Eur. J. Entomol. 122: 80-87, 2025 | DOI: 10.14411/eje.2025.010

Superparasitism and its effects on the fitness of the larval parasitoid, Coccygidium luteum (Hymenoptera: Braconidae)Original article

Patrick BESEH ORCID...1, *, Lakpo Koku AGBOYI ORCID...2, Benjamin MENSAH3, John ABRAHAM ORCID...3, *
1 Plant Protection and Regulatory Services Directorate, Ministry of Food and Agriculture, Accra, Ghana; e-mail: pkbeseh@gmail.com
2 CAB-International Ghana, P.O. Box CT 8630, Cantonments, Accra, Ghana; e-mail: L.Agboyi@cabi.org
3 Department of Conservation Biology and Entomology, School of Biological Sciences, University of Cape Coast, Cape Coast, Ghana; e-mails: bmensah@ucc.edu.gh, jabraham@ucc.edu.gh

The tendency of parasitoid wasps to oviposit in a previously parasitised host (superparasitism) has long been considered detrimental to their fitness, until recent evidence showed that it may be an adaptive strategy. The solitary koinobiont parasitoid, Coccygidium luteum, was observed to superparasitise the fall armyworm, Spodoptera frugiperda, under laboratory conditions. This study was conducted to elucidate the oviposition choice between unparasitised and previously parasitised hosts by C. luteum and to determine the effect of superparasitism on progeny development and adult fitness, using fall armyworm larvae as hosts. In a choice assay, previously parasitised and unparasitised hosts were simultaneously exposed to C. luteum for oviposition. Oviposition duration and preference were observed and the influence of superparasitism on the development of immature parasitoids and adult fitness were investigated by exposing host larvae to single, double and triple parasitism at 1 h intervals. Coccygidium luteum readily attacked both unparasitised and previously parasitised hosts without discrimination. However, the time spent ovipositing on the unparasitised host was significantly longer than that on a previously parasitised host. Superparasitism did not significantly affect progeny development and the fitness of adult C. luteum. Offspring development time and size of adult parasitoids were similar in superparasitised hosts compared to hosts that were parasitised once. We conclude that superparasitism in C. luteum will have no effect on its mass rearing for the biological control of S. frugiperda.

Keywords: Koinobiont, adaptive, parasitoid wasp, progeny, fitness, competition

Received: January 14, 2025; Revised: March 19, 2025; Accepted: March 19, 2025; Published online: April 28, 2025  Show citation

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BESEH, P., AGBOYI, L.K., MENSAH, B., & ABRAHAM, J. (2025). Superparasitism and its effects on the fitness of the larval parasitoid, Coccygidium luteum (Hymenoptera: Braconidae). EJE, 122, Article 80-87. https://doi.org/10.14411/eje.2025.010
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    References

