -241.

    • Search Google Scholar
  • Cabello, T. and Vargas, P. 1988. Response of Trichogramma cordubensis and T. pintoi to different densities of alternative host eggs. Les Colloques de l’INRA, 9: 165–172.

    Vargas P. , 'Response of Trichogramma cordubensis and T. pintoi to different densities of alternative host eggs ' (1988 ) 9 Les Colloques de l’INRA : 165 -172.

    • Search Google Scholar
  • 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: 515–524.

    Varga Z. , 'An improvement of the Holling type III functional response in entomophagous species model ' (2007 ) 15 J. Biol. Syst. : 515 -524.

    • Search Google Scholar
  • Cabello, T., Pino, M. del, Torres, A., Lara, L., and Blom, J. van der. 2005. Control biológico de Spodoptera exigua en cultivos hortícolas en invernaderos: cría del parasitoide. I Jornadas de Control Biorracional de Plagas. C.S.I.C. Barcelona: 19.

  • Cave, R.D. 2000. Biology, ecology and use in pest management of Telenomus remus. Biocontrol News Inf. 21: 21–26.

    Cave R.D. , 'Biology, ecology and use in pest management of Telenomus remus ' (2000 ) 21 Biocontrol News Inf. : 21 -26.

    • Search Google Scholar
  • Chapman, A.V., Kuhar, T.P., Schultz, P.B. and Brewster, C.C. 2009. Dispersal of Trichogramma ostriniae in potato fields. Environ. Entomol. 38: 677–685.

    Brewster C.C. , 'Dispersal of Trichogramma ostriniae in potato fields ' (2009 ) 38 Environ. Entomol. : 677 -685.

    • Search Google Scholar
  • 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: 452–455.

    Legner E.F. , 'Host-searching kairomones alter behavior of Chelonus sp. nr. curvimaculatus, a hymenopterous parasite of the pink bollworm, Pectinophora gossypiella ' (1982 ) 11 Environ. Entomol. : 452 -455.

    • Search Google Scholar
  • Chiri, A.A. and Legner, E.F. 1986. Response of three Chelonus species to kairomones in scales of six Lepidoptera. Can. Entomol. 118: 329–333.

    Legner E.F. , 'Response of three Chelonus species to kairomones in scales of six Lepidoptera ' (1986 ) 118 Can. Entomol. : 329 -333.

    • Search Google Scholar
  • Clausen, C.P. 1976. Phoresy among entomophagous insects. Annu. Rev. Entomol. 21:343–368.

    Clausen C.P. , 'Phoresy among entomophagous insects ' (1976 ) 21 Annu. Rev. Entomol. : 343 -368.

    • Search Google Scholar
  • 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: 149–165.

  • 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: 211–229.

    Parra J.R.P. , 'Ultrastructure of the natural and factitious host eggs of Trichogramma galloi and Trichogramma pretiosum ' (1999 ) 28 Int. J. Insect Morphol. Embryol. : 211 -229.

    • Search Google Scholar
  • Doutt, R.L. 1984. Características bio1ógicas de los adultos entomófagos. In: DeBach, P. (ed.). Control biológico de las plagas de insectos y malas hierbas. C.E.C.S.A., México, pp. 179–204.

    Doutt R.L. , '', in Control biológico de las plagas de insectos y malas hierbas , (1984 ) -.

  • Earl, S.L. and Graham, H.M. 1984. Interaction between Chelonus insularis and Telenomus remus, parasitoids of Spodoptera frugiperda. Southwest. Entomol. 9: 326–333.

    Graham H.M. , 'Interaction between Chelonus insularis and Telenomus remus, parasitoids of Spodoptera frugiperda ' (1984 ) 9 Southwest. Entomol. : 326 -333.

    • Search Google Scholar
  • 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: 85–93.

    Farias A.F. , 'Resposta funcional de Trichogramma pretiosum Riley parasitando ovos de Tuta absoluta: Efeito da idade do hospedeiro ' (2000 ) 29 An. Soc. Entomol. Bras. : 85 -93.

    • Search Google Scholar
  • 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.

    Hilker M. , 'Butterfly anti-aphrodisiac lures parasitic wasps ' (2005 ) 433 Nature : 704 -.

