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Sexual communication and related behaviours in Tephritidae: current knowledge and potential applications for Integrated Pest Management

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Abstract

Tephritidae are an enormous threat to fruit and vegetable production throughout the world, causing both quantitative and qualitative losses. Investigating mating sequences could help to unravel mate choice dynamics, adding useful information to improve behaviour-based control strategies. We review current knowledge about sexual communication and related behaviours in Tephritidae, with a focus on six key agricultural pests: Anastrepha ludens, Bactrocera cucurbitae, Bactrocera dorsalis, Bactrocera oleae, Ceratitis capitata and Rhagoletis pomonella. We examine features and the role of male–male combat in lekking sites, cues affecting mating dynamics, and some fitness-promoting female behaviours that occur at oviposition sites [the use of oviposition marking pheromones (OMPs) and female–female fights for single oviposition sites]. We outline future perspectives and potential contributions of knowledge about sexual communication to Integrated Pest Management programs for tephritid pests. Sexually selected traits are frequently good indicators of male fitness and knowledge of sexual selection processes may contribute to the improvement of the sterile insect technique (SIT), to select genotypes with high reproductive success and to promote sexually selected phenotypes through mass-rearing optimization. Furthermore, males’ exposure to parapheromones, such as phenyl propanoids (PPs), ginger root oil and trimedlure can enhance the mating success of sterile flies used in SIT programs. PPs are also a powerful tool to improve reduced-risk monitoring dispensers and the male annihilation technique, with low side effects on non-target insects. Lastly, we outline the possibility to sensitise or train mass-reared parasitoids on OMPs during the pre-release phase, in order to improve their post-release performance in the field.

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References

  • AliNiazee MT (1974) The Western cherry fruit fly, Rhagoletis indifferens (Diptera: Tephritidae): 2. Aggressive behavior. Can Entomol 106:1201–1204

    Google Scholar 

  • Aluja M, Boller EF (1992a) Host-marking pheromone of Rhagoletis cerasi: field development of synthetic pheromone as a novel cherry fly management strategy. Entomol Exp Appl 65:141–147

    Google Scholar 

  • Aluja M, Boller EF (1992b) Host-marking pheromone of Rhagoletis cerasi: foraging behavior in response to synthetic pheromonal isomers. J Chem Ecol 18:1299–1311

    CAS  PubMed  Google Scholar 

  • Aluja M, Díaz-Fleischer F (2006) Foraging behavior of Anastrepha ludens, A. obliqua and A. serpentina in response to feces extracts containing host marking pheromone. J Chem Ecol 32:367–389

    CAS  PubMed  Google Scholar 

  • Aluja M, Norrbom A (2010) Fruit flies (Tephritidae): phylogeny and evolution of behavior. CRC Press, Boca Raton

    Google Scholar 

  • Aluja M, Jacome I, Birke A, Lozada N, Quintero G (1993) Basic patterns of behavior in Anastrepha striata (Diptera, Tephritidae) flies under field-cage conditions. Ann Entomol Soc Am 86:776–793

    Google Scholar 

  • Aluja M, Diaz-Fleischer F, Boller EF, Hurter J, Edmunds AJF, Hagmanna L et al (2009) Application of feces extracts and synthetic analogues of the host marking pheromone of Anastrepha ludens significantly reduces fruit infestation by A. obliqua in tropical plum and mango backyard orchards. J Econ Entomol 102:2268–2278

    CAS  PubMed  Google Scholar 

  • Anjos-Duarte CS, Moreira Costa A, Joachim-Bravo IS (2011) Influence of female age on variation of mate choice behavior in Mediterranean fruit fly (Diptera: Tephritidae). J Insect Behav 24:11–21

    Google Scholar 

  • Arita LH, Kaneshiro KY (1988) Body size and differential mating success between males of two populations of the Mediterranean fruit fly. Pac Sci 42:173–177

    Google Scholar 

  • Arita LH, Kaneshiro KY (1989) Sexual selection and lek behavior in the Mediterranean fruit fly, Ceratitis capitata (Diptera: Tephritidae). Pac Sci 43:135–143

    Google Scholar 

  • Armsworth CG, Baxter IH, Barton LE, Poppy GM, Nansen C (2006) Effects of adhesive powders on the mating and flight behavior of Mediterranean fruit fly (Diptera: Tephritidae). J Econ Entomol 99:1194–1202

    PubMed  Google Scholar 

  • Armsworth CG, Rogers CD, Barton LE, Soares C, Poppy GM (2008) Uptake of adhesive powders from lure stations by Mediterranean fruit fly (Diptera: Tephritidae). J Appl Entomol 132:45–53

    Google Scholar 

  • Arredondo J, Díaz-Fleischer F (2006) Oviposition deterrents for the Mediterranean fruit fly, Ceratitis capitata (Diptera: Tephritidae) from fly faeces extracts. Bull Entomol Res 96:35–42

