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Estimating SIT-driven population reduction in the Mediterranean fruit fly, Ceratitis capitata, from sterile mating

Published online by Cambridge University Press:  20 January 2014

M. Juan-Blasco ,
B. Sabater-Muñoz ,
I. Pla ,
R. Argilés ,
P. Castañera ,
J. A. Jacas ,
M. V. Ibáñez-Gual  and
A. Urbaneja
M. Juan-Blasco
Affiliation:
Instituto Valenciano de Investigaciones Agrarias (IVIA), Centro de Protección Vegetal y Biotecnología, Unidad Asociada de Entomología UJI-IVIA-CIB (CSIC), E-46113 Moncada, Spain
B. Sabater-Muñoz
Affiliation:
Instituto Valenciano de Investigaciones Agrarias (IVIA), Centro de Protección Vegetal y Biotecnología, Unidad Asociada de Entomología UJI-IVIA-CIB (CSIC), E-46113 Moncada, Spain
I. Pla
Affiliation:
Departamento de Plagas, Transformaciones Agrarias SA (TRAGSA), E-46980 Paterna, Spain
R. Argilés
Affiliation:
Departamento de Plagas, Transformaciones Agrarias SA (TRAGSA), E-46980 Paterna, Spain
P. Castañera
Affiliation:
Departamento de Biología Medioambiental, Consejo Superior de Investigaciones Científicas (CSIC), Centro de Investigaciones Biológicas (CIB), Unidad Asociada de Entomología IVIA-CIB (CSIC), E-28040 Madrid, Spain
J. A. Jacas
Affiliation:
Departament de Ciències Agràries i del Medi Natural, Universitat Jaume I (UJI), Unitat Associada d'Entomologia UJI-IVIA, Campus del Riu Sec, E-12071 Castelló de la Plana, Spain
M. V. Ibáñez-Gual
Affiliation:
Departament de Matemàtiques, Universitat Jaume I (UJI), Campus del Riu Sec, E-12071 Castelló de la Plana, Spain
A. Urbaneja*
Affiliation:
Instituto Valenciano de Investigaciones Agrarias (IVIA), Centro de Protección Vegetal y Biotecnología, Unidad Asociada de Entomología UJI-IVIA-CIB (CSIC), E-46113 Moncada, Spain
*
*Author for correspondence Phone: +34 963424130 Fax: +34 963424001 E-mail: [email protected]
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Abstract

Area-wide sterile insect technique (SIT) programs assume that offspring reduction of the target population correlates with the mating success of the sterile males released. However, there is a lack of monitoring tools to prove the success of these programs in real-time. Field-cage tests were conducted under the environmental conditions of the Mediterranean coast of Spain to estimate: (a) the mating success of sterile Vienna-8 (V8) Ceratitis capitata males using molecular markers and (b) their efficacy to reduce C. capitata populations under six release ratios of wild females to wild males to V8 males (1:0:0, 1:1:0, 1:1:1, 1:1:5, 1:1:10, and 1:1:20). Statistical models were developed to predict: (a) the number of females captured in traps, (b) sperm ID (sterile or not) in spermathecae of the trapped females, and (c) the viable offspring produced, using release ratio and temperature as predictors. The number of females captured was affected by relative humidity. However, its influence in the model was low. Female captures were significantly higher in ratios 1:0:0 compared to ratios where V8 males were released. The proportion of V8 sperm in spermathecae increased with temperature and with the number of V8 males released, but leveled off between ratios 1:1:10 and 1:1:20. In all seasons, except winter (no offspring), viable offspring increased with temperature and was lowest for ratio 1:1:20. For the first time, a strong negative relationship between proportion of V8 sperm detected by molecular tools and C. capitata offspring was established. The models obtained should contribute to enhance the efficacy of SIT programs against this pest.