    1. Abang A.F., Nanga S.N., Kuate A.F., Kouebou C., Suh C., Masso C., Saethre M.G. & Mokpokpo Fiaboe K.K. 2021: Natural enemies of fall armyworm Spodoptera frugiperda (Lepidoptera: Noctuidae) in different agro-ecologies. - Insects 12: 509, 23 pp. Go to original source...
    2. Agboyi L.K., Mensah S.A., Clottey V.A., Beseh P., Glikpo R., Rwomushana I., Day R. & Kenis M. 2019: Evidence of leaf consumption rate decrease in fall armyworm, Spodoptera frugiperda, larvae parasitized by Coccygidium luteum. - Insects 10: 410, 9 pp. Go to original source...
    3. Agboyi L.K., Goergen G., Beseh P., Mensah S.A., Clottey V.A., Glikpo R., Buddie A., Cafà G., Offord L., Day R., Rwomushana I. & Kenis M. 2020: Parasitoid complex of fall armyworm, Spodoptera frugiperda, in Ghana and Benin. - Insects 11: 68, 15 pp. Go to original source...
    4. Amaya K.E., Asgari S., Jung R., Hongskula M. & Beckage N.E. 2005: Parasitization of Manduca sexta larvae by the parasitoid wasp Cotesia congregata induces an impaired host immune response. - J. Insect Physiol. 51: 505-512. Go to original source...
    5. Andrew N., Basio M. & Kim Y. 2006: Additive effect of teratocyte and calyx fluid from Cotesia plutellae on immunosuppression of Plutella xylostella. - Physiol. Entomol. 31: 341-347. Go to original source...
    6. Bai B. & Mackuer M. 1992: Influence of superparasitism on development rate and adult size in a solitary parasitoid wasp, Aphidius ervi. - Fun. Ecol 6: 302-304. Go to original source...
    7. Bakker K., Eijsackers H.J.P., van Lenteren J.C. & Meelis E. 1972: Some models describing the distribution of eggs of the parasite Pseudeucoila bochei (Hym., Cynip.) over its hosts, larvae of Drosophila melanogaster. - Oecologia 10: 29-57. Go to original source...
    8. Bakker K., van Alphen J.J.M., van Batenburg F.H.D., van der Hoeven N., Nell H.W., van Strien-van Liempt W.T.F.H. & Turlings T.C.J. 1985: The function of host discrimination and superparasitization in parasitoids. - Oecologia 67: 572-576. Go to original source...
    9. Caniço A., Mexia A. & Santos L. 2020: First report of native parasitoids of fall armyworm Spodoptera frugiperda Smith (Lepidoptera: Noctuidae) in Mozambique. - Insects 11: 615, 12 pp. Go to original source...
    10. Charnov E.L. & Skinner S.W. 1985: Complementary approaches to the understanding of parasitoid oviposition decisions. - Environ. Entomol. 14: 383-391. Go to original source...
    11. Chen W.-B., Vasseur L., Zhang S.-Q., Zhang H.-F., Mao J., Liu T.-S., Zhou X.-Y., Wang X., Zhang J., You M.-S. & Gurr G.M. 2020: Mechanism and consequences for avoidance of superparasitism in the solitary parasitoid Cotesia vestalis. - Sci. Rep. 10: 11463, 10 pp. Go to original source...
    12. Chen J., Fang G., Pang L., Sheng Y., Zhang Q., Zhou Y., Zhou S., Lu Y., Liu Z., Zhang Y., Li G., Shi M., Chen X., Zhan S. & Huang J. 2021: Neofunctionalization of an ancient domain allows parasites to avoid intraspecific competition by manipulating host behaviour. - Nature Commun. 12: 5489, 15 pp. Go to original source...
    13. Cock M.J.W., Beseh P.K., Buddie A.G., Cafá G. & Crozier J. 2017: Molecular methods to detect Spodoptera frugiperda in Ghana, and implications for monitoring the spread of invasive species in developing countries. - Sci. Rep. 7: 4103, 10 pp. Go to original source...
    14. Duval J.F., Brodeur J., Doyon J. & Boivin G. 2018: Impact of superparasitism time intervals on progeny survival and fitness of an egg parasitoid. - Ecol. Entomol. 43: 310-317. Go to original source...
    15. Farahani H.K., Ashour A., Zibaee A. & Abroon P.A.L. 2016: The effect of host nutritional quality on multiple components of Trichogramma brassicae fitness. - Bull. Entomol. Res. 106: 633-641. Go to original source...
