Hostname: page-component-cd9895bd7-mkpzs Total loading time: 0 Render date: 2024-12-25T17:59:30.623Z Has data issue: false hasContentIssue false
  • English
  • Français

Precocious sexual signalling and mating in Anastrepha fraterculus (Diptera: Tephritidae) sterile males achieved through juvenile hormone treatment and protein supplements

Published online by Cambridge University Press:  29 August 2012

M.C. Liendo ,
F. Devescovi ,
G.E. Bachmann ,
M.E. Utgés ,
S. Abraham ,
M.T. Vera ,
S.B. Lanzavecchia ,
J.P. Bouvet ,
P. Gómez-Cendra  and
J. Hendrichs
...Show all authors
M.C. Liendo
Affiliation:
Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Argentina
F. Devescovi
Affiliation:
Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Argentina
G.E. Bachmann
Affiliation:
Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Argentina
M.E. Utgés
Affiliation:
Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Argentina Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires (FCEyN, UBA), Argentina
S. Abraham
Affiliation:
Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Argentina Facultad de Agronomía y Zootecnia, Universidad Nacional de Tucumán (FAZ, UNT), Argentina
M.T. Vera
Affiliation:
Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Argentina Facultad de Agronomía y Zootecnia, Universidad Nacional de Tucumán (FAZ, UNT), Argentina
S.B. Lanzavecchia
Affiliation:
Instituto de Genética ‘E.A. Favret’, INTA, Los Reseros y Nicolás Repetto, 1712 Castelar, Buenos Aires, Argentina
J.P. Bouvet
Affiliation:
Estación Experimental Agropecuaria Concordia, INTA, Argentina
P. Gómez-Cendra
Affiliation:
Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires (FCEyN, UBA), Argentina
J. Hendrichs
Affiliation:
Joint FAO/IAEA Programme of Nuclear Techniques in Food and Agriculture, Insect Pest Control Section, Vienna, Austria
P.E.A. Teal
Affiliation:
Center for Medical, Agricultural, and Veterinary Entomology, US Department of Agriculture – Agricultural Research Service, Florida, USA
J.L. Cladera
Affiliation:
Instituto de Genética ‘E.A. Favret’, INTA, Los Reseros y Nicolás Repetto, 1712 Castelar, Buenos Aires, Argentina
D.F. Segura*
Affiliation:
Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Argentina Instituto de Genética ‘E.A. Favret’, INTA, Los Reseros y Nicolás Repetto, 1712 Castelar, Buenos Aires, Argentina
*
*Author for correspondence Fax: +54 11 4450 0805 E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Sexual maturation of Anastrepha fraterculus is a long process. Methoprene (a mimic of juvenile hormone) considerably reduces the time for sexual maturation in males. However, in other Anastrepha species, this effect depends on protein intake at the adult stage. Here, we evaluated the mating competitiveness of sterile laboratory males and females that were treated with methoprene (either the pupal or adult stage) and were kept under different regimes of adult food, which varied in the protein source and the sugar:protein ratio. Experiments were carried out under semi-natural conditions, where laboratory flies competed over copulations with sexually mature wild flies. Sterile, methoprene-treated males that reached sexual maturity earlier (six days old), displayed the same lekking behaviour, attractiveness to females and mating competitiveness as mature wild males. This effect depended on protein intake. Diets containing sugar and hydrolyzed yeast allowed sterile males to compete with wild males (even at a low concentration of protein), while brewer´s yeast failed to do so even at a higher concentration. Sugar only fed males were unable to achieve significant numbers of copulations. Methoprene did not increase the readiness to mate of six-day-old sterile females. Long pre-copulatory periods create an additional cost to the management of fruit fly pests through the sterile insect technique (SIT). Our findings suggest that methoprene treatment will increase SIT effectiveness against A. fraterculus when coupled with a diet fortified with protein. Additionally, methoprene acts as a physiological sexing method, allowing the release of mature males and immature females and hence increasing SIT efficiency.