  • Fatouros, N.E., Dicke, M., Mumm, R., Meiners, T. and Hilker, M. 2008. Foraging behavior of egg parasitoids exploiting chemical information. Behav. Ecol. 19: 677–689

    Hilker M. , 'Foraging behavior of egg parasitoids exploiting chemical information ' (2008 ) 19 Behav. Ecol. : 677 -689.

    • Search Google Scholar
  • Garay, J. and Mori, T.F. 2010. When is predator’s opportunism remunerative? Community Ecol. 11: 160–170.

    Mori T.F. , 'When is predator’s opportunism remunerative? ' (2010 ) 11 Community Ecol. : 160 -170.

    • Search Google Scholar
  • Garcia-Martin, M., Gamez, M. and Cabello, T. 2005. Estudio de respuesta funcional en sistemas parasitoide-huésped: aplicación en lucha biológica contra plagas. Ed. Universidad de Almeria. Almeria.

    Cabello T. , '', in Estudio de respuesta funcional en sistemas parasitoide-huésped: aplicación en lucha biológica contra plagas , (2005 ) -.

  • Garcia-Martin, M., Gámez, M. and Cabello, T. 2008. Functional response of Chelonus oculator according to temperature. Community Ecol. 9:45–51.

    Cabello T. , 'Functional response of Chelonus oculator according to temperature ' (2008 ) 9 Community Ecol. : 45 -51.

    • Search Google Scholar
  • Gauld, I. and Bolton, B. 1996. The Hymenoptera. Oxford University Press, Oxford.

    Bolton B. , '', in The Hymenoptera , (1996 ) -.

  • Godfray, H.C.J. and Müller, 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. 135–165.

  • 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. 355–381.

    Caltagirone L.E. , '', in Handbook of Biological Control: Principles and Applications of Biological Control , (1999 ) -.

  • Grossniklaus-Bürgin, 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, 305–321.

    Lanzrein B. , 'Physiological and endocrine changes associated with polydnavirus/venom in the parasitoidhost system Chelonus inanitus-Spodoptera littoralis ' (1998 ) 44 J. Insect Physiol. : 305 -321.

    • Search Google Scholar
  • Hassell, M.P. 1978. Arthropod Predator-prey Systems. Princeton University Press, Princeton.

    Hassell M.P. , '', in Arthropod Predator-prey Systems , (1978 ) -.

  • Hawkins, B.A. and Cornell, H.V. 1994. Maximum parasitism rates and successful biological control. Science 266: 1886.

    Cornell H.V. , 'Maximum parasitism rates and successful biological control ' (1994 ) 266 Science : 1886 -.

    • Search Google Scholar
  • 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: 493–506.

    Price P.W. , 'Is the biological control of insects a natural phenomenon? ' (1999 ) 86 Oikos : 493 -506.

    • Search Google Scholar
  • Hawlitzky, N. and Boulay, C. 1982. Régimes a1imentaires et developement chez Trichogramma maidis dans 1’oeuf d’ Anagasta kuehiniella. Les Trichogrammes. Les Colloques de l’INRA 9: 101–106.

    Boulay C. , 'Régimes a1imentaires et developement chez Trichogramma maidis dans 1’oeuf d’ Anagasta kuehiniella. Les Trichogrammes ' (1982 ) 9 Les Colloques de l’INRA : 101 -106.

    • Search Google Scholar
  • Headrick, D.H. and Goeden, R.D. 2001. Biological control as a tool for ecosystem management. Biol. Control 21: 249–257.

    Goeden R.D. , 'Biological control as a tool for ecosystem management ' (2001 ) 21 Biol. Control : 249 -257.

    • Search Google Scholar
  • 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. 202–240

    Hoddle M.S. , '', in Experimental Approaches to Conservation Biology , (2004 ) -.

  • Hohmann, C.L., Luck, R.F., Oatman, E.R. and Platner, G.R. 1988. Oviposition behavior of Trichogramma platneri. An. Soc. ent. Bras. 17: 185–195.

    Platner G.R. , 'Oviposition behavior of Trichogramma platneri ' (1988 ) 17 An. Soc. ent. Bras. : 185 -195.

    • Search Google Scholar
  • 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: 95–103.

