Conspecific and heterospecific host discrimination in two parasitoid species of the mealybug Pseudococcus viburni, the solitary Leptomastix epona and the gregarious Pseudaphycus flavidulus

PDF
Published: Jan 8, 2009
DOI: https://doi.org/10.12681/eh.11605
Keywords:
conspecific interspecific host discrimination multiparasitism multiple-species introduction parasitoid competition superparasitism
F. Karamaouna
Benaki Phytopathological Institute, Department of Pesticides’ Control and Phytopharmacy, Laboratory of Efficacy Evaluation of Pesticides, Greece
M.J.W. Copland
Department of Agricultural Sciences, Imperial College at Wye, University of London
Abstract
Leptomastix epona (Walker) and Pseudaphycus flavidulus (Brèthes) (Hymenoptera: Encyrtidae) are endoparasitoids of the mealybug Pseudococus viburni (Signoret) (Hemiptera: Pseudococcidae). Leptomastix epona is a solitary parasitoid originating from Europe and P. flavidulus is a gregarious parasitoid from South America. Conspecific and heterospecific host discrimination was examined between unparasitised female adult mealybugs and others already parasitized, at different time intervals between the primary and the following oviposition. Female wasps of L. epona discriminate between unparasitized hosts and hosts parasitized 0-96 hours previously by a conspecific selecting more often the first over the latter for oviposition. Females of P. flavidulus discriminate between unparasitized hosts and hosts parasitized prior to 0-72 hours by a conspecific. Conspecific superparasitism also occurs in both parasitoid species. The secondary sex ratio of L. epona and the clutch size of P. flavidulus are not affected by superparasitism whereas the secondary sex ratio of P. flavidulus in superparasitized hosts is more male biased than in single parasitized hosts. The solitary parasitoid L. epona does not discriminate between unparasitized hosts and hosts parasitized by P. flavidulus 0-3 or 24 hours previously. Nevertheless the gregarious parasitoid P. flavidulus discriminates between unparasitized hosts and hosts parasitized by L. epona 0-3 hours earlier, but it oviposits without discrimination in hosts heterospecifically parasitized 24 hours beforehand. When multiparasitism occurs at 0-3 hours after the first oviposition, L. epona is a superior competitor regardless of which species oviposits first. However, when the time interval between the two ovipositions is 24 hours, the probability of the offspring of P. flavidulus winning the competition with L. epona increases when either species oviposits first. The potential effect of multiparasitism on parasitoid coexistence is discussed in relation to prospects for multiplespecies introductions or augmentative releases for the biological control of the mealybug.
Article Details
  • Section
  • Articles
Creative Commons License

This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License.

Authors who publish with this journal agree to the following terms:

Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons 4.0 license.

Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g. post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal. Authors are permitted and encouraged to post their work online (preferably in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work.

