Abstract
Female black pupae from the Anastrepha ludens genetic sexing strain Tapachula-7 were evaluated as hosts for Coptera haywardi. We studied the host acceptance and the effects of age, irradiation and automated mechanical separation of black pupae on the emergence, survival, fecundity and flight ability of parasitoid C. haywardi adults. Our results indicated that black pupae are viable hosts for C. haywardi. Adult emergence was greater when the exposed pupae were three and five days old. The impact that occurred during mechanical separation reduced emergence by 16 %. The tested irradiation doses (25, 35 and 45 Gy) did not significantly affect adult emergence. No significant differences in longevity, fecundity or flight ability were observed between parasitoids that emerged from the Tapachula-7 black pupae and those that emerged from the standard mass-reared strain.
Similar content being viewed by others
References
Aluja M (1994) Bionomics and management of Anastrepha. Annu Rev Entomol 39:155–178
Aluja M, Sivinski J, Ovruski S, Guillén L, López M, Cancino J, Torres-Anaya A, Gallegos-Chan G, Ruíz L (2009) Colonization and domestication of seven species of native new world hymenopterous larval-prepupal and pupal fruit fly (Diptera: Tephritidae) parasitoids. Biocontrol Sci Technol 19:49–79
Baeza-Larios G, Sivinski J, Holler T, Aluja M (2002) The ability of C. haywardi (Oglobin) (Hymenoptera: Diapriidae) to locate and attack the pupae of the Mediterranean fruit fly, Ceratitis capitata (Wiedemann) (Diptera: Tephritidae), under seminatural conditions. Biol Control 23:213–218
Battaglia D, Poppy G, Powell W, Romano A, Tranfaglia A, Pennacchio F (2000) Physical and chemical cues influencing the oviposition behavior of Aphidius ervi. Entomol Exp Appl 94:219–227
Cancino J, Ruiz L, Sivinski J, Galvez F, Aluja M (2009) Rearing of five hymenopterous larval-prepupal (Braconidae: Figitidae) and three pupal (Diapriidae, Chalcidoidea, Eurytmidae) native parasitoids of the genus Anastrepha (Diptera: Tephritidae) on irradiated A. ludens larva and pupae. Biocontrol Sci Technol 19:193–209
Cancino J, Liedo P, Ruiz L, López G, Montoya P, Francisco J, Sivinski J, Aluja M (2012) Discrimination by C. haywardi (Hymenoptera: Diapriidae) of hosts previously attacked by conspecifics or by the larval parasitoid Diachasmimorpha longicaudata (Hymenoptera: Braconidae). Biocontrol Sci Technol 22:899–914
Chang FCL, Ozaki E, Kobayashi R (1982) Effect of mechanical sifting of pupae on the α-glycerophosphate dehydrogenase activity in adults of the Mediterranean fruit fly, Ceratitis capitata (Wiedemann) (Diptera: Tephritidae). Ann Entomol Soc Am 75:290–292
Cusson M, Laforge M, Regniere J, Beliveau C, Trudel D, Thireau J, Ballemare O, Keirstead N, Stolz D (2002) Multiparasitism of Chorisoneura fumiferana by the Ichneumonid Tranosema rostrale and the Tachinid Aclia interrupta: occurrence in the field and outcome of competition under laboratory conditions. Entomol Exp Appl 102:125–133
Denoth M, Frid L, Myers H (2002) Multiple agents in biological control: improve the odds? Biol Control 24:20–30
Domínguez J, Artiaga T, Solís E, Hernández E (2010) Métodos de colonización y cría masiva [Methods of colonization and mass rearing]. In: Montoya P, Toledo J, Hernández E (eds) Moscas de la fruta: fundamentos y procedimientos para su manejo [Fruit flies: basis and procedures for their management]. S y G Editores, Mexico, pp 259–276
Enkerlin WR (2005) Impact of fruit fly programmes using the sterile insect technique. In: Dyck VA, Hendrichs J, Robinson AS (eds) Sterile insect technique. principles and practice in area-wide integrated pest management. Springer, The Netherlands, pp 651–676
Fischer S, Samietz J, Wäckers F, Dorn S (2003) Perception of achromatic cues during host location of a pupal parasitoid. Entomol Exp Appl 106:63–66
