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Interaction between the aphid parasitoid Lysiphlebus testaceipes (Hymenoptera: Aphidiidae) and its hyperparasitoid Syrphophagus africanus (Hymenoptera: Encyrtidae)

Published online by Cambridge University Press:  21 March 2012

Komla Kyky Ganyo
Affiliation:
International Institute of Tropical Agriculture (Benin Station), 08 BP 0932 Tripostal, Cotonou, Benin Ecole Supérieure d'Agronomie, Université de Lomé, BP 1515, Lomé, Togo
Agbeko Kodjo Tounou
Affiliation:
Ecole Supérieure d'Agronomie, Université de Lomé, BP 1515, Lomé, Togo
Cyriaque Agboton
Affiliation:
International Institute of Tropical Agriculture (Benin Station), 08 BP 0932 Tripostal, Cotonou, Benin
Elie Ayitondji Dannon
Affiliation:
International Institute of Tropical Agriculture (Benin Station), 08 BP 0932 Tripostal, Cotonou, Benin
Barry Robert Pittendrigh
Affiliation:
Department of Entomology, University of Illinois at Urbana-Champaign, Urbana, IL61801, USA
Manuele Tamò*
Affiliation:
International Institute of Tropical Agriculture (Benin Station), 08 BP 0932 Tripostal, Cotonou, Benin
*
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Abstract

The interactions between the cowpea aphid Aphis craccivora Koch, its parasitoid Lysiphlebus testaceipes Cresson and hyperparasitoid Syrphophagus africanus Gahan were assessed in the laboratory. Host age preference for hyperparasitism was evaluated using parasitized aphids of different ages (i.e. 1, 2, 3, 4, 5 and 6 days old and mixed ages). We studied the influence of the hyperparasitoid on the parasitism efficiency of L. testaceipes, the effect of host age on some biological parameters of S. africanus, and its hyperparasitism based on aggregated or isolated mummies. The presence of S. africanus significantly affected aphid parasitism by L. testaceipes (21.2 ± 3.6 vs 36.6 ± 4.5%). Except for 1-day-old hosts, S. africanus successfully parasitized hosts of all tested ages, with preference for newly formed mummies (39.16 ± 3.31% parasitism in 5-day-old hosts). The development time of immature stages of the S. africanus progeny was significantly affected by host age. The sex ratio of the hyperparasitoid progeny was largely female biased and did not vary with host age. Syrphophagus africanus females from live parasitized aphids produced more offspring (36.55 ± 6.28 vs 25.00 ± 7.16) and lived longer (21.09 ± 1.57 vs 10.88 ± 2.31 days) than those from mummy hosts. Hyperparasitism rates were higher on aggregated mummies than on dispersed ones (36.00 ± 2.86 vs 20.66 ± 4.00%).

Type
Research Paper
Copyright
Copyright © ICIPE 2012

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References

Agboka, K., Tounou, A. K., Al-Moaalem, R., Poehling, H. M., Raupach, K. and Borgemeister, C. (2004) Life-table study of Anagrus atomus, an egg parasitoid of the green leafhopper Empoasca decipiens, at four different temperatures. Biocontrol 49, 261275.CrossRefGoogle Scholar
Ayal, Y. and Green, R. F. (1993) Optimal egg distribution among host patches for parasitoids subject to attack by hyperparasitoids. The American Naturalist 141, 120138.CrossRefGoogle ScholarPubMed
Barahoei, H., Massoud, S. and Mehrparvar, M. (2011) Morphometric differentiation of five biotypes of Lysiphlebus fabarum (Marshall) (Hymenoptera: Braconidae: Aphidiinae) in Iran. Zootaxa 2745, 4352.CrossRefGoogle Scholar
Barbosa, P. and Frongillo, E. A. (1979) Host parasitoid interactions affecting reproduction and oviposition by Brachymeria intermedia (Hymenoptera: Chalcididae). Entomophaga 24, 139143.CrossRefGoogle Scholar
