Abstract
The reproductive compatibility between four different species/populations of the tephritid parasitoid Psyttalia (Walker) species from Kenya and individuals of the morphologically identical Psyttalia concolor (Szépligeti) (Hymenoptera: Braconidae) from a laboratory culture in Italy used in augmentative biological control of olive fly, Bactrocera oleae (Gmelin) (Diptera: Tephritidae) was assessed through cross mating tests using single-pair and group mating methods. Reciprocal crosses among the species resulted in the production of viable offsprings up to the second generation. In spite of the successful production of viable offspring in the laboratory, Psyttalia species are known to have specific host fruit and/or host fly preferences and populations/species may be isolated in one way or the other. However, it is not known whether these populations/species interbreed in the field. We discuss the ability of these parasitoids to interbreed and the potential effects of that on their use as biological control agents, especially in environments where other closely related species are present or in situations where multiple parasitoid introductions are intended.
Similar content being viewed by others
References
Billah MK (2004) Biosystematic studies of Psyttalia species (Hymenoptera: Braconidae): Parasitoids attacking fruit-infesting flies (Diptera: Tephritidae) in Africa. PhD thesis, University of Ghana, Legon-Accra, 236 pp
Billah MK, Kimani-Njogu S, Overholt WA, Wharton RA, Wilson DD, Cobblah MA (2005) The effect of host larvae on three Psyttalia species (Hymenoptera: Braconidae): parasitoids of fruit-infesting flies (Diptera: Tephritidae). Intl J Trop Insect Sc 25(3):168–175
Bokonon-Ganta AH, Ramadan MM, Wang X-G, Messing RH (2005) Biological performance and potential of Fopius ceratitivorus (Hymenoptera: Braconidae), an egg-larval parasitoid of tephritid fruit flies newly imported to Hawaii. Biol Control 33:238–247
Briggs CJ (1993) Competition among parasitoid species on a stage-structured host and its effects on host suppression. Am Naturalist 141:372–396
Charnov EL (1982) The theory of sex allocation. Princeton University Press, Princeton, USA
Charnov EL, Los-den Hartogh RL, Jones WT, van den Assem J (1981) Sex ratio evolution in a variable environment. Nature 289:27–33
Claridge MF (1991) Genetic and biological diversity of insect pests and their natural enemies. In: Hawksworth DL (ed) Biodiversity of microorganisms and invertebrates; its role in sustainable agriculture. CAB International, Wallingford, pp 183–194
Clausen CP, Clancy DW, Chock QC (1965) Biological control of the oriental fruit fly and other fruit flies in Hawaii. USDA Tech Bull 1322
Copeland RS, White IM, Okumu M, Machera P, Wharton RA (2004) Insects associated with fruits of the Oleaceae (Asteridae, Lamiales) in Kenya, with special reference to the Tephritidae (Diptera). Bis Mus Bull Entomol 12:135–164
Copeland RS, Wharton RA, 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. Ann Entomol Soc Am 99(2):261–278
DeBach P, Rosen D (1991) Biological control by natural enemies, 2nd edn. Cambridge University Press, Cambridge, 440 pp
De Meyer M (1996) Revision of the subgenus Ceratitis (Pardalaspis) Bezzi, 1918 (Diptera, Tephritidae, Ceratitini). Syst Entomol 21:15–26
De Meyer M (1998) Revision of the subgenus Ceratitis (Ceratalaspis) Hancock (Diptera: Tephritidae). Bull Entomol Res 88:257–290
De Meyer M (2000) Systematic revision of the subgenus Ceratitis MacLeay s. (Diptera: Tephritidae). Zool J Linn Soc 128:439–467