    CAS  PubMed  Google Scholar 

  • Averill AL, Prokopy RJ (1989) Host-marking pheromones. In: Robinson AS, Hooper G (eds) Fruit flies: their biology, natural enemies and control. Elsevier, Amsterdam, pp 207–219

    Google Scholar 

  • Baker R, Bacon AJ (1985) The identification of spiroacetals in the volatile secretions of two species of fruit fly (Dacus dorsalis, Dacus cucurbitae). Experientia 41:1484–1485

    CAS  Google Scholar 

  • Baker R, Herbert RH, Howse PE, Jones OT, Francke W, Reith W (1980) Identification and synthesis of the major sex pheromone of the olive fly, Dacus oleae. J Chem Soc Chem Commun 1:52–54

    Google Scholar 

  • Baker R, Herbert RH, Lomer RA (1982a) Chemical components of the rectal gland secretions of male Dacus cucurbitae, the melon fly. Experientia 38:232–233

    CAS  Google Scholar 

  • Baker R, Herbert RH, Parton AH (1982b) Isolation and synthesis of 3- and 4-hydroxy-1,7dioxaspiro[5.5]undecanes from the olive fly (Dacus oleae). J Chem Soc Chem Commun 1982:601–603

    Google Scholar 

  • Baker R, Herbert RH, Grant GG (1985) Isolation and identification of the sex pheromone of the Mediterranean fruit fly, Ceratitis capitata (Wied). J Chem Soc Chem Commun 1985:824–825

    Google Scholar 

  • Battiste MA, Strekowski L, Vanderbilt DP, Visnick M, King RW, Nation JL (1983) Anastrephin and epianastrephin, novel lactone components isolated from the sex pheromone blend of male Caribbean and Mexican fruit flies. Tetrahedron Lett 24:2611–2614

    CAS  Google Scholar 

  • Bauer G (1986) Life-history strategy of Rhagoletis alternata (Diptera: Trypetidae), a fruit fly operating in a ‘non-interactive’ system. J Anim Ecol 55:785–794

    Google Scholar 

  • Benelli G (2014) Aggressive behavior and territoriality in the olive fruit fly, Bactrocera oleae (Rossi) (Diptera: Tephritidae): role of residence and time of day. J Insect Behav 27:145–161

    Google Scholar 

  • Benelli G, Canale A (2012a) Do Psyttalia concolor (Hymenoptera: Braconidae) males gain in mating competitiveness from being courted by other males while still young? Entomol Sci 15:257–260

    Google Scholar 

  • Benelli G, Canale A (2012b) Learning of visual cues in the fruit fly parasitoid Psyttalia concolor (Szépligeti) (Hymenoptera: Braconidae). Biocontrol 57:767–777

    Google Scholar 

  • Benelli G, Canale A, Bonsignori G, Ragni G, Stefanini C, Raspi A (2012a) Male wing vibration in the mating behavior of the olive fruit fly Bactrocera oleae (Rossi) (Diptera: Tephritidae). J Insect Behav 25:590–603

    Google Scholar 

  • Benelli G, Bonsignori G, Stefanini C, Canale A (2012b) Courtship and mating behaviour in the fruit fly parasitoid Psyttalia concolor (Szépligeti) (Hymenoptera: Braconidae): the role of wing fanning. J Pest Sci 85:55–63

    Google Scholar 

  • Benelli G, Flamini G, Canale A, Cioni PL, Conti B (2012c) Toxicity evaluation of different essential oil formulations against the Mediterranean fruit fly Ceratitis capitata (Wiedemann) (Diptera Tephritidae). Crop Protect 42:223–229

    CAS  Google Scholar 

  • Benelli G, Bonsignori G, Stefanini C, Raspi A, Canale A (2013a) The production of female sex pheromone in Bactrocera oleae (Rossi) young males does not influence their mating chances. Entomol Sci 16:47–53

    Google Scholar 

  • Benelli G, Revadi S, Carpita A, Giunti G, Raspi A, Anfora G, Canale A (2013b) Behavioral and electrophysiological responses of the parasitic wasp Psyttalia concolor (Szépligeti) (Hymenoptera: Braconidae) to Ceratitis capitata-induced fruit volatiles. Biol Control 64:116–124

    CAS  Google Scholar 

  • Benelli G, Canale A, Flamini G, Cioni PL, Demi F, Ceccarini L, Macchia M, Conti B (2013c) Biotoxicity of Melaleuca alternifolia (Myrtaceae) essential oil against the Mediterranean fruit fly, Ceratitis capitata (Diptera: Tephritidae), and its parasitoid Psyttalia concolor (Hymenoptera: Braconidae). Ind Crops Prod 50:596–603

    CAS  Google Scholar 

  • Ben-Yosef M, Aharon Y, Jurkevitch E, Yuval B (2010) Give us the tools and we will do the job: symbiotic bacteria affect olive fly fitness in a diet-dependent fashion. Proc R Soc B 277:1545–1552

    CAS  PubMed Central  PubMed  Google Scholar 

  • Beris EI, Papachristos DP, Fytrou A, Antonatos SA, Kontodimas DC (2013) Pathogenicity of three entomopathogenic fungi on pupae and adults of the Mediterranean fruit fly, Ceratitis capitata (Diptera: Tephritidae). J Pest Sci 86:275–284

