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Survival ability of Mexican fruit fly males from different strains in presence of the predatory orb-weaving spider Argiope argentata (Araneae: Araneidae)

Published online by Cambridge University Press:  18 April 2018

A. Dor  and
P. Liedo
A. Dor*
Affiliation:
Consejo Nacional de Ciencias y Tecnologías commissioned to El Colegio de la Frontera Sur, Carretera Antiguo Aeropuerto Km 2.5, C. P. 30700, Tapachula, Chiapas, Mexico
P. Liedo
Affiliation:
El Colegio de la Frontera Sur, Carretera Antiguo Aeropuerto km. 2.5, C.P. 30700 Tapachula, Chiapas, Mexico
*
*Author for correspondence Phone: +52 962 628 9800 Fax: +52 962 628 9806 E-mail: ador@ecosur.mx
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Abstract

The sterile insect technique (SIT) is a key element for the integrated management of pest populations of the Mexican fruit fly, Anastrepha ludens, in Mexico. Its success depends on the survival of mass-reared sterile males and their ability to mate with wild females. However, colonization and mass-rearing conditions can adversely affect their ability to avoid predators. To test if colony management strategies could contribute to improve field survival abilities of mass-reared flies, we compared the survival of males exposed to the orb-weaver spider Argiope argentata. Males compared originated from three strains with different colonization strategies: (a) a colony started from field-collected wild flies (replacement), (b) a colony started by hybridizing wild males with mass-reared adapted females (hybrid) and (c) a colony started with mass-reared males selected on the basis of their survival ability and mating competitiveness in field cages (selected). Mass-reared males and wild males were used as controls. Males were exposed to spiders under laboratory cage conditions. Overall, wild males showed better survival ability than mass-reared males. Regarding the colonization approach, wild males survived better than a hybrid, replaced and selected males. We conclude that mass-rearing conditions have a strong negative effect on the ability of males to escape spiders. The colonization systems evaluated did not counter this effect. The lower survival of males from the selected colony suggests that the selection over one generation did not contribute to improve males’ predator avoidance and escape abilities and probably needs to be modified. Possible explanations for this and implications on colonization and colony management for SIT purpose are discussed.

Keywords

predation avoidancesterile insect techniquemass-rearingcolony managementAnastrepha ludensTephritidae
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 109 , Issue 3 , June 2019 , pp. 279 - 286
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Copyright
Copyright © Cambridge University Press 2018 