    Jennings D.T. , 'Availability and acceptability of spruce budworm eggs to parasitism by the egg parasitoid, Trichogramma minutum ' (1982 ) 25 Entomophaga : 95 -103.

    • Search Google Scholar
  • 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: 724–732.

    Price P.W. , 'Playing chutes and ladders: heterogeneity and the relative roles of bottom-up and top-down forces in natural communities ' (1992 ) 73 Ecology : 724 -732.

    • Search Google Scholar
  • Jandel Scientific, 1994. Table Curve 2D-User’s manual. Version 2.0. Jandel Scientific. San Rafael.

    '', in Table Curve 2D-User’s manual. Version 2.0 , (1994 ) -.

  • Jarjees, E.A. and Merritt D.J. 2002. Development of Trichogramma australicum in Helicoverpa host eggs. Austral. J. Entomol. 41: 310–315.

    Merritt D.J. , 'Development of Trichogramma australicum in Helicoverpa host eggs ' (2002 ) 41 Austral. J. Entomol. : 310 -315.

    • Search Google Scholar
  • 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: 103–110.

    Gordh G. , 'Anatomy of the mouthparts and digestive tract during feeding in larvae of the parasitoid wasp Trichogramma australicum ' (1998 ) 27 Int. J. Insect Morphol. Embryol. : 103 -110.

    • Search Google Scholar
  • Jones, D, 1996. Biochemical interaction between Cheloninae wasps and their Lepidopteran hosts: after a decade of research — the parasite in control. Insect Biochem. Mol. Biol. 26: 981–996.

    Jones D. , 'Biochemical interaction between Cheloninae wasps and their Lepidopteran hosts: after a decade of research — the parasite in control ' (1996 ) 26 Insect Biochem. Mol. Biol. : 981 -996.

    • Search Google Scholar
  • Juliano, S.A. 1982. Influence of host age on host acceptability and suitability for a species of Trichogramma attacking aquatic Diptera. Can. Entomol. 114: 713–720.

    Juliano S.A. , 'Influence of host age on host acceptability and suitability for a species of Trichogramma attacking aquatic Diptera ' (1982 ) 114 Can. Entomol. : 713 -720.

    • Search Google Scholar
  • Kainoh, Y. and Brown, J.J. 1994. Amino acids as oviposition stimulants for the egg-larval parasitoide, Chelonus sp. near curvimaculatus. Biol. Control 4: 22–25.

    Brown J.J. , 'Amino acids as oviposition stimulants for the egg-larval parasitoide, Chelonus sp. near curvimaculatus ' (1994 ) 4 Biol. Control : 22 -25.

    • Search Google Scholar
  • 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: 287–296.

    Lanzrein B. , 'Stage-dependent strategies of host invasion in the egg-larval parasitoid Chelonus inanitus ' (2005 ) 51 J. Insect Physiol. : 287 -296.

    • Search Google Scholar
  • 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: 164–171.

    Sithananthama S. , 'Functional response of six indigenous trichogrammatid egg parasitoids in Kenya: influence of temperature and relative humidity ' (2005 ) 32 Biol. Control : 164 -171.

    • Search Google Scholar
  • Klomp, H. and Teerink, B.J. 1962. Host selection and number of eggs per oviposition in the egg-parasite Trichogramma embryophagum. Nature 195: 1020–1021.

    Teerink B.J. , 'Host selection and number of eggs per oviposition in the egg-parasite Trichogramma embryophagum ' (1962 ) 195 Nature : 1020 -1021.

    • Search Google Scholar
  • 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.

    Laurenne N. , '', in Phylogeny of a taxonomically difficult group and evolution of host location mechanism , (2008 ) -.

  • 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. 65:1087–1089.

    Sparks A.N. , 'Ahost-seeking stimulant for the egg parasite, Trichogramma evanescens. Its source and demonstration of its laboratory and field activity ' (1972 ) 65 Ann. Entomol. Soc. Am. : 1087 -1089.

    • Search Google Scholar
  • 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: 1323–1331.

    Tumlinson J.H. , '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 ' (1982 ) 8 J. Chem. Ecol. : 1323 -1331.

    • Search Google Scholar
  • 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. 41–62.