    Google Scholar 

  • Biggs JD (1972) Aggressive behavior in the adult apple maggot (Diptera: Tephritidae). Can Entomol 104:349–353

    Google Scholar 

  • Boller EF, Hurther J (1998) The marking pheromone of the cherry fruit fly: a novel non-toxic and ecologically safe technique to protect cherries against cherry fruit fly infestation. In: International symposium on insect pheromones. Proceedings: contributed papers–abstracts, Wageningen, March 1998, pp 99–101

  • Bonizzoni M, Gomulski LM, Mossinson S, Guglielmino CR, Malacrida AR, Yuval B, Gasperi G (2006) Is polyandry a common event among wild populations of the pest Ceratitis capitata? J Econ Entomol 99:1420–1429

    PubMed  Google Scholar 

  • Boyce AM (1934) Bionomics of the walnut husk fly, Rhagoletis completa. Hilgardia 8:363–579

    Google Scholar 

  • Bradbury JW, Vehrencamp SL, Gibson RM (1989) Dispersion of displaying male sage grouse. I. Patterns of temporal variation. Behav Ecol Sociobiol 24:1–14

    Google Scholar 

  • Briceño RD, Eberhard WG (1998) Medfly courtship duration: a sexually selected reaction norm changed by crowding. Ethol Ecol Evol 10:369–382

    Google Scholar 

  • Briceño RD, Eberhard WG (2000a) Possible Fisherian changes in female mate-choice criteria in a mass-reared strain of Ceratitis capitata (Diptera: Tephritidae). Ann Entomol Soc Am 93(343):345

    Google Scholar 

  • Briceño RD, Eberhard W (2000b) Male wing positions during courtship by Mediterranean fruit flies (Ceratitis capitata) (Diptera: Tephritidae). J Kans Entomol Soc 73:111–115

    Google Scholar 

  • Briceño RD, Eberhard W (2002) Decisions during courtship by male and female medflies (Diptera: Tephritidae): correlated changes in male behavior and female acceptance criteria in mass reared flies. Fla Entomol 85:14–31

    Google Scholar 

  • Briceño D, Ramos D, Eberhard W (1996) Courtship behaviour of male Ceratitis capitata (Diptera: Tephritidae) in captivity. Fla Entomol 79:130–143

    Google Scholar 

  • Briceño RD, Ramos D, Eberhard WG (1999) Aggressive behavior in medflies (Ceratitis capitata) and its modification by mass rearing (Diptera: Tephritidae). J Kans Entomol Soc 72:17–27

    Google Scholar 

  • Briceño RD, Eberhard WG, Vilardi JC, Liedo P, Shelly TE (2002) Variation in the intermittent buzzing songs of male medflies (Diptera: Tephritidae) associated with geography, mass-rearing, and courtship success. Fla Entomol 85:32–40

    Google Scholar 

  • Briceño RD, Eberhard W, Vilardi J, Cayol JP, Shelly T (2007) Courtship behaviour of different wild strains of Ceratitis capitata (Diptera: Tephritidae). Fla Entomol 90:15–18

    Google Scholar 

  • Burk T (1981) Signaling and sex in acalyptrate flies. Fla Entomol 64:30–43

    Google Scholar 

  • Burk T (1983) Behavioral ecology of mating in the Caribbean fruit fly, Anastrepha suspensa (Loew) (Diptera: Tephritidae). Fla Entomol 66:330–344

    Google Scholar 

  • Burk T (1984) Male-male interactions in the Caribbean fruit flies, Anastrepha suspensa (Loew) (Diptera: Tephritidae): territorial fights and signaling stimulation. Fla Entomol 67:542–547

    Google Scholar 

  • Burk T, Calkins CO (1983) Medfly mating behaviour and control strategies. Fla Entomol 66:3–18

    Google Scholar 

  • Burk T, Webb JC (1983) Effect of male size on calling propensity, song parameters and mating success in Caribbean fruit flies, Anastrepha suspensa (Loew) (Diptera: Tephritidae). Ann Entomol Soc Am 76:678–682

    Google Scholar 

  • Câmara de Aquino J, Joachim-Bravo IS (2013) Relevance of male size to female mate choice in Ceratitis capitata (Diptera: Tephritidae): investigations with wild and laboratory-reared flies. J Insect Behav. doi:10.1007/s10905-013-9410-8

    Google Scholar 

  • Canale A, Benelli G (2012) Impact of mass-rearing on the host-seeking behaviour and parasitism by the fruit fly parasitoid Psyttalia concolor (Szépligeti) (Hymenoptera: Braconidae). J Pest Sci 85:65–74

    Google Scholar 

  • Canale A, Carpita A, Conti B, Canovai R, Raspi A (2012) Effect of age on 1,7-dioxaspiro-[5.5]-undecane production in both sexes of olive fruit fly, Bactrocera oleae (Rossi) (Diptera Tephritidae). IOBC Bull 72:219–225

