Hostname: page-component-cd9895bd7-8ctnn Total loading time: 0 Render date: 2024-12-26T13:57:50.410Z Has data issue: false hasContentIssue false
  • English
  • Français

Comparison of five allopatric fruit fly parasitoid populations (Psyttalia species) (Hymenoptera: Braconidae) from coffee fields using morphometric and molecular methods

Published online by Cambridge University Press:  13 December 2007

M.K. Billah ,
S.W. Kimani-Njogu ,
R.A. Wharton ,
J.B. Woolley  and
D. Masiga
M.K. Billah*
Affiliation:
International Centre of Insect Physiology and Ecology (ICIPE), Box 30772–00100 GPO, Nairobi, Kenya
S.W. Kimani-Njogu
Affiliation:
Species2000 Project, Centre for Plant Diversity & Systematics, University of Reading, RG6 6AS, UK
R.A. Wharton
Affiliation:
Department of Entomology, Texas A&M University, College Station, Texas77843, USA
J.B. Woolley
Affiliation:
Department of Entomology, Texas A&M University, College Station, Texas77843, USA
D. Masiga
Affiliation:
International Centre of Insect Physiology and Ecology (ICIPE), Box 30772–00100 GPO, Nairobi, Kenya
*
*Author for correspondence Fax: +254-20-8632001/2 E-mail: [email protected] or [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Morphometric studies of five allopatric parasitoid populations (genus Psyttalia Walker) from coffee plantations in Cameroon (Nkolbisson), Ghana (Tafo) and Kenya (Rurima, Ruiru and Shimba Hills) and one non-coffee population (from Muhaka, Kenya) were compared with individuals of Psyttalia concolor (Szépligeti), a species released in several biological control programmes in the Mediterranean Region since the 20th Century. Analyses of wing vein measurements showed the second submarginal cell of the fore wing and its adjoining veins had the heaviest principal component weights and served as the main contributing variables in the diagnostic differentiation of the populations. Two populations (Rurima and Ruiru) were found to be the closest to each other and with the strongest phenetic affinity toward P. concolor (and forming one cluster). Populations from Shimba Hills (of unknown identity), Nkolbisson (P. perproximus (Silvestri)) and Tafo formed a second cluster and were separated from P. concolor. Comparison using amplified fragment length polymorphism (AFLP) also showed the Shimba, Nkolbisson and Tafo populations forming a cluster in a dendrogram generated from their genetic distances, with the Shimba and Tafo populations placed as the most closely related species. Based on consistent morphological similarities, morphometric and ecological data coupled with the genetic evidence from AFLP data, the Shimba population is suggested as belonging to the P. perproximus group and, thus, represents a new occurrence record in Kenya. Our results also support earlier conclusion from cross mating data that populations from Rurima and Ruiru belong to the Psyttalia concolor species-group.

Keywords

morphometryallopatric populationsparasitoidsPsyttaliaphenetic affinityMahalanobis distanceAFLPgenetic distancedendrogramspecies-group
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 98 , Issue 1 , February 2008 , pp. 63 - 75
Copyright
Copyright © Cambridge University Press 2008

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

Alvarez, J.M. & Hoy, M.A. (2002) Evaluation of the ribosomal ITS2 DNA sequences in separating closely related populations of the parasitoid Ageniaspis (Hymenoptera: Encyrtidae). Annals of the Entomological Society of America 95, 250–256.CrossRefGoogle Scholar
Baer, C.F., Tripp, D.W., Bjorksten, A. & Antolin, M.F. (2004) Phylogeography of a parasitoid wasp (Diaretiella rapae): no evidence of host-associated lineages. Molecular Ecology 13, 1859–1869.CrossRefGoogle Scholar
