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Parasitism of the soybean aphid, Aphis glycines by Binodoxys communis: the role of aphid defensive behaviour and parasitoid reproductive performance

Published online by Cambridge University Press:  25 February 2008

K.A.G. Wyckhuys ,
L. Stone ,
N. Desneux ,
K.A. Hoelmer ,
K.R. Hopper  and
G.E. Heimpel
K.A.G. Wyckhuys*
Affiliation:
Horticulture Research Center, Universidad Jorge Tadeo Lozano, Chia (Cundinamarca), Colombia
L. Stone
Affiliation:
Saint Olaf College, Northfield, Minnesota, USA
N. Desneux
Affiliation:
Department of Entomology, University of Minnesota, St. Paul, USA
K.A. Hoelmer
Affiliation:
Beneficial Insect Introductions Research Unit, USDA-ARS, Newark, Delaware, USA
K.R. Hopper
Affiliation:
Beneficial Insect Introductions Research Unit, USDA-ARS, Newark, Delaware, USA
G.E. Heimpel
Affiliation:
Department of Entomology, University of Minnesota, St. Paul, USA
*
*Author for correspondence Fax: +57 1-8650127 E-mail: kwyckhuys@hotmail.com
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Abstract

The Asian parasitoid, Binodoxys communis (Gahan) (Hymenoptera: Braconidae), is a candidate for release against the exotic soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), in North America. In this study, we examined preferences by B. communis for the different developmental stages of A. glycines and investigated consequences of these preferences for parasitoid fitness. We also determined to what extent aphid defensive behaviours mediate such preferences. We found that B. communis readily attacks and successfully develops in the different A. glycines developmental stages. Binodoxys communis development time gradually increased with aphid developmental stage, and wasps took longest to develop in alates. An average (±SE) of 54.01±0.08% of parasitized A. glycines alatoid nymphs transformed into winged adult aphids prior to mummification. No-choice assays showed a higher proportion of successful attacks for immature apterous A. glycines nymphs compared to adults and alatoid nymphs. Also, choice trials indicated avoidance and lower attack and oviposition of adults and alatoid nymphs. The different aphid stages exhibited a range of defensive behaviours, including body raising, kicking and body rotation. These defenses were employed most effectively by larger aphids. We discuss implications for the potential establishment, spread and biological control efficacy of A. glycines by B. communis in the event that it is released in North America.

Keywords

biological controlhost qualityhost selectionkoinobiont parasitoidsfitnesslife historyphoresy
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 98 , Issue 4 , August 2008 , pp. 361 - 370
Copyright
Copyright © 2008 Cambridge University Press

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References

Battaglia, D., Pennacchio, F., Romano, A. & Tranfaglia, A. (1995) The role of physical cues in the regulation of host recognition and acceptance behavior of Aphidius ervi Haliday (Hymenoptera: Braconidae). Journal of Insect Behavior 8, 739–750.CrossRefGoogle Scholar
Chau, A. & Mackauer, M. (1997) Dropping of pea aphids from feeding site: a consequence of parasitism by the wasp, Monoctonus paulensis. Entomologia Experimentalis et Applicata 83, 247–252.CrossRefGoogle Scholar
Chau, A. & Mackauer, M. (2000) Host-instar selection in the aphid parasitoid Monoctonus paulensis (Hymenoptera: Braconidae, Aphidiinae): a preference for small aphids. European Journal of Entomology 97, 347–353.CrossRefGoogle Scholar