Downloads
Download data is not yet available.
References
Alphen, J.J.M. van, M.J. van Dijken and J.K. Waage. 1987. A functional approach to superparasitism: host discrimination needs to be learnt. Netherlands Journal of Zoology, 37: 167-179.
Alphen, J.J.M. van and M. Visser. 1990. Superparasitism as an adaptive strategy for insect parasitoids. Annu. Rev. Entomol., 35: 59-79.
Baaren, J. van and J.-P. Nènon. 1996. Intraspecific larval competition in the solitary parasitoids, Apoanagyrus (Epidinocarsis) lopezi and Leptomastix dactylopii. Entomol. Exp. Appl., 81: 325-333.
Ben-Dov, Y. 1994. A Systematic catalogue of the mealybugs of the world (Insecta: Homoptera, Coccoidea: with data on geographical distribution, host Plants, biology and economic importance). Intercept Publications Ltd., Andover, 686 pp.
Bokonon-Ganta, A.H., J.J.M. van Alphen and P. Neuenschwander. 1996. Competition between Gyranusoidea tebygi and Anagyrus mangicola, parasitoids of the mango mealybug, Rastrococcus invadens: interspecific host discrimination and larval competition. Entomol. Exp. Appl., 79:179-185.
Chow, F.J. and M. Mackauer. 1986. Host discrimination and larval competition in the aphid parasite Ephedrus californicus. Entomol. Exp. Appl., 41: 243-254.
Daane, K.M., 1999. Investigation of a cooperative based insectary and augmentation program for grape, longtailed and obscure mealybugs. Pest Management Grants Final Report to the Department of Pesticide Regulation, pp.23.
Daane, K.M., R. Malakar-Kuenen, M. Guillén, W.J. Bentley, M. Bianchi and D. González. 2002. Abiotic and biotic pest refuges hamper biological control of mealybugs in California vineyards. In: The Proceedings of the 1st International Symposium of Biological Control of Arthropods, January 14-18, 2002, U.S.D.A. Forest Service, Honolulu, Hawai, U.S., pp. 573.
Daane, K.M., M. Battany, E. Nelson, M. Cooper, K. Sime, J.R. Hagler. 2004. Investigation of the grape mealybug complex and its natural enemies to improve biological control. American Vineyard Foundation Annual Research Reports Crop Year 2004, pp.30.
DeBach, P. (ed) 1964. Biological Control of Insect Pests and Weeds. Chapman and Hall, London, 844 pp.
Dijken, M.J. van, P. van Stratum and J.J.M. van Alphen. 1993. Superparasitism and sex ratio in the solitary parasitoid Epidinocarsis lopezi. Entomol. Exp. Appl., 68: 51-58.
Dijken, M.J. van and J.K. Waage. 1987. Self and conspecific superparasitism by the egg parasitoid Trichogramma evanescens. Entomol. Exp. Appl., 43: 183-192.
Dorn, S. and N.E. Beckage. 2007. Superparasitism in gregarious hymenopteran parasitoids: ecological, behavioural and physiological perspectives. Physiol. Entomol., 32: 199- 211.
Ehler, L.E. and R.W. Hall. 1982. Evidence for competitive exclusion of introduced natural enemies in biological control. Environ. Entomol., 11: 1-4.
EPPO Standards on Phytosanitary Measures – Safe Use of Biological Control. 2002. List of Biological Control Agents Widely Used in the EPPO Region [PM 3/(2)]. EPPO.
Godfray, H.C.J. 1994. Parasitoids: Behavioural and Evolutionary Ecology. Princeton University Press, Princeton, 473 pp.
Gonzalez, R.H. 1991. Mealybugs (Hom. Pseudococcidae), a new pest problem of japanese plums in Chile. Revista Fruticola, 12: 3-7.
Gutierrez, A.P., P. Neuenschwander and J.J.M. van Alphen. 1993. Factors affecting biological control of cassava mealybug by exotic parasitoids: a ratio dependent supply-demand driven model. J. Appl. Anim. Ecol., 30: 706-721.
Hamilton W.D. 1967. Extraordinary sex ratios. Science 156: 477-488.
Hassell, M.P. and J.K. Waage. 1984. Hostparasitoid population interactions. Annu. Rev. Entomol., 29: 89-114.
Hubbard, S.F., G. Marris, A. Reynolds and G.W. Rowe. 1987. Adaptive patterns in the avoidance of superparasitism by solitary parasitic wasps. J. Anim. Ecol., 56: 387-401.
Huffaker, C.B. and P.S. Messenger. 1976. Theory and Practice of Biological Control. Academic Press, New York, 788 pp.
Islam, K.S. and M.J.W. Copland. 2000. Influence of egg load and oviposition time interval on the host discrimination and offspring survival of Anagyrus pseudococci (Hymenoptera: Encyrtidae), a solitary endoparasitoid of citrus mealybug Planococcus citri (Hemiptera: Pseudococcidae). Bull. Entomol. Res., 90: 69-75.
Jong, P.W. de and J.J.M. van Alphen. 1989. Host size selection and sex allocation in Leptomastix dactylopii, a parasitoid of Planococcus citri. Entomol. Exp. Appl., 50: 161-169.
Kakehashi, N., Y. Suzuki and Y. Iwasa. 1984. Niche overlap of parasitoid systems: its consequence to single versus multiple introduction controversy in biological control. J. Anim. Ecol., 21: 115-131.