Barbosa, P., Martinat, P. and Bennett, R. (1986) Consequences of maternal age and host deprivation on the production and development of Brachymeria intermedia (Nees) and the mortality of its gypsy moth (Lymantria dispar) host. Zeitschrift fuer Angewandte Entomologie 1001, 215223.Google Scholar
Boenisch, A., Petersen, G. and Wyss, U. (1997) Influence of the hyperparasitoid Dendrocerus carpenteri on the reproduction of the grain aphid Sitobion avenae. Ecological Entomology 22, 16.CrossRefGoogle Scholar
Bokonon-Ganta, A. H., Neuenschwander, P., van Alphen, J. J. M. and Vos, M. (1995) Host stage selection and sex allocation by Anagyrus mangicola (Hymenoptera: Encyrtidae), a parasitoid of mango mealybug, Rastrococcus invadens (Homoptera: Pseudococcidae). Biological Control 5, 479486.CrossRefGoogle Scholar
Briggs, C. J. (1993) Competition among parasitoid species on a stage-structured host and its effect on host suppression. The American Naturalist 141, 372397.CrossRefGoogle Scholar
Brodeur, J. (2000) Host specificity and trophic relationships of hyperparasitoids, pp. 139162. In Parasite Population Biology (edited by Hochberg, M. and Ives, A. R.). Princeton University Press, Princeton, New Jersey.Google Scholar
Brodeur, J. and Rosenheim, J. A. (2000) Intraguild interactions in aphid parasitoids. Entomologia Experimentalis et Applicata 97, 93108.CrossRefGoogle Scholar
Brodeur, J., Geervliet, J. B. F. and Vet, L. E. M. (1996) The role of host species, age and defensive behaviour on ovipositional decisions in a solitary specialist and a gregarious generalist parasitoid (Cotesia species). Entomologia Experimentalis et Applicata 81, 125132.CrossRefGoogle Scholar
Buitenhuis, R. (2004) A comparative study of the life history and foraging behaviour of aphid hyperparasitoids. PhD dissertation, Université Laval, Québec. 172 pp..Google Scholar
Chen, K. R., Xu, Z. Y., Zhang, Z. Y., Fang, X. P. and Yan, L. Y. (1999) Biological characters and sequence analysis of coat protein gene of Chinese strains of peanut stripe virus (PStV). Chinese Journal of Oil Crop Sciences 21, 5559.Google Scholar
CIRAD (2007) Les criquets ravageurs: Dynamique des populations. Available at: http://locust.cirad.fr/tout_savoir/dynpop/dynampop (accessed December 2009).Google Scholar
Coceano, P. G., Peressini, S. and Bianchi, G. L. (1998) The role of winged aphid species in the natural transmission of soybean mosaic potyvirus to soybean in North-east Italy. Phytopathologia Mediterranea 37, 111118.Google Scholar
Colfer, R. G. and Rosenheim, J. A. (2001) Predation on immature parasitoids and its impact on aphid suppression. Oecologia 126, 292304.CrossRefGoogle ScholarPubMed
Couture, I. (1997) Susceptibilité des parasitoïdes Aphidius nigripes (Ashmead) et Praon simulans (Provancher) à l'hyperparasitoïde Asaphes suspensus. Mémoire MSc, Université Laval, Canada. 78 pp..Google Scholar
Dogramaci, M., Mayo, Z. B., Wright, R. J. and Reese, J. C. (2004) Tritrophic interaction of parasitoid Lysiphlebus testaceipes (Hymenoptera: Aphidiidae), greenbug, Schizaphis granimum (Homoptera: Aphididae) and greenbug resistant sorghum hybrids. Journal of Economic Entomology 98, 202205.CrossRefGoogle Scholar
Gerling, D., Roitberg, B. D. and Mackauer, M. (1990) Instar-specific defense of the pea aphid, Acyrthosiphon pisum: influence on oviposition success of the parasite Aphelinus asychis (Hymenoptera: Aphelinidae). Journal of Insect Behavior 3, 501514.CrossRefGoogle Scholar