Baker, D.A., Loxdale, H.D. & Edwards, O.R. (2003) Genetic variation and founder effects in the parasitoid wasp, Diaretiella rapae (M'Intosh) (Hymenoptera: Braconidae: Aphidiidae), affecting its potential as a biological control agent. Molecular Ecology 12, 3303–3311.Google Scholar
Barari, H., Ferguson, A.W., Piper, R.W., Smith, E., Quicke, D.L.J. & Williams, I.H. (2005) The separation of two hymenopteran parasitoids, Tersilochus obscurator and Tersilochus microgaster (Ichneumonidae), of stem-mining pests of winter oilseed rape using DNA, morphometric and ecological data. Bulletin of Entomological Research 95, 299–307.Google Scholar
Bianchi, F.A. & Krauss, N.H. (1937) Fruit fly investigations in East Africa. Hawaiian Planters Record 41, 299–306.Google Scholar
Billah, M.K. (2004) Biosystematic studies of Psyttalia species (Hymenoptera: Braconidae): Parasitoids attacking fruit-infesting flies (Diptera: Tephritidae) in Africa. 236 pp. PhD thesis, University of Ghana, Legon-Accra.Google Scholar
Billah, M.K., Kimani-Njogu, S., Overholt, W.A., Wharton, R.A., Wilson, D.D. & Cobblah, M.A. (2005) The effect of host larvae on three Psyttalia species (Hymenoptera: Braconidae): parasitoids of fruit-infesting flies (Diptera: Tephritidae). International Journal of Tropical Insect Science 25(3), 168–175.CrossRefGoogle Scholar
Bokonon-Ganta, A.H., Ramadan, M.M., Wang, X.-G. & Messing, R.H. (2005) Biological performance and potential of Fopius ceratitivorus (Hymenoptera: Braconidae), an egg-larval parasitoid of tephritid fruit flies newly imported to Hawaii. Biological Control 33, 238–247.CrossRefGoogle Scholar
Bookstein, F.L., Chernoff, B., Elder, R., Humphries, J., Smith, G. & Strauss, R. (1985) Morphometrics in evolutionary biology. The Academy of Natural Science of Philadelphia, Special Publication, No. 15, 277 pp.Google Scholar
Brown, J.M., Pellmyr, O., Thompson, J.N. & Harrison, R.G. (1994) Phylogeny of Greya (Lepidoptera: Prodoxidae), based on nucleotide sequence variation in mitochondrial cytochrome oxidase I and II: congruence with morphological data. Molecular Biology and Evolution 11, 128–141.Google Scholar
Campbell, B., Heraty, J.M., Rasplus, J.-Y., Chan, K., Stephan-Campbell, J.D. & Babcock, C. (2000) Molecular systematics of the Chalcidoidea using 28S-D2 rDNA. pp. 59–71in Austin, A.D. & Dowton, M. (Eds) Hymenoptera: Evolution, Biodiversity and Biological Control. Collingwood, Victoria, Australia, CSIRO Publishing.Google Scholar
Carmichael, A.E., Wharton, R.A. & Clarke, A.R. (2005) Opiine parasitoids (Hymenoptera: Braconidae) of tropical fruit flies (Diptera: Tephritidae) of the Australian and South Pacific region. Bulletin of Entomological Research 95, 545–569.Google Scholar
Caterino, M.S., Cho, S. & Sperling, F.A.H. (2000) The current state of insect molecular systematics: A thriving tower of Babel. Annual Review of Entomology 45, 1–54.Google Scholar
Chinajariyawong, A., Clark, A.R., Jirasurat, M., Kritsaneepiboon, S., Lahey, H.A., Vijaysegaran, S. & Walter, G.H. (2000) Survey of opiine parasitoids of fruit flies (Diptera: Tephritidae) in Thailand and Malaysia. Raffles Bulletin of Zoology 48, 71–101.Google Scholar
Clausen, C.P., Clancy, D.W. & Chock, Q.C. (1965) Biological control of the Oriental fruit fly and other fruit flies in Hawaii. USDA Technical Bulletin, No. 1322.Google Scholar
Copeland, R.S., White, I.M., Okumu, M., Machera, P. & Wharton, R.A. (2004) Insects associated with fruits of the Oleaceae (Asteridae, Lamiales) in Kenya, with special reference to the Tephritidae (Diptera). Bishop Museum Bulletins in Entomology 12, 135–164.Google Scholar
Copeland, R.S., Wharton, R.A., Luke, Q., De Meyer, M., Lux, S., Zenz, N., Machera, P. & Okumu, M. (2006) Geographic distribution, host fruit, and parasitoids of African fruit fly pests Ceratitis anonae, Ceratitis cosyra, Ceratitis fasciventris and Ceratitis rosa (Diptera: Tephritidae) in Kenya. Annals of the Entomological Society of America 99(2), 261–278.CrossRefGoogle Scholar