    Google Scholar 

  • Canale A, Germinara SG, Carpita A, Benelli G, Bonsignori G, Stefanini C, Raspi A, Rotundo G (2013a) Behavioural and electrophysiological responses of the olive fruit fly, Bactrocera oleae (Rossi) (Diptera: Tephritidae), to male- and female-borne sex attractants. Chemoecology 23:155–164

    CAS  Google Scholar 

  • Canale A, Benelli G, Conti B, Lenzi G, Flamini G, Francini A, Cioni PL (2013b) Ingestion toxicity of three Lamiaceae essential oils incorporated in protein baits against the olive fruit fly, Bactrocera oleae (Rossi) (Diptera Tephritidae). Nat Prod Res 27:2091–2099

    CAS  PubMed  Google Scholar 

  • Carpita A, Canale A, Raffaelli A, Saba A, Benelli G, Raspi A (2012) (Z)-9-tricosene identified in rectal gland extracts of Bactrocera oleae males: first evidence of a male-produced female attractant in olive fruit fly. Naturwissenschaften 99:77–81

    CAS  PubMed  Google Scholar 

  • Cavalloro R, Mazomenos BE, Pomonis JG (1983) Male olive fruit fly pheromone: isolation identification and lab bioassays. Econ Import 16–19

  • Cavender GL, Goeden RD (1982) Life history of Trupanea bisetosa (Diptera: Tephritidae) on wild sunflower in Southern California. Ann Entomol Soc Am 75:400–406

    Google Scholar 

  • Chambers DL, Ohinata K, Fujimoto M, Kashiwai S (1974) Treating tephritids with attractants to enhance their effectiveness in sterile-release programs. J Econ Entomol 65:279–282

    Google Scholar 

  • Chang CL, Cho IK, Li QX, Manoukis NC, Vargas RI (2013) A potential field suppression system for Bactrocera dorsalis Hendel. J Asia Pac Entomol 16:513–519

    CAS  Google Scholar 

  • Chinajariyawong A, Drew RAI, Meats A, Balagawi S, Vijaysegaran S (2010) Multiple mating by females of two Bactrocera species (Diptera: Tephritidae: Dacinae). Bull Entomol Res 100:325–330

    CAS  PubMed  Google Scholar 

  • Churchill-Stanland C, Stanland R, Wong TTY, Tanaka N, McInnis DO, Dowell RV (1986) Size as a factor in the mating propensity of Mediterranean fruit flies, Ceratitis capitata (Diptera: Tephritidae), in the laboratory. J Econ Entomol 79:614–619

    Google Scholar 

  • Cirio U (1971) Reperti sul meccanismo stimolo-risposta nell’ovideposizione del Dacus oleae Gmelin (Diptera: Trypetidae). Redia 52:577–600

    Google Scholar 

  • Círio U (1972) Osservazioni sul comportamento di oviposizione della Rhagoletis completa in laboratorio. In: IX Congress of the italian entomological society. Proceedings: contributed papers–abstracts, Italia, 1972, pp 99–117

  • Cook SM, Kham ZR, Pickett JA (2007) The use of push-pull strategies in integrated pest management. Annu Rev Entomol 52:375–400

    CAS  PubMed  Google Scholar 

  • Daane KM, Johnson MW (2010) Olive fruit fly: managing an ancient pest in modern times. Annu Rev Entomol 55:151–169

    CAS  PubMed  Google Scholar 

  • Debouzie D (1989) Biotic mortality factors in tephritid populations. In: Robinson AS, Hooper G (eds) World crop pests, vol 3B., Fruit flies: their biology, natural enemies and control. Elsevier, New York, pp 221–227

  • Díaz-Fleischer F, Arredondo J (2011) Light conditions affect sexual performance in a lekking tephritid fruit fly. J Exp Biol 214:2595–2602

    PubMed  Google Scholar 

  • Díaz-Fleischer F, Arredondo J, Aluja M (2009) Enriching early adult environment affects the copulation behaviour of a tephritid fly. J Exp Biol 212:2120–2127

    PubMed  Google Scholar 

  • Dodson G (1986) Lek mating system and large male aggressive advantage in a gall-forming tephritid fly (Diptera: Tephritidae). Ethology 72:99–108

    Google Scholar 

  • Dodson G (1987) Biological observation on Aciurina trixa and Valentibulla dodsoni (Diptera: Tephritidae) in New Mexico. Ann Entomol Soc Am 80:494–500

    Google Scholar 

  • Dong YC, Wang ZJ, Clarke AR, Pereira R, Desneux N, Niu CY (2013) Pupal diapause development and termination is driven by low temperature chilling in Bactrocera minax. J Pest Sci 86:429–436

    Google Scholar 

  • Drew RAI, Yuval B (2000) The evolution of fruit fly feeding behavior. In: Aluja M, Norrbom AL (eds) Fruit flies (Tephritidae): phylogeny and evolution of behavior. CRC Press, Boca Raton, pp 731–749