Godfray, H. C. J. (1994) Parasitoids: Behavioral and Evolutionary Ecology. Princeton University Press, Princeton, New Jersey. 473 pp.CrossRefGoogle Scholar
Goubault, M., Krespi, L., Boivin, G., Poinsot, D., Nenon, J.-P. and Cortesero, A. M. (2004) Intraspecific variations in host discrimination behavior in the pupal parasitoid Pachycrepoideus vindemmiae Rondani (Hymenoptera: Pteromalidae). Environmental Entomology 3, 362369.CrossRefGoogle Scholar
Grasswitz, T. R. and Reese, B. D. (1998) Biology and host selection behaviour of the aphid hyperparasitoid Alloxysta victrix in association with the primary parasitoid Aphidius colemani and the host aphid Myzus persicae. Biocontrol 43, 261271.CrossRefGoogle Scholar
Gutierrez, A. P. and van den Bosch, R. (1970) Studies on host selection and host specificity of the aphid hyperparasite Charips victrix (Hymenoptera: Cynipidae): 2. The bionomics of Charips victrix. Annals of the Entomological Society of America 63, 13551360.CrossRefGoogle Scholar
Harvey, J. A. and Thompson, D. J. (1995) Host behaviour and its influence on foraging and acceptance by solitary parasitoid wasps. Entomophaga 40, 193210.CrossRefGoogle Scholar
Harvey, J. A., Bezember, T. M., Elzinga, J. A. and Strand, M. R. (2004) Development of the solitary endoparasitoid Microplitis demolitor: host quality does not increase with host age and size. Ecological Entomology 29, 3543.CrossRefGoogle Scholar
Heng-Moss, T., Baxendale, F. and Riordan, T. (2001) Interactions between the parasitoid Rhopus nigroclavatus (Ashmead) (Hymenoptera: Encyrtidae) and its mealybug hosts Tridiscus sporoboli (Cockerell) and Trionymus sp. (Homoptera: Pseudococcidae). Biological Control 22, 201206.CrossRefGoogle Scholar
Hoffer, A. and Starý, P. (1970) A review of biologies of Palearctic Aphidencyrtus species (Hym., Chalcidoidea, Encyrtidae). Studia Entomologica Forestalia 1, 8195.Google Scholar
Hofsvang, B. T. and Hagvar, E. B. (1991) Aphid parasitoids (Hymenoptera, Aphidiidae): biology, host selection and use in biological control. Biocontrol News and Information 12, 1341.Google Scholar
Höller, C., Borgemeister, C., Haardt, H. and Powell, W. (1993) The relationship between primary parasitoids and hyperparasitoids of cereal aphids: an analysis of field data. Journal of Animal Ecology 62, 1221.CrossRefGoogle Scholar
Horn, D. J. (1989) Secondary parasitism and population dynamics of aphid parasitoids (Hymenoptera: Aphidiidae). Journal of the Kansas Entomological Society 62, 203210.Google Scholar
Hufbauer, R. A. and Via, S. (1999) Evolution of an aphid–parasitoid interaction: variation in resistance to parasitism among aphid populations specialized on different plants. Evolution 53, 14351445.Google ScholarPubMed
Islam, W. (1994) Effect of host age on rate of development of Dinarmus basalis Rond. (Hymenoptera: Pteromalidae). Journal of Applied Entomology 118, 392398.CrossRefGoogle Scholar
Jackai, L. E. N. and Daoust, R. A. (1986) Insect pests of cowpeas. Annual Review of Entomology 31, 95119.CrossRefGoogle Scholar
Jones, D. B., Giles, K. L., Berberet, R. C., Royer, T. A., Elliott, N. C. and Payton, M. E. (2003) Functional responses of an introduced parasitoid and an indigenous parasitoid on greenbug at four temperatures. Environmental Entomology 32, 425432.CrossRefGoogle Scholar
Kaneko, S. (2002) Aphid-attending ants increase the number of emerging adults of the aphid's primary parasitoid and hyperparasitoids by repelling intraguild predators. Entomological Science 5, 131146.Google Scholar
