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A new substitute host and its effects on some biological properties of Ooencyrtus kuvanae

Published online by Cambridge University Press:  22 March 2017

Hilal Tunca ,
Marine Venard ,
Etty-Ambre Colombel  and
Elisabeth Tabone
Hilal Tunca*
Affiliation:
Department of Plant Protection, Faculty of Agriculture, Ankara University, 06110, Ankara Dıskapı, Turkey
Marine Venard
Affiliation:
INRA, UEFM site Villa Thuret, Laboratoire BioContrôle, 90 Chemin Raymond, 06160, Antibes, France
Etty-Ambre Colombel
Affiliation:
INRA, UEFM site Villa Thuret, Laboratoire BioContrôle, 90 Chemin Raymond, 06160, Antibes, France
Elisabeth Tabone
Affiliation:
INRA, UEFM site Villa Thuret, Laboratoire BioContrôle, 90 Chemin Raymond, 06160, Antibes, France
*
*Author for correspondence Phone: +90 312 5961384 Fax: +90 312 3187029 E-mail: htunca@ankara.edu.tr
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Abstract

Lymantia dispar (L.) (Lepidoptera: Lymantriidae), commonly known as the gypsy moth, is a serious forest pest, and beneficial insects are particularly important for reducing its population numbers. Ooencyrtus kuvanae (Howard) (Hymenoptera: Encyrtidae) is an arrhenotokous, solitary egg parasitoid of L. dispar. In this study, we evaluated a new substitute host, Philosamia ricini (Danovan) (Lepidoptera: Saturniidae) for O. kuvanae. We investigated some of the biological effects of O. kuvanae on P. ricini eggs. In this context, the importance of the age of the female parasitoid (1, 3 or 5 days old), host age (1–2 and 3–4 days old) and host number (40, 60 and 80 host eggs) were examined under laboratory conditions (25 ± 1 °C, 65 ± 5% relative humidity and a 16 : 8 h photoperiod [light : dark]). The highest rate of offspring production (89.90%) occurred with 40 (1–2-day-old) host eggs and 5-day-old females. The mean developmental period ranged from 16.5 ± 0.08 days to 18.7 ± 0.08 days. The mean lifespan of the parasitoid was 51.10 ± 1.1 (n = 60) days with bio-honey and 3.92 ± 0.14 (n = 60) days without food. The mean fecundity was 68.88 ± 3.22 offspring/female. Peak adult emergence occurred between 2 and 9 days. The mean oviposition and mean post-oviposition periods of the female parasitoid were 22.76 ± 1.37 days and 13.64 ± 1.40 days, respectively. O. kuvanae was reared for more than ten generations on the eggs of P. ricini. Based on our findings, P. ricini can be used to rear O. kuvanae for the biological control of L. dispar.