Chau, A. & Mackauer, M. (2001) Host-instar selection in the aphid parasitoid Monoctonus paulensis (Hymenoptera: Braconidae, Aphidiinae): assessing costs and benefits. Canadian Entomologist 133, 549–564.CrossRefGoogle Scholar
Christiansen-Weniger, P. & Hardie, J. (2000) The influence of parasitism on wing development in male and female pea aphids. Journal of Insect Physiology 46, 861–867.CrossRefGoogle ScholarPubMed
Colinet, H., Salin, C., Boivin, G. & Hance, Th. (2005) Host age and fitness-related traits in a koinobiont aphid parasitoid. Ecological Entomology 30, 473–479.CrossRefGoogle Scholar
De Farias, A.M.I. & Hopper, K.R. (1999) Oviposition behavior of Aphelinus asychis and Aphidius matricariae and defense behavior of their host Diuraphis noxia. Environmental Entomology 28, 858–862.CrossRefGoogle Scholar
Demmon, A.S., Nelson, H.J., Ryan, P.J., Ives, A.R. & Snyder, W.E. (2004) Aphidius ervi (Hymenoptera: Braconidae) increases its adult size by disrupting host wing development. Environmental Entomology 33, 1523–1527.CrossRefGoogle Scholar
Desneux, N., Wajnberg, E., Fauverge, X., Privet, S. & Kaiser, L. (2004) Oviposition behavior and patch-time allocation in two aphid parasitoids exposed to deltamethrin residues. Entomologia Experimental et Applicata 112, 227–235.CrossRefGoogle Scholar
Dixon, A.F.G. (1998) Aphid Ecology. 288 pp. London, UK, Chapman & Hall.Google Scholar
Faul, F., Erdfelder, E., Lang, A.-G. & Buchner, A. (2007). G*Power 3: A flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behavior Research Methods 39, 175–191.CrossRefGoogle Scholar
Gerling, D., Roitberg, B.D. & 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, 501–514.CrossRefGoogle Scholar
Godfray, H.C.J. (1994) Parasitoids: Behavioral and Evolutionary Ecology. 488 pp. Princeton, NJ, USA, Princeton University Press.CrossRefGoogle Scholar
Hågvar, E.B. & Hofsvang, T. (1991) Aphid parasitoids (Hymenoptera: Aphidiidae): biology, host selection and use in biological control. Biocontrol News and Information 12, 13–41.Google Scholar
Harvey, J.A. (2005) Factors affecting the evolution of development strategies in parasitoid wasps: the importance of functional constraints and incorporating complexity. Entomologia Experimentalis et Applicata 117, 1–13.CrossRefGoogle Scholar
Heimpel, G.E., Ragsdale, D.W., Venette, R., Hopper, K.R., O'Neil, R.J., Rutledge, C.E. & Wu, Z. (2004) Prospects for importation biological control of the soybean aphid: anticipating potential costs and benefits. Annals of the Entomological Society of America 97, 249–258.CrossRefGoogle Scholar
Henry, L.M., Gillespie, D.R. & Roitberg, B.D. (2005) Does mother really know best? Oviposition preference reduces reproductive performance in the generalist parasitoid Aphidius ervi. Entomologia Experimentalis et Applicata 116, 167–174.CrossRefGoogle Scholar
Hight, S.C., Eikenbary, R.D., Miller, R.J. & Starks, K.J. (1972) The greenbug and Lysiphlebus testaceipes. Environmental Entomology 1, 205–209.CrossRefGoogle Scholar
Hodgson, E.W., Venette, R.C., Abrahamson, M. & Ragsdale, D.W. (2005) Alate production of soybean aphid (Homoptera: Aphididae) in Minnesota. Environmental Entomology 34, 1456–1463.CrossRefGoogle Scholar
Hoelmer, K.A. & Kirk, A.A. (2005) Selecting arthropod biological control agents against arthropod pests: can the science be improved to decrease the risk of releasing ineffective agents? Biological Control 34, 255–264.CrossRefGoogle Scholar