Keywords

sterile insect techniquesexual maturationmating competitivenesslekking behaviourjuvenile hormonemethoprenenutrition
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 103 , Issue 1 , February 2013 , pp. 1 - 13
Copyright
Copyright © Cambridge University Press 2012

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

Abraham, S., Goane, L., Cladera, J. & Vera, M.T. (2011) Effects of male nutrition on sperm storage and remating behavior in wild and laboratory Anastrepha fraterculus (Diptera: Tephritidae) females. Journal of Insect Physiology 57, 1501–1509.Google Scholar
Allinghi, A., Calcagno, G., Petit-Marty, N., Gómez Cendra, P., Segura, D., Vera, M.T., Cladera, J., Gramajo, C., Willink, E. & Vilardi, J. (2007a) Compatibility and competitiveness of a laboratory strain of Anastrepha fraterculus (Diptera: Tephritidae) after irradiation treatment. The Florida Entomologist 90, 27–32.Google Scholar
Allinghi, A., Gramajo, C., Willink, E. & Vilardi, J. (2007b) Induction of sterility in Anastrepha fraterculus (Diptera: Tephritidae) by gamma radiation. The Florida Entomologist 90, 96–102.Google Scholar
Aluja, M., Jácome, I. & Macías-Ordóñez, R. (2001) Effects of adult nutrition on male sexual performance in four neotropical fruit fly species of the genus Anastrepha (Diptera: Tephritidae). Journal of Insect Behavior 14, 759–775.Google Scholar
Aluja, M., Ordano, M., Teal, P.E., Sivinski, J., García-Medel, D. & Anzures-Dadda, A. (2009) Larval feeding substrate and species significantly influence the effect of a juvenile hormone analog on sexual development/performance in four tropical tephritid flies. Journal of Insect Physiology 55, 231–242.Google Scholar
Blay, S. & Yuval, B. (1997) Nutritional correlates of reproductive success of male Mediterranean fruit flies (Diptera: Tephritidae). Animal Behaviour 54, 59–66.Google Scholar
Braga Sobrinho, R., Guimaraes, J.A., Araujo, E.L. & Moreira, M.A.B. (2010) Suitable larval diet for Anastrepha fraterculus (Diptera: Tephritidae). p. 226 in Proceedings of the 8th International Symposium on Fruit Flies of Economic Importance. 26 September–1 October 2010, Valencia, Spain.Google Scholar
Briceño, R.D. & Eberhard, W.G. (1998) Medfly courtship duration: a sexually selected reaction norm changed by crowding. Ethology Ecology and Evolution 10, 369–382.Google Scholar
Briceño, R.D. & Eberhard, W.G. (2002) Decisions during courtship by male and female medflies (Diptera: Tephritidae): correlated changes in male behavior and female acceptance criteria in mass-reared flies. The Florida Entomologist 85, 14–31.Google Scholar
Calcagno, G.E., Vera, M.T., Manso, F., Lux, S.A., Norry, F.M., Munyiri, F.N. & Vilardi, J.C. (1999) Courtship behavior of wild and mass-reared Mediterranean fruit fly (Diptera: Tephritidae) males from Argentina. Journal of Economic Entomology 92, 373–379.Google Scholar
Carhan, A., Allen, F., Armstrong, J.D., Goodwin, S.F. & O'Dell, M.C. (2005) Female receptivity phenotype of icebox mutants caused by a mutation in the L1-type cell adhesion molecule neuroglian. Genes, Brain and Behavior 4, 449–465.Google Scholar
Cayol, J.P., Vilardi, J., Rial, E. & Vera, M.T. (1999) New indices and method to measure the sexual compatibility and mating performance of Ceratitis capitata (Diptera: Tephritidae) laboratory strains under field cage conditions. Journal of Economic Entomology 92, 140–145.Google Scholar