Keywords

Lymantia disparPhilosamia riciniOoencyrtus kuvanaebiology
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 107 , Issue 6 , December 2017 , pp. 742 - 748
Copyright
Copyright © Cambridge University Press 2017 

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References

Amalin, D.M., Peña, J.E. & Duncan, R.E. (2005) Effects of host age, female parasitoid age, and host plant on parasitism of Ceratogramma etiennei (Hymenoptera: Trichogrammatidae). Florida Entomologist 88 (1), 77–82.Google Scholar
Aung, K.S.D., Takagi, M. & Ueno, T. (2010) Effect of female's age on the progeny production and sex ratio of Ooencyrtus nezarae, an egg parasitoid of the bean bug Riptortus clavatus. Journal of Faculty Agriculture, Kyushu University 55 (1), 83–85.Google Scholar
Brown, M.W. (1984) Literature review of Ooencyrtus kuvanae (Hym.: Encyrtidae), an egg parasite of Lymantria dispar (Lep.: Lymantriidae). Entomophaga 29 (3), 249–265.Google Scholar
Campan, E. & Benrey, B. (2004) Behavior and performance of a specialist and a generalist parasitoid of bruchids on wild and cultivated beans. Biological Control 30, 220–228.Google Scholar
Consoli, F.L., Parra, J.R.P. & Zucchi, R.A. (2000) Egg Parasitoids in Agroecosystems with Emphasis on Trichogramma. Dordrecht, Heidelberg, London, New York, Springer. 473 pp.Google Scholar
Crossman, S.S. (1925) Two imported egg parasites of the gypsy moth, Anastatus bifasciatus Fonsc. and Schedius kuvanae Howard. Journal of Agricultural Research 30, 643–675.Google Scholar
Da Rocha, L., Kolberg, R., Mendonça, J.R.M.S. & Redaelli, L.R. (2006) Effects of egg age of Spartocera dentiventris (berg) (Hemiptera: Coreidae) on parasitism by Gryon gallardoi (Brethes) (Hymenoptera: Scelionidae). Neotropical Entomology 35, 654–659.Google Scholar
Eliopoulos, P., Stathas, J.G. & Bouras, S.L. (2005) Effects and interactions of temperature, host deprivation and adult feeding on the longevity of the parasitoid Venturia canescens (Hymenoptera: Ichneumonidae). European Journal of Entomology 102 (2): 181–187.Google Scholar
El Sharkawy, M.A.A. (2011) Effect of egg age and fertility on some biological aspects of three Trichogramma species. Egyptian Journal of Agricultural Research 89 (4), 1313–1326.Google Scholar
Fabel, S. (2000) Effects of Lymantria dispar, the Gypsy moth, on broadleaved forests in eastern North America. Restoration and Reclamation Review 6 (6), 1–15.Google Scholar
Fedde, V.H., Fedde, G.F. & Drooz, A.T. (1982) Factitious hosts in insect parasitoid rearings. Entomophaga 27(4), 379–386.Google Scholar
Francisco, J.A. (2001) The effects of egg production on longevity in the parasitoid Mastrus ridibundus. nature.berkeley.edu/classes/es196/projects/.../Francisco.pdf.Google Scholar
Gilbert, F.S. & Jervis, M.A. (1998) Functional, evolutionary and ecological aspects of feeding-related mouthpart specializations in parasitoid flies. Biological Journal of the Linnean Society 63, 495–535.Google Scholar
Godfray, H.C.J. (1994) Parasitoids: Behavioral and Evolutionary Ecology. Princeton, NJ, USA, Princeton University Press.Google Scholar
Gould, J.R., Elkinton, J.S. & Wallner, W.E. (1990) Density-dependent suppression of experimentally created gypsy moth Lymantria dispar (Lepidoptera: Lymantriidae) populations by natural enemies. Journal of Animal Ecology 59, 213–233.Google Scholar