Hopper, K.R. (1986) Preference, acceptance and fitness components of Microplitis croceipes (Hymenoptera: Braconidae) attacking various instars of Heliothis virescens (Lepidoptera: Noctuidae). Environmental Entomology 15, 274–280.CrossRefGoogle Scholar
Hopper, K.R. & King, E.G. (1984) Preference of Microplitis croceipes (Hymenoptera: Braconidae) for instars and species of Heliothis (Lepidoptera: Noctuidae). Environmental Entomology 13, 1145–1150.CrossRefGoogle Scholar
Hughes, R.D. (1963) Population dynamics of the cabbage aphid, Brevicoryne brassicae (L.). Journal of Animal Ecology 32, 393–424.CrossRefGoogle Scholar
Ives, A.R., Schooler, S.S., Jagar, V.J., Knuteson, S.E., Grbic, M. & Settle, W.H. (1999) Variability and parasitoid foraging efficiency: a case study of pea aphids and Aphidius ervi. American Naturalist 154, 652–673.CrossRefGoogle ScholarPubMed
Jenner, W. & Kuhlmann, U. (2006) Significance of host size for a solitary endoparasitoid: a trade-off between fitness parameters. Basic and Applied Ecology 7, 461–471.CrossRefGoogle Scholar
Kelly, E.O.G. (1917) The green-bug (Toxoptera graminum Rond.) outbreak of 1916. Journal of Economic Entomology 10, 233–248.CrossRefGoogle Scholar
Kouamé, K.L. & Mackauer, M. (1991) Influence of aphid size, age and behaviour on host choice by the parasitoid wasp Ephedrus californicus: a test of host-size models. Oecologia 88, 197–203.CrossRefGoogle ScholarPubMed
Lacoume, S., Bressac, C. & Chevrier, C. (2006) Effect of host size on male fitness in the parasitoid wasp Dinarmus basalis. Journal of Insect Physiology 52, 249–254.CrossRefGoogle ScholarPubMed
Landau, S. & Everitt, B.S. (2004) A Handbook of Statistical Analyses Using SPSS. 354 pp. Boca Raton, FL, USA, Chapman & Hall/CRC Press.Google Scholar
Lawrence, P.O., Baranowski, R.M. & Greany, P.D. (1976) Effect of host age on development of Biosteres longicaudatus, a parasitoid of the Carribean fruitfly, Anastrepha suspense. Florida Entomologist 59, 33–39.CrossRefGoogle Scholar
Le Ralec, A., Curty, C. & Wajnberg, K. (2005) Inter-specific variation in the reactive distance of different aphid-parasitoid associations: analysis from automatic tracking of the walking path. Applied Entomology and Zoology 40, 413–420.CrossRefGoogle Scholar
Lewis, W.J. & Redlinger, L.J. (1969) Suitability of eggs of the almond moth Cadra cautella of various ages for parasitism by Trichogramma evanescens. Annals of the Entomological Society of America 62, 1482–1484.CrossRefGoogle Scholar
Li, B.P. & Mills, N. (2004) The influence of temperature on size as an indicator of host quality for the development of a solitary koinobiont parasitoid. Entomologia Eperimentalis et Applicata 110, 249–256.CrossRefGoogle Scholar
Lin, L.A. & Ives, A.R. (2003) The effect of parasitoid host size preference on host population growth rates: an example of Aphidius colemani and Aphis glycines. Ecological Entomology 28, 542–550.CrossRefGoogle Scholar
Liu, J., Wu, K.M., Hopper, K.R. & Zhao, K.J. (2004) Population dynamics of Aphis glycines (Homoptera: Aphididae) and its natural enemies in soybean in northern China. Annals of the Entomological Society of America 97, 235–239.CrossRefGoogle Scholar
Liu, S.S., Morton, R. & Hughes, R.D. (1984) Oviposition preferences of a hymenopterous parasite for certain instars of its aphid host. Entomologia Experimentalis et Applicata 35, 249–254.Google Scholar
Losey, J.E. & Denno, R.F. (1998) The escape response of pea aphids to foliar-foraging predators: factors affecting dropping behaviour. Ecological Entomology 23, 53–61.CrossRefGoogle Scholar
