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Host size, superparasitism and sex ratio in mass-reared Diachasmimorpha longicaudata, a fruit fly parasitoid

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Abstract

We analyzed the relationship among host size, superparasitism and sex-ratio in mass reared Diachasmimorpha longicaudata (Hymenoptera: Braconidae). Individual host pupae of Anastrepha ludens (Diptera: Tephritidae) were measured (length and width), and the number of oviposition scars per pupa was used as a reliable indicator of superparasitism. The probability of an emerging parasitoid being a female was positively associated with the number of oviposition scars on the host cuticle, but not with the host size. The number of scars per host pupae from which females emerged was slightly but significantly higher than in those pupae giving raise to males. In D. longicaudata, the influence of host size on sex allocation decisions of individual females seems to be overridden by the level of superparasitism, which itself was positively correlated with pupa length. This suggests that larger pupae could experience a higher number of ovipositions than their smaller counterparts, and that a high level of superparasitism may conduct to a female biased sex ratio. We discuss the relevance of these findings which could provide new elements (e.g., the manipulation of superparasitism) for optimizing the mass rearing of this parasitoid.

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References

  • Cancino J, Montoya P (2008) Advances and perspectives in the mass rearing of fruit fly parasitoids in Mexico. In: Sugayama R, Zucchi RA, Ovruski SM, Sivinski J (eds) Fruit flies of economic importance: from basic to applied knowledge. Press Color, Bahia Brazil, pp 133–143

    Google Scholar 

  • Cancino J, Ruiz L, Gómez Y, Toledo J (2002) Irradiación de larvas de Anastrepha ludens (Loew) (Diptera: Tephritidae) para inhibir la emergencia de moscas en la cría del parasitoide Diachasmimorpha longicaudata (Ashmead) (Hymenoptera: Braconidae). Folia Entomol Mex 41:195–208

    Google Scholar 

  • Cancino J, Ruiz L, López P, Moreno FDM (2010) Cría masiva de parasitoides In: Montoya P, Toledo J, Hernández E (eds) Moscas de la Fruta: Fundamentos y Procedimientos para su Manejo. S y G Editores, México DF, pp 287–302

  • Charnov EL (1982) The theory of sex allocation. Princeton University Press, Princeton

    Google Scholar 

  • Darrouzet E, Imbert E, Chevier C (2003) Self-superparasitism consequences for offspring sex ratio in the solitary ectoparasitoid Eupelmus vuilleti. Entomol Exp Appl 109:167–171

    Article  Google Scholar 

  • Darrouzet E, Boivin G, Chevrier C (2008) Sex allocation decision under superparasitism by the parasitoid wasp Eupelmus vuilleti. J Insect Behav 21:181–191

    Article  Google Scholar 

  • Fisher RA (1930) The genetical theory of natural selection. Oxford University Press, Oxford

    Google Scholar 

  • Godfray HCJ (1994) Parasitoids behavioral and evolutionary ecology. Princeton University Press, Princeton

    Google Scholar 

  • González P, Montoya P, Pérez-Lachaud G, Cancino J, Liedo P (2007) Superparasitism in mass reared Diachasmimorpha longicaudata (Ashmead) (Hymenoptera: Braconidae), a parasitoid of fruit flies (Diptera: Tephritidae). Biol Control 40:320–326

    Article  Google Scholar 

  • González P, Montoya P, Pérez-Lachaud G, Cancino J, Liedo P (2010) Host discrimination and superparasitism in wild and mass-reared Diachasmimorpha longicaudata (Hym.: Braconidae) females. Biocontrol Sci Technol 20:137–148

    Article  Google Scholar 

  • Hardy ICW (1994) Sex ratio and mating structure in the parasitoid Hymenoptera. Oikos 69:3–20

    Article  Google Scholar 

  • Heimpel GE (1997) Extraordinary sex ratios for extraordinary reasons. Trends Ecol Evol 12:298–299

    Article  Google Scholar 

  • Heimpel GE, Lundgren JG (2000) Sex ratios of commercially reared biological control agents. Biol Control 19:77–93

    Article  Google Scholar 

  • Irvin NA, Hoddle MS (2006) The effect of intraspecific competition on progeny sex ratio in Gonotacerus spp. for Homalodisca coagulta egg masses: economic implications for mass rearing and biological control. Biol Control 39:162–170

    Article  Google Scholar 

  • Jones WT (1982) Sex ratio and host size in a parasitoid wasp. Behav Ecol Sociobiol 10:207–210