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References

Aluja, M. (1994) Bionomics and management of Anastrepha. Annual Review of Entomology 39, 155–178.Google Scholar
Aluja, M., Jacome, I. & Macias-Ordoñez, R. (2001) Effect of adult nutrition on male sexual performance in four neo-tropical fruit by species of the genus Anastrepha (Diptera: Tephritidae). Journal of Insect Behavior 14, 759–775.Google Scholar
Bosa, C.F., Cruz, L., Zepeda-Cisneros, C., Valle-Mora, J.F., Guillén-Navarro, K. & Liedo, P. (2016) Sexual behavior and male volatile compounds in wild and mass-reared strains of the Mexican fruit fly Anastrepha ludens (Loew) (Diptera: Tephritidae) held under different colony management regimes. Insect Science 23, 105–116.Google Scholar
Bradbury, J.W. (1981) The evolution of leks. pp. 138–169 in Alexander, R.D. & Tinkle, D.W. (Eds) Natural Selection and Social Behavior: Recent Research and New Theory. New York, Chiron Press.Google Scholar
Burk, T. (1982) Evolutionary significance of predation on sexually signaling males. Florida Entomologist 65, 90–104.Google Scholar
Cayol, J.P. (2000) Changes in sexual behavior and life history traits of tephiritid species caused by mass-rearing processes. pp. 843–859 in Aluja, M. & Norrbom, A.L. (Eds) Fruit Flies (Tephritidae): Phylogeny and Evolution of Behavior. Boca Ratón, FL, CRC Press.Google Scholar
Craig, C.L., Wolf, S.G., Davis, J.L.D., Hauber, M.E. & Maas, J.L. (2001) Signal polymorphism in the web-decorating spider Argiope argentata is correlated with reduced survivorship and the presence of stingless bees, its primary prey. Evolution 55, 986–993.Google Scholar
Domínguez, J., Artiaga, T., Solís, E. & Hernández, E. (2010) Métodos de colonización y cría masiva. pp. 259–276 in Montoya, P., Toledo, J. & Hernández, E. (Eds) Moscas de la fruta: Fundamentos y procedimientos para su manejo. Mexico D. F., S y G Editores.Google Scholar
Dor, A., Valle-Mora, J.F., Rodríguez-Rodríguez, S. E. & Liedo, P. (2014) Predation of Anastrepha ludens (Diptera: Tephritidae), by Norops serranoi (Reptilia: Polychrotidae): functional response and evasion ability. Environmental Entomology 43, 706–715.Google Scholar
Eberhard, W.G. (2000) Sexual behavior and sexual selection in the Mediterranean fruit fly, Ceratitis capitata (Dacinae: Ceratidini). pp. 459–490 in Aluja, M. & Norrbom, A.L. (Eds) Fruit Flies (Tephritidae): Phylogeny and Evolution of Behavior. Boca Raton, FL, CRC Press.Google Scholar
Fisher, K. & Cáceres, C.A. (2000). A filter rearing system for mass reared genetic sexing strains of Mediterranean fruit fly (Diptera: Tephritidae). pp. 543–550 in Tan, K.H. (Ed.) Area-Wide Management of Fruit Flies and Other Major Insect Pests. Penang, Malaysia, Universiti Sains Malaysia Press.Google Scholar
Franz, G. (2005) Genetic sexing strains in the Mediterranean fruit fly, as an example for other species amenable to large scale rearing for the sterile insect technique. pp. 427–451 in Dyck, V.A., Hendrichs, J. & Robinson, A. (Eds) Sterile Insect Technique: Principles and Practice in Area-Wide Integrated Pest Management. The Netherlands, Springer.Google Scholar
González-López, G.I., Rao, D., Díaz-Fleischer, F., Orozco-Dávila, D. & Pérez-Staples, D. (2016) Antipredator behavior of the new mass reared unisexual strain of the Mexican fruit fly. Bulletin of Entomological Research 106, 314–321.Google Scholar
Gutiérrez, J.M. (2010) El programa Moscas de la Fruta en México. pp. 3–9. in Montoya, P., Toledo, J. & Hernández, E. (Eds.) Moscas de la fruta: Fundamentos y procedimientos para su manejo. Mexico D. F., S y G Editores.Google Scholar
Hagen, K.S. & Finney, G.L. (1950) A food supplement for effectively increasing the fecundity of certain tephritid species. Journal of Economical Entomology 43, 735.Google Scholar
Harris, D.J., Wood, R.J. & Bailey, S.E.R. (1986) Selection for fast and slow mating lines in the medfly and analysis of elements of courtship behavior. pp. 163–178 in Mangel, M. Carey, J.R. & Plant, R.E. (Eds.) Pest Control: Operations and Systems Analysis in Fruit Fly Management. Berlin, Springer-Verlag.Google Scholar
Harris, D.J., Wood, R.J. & Bailey, S.E.R. (1988) Two-way selection for mating activity in the Mediterranean fruit fly Ceratitis capitata. Entomologia Experimentalis et Applicata 47, 239–248.Google Scholar
Hendrichs, J. (1986) Sexual selection in wild and sterile Caribbean fruit flies, Anastrepha suspensa (Loew) (Diptera: Tephritidae). M. S. Thesis, University of Florida, Gainesville, FL.Google Scholar
Hendrichs, M.A. & Hendrichs, J. (1998) Perfumed to be killed: interception of Mediterranean fruit fly (Diptera: Tephritidae) sexual signaling by predatory foraging wasps (Hymenoptera: Vespidae). Annals of the Entomological Society of America 91, 229–234.Google Scholar
