Eur. J. Entomol. 102 (3): 475-481, 2005 | DOI: 10.14411/eje.2005.068

Sex ratio shift caused by hyperparasitism in the solitary parasitoid Lysiphlebus hirticornis (Hymenoptera: Braconidae: Aphidiinae)

Manfred MACKAUER1, Wolfgang VÖLKL2
1 Department of Biological Sciences, Simon Fraser University, 8888 University Drive, Burnaby, B.C., V5A 1S6, Canada; e-mail: mackauer@sfu.ca
2 Lehrstuhl für TierGkologie I, Universität Bayreuth, D-95440 Bayreuth, Germany; e-mail: wolfgang.voelkl@uni-bayreuth.de

We examined the influence of offspring mortality caused by hyperparasitism on the secondary sex ratio of Lysiphlebus hirticornis Mackauer, a solitary endoparasitoid of the aphid Metopeurum fuscoviride Stroyan, in the field. Females of L. hirticornis produce pseudo-gregarious broods, which may comprise more than 200 offspring. Hyperparasitoids [mainly Syrphophagus aphidivorus (Mayr)] attacked and killed up to 60% of the primary parasitoids inside mummified aphids, especially late in the season. Hyperparasitized broods were larger than hyperparasitoid-free broods, which suggests that the risk of hyperparasitism increased with mummy density. We tested the hypothesis that mortality caused by hyperparasitism is greater for female than male offspring of L. hirticornis. If mummy quality scales with mummy size, hyperparasitoids should choose the relatively larger over the relatively smaller mummies. In the absence of hyperparasitism, broods of L. hirticornis included approximately two daughters for each son; the sex ratio did not vary with brood size. In hyperparasitized broods, the sex ratio was nearly even. This result indicates that relatively more female offspring (developing in the larger mummies) than male offspring (developing in the smaller mummies) were killed by hyperparasitoids. We propose that sex-differential offspring mortality in L. hirticornis is the result of differences in optimal host choice between the primary parasitoid and the hyperparasitoids.

Keywords: Aphidiinae, Braconidae, Lysiphlebus hirticornis, aphid parasitoid, offspring mortality, hyperparasitism, Syrphophagus aphidivorus, sex ratio

Received: December 8, 2004; Revised: February 15, 2005; Accepted: February 15, 2005; Published: August 15, 2005  Show citation

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MACKAUER, M., & VÖLKL, W. (2005). Sex ratio shift caused by hyperparasitism in the solitary parasitoid Lysiphlebus hirticornis (Hymenoptera: Braconidae: Aphidiinae). EJE, 102(3), 475-481. doi: 10.14411/eje.2005.068
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    References

    1. ASSEM J. VAN DEN, GIJSWIJT J.J. & NUBEL B.K. 1980: Observations on courtship and mating strategies in a few species of parasitic wasps (Chalcidoidea). Neth. J. Zool. 30: 208-227 Go to original source...
    2. ASSEM J. VAN DEN, VAN IERSEL J.J.A. & LOS-DEN HARTOG R.L. 1989: Is being large more important for female than male parasitic wasps? Behaviour 108: 160-195 Go to original source...
    3. BAAREN J. VAN, LANDRY B.L. & 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 Go to original source...
    4. BRODEUR J. 2000: Host specificity and trophic relationships of hyperparasitoids. In Hochberg M. & Ives A.R. (eds): Parasite Population Biology. Princeton University Press, Princeton, NJ, pp. 139-162 Go to original source...
    5. BRODEUR J. & ROSENHEIM J.A. 2000: Intraguild interactions in aphid parasitoids. Entomol. Exp. Appl. 97: 93-108 Go to original source...
    6. BUDENBERG W.J. 1990: Honeydew as a contact kairomone for aphid parasitoids. Entomol. Exp. Appl. 55: 139-148 Go to original source...