    Mackauer M. , '', in Critical Issues in Biological Control , (1990 ) -.

  • 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: 337–343.

    Lim U.T. , 'Host discrimination and interspecific competition of Trissolcus nigripedius and Telenomus gifuensis, sympatric parasitoid of Dolycoris baccarum ' (2008 ) 45 Biol. Control : 337 -343.

    • Search Google Scholar
  • Makeea, H. 2006. Effect of host egg viability on reproduction and development of Trichogramma cacoeciae and T. principium. Biocontrol Sci. Tech. 16: 195–204.

    Makeea H. , 'Effect of host egg viability on reproduction and development of Trichogramma cacoeciae and T. principium ' (2006 ) 16 Biocontrol Sci. Tech. : 195 -204.

    • Search Google Scholar
  • McGregor, R. and Henderson, D. 1998. The influence of oviposition experience on response to host pheromone in Trichogramma sibericum. J. Insect Behav. 11: 621–632.

    Henderson D. , 'The influence of oviposition experience on response to host pheromone in Trichogramma sibericum ' (1998 ) 11 J. Insect Behav. : 621 -632.

    • Search Google Scholar
  • Miller, J.C., 1977. Ecological relationships among parasites of Spodoptera praefica. Environ. Entomol. 6: 581–585.

    Miller J.C. , 'Ecological relationships among parasites of Spodoptera praefica ' (1977 ) 6 Environ. Entomol. : 581 -585.

    • Search Google Scholar
  • 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. 191–220.

    Mills N. , '', in Trophic and Guild Interactions in Biological Control , (2006 ) -.

  • 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: 208–216.

    Lacan I. , 'Ratio dependence in the functional response of insect parasitoides: evidence from Trichogramma minutum foraging for eggs in small host patches ' (2004 ) 29 Ecol. Entomol. : 208 -216.

    • Search Google Scholar
  • Morrison, G. and Lewis, W. J. 1981. The allocation of searching time by Trichogramma pretiosum in host-containing patches. Entomol. Exp. Appl. 30: 31–39.

    Lewis W. J. , 'The allocation of searching time by Trichogramma pretiosum in host-containing patches ' (1981 ) 30 Entomol. Exp. Appl. : 31 -39.

    • Search Google Scholar
  • 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.

    Christopoulos A. , '', in Fitting Models to Biological Data Using Linear and Nonlinear Regression: A Practical Guide to Curve Fitting , (2003 ) -.

  • Nagarkatti, S. and Nagaraja, H. 1977. Biosystematics of Trichogramma and Trichograrnmatoidea species. Annu. Rev. Entomo1. 22: 157–176.

    Nagaraja H. , 'Biosystematics of Trichogramma and Trichograrnmatoidea species ' (1977 ) 22 Annu. Rev. Entomo1. : 157 -176.

    • Search Google Scholar
  • Neher, D.A. 1999. Soil community composition and ecosystem processes: comparing agricultural ecosystems with natural ecosystems. Agroforest. Syst. 45: 159–185.

    Neher D.A. , 'Soil community composition and ecosystem processes: comparing agricultural ecosystems with natural ecosystems ' (1999 ) 45 Agroforest. Syst. : 159 -185.

    • Search Google Scholar
  • 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: 313–327.

    Lewis W.J. , 'How Trichogramma parasitoids use moth sex pheromones as kairomones: orientation behaviour in a wind tunnel ' (1991 ) 16 Physiol. Entomol. : 313 -327.

    • Search Google Scholar
  • 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: 129–132.

    Saglam O. , 'Overwintering of the egg parasitoids Trichogramma brassicae and T. cacoeciae in the Thrace region of Turkey ' (2005 ) 78 J. Pest Sci. : 129 -132.

    • Search Google Scholar
  • Pak, G.A. and Oatman, E.R. 1982. Biology of Trichogramma brevicapillum. Ent. Exp. App1. 32: 61–67.

    Oatman E.R. , 'Biology of Trichogramma brevicapillum ' (1982 ) 32 Ent. Exp. App1. : 61 -67.

  • Pennacchio, F. and Strand, M.R. 2006. Evolution of developmental strategies in parasitic Hymenoptera. Annu. Rev. Entomol. 51: 233–258.

