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Host availability affects the interaction between pupal parasitoid Coptera haywardi (Hymenoptera: Diiapridae) and larval–pupal parasitoid Diachasmimorpha longicaudata (Hymenoptera: Braconidae)

Published online by Cambridge University Press:  12 February 2018

P. Montoya ,
C. Gálvez  and
F. Díaz-Fleischer
P. Montoya*
Affiliation:
Programa Moscafrut SAGARPA-IICA, Camino a los Cacaoatales S/N, C.P. 30860, Metapa de Domínguez, Chiapas, México
C. Gálvez
Affiliation:
Programa Moscafrut SAGARPA-IICA, Camino a los Cacaoatales S/N, C.P. 30860, Metapa de Domínguez, Chiapas, México Instituto de Biociencias, Universidad Autónoma de Chiapas, Campus IV, C.P. 30700, Tapachula, Chiapas, México
F. Díaz-Fleischer
Affiliation:
INBIOTECA, Universidad Veracruzana, Av. de las Culturas Veracruzanas 101, Col. Emiliano Zapata, Xalapa, Veracruz, C.P. 91090, México
*
*Author for correspondence Phone: +52 9626435059 Fax: +52 9626435059 E-mail: pablo.montoya@iica-moscafrut.org.mx
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Abstract

The use of multiple species in biological control programmes is controversial when interactions among them are not fully understood. We determined the response of the pupal parasitoid Coptera haywardi (Oglobin) to different availability of Anastrepha ludens (Loew) pupae previously parasitized or not by larval–pupal Diachasmimorpha longicaudata (Ashmead). The two types of pupae were exposed at different ages and proportions to different numbers of C. haywardi females for 48 h. The performance of C. haywardi adults emerging from parasitized and unparasitized pupae was measured. Coptera haywardi prefers to attack unparasitized A. ludens pupae rather than pupae parasitized by D. longicaudata. However, when the availability of unparasitized pupae was low or the number of foraging females was high, C. haywardi competed against early immature stages of the D. longicaudata, or hyperparasitized, feeding directly on the advanced-immature developmental stages of the early acting species. Adults of C. haywardi emerging as hyperparasitoids were no different in size, fecundity and longevity from those emerging as primary parasitoids. Our data suggest that simultaneous use of these species in augmentative biological control projects may be feasible but should be carefully planned in order to avoid any detrimental effect of its interaction.

Keywords

competitionhyperparasitismhost discriminationmultiple agentsaugmentative biological control
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 109 , Issue 1 , February 2019 , pp. 15 - 23
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Copyright
Copyright © Cambridge University Press 2018 