    7. BUITENHUIS R., BOIVIN G., VET L.E.M. & BRODEUR J. 2004a: Preference and performance of the hyperparasitoid Syrphophagus aphidivorus (Hymenoptera: Encyrtidae): fitness consequences of selecting hosts in live aphids or aphid mummies. Ecol. Entomol. 29: 648-656 Go to original source...
    8. BUITENHUIS R., MCNEIL J.N., BOIVIN G. & BRODEUR J. 2004b: The role of honeydew in host searching of aphid hyperparasitoids. J. Chem. Ecol. 30: 273-285 Go to original source...
    9. CAMPBELL A., FRAZER B.D., GILBERT N., GUTIERREZ A.P. & MACKAUER M. 1974: Temperature requirements of some aphids and their parasites. J. Appl. Ecol. 11: 431-438 Go to original source...
    10. CHAU A. & MACKAUER M. 2001: Host-instar selection in the aphid parasitoid Monoctonus paulensis (Hymenoptera: Braconidae, Aphidiinae): assessing costs and benefits. Can. Entomol. 133: 549-564. Go to original source...
    11. CHOW A. & MACKAUER M. 1996: Sequential allocation of offspring sexes in the hyperparasitoid wasp, Dendrocerus carpenteri. Anim. Behav. 51: 859-870 Go to original source...
    12. CHOW A. & MACKAUER M. 1999: Host handling and specificity of the hyperparasitoid wasp, Dendrocerus carpenteri (Curtis) (Hym., Megaspilidae): importance of host age and species. J. Appl. Entomol. 123: 83-91 Go to original source...
    13. CLOUTIER C. & BAUDUIN F. 1990: Searching behavior of the aphid parasitoid Aphidius nigripes (Hymenoptera: Aphidiidae) foraging on potato plants. Environ. Entomol. 19: 222-228 Go to original source...
    14. CLOUTIER C., LEVESQUE A., EAVES D.M. & MACKAUER M. 1991: Maternal adjustment of sex ratio in response to host size in the aphid parasitoid Ephedrus californicus. Can. J. Zool. 69: 1489-1495 Go to original source...
    15. CLOUTIER C., DUPERRON J., TERTULIANO M. & MCNEIL J.N. 2000: Host instar, body size and fitness in the koinobiotic parasitoid Aphidius nigripes. Entomol. Exp. Appl. 97: 29-40 Go to original source...
    16. COLFER R.G. & ROSENHEIM J.A. 2001: Predation on immature parasitoids and its impact on aphid suppression. Oecologia 126: 292-304 Go to original source...
    17. COOK J.M. & CROZIER R.H. 1995: Sex determination and population biology in the Hymenoptera. Trends Ecol. Evol. 10: 281-286 Go to original source...
    18. DETTNER K. & LIEPERT C. 1994: Chemical mimicry and camouflage. Annu. Rev. Entomol. 39: 129-154 Go to original source...
    19. FERRARI J., DARBY A.C., DANIELL T.J., GODFRAY H.C.J. & DOUGLAS A.E. 2004: Linking the bacterial community in pea aphids with host-plant use and natural enemy resistance. Ecol. Entomol. 29: 60-65 Go to original source...
    20. GODFRAY H.C.J. 1994: Parasitoids: Behavioral and Evolutionary Ecology. Princeton University Press, Princeton, NJ, 473 pp Go to original source...
    21. GRIFFITHS D.C. 1961: The development of Monoctonus paludum Marshall (Hym., Braconidae) in Nasonovia ribis-nigri on lettuce, and immunity reactions in other lettuce aphids. Bull. Entomol. Res. 52: 147-163 Go to original source...
    22. HAN B. & CHEN Z. 2002: Behavioral and electrophysiological responses of natural enemies to synomones from tea shoots and kairomones from tea aphids, Toxoptera aurantii. J. Chem. Ecol. 28: 2203-2219 Go to original source...
    23. HARDY I.C.W. & COOK J.M. 1995: Brood sex ratio variance, developmental mortality and virginity in a gregarious parasitoid wasp. Oecologia 103: 162-169 Go to original source...