    Strand M.R. , 'Evolution of developmental strategies in parasitic Hymenoptera ' (2006 ) 51 Annu. Rev. Entomol. : 233 -258.

    • Search Google Scholar
  • Polaszek A. 2010. Species diversity and host associations of Trichogramma in Eurasia. In: Cônsoli, F.L., Parra, J.R.P. and Zucchi, R.A. (Eds.). Egg Parasitoids in Agroecosystems with Emphasis on Trichogramma. Springer. Dordrecht, pp. 237–266.

    Polaszek A. , '', in Egg Parasitoids in Agroecosystems with Emphasis on Trichogramma , (2010 ) -.

  • Quicke, D.L.J., 1997. Parasitic Wasps. Chapman & Hall, London.

    Quicke D.L.J. , '', in Parasitic Wasps , (1997 ) -.

  • 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: 229–236

    Tabone E. , 'Functional response of Trichogramma chilonis to Galleria mellonella and Chilo sacchariphagus eggs ' (2006 ) 118 Entomol. Exp. Appl. : 229 -236.

    • Search Google Scholar
  • Rechav, Y. and Orion, T. 1975. The development of the immature stages of Chelonus inanitus. Ann. Entomol. Soc. Am. 68: 457–462.

    Orion T. , 'The development of the immature stages of Chelonus inanitus ' (1975 ) 68 Ann. Entomol. Soc. Am. : 457 -462.

    • Search Google Scholar
  • Rodriguez, H., Cabello, T. and Vargas, P. 1988a. Influencia de la dieta en el desarrollo de Ephestia kuehniella. Bol. San. Veg. Plagas 14: 363–369.

    Vargas P. , 'Influencia de la dieta en el desarrollo de Ephestia kuehniella ' (1988 ) 14 Bol. San. Veg. Plagas : 363 -369.

    • Search Google Scholar
  • Rodriguez, H., Cabello, T. and Vargas, P. 1988b. Influencia de la dieta e iluminación en la longevidad, fecundidad y fertilidad de Ephestia kuehniella. Bol. San. Veg. Plagas 14: 561–566.

    Vargas P. , 'Influencia de la dieta e iluminación en la longevidad, fecundidad y fertilidad de Ephestia kuehniella ' (1988 ) 14 Bol. San. Veg. Plagas : 561 -566.

    • Search Google Scholar
  • Rosenheim, J.A. 1998. Higher-order predators and the regulation of insect herbivore populations. Annu. Rev. Entomol. 43:421–47.

    Rosenheim J.A. , 'Higher-order predators and the regulation of insect herbivore populations ' (1998 ) 43 Annu. Rev. Entomol. : 421 -47.

    • Search Google Scholar
  • Royer, L., Fournet, S., Brunel, E. and Boivin, G. 1999. Intra- and interspecific host discrimination by host-seeking larvae of coleopteran parasitoids. Oecologia 118:59–68.

    Boivin G. , 'Intra- and interspecific host discrimination by host-seeking larvae of coleopteran parasitoids ' (1999 ) 118 Oecologia : 59 -68.

    • Search Google Scholar
  • Scholz, D. and Höller, 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: 289–300.

    Höller C. , 'Competition for host between two hyperparasitoids of aphids, Dentrocerus laticeps and Dendrocerus carpenter: The benefit of interspecific host discrimination ' (1992 ) 5 J. Insect Behav. : 289 -300.

    • Search Google Scholar
  • Shaw M.R., 1994. Parasitoid host ranges. In: Hawkins B.A. and Sheenhan W. (Eds.), Parasitoid Community Ecology. Oxford University Press, Oxford, pp. 111–144.

    Shaw M.R. , '', in Parasitoid Community Ecology , (1994 ) -.

  • Shaw M.R. 2006. Habitat considerations for parasitic wasps (Hymenoptera). J. Insect Conserv. 10: 117–127.

    Shaw M.R. , 'Habitat considerations for parasitic wasps (Hymenoptera) ' (2006 ) 10 J. Insect Conserv. : 117 -127.

    • Search Google Scholar
  • 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.

    Huddleston T. , '', in Handbooks for the Identification of British insect , (1991 ) -.

  • SPSS 2009. Pasw Statistics Base 18. SPSS Inc. Chicago.

