Hostname: page-component-78c5997874-xbtfd Total loading time: 0 Render date: 2024-11-05T05:08:01.018Z Has data issue: false hasContentIssue false
  • English
  • Français

Immature development and adult eclosion of Ufens principalis Owen (Hymenoptera: Trichogrammatidae), an egg parasitoid of Homalodisca spp. (Hemiptera: Cicadellidae) in southern California

Published online by Cambridge University Press:  11 December 2009

A.K. Al-Wahaibi  and
J.G. Morse
A.K. Al-Wahaibi
Affiliation:
Department of Entomology, University of California, 3401 Watkins Drive, Riverside, CA92521, USA
J.G. Morse*
Affiliation:
Department of Entomology, University of California, 3401 Watkins Drive, Riverside, CA92521, USA
*
*Author for correspondence Fax: 951-827-3086 E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The biology of the immature stages and adult eclosion of Ufens principalis Owen, an important parasitoid of Homalodisca eggs in southern California, were studied. The duration of the egg, larval and pupal stages at 26.7°C were 0–1, 7 and 9 days, respectively. Sacciform larvae, which developed gregariously within host eggs, were motile until about five days of age, and then became sessile. Parasitized host eggs changed from whitish and soft when freshly-laid to yellow-orange and hard at five days and older. This change was accompanied by formation of septal walls separating the mature larvae and pupae. The rate of immature development had a strong positive linear relationship (R2=0.853, n=98) with temperatures in the range of 20.0–30.3°C. The theoretical minimum threshold for immature development was 13.5°C, and the required heat units were 241.0 degree-days. Adult eclosion from host eggs occurred mostly (85%) on the first two days of emergence. Although most females emerged during the morning hours (0600–1200 h), males tended to emerge earlier than females with equal emergence during the morning and late night hours (2400–0600 h). The rate of successful adult emergence was high (88%). The ratio of eclosed adults to the number of exit holes was 1.18, indicating that most adults tended to independently cut their exit holes. The number of exit holes had a strong negative relationship (R2=0.711, n=125) with exit hole size, suggesting that larger numbers of developing immatures per host egg result in an overall decrease in adult size.

Keywords

glassy-winged sharpshootersmoke-tree sharpshooterbiological controllife cycledegree-daysgregarious parasitoidstemperaturetemporal distributionadult sizebehaviourmorphometrics
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 100 , Issue 4 , August 2010 , pp. 467 - 479
Copyright
Copyright © Cambridge University Press 2009

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Al-Wahaibi, A.K. (2004) Studies on two Homalodisca species (Hemiptera: Cicadellidae) in southern California: biology of the egg stage, host plant and temporal effects on oviposition and associated egg parasitism, and the biology and ecology of two of their egg parasitoids, Ufens A and Ufens B (Hymenoptera: Trichogrammatidae). PhD dissertation, University of California, Riverside, CA.Google Scholar
Al-Wahaibi, A.K. & Morse, J.G. (2000) Oviposition of Homalodisca species (Hemiptera: Cicadellidae) and associated egg parasitoids on citrus: cultivar effects. p. 101in Hoddle, M.S. (Ed.). Proceedings of the Second California Conference on Biological Control. University of California, Riverside, CA, 11–12 July 2000, Riverside, CA.Google Scholar
AI-Wahaibi, A.K., Owen, A.K. & Morse, J.G. (2005) Description and behavioral biology of two Ufens species (Hymenoptera: Trichogrammatidae), egg parasitoids of Homalodisca species (Hemiptera: Cicadellidae) in southern California. Bulletin of Entomological Research 95, 275–288.Google Scholar