    24. HARDY I.C.W., DIJKSTRA L.J., GILLIS J.E.M. & LUFT P.A. 1998: Patterns of sex ratio, virginity and developmental mortality in gregarious parasitoids. Biol. J. Linn. Soc. 64: 239-270 Go to original source...
    25. HARVEY J.A., VET L.E.M., JIANG N. & GOLS R. 1998: Nutritional ecology of the interaction between larvae of the gregarious ectoparasitoid, Muscidifurax raptorellus (Hymenoptera: Pteromalidae), and their pupal host, Musca domestica (Diptera: Muscidae). Physiol. Entomol. 23: 113-120 Go to original source...
    26. HARVEY J.A., BEZEMER T.M., ELZINGA J.A. & STRAND M.R. 2004: Development of the solitary endoparasitoid Microplitis demolitor: host quality does not increase with host age and size. Ecol. Entomol. 29: 35-43 Go to original source...
    27. HEINZ K.M. 1996: Host size selection and sex allocation behaviour among parasitoid trophic levels. Ecol. Entomol. 21: 218-226 Go to original source...
    28. HOLLER C., BORGEMEISTER C., HAARDT H. & POWELL W. 1993: The relationship between primary parasitoids and hyperparasitoids of cereal aphids: an analysis of field data. J. Anim. Ecol. 62: 12-21 Go to original source...
    29. HOLLER C., MICHA S.G., SCHULZ S., FRANCKE W. & PICKETT J.A. 1994: Enemy-induced dispersal in a parasitic wasp. Experientia 50: 270-278 Go to original source...
    30. HUBNER G. & VOLKL W. 1996: Behavioral strategies of aphid hyperparasitoids to escape aggression by honeydewcollecting ants. J. Ins. Behav. 9: 143-157 Go to original source...
    31. HUFBAUER R.A. 2002: Evidence for nonadaptive evolution in parasitoid virulence following a biological control introduction. Ecol. Applications 12: 66-78 Go to original source...
    32. HUFBAUER R.A. & VIA S. 1999: Evolution of an aphid-parasitoid interaction: variation in resistance to parasitism among aphid populations specialized on different plants. Evolution 53: 1435-1445 Go to original source...
    33. KANEKO S. 2003: Impacts of two ants, Lasius niger and Pristomyrmex pungens (Hymenoptera: Formicidae), attending the brown citrus aphid, Toxoptera citricidus (Homoptera: Aphididae), on the parasitism of the aphid by the primary parasitoid, Lysiphlebus japonicus (Hymenoptera: Aphidiidae), and its larval survival. Appl. Entomol. Zool. 38: 347-357 Go to original source...
    34. KANUCK M.J. & SULLIVAN D.J. 1992: Ovipositional behavior and larval development of Aphidencyrtus aphidivorus (Hymenoptera: Encyrtidae), an aphid hyperparasitoid. J. N. Y. Entomol. Soc. 100: 527-532
    35. KING B.H. 1993: Sex ratio manipulation by parasitoid wasps. In Wrensch D.R. & Ebbert M.A. (eds): Evolution and Diversity of Sex Ratio in Insects and Mites. Chapman & Hall, New York, pp. 418-441 Go to original source...
    36. KLINGAUF F. 1966: Abwehr- und Meidereaktionen von Blattlaeusen (Aphididae) bei Bedrohung durch Raeuber und Parasiten. Z. Angew. Entomol. 60: 269-317 Go to original source...
    37. LIEPERT C. & DETTNER K. 1993: Recognition of aphid parasitoids by honeydew-collecting ants: the role of cuticular lipids in a chemical mimicry system. J. Chem. Ecol. 19: 2143-2153 Go to original source...
    38. LOSEY J.E. & DENNO R.F. 1998: The escape response of pea aphids to foliar-foraging predators: factors affecting dropping behaviour. Ecol. Entomol. 23: 53-61 Go to original source...