Delucchi, V. (1957) Les parasites de la mouche des olives. Entomophaga 2, 106–118.Google Scholar
Drew, R.A.I., Tsuruta, K. & White, I.M. (2005) A new species of pest fruit fly (Diptera: Tephritidae: Dacinae) from Sri Lanka and Africa. African Entomology 13, 149–154.Google Scholar
Fischer, M. (1958) Ueber dei Variabilitaet von Toxonomisch wichtigen merkmalen bei Opius concolor Szepl. (Hymenoptera: Braconidae). Entomophaga 3, 55–66.CrossRefGoogle Scholar
Fischer, M. (1963) Das Genus Austroopius Szépligeti. Mitteilungen der Zoologie am Museum Berlin 39, 173–186.Google Scholar
Fischer, M. (1971) Hym. Braconidae. World Opiinae. Index of Entomophagous Insect. 189 pp. Paris, Le Francois.Google Scholar
Fischer, M. (1972) Hymenoptera: Braconidae (Opiinae I). Das Tierreich 91, 1–620.Google Scholar
Fischer, M. (1987) Hymenoptera: Opiinae III – äthiopische, orientalische, australische und ozeanische Region. Das Tierreich 104, 1–734.Google Scholar
Gillespie, J.J., Munro, J.B., Heraty, J.M., Yoder, M.J., Owen, A.K. & Carmichael, A. (2005) A secondary structural model of the 28S rRNA expansion segments D2 and D3 from chalcidoid wasps (Hymenoptera: Chalcidoidea): Implications for multiple sequence alignment and phylogeny reconstruction. Molecular Biology and Evolution 22, 1593–1608.CrossRefGoogle Scholar
Greathead, D.J. (1976). Mediterranean fruit fly, Olive fly. pp. 37–43. in Greathead, D. J. (Ed.). A review of biological control in western and southern Europe. Commonwealth Institute of Biological Control Technical Communications 7.Google Scholar
Greenstone, M.H. (2006) Molecular methods for assessing insect parasitism. Bulletin of Entomological Research 96, 1–13.CrossRefGoogle ScholarPubMed
Han, J.-Y. & McPheron, B.A. (1997) Molecular phylogenetic study of Tephritidae (Insecta: Diptera) sing partial sequences of the Mitochondrial 16S Ribosomal DNA. Molecular Phylogenetics and Evolution 7(1), 17–32.CrossRefGoogle Scholar
Heraty, J.M. (2004) Molecular systematics, Chalcidoidea and biological control. pp. 39–71in Ehler, L.E., Sforza, R. & Mateille, T. (Eds) Genetics, Evolution and Biological Control. London, CAB International.Google Scholar
Heraty, J.M. & Woolley, J.B. (1993) Separate species or polymorphism: A recurring problem in Kapala (Hymenoptera: Eucharitidae). Annals of the Entomological Society of America 86(5), 517–531.CrossRefGoogle Scholar
Hillis, D.M. (1987) Molecular versus morphological approaches to systematics. Annual Review of Ecology and Systematics 18, 23–42.Google Scholar
Jolicoeur, P. & Mosimann, J.E. (1960) Size and shape variation in the painted turtle. A principal component analysis. Growth 24, 339–354.Google Scholar
Kankare, M., Jensen, M.K., Kester, K.M. & Saccheri, I.J. (2004) Characterization of microsatellite loci in two primary parasitoids of the butterfly Melitaea cinxia, Cotesia melitaearum and Hyposoter horticola (Hymenoptera). Molecular Ecology Notes 4, 231–233.CrossRefGoogle Scholar
Kazachkova, N., Fahleson, J. & Meijer, J. (2004) Establishment of the Amplified Fragment Length Polymorphism (AFLP) technique for genotyping of pollen beetle (Meligethes aeneus) – a noxious insect pest on oilseed rape (Brassica napus). Molecular Biology Reports 31, 37–42.CrossRefGoogle ScholarPubMed
Kimani-Njogu, S.W. & Wharton, R.A. (2002) Two new species of Opiinae (Hymenoptera: Braconidae) attacking fruit-infesting Tephritidae (Diptera) in western Kenya. Proceedings of the Entomological Society of Washington 104, 79–90.Google Scholar
Kimani-Njogu, S.W., Overholt, W.A., Woolley, J.B. & Omwega, C.O. (1998) Electrophoretic and phylogenetic analyses of selected allopatric populations of the Cotesia flavipes complex (Hymenoptera: Braconidae), parasitoids of cereal stem borers. Biochemical Systematics and Ecology 26, 285–296.CrossRefGoogle Scholar