Mackauer, M. (1973) Host selection and host suitability in Aphidius smithi. pp. 20–29in Lowe, A.D. (Ed.) Perspectives in Aphid Biology. Christchurch, New Zealand, Entomological Society of New Zealand.Google Scholar
Mackauer, M., Michaud, J.P. & Völkl, W. (1996) Host choice by aphidiid parasitoids (Hymenoptera: Aphidiidae): host recognition, host quality and host value. Canadian Entomologist 128, 959–980.CrossRefGoogle Scholar
Manly, B.F.J. (1974) A model for certain types of selection experiments. Biometrics 30, 281–294.CrossRefGoogle Scholar
McWilliams, D.A., Berglund, D.R. & Endres, G.J. (2004) Soybean growth and management. North Dakota State University, Extension Publication No. A-1174. http://www.ag.ndsu.edu/pubs/plantsci/rowcrops/a1174/a1174w.htm. Accessed on March 2, 2007.Google Scholar
Murdoch, W.W., Nisbet, R.M., Blythe, S.P., Gurney, W.S.C. & Reeve, J.D. (1987) An invulnerable age class and stability in delay-differential parasitoid-host models. American Naturalist 129, 263–282.CrossRefGoogle Scholar
Murdoch, W.W., Briggs, C.J. & Nisbet, R.M. (2003) Consumer-Resource Dynamics. Monographs in Population Biology. 456 pp. Princeton, NJ, USA, Princeton University Press.Google Scholar
Nechols, J.R. & Kikuchi, R.S. (1985) Host selection of the spherical mealybug (Homoptera: Pseudococidae) by Anagyrus indicus (Hymenoptera: Encyrtidae): influence of host age on parasitoid oviposition, development, sex ratio and survival. Environmental Entomology 14, 32–37.CrossRefGoogle Scholar
Nelson, E.H. & Rosenheim, J.A. (2005) Encounters between aphids and their predators: the relative frequencies of disturbance and consumption. Entomologia Experimentalis et Applicata 118, 211–219.CrossRefGoogle Scholar
Perdikis, D.C., Lykouressis, D.R., Garantonakis, N.G. & Iatrou, S.A. (2004) Instar preference and parasitization of Aphis gossypii and Myzus persicae (Hemiptera: Aphididae) by the parasitoid Aphidius colemani (Hymenoptera: Aphididae). European Journal of Entomology 101, 333–336.CrossRefGoogle Scholar
Ragsdale, D.W., Voegtlin, D.J. & O'Neil, R.J. (2004) Soybean aphid biology in North America. Annals of the Entomological Society of America 97, 204–208.CrossRefGoogle Scholar
Rakhshani, E., Talebim, A.A., Kavallieratos, N. & Fathipour, Y. (2004) Host stage preference, juvenile mortality and functional response of Trioxys pallidus. Biologia 59, 197–203.Google Scholar
Rauwald, K.S. & Ives, A.R. (2001) Biological control in disturbed agricultural systems and the rapid recovery of parasitoid populations. Ecological Applications 11, 1224–1234.CrossRefGoogle Scholar
Rivero, A. (2000) The relationship between host selection behaviour and offspring fitness in a koinobiont parasitoid. Ecological Entomology 25, 467–472.CrossRefGoogle Scholar
Rogers, C.E., Jackson, H.B., Eikenbary, R.D. & Starks, K.J. (1972) Host-parasitoid interaction of Aphis helianthi on sunflowers with introduced Aphelinus asychis, Ephedrus plagiator, and Praon gallicum, and native Aphelinus nigritus and Lysiphlebus testaceipes. Annals of the Entomological Society of America 65, 38–41.CrossRefGoogle Scholar
Roitberg, B.D., Boivin, G. & Vet, L.E.M. (2001) Fitness, parasitoids and biological control: an opinion. Canadian Entomologist 133, 429–438.CrossRefGoogle Scholar
Sequeira, R. & Mackauer, M. (1987) Host instar preference of the aphid parasite Praon pequodorum (Hymenoptera: Aphidiidae). Entomologia Generalis 12, 259–265.CrossRefGoogle Scholar