    39. LUCK R., MESSENGER P.S. & BARBIERI J.F. 1981: The influence of hyperparasitism on the performance of biological control agents. In Rosen D. (ed.): The Role of Hyperparasitism in Biological Control: a Symposium. Division of Agricultural Sciences, University of California, Berkeley, CA, Vol. 4103: 34-42
    40. MACKAUER M. 1976: The sex ratio in field populations of some aphid parasites. Ann. Entomol. Soc. Am. 69: 453-456 Go to original source...
    41. MACKAUER M. & LARDNER R.M. 1995: Sex-ratio bias in an aphid parasitoid-hyperparasitoid association: a test of two hypotheses. Ecol. Entomol. 20: 118-124 Go to original source...
    42. MACKAUER M. & STARY P. 1967: World Aphidiidae (Hym. Ichneumonoidea). Le Francois, Paris, 195 pp
    43. MACKAUER M. & VOLKL W. 1993: Regulation of aphid populations by aphidiid wasps: does parasitoid foraging behaviour or hyperparasitism limit impact? Oecologia 94: 339-350 Go to original source...
    44. MACKAUER M. & VOLKL W. 2002: Brood-size and sex-ratio variation in field populations of three species of solitary aphid parasitoids (Hymenoptera: Braconidae, Aphidiinae). Oecologia 131: 296-305 Go to original source...
    45. MACKAUER M., MICHAUD J.P. & VOLKL W. 1996: Host choice by aphidiid parasitoids (Hymenoptera: Aphidiidae): host recognition, host quality, and host value. Can. Entomol. 128: 959-980 Go to original source...
    46. MEYHOFER R. & KLUG T. 2002: Intraguild predation on the aphid parasitoid Lysiphlebus fabarum (Marshall) (Hymenoptera: Aphidiidae): mortality risks and behavioral decisions made under the threats of predation. Biol. Control 25: 239-248 Go to original source...
    47. MISHRA S. & SINGH R. 1991: Sex ratio of the aphid parasitoid Lysiphlebus delhiensis (Subba Rao & Sharma) (Hym., Aphidiidae) in field populations. J. Appl. Entomol. 111: 72-77. Go to original source...
    48. NAGELKERKE C.J. & HARDY I.C.W. 1994: The influence of developmental mortality on optimal sex allocation under local mate competition. Behav. Ecol. 5: 401-411 Go to original source...
    49. OLIVER K.M., RUSSELL J.A., MORAN N. & HUNTER M.S. 2003: Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proc. Nat. Acad. Sci. USA 100: 1803-1807 Go to original source...
    50. OTTO M. & MACKAUER M. 1998: The developmental strategy of an idiobiont ectoparasitoid, Dendrocerus carpenteri: influence of variations in host quality on offspring growth and fitness. Oecologia 117: 353-364 Go to original source...
    51. PANDEY S. & SINGH R. 1999: Host size induced variation in progeny sex ratio of an aphid parasitoid Lysiphlebia mirzai. Entomol. Exp. Appl. 90: 61-67 Go to original source...
    52. SALT G. & VAN DEN BOSCH R. 1967: The defense reactions of three species of Hypera (Coleoptera, Curculionidae) to an ichneumon wasp. J. Invertebr. Path. 9: 164-177 Go to original source...
    53. SANDLAN K. 1979: Sex ratio regulation in Coccygomimus turionella Linnaeus (Hymenoptera: Ichneumonidae) and its ecological implications. Ecol. Entomol. 4: 365-378 Go to original source...
    54. SEQUEIRA R. & MACKAUER M. 1992: Nutritional ecology of an insect host-parasitoid association: the pea aphid - Aphidius ervi system. Ecology 73: 183-189 Go to original source...
    55. SEQUEIRA R. & MACKAUER M. 1993: Seasonal variation in body size and offspring sex ratio in field populations of the parasitoid wasp, Aphidius ervi (Hymenoptera: Aphidiidae). Oikos 68: 340-346 Go to original source...