Hagen, K.S. (1986) Ecosystem analysis: plant cultivars (HPR), entomophagous species and food supplements. pp. 151–197 in Boethel, D.J. & Eikenhary, R.D. (Eds) Interactions of Plant Resistance and Parasitoids and Predators of Insects. Chichester/New York, Ellis Horwood/John Wiley & Sons.Google Scholar
Heimpel, G.E. & Collier, T.R. (1996) The evolution of host-feeding behaviour in insect parasitoids. Biological Reviews of the Cambridge Philosophical Society 71, 373–400.Google Scholar
Heimpel, G.E., Rosenheim, J.A. & Kattari, D. (1997) Adult feeding and lifetime reproductive success in the parasitoid Aphytis melinus. Entomologia Experimentalis et Applicata 83, 305–315.Google Scholar
Hérard, F. & Mercadier, G. (1980) Bionomies compares de deux souches (Maroccaine et Américaine) d’ Ooencytus kuvanae (Hym.: Encyrtidae), parasite oophage de Lymantria dispar (Lep.: Lymantriidae). Entomophaga, 25, 129–138.Google Scholar
Hoffmann, M.P., Ode, P.R., Walker, D.L., Gardner, J., van Nouhuys, S. & Shelton, A.M. (2001) Performance of Trichogramma ostriniae (Hymenoptera: Trichogrammatidae) reared on factitious hosts, including the target host, Ostrinia nubilalis (Lepidoptera: Crambidae). Biological Control 21, 1–10.Google Scholar
Hofstetter, R.W. & Raffa, K.F. (1998) Endogenous and exogenous factors affecting the orientation and development of the gypsy moth egg parasite, Ooencyrtus kuvanae. Entomologia Experimentalis et Applicata 88, 123–135.Google Scholar
Höfte, H. & Whiteley, H.R. (1989) Insecticidal crystal proteins of Bacillus thuringiensis. Microbiol Review 53, 242–255.Google Scholar
Humble, L. & Stewart, A.J. (1994) Forest Pest Leaflet: Gypsy Moth Canadian Forest Service. Burnaby, BC, Natural Resources Canada. http://www.pfc.cfs.nrcan.gc.ca/cgi-bin/bstore/catalog_e.pl?catalog=3456, Electronic version accessed on 20060619.Google Scholar
Hunter, M. L. (1999) Maintaining Biodiversity in Forest Ecosystems. Cambridge University Press, Cambridge, UK, ISBN: 0-521-63104-1.Google Scholar
Husni, , Yooichi, K. & Hiroshi, H. (2001) Effects of host pupal age on host preference and host suitability in Brachymeria lasus (Walker) (Hymenoptera: Chalcididae). Applied Entomology and Zoology 36 (1), 97–102.Google Scholar
Islam, W. (1994) Effect of host age on rate of development of Dinarmus basalis (Rond.) (Hymenoptera: Pteromalidae). Journal of Applied Entomology 118, 392–398.Google Scholar
Jacob, H.S. & Evans, E.W. (1998) Effects of sugar spray and aphid honeydew on field populations of the parasitoid Bathyplectes curculionis (Hymenoptera: Ichneumonidae). Environmental Entomology 27, 1563–1568.Google Scholar
Jacob, H.S., Joder, A. & Batchelor, K.L. (2006) Biology of Stethynium sp. (Hymenoptera: Mymaridae), a native parasitoid of an introduced weed biological control agent. Environmental Entomology 35, 630–636.Google Scholar
Jervis, M.A. & Kidd, N.A.C. (1986) Host-feeding strategies in hymenopteran parasitoids. Biological Reviews 61, 395–434.Google Scholar
Jervis, M.A. & Kidd, N.A.C. (1996) Insect Natural: Enemies, Practical Approaches to their Study and Evaluation. Chapman & Hall, London.Google Scholar
Jervis, M.A. & Kidd, N.A.C. (1999) Parasitoid adult nutritional ecology: implications for biological control. pp. 131–151 in Hawkins, B.A. & Cornell, H.V. (Eds) Theoretical Practical Approaches to Biology Control. Cambridge, Cambridge University Press.Google Scholar
Jervis, M.A., Kidd, N.A.C, Fitton, M.G., Huddleston, T. & Dawah, H.A. (1993) Flower-visiting by hymenopteran parasitoids. Journal of Natural History 27, 67–105.Google Scholar