Dyck, V.A., Reyes Flores, J., Vreysen, M.J.B., Regidor Fernández, E.E., Teruya, T., Barnes, B., Gómez Riera, P., Lindquist, D. & Loosjes, M. (2005) Management of area-wide integrated pest management programmes that integrate the sterile insect technique. pp. 525–545in Dyck, V.A., Hendrichs, J. & Robinson, A.S. (Eds) Sterile Insect Technique: Principles and Practice in Area-Wide Integrated Pest Management. The Netherlands, Springer, Dordrecht.Google Scholar
Enkerlin, W. (2007) Guidance for packing, shipping, holding and release of sterile flies in area-wide fruit fly control programmes. FAO Plant Production and Protection Paper 190. FAO, Rome, Italy.Google Scholar
Fanson, B.G. & Taylor, P.W. (2012) Additive and interactive effects of nutrient classes on longevity, reproduction, and diet consumption in the Queensland fruit fly (Bactrocera tryoni). Journal of Insect Physiology 58, 327–334.Google Scholar
FAO/IAEA/USDA (2003) Manual for product quality control and shipping procedures for sterile mass-reared tephritid fruit flies. International Atomic Energy Agency, Vienna, Austria.Google Scholar
Franz, G. (2005) Genetic sexing strains in Mediterranean fruit fly, an example for other species amenable to large-scale rearing for the sterile insect technique. pp. 427–451in Dyck, V.A., Hendrichs, J. & Robinson, A.S. (Eds) Sterile Insect Technique: Principles and Practice in Area-Wide Integrated Pest Management. The Netherlands, Springer, Dordrecht.CrossRefGoogle Scholar
García Carrión, J. (2010) Artificial rearing of Anastrepha fraterculus (Wiedemann 1830) (Diptera: Tephritidae): egg-viability and models of cage. p. 69 in Proceeding of the12th Workshop of the Arthropod Mass Rearing and Quality Control Working Group of the IOBC “Blueprint for the future of arthropod rearing and quality assurance”. 19–22 October 2010, Vienna, Austria.Google Scholar
García Carrión, J., Alburqueque, M. & Quintanilla, L. (2010) Mating competitiveness of sterile mass-reared males and females populations of Anastrepha fraterculus (Wiedemann) (Diptera: Tephritidae). pp. 62–69 in Proceedings of the 8th International Symposium on Fruit Flies of Economic Importance. 26 September–1 October 2010, Valencia, Spain.Google Scholar
Gavriel, S., Gazit, Y. & Yuval, B. (2010) Effect of diet on survival, in the laboratory and the field, of sterile male Mediterranean fruit flies. Entomologia Experimentalis et Applicata 135, 96–104.Google Scholar
Gavriel, S., Gazit, Y., Leach, A., Mumford, J. & Yuval, B. (2012) Spatial patterns of sterile Mediterranean fruit fly dispersal. Entomologia Experimentalis et Applicata 142, 17–26.Google Scholar
Gómez Cendra, P., Segura, D., Allinghi, A., Cladera, J. & Vilardi, J. (2007) Comparison of longevity between a laboratory strain and a natural population of Anastrepha fraterculus (Diptera: Tephritidae) under field cage conditions. The Florida Entomologist 90, 147–153.Google Scholar
Guillén, D. & Sánchez, R. (2007) Expansion of the National Fruit Fly Control Program in Argentina. pp. 653–660in Vreysen, M.J.B., Robinson, A.S. & Hendrichs, J. (Eds) Area-Wide Control of Insect Pests: From Research to Field Implementation. Joint FAO/IAEA Programme of Nuclear Techniques in Food and Agriculture. Dordrecht, The Netherlands, Vienna, Austria. Springer.CrossRefGoogle Scholar