    56. SINGH R. & PANDEY S. 1997: Offspring sex ratio in Aphidiinae (Hymenoptera: Braconidae): a review and bibliography. J. Aphidol. 11: 61-82
    57. SNYDER W.E. & IVES A.R. 2003: Interactions between specialist and generalist natural enemies: parasitoids, predators, and pea aphid biocontrol. Ecology 84: 91-107 Go to original source...
    58. SOKAL R.R. & ROHLF F.J. 1995: Biometry, 3rd ed. W.H. Freeman, New York, NY, 887 pp
    59. STADLER B. & MACKAUER M. 1996: Influence of plant quality on interactions between the aphid parasitoid Ephedrus californicus Baker (Hymenoptera: Aphidiidae) and its host, Acyrthosiphon pisum (Harris) (Homoptera: Aphididae). Can. Entomol. 128: 27-39 Go to original source...
    60. SULLIVAN D.J. & VOLKL W. 1999: Hyperparasitism: multitrophic ecology and behaviour. Annu. Rev. Entomol. 44: 291-315 Go to original source...
    61. SUZUKI Y., TSUJI H. & SASAKAWA M. 1984: Sex allocation and effects of superparasitism on secondary sex ratios in the gregarious parasitoid, Trichogramma chilonis (Hymenoptera: Trichogrammatidae). Anim. Behav. 32: 478-484 Go to original source...
    62. TAKAGI M. 1986: The reproductive strategy of the gregarious parasitoid, Pteromalus puparum (Hymenoptera: Pteromalidae). 2. Host size discrimination and regulation of the number and sex ratio of progeny in a single host. Oecologia 70: 321-325 Go to original source...
    63. VISSER M.E. 1994: The importance of being large: the relationship between size and fitness in females of the parasitoid Aphaereta minuta (Hymenoptera: Braconidae). J. Anim. Ecol. 63: 963-978 Go to original source...
    64. VOLKL W. 1994: The effect of ant-attendance on the foraging behaviour of the aphid parasitoid Lysiphlebus cardui. Oikos 70: 149-155 Go to original source...
    65. VOLKL W. 1997: Interactions between ants and aphid parasitoids: patterns and consequences. In Dettner K., Bauer G. & VGlkl W. (eds): Vertical Food Web Interactions: Evolutionary Patterns and Driving Forces. Springer, Berlin, pp. 225-240 (Ecological Studies 130) Go to original source...
    66. VOLKL W. & MACKAUER M. 2000: Oviposition behaviour of aphidiine wasps (Hymenoptera: Braconidae, Aphidiinae): morphological adaptations and evolutionary trends. Can. Entomol. 132: 197-212 Go to original source...
    67. VOLKL W., HUBNER G. & DETTNER K. 1994: Interactions between Alloxysta brevis (Hymenoptera, Cynipoidea, Alloxystidae) and honeydew collecting ants: how an aphid parasitoid overcomes ant aggression by chemical defense. J. Chem. Ecol. 20: 2621-2635 Go to original source...
    68. VOLKL W., KRANZ P., WEISSER W. & HUBNER G. 1995: Patch time allocation and resource exploitation in aphid primary parasitoids and hyperparasitoids searching simultaneously within aphid colonies. J. Appl. Entomol. 119: 399-404 Go to original source...
    69. WAAGE J.K. 1986: Family planning in parasitoids: adaptive patterns of progeny and sex allocation. In Waage J. & Greathead D. (eds): Insect Parasitoids. 13th Symposium of the Royal Entomological Society of London. Academic, London, pp. 63-95
    70. WEISSER W.W. 2000: Metapopulation dynamics in an aphidparasitoid system. Entomol. Exp. Appl. 97: 83-92 Go to original source...
    71. WELLINGS P.W., MORTON R. & HART P.J. 1986: Primary sex-ratio and differential progeny survivorship in solitary haplo-diploid parasitoids. Ecol. Entomol. 11: 341-348 Go to original source...
    72. WYLIE H.G. 1965: Effects of superparasitism on Nasonia vitripennis (Walk.) (Hymenoptera: Pteromalidae). Can. Entomol. 97: 326-331 Go to original source...

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