Kanuck, M. J. and Sullivan, D. J. (1992) Ovipositional behaviour and larval development of Aphidencyrtus aphidivorus (Hymenoptera: Encyrtidae), an aphid hyperparasitoid. Journal of New York Entomology Society 100, 527532.Google Scholar
Karungi, J., Adipala, E., Ogenga-Latigo, M. W., Kyamanywa, S., Oyobo, N. and Jackai, L. E. N. (2000) Pest management in cowpea. Part 2. Integrating planting time, plant density and insecticide application for management of cowpea field insect pests in eastern Uganda. Crop Protection 19, 237245.CrossRefGoogle Scholar
Lauzière, I., Brodeur, J. and Perez-Lachaud, G. (2001) Host stage selection and suitability in Cephalonomia stephanoderis Betrem (Hymenoptera: Bethylidae), a parasitoid of the coffee berry borer. Biological Control 21, 128133.CrossRefGoogle Scholar
Liepert, C. and Dettner, K. (1993) Recognition of aphid parasitoids by honeydew-collecting ants: the role of cuticular lipids in a chemical mimicry system. Journal of Chemical Ecology 19, 21432153.CrossRefGoogle Scholar
Liepert, C. and Dettner, K. (1996) Role of cuticular hydrocarbons of aphid parasitoids in their relationship to aphid-attending ants. Journal of Chemical Ecology 22, 695707.CrossRefGoogle ScholarPubMed
Luck, R. F., Messenger, P. S. and Barbieri, J. (1981) The influence of hyperparasitism on the performance of biological control agents, pp. 3443. In The Role of Hyperparasitism in Biological Control: A Symposium (edited by Rosen, D.). Division of Agricultural Sciences, University of California, Berkeley, California.Google Scholar
Mackauer, M. and Völkl, W. (1993) Regulation of aphid populations by aphidiid wasps: does parasitoid foraging behaviour or hyperparasitism limit impact? Oecologia 94, 339350.CrossRefGoogle ScholarPubMed
Mackauer, M. and Völkl, W. (2005) Sex ratio shift caused by hyperparasitism in the solitary parasitoid Lysiphlebus hirticornis (Hymenoptera: Braconidae: Aphidiidae). European Journal of Entomology 102, 475481.CrossRefGoogle Scholar
Matin, S. B., Sahragard, A. and Rasoolian, G. (2009) Some biological parameters of Lysiphlebus fabarum (Hymenoptera: Aphidiidae), a parasitoid of Aphis fabae (Homoptera: Aphidiidae) under labaratory conditions. Munis Entomology and Zoology 4, 193200.Google Scholar
May, R. M. and Hassell, M. P. (1981) The dynamics of multiparasitoid–host interactions. The American Naturalist 117, 234261.CrossRefGoogle Scholar
Mertins, J. W. (1985) Hyperparasitoids from pea aphid mummies, Acyrthosiphon pisum (Homoptera: Aphididae), in North America. Annals of the Entomological Society of America 78, 186195.CrossRefGoogle Scholar
Messing, R. H. and Klungness, L. M. (2001) A two-year survey of the melon aphid, Aphis gossypii Glover, on crop plants in Hawaii. Proceedings of the Hawaiian Entomological Society 35, 91101.Google Scholar
Müller, C. B., Adriaanse, I. C. T., Belshaw, R. and Godfray, H. C. J. (1999) The structure of aphid–parasitoid community. Journal of Animal Ecology 68, 346370.CrossRefGoogle Scholar
Muratori, F., Le Ralec, A., Lognay, G. and Hance, T. (2006) Epicuticular factors involved in host recognition for the aphid parasitoid Aphidius rhopalosiphi. Journal of Chemical Ecology 32, 579593.CrossRefGoogle ScholarPubMed
Nufio, C. R. and Papaj, D. R. (2001) Host marking behavior in phytophagous insects and parasitoids. Entomologia Experimentalis et Applicata 99, 273293.CrossRefGoogle Scholar