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References

Agresti, A. (1996) An Introduction to Categorical Data Analysis. New York, John Wiley.Google Scholar
Aluja, M., Guillen, J., Liedo, P., Cabrera, M., Ríos, E., de la Rosa, G., Celedonio, H. & Mota, D. (1990) Fruit infesting tephritids (Diptera: Tephritidae) and associated parasitoids in Chiapas, Mexico. Entomophaga 35, 39–48.Google Scholar
Bader, A.E., Heinz, K.M., Wharton, R.A. & Bográn, C.E. (2006) Assessment of interspecific interactions among parasitoids on the outcome of inoculative biological control of leafminers attacking chrysanthemum. Biological Control 39, 441–452.Google Scholar
Bonsall, M.B., Jansen, V.A.A. & Hassell, M.P. (2004) Life history trade-offs assemble ecological guilds. Science 306, 111–113.Google Scholar
Briggs, C.J. (1993) Competition among parasitoid species on a stage-structured host and its effect on host suppression. The American Naturalist 141, 372–397.Google Scholar
Brodeur, J. (2000) Host specificity and trophic relationships of hyperparasitoids. pp. 163–183 in Hochberg, M.E. & Ives, R.A. (Eds) Parasitoids Population Biology. Princeton, New Jersey, Princeton University Press.Google Scholar
Cancino, J. & Yoc, M. (1993) Methods proposed to apply quality control in the mass rearing of Diachasmimorpha longicaudata. pp. 37–47 in Nicoli, G., Benuzzi, M. & Leppla, N. (Eds) Quality Control of Mass Reared Arthropods, Rimini, Italy, IOBC.Google Scholar
Cancino, J., Ruiz, L., López, P. & Moreno, F.M. (2010) Cría masiva de parasitoids. pp. 291–306 in Montoya, P., Toledo, J., Hernández, E. (Eds) Moscas de la Fruta: Fundamentos y Procedimientos para su Manejo. Mexico, D.F., S y G Editores.Google Scholar
Cancino, J., Liedo, P., Ruiz, L., López, G., Montoya, P., Barrera, J.F., Sivinski, J. & Aluja, M. (2012) Discrimination by Coptera haywardi (Hymenoptera: Diapriidae) of hosts previously attacked by conspecifics or by the larval parasitoid Diachasmimorpha longicaudata (Hymenoptera: Braconidae). Biocontrol Science and Technology 22, 899–914.Google Scholar
Carabajal-Paladino, L.Z., Papeschi, A.G. & Cladera, J.L. (2010) Immature stages of development in the parasitoid wasp, Diachasmimorpha longicaudata. Journal of Insect Science 10, 56. Available online: insectsicence.org/10.56.Google Scholar
Crawley, M.J. (1993) GLIM for Ecologists. Oxford, Blackwell.Google Scholar
Denoth, M., Frid, L. & Myers, J.H. (2002) Multiple agents in biological control: improving the odds?. Biological Control 24, 20–30.Google Scholar
Domínguez, J., Artiaga-López, T., Solís, E. & Hernández, E. (2010) Métodos de colonización y cría masiva. pp. 259–276 in Montoya, P., Toledo, J. & Hernández, E. (Eds) Moscas La Fruta: Fundamentos y Procedimientos para su Manejo. Mexico, D.F., S y G Editores.Google Scholar
Ehler, L.E. (1979) Utility of facultative secondary parasitoids in biological control. Environmental Entomology 4, 353–354.Google Scholar
Ehler, L.E. (1990) Introduction strategies in biological control of insects. pp. 111–134 in Mackauer, M., Ehler, L. & Roland, J. (Eds) Critical Issues in Biological Control. Andover, UK, Intercep.Google Scholar
Francis, B., Green, M. & Payne, C. (1993) Statistical System for Generalized Linear Interactive Modelling. Oxford, UK, Clarendon Press.Google Scholar
Godfray, H.C.J. (1994) Parasitoids. Behavioral and Evolutionary Ecology. pp. 9–11. Princeton, Princeton University Press.Google Scholar
Grandgirard, J., Poinsot, D., Krespi, L., Nénon, L. & Cortesero, A. (2002) Costs of secondary parasitism in the facultative hyperparasitoid Pachycrepoideus dubius: does host size matter? Entomologia Experimentalis et Applicata 103, 239–248.Google Scholar
Guzmán-Salinas, J. & Montoya, P. (2008) Efecto del tamaño del fruto hospedero en el parasitismo aditivo de tres especies de parasitoides atacando Anastrepha ludens (Diptera: Tephritidae). pp. 128–132 in Memorias del XXXI Congreso Nacional de Control Biológico Zacatecas, Mexico.Google Scholar