Bakkendorf, O. (1934) Biological investigations on some Danish hymenopterous egg parasites, especially in homopterous eggs, with taxonomic remarks and descriptions of new species. Entomologisc Forening 19, 1–134.Google Scholar
Bartlett, B.R. & Ball, J.C. (1964) The developmental biologies of two encyrtid parasites of Coccus hesperidium and their intrinsic competition. Annals of the Entomological Society of America 57, 496–503.Google Scholar
Blua, M.J., Phillips, P.A. & Redak, R.A. (1999) A new sharpshooter threatens both crops and ornamentals. California Agriculture 53, 22–25.Google Scholar
Burks, R.A. & Redak, R.A. (2003) The identity and reinstatement of Homalodisca liturata Ball and Phera lacerta Fowler (Hemiptera: Cicadellidae). Proceedings of the Entomological Society of Washington 105, 674–678.Google Scholar
Cabrera, B.J., Marsh, P.M., Lewis, V.R. & Seybold, S.J. (2002) A new species of Heterospilus (Hymenoptera: Braconidae) associated with the deathwatch beetle, Hemicoelus gibbicollis (Leconte) (Coleoptera: Anobiidae). Pan-Pacific Entomologist 78, 7–16.Google Scholar
Ceresa-Gastaldo, L. & Chiappini, E. (1994) Observations on the cocoon of Oligosita krygeri Girault (Hymenoptera: Trichogrammatidae) oophagous parasitoid of Cicadella viridis (L.) (Homoptera: Cicadellidae). Norwegian Journal of Agricultural Science Supplement 16, 131–140.Google Scholar
Chandra, G. (1980) Taxonomy and bionomics of the insect parasites of rice leafhoppers and planthoppers in the Phillippines and their importance in natural biological control. Phillipine Entomologist 4, 119–139.Google Scholar
Clausen, C.P. (1940) Entomophagous Insects. 688 pp. New York, McGraw-Hill.Google Scholar
Flock, R.A., Doutt, R.L., Dickson, R.C. & Laird, E.F. (1962) A survey of beet leafhopper egg parasites in the Imperial Valley, California. Journal of Economic Entomology 55, 277–281.Google Scholar
Freitag, J.H., Frazier, N.W. & Flock, R.A. (1952) Six new leafhopper vectors of Pierce's disease virus. Phytopathology 42, 533–534.Google Scholar
Grandgirard, J., Hoddle, M.S., Triapitsyn, S.V., Petiti, J.N., Roderick, G.K. & Davies, N. (2007) First records of Gonatocerus dolichocerus Ashmead, Palaeoneura sp., Anagrus sp (Hymenoptera: Mymaridae), and Centrodora sp (Hymenoptera: Aphelinidae) in French Polynesia, with notes on egg parasitism of the glassy-winged sharpshooter, Homalodisca vitripennis (Germar) (Hemiptera: Cicadellidae). Pan-Pacific Entomologist 83, 177–184.Google Scholar
Henriquez, N.P. & Spence, J.R. (1993) Studies of Lathromeroidea sp. nov. (Hymenoptera: Trichogrammatidae), a parasitoid of gerrid eggs. Canadian Entomologist 125, 693–702.Google Scholar
Hoddle, M.S. & Triapitsyn, S.V. (2004). Searching for and collecting egg parasitoids of glassy-winged sharpshooter in the central and eastern USA. pp. 342–344in Tariq, M.A., Oswalt, S., Blincoe, P., Ba, A., Lorick, T. & Esser, T. (Eds) Proceedings of 2004 Pierce's Disease Research Symposium. 7–10 December 2004, San Diego, CA.Google Scholar
Hoffmann, M.P., Walker, D.L. & Shelton, A.M. (1995) Biology of Trichogramma ostriniae (Hym.: Trichogrammatidae) reared on Ostrinia nubilalis (Lep.:Pyralidae) and survey for additional hosts. Entomophaga 40, 387–402.CrossRefGoogle Scholar
Hohmann, C.L., Luck, R.F. & Oatman, E.R. (1988) A comparison of longevity and fecundity of adult Trichogramma platneri (Hymenoptera: Tichogrammatidae) reared from eggs of the cabbage looper and the angoumois grain moth, with and without access to honey. Journal of Economic Entomology 81, 1307–1312.CrossRefGoogle Scholar