    Article  Google Scholar 

  • Karamaouna F, Copland MJW (2000) Host suitability and host size preference of Leptomastix epona and Pseudaphycus flavidulus, two endoparasitoids of the mealybug Pseudococcus viburni, and host size effect on parasitoid sex ratio and clutch size. Entomol Exp Appl 96:149–158

    Article  Google Scholar 

  • Khafagi WE, Hegazi EM (2008) Does superparasitism improve host suitability for parasitoid development? A case study in the Microplitis rufiventris–Spodoptera littoralis system. BioControl 53:427–438

    Article  Google Scholar 

  • King BH (1988) Sex ratio manipulation in response to host size by the parasitoid wasp Sphalangia cameroni: a laboratory study. Evolution 42:1190–1198

    Article  Google Scholar 

  • King BH (1989) Host-size dependent sex ratios among parasitoids wasps: does host growth matter? Oecologia 78:420–426

    Article  Google Scholar 

  • King BH (1993) Sex ratio manipulation by parasitoid wasps. In: Wrensch DL, Ebberte M (eds) Evolution and diversity of sex ratio in insects and mites. Chapman and Hall, New York, pp 418–441

    Google Scholar 

  • King BH (1995) How do female parasitoid wasps assess host size during sex ratio manipulation? Anim Behav 48:511–518

    Article  Google Scholar 

  • Lawrence PO (2005) Morphogenesis and cytopathic effects of the Diachasmimorpha longicaudata entomopoxvirus in host haemocytes. J Insect Physiol 51:221–233

    Article  CAS  PubMed  Google Scholar 

  • Lawrence PO, Akin D (1990) Virus-like particles in the accessory glands of Biosteres longicaudatus. Can J Zool 68:539–546

    Article  Google Scholar 

  • Lebreton S, Chevrier C, Darrouzet E (2010) Sex allocation strategies in response to conspecifics’ offspring sex ratio in solitary parasitoids. Behav Ecol 21:107–112

    Article  Google Scholar 

  • López OP, Hénaut Y, Cancino J, Lambin M, Cruz-López L, Rojas JC (2009) Is host size an indicator of quality in the mass-reared parasitoid Diachasmimorpha longicaudata (Hymenoptera, Braconidae)? Fla Entomol 92:441–449

    Article  Google Scholar 

  • Montoya P, Liedo P, Benrey B, Barrera JF, Cancino J, Sivinski J, Aluja M (2000a) Biological control of Anastrepha spp. (Diptera: Tephritidae) in mango orchards through augmentative releases of Diachasmimorpha longicaudata (Ashmead) (Hymenoptera: Braconidae). Biol Control 18:212–224

    Article  Google Scholar 

  • Montoya P, Liedo P, Benrey B, Barrera JF, Cancino J, Aluja M (2000b) Functional response and superparasitism by Diachasmimorpha longicaudata (Hymenoptera: Braconidae), a parasitoid of fruit flies (Diptera: Tephritidae). Ann Entomol Soc Am 93:47–54

    Article  Google Scholar 

  • Montoya P, Benrey B, Barrera JF, Zenil M, Ruiz L, Liedo P (2003) Oviposition behavior and conspecific host discrimination in Diachasmimorpha longicaudata (Hymenoptera: Braconidae), a fruit fly parasitoid. Biocontrol Sci Technol 13:683–690

    Article  Google Scholar 

  • Montoya P, Cancino J, Zenil M, Gutiérrez JM, Santiago G (2007) The augmentative biological control component in the Mexican campaign against Anastrepha fruit flies. In: Vreysen MJB, Robinson AS, Hendrichs J (eds) Area-wide control of insects pests: from research to field implementation. Springer, Dordrecht, pp 661–670

    Chapter  Google Scholar 

  • Morrison LLW, Sanford DP, Gilbert LE (1999) Sex ratio variation as a function of host size in Pseudacteon flies (Diptera: Phoridae), parasitoids of Solenopsis fire ants (Hymenoptera: Formicidae). Biol J Linn Soc 66:257–267

    Google Scholar 

  • Napoleon ME, King BH (1999) Offspring sex ratio response to host size in the parasitoid wasp Sphalangia endius. Behav Ecol Sociobiol 46:325–332

    Article  Google Scholar 

  • Ode PJ, Hardy IWC (2008) Parasitoid sex ratios and biological control. In: Wajnberg E, Bernstein C, van Alphen JJM (eds) Behavioural ecology of insect parasitoids: from theoretical approaches to field applications. Blackwell Publishing, Oxford, pp 253–291