Harvey, J.A., Pashalidou, F., Soler, R. & Bezemer, T.M. (2011) Intrinsic competition between two secondary hyperparasitoids results in temporal trophic switch. Oikos 120, 226–233.Google Scholar
Harvey, J.A., Poelman, E.H. & Tanaka, T. (2013) Intrinsic inter- and intraspecific competition in parasitoid wasps. Annual Review of Entomology 58, 333–351.Google Scholar
Hawkins, B.A. (1992) Parasitoid-host food webs and donor control. Oikos 65, 159–162.Google Scholar
Heinz, K.M. & Nelson, J.M. (1996) Interspecific interactions among natural enemy of Bemisia in an inundative biological control program. Biological Control 6, 384–393.Google Scholar
Jiménez y Jiménez, E. (1956) Las moscas de la fruta y sus enemigos naturales. Fitofilo 16, 4–11.Google Scholar
Knipling, E.F. (1977) The theoretical basis for augmentation of natural enemies. pp. 79–123 in Ridgway, R.L. & Vinson, S.B. (Eds) Biological Control by Augmentation of Natural Enemies. Volume 11 of the series Environmental Science Research. NY, Plenum Press.Google Scholar
López, M., Aluja, M. & Sivinski, J. (1999) Hymenopterous larval–pupal and pupal parasitoids of Anastrepha flies (Diptera: Tephritidae) in Mexico. Biological Control 15, 119–120.Google Scholar
May, R.M. & Hassell, M.P. (1981) The dynamics of multiparasitoid–host interactions. American Naturalist 117, 234–261.Google Scholar
Mills, N.J. & Gutierrez, A. (1999) Biological control of insect pests. pp. 89–102 in Hawkins, B. & Cornell, H.V. (Eds) Theoretical Approaches to Biological Control. Cambridge, UK, Cambridge University Press.Google Scholar
Montoya, P., Liedo, P., Benrey, B., Cancino, J., Barrera, J.F., Sivinski, J. & Aluja, M. (2000 a) Biological control of Anastrepha spp. (Diptera: Tephritidae) in mango orchards through augmentative releases of Diachasmimorpha longicaudata (Ashmead) (Hymenoptera: Braconidae). Biological Control 18, 216–224.Google Scholar
Montoya, P., Liedo, P., Benrey, B., Barrera, J.F., Cancino, J. & Aluja, M. (2000 b) Functional response and superparasitism by Diachasmimorpha longicaudata (Hymenoptera: Braconidae), a parasitoid of fruit flies (Diptera: Tephritidae). Annals of Entomological Society of America 93, 47–54.Google Scholar
Montoya, P., Cancino, J., Zenil, M., Santiago, G. & Gutierrez, J.M. (2007) The augmentative biological control components in the Mexican National Campaign against Anastrepha spp. Fruit flies. pp. 661–670 in Vreysen, M., Robinson, A. & Hendrichs, J. (Eds) Area-wide Control of Insect Pests. The Netherlands, Springer.Google Scholar
Montoya, P., Ayala, A., López, P., Cancino, J., Cabrera, H., Cruz, J., Martínez, M.A., Figueroa, I. & Liedo, P. (2016) Natural parasitism in fruit fly populations in disturbed areas adjacent to commercial mango orchards in Chiapas and Veracruz, Mexico. Environmental Entomology 42, 328–337.Google Scholar
Ovruski, S., Aluja, M., Sivinski, J. & Wharton, R.A. (2000) Hymenopteran parasitoids on fruit-infesting Tephritidae (Diptera) in Latin America and the southern United States: diversity, distribution, taxonomic status and their use in fruit fly biological control. Integrated Pest Management Reviews 5, 81–107.Google Scholar
Pedersen, B.S. & Mills, N.J. (2004) Single vs. multiple introduction in biological control: the roles of parasitoid efficiency, antagonism and niche overlap. Journal of Applied Ecology 41, 973–984.Google Scholar
Pérez-Lachaud, G., Batchelor, T.M. & Hardy, I.C.W. (2004) Wasp eat wasp: facultative hyperparasitism and intra-guild predation by bethylid wasps. Biological Control 30, 149–155.Google Scholar
Powell, W., Walton, M. & Jervis, M.A. (1996) Populations and communities. pp. 223–292 in Jervis, M.A. & Kidd, N.A.C. (Eds) Insect Natural Enemies. Practical Approaches to Their Study and Evaluations. Oxford, Great Britain, Chapman and Hall.Google Scholar