Keywords

fruit fliesmating successmonitoring tooloverflooding ratioTephritidaeVienna-8
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 104 , Issue 2 , April 2014 , pp. 233 - 242
Copyright
Copyright © Cambridge University Press 2014 

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References

Abbott, W.S. (1925) A method of computing the effectiveness of an insecticide. Journal of Economic Entomology 18, 265–267.CrossRefGoogle Scholar
Aketarawong, N., Chinvinijkul, S., Orankanok, W., Guglielmino, C.R., Franz, G., Malacrida, A.R. & Thanaphum, S. (2011) The utility of microsatellite DNA markers for the evaluation of area-wide integrated pest management using SIT for the fruit fly, Bactrocera dorsalis (Hendel), control programs in Thailand. Genetica 139, 129–140.CrossRefGoogle ScholarPubMed
Aluja, M. & Mangan, R.L. (2008) Fruit Fly (Diptera: Tephritidae) host status determination: critical conceptual, methodological, and regulatory considerations. Annual Review of Entomology 53, 473–502.Google Scholar
Barclay, H.J. (2005) Mathematical models for the use of sterile insects. pp. 147–174 in Dyck, V.A., Hendrichs, J. & Robinson, A.S. (Eds) Sterile Insect Technique. Principles and Practice in Area-Wide Integrated Pest Management. Dordrecht, The Netherlands, Springer.Google Scholar
Barry, J.D., McInnis, D.O., Gates, D. & Morse, J.G. (2003) Effects of irradiation on Mediterranean fruit flies (Diptera: Tephritidae): Emergence, survivorship, lure attraction, and mating competition. Journal of Economic Entomology 96 (3), 615–622.Google Scholar
Barry, J.D., Blessinger, T. & Morse, J.G. (2004) Recapture of sterile Mediterranean fruit flies (Diptera: Tephritidae) in California's preventative release program. Journal of Economic Entomology 97 (5), 1554–1562.CrossRefGoogle ScholarPubMed
Bateman, M.A. (1972) The ecology of fruit flies. Annual Review of Entomology 17, 493–518.CrossRefGoogle Scholar
Bonizzoni, M., Katsoyannos, B.I., Marguerie, R., Guglielmino, C.R., Gasperi, G., Malacrida, A. & Chapman, T. (2002) Microsatellite analysis reveals remating by wild Mediterranean fruit fly females, Ceratitis capitata . Molecular Ecology 11, 1915–1921.CrossRefGoogle ScholarPubMed
Breslow, N.E. & Clayton, D.G. (1993) Approximate inference in generalized linear mixed models. Journal of the American Statistical Association 88, 9–25.Google Scholar
Burk, T. & Calkins, C.O. (1983) Medfly mating behavior and control strategies. Florida Entomologist 66 (1), 33–18.Google Scholar
Calkins, C. & Parker, A. (2005) Sterile insect quality. pp. 269–296 in Dyck, V.A., Hendrichs, J. & Robinson, A.S. (Eds) Sterile Insect Technique. Principles and Practice in Area-Wide Integrated Pest Management. Dordrecht, The Netherlands, Springer.CrossRefGoogle Scholar
Christenson, L.D. & Foote, R.H. (1960) Biology of fruit flies. Annual Review of Entomology 5, 171–192.CrossRefGoogle Scholar
Duyck, P.F. & Quilici, S. (2002) Survival and development of different life stages of three Ceratitis spp. (Diptera: Tephritidae) reared at five constant temperatures. Bulletin of Entomological Research 92, 461–469.Google Scholar
[EPPO] European and Mediterranean Plant Protection Organization. (2013) PQR – EPPO database on quarantine pests. Available via http://www.eppo.int Google Scholar