De Meyer M, Copeland RS, Lux SA, Mansell M, Quilici S, Wharton R, White IM, Zenz N (2002) Annotated checklist of host plants for Afrotropical fruit flies (Diptera: Tephritidae) of the genus Ceratitis. Musée Roy Afriq Centr Tervuren Belgique 27:1–91
Diehl SR, Bush GL (1984) An evolutionary and applied perspective of insect biotypes. Annu Rev Entomol 29:471–483
Gauld ID (1986) Taxonomy, its limitations and its role in understanding parasitoid biology. In: Waage JK, Greathead D (eds) Insect parasitoids, Academic Press, London, pp 1–22
Godfray HCJ (1994) Parasitoids: behaviour and evolutionary ecology. Princeton Univercity Press, NJ, USA, 473 pp
Greathead DJ (1976) Mediterranean fruit fly, Olive fly. In: Greathead DJ (ed) A review of biological control in western and southern Europe, Commonw Inst Biol Cont Techn Com, vol 7. pp 37–43
Grissell EE, Schauff ME (1997) A handbook of the families of Nearctic Chalcidoidea (Hymenoptera), 2nd edn, Revised. Entomol Soc Wash, 87 pp
Gujar GT, Chandrashekaran S, Kalia V (2006) Hybrid parasitoids for pest management. Opinion Curr Sci 90(7):907
Hall RW (1993) Alteration of sex ratios of parasitoids for use in biological control. In: Wrensch DL, Ebbert MA (eds) Evolution and diversity of sex ratio in insects and mites. Chapman and Hall, New York, pp 542–547
Hooper GHS (1987) Application of quality control procedures for large scale rearing of Mediterranean fruit fly. Ent Exp Appl 44:161–167
Hopper KR, Roush RT, Powell W (1993) Management of genetics of biological control introductions. Annu Rev Entomol 38:27–51
Janssen A (1989) Optimal host selection by Drosophila parasitoids in the field. Func Ecol 3:469–479
Jervis M, Kidd N (eds) (1996) Insect natural enemies. Practical approaches to their study and evaluation. Chapman and Hall, London, UK, 491 pp
Kimani-Njogu SW, Wharton RA (2002) Two new species of Opiinae (Hymenoptera: Braconidae) attacking fruit-infesting Tephritidae (Diptera) in western Kenya. Proc Entomol Soc Wash 104:79–90
Kimani SW, Overholt WA (1995) Biosystematics of the Cotesia flavipes complex (Hymenoptera: Braconidae): interspecific hybridization, sex pheromone and mating behaviour studies. Bull Entomol Res 85:379–386
Kimani-Njogu SW, Trostle MK, Wharton RA, Woolley JB, 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. Biol Control 20:167–174
King BH (1987) Offspring sex ratios in parasitoid wasps. Quarterly Rev Biol 62:367–396
Liquido NJ, Shinoda LA, Cunningham RT (1991) Host plants of the Mediterranean fruit fly: an annotated worldview. ESA Misc Pub 77:1–52
Liu S-S, Gebremeskel FB, Shi Z-H (2002) Reproductive compatibility and variation in survival and sex ratio between two geographic populations of Diadromus collaris, a pupal parasitoid of the Diamondback moth, Plutella xylostella. BioControl 47:625–643
Lopez M, Sivinski J, Rendon P, Holler T, Bloem K, Copeland R, Trostle M, Aluja M (2003) Colonization of Fopius ceratitivorus, a newly discovered African egg-pupal parasitoid (Hymenoptera: Braconidae) of Ceratitis capitata (Diptera: Tephritidae). Florida Entomologist 86(1):53–60
Mackauer M (1969) Sexual behaviour and hybridization between three species of Aphidius Nees, parasitic on the pea aphid. Proc Entomol Soc Wash 71:339–351
Messing R, Roitberg B, Brodeur J (2006) Effects of competition, displacement and intraguild predation in biocontrol and evaluation methods. In: Bigler F, Babendreier D, Kuhlman U (eds) Environmental impact of invertebrates in biological control of arthropods: methods and risk assessment. Wallingford, UK, CAB Int, pp 64–77
Mitchell WC, Andrew CO, Hagan KS, Hamilton RA, Harris EJ, Maehler KL, Rhode RA (1977) The Mediterranean fruit fly and its economic impact in Central American countries and Panama. Univ. of California/Agency for International Development, Pest Mgt and Rel Envir Prot, 189 pp