Price, P.W. (1972) Parasitiods utilizing the same host: adaptive nature of differences in size and form. Ecology 53, 190–195.Google Scholar
Rosenheim, J.A. (1998) Higher-order predators and the regulations of insect herbivore populations. Annual Review of Entomology 43, 421–447.Google Scholar
Rosenheim, J.A., Kaya, H.K., Elher, L.E., Marois, J.J. & Jaffee, B.A. (1995) Intraguild predation among biological control agents: theory and evidence. Biological Control 5, 303–335.Google Scholar
Sivinski, J. (1996) The past and potential of biological control of fruit flies. pp. 369–375 in McPheron, B.A. & Steck, G.J. (Eds) Economic Fruit Flies: A World Assessment of Their Biology and Management. DelRay Beach, FL, St. Lucie Press.Google Scholar
Sivinski, J., Smittie, B. & Burns, E. (1991) Effects of irradiating host larvae in the mass-reared braconid Diachasmimorpha longicaudata in Abstract of the “5th International Workshop, IOBC Mutuality Control of Mass Reared Arthropods”. Wageningen, The Netherlands, International Agricultural Center.Google Scholar
Sivinski, J., Calkins, C., Baranowski, R.M., Harris, D., Brambila, J., Diaz, J., Burns, R., Holler, T. & Dodson, G. (1996) Suppression of a Caribbean fruit fly Anastrepha suspensa (Loew) (Diptera: Tephritidae) population through augmentative releases of the parasitoid Diachasmimorpha longicaudata (Ashmead) (Hymenoptera: Braconidae). Biological Control 6, 177–185.Google Scholar
Sivinski, J., Aluja, M. & López, M. (1997) Spatial and temporal distributions of braconid parasitoids of Mexican Anastrepha spp. in the canopies of host fruit trees. Annals of the Entomological Society of America 90, 604–618.Google Scholar
Sivinski, J., Vulinec, K., Menezes, E. & Aluja, M. (1998) The bionomics of Coptera haywardi (Oglobin) (Hymenoptera: Diapriidae) and other pupal parasitoids of tephritid fruit flies (Diptera). Biological Control 11, 193–202.Google Scholar
Stiling, P. & Cornelissen, T. (2005) What makes a successful biocontrol agent? A meta-analysis of biological control agent performance. Biological Control 34, 236–246.Google Scholar
Statgraphics (2008) Statgraphics Centurion XV, User Manual. Warrenton, Virginia, USA, Statpoint Technologies, Inc., 287pp.Google Scholar
Sullivan, D. (1987) Insect hyperparasitism. Annual Review of Entomology 32, 49–70.Google Scholar
Sullivan, D. & Völkl, W. (1999) Hyperparasitism: Multitrophic ecology and behavior. Annual Review of Entomology 44, 291–315.Google Scholar
Wang, X.G. & Messing, R.H. (2004) The ectoparasitic pupal parasitoid, Pachycrepoideus vindemmiae (Hymenoptera: Pteromalidae), attacks other primary tephritid fruit fly parasitoids: host expansion and potential non-target impact. Biological Control 31, 227–236.Google Scholar
Wang, X.G., Bokonon-Ganta, A.H. & Messing, R.H. (2008) Intrinsic inter-specific competition in a guild of tephritid fruit fly parasitoids: effect of co-evolutionary history on competitive superiority. Biological Control 44, 312–320.Google Scholar
White, E., Bernal, J., Gonzáles, D. & Triapitsyn, S. (1998) Facultative hyperparasitism in Brachymeria pomonae (Hymenoptera: Chalcididae). European Journal of Entomology 95, 359–366.Google Scholar
Wong, T.T.Y. & Ramadan, M.M. (1987) Parasitization of the Mediterranean and Oriental fruit flies (Diptera: Tephritidae) in the Kula area of Maui, Hawaii. Journal of Economic Entomology 80, 77–80.Google Scholar
Wong, T.T.Y., Ramadan, M.M., McInnis, D.O., Mochizuki, N.L., Nishimoto, J.A. & Herr, J.C. (1991) Augmentative releases of Diachasmimorpha tryoni (Hymenoptera: Braconidae) to suppress a Mediterranean fruit fly population in Kula Maui, Hawaii. Biological Control 1, 2–7.Google Scholar
Xu, H.Y., Yang, N.W. & Wan, F.H. (2013) Competitive interactions between parasitoids provide new insight into host suppression. PLoS ONE 8(11), e82003. https://doi.org/10.1371/journal.pone.0082003.Google Scholar