Happ, G.M. (1992) Maturation of the male reproductive system and its endocrine regulation. Annual Review of Entomology 37, 303–320.Google Scholar
Haq, I., Cáceres, C., Hendrichs, J., Teal, P.E.A., Stauffer, C. & Robinson, A.S. (2010a) Methoprene modulates the effect of diet on male melon fly, Bactrocera cucurbitae, performance at mating aggregations. Entomologia Experimentalis et Applicata 136, 21–30.Google Scholar
Haq, I., Cáceres, C., Hendrichs, J., Teal, P., Wornoayporn, V., Stauffer, C. & Robinson, A.S. (2010b) Effects of the juvenile hormone analogue methoprene and dietary protein on male melon fly Bactrocera cucurbitae (Diptera: Tephritidae) mating success. Journal of Insect Physiology 56, 1503–1509.Google Scholar
Hendrichs, J., Katsoyannos, B.J. & Prokopy, R.J. (1993a) Bird feces in the nutrition of adult Mediterranean fruit flies Ceratitis capitata (Diptera: Tephritidae) in nature. Mitteilungen der Deutschen Gesellschaft für Allgemeine und Angewandte Entomologie 8, 703–707.Google Scholar
Hendrichs, J., Wornoayporn, V., Katsoyannos, B.I. & Gaggl, K. (1993b) First field assessment of the dispersal and survival of mass reared sterile Mediterranean fruit fly males of an embryonal, temperature sensitive genetic sexing strain. pp. 453–462in Hendrichs, J. (Ed.) Management of Insect Pests: Nuclear and Related Molecular and Genetic Techniques. Vienna, Austria, IAEA.Google Scholar
Hendrichs, M.A., Wornoayporn, V., Katsoyannos, B. & Hendrichs, J. (2007) Quality control method to measure predator evasion in wild and mass-reared Mediterranean fruit flies (Diptera: Tephritidae). The Florida Entomologist 90, 64–70.Google Scholar
Hernández-Ortiz, V., Bartolucci, A., Frias, D., Moralles-Valles, P. & Selivon, D. (2012) Cryptic species of the Anastrepha fraterculus complex (Diptera: Tephritidae): a multivariate approach for the recognition of South American morphotypes. Annals of the Entomological Society of America 105, 305–318.Google Scholar
Jaldo, H.E., Gramajo, M.C. & Willink, E. (2001) Mass rearing of Anastrepha fraterculus (Diptera: Tephritidae): a preliminary strategy. The Florida Entomologist 84, 716–718.Google Scholar
Kaspi, R. & Yuval, B. (2000) Post-teneral protein feeding improves sexual competitiveness but reduces longevity of mass-reared sterile male Mediterranean fruit flies (Diptera: Tephritidae). Annals of the Entomological Society of America 93, 949–955.Google Scholar
Kaspi, R., Taylor, P.W. & Yuval, B. (2000) Diet and size influence sexual advertisement and copulatory success of males in Mediterranean fruit fly leks. Ecological Entomology 25, 279–284.Google Scholar
Knipling, E.F. (1959) Sterile-male method of population control. Science 130, 902–904.Google Scholar
Lance, D. & McInnis, D.O. (2005) Biological basis of the sterile insect technique. pp. 69–94in Vreysen, M.J.B., Robinson, A.S. & Hendrichs, J. (Eds) Area-Wide Control of Insect Pests: From Research to Field Implementation. Joint FAO/IAEA Programme of Nuclear Techniques in Food and Agriculture. Dordrecht, The Netherlands, Vienna, Austria. Springer.Google Scholar
Levy, K., Shelly, T.E. & Yuval, B. (2005) Effects of the olfactory environment and nutrition on the ability of male Mediterranean fruit flies to endure starvation. Journal of Economic Entomology 98, 61–65.Google Scholar