[FAO/IAEA/USDA] Food and Agriculture Organization of the United Nations/International Atomic Energy Agency/United States Department of Agriculture. (2003) Manual for Product Quality Control and Shipping Procedures for Sterile Mass-Reared Tephritid Fruit Flies. pp. 85, Vienna, Austria, International Atomic Energy Agency.Google Scholar
Fritz, A.H., Dhakal, P., Fritz, G.N. & Kirby, L.A. (2010) Isolating, amplifying and quantifying sperm DNA in Anastrepha suspensa (Diptera: Tephritidae). Florida Entomologist 93 (1), 63–72.CrossRefGoogle Scholar
Hendrichs, J. & Hendrichs, M.A. (1990) Mediterranean fruit fly (Diptera: Tephritidae) in nature: location and diel pattern of feeding and other activities on fruiting and non-fruiting hosts and nonhosts. Annals of the Entomological Society of America 83 (3), 632–641.CrossRefGoogle Scholar
Hendrichs, J., Robinson, A.S., Cayol, J.P. & Enkerlin, W. (2002) Medfly areawide sterile insect technique programmes for prevention, suppression or eradication: the importance of mating behavior studies. Florida Entomologist 85 (1), 1–13.Google Scholar
Hendrichs, J., Vreysen, M.J.B., Enkerlin, W.R. & Cayol, J.P. (2005) Strategic options in using sterile insects for area-wide integrated pest management. pp. 563–600 in Dyck, V.A., Hendrichs, J. & Robinson, A.S. (Eds) Sterile Insect Technique. Principles and Practice in Area-Wide Integrated Pest Management. Dordrecht, The Netherlands, Springer.Google Scholar
Hendrichs, J., Kenmore, P., Robinson, A.S. & Vreysen, M.J.B. (2007) Areawide integrated pest management (AW-IPM): principles, practice and prospects. pp 3–33 in Vreysen, M.J.B., Robinson, A.S. & Hendrichs, J. (Eds) Area-Wide Control of Insect Pests: From Research to Field Implementation. Dordrecht, The Netherlands, Springer.Google Scholar
Holbrook, F.R. & Fujimoto, M.S. (1970) Mating competitiveness of unirradiated and irradiated Mediterranean fruit flies. Journal of Economic Entomology 63 (4), 1175–1176.Google Scholar
[IAEA] International Atomic Energy Agency. (2003) Trapping Guidelines for Area-Wide Fruit Fly Programmes. pp. 48, Vienna, Austria, International Atomic Energy Agency.Google Scholar
Itô, Y. & Yamamura, K. (2005) Role of population and behavioural ecology in the sterile insect technique. pp. 177–208 in Dyck, V.A., Hendrichs, J. & Robinson, A.S. (Eds) Sterile Insect Technique. Principles and Practice in Area-Wide Integrated Pest Management. Dordrecht, The Netherlands, Springer.Google Scholar
Juan-Blasco, M., Tena, A., Vanaclocha, P., Cambra, M., Urbaneja, A. & Monzó, C. (2011) Efficacy of a micro-encapsulated formulation compared with a sticky barrier for excluding ants from citrus canopies. Journal of Applied Entomology 135, 467–472.Google Scholar
Juan-Blasco, M., Urbaneja, A., San Andrés, V., Castañera, P. & Sabater-Muñoz, B. (2013 a) Improving the sterile sperm identification method for its implementation in the area-wide Sterile Insect Technique program against Ceratitis capitata (Diptera: Tephritidae) in Spain. Journal of Economic Entomology 106, 2541–2547.Google Scholar
Juan-Blasco, M., Urbaneja, A. & Sabater-Muñoz, B. (2013 a) Improving the sterile sperm identification method for its implementation in the area-wide Sterile Insect Technique program against Ceratitis capitata (Diptera: Tephritidae) in Spain. Journal of Economic Entomology, accepted 10 July 2013. doi:http://dx.doi.org/10.1603/EC13064 Google Scholar