Hosmer, D.W. & Lemeshow, S. (2000) Applied Logistic Regression. 392 pp. New York, NY, Wiley.CrossRefGoogle Scholar
Huber, J.T. (1988) The species groups of Gonatocerus Nees in North America with a revision of the sulphuripes and ater groups (Hymenoptera: Mymaridae). Memoirs of the Entomological Society of Canada 141, 1–109.Google Scholar
Huffaker, C.B., Holloway, J.K., Doutt, R.L. & Finney, G.L. (1954) Introduction of egg parasites of the beet leafhopper. Journal of Economic Entomology 47, 785–789.Google Scholar
Hutchison, W., Moratorio, M. & Martin, J.M. (1990) Morphology and biology of Trichogrammatoidea bactrae (Hymenoptera: Trichogrammatidae), imported from Australia as a parasitoid of pink bollworm (Lepidoptera: Gelechiidae) eggs. Annals of the Entomological Society of America 83, 46–54.CrossRefGoogle Scholar
Jacas, J., Pena, J.E. & Duncan, R.E. (2007) Morphology and development of immature stages of Fidiobia domica (Hymenoptera: Platygasteridae: Sceliotrachelinae). Annals of the Entomological Society of America 100, 413–417.Google Scholar
Jacas, J., Pena, J.E. & Duncan, R.E. (2009) Morphology and development of immature stages of Brachyufens osborni (Hymenoptera: Trichogrammatidae), an egg parasitoid of broad-nosed weevil species (Coleoptera: Curculionidae). Annals of the Entomological Society of America 102, 112–118.Google Scholar
Jervis, M.A. & Copland, M.J.W. (1996) The life cycle. pp. 63–161 in Jervis, M. & Kidd, N. (Eds) Insect Natural Enemies: Practical Approaches to Their Study and Evaluation. London, Chapman and Hall.Google Scholar
Jesu, R. & Laudonia, S. (1997) Gli stadi preimmaginali di Lathromeris cecidomyiiae Viggiani et Laudonia (Hymenoptera: Trichogrammatidae). Bollettino del Laboratorio di Entomologia Agraria Filippo Silvestri 53, 13–17.Google Scholar
Kapranas, A. (2002) Clutch size, pattern of sex allocation and encapsulation of Metaphycus sp. near flavus (Hymenoptera: Encyrtidae) eggs by brown soft scale, Coccus hesperidium L. (Homoptera: Coccidae). MSc thesis, University of California, Riverside, CA.Google Scholar
Krugner, R., Johnson, M.W., Russell, L.G. & Morse, J.G. (2008) Host specificity of Anagrus epos: a potential biological control agent of Homalodisca vitripennis. BioControl 53, 439–449.Google Scholar
Lauziere, I., Ciomperlik, M.A. & Wendel, L.E. (2002) Biological control of the glassy-winged sharpshooter in Kern County, California. pp. 81–82in Tariq, M.A., Oswalt, S., Blincoe, P. & Esser, T. (Eds) Proceedings of the Pierce's Disease Research Symposium. California Department of Food & Agriculture, Sacramento, CA, 15–18 December 2002, San Diego CA.Google Scholar
Logarzo, G.A., Virla, E.G., Triapitsyn, S.V. & Jones, W.A. (2004) Biology of Zagella delicata (Hymenoptera: Trichogrammatidae), an egg parasitoid of the sharpshooter Tapajosa rubromarginata (Hemiptera: Clypeorrhyncha: Cicadellidae) in Argentina. Florida Entomologist 87, 511–516.Google Scholar
Leopold, R.A. (2003). Interspecific competition between Gonatocerus ashmeadi, G. triguttattus, and G. fasciatus for glassy-winged sharpshooter egg masses. p. 225in Tariq, M.A., Oswalt, S., Blincoe, P., Spencer, R., Houser, L., Ba, A. & Esser, T. (Eds). Proceedings of the 2003 Pierce's Disease Research Symposium. California Department of Food & Agriculture, Sacramento, CA, 8–11 December 2003, San Diego, CA.Google Scholar
Mills, N.J. & Kuhlmann, U. (2000) The relationship between egg load and fecundity among Trichogramma parasitoids. Ecological Entomology 25, 315–324.Google Scholar
Morgan, D.J.W., Triapitsyn, S.V., Redak, R.A., Bezark, L.G. & Hoddle, M.S. (2000) Biological control of the glassy-winged sharpshooter: current status and future potential. pp. 167–171in Hoddle, M.S. (Ed.) Proceedings, Second California Conference on Biological Control. University of California, Riverside, CA, 11–12 July 2000, Riverside, CA.Google Scholar