Jervis, M.A., Kidd, N.A.C. & Heimpel, G.E. (1996) Parasitoid adult feeding behavior and biocontrol a review. Biocontrol News and Information 17, 11–26.Google Scholar
Jervis, M.A., Ellers, J. & Harvey, J.A. (2008) Resource acquisition, allocation and utilization in parasitoid reproductive strategies. Annual Review of Entomology 53, 361–385.Google Scholar
Kamay, B.A. (1976) The effects of various constant temperatures on oviposition, sex ratio, and rate of development of the gypsy moth egg parasite, Ooencyrtus kuwanai Howard. M.S. Thesis, Southern Connecticut state College, New Haven, Connecticut. 50 pp.Google Scholar
Keena, M.A., Coté, M.J., Grinberg, P.S. & Wallner, W. E. (2008) World distribution of female flight and genetic variation in Lymantria dispar (Lepidoptera: Lymantriidae). Environmental Entomology 37, 636–649.Google Scholar
King, B.H. (1987) Offspring sex ratios in parasitoid wasps. Quarterly Review of Biology 62, 367–396.Google Scholar
King, B.H. (1998) Host age response in the parasitoid wasp Spalangia cameroni (Hymenoptera: Pteromalidae). Journal of Insect Behavior 11 (1), 103–117.Google Scholar
Lance, D.R. (1983) Host-seeking behavior of the gypsy moth: the influence of polyphagy and highly apparent host plants. pp. 210–224 in Ahmad, S. (Ed.) Herbivorous Insects: Host-Seeking Behavior and Mechanisms. New York, Academic Press.Google Scholar
Liebhold, A.M., Gottschalk, K.W., Muzika, R.M., Montgomery, M.E., Young, R., O'day, K. & Kelly, B. (1995) Suitability of North American tree species to gypsy moth: a summary of field and laboratory tests. General Technical Report NE-211. Randor, PA, USDA Forest Service, 34 pp.Google Scholar
Liu, S., Zhang, G. & Zhang, F. (1998) Factors influencing parasitism of Trichogramma denrolimi on the eggs of the Asian corn borer, Ostrinia furnacalis. BioControl 43, 273–287.Google Scholar
McCullough, D.M. & Bauer, L.S. (2000) Bt: One Option for Gypsy Moth Management. E-2421. East Lansing, MI, Michigan State University Extension, Michigan Agricultural Experiment Station.Google Scholar
McCullough, D.M., Raffa, K.A. & Williamson, R.C. (1999) Natural Enemies of Gypsy Moth: The GoodGuys!. Extension Bulletin E-2700, April, 1–4.Google Scholar
McKenzie, J.D. & Goldman, R. (2005) The Student Guide to Minitab Release 14. Boston, Pearson Education.Google Scholar
MINITAB Release 14. (2004) Statistical Software for Windows.Google Scholar
Mondy, N., Corio-Costet, M.F., Bodin, A., Mandon, N., Vannier, F. & Monge, J.P. (2006) Importance of sterols acquired through host feeding in synovigenic parasitoid oogenesis. Journal of Insect Physiology 52, 897–904.Google Scholar
Monje, J.C., Zebitz, C.P.W. & Ohnesorge, B. (1999) Host and host age preference of Trichogramma galloi and T. pretiosum (Hymenoptera: Trichogrammatidae) reared on different hosts. Journal of Economic Entomology 92, 97–103.Google Scholar
Mrdaković, M., Mataruga, P.V., Ilijin, L., Vlahović, M., Tomanić, J.M., Mirčić, D. & Lazarević, J. (2013) Response of Lymantria dispar (Lepidoptera: Lymantriidae) larvae from differently adapted populations to allelochemical stress: effects of tannic acid. European Journal of Entomology 110 (1), 55–63.Google Scholar
Nechols, J.R., Tracy, J.L. & Vogt, E.A. (1989) Comparative ecological studies of indigenous egg parasitoids (Hymenoptera: Scelionidae; Encyrtidae) of the squash bug, Anasa tristis (Hemiptera: Coreidae). Journal of the Kansas Entomological Society 62, 177–188.Google Scholar