Mohamed SA, Overholt WA, Wharton RA, Lux SA, Eltoum EM (2003). Host specificity of Psyttalia cosyrae (Hymenoptera: Braconidae) and the effect of different host species on parasitoid fitness. Biol Control 28:155–163
Nagarkatti S (1975). Two new species of Trichogramma (Hymenoptera: Trichogrammatidae) from the USA. Entomophaga 20:245–248
Phillips CB, Emberson RM Goldson SL (1993) Host-associated morphological variation in Canterbury (New Zealand) populations of the parasitoid Microctonus aethiopoides Loan (Hymenoptera: Braconidae, Euphorinae). Proceedings of the 6th Australasian conference grassland invertebrate ecology, pp 405–414
Pinto JD, Stouthamer R (1994) Systematics of the Trichogrammatidae with emphasis on Trichogramma. In: Wajnberg E, Hassan SA (eds) Biological control with egg parasitoids. CAB International, Wallingford, pp 1–36
Pinto JD, Oatman ER, Platner GR (1986) Trichogramma pretiosum and a new cryptic species occurring sympatrically in southwestern North America (Hymenoptera: Trichogrammatidae). Ann Entomol Soc Am 79:1019–1028
Pinto JD, Stouthamer R, Platner GR, Oatman ER (1991) Variation in reproductive compatibility in Trichogramma and its taxonomic significance (Hymenoptera: Trichogrammatidae). Ann Entomol Soc Am 84:37–46
Pinto JD, Kazmer DJ, Platner GR, Sassaman CA (1992) Taxonomy of the Trichogramma minutum complex (Hymenoptera: Trichogrammatidae): allozymic variation and its relationship to reproductive and geographic data. Ann Entomol Soc Am 85:413–422
Pinto JD, Platner GR, Sassaman CA (1993) Electrophoretic study of two closely related species of North American Trichogramma: T. pretiosum and T. deion (Hymenoptera: Trichogrammatidae). Ann Entomol Soc Am 86(6):702–709
Raspi A, Loni A (1994) Alcune note sull’allevamenton massale di Opius concolor Szépligeti (Hymenoptera: Braconidae) e su recenti tentative d’introduzione della specie in Toscana e Liguria. Frustula Entomologica 30:135–145
Rosen D (1986) The role of taxonomy in effective biological control programs. Agric Ecosys Envir 15:121–129
Salt G (1941) The effects of hosts upon their insect parasites. Biol Revs 16:239–264
Salt G (1963) The defense reactions of insects to metazoan parasites. Parasitology 53:527–642
SAS Institute Inc. (2001) SAS/STAT® User’s Guide, Version 8.2. Cary, NC, USA
Silvestri F (1914) Report of an expedition to Africa in search of the natural enemies of fruit flies. Hawaiian Board of Agriculture and Forestry Division, Entomol Bull No. 3, 176 pp (Translation of 1913 report in Italian)
Sivinski JM, Webb JC (1989) Acoustic courtship signals produced during courtship in Diachasmimorpha (= Biosteres) longicaudata (Hymenoptera: Braconidae) and other Braconidae. Ann Entomol Soc Am 82:116–120
Smith DC, Lyons SA, Berlocher SH (1993) Production and electrophoretic variation of F1 hybrids between the sibling species Rhagoletis pomonella and R. Cornivora. Ent Exp Appl 69:209–213
Sokal RR, Rohlf FJ (1995) Biometry: the principles and practice of statistics in biological research, 3rd edn. W. H. Freeman and Company, USA, 887 pp
Stouthamer R, Jochemsen P, Platner, GR Pinto JD (2000). Crossing incompatibility between Trichogramma minutum and T. platneri (Hymenoptera: Trichogrammatidae): implications for application in biological control. Environ Entomol 29(4):832–837
van den Assem J, Jachmann F (1982) The coevolution of receptivity signalling and body size in the Chalcidoidea. Behaviour 80:96–105