Kimani-Njogu, S.W., Trostle, M.K., Wharton, R.A., Woolley, J.B. & Raspi, A. (2001) Biosystematics of the Psyttalia concolor species complex (Hymenoptera: Braconidae: Opiinae): the identity of populations attacking Ceratitis capitata (Diptera: Tephritidae) in coffee in Kenya. Biological Control 20, 167–174.Google Scholar
Knipling, E.F. (1992) Principles of insect parasitism analyzed from new perspectives – Practical implications for regulating insect populations by biological control means. USDA Agricultural Handbook No. 693, 337 pp.Google Scholar
Kumar, S., Tamura, K. & Nei, M. (2004) MEGA 3: Integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Briefings in Bioinformatics 5, 150–163.Google Scholar
Landry, B., Powell, J.A. & Sperling, F.A.H. (1999) Systematics of the Argyrotaenia franciscana (Lepidoptera: Tortricidae) species group: evidence from mitochondrial DNA. Annals of the Entomological Society of America 92, 40–46.Google Scholar
Loxdale, H.D. & Lushai, G. (1998) Molecular markers in entomology. Bulletin of Entomological Research 88, 577–600.Google Scholar
Lux, S.A., Copeland, R.S., White, I.M., Manrakhan, A. & Billah, M.K. (2003) A New Invasive Fruit Fly Species from the Bactrocera dorsalis (Hendel) Group Detected in East Africa. Insect Science and its Application 23(4), 355–361.Google Scholar
Machal, P. (1910) Sur un Braconide nouveau, parasite du Dacus oleae. Bulletin de la Société Entomologique de France 1910, 243–244.CrossRefGoogle Scholar
Marcus, L.F. (1990) Traditional morphometrics. pp. 77–122 in Proceedings of the Michigan Morphometrics Workshop. Special Publication No. 2. Ann Arbor, Michigan, University of Michigan. Museum of Zoology.Google Scholar
Masaba, D.M., Owuor, J.B.O. & Gathaara, M.P.H. (1986) Arabica coffee production in Kenya: An overview. Outlook on Agriculture 15(2), 88–92.Google Scholar
Masiga, D., Tait, A. & Turner, C.M.R. (2000) Amplified Restriction Fragment Length Polymorphism in parasite genetics. Parasitology Today 16(8), 350–353.CrossRefGoogle ScholarPubMed
Messing, R.H., Klungness, L.M., Purcell, M. & Wong, T. (1993) Quality control parameters of mass-reared opiine parasitoids used in augmentative biological control of tephritid fruit flies in Hawaii. Biological Control 3, 140–147.Google Scholar
Monastero, S. (1931) Un nuovo parassita endofaga della mosca delle olive trovato in Altavilla Milicia (Silicia). Atti della Reale Accademia della Scienze Palermo 16, 1–6.Google Scholar
Monastero, S. (1934) Studio sulla posizione sistematica dell'Opius siculus Monastero endofago della mosca delle olive. Atti della Reale Accademia della Scienze Palermo 18, 371–389.Google Scholar
Muesebeck, C.F.W. (1931) Descriptions of a new genus and eight new species of Ichneumon-flies with taxonomic notes. Proceedings of the United States National Museum 76, 1–16.CrossRefGoogle Scholar
Neff, N.A. & Marcus, L.F. (1980) A Survey of Multivariate Methods for Systematics. 243 pp. New York, Privately Published and A.M.N.H.Google Scholar
Nei, M. (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89, 583–590.Google Scholar
Oerke, E.-C., Dehne, H-W., Schönbeck, F. & Weber, A. (1994) Crop Production and Crop Protection: Estimated Losses in Major Food and Cash Crops. 808 pp. Amsterdam, Elsevier Science Publishers.Google Scholar
Ovruski, S., Aluja, M., Sivinski, J. & Wharton, R.A. (2000) Hymenoptera parasitoids on fruit-infesting Tephritidae (Diptera) in Latin America and the southern United States: Diversity, distribution, taxonomic status and their use in fruit fly biocontrol. Integrated Pest Management Review 5, 81–107.Google Scholar
PopGen 32 (1997) Population Genetic Analysis software, version 1.31. Canada, University of Alberta and Centre for International Forestry Research.Google Scholar