Osanai, M., Okudaira, M., Naito, J., Demura, M. & Asakura, T. (2000) Biosynthesis of L-alanine, a major amino acid of fibroin in Samia cynthia ricini. Insect Biochemistry and Molecular Biology 30, 225–232.Google Scholar
Pak, G.A., Buis, H.C.E.M., Heck, I.C.C. & Hermans, M.L.G. (1986) Behavioural variations among strains of Trichogramma spp.: host-age selection. Entomologia Experimentalis et Applicata 40, 247–258.Google Scholar
Papadopoulou, Sm., Chryssochoides, C. & Katanos, J. (2009). Control of Lymantria dispar L. for eliminating the risk of forage production loss for small ruminants. Nutritional and Foraging Ecology of Sheep and Goats 85, 197–199.Google Scholar
Parra, J.R.P. (1997) Técnicas de criação de Anagasta kuehniella, hospedeiro alternativo para produção de Trichogramma. pp. 121–150 in Parra, J.R.P. & Zucchi, R.A. (Eds) Trichogramma e o controle biológico aplicado, Piracicaba, FEALQ/USP.Google Scholar
Peñaflor, M.F.G.V., De Moraes Sarmento, M.M., Da Silva, C.S.B., Werneburg, A.G. & Bento, J.M.S. (2012) Effect of host egg age on preference, development and arrestment of Telenomus remus (Hymenoptera: Scelionidae). European Journal of Entomology 109 (1), 15–20.Google Scholar
Perera, M.C.D. & Hemachandra, K.S. (2014) Study of longevity, fecundity and oviposition of Trichogrammatoidea bactrae Nagaraja (Hymenoptera: Trichogrammatidae) to facilitate mass rearing. Journal of Tropical Agriculture 25, 502–509.Google Scholar
Peverieri, G.S., Furlan, P., Benassai, D., Caradonna, S., Strong, W.B. & Roversi, P.F. (2013) Host egg age of Leptoglossus occidentalis (Heteroptera: Coreidae) and parasitism by Gryon pennsylvanicum (Hymenoptera: Platygastridae). Journal of Economic Entomology 106 (2), 633–640.Google Scholar
Pizzol, J., Desneux, N., Wajnberg, E. & Thiéry, D. (2012) Parasitoid and host egg ages have independent impact on various biological traits in a Trichogramma species. Journal of Pest Science 85 (4), 489–496.Google Scholar
Pu, T.S., Liu, Z.H. & Zhang, Y.X. (1988) Studies on Trichogramma. Colloq Inra 43, 551–556.Google Scholar
Ramos, J.A.M. & Cate, J.R. (1992) Rate of increase and adult longevity of Catolaccus grandis (Burks) (Hymenoptera: Pteromalidae) in the laboratory of four temperatures. Environmental Entomology 21, 620–627.Google Scholar
Reznik, S.Ya. & Umarova, T.Ya. (1990) The influence of host's age on the selectivity of parasitism and fecundity of Trichogramma. Entomophaga 35, 31–37.Google Scholar
Saito, H. (1998) Purification and characterization of two insecticyanin-type proteins from the larval hemolymph of the Eri-silkworm, Samia cynthia ricini. Biochimica et Biophysica Acta 1380, 141–150.Google Scholar
Sánchez-Bayo, F., van den Brink, P.J. & Mann, R.M. (2011) Ecological Impacts of Toxic Chemicals. ISBN: 978-1-60805-663-7.Google Scholar
SAS Institute (2003) SAS/STAT Version 8.2. Cary, NC, SAS Institute.Google Scholar
Shuker, D.M. & West, S.A. (2004) Information constraints and the precision of adaptation: sex ratio manipulation in wasps. Proceedings of the National Academy of Science USA 101, 10363–10367. (doi:10.1073/pnas.030804101).Google Scholar
Strand, M.R. (1986) The physiological interactions of parasitoids with their hosts and their influence on reproductive strategies. pp. 97–136 in Waage, J. & Greathead, D. (Eds) Insect Parasitoids. London, Academic Press.Google Scholar
Tadic, M.D. & Bincev, B. (1959) Ooencyrtus kuvanae How in Yugoslavia. Zaštita Bilja 10, 51–59.Google Scholar