Liedo, P., Salgado, S., Oropeza, A. & Toledo, J. (2007) Improving mating performance of mass-reared sterile Mediterranean fruit flies (Diptera: Tephritidae) through changes in adult holding conditions: demography and mating competitiveness. The Florida Entomologist 90, 33–40.Google Scholar
Malavasi, A., Morgante, J.S. & Prokopy, R.J. (1983) Distribution and activities of Anastrepha fraterculus (Diptera: Tephritidae) flies on host and non-host trees. Annals of the Entomological Society of America 76, 286–292.Google Scholar
McInnis, D.O., Rendon, P. & Komatsu, J. (2002) Mating and remating of medflies (Diptera: Tephritidae) in Guatemala: individual fly marking in field cages. The Florida Entomologist 85, 126–137.Google Scholar
Norrbom, A.L. (2004) Fruit fly (Tephritidae) host plant database. Version November 2004. Available online at http://www.sel.barc.usda.gov:8080/diptera/Tephritidae/TephHosts/search.html (accessed June 2012).Google Scholar
Ortiz, G. (1999) Potential use of the sterile insect technique against the South American fruit fly. pp. 121–130in Hendrichs, J. (Ed.) The South American Fruit Fly, Anastrepha fraterculus (Wied.): Advances in Artificial Rearing,Taxonomic Status and Biological Studies. Vienna, Austria, IAEA.Google Scholar
Oviedo, A., Nestel, D., Papadopoulos, N.T., Ruiz, M.J., Prieto, S.C., Willink, E. & Vera, M.T. (2011) Management of protein intake in the fruit fly Anastrepha fraterculus. Journal of Insect Physiology 57, 1622–1630.CrossRefGoogle ScholarPubMed
Pereira, R., Sivinski, J. & Teal, P.E.A. (2009) Influence of methoprene and dietary protein on male Anastrepha suspensa (Diptera: Tephritidae) mating aggregations. Journal of Insect Physiology 55, 328–335.CrossRefGoogle ScholarPubMed
Pereira, R., Sivinski, J. & Teal, P.E.A. (2010) Influence of a juvenile hormone analog and dietary protein on male Anastrepha suspensa (Diptera: Tephritidae) sexual success. Journal of Economic Entomology 103, 40–46.Google Scholar
Pereira, R., Teal, P.E.A., Conway, H., Worley, J. & Sivinski, J. (2011a) Influence of methoprene and protein on maturation and sexual performance of sterile Anastrepha ludens (Diptera: Tephritidae) males. Journal of Applied Entomology, doi: 10.1111/j.1439-0418.2011.01668.x.Google Scholar
Pereira, R., Yuval, B., Liedo, P., Teal, P.E.A., Shelly, T.E., McInnis, D.O. & Hendrichs, J. (2011b) Improving sterile male performance in support of programmes integrating the sterile insect technique against fruit flies. Journal of Applied Entomology, doi: 10.1111/j.1439-0418.2011.01664.x.Google Scholar
Pérez-Staples, D., Prabhu, V. & Taylor, P.W. (2007) Post-teneral protein feeding enhances sexual performance of Queensland fruit flies. Physiological Entomology 32, 225–232.Google Scholar
Pérez-Staples, D., Weldon, C.W. & Taylor, P.W. (2009) Pre-release feeding on yeast hydrolysate enhances sexual competitiveness of sterile male Queensland fruit flies in field cages. Entomologia Experimentalis et Applicata 131, 159–166.Google Scholar
Petit-Marty, N., Vera, M.T., Calcagno, G., Cladera, J.L., Segura, D.F., Allinghi, A., Rodriguero, M., Gómez Cendra, P., Viscarret, M.M. & Vilardi, J.C. (2004) Sexual behaviour and mating compatibility among four populations of Anastrepha fraterculus (Diptera: Tephritidae) from Argentina. Annals of the Entomological Society of America 97, 1320–1327.Google Scholar