Juan-Blasco, M., Sabater-Muñoz, B., Argilés, R., Jacas, J.A., Castañera, P. & Urbaneja, A. (2013 b) Molecular sterile sperm detection to monitor Ceratitis capitata population reduction in SIT programs. Pest Management Science 69, 857–864.Google Scholar
Juan-Blasco, M., San Andrés, V., Martínez-Utrillas, M.A., Argilés, R., Pla, I., Urbaneja, A. & Sabater-Muñoz, B. (2013 c) Alternatives to ginger root oil aromatherapy for improved mating performance of sterile Ceratitis capitata (Diptera: Tephritidae) males. Journal of Applied Entomology 137, 244–251.CrossRefGoogle Scholar
Katsoyannos, B.I., Papadopoulos, N.T., Kouloussis, N.A., Heath, R. & Hendrichs, J. (1999) Method of assessing the fertility of wild Ceratitis capitata (Diptera: Tephritidae) females for use in sterile insect technique programs. Journal of Economic Entomology 92 (3), 590–597.Google Scholar
Klassen, W. (2005) Area-wide integrated pest management and the sterile insect technique. pp. 39–68 in Dyck, V.A., Hendrichs, J. & Robinson, A.S. (Eds) Sterile Insect Technique. Principles and Practice in Area-Wide Integrated Pest Management. Dordrecht, The Netherlands, Springer.CrossRefGoogle Scholar
Knipling, E.F. (1955) Possibilities of insect control or eradication through the use of sexual sterile males. Journal of Economic Entomology 48 (4), 459–462.Google Scholar
Lance, D.R. & McInnis, D.O. (2005) Biological basis of the sterile insect technique. pp. 69–94 in Dyck, V.A., Hendrichs, J. & Robinson, A.S. (Eds) Sterile Insect Technique. Principles and Practice in Area-Wide Integrated Pest Management. Dordrecht, The Netherlands, Springer.Google Scholar
Liebhold, A.M. & Tobin, P.C. (2008) Population ecology of insect invasions and their management. Annual Review of Entomology 53, 387–408.Google Scholar
Liquido, N.J., Shinoda, L.A. & Cunningham, R.T. (1991) Host plants of the Mediterranean fruit fly (Diptera: Tephritidae): an annotated world review. Miscellaneous Publications of the Entomological Society of America 77, 1–52.Google Scholar
Martínez-Ferrer, M.T., Navarro, C., Campos, J.M., Marzal, C., Fibla, J.M., Bargues, L. & Garcia-Marí, F. (2010) Seasonal and annual trends in field population of Mediterranean fruit fly, Ceratitis capitata, in Mediterranean citrus groves: comparison of two geographic areas in eastern Spain. Spanish Journal of Agricultural Research 8 (3), 757–765.Google Scholar
Martínez-Ferrer, M.T., Campos, J.M. & Fibla, J.M. (2012) Field efficacy of Ceratitis capitata (Diptera: Tephritidae) mass trapping technique on clementine groves in Spain. Journal of Applied Entomology 136, 181–190.CrossRefGoogle Scholar
McInnis, D.O., Tam, S., Grace, C. & Miyashita, D. (1994) Population suppression and sterility rates induced by variable sex ratio sterile insect releases of Ceratitis capitata (Diptera:Tephritidae) in Hawaii. Annals of the Entomological Society of America 87, 231–240.CrossRefGoogle Scholar
Meixner, M.D., McPheron, B.A., Silva, J.G., Gasparich, G.E. & Sheppard, W.S. (2002) The Mediterranean fruit fly in California: evidence for multiple introductions and persistent populations based on microsatellite and mitochondrial DNA variability. Molecular Ecology 11, 891–899.Google Scholar
Miranda, M.A., Alonso, R. & Alemany, A. (2001) Field evaluation of medfly (Dipt., Tephritidae) female attractants in a Mediterranean agrosystem (Balearic Islands, Spain). Journal of Applied Entomology 125, 333–339.CrossRefGoogle Scholar