Takasu, K. & Hirose, Y. (1993) Host acceptance behavior by the host-feeding egg parasitoid, Ooencyrtus nezarae (Hymenoptera: Encyrtidae): host age effects. Annals of the Entomological Society of America 86 (1), 117–121.Google Scholar
Tiradon, M., Bonnet, A., Do Thi, K.H., Colombel, E., Buradino, M. & Tabone, E. (2013) Evaluation of a new biological pest control method against the palm borer, Paysandisia archon using oophagous parasitoids, in Proceedings AFPP of the ‘conférence méditerranéenne sur les ravageurs des palmiers.Google Scholar
Tong, L., Chun-xiang, H. & Guo-cai, Z. (2000) Life circle and bionomics of Lymantria dispar. Journal of Forestry Research 11 (4), 255–258.Google Scholar
Tunca, H., Gökçek, N. & Özkan, C. (2002) Farklı besin çeşitlerinin Chelonus oculator Panzer (Hymenoptera: Braconidae)'un ergin yaşam süresine etkileri. Türkiye 5. Biyolojik Mücadele Kongresi, 4–7 Eylül 2002, Erzurum, s 127–135.Google Scholar
Tunca, H., Colombel, E.A., Sousan, B.T., Buradino, M., Galio, F. & Tabone, E. (2015) Optimal biological parameters for rearing Ooencyrtus pityocampae on the new laboratory host Philosamia ricini. Journal of Applied Entomology 140 (7), 527–535.Google Scholar
Ueno, T. (2005) Effect of host age and size on offspring sex ratio in the pupal parasitoid Pimpla (=Coccygomimus) luctuosa (Hymenoptera: Ichneumonidae). Journal of the Faculty of Agriculture Kyushu University 50, 399–405.Google Scholar
Ueno, T. & Ueno, K. (2007) The effects of host-feeding on synovigenic egg development in an endoparasitic wasp, Itoplectis naranyae. Journal of Insect Science 7, 1–13.Google Scholar
Vinson, S.B. (1985) The behavior of parasitoids. vol. 9, pp. 417–469 in Kerkut, G. A. & Gilbert, L. I. (Eds) Comprehensive Insect Physiology, Biochemistry and Pharmacology. Oxford, Pergamon Press.Google Scholar
Vinson, S.B. (1998) The general host selection behavior of parasitoid Hymenoptera and a comparison of initial strategies utilized by larvaphagous and oophagous species. Biological Control 11, 79–96.Google Scholar
Vinson, S.B. & Iwantsch, G.F. (1980) Host suitability for insect parasitoids. Annual Review of Entomology 25, 397–419.Google Scholar
Wang, J.J., Liu, X.B., Zhang, Y.A., Wen, C. & Wei, J.R. (2013) The reproductive capability of Ooencyrtus kuvanae reared on eggs of the factitious host Antheraea pernyi. Journal of Applied Entomology 138, 267–272.Google Scholar
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.Google Scholar
Wylie, H.G. (1964) Effect of host age on rate of development time of Nasonia vitripennis (Walk) (Hymenoptera: Pteromalidae). Canadian Entomologist 96 (7), 1023–1027.Google Scholar
Yang, Z.Q., Achterberg, C.V., Choi, W.Y. & Marsh, P.M. (2005) First recorded parasitoid from China of Agrilus planipennis: a new species of Spathius (Hymenoptera: Braconidae: Doryctinae). Annals of the Entomological Society of America 98, 636–642.Google Scholar
Zar, J.H. (1999) Biostatistical Analysis. 4th edn. Upper Sadle River, New Jersey, USA, Prentice-Hall.Google Scholar
Zhao, H.Y., Zeng, L., Xu, Y.J., Lu, Y.Y., & Liang, G.W. (2013) Effects of host Age on the Parasitism of Pachycrepoideus vindemmiae (Hymenoptera: Pteromalidae), an Ectoparasitic Pupal Parasitoid of Bactrocera cucurbitae (Diptera: Tephritidae). Florida Entomologist 96 (2), 451–457.Google Scholar
Zhou, Y., Abram, P., Boivin, G. & Brodeur, J. (2014) Increasing host age does not have the expected negative effects on the fitness parameters of an egg parasitoid. Entomologia Experimentalis et Applicata 151 (2), 106–111.Google Scholar