Nagarkatti, S. & Nagaraja, H. (1977) Biosystematics of Trichogramma and Trichogrammatoidea species. Annual Review of Entomology 22, 157–176.Google Scholar
Owen, A.K. (2005). Systematics of the Trichogrammatidae (Hymenoptera: Chalcidoidea): a molecular phylogeny of the family and worldwide revision of Ufens Girault. PhD dissertation, University of California, Riverside, CA.Google Scholar
Pavlik, J. (1993) The size of the female and quality assessment of mass-reared Trichogramma spp. Entomologia Experimentalis et Applicata 66, 171–177.Google Scholar
Pinto, J.D. (2006) A review of the new world genera of Trichogrammatidae (Hymenoptera). Journal of Hymenoptera Research 15, 38–163.Google Scholar
Pinto, J.D., Frommer, S.I. & Manweiler, S.A. (1987) The insects of jojoba, Simmondsia chinensis, in natural stands and plantations in southwestern North America. Southwestern Entomologist 12, 287–298.Google Scholar
Powers, N.R. (1973) The biology and host plant relations of Homalodisca lacerta (Fowler) in southern California. MSc thesis, California State University, San Diego, CA.Google Scholar
Purcell, A.H., Saunders, S.R., Hendson, M., Grebus, M.E. & Henry, M.J. (1999) Causal role of Xylella fastidiosa in oleander leaf scorch disease. Phytopathology 89, 53–58.Google Scholar
Quicke, D.L.J. (1997) Parasitic Wasps. 470 pp. London, Chapman and Hall.Google Scholar
Rojas-Rousse, D., Gerding, M. & Cespedes, M. (1996) Caracterizacion de huevos Parasitados por Uscana senex (Hymenoptera: Trichogrammatidae). Agricultura Tecnica (Chile) 56, 211–213.Google Scholar
Rounbehler, M.D. & Ellington, J.J. (1973) Some biological effects of selected light regimes on Trichogramma semifumatum (Hymenoptera: Trichogrammatidae). Annals of the Entomological Society of America 66, 6–10.Google Scholar
SAS Institute (1996) JMP IN Version 3. SAS Institute, Cary, NC.Google Scholar
Schmidt, J.M. (1994) Host recognition and acceptance by Trichogramma. pp. 165–200in Wajnberg, E. & Hassan, S.A. (Eds) Biological Control with Egg Parasitoids. Wallingford, UK, CAB International.Google Scholar
Setamou, M. & Jones, W.A. (2005) Biology and biometry of sharpshooter Homalodisca coagulata (Homoptera: Cicadellidae) reared on cowpea. Annals of the Entomological Society of America 98, 322–328.Google Scholar
Takada, Y., Kawamura, S. & Tanaka, T. (2000) Biological characteristics: growth and development of the egg parasitoid Trichogramma dendrolimi (Hymenoptera: Trichogrammatidae) on the cabbage armyworm Mamestra brassicae (Lepidoptera: Noctuidae). Applied Entomology & Zoology 35, 369–379.Google Scholar
Takiya, D.N., McKamey, S.H. & Cavichioli, R.R. (2006) Validity of Homalodisca and of H. vitripennis as the name for glassy-winged sharpshooter (Hemiptera: Cicadellidae: Cicadellinae). Annals of the Entomological Society of America 99, 648–655.Google Scholar
Taylor, T.H.C. (1937) The Biological Control of an Insect in Fiji: An Account of the Coconut Leaf-mining Beetle and its Parasite Complex. 239 pp. London, Imperial Institute of Entomology.Google Scholar
Tipping, C., Triapitsyn, S.V. & Mizell, R.F. (2005) A new host record for the egg parasitoid Paracentrobia americana (Girault) (Hymenoptera: Trichogrammatidae) of the proconiine sharpshooter Homalodisca insolita (Walker) (Hemiptera: Clypeorryncha: Cicadellidae). Florida Entomologist 88, 217–218.Google Scholar
Triapitsyn, S.V. (2003) Taxonomic notes on the genera and species of Trichogrammatidae (Hymenoptera)-egg parasitoids of the Proconiine sharpshooters (Hemiptera: Clypeorrhyncha: Cicadellidae: Proconiini) in southeastern USA. Transactions of the American Entomological Society 129, 245–265.Google Scholar