    Google Scholar 

  • Dukas R, Prokopy RJ, Papaj DR, Duan JJ (2001) Egg laying behavior of Mediterranean fruit flies (Diptera: Tephritidae): is social facilitation important? Fla Entomol 84:665–671

    Google Scholar 

  • Edmunds AJF, Aluja M, Diaz-Fleischer F, Patrian B, Hagmann L (2010) Host marking pheromone (HMP) in the Mexican fruit fly Anastrepha ludens. Chimia 64:37–42

    CAS  PubMed  Google Scholar 

  • Ekesi S, Billah MK (2007) A field guide to the management of economically important tephritid fruit flies in Africa. ICIPE Science, Nairobi

    Google Scholar 

  • Ekesi S, Mohamed SA (2011) Mass rearing and quality control parameters for tephritid fruit flies of economic importance in Africa. In: Akyar I (ed) Wide spectra of quality control. InTech, Rijeka

    Google Scholar 

  • Ekesi S, Billah MK, Peterson W, Nderitu W, Lux SA, Rwomushana I (2009) Evidence for competitive displacement of Ceratitis cosyra by the invasive fruit fly Bactrocera invadens (Diptera: Tephritidae) on mango and mechanisms contributing to the displacement. J Econ Entomol 102:981–991

    PubMed  Google Scholar 

  • El-Sayed AM (2013) The pherobase: database of insect pheromones and semiochemicals. http://pherobase.com. Accessed 27 Dec 2013

  • Estes AM, Nestel D, Belcari A, Jessup A, Rempoulakis P, Economopoulos AP (2012) A basis for the renewal of sterile insect technique for the olive fly, Bactrocera oleae (Rossi). J Appl Entomol 136:1–16

    Google Scholar 

  • Fanson BG, Fanson KV, Taylor PW (2012) Cost of reproduction in the Queensland fruit fly: Y model vs. lethal protein hypothesis. Proc R Soc B 279:4893–4900

    PubMed Central  PubMed  Google Scholar 

  • Faria M, Pereira R, Dellinger T, Teal P (2008) Influence of methoprene and protein on survival, maturation, and sexual performance of male Ceratitis capitata. J Appl Entomol 132:812–819

    CAS  Google Scholar 

  • Feron M, Andriew AJ (1962) Etude des signaux acoustiques du male dans le comportement sexual des Dacus oleae Gmel. (Diptera: Trypetidae). Ann Epiphyt 13:269–276

    Google Scholar 

  • Fiske P, Rintamäki PT, Karvonen E (1998) Mating success in lekking males: a meta-analysis. Behav Ecol 9:328–338

    Google Scholar 

  • Fitt GP (1981) The influence of age, nutrition and time of day on the responsiveness of male Dacus opiliae to the synthetic lure, methyl eugenol. Entomol Exp Appl 30:83–90

    CAS  Google Scholar 

  • Fitt GP (1984) Oviposition behaviour of two tephritid fruit flies, Dacus tryoni and Dacus jarvisi, as influenced by the presence of larvae in the host fruit. Oecologia 62:37–46

    Google Scholar 

  • Fletcher BS (1987) The biology of dacine fruit flies. Annu Rev Entomol 32:115–144

    Google Scholar 

  • Fletcher MT, Jacobs MF, Krohn S, Drew RAI, Haniotakis GE, Francke W (1992) Absolute stereochemistry of the 1,7-dioxaspiro[5.5]undecanols in fruit-fly species, including the olive fly. J Chem Soc Chem Commun 1992:1457–1459

    Google Scholar 

  • Gariboldi P, Verotta L, Fanelli R (1983) Studies on the sex pheromone of Dacus oleae. Analysis of the substances contained in the rectal glands. Experientia 39:502–505

    CAS  Google Scholar 

  • Gavriel S, Gazit Y, Yuval B (2009) Remating by female Mediterranean fruit flies (Ceratitis capitata, Diptera: Tephritidae): Temporal patterns and modulation by male condition. J Insect Physiol 55:637–642

    CAS  PubMed  Google Scholar 

  • Gerofotis CD, Ioannou CS, Papadopoulos NT (2013) Aromatized to find mates: α-pinene aroma boosts the mating success of adult olive fruit flies. PLoS One 8:e81336

    PubMed Central  PubMed  Google Scholar 

  • Gil-Ortiz R (2012) Development of new ecological long-lasting dispensers of semiochemicals for the control of Bactrocera oleae (Rossi). Pest Manag Sci. doi:10.1002/ps.3415

    PubMed  Google Scholar 

  • Girolami V, Vianello A, Strapazzon A, Ragazzi E, Veronese G (1981) Ovipositional deterrents in Dacus oleae. Entomol Exp Appl 29:177–188

    CAS  Google Scholar 

  • Goncalves GB, Silva CE, De Lima MA, Vanickova L, Tomcala A, Do Nascimiento RR (2013) Pheromone communication in Anastrepha obliqua (Diptera: Tephritidae): a comparison of the volatiles and salivary gland extracts of two wild populations. Fla Entomol 96:1365–1374