van den Bosch R, Hom R, Matteson P, Frazer BD, Messenger PS, Davies CS (1979) Biological control of the walnut aphid in California: impact of the parasite, Trioxys pallidus. Hilgardia 47:1–15
Vera MT, Caceres C, Wornoayporn V, Islam A, Robinson AS, de La Vega MH, Hendrichs J, Cayol J-P (2006) Mating incompatibility among populations of the South American fruit fly Anastrepha frateculus (Diptera: Tephritidae). Ann Entomol Soc Am 99(2):387–397
Vinson SB, Iwantsch GF (1980) Host suitability for insect parasitoids. An Rev Entomol 25:397–419
Wajnberg E, Boulétreau M, Prévost G, Fouillet P (1990) Developmental relationships between Drosophila larvae and their endoparasitoid Leptopilina (Hymenoptera: Cynipidae) as affected by crowding. Arch Insect Biochem Physiol 13:293–245
Wang X-G, Messing RH (2003) Intra- and interspecific competition by Fopius arisanus and Diachasmimorpha tryoni (Hymenoptera: Braconidae), parasitoids of tephritid fruit flies. Biol Control 27:251–259
Weems HV (1981) Mediterranean fruit fly, Ceratitis capitata (Wiedemann) (Diptera: Tephritidae). Fla Dept Agric And Consumer Service, Div Plant Industry, Entomol Cir No 230, 8 pp
Wharton RA (1989a) Control; Classical biological control of fruit-infesting Tephritidae. In: Robinson AS, Hooper G (eds) Fruit flies; their biology, natural enemies and control. World crop pests, 3(B). Elsevier Science Publishers, Amsterdam, pp 303–313
Wharton RA (1989b) Biological control of fruit-infesting Tephritidae. In: R Cavalloro (ed) Fruit flies of Economic Importance 87. Proceedings of the CEC/IOBC international symposium, Rome, 1987, Balkema, Rotterdam, pp 323–332
Wharton RA (1997a) Generic relationships of opiine Braconidae (Hymenoptera) parasitic on fruit-infesting Tephritidae (Diptera). Contri Am Entomol Inst 30:1–53
Wharton RA 1997b. Key to new world genera of Opiinae. In: RA Wharton, Marsh PM, Sharkey MJ (eds) Manual of the New world Genera of the family Braconidae (Hymenoptera). Special publ Intl Soc Hym No 1
Wharton RA, Gilstrap FE (1983) Key to and status of opiine braconid (Hymenoptera) parasitoids used in biological control of Ceratitis and Dacus s.l. (Diptera: Tephritidae). Ann Entomol Soc Am 76:721–742
Wharton RA, Trostle MK, Messing RH, Copeland RS, Kimani-Njogu SW, Lux S, Overholt WA, Mohamed S, Sivinski J (2000) Parasitoids of medfly, Ceratitis capitata, and related tephritids in Kenyan coffee: a predominantly koinobiont assemblage. Bull Entomol Res 90:517–526
White IM, Elson-Harris MM (1992) Fruit flies of economic significance: their identification and bionomics. CAB International, Wallingford, UK, 602 pp
Acknowledgements
The authors will like to acknowledge the following for their contributions and support; ICIPE and the African Fruit Fly Initiative (AFFI) (for logistics and biological materials). We would also like to thank S. Dupas (IRD, Paris, France), M. De Meyer (Tervuren Museum, Belgium), M. Mansell (USDA-APHIS, South Africa), I. M. White (NHM, UK), M. Wandago, J. Rume and P. Nderitu (all of ICIPE) for various contributions. Funding was by the Dutch Government (DSO) through the African Regional Postgraduate Programme in Insect Science (ARPPIS), and in part by the International Foundation for Science (IFS), Sweden (Grant No. C3190/1 to M. K. Billah of University of Ghana and ICIPE).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Billah, M.K., Kimani-Njogu, S.W., Wharton, R.A. et al. Cross mating studies among five fruit fly parasitoid populations: potential biological control implications for tephritid pests . BioControl 53, 709–724 (2008). https://doi.org/10.1007/s10526-007-9108-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10526-007-9108-y