Obopile, M. (2006) Economic threshold and injury levels for control of cowpea aphid, Aphis craccivora Linnaeus (Homoptera: Aphididae) on cowpea. African Plant Protection 12, 111115.Google Scholar
Ofuya, I. I. (1987) A population explosion of Aphis craccivora Koch (Homoptera: Aphididae) in cowpeas protected with cypermethrin. FAO Plant Protection Bulletin 35, 7577.Google Scholar
Oliver, K. M., Russell, J. A., Moran, N. and Hunter, M. S. (2003) Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proceedings of the National Academy of Sciences of the USA 100, 18031807.CrossRefGoogle ScholarPubMed
Otto, M. and 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, 353364.CrossRefGoogle ScholarPubMed
Petersen, G. (2000) Signalstoffe in der innerartlichen Kommunikation des Hyperparasitoiden Alloxysta victrix (Hymenoptera: Cynipidae) und ihre Wirkung auf den Primärparasitoiden Aphidius uzbekistanicus und die große Getreideblattlaus Sitobion avenae. PhD thesis, Christian-Albrechts University, Kiel, Germany. 123 pp..Google Scholar
Pettersson, J., Karunaratne, S., Ahmed, E. and Kumar, V. (1998) The cowpea aphid, Aphis craccivora, host plant odours and pheromones. Entomologia Experimentalis et Applicata 88, 177184.CrossRefGoogle Scholar
Pimentel, D., Acquay, H., Biltdnen, M., Rice, P., Silva, M., Nelson, J., Lipner, V., Giordano, S., Horowitz, A. and D'Amore, M. (1992) Environmental and economic costs of pesticide use. BioScience 42, 750760.CrossRefGoogle Scholar
Pons, X., Lumbierres, B., Antoni, R. and Starý, P. (2011) Parasitoid complex of alfalfa aphids in an IPM intensive crop system in northern Catalonia. Journal of Pest Science 84, 437445.CrossRefGoogle Scholar
Rakhshani, E., Talebi, A. A., Kavallieratos, N. G., Rezwani, A., Manzari, S. and Zeljko, T. (2005) Parasitoid complex (Hymenoptera: Braconidae: Aphidiinae) of Aphis craccivora Koch (Hemiptera: Aphidoidea) in Iran. Journal of Pesticide Science 78, 193198.Google Scholar
Rasekh, A., Michaud, J. P., Kharazi-Pakdel, A. and Allahyari, H. (2010) Ant mimicry by an aphid parasitoid, Lysiphlebus fabarum. Journal of Insect Science 10, 126. insectscienceorg/10.126.CrossRefGoogle ScholarPubMed
Rodrigues, S. M. M. and Bueno, V. H. P. (2001) Parasitism rates of Lysiphlebus testaceipes Cresson (Hymenoptera: Aphidiidae) on Schizaphis graminum (Rond.) and Aphis gossypii Glover (Homoptera: Aphididae). Neotropical Entomology 30, 625629.CrossRefGoogle Scholar
Sæthre, M.-G., Godonou, I., Hofsvang, T., Tepa-Yotto, G. T., and James, B. (2011) Aphids and their natural enemies in vegetable agroecosystems in Benin. International Journal of Tropical Insect Science 31, 103117.CrossRefGoogle Scholar
Salt, G. and van den Bosch, R. (1967) The defense reactions of three species of Hypera (Coleoptera, Curculionidae) to an ichneumon wasp. Journal of Invertebrate Pathology 9, 164177.CrossRefGoogle Scholar
Sanders, D. and van Veen, F. J. F. (2010) The impact of an ant–aphid mutualism on the functional composition of the secondary parasitoid community. Ecological Entomology 35, 704710.CrossRefGoogle Scholar
Shi, D. S. (1987) Studies on the parasitoids of cotton aphid. III. Bionomics of Aphidencyrtus aphidivorus (Mayr), a hyperparasitoid of cotton aphid (in Chinese). Contributions from the Shangai Institute of Entomology 6, 3541.Google Scholar
Singh, S. R. and Jackai, L. E. N. (1985) Insect pests of cowpeas in Africa: their life cycle, economic importance, and potential for control, pp. 217231. In Cowpea Research, Production and Utilization (edited by Singh, S. R. and Rachie, K. O.). Wiley, Chichester.Google Scholar