    16. Gandon S., Rivero A. & Varaldi J. 2006: Superparasitism evolution: Adaptation or manipulation? - Am. Nat. 167: E1-E22. Go to original source...
    17. Gao S., Tang Y., Wei K., Wang X., Yang Z. & Zhang Y. 2016: Relationships between body size and parasitic fitness and offspring performance of Sclerodermus pupariae (Hymenoptera: Bethylidae). - PLoS ONE 11: e0156831, 14 pp. Go to original source...
    18. Goergen G., Kumar P.L., Sankung S.B., Togola A. & Tamò M. 2016: First report of outbreaks of the fall armyworm Spodo­ptera frugiperda (J.E. Smith) (Lepidoptera, Noctuidae), a new alien invasive pest in West and Central Africa. - PLoS ONE 11: e0165632, 9 pp. Go to original source...
    19. Goubault M., Fourrier J., Krespi L., Poinsot D. & Cortesero A.M. 2004: Selection strategies of parasitized hosts in a generalist parasitoid depend on patch quality but also on host size. - J. Insect Behav. 17: 99-113. Go to original source...
    20. Gu H., Wang Q. & Dorn S. 2003: Superparasitism in Cotesia glomerata: Response of hosts and consequences for parasitoids. - Ecol. Entomol. 28: 422-431. Go to original source...
    21. Hajek A.E. 2012: Insect parasitoids: attack by aliens. In Natural Enemies An Introduction to Biological Control. Cambridge University Press, pp. 145-169.
    22. Hart J.T., Jonge de J., Colle C., Dicke M., Van Lenteren J. C. & Ramakers P.M.J. 1978: Host selection, host discrimination and functional response of Aphidius matricariae Haliday (Hymenoptera: Braconidae), a parasite of the green peach aphid, Myzus persicae (Sulz.). - Med. Fac. Landbouww. Rijksuniv. Gent 43: 441-453.
    23. Harvey J.A., Harvey I.F. & Thompson D.J. 1993: The effect of superparasitism on development of the solitary parasitoid wasp, Venturia canescens (Hymenoptera: Ichneumonidae). - Ecol. Entomol. 18: 203-208. Go to original source...
    24. Hubbard S.F., Marris G., Reynolds A. & Rowe G.W. 1987: Adaptive patterns in the avoidance of superparasitism by solitary parasitic wasps. - J. Anim. Ecol. 56: 387-401. Go to original source...
    25. King B.H. & Napoleon M.E. 2006: Using effects of parasitoid size on fitness to test a host quality model assumption with the parasitoid wasp Spalangia endius. - Can. J. Zool. 84: 1678-1682. Go to original source...
    26. Li H., Jiang S.-S., Zhang H.-W., Geng T., Wyckhuys K.A.G. & Wu K. 2021: Two-way predation between immature stages of the hoverfly Eupeodes corollae and the invasive fall armyworm (Spodoptera frugiperda J.E. Smith). - J. Integr. Agric. 20: 829-839. Go to original source...
    27. Liu P.C., Zhao B., Cao D.D. & Wei J.R. 2021: Oviposition decisions in an endoparasitoid under self-superparasitism conditions. - J. Asia-Pacific Entomol. 24: 443-447. Go to original source...
    28. Luna M.G., Desneux N. & Schneider M.I. 2016: Encapsulation and self-superparasitism of Pseudapanteles dignus (Muesebeck) (Hymenoptera: Braconidae), a parasitoid of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). - PLoS ONE 11: e0163196, 10 pp. Go to original source...
    29. Mackauer M. & Chow A. 2016: Females of the parasitoid wasp, Dendrocerus carpenteri (Hymenoptera: Megaspilidae), adjust offspring sex allocation when competing for hosts. - Eur. J. Entomol. 113: 542-550. Go to original source...
    30. Otim M.H., Aropet S.A., Opio M., Kanyesigye D., Opolot H.N. & Tay W.T. 2021: Parasitoid distribution and parasitism of the fall armyworm Spodoptera frugiperda (Lepidoptera: Noctuidae) in different maize producing regions of Uganda. - Insects 12: 128, 18 pp. Go to original source...
    31. Ozkan C. 2006: Effect of host diet on the development of the solitary egg-larval parasitoid Chelonus oculator in superparasitized Ephestia kuehniella. - Phytoparasitica 34: 338-346. Go to original source...