    Google Scholar 

  • Haq I, Hendrichs J (2013) Pre-release feeding on hydrolysed yeast and methoprene treatment enhances male Bactrocera cucurbitae Coquillett (Diptera: Tephritidae) longevity. J Appl Entomol 137(Suppl 1):99–102

    CAS  Google Scholar 

  • Haq I, Vreysen MJB, Teal PEA, Hendrichs J (2013) Methoprene application and diet protein supplementation to male melon fly, Bactrocera cucurbitae, modifies female remating behavior. Insect Sci. doi:10.1111/1744-7917.12073

    Google Scholar 

  • Harwood JF, Vargas RI, Care JR (2013) Leg impairment magnifies reproductive costs in male Mediterranean fruit flies, Ceratitis capitata. Entomol Exp Appl 147:73–81

    PubMed Central  PubMed  Google Scholar 

  • Headrick D, Goeden RD (1990) Life history of Paracantha gentilis (Diptera: Tephritidae). Ann Entomol Soc Am 83:776–785

    Google Scholar 

  • Headrick DH, Goeden RD (1994) Reproductive behavior of California fruit flies and the classification and evolution of Tephritidae (Diptera) mating systems. Stud Dipterol 1:194–252

    Google Scholar 

  • Heath RR, Landolt PJ, Tumlinson JH, Chambers DL, Murphy RE, Doolittle RE, Dueben BD, Sivinski J, Calkins CO (1991) Analysis, synthesis, formulation, and field testing of three major components of male Mediterranean fruit fly pheromone. J Chem Ecol 17:1925–1940

    CAS  PubMed  Google Scholar 

  • Hee AKW, Tan KH (2004) Male sex pheromonal components derived from methyl eugenol in the hemolymph of the fruit fly Bactrocera papayae. J Chem Ecol 30:2127–2138

    CAS  PubMed  Google Scholar 

  • Hoffmeister TS, Roitberg BD, Lalonde RG (2000) Catching Ariadne by her thread: how a parasitoid exploits the herbivore’s marking trails to locate its host. Entomol Exp Appl 95:77–85

    Google Scholar 

  • Höglund J, Alatalo R (1995) Leks. Princeton University Press, Princeton

    Google Scholar 

  • Höglund J, Lundberg A (1987) Sexual selection in a monomorphic lek-breeding bird: correlates of male mating success in the great snipe Gallinago media. Behav Ecol Sociobiol 21:211–216

    Google Scholar 

  • Jacobson M, Ohinata K (1980) Unique occurrence of fenchol in the animal kingdom. Experientia 36:629–630

    CAS  Google Scholar 

  • Jacobson M, Ohinata K, Chambers DL, Jones WA, Fujimoto MS (1973) Insect sex attractants. 13. Isolation, identification, and synthesis of sex pheromones of the male Mediterranean fruit fly. J Med Chem 16:248–251

    CAS  PubMed  Google Scholar 

  • Janetos AC (1980) Strategies of female mate choice: a theurgical analysis. Behav Ecol Sociobiol 7:107–112

    Google Scholar 

  • Jang EB, Light DM, Binder RG, Flath RA, Carvalho LA (1994) Attraction of female Mediterranean fruit flies to the five major components of male-produced pheromone in a laboratory flight tunnel. J Chem Ecol 20:9–20

    CAS  PubMed  Google Scholar 

  • Jiménez-Pérez A, Wang Q, Arzuffi R (2013) Mating behaviour of Cnepahsia jactalana (Lepidoptera: Tortricidae), an important pest of kiwifruit. J Econ Entomol 106:1373–1378

    PubMed  Google Scholar 

  • Jones TM, Quinnell RJ, Balmford A (1998) Fisherian flies: benefits of female choice in a lekking sandfly. Proc R Soc B 265:1651–1657

    PubMed Central  Google Scholar 

  • Kanmiya K (1988) Acoustic studies on the mechanism of sound production in the mating songs of the melon fly, Dacus cucurbitae Coquillett (Diptera: Tephritidae). J Ethol 6:143–151

    Google Scholar 

  • Kanmiya K, Nakagawa K, Tanaka A, Kamiwada H (1987a) Comparison of acoustic properties of tethered flight sounds for wild, mass-reared, and irradiated melon flies, Dacus cucurbitae Coquillett (Diptera: Tephritidae). Appl Entomol Zool 22:85–97

    Google Scholar 

  • Kanmiya K, Nakagawa K, Tanaka A, Kamiwada H (1987b) Selection of effective ages and parameters for qualitative discrimination between wild, mass-reared, and irradiated strains through comparison of tethered flight sounds of the melon flies, Dacus cucurbitae Coquillett (Diptera: Tephritidae). Appl Entomol Zool 22:316–324

    Google Scholar 

  • Kanmiya K, Tanaka A, Kamiwada H, Nakagawa K, Nishioka T (1987c) Time-domain analysis of the male courtship songs produced by wild, mass-reared, and by irradiated melon flies, Dacus cucurbitae Coquillett (Diptera: Tephritidae). Appl Entomol Zool 22:181–194