    '', in Pasw Statistics Base 18 , (2009 ) -.

  • 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. 97–136.

    Strand M.R. , '', in Insect Parasitoid , (1986 ) -.

  • Tobias, V.I., 1975. A Review of the Braconidae (Hymenoptera) of the USSR. Publishing Co. PVT. LTD, New Delhi.

    Tobias V.I. , '', in A Review of the Braconidae (Hymenoptera) of the USSR , (1975 ) -.

  • 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. 512–588.

    Medvedv G.S. , '', in Keys to the Insects of the European Part of the USSR , (1997 ) -.

  • 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: 352–359.

    Strien-van Liempt W.T.F.H. , 'Why is there no interspecific host discrimination in the two coexisting larval parasitoid of Drosophila species: Leptopilina heterotoma and Asorbara tabida ' (1985 ) 67 Oecologia : 352 -359.

    • Search Google Scholar
  • 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: 1137–1142.

    Iwabuchi K. , 'Physiological suppression of the larval parasitoid Glyptapantles pallipes by the polyembryonic parasitoid Compidosoma floridanum ' (2006 ) 52 J. Insect Physiol. : 1137 -1142.

    • Search Google Scholar
  • van Driesche, R.G., Hoddle, M.S. and Center, T.D. 2007. Control de plagas y malezas por enemigos naturales. USDA-USFS, Washington.

    Center T.D. , '', in Control de plagas y malezas por enemigos naturales , (2007 ) -.

  • 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: 639–650.

    Hanski I. , 'Colonization rates and distances of a host butterfly and two specific parasitoids in a fragmented landscape ' (2002 ) 71 J. Anim. Ecol. : 639 -650.

    • Search Google Scholar
  • Vinson, S.B. 1976. Host selection by insect parasitoide. Annu. Rev. Entomol. 21: 109–133.

    Vinson S.B. , 'Host selection by insect parasitoide ' (1976 ) 21 Annu. Rev. Entomol. : 109 -133.

    • Search Google Scholar
  • 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: 79–96.

    Vinson S.B. , 'The general host selection behavior of parasitoid Hymenoptera and a comparison of initial strategies utilized by larvaphagous and oophagous species ' (1998 ) 11 Biol. Control. : 79 -96.

    • Search Google Scholar
  • Voegele, J., Brun, P. and Daumal, J. 1974. Les Trichogrammes: 1.-Modalités de la prise de possession et de l’élimination de l’hote chez le parasite embryonnaire Trichogramma brasiliensis. Ann. Soc. Entomol. Fr. 10: 737–761.

    Daumal J. , 'Les Trichogrammes: 1.-Modalités de la prise de possession et de l’élimination de l’hote chez le parasite embryonnaire Trichogramma brasiliensis ' (1974 ) 10 Ann. Soc. Entomol. Fr. : 737 -761.

    • Search Google Scholar
  • Volkoff, A.N., Daumal, J., Barry, P., François, 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: 459–466.

    Rossi M.M. , 'Development of Trichogramma cacoeciae: time table and evidence for a single larval instar ' (1995 ) 24 Int. J. Insect Morphol. Embryol. : 459 -466.

    • Search Google Scholar
  • Wajnberg, E., Bernstein, C. and van Alphen, J. (Eds.) 2008. Behavioral Ecology of Insect Parasitoids: From Theoretical Approaches to Field Applications. Blackwell, Malden.

    '', in Behavioral Ecology of Insect Parasitoids: From Theoretical Approaches to Field Applications , (2008 ) -.

  • Wang, B. and Ferro, D.N. 1998. Functional responses of Trichogramma ostriniae to Ostrinia nubilalis under laboratory and field conditions. Environ. Entomol. 27: 752–758.

    Ferro D.N. , 'Functional responses of Trichogramma ostriniae to Ostrinia nubilalis under laboratory and field conditions ' (1998 ) 27 Environ. Entomol. : 752 -758.

    • Search Google Scholar
  • Zwölfer, 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. 405–416.

    Zwölfer H. , '', in Dynamics of populations. Proceedings of the Advanced Study Institute on Dynamics of Numbers in Populations, Oosterbeek, 1970 , (1971 ) -.