Francis B, Green M, Payne C (1993) Statistical system for generalized linear interactive modelling. Clarendon Press, Oxford, UK
Franz G, Gencheva E, Kerremans P (1994) Improved stability of genetic sex separation strains for the Mediterranean fruit fly, Ceratitis capitata. Genome 37:72–82
Franz G, Kerremans PH, Rendon P, Hendrichs J (1996) Development and application of genetic sexing systems for the Mediterranean fruit fly based on a temperature sensitive lethal. In: McPheron BA, Steck GJ (eds) Fruit fly pests: a world assessment of their biology and management. St. Lucie Press, Delray Beach Fl, USA, pp 185–191
González PI, Montoya P, Pérez-Lachaud G, Cancino J, Liedo P (2007) Superparasitism in mass reared Diachasmimorpha longicaudata (Asmead) (Hymenoptera: Braconidae), a parasitoid of fruit flies (Diptera: Tephritidae). Biol Control 40:320–326
Guillén L, Aluja M, Equihua M, Sivinski J (2002) Performance of two fruit fly (Diptera: Tephritidae) pupal parasitoids (C. haywardi [Hymenotera: Diapriidae] and Pachycrepoideus vindemiae [Hymenoptera: Pteromalidae]) under different environmental soil conditions. Biol Control 23:219–222
Hallman GJ (2000) Expanding radiation quarantine treatments beyond fruit flies. Agricult Forest Entomol 2:85–95
Harris MO, Foster SP (1995) Behavior and integration. In: Cardé RT, Bell W (eds) Chemical ecology of insects. Chapman and Hall, New York, USA, pp 3–46
Hendrichs J, Franz G, Rendón P (1995) Increased effectiveness and applicability of the sterile insect technique through male-only releases for control of Mediterranean fruit flies during fruiting seasons. J Appl Entomol 119:371–377
Henneman ML, Dyreson EG, Takabayashi J, Raguso RA (2002) Response to walnut olfactory and visual cues by the parasitic wasp Diachasmimorpha juglandis. J Chem Ecol 11:2221–2244
Hepdurgn B, Turanli T, Zümreoglu A (2009) Parasitism rate and sex ratio of Psyttalia (=Opius) concolor (Hymenoptera: Braconidae) reared on irradiated Ceratitis capitata larvae (Diptera: Tephritidae). Biocontrol Sci Technol 19:157–165
Hooper GH (1989) The effect of ionizing radiation on reproduction. In: Robinson AS, Hooper GHS (eds) World crops pests. fruit flies: their biology, natural enemies and control. Elsevier, New York, USA, pp 153–161
Little HF, Kobayashi RM, Ozaki ET, Cunningham RT (1981) Irreversible damage to flight muscles resulting from disturbance of pupae during rearing of the Mediterranean fruit fly, Ceratitis capitata. Ann Entomol Soc Am 74:24–26
Lobdell CE, Yong TH, Hoffmann MP (2005) Host color preferences and short range searching behavior of the egg parasitoid Trichogramma ostriniae. Entomol Exp Appl 116:127–134
López M, Aluja M, Sivinski J (1999) Hymenopterous larval-pupal and pupal parasitoids of Anastrepha flies (Diptera: Tephritidae) in Mexico. Biol Control 15:119–129
Montoya P, Liedo P, Benrey B, Cancino J, Barrera JF, Sivinski J, Aluja M (2000) Biological control of Anastrepha spp. (Diptera: Tephritidae) in mango orchards trough augmentative releases of Diachasmimorpha longicaudata (Ashmead) (Hymenoptera: Braconidae). Biol Control 18:216–224
Montoya P, Cancino J, Zenil M, Santiago G, Gutiérrez JM (2007) The augmentative biological control component in the Mexican campaign against Anastrepha spp. fruit flies. In: Vreysen MJB, Robinson AS, Hendrichs J (eds) Area-wide control of insect pests: from research to field implementation. Springer, The Netherlands, pp 661–670
Montoya P, Cancino J, Pérez-Lachaud G, Liedo P (2011) Host size superparasitism and sex ratio in mass-reared Diachasmimorpha longicaudata, a fruit fly parasitoid. BioControl 56:11–17
Montoya P, Cancino J, Ruiz L (2012) Packing of fruit fly parasitoids for augmentative releases. Insects 3:889–899
Orozco D, Meza S, Zepeda S, Solís E, Quintero F (2013) Tapachula-7, a new genetic sexing strain of the Mexican fruit fly (Diptera: Tephritidae): sexual compatibility and competitiveness. J Econ Entomol 106:735–741