    Google Scholar 

  • Kaspi R, Taylor PW, Yuval B (2000) Diet and size influence sexual advertisement and copulatory success of males in Mediterranean fruit fly leks. Ecol Entomol 25:279–284

    Google Scholar 

  • Katsoyannos BI (1975) Oviposition-deterring, male-arresting, fruit-marking pheromone in Rhagoletis cerasi. Environ Entomol 4:801–807

    Google Scholar 

  • Katsoyannos BI, Boller EF (1976) First field application of oviposition-deterring marking pheromone of European cherry fruit fly. Environ Entomol 5:151–152

    Google Scholar 

  • Katsoyannos BI, Boller EF (1980) 2nd field application of oviposition-deterring pheromone of the European cherry fruit fly, Rhagoletis cerasi (Diptera: Tephritidae). J Appl Entomol 89:278–281

    CAS  Google Scholar 

  • Keiser I, Kobayashi RM, Chambers DL, Schneider EL (1973) Relation of sexual dimorphism in the wings, potential stridulation, and illumination to mating of oriental fruit flies, melon flies, and Mediterranean fruit flies in Hawaii. Ann Entomol Soc Am 66:937–941

    Google Scholar 

  • Khoo CCH, Tan KH (2000) Attraction of both sexes of melon fly, Bactrocera cucurbitae, to conspecific males—a comparison after pharmacophagy of cue-lure and a new attractant—zingerone. Entomol Exp Appl 97:317–320

    CAS  Google Scholar 

  • Khoo CCH, Tan KH (2005) Rectal gland of Bactrocera papayae: ultrastructure, anatomy, and sequestration of autofluorescent compounds upon methyl eugenol consumption by the male fruit fly. Microsc Res Tech 67:219–226

    PubMed  Google Scholar 

  • Kirkendall LR (1983) The evolution of mating systems in bark and ambrosia beetles (Coleoptera: Scolytidae and Platypodidae). Zool J Linn Soc 77:293–352

    Google Scholar 

  • Kirkpatrick M, Ryan MJ (1991) The evolution of mating preferences and the paradox of the lek. Nature 350:33–38

    Google Scholar 

  • Koyama J (1989) Mating pheromones. Tropical dacines. In: Robinson AS, Hooper G (eds) Fruit flies. Their biology, natural enemies and control, vol 3A. Elsevier, Amsterdam, pp 165–168

    Google Scholar 

  • Koyama J, Kakinohana H, Miyatake T (2004) Eradication of the melon fly, Bactrocera cucurbitae, in Japan: importance of behavior, ecology, genetics, and evolution. Annu Rev Entomol 49:331–349

    CAS  PubMed  Google Scholar 

  • Kraaijeveld K, Chapman T (2004) Effects of male sterility on female remating in the Mediterranean fruit fly, Ceratitis capitata. Proc R Soc B 271:S209–S211

    PubMed Central  PubMed  Google Scholar 

  • Kuba H, Koyama J (1985) Mating behavior of wild melon flies, Dacus cucurbitae Coquillett (Diptera: Tephritidae) in a field cage: courtship behavior. Appl Entomol Zool 20:365–372

    Google Scholar 

  • Kuba H, Sokei Y (1988) The production of pheromone clouds by spraying in the melon fly, Dacus cucurbitae Coquillett (Diptera: Tephritidae). J Ethol 6:105–110

    Google Scholar 

  • Kumaran N, Balagawi S, Schutze MK, Clarke AR (2013) Evolution of lure response in tephritid fruit flies: phytochemicals as drivers of sexual selection. Anim Behav 85:781–789

    Google Scholar 

  • Lalonde RG, Roitberg BD (1992) Host selection behavior of the thistle-feeding fly: choices and consequences. Oecologia 90:534–539

    Google Scholar 

  • Lance DR, McInnis DO (2005) Biological basis of the sterile insect technique. Sterile insect technique: principles and practice. In: Dyck VA, Hendrichs J, Robinson AS (eds) Area-wide integrated pest management. Springer, Dordrecht, pp 69–94

    Google Scholar 

  • Lance DR, McInnis DO, Rendon P, Jackson CG (2000) Courtship among sterile and wild Ceratitis capitata (Diptera: Tephritidae) in field cages in Hawaii and Guatemala. Ann Entomol Soc Am 93:1179–1185

    Google Scholar 

  • Landolt PJ, Heath RR (1988) Effects of age, mating, and time of day on behavioral responses of female papaya fruit fly, Toxotrypana curvicauda Gerstaecker (Diptera: Tephritidae), to synthetic sex pheromone. Environ Entomol 17:47–51

    CAS  Google Scholar 

  • Landolt PJ, Hendrichs J (1983) Reproductive behavior of the papaya fruit fly, Toxotrypana curvicauda Gerstaecker (Diptera: Tephritidae). Ann Entomol Soc Am 76:413–417