Prabhu, V., Pérez-Staples, D. & Taylor, P.W. (2008) Protein: carbohydrate ratios promoting sexual activity and longevity of male Queensland fruit flies. Journal of Applied Entomology 132, 575–582.CrossRefGoogle Scholar
Ringo, J.M. (2002) Hormonal regulation of sexual behavior in insects. pp. 93–114in Pfaff, D. (Ed.) Hormones, Brain and Behavior. New York, NY, USA, Elsevier Science.Google Scholar
Rull, J., Abraham, S., Kovaleski, A., Segura, D.F., Islam, A., Wornoayporn, V., Dammalage, T., Tomas, U.S. & Vera, M.T. (2012) Random mating and reproductive compatibility among Argentinean and southern Brazilian populations of Anastrepha fraterculus (Diptera: Tephritidae). Bulletin of Entomological Research 102(4), 435–443.Google Scholar
Sciurano, R.B., Segura, D.F., Rodriguero, M., Gómez Cendra, P., Allinghi, A., Cladera, J.L. & Vilardi, J.C. (2007) Sexual selection on multivariate phenotypes in Anastrepha fraterculus (Diptera: Tephritidae) from Argentina. The Florida Entomologist 90, 163–170.Google Scholar
Segura, D.F., Petit-Marty, N., Sciurano, R.B., Vera, M.T., Calcagno, G., Allinghi, A., Gómez Cendra, P., Cladera, J.L. & Vilardi, J.C. (2007) Lekking behavior of Anastrepha fraterculus (Diptera: Tephritidae). The Florida Entomologist 90, 154–162.Google Scholar
Segura, D.F., Cáceres, C., Vera, M.T., Wornoayporn, V., Islam, A., Teal, P.E.A., Cladera, J.L., Hendrichs, J. & Robinson, A.S. (2009) Enhancing mating performance after juvenile hormone treatment in Anastrepha fraterculus: a differential response in males and females acts as a physiological sexing system. Entomologia Experimentalis et Applicata 131, 75–84.Google Scholar
Segura, D.F., Utgés, M.E., Liendo, M.C., Rodríguez, M.F., Devescovi, F., Vera, M.T., Teal, P.E.A. & Cladera, J.L. (2010) Methoprene treatment reduces the pre-copulatory period in Anastrepha fraterculus (Diptera: Tephritidae) sterile males. Journal of Applied Entomology, doi: 10.1111/j.1439-0418.Google Scholar
Segura, D.F., Vera, M.T., Rull, J., Wornoayporn, V., Islam, A. & Robinson, A.S. (2011) Assortative mating among Anastrepha fraterculus (Diptera: Tephritidae) hybrids as a possible route to radiation of the fraterculus cryptic species complex. Biological Journal of the Linnean Society 102, 346–354.Google Scholar
Shelly, T.E. (2000) Male signalling and lek attractiveness in the Mediterranean fruit fly. Animal Behaviour 60, 245–251.Google Scholar
Shelly, T.E. & Kennelly, S. (2002) Influence of male diet on male mating success and longevity and female remating in the Mediterranean fruit fly (Diptera: Tephritidae) under laboratory condition. The Florida Entomologist 85, 572–578.Google Scholar
Shelly, T.E., Edu, J. & Pahio, E. (2005) Influence of diet and methyl eugenol on the mating success of males of the Oriental fruit fly, Bactrocera dorsalis (Diptera: Tephritidae). The Florida Entomologist 88, 307–313.Google Scholar
Shelly, T.E., Edu, J. & Pahio, E. (2007) Condition-dependent mating success in male fruit flies: ingestion of a pheromone precursor compensates for a low-quality diet. Journal of Insect Behavior 20, 347–365.Google Scholar
StatSoft Inc. (2006) STATISTICA for Windows (Computer program manual). Tulsa, OK, USA.Google Scholar