    Chapter  Google Scholar 

  • Ode PJ, Heinz KM (2002) Host-size dependent sex ratio theory and improving mass reared parasitoid sex ratios. Biol Control 24:31–41

    Article  Google Scholar 

  • Quicke DLJ (1997) Parasitic wasps. Chapman and Hall, London

    Google Scholar 

  • Santolamazza-Carbone S, Cordero-Rivera A (2003) Superparasitism and sex ratio adjustment in a wasp parasitoid: results at variance with Local Mate Competition? Oecologia 136:365–373

    Article  PubMed  Google Scholar 

  • Sivinski J (1996) The past and potential of biological control of fruit flies. In: Mc Pheron BA, Stek GJ (eds) Fruit flies pests: a world assessment of their biology and management. St. Louis Press, Delray Beach, pp 369–375

    Google Scholar 

  • Statgraphics (2008) Statgraphics Centurion XV user manual. Statgraphics, USA, 287 pp

  • van Alphen JJM, Visser ME (1990) Superparasitism as an adaptive strategy for insects parasitoids. Annu Rev Entomol 35:59–79

    Article  PubMed  Google Scholar 

  • van Baaren J, Landry BL, Boivin G (1999) Sex allocation and larval competition in a superparasitizing solitary egg parasitoid: competing strategies for an optimal sex ratio. Funct Ecol 13:66–71

    Article  Google Scholar 

  • Waage JK (1982) Sex ratio and population dynamics of natural enemies—some possible interactions. Ann Appl Biol 101:154–164

    Google Scholar 

  • Waage JK, Carl KP, Mills NJ, Greathead DJ (1985) Rearing entomophagous insects. In: Singh P, Moore RF (eds) Handbook of insect rearing, vol 1. Elsevier, Amsterdam, pp 45–66

    Google Scholar 

  • Wang XG, Messing RH (2003) Intra- and interspecific competition by Fopius arisanus and Diachasmimorpha tryoni (Hymenoptera: Braconidae), parasitoids of tephritid fruit flies. Biol Control 27:251–259

    Article  CAS  Google Scholar 

  • Werren HJ (1980) Sex ratio adaptation to local mate competition in a parasitic wasp. Science 208:1157–1159

    Article  CAS  PubMed  Google Scholar 

  • Wilson K, Hardy ICW (2002) Statistical analysis of sex ratios: an introduction. In: Hardy IAC (ed) Sex ratios: concepts and research methods. Cambridge University Press, Cambridge, pp 49–92

    Google Scholar 

  • Wylie HG (1976) Interference among females of Nasonia vitripennis (Hymenoptera: Pteromalidae) and its effect on sex ratio of their progeny. Can Entomol 108:655–661

    Article  Google Scholar 

  • Wylie HG (1979) Sex ratio variability of Muscidifurax zaraptor (Hymenoptera: Pteromalidae). Can Entomol 111:105–109

    Article  Google Scholar 

Download references

Acknowledgments

We are grateful to Trevor Williams (INECOL) for helpful revision of an earlier version of this manuscript. We thank Javier Valle-Mora (ECOSUR) for statistical advice, and Velizario Rivera and Gladys Lopez for technical assistance. We also thank Julio Dominguez for providing insects. This research was funded by the Programa Moscafrut SAGARPA-IICA, Mexico.

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Authors and Affiliations

  1. Programa Moscafrut SAGARPA-IICA, Av. Central Poniente 14, 30700, Tapachula, CHIS, Mexico

    Pablo Montoya & Jorge Cancino

  2. El Colegio de la Frontera Sur, Apartado Postal 36, 30700, Tapachula, CHIS, Mexico

    Gabriela Pérez-Lachaud & Pablo Liedo

Authors
  1. Pablo Montoya
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  2. Jorge Cancino
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  3. Gabriela Pérez-Lachaud
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  4. Pablo Liedo
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Correspondence to Pablo Montoya.

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Handling Editor: Torsten Meiners.

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Montoya, P., Cancino, J., Pérez-Lachaud, G. et al. Host size, superparasitism and sex ratio in mass-reared Diachasmimorpha longicaudata, a fruit fly parasitoid. BioControl 56, 11–17 (2011). https://doi.org/10.1007/s10526-010-9307-9

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  • DOI: https://doi.org/10.1007/s10526-010-9307-9

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