Karamaouna, F. 1999. Biology of the parasitoids Leptomastix epona (Walker) and Pseudaphycus flavidulus (Brèthes) and behavioural interactions with the host mealybug Pseudococcus viburni (Signoret). Ph.D. Thesis, University of London, 333 pp.
Karamaouna, F. and M.J.W. Copland. 2000a. Host suitability, quality 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.
Karamaouna, F. and M.J.W. Copland. 2000b. Oviposition behaviour, influence of experience on host size selection, and niche overlap of the solitary Leptomastix epona and the gregarious Pseudaphycus flavidulus, two endoparasitoids of the mealybug Pseudococcus viburni. Entomol. Exp. Appl., 97: 301-308.
Karamaouna, F. and M.J.W. Copland. 2002. Larval development of the endoparasitoid Leptomastix epona (Hymenoptera: Encyrtidae) and factors influencing egg and larval mortality by encapsulation in the mealybug Pseudococcus viburni (Hemiptera: Pseudococcidae), In: Abstracts of the VIIth European Congress of Entomology, October 7-13, 2002, Thessaloniki, Greece. p. 93.
Lenteren, J.C. van 1976. The development of host discrimination and the prevention of superparasitism in the parasite Pseudeucoila bochei Weld (Hym.: Cynipidae) Netherlands Journal of Zoology, 26: 1-83.
Lenteren, J.C. van 1981. Host discrimination by parasitoids. In: D.A. Nordlund, R.L. Jones & W.J. Lewis (eds). Semiochemicals, their Role in Pest Control. Wiley, New York, pp. 153-180.
Lenteren, J.C. van, K. Bakker and J.J.M. van Alphen. 1978. How to analyse host discrimination. Ecol. Entomol., 3: 71-75.
Mackauer, M., L.E. Ehler and J. Ronald. 1990. Critical Issues in Biological Control. Intercept, Andover, 330 pp.
May, R.M. and M.P. Hassell. 1981. The dynamics of multiparasitoid-host interactions. American Naturalist, 117: 234-261.
Micha, S.G., P.W. Wellings and R. Morton. 1992. Time-related rejection of parasitized hosts in the aphid parasitoid Aphidius ervi. Entomol. Exp. Appl., 62: 155-161.
Minitab Inc. 1995. Minitab User's Guide: Release 10 Xtra for Windows and Macintosh. State College, Pennsylvania.
Panis, A. 1986. Biological features of Pseudococcus affinis, Maskell (Homoptera: Pseudococcidae) as a guideline of its control in water-sprinkled citrus orchards. In: Cavallor and E. DiMartino (eds) Integrated Pest Control in Citrus Groves. Balkema, Rotterdam. pp. 59-65.
Pedata, P.A., M. Giorgini and E. Guerrieri. 2002. Interspecific host discrimination and within competition between Encarsia formosa and E. pergandiella (Hymenoptera: aphelinidae), two endoparasitoids of whiteflies (Heniptera: Aleyrodidae). Bull. Entomol. Res., 92: 521-528.
Phillips, P.A. and C.J. Sherk. 1991. To control mealybugs, stop honeydew-seeking ants. California Agriculture, 45: 26-28.
Pijls, J.W.A.M., K.D. Hofker, M.J. van Staalduinenand and J.J.M. van Alphen. 1990. Interspecific host discrimination and competition by Apoanagyrus (Epidinocarsis) lopezi and A. diversicornis, parasitoids of the cassava mealybug, Phenacoccus manihoti. Mededelingen van de Faculteit Landbouwwetenschappen van deRijksuniversiteit Gent, 55: 405-415.
Potting, R.P.J., H.M. Snellen. and L.E.M. Vet. 1997. Fitness consequences of superparasitism and mechanism of host discrimination in the stemborer parasitoid Cotesia flavipes. Entomol. Exp. Appl., 82: 341-348.
Shuker, D.M. and S.A. West. 2004. Information constraints and the precision of adaptation: Sex ratio manipulation in wasps. Proceedings of the National Academy of Sciences of the United States of America, 101: 10363-10367.
Smith, H.S. 1929. Multiple parasitism: its relation to the biological control of insect pests. Bull. Entomol. Res., 20: 141-149.
Suzuki Y. and Y. Iwasa. 1980. A sex ratio theory of gregarious parasitoids. Res. Popul. Ecol., 22: 366-382.
Turnbull, A.L. and D.A. Chant. 1961. The practice and theory of biological control of insects in Canada. Can. J. Zool., 39: 697-753.
Ueno, T. 1999. Multiparasitism and host feeding by solitary parasitoid wasps (Hymenoptera: Ichneumonidae) based on the pay-off from parasitized hosts. Behaviour, 92: 601-608.
Waage, J.K. 1986. Family planning in insect parasitoids. In: J.K. Waage and D. Greathead (eds). Insect Parasitoids. Academic Press, London. pp. 63-95.
Wai, K.M.and K. Fujii. 1990. Intraspecific larval competition among wasps parasitic of bean weevil larvae. Res. Popul. Ecol., 32: 85-98.
Wang, X.G. and R.H. Messing. 2004. Two different life-history strategies determine the competitive outcome between Dirrhinus giffardii (Chalcididae) and Pachycrepoideus vindemmiae (Pteromalidae), ectoparasitoids of cyclorrhaphus Diptera. Bull. Entomol. Res., 94: 473-480.
Werren, J.H. 1980. Sex ratio adaptations to local mate competition in a parasitic wasp. Science 208: 1157-1159.
Williams, D.J. 1962. The British Pseudococcidae. Bulletin of British Museum (Natural History), London, No 12. pp. 1-79.