Hendrichs, J., Wornoayporn, V., Katsoyanno, B.I. & Gaggl, K. (1993) 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. 453–462 in Proceedings of a Symposium Jointly organized by IAEA and FAO, Vienna, 19–23 October 1992. Management of Insect Pests: Nuclear and Related Molecular and Genetic Techniques. Vienna, Austria, IAEA.Google Scholar
Hendrichs, M.A., Wornoayporn, V., Katsoyanos, B. & Hendrichs, J. (2007) Quality control method to measure predator evasion in wild and mass-reared medflies. Florida Entomologist 90, 64–70.Google Scholar
Hernández, E., Toledo, J., Artiaga-López, T. & Flores, S. (2009) Demographic changes in Anastrepha obliqua (Diptera: Tephritidae) throughout the laboratory colonization process. Journal of Economic Entomology 102, 542–551.Google Scholar
Hernández-Ortiz, V. (1992) El género Anastrepha Schiner en México (Diptera: Tephritidae): Taxonomía, Distribución y sus Plantas Huéspedes. Xalapa, Veracruz, México. Instituto de Ecología y Sociedad Mexicana de entomología, Publ. 33.Google Scholar
Hernández-Ortiz, V. (1993) Taxonomy, distribution and natural host plants of Anastrepha fruit flies in Mexico. pp. 32–34 in Aluja, M. & Liedo, P. (Eds) Fruit Flies: Biology and Management. New York, Springer-Verlag.Google Scholar
Hernández-Ortiz, V. & Aluja, M. (1993) Listado de especies del género neotropical Anastrepha (Diptera: Tephritidae) con notas sobre su distribución y plantas hospederas. Folia Entomológica Mexicana 88, 89–105.Google Scholar
Leftwich, P.T., Kokidou, M., Rempoulakis, P., Gong, H.F., Zacharopoulou, A., Fu, G., Chapman, T., Economopoulos, A., Vontas, J & Luke, A. (2014) Genetic elimination of field-cage populations of Mediterranean fruit flies. Proceedings of the Royal Society B 281, 20141372.Google Scholar
Levi, H.W. (1968) The spider genera Gea and Argiope in America (Araneae: Araneidae). Bulletin of the Museum of Comparative Zoology, Harvard 136, 319–352.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. Florida Entomologist 90, 33–40.Google Scholar
Lima, S.L. (1998) Stress and decision making under the risk of predation: recent developments from behavioral, reproductive, and ecological perspectives. Advances in the Study of Behavior 27, 215–290.Google Scholar
Lima, S.L. & Dill, L.M. (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Canadian Journal of Zoology 68, 619–640.Google Scholar
Lind, J. & Cresswell, W. (2005) Determining the fitness consequences of antipredation behavior. Behavioral Ecology 16, 945–956.Google Scholar
Lubin, Y.D. (1975) Stabilimentum and barrier webs in the orb webs of Argiope argentata (Araneae: Araneidae) on Daphne and Santa Cruz Islands, Galapagos. Journal of Arachnology 2, 119–126.Google Scholar
Lux, S.A., Munyiri, F.N., Vilardi, J.C., Liedo, P., Economopoulos, A., Hasson, O., Quilici, S., Gaggl, K., Cayol, J.P. & Rendon, P. (2002). Consistency in courtship pattern among populations of medfly (Diptera: Tephritidae): comparisons among wild strains and strains mass reared for SIT operations. Florida Entomologist 85, 113–125.Google Scholar
Magnhagen, C. (1991). Predation risk as a cost of reproduction. Trends in Ecology & Evolution 6, 183–186.Google Scholar
McInnis, D.O., Lance, D.R. & Jackson, C.G. (1996) Behavioral resistance to the sterile insect technique by Mediterranean fruit fly (Diptera: Tephritidae) in Hawaii. Annals of the Entomological Society of America 89, 739–744.Google Scholar
McInnis, D.O., Shelly, T.E. & Komatsu, J. (2002) Improving male mating competitiveness and survival in the field for medfly, Ceratitis (Diptera: Tephritidae) SIT programs. Genetica 116, 117–124.Google Scholar
McInnis, D.O., Paranhos, B.J. & Shelly, T.E. (2013) Survival of sterile male Mediterranean fruit flies in large field cages after release at different ages. Journal of Applied Entomology 137 (Suppl. 1), 43–48.Google Scholar
Miyatake, T. (1998) Genetic changes of life history and behavioral traits during mass-rearing in the melon fly Bactrocera cucurbitae (Diptera: Tephritidae). Researches on Population Ecology 40, 301–310.Google Scholar
Miyatake, T. (2011) Insect quality control: synchronized sex, mating system, and biological rhythm. Applied Entomology and Zoology 46, 3–14.Google Scholar
O'Steen, S., Cullum, A.J. & Bennett, A.F. (2002) Rapid evolution of escape ability in Trinidian guppies (Poecilia reticulata). Evolution 56, 776–784.Google Scholar
Orozco-Dávila, D., Domínguez, J., Reyes, J., Villaseñor, A. & Gutiérrez, J.M. (2004) SIT and biological control of Anastrepha fruit flies in Mexico. pp. 245–249 in Barnes, B. (Ed.) Proceedings, 6th International Symposium on Fruit Flies of Economic Importance, Stellenbosch, 6–10 May 2002. Johannesburg, Isteg Scientific Publications.Google Scholar
Orozco-Dávila, D., Hernández, R., Meza, J.S. & Domínguez, J. (2007) Sexual competitiveness and compatibility between mass-reared sterile flies and wild populations of Anastrepha ludens (Diptera:Tephritidae) from different regions of Mexico. Florida Entomologist 90, 19–26.Google Scholar