    32. Plantegenest M., Outreman Y., Goubault M. & Wajnberg E. 2004: Parasitoids flip a coin before deciding to superparasitize. - J. Anim. Ecol. 73: 802-806. Go to original source...
    33. Potting R.P.J., Snellen H.M. & Vet L.E.M. 1997: Fitness consequences of superparasitism and mechanism of host discrimination in the stemborer parasitoid Cotesia flavipes. - Entomol. Exp. Appl. 82: 341-348. Go to original source...
    34. Ruschioni S., Van Loon J.J.A., Smid H.M. & Van Lenteren J.C. 2015: Insects can count: Sensory basis of host discrimination in parasitoid wasps revealed. - PLoS ONE 10: e0138045, 11 pp. Go to original source...
    35. 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. Go to original source...
    36. Song H., Meng L. & Li B. 2017: Fitness consequences of body-size-dependent parasitism in a gregarious parasitoid attacking the 7-spot ladybird, Coccinella septempunctata (Coleoptera: Coccinellidae). - Biol. Contr. 113: 73-79. Go to original source...
    37. Stelinski L.L., Oakleaf R. & Rodriguez-Saona C. 2007: Oviposition-deterring pheromone deposited on blueberry fruit by the parasitic wasp, Diachasma alloeum. - Behaviour 144: 429-445. Go to original source...
    38. Tunca H. & Kilinçer N. 2009: Effect of superparasitism on the development of the solitary parasitoid Chelonus oculator Panzer (Hymenoptera: Braconidae). - Turkish J. Agric. For. 33: 463-468. Go to original source...
    39. Tunca H., Buradino M., Colombel E.A. & Tabone E. 2016: Tendency and consequences of superparasitism for the parasitoid Ooencyrtus pityocampae (Hymenoptera: Encyrtidae) in parasitizing a new laboratory host, Philosamia ricini (Lepido­ptera: Saturniidae). - Eur. J. Entomol. 113: 51-59. Go to original source...
    40. Ugur A. 1986: The effect of superparasitism on development of Pimpla turionellae (L.) (Hymenoptera: Ichneumonidae). - Turk. Entomol. Derg. 20: 51-58.
    41. Van Alphen J.J.M. 1988: Patch-time allocation by insect parasitoids: Superparasitism and aggregation. In de Jong G. (ed.): Population Genetics and Evolution. Springer, Berlin, Heidelberg, pp. 215-221. Go to original source...
    42. Van Alphen J.J.M. & Visser M.E. 1990: Superparasitism as an adaptive strategy for insect parasitoids. - Annu. Rev. Entomol. 35: 59-79. Go to original source...
    43. Van Baaren J. & Boivin G. 1988: Learning affects host discrimination behavior in a parasitoid wasp. - Behav. Ecol. Sociobiol. 42: 9-16. Go to original source...
    44. Van Baaren J., Boivin G. & Nénon J.P. 1995: Intraspecific hyperparasitism in a primary hymenopteran parasitoid. - Behav. Ecol. Sociobiol. 36: 237-242. Go to original source...
    45. Van Dijken M.J. & Waage J.K. 1987: Self and conspecific superparasitism by the egg parasitoid Trichogramma evanescens. - Entomol. Exp. Appl. 43: 183-192. Go to original source...
    46. Van Lenteren J.C. 1976: The development of host discrimination and the prevention of superparasitism in the parasite Pseudeucoila bochei Weld (Hym: Cynipidae). - Neth. J. Zool. 26: 1-83. Go to original source...
    47. Van Lenteren J.C. 1981: Host discrimination by parasitoids. In Nordlung D.A., Jones R.L. & Lewis W.J. (eds): Semiochemicals: Their Role in Pest Control. John Wiley, New York, pp. 153-173.
    48. Waage J.K. 1986: Family planning in parasitoids: Adaptive patterns of progeny and sex allocation. In Waage J.K. & Greathead D. (eds): Insect Parasitoids. 13th Symposium of the Royal Entomological Society of London. Academic Press, Boston, MA, pp. 63-95.
    49. White J.A. & Andow D.A. 2008: Benefits of self-superparasitism in a polyembryonic parasitoid. - Biol. Contr. 46: 133-139. Go to original source...

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