Snyder, W. E. and Ives, A. R. (2003) Interactions between specialist and generalist natural enemies: parasitoids, predators, and pea aphid biocontrol. Ecology 84, 91107.CrossRefGoogle Scholar
Stary, P. (1976) Aphid Parasites (Hymenoptera, Aphidiidae) of the Mediterranean Area. Vol. 86. Springer Science + Business Media, Heidelberg. 95 pp.CrossRefGoogle Scholar
Stephens, D. W. and Krebs, J. R. (1986) Foraging Theory. Princeton University Press, Princeton, New Jersey. 262 pp.Google Scholar
Sullivan, D. J. (1987) Insect hyperparasitism. Annual Review of Entomology 32, 4970.CrossRefGoogle Scholar
Sullivan, D. J. and van den Bosch, R. (1971) Field ecology of the primary parasites and hyperparasites of the potato aphid, Macrosiphum euphorbiae, in the East San Francisco Bay area. Annals of the Entomology Society of America 64, 389394.CrossRefGoogle Scholar
Sullivan, D. J. and Völkl, W. (1999) Hyperparasitism: multitrophic ecology and behaviour. Annual Review of Entomology 44, 291315.CrossRefGoogle Scholar
Tian, X., Sabbagh, G. J., Cuperus, G. W. and Gregory, M. (1996) Evaluating potential environmental impact of insecticide applications in a boll weevil eradication program. American Water Resources Association 32, 10271037.Google Scholar
Ueno, T. (1997) Host age preference and sex allocation in the pupal parasitoid Itoplectis naranyae (Hymenoptera: Ichneumonidae). Annals of the Entomological Society of America 90, 640645.CrossRefGoogle Scholar
Ueno, T. (1999) Host-size-dependent sex ratio in a parasitoid wasp. Researches on Population Ecology 41, 4757.CrossRefGoogle Scholar
van Alphen, J. J. M. and Vet, L. E. M. (1986) An evolutionary approach to host finding, pp. 2361. In Insect Parasitoids (edited by Waage, J. and Greathead, D.). Academic Press, New York.Google Scholar
van Baaren, J., Landry, B. L. and Boivin, G. (1999) Sex allocation and larval competition in a superparasitizing solitary egg parasitoid: competing strategies for an optimal sex ratio. Functional Ecology 13, 6671.CrossRefGoogle Scholar
Van Driesche, R. G. (1983) Meaning of ‘percent parasitism’ in studies of insect parasitoids. Environmental Entomology 12, 16111622.CrossRefGoogle Scholar
van Veen, F. J. F., Rajkumar, A., Müller, C. B. and Godfray, H. C. J. (2001) Increased reproduction by pea aphids in the presence of secondary parasitoids. Ecological Entomology 26, 425429.CrossRefGoogle Scholar
Völkl, W., Kranz, P., Weisser, W. and Hübner, G. (1995) Patch time allocation and resource exploitation in aphid primary parasitoids and hyperparasitoids searching simultaneously within aphid colonies. Journal of Applied Entomology 119, 399404.CrossRefGoogle Scholar
Weisser, W. W., Houston, A. I. and Völkl, W. (1994) Foraging strategies in solitary parasitoids: the trade-off between female and offspring mortality risks. Evolutionary Ecology 8, 587597.CrossRefGoogle Scholar
Wylie, H. G. (1964) Effect of host age on rate of development of Nasonia vitripennis (Walk.) (Hymenoptera: Pteromalidae). The Canadian Entomologist 96, 10231027.CrossRefGoogle Scholar
Wylie, H. G. (1965) Effects of superparasitism on Nasonia vitripennis (Walk.) (Hymenoptera: Pteromalidae). The Canadian Entomologist 97, 326331.CrossRefGoogle Scholar
Zanzana, K. (2008) Parasitisme de Aphidius sp. (Hymenoptera: Braconidae) sur l'aphide du niébé A. craccivora Koch (Homoptera: Aphididae): effets des stades de développement et de la densité. Mémoire de DIT, Université d'Abomey-Calavi, Benin. 62 pp..Google Scholar