Orozco-Dávila, D., Meza, J.S., Zepeda, S., Solís, E. & Quintero-Fong, L. (2013) Tapachula-7, a new genetic strain of the Mexican fruit fly (Diptera:Tephritidae): sexual compatibility and competitiveness. Journal of Economical Entomologist 106, 735–741.Google Scholar
Orozco-Dávila, D., Quintero, L., Hernández, E., Solís, E., Artiaga, T., Hernández, R., Ortega, C. & Montoya, P. (2017) Mass rearing and sterile insect releases for the control of Anastrepha spp. pests in Mexico – a review. Entomologia Experimentalis et Applicata SI Sterile Insect Technique 164(3): 176–187.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 (Suppl.), 178–190.Google Scholar
Pinson, E., Tejada, L.O., Toledo, J., Enkerlin, W., Celedenio-Hurtado, H., Valle-Mora, J.F., Pérez, J.N. & Liedo, P. (2006) Caracterización de la adaptación de Anastrepha serpentina (Wied.) (Diptera: Tephritidae) a condiciones de cría masiva. Folia Entomológica Mexicana 45, 97–112.Google Scholar
Quintero-Fong, L., Toledo, J., Ruiz, L., Rendón, P., Orozco-Dávila, D., Cruz, L. & Liedo, P. (2016) Selection by mating competitiveness improves the performance of Anastrepha ludens males of the genetic sexing strain Tapachula-7. Bulletin of Entomological Research 106, 624–632.Google Scholar
R Core Team (2013) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. Available online at http://www.R-project.org/.Google Scholar
Rao, D., Aguilar-Argüello, S., Montoya, P. & Díaz-Fleischer, F. (2013) The effect of irradiation and mass-rearing on the anti-predator behaviour of the Mexican fruit fly Anastrepha ludens (Diptera:Tephritidae). Bulletin of Entomological Research 104, 176–181.Google Scholar
Robinson, M.H. (1969) Predatory behavior of Argiope argentata (Fabricius). American Zoologist 9, 161–173.Google Scholar
Robinson, M.H. & Olazarri, J. (1971) Units of behavioural and complex sequences in the predatory behaviour of Argiope argentata (Fabricius): (Araneae: Araneidae). Smithsonian Contributions to Zoology 65, 345–358.Google Scholar
Robinson, M.H. & Robinson, B. (1970) Prey caught by a sample of population of the spider Argiope argentata (Araneae: Araneidae) in Panama: a year's census data. Zoological Journal of the Linnean Society 49, 345–358.Google Scholar
Rull, J. & Barreda-Landa, A. (2007) Colonization of a hybrid strain to restore male Anastrepha ludens (Diptera: tephritidae) mating competitiveness for Sterile Insect Technique programs. Journal of Economical Entomology 100, 752–758.Google Scholar
Rull, J., Brunel, O. & Mendez, M.E. (2005) Mass-rearing history negatively affects mating success of male Anastrepha ludens (Diptera: Tephritidae) reared for sterile insect technique programs. Journal of Economical Entomology 98, 1510–1516.Google Scholar
Sánchez-Rosario, M. (2013) Competitividad sexual de machos de Anastrepha ludens (Loew) (Diptera: Tephritidae) sometidos a diferentes sistemas de cría. Bachelor Theses, BUAP – Escuela De Biología, Puebla, Mexico, 73 pp.Google Scholar
Sánchez-Rosario, M., Pérez-Staples, D., Toledo, J., Valle-Mora, J. & Liedo, P. (2017) Artificial selection on mating competitiveness of Anastrepha ludens for sterile insect technique application. Entomología Experimentalis et Applicata 162, 133–147.Google Scholar
Schmidt, O.J., Krivan, V. & Ovadia, O. (2004) Trophic cascades: the primacy of trait-mediated indirect interactions. Ecology Letters 7, 153–163.Google Scholar
Shelly, T.E. (2001) Outcrossing and mating competitiveness of male Mediterranean fruit flies (Diptera: Tephritidae). Results from the world's oldest mass-reared strain. Proceedings of the Hawaiian Entomological Society 35, 49–54.Google Scholar
Shelly, T.E., Rendón, P., Hernández, E., Salgado, S., McInnis, D., Villalobos, E. & Liedo, P. (2003) Effects of diet, ginger root oil, and elevation on the mating competitiveness of male Mediterranean fruit flies (Diptera: Tephritidae) from a mass-reared, genetic sexing strain in Guatemala. Journal of Economical Entomology 96, 1132–1141.Google Scholar
Tejeda, M.T., Arredondo, J., Liedo, P., Pérez-Staples, D., Ramos-Morales, P. & Díaz-Fleischer, F. (2016) Reasons for success: rapid evolution for desiccation resistance and life-history changes in the polyphagous fly Anastrepha ludens. Evolution 70, 2583–2594.Google Scholar
Whittier, T.S., Nam, F.Y., Shelly, T.E. & Kaneshiro, K.Y. (1994) Male courtship success and female discrimination in the Mediterranean fruit fly (Diptera: Tephritidae). Journal of Insect Behavior 7, 159–170.Google Scholar
Zepeda–Cisneros, C.S., Meza Hernández, J.S., Palacios, J.I., Martínez, V.G., de León Crisóstomo, A.H. & Flores-García, H. (2014) Development, genetic and cytogenetic analyses of sexing strains of the Mexican fruit fly Anastrepha ludens Loew (Diptera: Tephritidae). BMC Genetics 15(Suppl. 2), S1.Google Scholar