Purcell, M., Herr, J.C., Messing, R.H. & Wong, T. (1998) Interactions between augmentatively released Diachasmimorpha longicaudata (Hymenoptera: Braconidae) and a complex of opiine parasitoids in a commercial guava orchard. Biocontrol Science and Technology 8, 139–151.CrossRefGoogle Scholar
Quicke, D.L.J. (2004) The world of DNA barcoding and morphology – collision or synergism and what of the future. Systematist 23, 8–12.Google Scholar
Ramadan, M.M. (2004) Mass-rearing biology of Fopius vandenboschi (Hym: Braconidae). Journal of Applied Entomology 128, 226–232.Google Scholar
Reineke, A., Karlovsky, P. & Zebitz, C.P.W. (1999) Amplified fragment length polymorphism analysis of different geographic populations of the gypsy moth, Lymantria dispar (Lepidoptera: Lymantriidae). Bulletin of Entomological Research 89, 79–88.Google Scholar
Rohlf, F.J. & Bookstein, F.L. (1987) A comment on shearing as a method for size correction. Systematic Zoology 36, 356–367.Google Scholar
Rohlf, F.J. & Bookstein, F.L. (1990) Proceedings of the Michigan Morphometrics Workshop. Special Publication No. 2 (The Blue Book). Ann Arbor, Michigan, University of Michigan, Museum of Zoology.Google Scholar
SAS Institute Inc. (2001) SAS/STAT® User's Guide, Version 8.2. Cary, NC, USA.Google Scholar
Sheppard, W.S., Steck, G.S. & McPheron, B.A. (1992) Geographic populations of the medfly may be differentiated by mitochondrial DNA variation. Experimentia 48, 1010–1013.Google Scholar
Silvestri, F. (1913) Viaggio in Africa per cercave parassiti di mosche dei frutti. Bollettino del Laboratorio di Zoologia Generale e Agraria, Portici 8, 1–164.Google Scholar
Silvestri, F. (1914) Report of an expedition to Africa in search of the natural enemies of fruit flies. Hawaiian Board of Agriculture & Forestry Division. Entomological Bulletin 3, 176 pp. (Translation of 1913 report in Italian).Google Scholar
Sivinski, J.Vulinec, K. & Aluja, M. (2001) Ovipositor length in a guild of parasitoid (Hymenoptera: Braconidae) attacking Anastrepha species fruit flies (Diptera: Tephritidae) in Southern Mexico. Annals of the Entomological Society of America 94(6), 886–895.Google Scholar
Sneath, P.H.A. & Sokal, R.R. (1973) Numerical Taxonomy: The Principles and Practice of Numerical Classification. 573 pp. San Francisco, W. H. Freeman & Co.Google Scholar
Sokal, R.R. & Rohlf, F.J. (1995) Biometry: The Principles and Practice of Statistics in Biological Research. 3rd edn.887 pp. San Francisco, W. H. Freeman & Co.Google Scholar
Steck, G.J., Gilstrap, F., Wharton, R.A. & Hart, W.G. (1986) Braconid parasitoids of Tephritidae infesting coffee and other fruits in West-central Africa. Entomophaga 31, 59–67.CrossRefGoogle Scholar
Szépligeti, G. (1910) Description d'une espéce nouvelle d'Opius (Braconidae) de l'Afrique méridionale. Bollettino del Laboratorio di Zoologia Generale e Agraria Portici 4, 346.Google Scholar
Triapitsyn, S.V., Vickerman, D.B., Heraty, J.M. & Logarzo, G.A. (2006) A new species of Gonatocerus (Hymenoptera: Mymaridae) parasitic on proconiine sharpshooters (Hemiptera: Cicadellidae) in the New World. Zootaxa 1158, 55–67.Google Scholar
Umphrey, G.J. (1996) Morphometric discrimination among sibling species in the fulva-rudis-texana complex of the ant genus Aphaenogaster (Hymenoptera: Formicidae). Canadian Journal of Zoology 74(3), 528–559.CrossRefGoogle Scholar
Unruh, T.R., White, W., Gonzalez, D. & Woolley, J.B. (1989) Genetic relationships among seventeen Aphidius (Hymenoptera: Aphidiidae) populations, including six species. Annals of the Entomological Society of America 82, 754–762.Google Scholar
Vos, P., Hogers, R., Bleeker, M., Reijans, M., van de Lee, T., Hornes, M., Frijters, A., Pot, J., Peleman, J., Kuiper, M. & Zabeau, M. (1995) AFLP: a new technique for DNA fingerprinting. Nucleic Acids Research 23, 4407–4414.CrossRefGoogle ScholarPubMed