Mumford, J.D. (2005) Application of benefit/cost analysis to insect pest control using the sterile insect technique. pp 481–498 in Dyck, V.A., Hendrichs, J. & Robinson, A.S. (Eds) Sterile Insect Technique. Principles and Practice in Area-Wide Integrated Pest Management. Dordrecht, The Netherlands, Springer.Google Scholar
Myers, J.H., Savoie, A. & Van Randen, E. (1998) Eradication and pest management. Annual Review of Entomology 43, 471–491.Google Scholar
Nagel, P. & Peveling, R. (2005) Environment and the sterile insect technique pp. 499–524 in Dyck, V.A., Hendrichs, J. & Robinson, A.S. (Eds) Sterile Insect Technique. Principles and Practice in Area-Wide Integrated Pest Management. Dordrecht, The Netherlands, Springer.CrossRefGoogle Scholar
Navarro-Llopis, V., Alfaro, F., Domínguez, J., Sanchis, J. & Primo, J. (2008) Evaluation of traps and lures for mass-trapping of Mediterranean fruit fly in citrus groves. Journal of Economic Entomology 101 (1), 126–131.Google Scholar
Navarro-Llopis, V., Vacas, S., Sanchis, J., Primo, J. & Alfaro, C. (2011) Chemosterilant bait stations coupled with sterile insect technique: an integrated strategy to control the Mediterranean fruit fly (Diptera: Tephritidae). Journal Economic Entomology 104 (5), 1647–1655.Google Scholar
Papadopoulos, N.T., Katsoyannos, B.I., Carey, J.R. & Kouloussis, N.A. (2001) Seasonal and annual occurrence of the Mediterranean fruit fly (Diptera: Tephritidae) in northern Greece. Annals of the Entomological Society of America 94, 41–50.Google Scholar
Pereira, R., Yuval, B., Liedo, P., Teal, P.E.A., Shelly, T.E., McInnis, D.O. & Hendrichs, J. (2013) Improving sterile male performance in support of programmes integrating the sterile insect technique against fruit flies. Journal of Applied Entomology 137, 178–190.Google Scholar
R Development Core Team (2013) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. Available via http://www.R-project.org Google Scholar
Rendón, P., McInnis, D.O., Lance, D. & Stewart, J. (2004) Medfly (Diptera: Tephritidae) genetic sexing: large-scale field comparison of males-only and bisexual sterile fly releases in Guatemala. Journal of Economic Entomology 97 (5), 1547–1553.Google Scholar
Sabater-Muñoz, B., Martins, D.S., Skouri, W., Laurín, C., Tur, C. & Beitia, F. (2009) Primeros ensayos sobre la utilización de Diachasmimorpha tryoni (Hymenoptera, Braconidae) para el control biológico de Ceratitis capitata (Diptera, Tephritidae) en la Comunidad Valenciana. Levante Agrícola 398, 372–376 (in Spanish).Google Scholar
San Andrés, V., Urbaneja, A., Sabater-Muñoz, B. & Castañera, P. (2007 a) A novel molecular approach to assess mating success of sterile Ceratitis capitata (Diptera: Tephritidae) males in sterile insect technique programs. Journal of Economic Entomology 100 (4), 1444–1449.Google Scholar
San Andrés, V., Ortego, F., Castañera, P. (2007 b) Effects of gamma-irradiation on midgut proteolytic activity of the Mediterranean fruit fly, Ceratitis capitata (Diptera: Tephritidae). Archives of Insect Biochemistry and Physiology 65 (1), 11–19.Google Scholar
San Andrés, V., Pérez-Panadés, J., Carbonell, E.A., Castañera, P. & Urbaneja, A. (2009) Effects of post-teneral nutrition and ginger root oil exposure on longevity and mortality in bait treatments of sterile male Ceratitis capitata . Entomologia Experimentalis et Applicata 132, 256–263.Google Scholar