Steck, G.J. (1999) Taxonomic status of Anastrepha fraterculus. pp. 13–20in Hendrichs, J. (Ed.) The South American Fruit Fly, Anastrepha fraterculus (Wied.): Advances in Artificial Rearing,Taxonomic Status and Biological Studies. Vienna, Austria, IAEA.Google Scholar
Taylor, P.W. & Yuval, B. (1999) Postcopulatory sexual selection in Mediterranean fruit flies, Ceratitis capitata: advantages for large and protein-fed males. Animal Behaviour 58, 247–254.Google Scholar
Teal, P.E.A., Gómez-Simuta, Y. & Proveaux, A.T. (2000) Mating experience and juvenile hormone enhance sexual signalling and mating in male Caribbean fruit flies. Proceedings of the National Academy of Sciences of the USA 97, 3708–3712.Google Scholar
Teal, P.E.A., Pereira, R., Segura, D.F., Haq, I., Gómez-Simuta, Y., Robinson, A.S. & Hendrichs, J. (2011) Methoprene and protein supplements accelerate reproductive development and improve mating success of male tephritid flies. Journal of Applied Entomology, doi: 10.1111/j.1439-0418.2010.01606.x.Google Scholar
Utgés, M.E., Vilardi, J.C., Oropeza, A., Toledo, J. & Liedo, P. (2011) Pre-release diet effect on field survival and dispersal of Anastrepha ludens and Anastrepha obliqua (Diptera: Tephritidae). Journal of Applied Entomology, doi: 10.1111/j.1439-0418.2011.01663.x.Google Scholar
Vera, M.T., Cladera, J.L., Calcagno, G., Vilardi, J.C., McInnis, D.O., Stolar, E., Segura, D.F., Peti-Marty, N., Krsticevic, F., Gómez Cendra, P., Rodriguero, M., Barborini, K., Heer, T., Allinghi, A., Bonpland, G., Hansen, L. & Segade, G. (2003) Remating of wild Ceratitis capitata (Diptera: Tephritidae) females in field cages. Annals of the Entomological Society of America 96, 563–570.Google Scholar
Vera, M.T., Cáceres, C., Wornoayporn, V., Islam, A., Robinson, A.S., de la Vega, M.H., Hendrichs, J. & Cayol, J.P. (2006) Mating incompatibility among populations of the South American fruit fly Anastrepha fraterculus (Diptera: Tephritidae). Annals of the Entomological Society of America 99, 387–397.Google Scholar
Vera, M.T., Abraham, S., Oviedo, A. & Willink, E. (2007) Demographic and quality control parameters of Anastrepha fraterculus (Diptera: Tephritidae) maintained under artificial rearing. The Florida Entomologist 90, 53–57.Google Scholar
Vera, M.T., Ruiz, M.J., Oviedo, A., Abraham, S., Mendoza, M., Segura, D.F., Kouloussis, N. & Willink, E. (2010) Fruit compounds affect male sexual success in the South American fruit fly, Anastrepha fraterculus (Diptera: Tephritidae). Journal of Applied Entomology. doi: 10.1111/j.1439-0418.2010.01516.x.Google Scholar
Yuval, B., Kaspi, R., Shloush, S. & Warburg, M.S. (1998) Nutritional reserves regulate male participation in Mediterranean fruit fly leks. Ecological Entomology 23, 211–215.CrossRefGoogle Scholar
Yuval, B., Kaspi, R., Field, S.A., Blay, S. & Taylor, P. (2002) Effects of post-teneral nutrition on reproductive success of male Mediterranean fruit flies (Diptera: Tephritidae). The Florida Entomologist 85, 165–170.Google Scholar
Yuval, B., Maor, M., Levy, K., Kaspi, R., Taylor, P.T. & Shelly, T. (2007) Breakfast of champions or kiss or death? Survival and sexual performance of protein-fed, sterile Mediterranean fruit flies (Diptera: Tephritidae). The Florida Entomologist 90, 115–122.Google Scholar
Zar, J. (1996) Biostatistical Aanalysis. Upper Saddle River, NJ, USA, Prentice-Hall.Google Scholar