Ovruski S, Aluja M, Sivinski J, Wharton R (2000) Hymenopteran parasitoids on fruit infesting Tephritidae (Diptera) in Latin America and Southern United States: diversity, distribution, taxonomic status and their use in fruit fly biological control. Int Pest Manag Rev 5:81–107
Ozaki ET, Kobayashi RM (1982) Effects of duration and intensity of sifting pupae of various ages on adult eclosion and flight capability of the Mediterranean fruit fly (Diptera: Tephritidae). J Econ Entomol 75:773–776
Paine TD, Paine EO, Hanks LM, Millar JG (2000) Resource partitioning among parasitoids (Hymenoptera: Braconidae) of Phoracantha semipunctata in their native range. Biol Control 19:223–231
Pedersen BS, Mills NI (2004) Single vs. multiple introductions in biological control: the roles of parasitoids efficiency, antagonism and niche overlap. J Appl Entomol 41:973–984
Rendón P, McInnis D, Lance D, Stewart J (2004) Medfly (Diptera: Tephritidae) genetic sexing: large-scale field comparison of males-only and bisexual sterile fly releases in Guatemala. J Econ Entomol 5:1547–1553
Reyes J, Santiago G, Hernández P (2000) Mexican fruit fly eradication programme. In: Tan KH (ed) Area-wide control of fruit flies and other insect pests. Penerbit University Sains, Pulau Pinang, Malaysia, pp 377–380
Robinson AS, Franz G, Fisher K (1999) Genetic sexing strain in the medfly, Ceratitis capitata: development, mass rearing and field testing. Trends Entomol 1:81–104
Rousse P, Chiroleu F, Veslot J, Quilici S (2007) The host-and microhabitat olfactory location by Fopius arisanus suggests a broad potential host range. Physiol Entomol 32:313–321
Sivinski J, Calkins CO, Baranowski RM, Harris D, Brambila J, Diaz J, Burns RE, Holler T, Dodson D (1996) Suppression of a Caribbean fruit fly (Anastrepha suspensa (Loew) Diptera: Tephritidae) population through releases of the parasitoids Diachasmimorpha longicaudata (Ashmead) (Hymenoptera: Braconidae). Biol Control 6:177–185
Sivinski J, Vulinec K, Menezes E, Aluja M (1998) The bionomics of C. haywardi (Ogloblin) (Hymenoptera: Diapriidae) and other pupal parasitoids of Tephritidae fruit flies (Diptera). Biol Control 11:193–202
Snyder WE, Ballard SN, Yang S, Clevenger GM, Miller TD, Hatten T, Berryman AA (2004) Complementary biocontrol of aphids by ladybird beetle Harmonia axyrids and the parasitoid Aphelinus asychis on greenhouse roses. Biol Control 30:229–235
van Alphen JJM, Visser ME (1990) Superparasitism as an adaptive strategy for insect parasitoids. Annu Rev Entomol 3:59–79
Zar JH (1984) Biostatistical analysis. Prentice-Hall, Englewood Cliffs, USA
Zepeda S (2010) Development of genetic sexing strains. In: Montoya P, Toledo J, Hernández E (eds) Moscas de la fruta: fundamentos y procedimientos para su manejo [Fruit flies: basis and procedures for their management]. S y G Editores, Mexico, pp 333–342
Acknowledgments
The authors thank to Julio Rojas (Ecosur) for helpful review of this manuscript and Javier Valle-Mora (Ecosur) for assistance in the statistical analyses. Yeudiel Gómez and the Moscamed irradiation plant staff help us irradiating the biological material. Dina Orozco (Moscafrut facility SAGARPA-IICA) provided the biological materials. We also thank the National Council for Science and Technology (CONACYT) for the scholarship granted to FLA.
Author information
Authors and Affiliations
Corresponding author
Additional information
Handling Editor: Dirk Babendreier.
Rights and permissions
About this article
Cite this article
López-Arriaga, F., Montoya, P., Cancino, J. et al. Female pupae of the genetic sexing strain “Tap-7” of Anastrepha ludens as hosts of Coptera haywardi . BioControl 59, 149–157 (2014). https://doi.org/10.1007/s10526-013-9552-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10526-013-9552-9