Triapitsyn, S.V. & Hoddle, M.S. (2001) Search for and collect egg parasitoids of glassy-winged sharpshooter in southeastern USA and northeastern Mexico. pp. 133–134in Tariq, M.A., Oswalt, S. & Esser, T. (Eds) Proceedings of the Pierce's Disease Research Symposium. California Department of Food & Agriculture, Sacramento, CA, 5–7 December 2001, San Diego, CA.Google Scholar
Triapitsyn, S.V. & Hoddle, M.S. (2002) Search for and collect egg parasitoids of glassy-winged sharpshooter in southeastern USA and northeastern Mexico. pp. 95–94 in Tariq, M.A., Oswalt, S., Blincoe, P. & Esser, T. (Eds) Proceedings of the Pierce's Disease Research Symposium. California Department of Food & Agriculture, Sacramento, CA, 15–18 December 2002, San Diego, CA.Google Scholar
Triapitsyn, S.V., Mizell, R.F., Bossart, J.L. & Carlton, C.E. (1998) Egg parasitoids of Homalodisca coagulata (Homoptera: Cicadellidae). Florida Entomologist 81, 241–243.Google Scholar
Triapitsyn, S.V., Bezark, L.G. & Morgan, D.J. (2002) Redescription of Gonatocerus atriclavus Girault (Hymenoptera: Mymaridae), with notes on other egg parasitoids of sharpshooters (Homoptera: Cicadellidae: Proconiini) in northeastern Mexico. Pan-Pacific Entomologist 78, 34–42.Google Scholar
Triapitsyn, S.V., Morgan, D.J., Hoddle, M.S. & Berezovskiy, V.V. (2003) Observations on the biology of Gonatocersu fasciatus Girault (Hymenoptera: Mymaridae), egg parasitoid of Homalodisca coagulata (Say) and Oncometopia orbona (Fabricius) (Hemiptera: Clypeorrhyncha: Cicadellidae). Pan-Pacific Entomologist 79, 75–76.Google Scholar
Tothill, J.D., Taylor, T.H.C. & Paine, R.W. (1930) The Coconut Moth in Fiji. 269 pp. London, Imperial Bureau of Entomology.Google Scholar
Turner, W.F. & Pollard, H.N. (1959) Life histories and behavior of five insect vectors of phony peach disease. USDA Technical Bulletin 1188, 1–28.Google Scholar
UCOP (2000) Report of the University of California Pierce's disease research and emergency response task force. University of California, Oakland, CA.Google Scholar
Van Huis, A. & Appiah, S.O. (1995) Uscana lariophaga, West-African egg parasitoid of the cowpea bruchid beetle Callosobruchus maculatus: photoperiod, parasitization, and eclosion interactions. Entomologia Experimentalis et Applicata 76, 1–6.Google Scholar
Varela, L.G., Smith, R.J. & Phillips, P.A. (2001) Pierce's disease. University of California Agricultural & Natural Resources Publication 21600. University of California, Oakland, CA.Google Scholar
Vungsilabutr, P. (1978) Biological and morphological studies of Paracentrobia andoi (Ishi) (Hymenoptera: Trichogrammatidae), a parasite of the green rice leafhopper, Nephotettix cincticeps Uhler (Homoptera: Deltocepahalidae). Esakia 11, 29–51.CrossRefGoogle Scholar
Waage, J.K. (1986) Family planning in parasitoids: adaptive patterns of progeny and sex allocation. pp. 63–95in Waage, J. & Greathead, D. (Eds) Insect Parasitoids. London, Academic Press.Google Scholar
Waloff, N. & Jervis, M.A. (1987) Communities of parasitoids associated with leafhoppers and planthoppers in Europe. Advances in Ecological Research 17, 281–402.Google Scholar
Williams, L.H., Barnes, H.M. & Yates, H.O. III (1979) Beetle (Xyletinus peltatus) and parasite exit hole densities and beetle larval populations in southern pine floor joists. Environmental Entomology 8, 300–303.Google Scholar
Wu, Z.X., Cohen, A.C. & Nordlund, D.A. (2000) The feeding behavior of Trichogramma brassicae: new evidence for selective ingestion of solid food. Entomologia Experimentalis et Applicata 96, 1–8.CrossRefGoogle Scholar