Sequeira, R. & Mackauer, M. (1992a) Covariance of adult size and development time in the parasitoid wasps Aphidius ervi in relation to its host, Acyrthosiphum pisum. Evolutionary Ecology 6, 34–44.CrossRefGoogle Scholar
Sequeira, R. & Mackauer, M. (1992b) Nutritional ecology of an insect host parasitoid association – the pea aphid Aphidius ervi system. Ecology 73, 183–189.CrossRefGoogle Scholar
Sequeira, R. & Mackauer, M. (1993) The nutritional ecology of a parasitoid wasp, Ephedrus californicus Baker (Hymenoptera: Aphidiidae). Canadian Entomologist 125, 423–430.CrossRefGoogle Scholar
Sharmila, P. & Rajendra, S. (1999) Host size induced variation in progeny sex ratio of an aphid parasitoid Lysiphlebia myrzai. Entomologia Experimentalis et Applicata 90, 61–67.Google Scholar
Stadler, B., Weisser, W.W. & Houston, A.I. (1994) Defense reactions in aphids – the influence of state and future reproductive success. Journal of Animal Ecology 63, 419–430.CrossRefGoogle Scholar
Villagra, C.A., Ramirez, C.C. & Niemeyer, H. (2002) Anti-predator responses of aphids to parasitoids change as function of aphid physiological state. Animal Behaviour 64, 677–683.CrossRefGoogle Scholar
Vinson, S.B. (1972) Effect of the parasitoid Campoletis sonorensis on the growth of its host, Heliothis virescens. Journal of Insect Physiology 18, 1509–1514.CrossRefGoogle Scholar
Völkl, W. & Mackauer, M. (2000) Oviposition behaviour of aphidiine wasps (Hymenoptera: Braconidae, Aphidiinae): morphological adaptations and evolutionary trends. Canadian Entomologist 132, 197–212.CrossRefGoogle Scholar
Walker, A.M. & Hoy, M.A. (2003) Responses of Lipolexis oregmae (Hymenoptera: Aphidiidae) to different instars of Toxoptera citricida (Homoptera: Aphididae). Journal of Economic Entomology 96, 1685–1692.CrossRefGoogle ScholarPubMed
Wang, X.G. & Liu, S.S. (2002) Effects of host age on the performance of Diadromus collaris, a pupal parasitoid of Plutella xylostella. Biocontrol 47, 293–307.CrossRefGoogle Scholar
Weisser, W.W. (1994) Age-dependent foraging behaviour and host instar preference of the aphid parasitoid Lysiphlebus cardui. Entomologia Experimentalis et Applicata 76, 133–141.CrossRefGoogle Scholar
Weisser, W.W. (1995) Within-patch foraging behaviour of the aphid parasitoid Aphidius funebris: plant architecture, host behaviour and individual variation. Entomologia Experimentalis et Applicata 76, 133–141.CrossRefGoogle Scholar
Wu, Z., Hopper, K.R., O'Neil, R.J., Voegtlin, D.J., Prokrym, D.R. & Heimpel, G. (2004) Reproductive compatibility and genetic variation between two strains of Aphelinus albipodus (Hymenoptera: Aphelinidae), a parasitoid of the soybean aphid, Aphis glycines (Homoptera: Aphididae). Biological Control 31, 311–319.CrossRefGoogle Scholar
Wyckhuys, K.A.G. & Heimpel, G.E. (2007) Response of the soybean aphid parasitoid Binodoxys communis to olfactory cues from target and non-target host-plant complexes. Entomologia Experimentalis et Applicata 123, 149–158.CrossRefGoogle Scholar
Wyckhuys, K.A.G., Koch, R.L. & Heimpel, G.E. (2007a) Physical and ant-mediated refuges from parasitism: implications for non-target effects in biological control. Biological Control 40, 306–313.CrossRefGoogle Scholar
Wyckhuys, K.A.G., Hopper, K.R., Wu, K.M., Straub, C., Gratton, C. & Heimpel, G.E. (2007b) Predicting potential ecological impact of soybean aphid biological control introductions. CABI Biocontrol News and Information 28, 30N–34N.Google Scholar