Shelly, T.E., McInnis, D.O., Rodd, C., Edu, J. & Pahio, E. (2007 a) Sterile insect technique and Mediterranean fruit fly (Diptera: Tephritidae): assessing the utility of aromatherapy in a Hawaiian coffee field. Journal of Economic Entomology 100 (2), 273–282.CrossRefGoogle Scholar
Shelly, T.E., Edu, J. & Pahio, E. (2007 b) Age-dependent variation in mating success of sterile male Mediterranean fruit flies (Diptera: Tephritidae): implications for sterile insect technique. Journal of Economic Entomology 100 (4), 1180–1187.Google Scholar
Tormos, J., Asis, J., Sabater-Muñoz, B., Baños, L., Gayubo, S.F. & Beitia, F. (2012) Superparasitism in laboratory rearing of Spalangia cameroni (Hymenoptera: Pteromalidae), a parasitoid of medfly (Diptera: Tephritidae). Bulletin of Entomological Research 102, 51–61.CrossRefGoogle ScholarPubMed
Urbaneja, A., Chueca, P., Montón, H., Pascual-Ruiz, S., Dembilio, O., Vanaclocha, P., Abad-Moyano, R., Pina, T. & Castañera, P. (2009) Chemical alternatives to malathion for controlling Ceratitis capitata (Diptera: Tephritidae), and their side effects on natural enemies in Spanish citrus orchards. Journal of Economic Entomology 102 (1), 144–151.Google Scholar
Vargas, R.I., Harris, E.J. & Nishida, T. (1983) Distribution and seasonal occurrence of Ceratitis capitata (Wiedemann) (Diptera: Tephritidae) on the island of Kauai in the Hawaiian Islands. Environmental Entomology 12, 303–310.Google Scholar
Vreysen, M.J. (2001) Principles of area-wide integrated tsetse fly control using the sterile insect technique. Medécine Tropicale 61, 397–411.Google Scholar
Vreysen, M. (2005) Monitoring sterile and wild insects in area-wide integrated pest management programmes. pp. 325–361 in Dyck, V.A., Hendrichs, J. & Robinson, A.S. (Eds) Sterile Insect Technique. Principles and Practice in Area-Wide Integrated Pest Management. Dordrecht, The Netherlands, Springer.Google Scholar
Warburg, M.S. & Yuval, B. (1997) Circadian patterns of feeding and reproductive activities of Mediterranean fruit flies (Diptera: Tephritidae) on various hosts in Israel. Annals of the Entomological Society of America 90, 487–495.Google Scholar
Waterhouse, D.F., LaChance, L.E. & Whitten, M.J. (1976) Use of autocidal methods. pp. 637–59 in Huffaker, D.B. & Messenger, P.S. (Eds) Theory and Practice of Biological Control. New York, San Francisco, London, Academic Press.CrossRefGoogle Scholar
White, I.M. & Elson-Harris, M.M. (1992) Fruit Flies of Economic Significance: Their Identification and Bionomics. Wallingford, UK/Canberra, CAB International/Australian Centre for International Agricultural Research.Google Scholar
Wong, T.T.Y., Kobayashi, R.M. & McInnis, D.O. (1986) Mediterranean fruit fly (Diptera:Tephritidae): methods of assessing the effectiveness of sterile insect releases. Journal of Economic Entomology 79 (6), 1501–1506.Google Scholar
Yamagishi, M., Kakinohana, H., Kuba, H., Kohama, T., Nakamoto, Y., Sokei, Y. & Kinjo, K. (1993) Eradication of the melon fly from Okinawa, Japan, by means of the sterile insect technique. pp. 49–60 in Proceedings of an IAEA/FAO Symposium «IAEA-SM-327/4-Management of insect pests: nuclear and related molecular and genetic techniques», 19–23 October 1992, Vienna, Austria.Google Scholar
Yamanaka, T. & Liebhold, A.M. (2009) Spatially implicit approaches to understanding the manipulation of mating success for insect invasion management. Population Ecology 51, 427–444.CrossRefGoogle Scholar
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