Walker, F. (1860) Characters of some apparently undescribed Ceylon Insects. Annals and Magazine of Natural History 3(5), 304–311.Google Scholar
Waterhouse, D.F. (1993) Biological Control: Pacific Prospects, Supplement 2. 138 pp. Canberra, Australian Centre for International Agricultural Research (ACIAR).Google Scholar
Wharton, R.A. (1987) Changes in nomenclature and classification of some opiine Braconidae (Hymenoptera). Proceedings of the Entomological Society of Washington, 89, 61–73.Google Scholar
Wharton, R.A. (1988) Classification of the Braconid subfamily Opiinae (Hymenoptera). The Canadian Entomologist 120, 333–360.Google Scholar
Wharton, R.A. (1989) Control; classical biological control of fruit-infesting Tephritidae. pp. 303–313in Robinson, A.S. & Hooper, G. (Eds) Fruit Flies; their Biology, Natural Enemies and Control. World Crop Pests, 3(B). Amsterdam, Elsevier Science Publishers.Google Scholar
Wharton, R.A. (1997a) Generic relationships of opiine Braconidae (Hymenoptera) parasitic on fruit- infesting Tephritidae (Diptera). Contributions of the American Entomological Institute 30, 1–53.Google Scholar
Wharton, R.A. (1997b) Subfamily Opiinae. pp. 378–395in Wharton, R.A., Marsh, P.M. & Sharkey, M.J. (Eds) Manual of the new world Genera of the family Braconidae (Hymenoptera). Washington, D.C., The International Society of Hymenopterists (Special publication, 1).Google Scholar
Wharton, R.A. (1999) A review of the Old World genus Fopius Wharton (Hymenoptera: Braconidae: Opiinae), with description of two new species reared from fruit-infesting Tephritidae (Diptera). Journal of Hymenoptera Research 8, 48–64.Google Scholar
Wharton, R.A. & Gilstrap, F.E. (1983) Key to and status of opiine braconid (Hymenoptera) parasitoids used in biological control of Ceratitis and Dacus s. l. (Diptera: Tephritidae). Annals of the Entomological Society of America 76, 721–742.Google Scholar
Wharton, R.A., Trostle, M.K., Messing, R.H., Copeland, R.S., Kimani-Njogu, S.W., Lux, S., Overholt, W.A., Mohamed, S. & Sivinski, J. (2000) Parasitoids of medfly, Ceratitis capitata, and related tephritids in Kenyan coffee: a predominantly koinobiont assemblage. Bulletin of Entomological Research 90, 517–526.Google Scholar
Wharton, R.A., Yoder, M.J., Gillespie, J.J., Patton, J.C. & Honeycutt, R.L. (2006) Relationships of Exodontiella, a non-alysiine, exodont member of the family Braconidae (Insecta, Hymenoptera). Zoologica Scripta 35, 323–340.Google Scholar
White, I.M. & Elson-Harris, M.M. (1992) Fruit Flies of Economic Significance: Their Identification and Bionomics. 602 pp. Wallingford, UK, CAB International.Google Scholar
Will, K.W. & Rubinoff, D. (2004) Myth of the molecule: DNA barcodes for species cannot replace morphology for identification and classification. Cladistics 20, 47–55.Google Scholar
Willard, H.F. & Mason, A.C. (1937) Parasitization of the Mediterranean fruit fly in Hawaii, 1914–1933. USDA Circular 439, 1–18.Google Scholar
Wool, D. & Hales, D.F. (1997) Phenotypic plasticity in Australian cotton aphid (Homoptera: Aphididae): host plant effects on morphological variation. Annals of the Entomological Society of America 90, 316–328.Google Scholar
Woolley, J.B. & Browning, H.W. (1987) Morphometric analysis of uniparental Aphytis reared from Chaff scale, Pariatoria pergondii Comstock, on Texas citrus (Hymenoptera: Aphelinidae, Homoptera: Diaspididae). Proceedings of the Entomological Society of Washington 89, 77–94.Google Scholar
Woolley, J.B., Rose, M. & Krauter, P. (1994) Morphometric comparisons of Aphytis species in the lingnanensis group (Hymenoptera: Aphelinidae). pp. 223–244in Rosen, D. (Ed.) Advances in Aphytis Research. Andover, UK, Intercept Ltd.Google Scholar