    Google Scholar 

  • Landolt PJ, Heath RR, Agee HR, Tumlinson JH, Calkins CO (1988) Sex pheromone-based trapping system for papaya fruit fly (Diptera: Tephritidae). J Econ Entomol 81:1163–1169

    Google Scholar 

  • Landolt PJ, Reed HC, Heath RR (1992) Attraction of female papaya fruit fly (Diptera: Tephritidae) to male pheromone and host fruit. Environ Entomol 21:1154–1159

    Google Scholar 

  • Lauzon CR, Potter SE (2012) Description of the irradiated and nonirradiated midgut of Ceratitis capitata Wiedemann (Diptera: Tephritidae) and Anastrepha ludens Loew (Diptera: Tephritidae) used for sterile insect technique. J Pest Sci 85:217–226

    Google Scholar 

  • Leftwich PT, Edward DA, Alphey L, Gage MJG, Chapman T (2012) Variation in adult sex ratio alters the association between courtship, mating frequency and paternity in the lek-forming fruitfly Ceratitis capitata. J Evol Biol 25:1732–1740

    CAS  PubMed  Google Scholar 

  • Levi-Zada A, Nestel D, Fefer D, Nemni-Lavy E, Deloya-Kahane I, David M (2012) Analyzing diurnal and age-related pheromone emission of the olive fruit fly, Bactrocera oleae by sequential SPME-GCMS analysis. J Chem Ecol 38:1036–1041

    CAS  PubMed  Google Scholar 

  • Liedo P, De Leon E, Barrios MI, Valle-Mora JF, Ibarra G (2002) Effect of age on the mating propensity of the Meditarreanean fruit fly (Diptera: Tephritidae). Fla Entomol 85:94–101

    Google Scholar 

  • Liu X, Jin Y, Ye H (2013) Recent spread and climatic ecological niche of the invasive guava fruit fly, Bactrocera correcta, in mainland China. J Pest Sci 86:449–458

    Google Scholar 

  • Lux SA, Munyiri FN, Vilardi JC, Liedo P, Economopoulos A et al (2002) Consistency in courtship pattern among populations of medfly (Diptera: Tephritidae): comparisons among wild strains and strains mass reared for SIT operations. Fla Entomol 85:113–125

    Google Scholar 

  • Mankin RW, Lemon M, Harmer AMT, Evans CS, Taylor PW (2008) Time-pattern and frequency analyses of sounds produced by irradiated and untreated male Bactrocera tryoni (Diptera: Tephritidae) during mating behavior. Ann Entomol Soc Am 101:664–674

    Google Scholar 

  • Mazomenos BE, Haniotakis GE (1981) A multicomponent female sex pheromone of Dacus oleae Gmelin: isolation and bioassay. J Chem Ecol 7:1561–1573

    Google Scholar 

  • Mazomenos BE, Haniotakis GE (1985) Male olive fruit fly attraction to synthetic sex pheromone components in laboratory and field tests. J Chem Ecol 11:397–405

    CAS  PubMed  Google Scholar 

  • McInnis DO, Shelly TE, Komatsu J (2002) Improving male mating competitiveness and survival in the field for medfly, Ceratitis capitata (Diptera: Tephritidae) SIT programs. Genetica 116:117–124

    CAS  PubMed  Google Scholar 

  • McInnis D, Kurashima R, Shelly T, Komatsu J, Edu J, Pahio E (2011) Prerelease exposure to methyl eugenol increases the mating competitiveness of sterile males of the Oriental fruit fly (Diptera: Tephritidae) in a Hawaiian Orchard. J Econ Entomol 104:1969–1978

    CAS  PubMed  Google Scholar 

  • Messina FJ, Subler JK (1995) Conspecific and heterospecific interactions of male Rhagoletis flies (Diptera: Tephritidae) on a shared host. J Kans Entomol Soc 68:206–213

    Google Scholar 

  • Miranda X (2000) Sexual dimorphism in the aristae of Ceratitis capitata (Diptera, Tephritidae) and its possible importance in courtship. J N Y Entomol Soc 108:339–348

    Google Scholar 

  • Moradian NR, Walker SE (2008) Relationships between body size and sound-producing structures in crickets: do large males have large harps? Invertebr Biol 127:444–451

    Google Scholar 

  • Moreno DS, Sanchez M, Robacker DC, Worley J (1991) Mating competitiveness of irradiated Mexican fruit-fly (Diptera, Tephritidae). J Econ Entomol 84:1227–1234

    Google Scholar 

  • Ngumbi EN, Jordan M, Fadamiro HY (2012) Comparison of associative learning of host-related plant volatiles in two parasitoids with different degrees of host specificity, Cotesia marginiventris and Microplitis croceipes. Chemoecology 22:207–215

    CAS  Google Scholar 

  • Nishida R, Fukami H (1990) Sequestration of distasteful compounds by some pharmacophagous insects. J Chem Ecol 16:151–164

    CAS  PubMed  Google Scholar 

  • Nishida R, Tan KH, Fukami H (1988a) Cis-3,4-dimethoxycinnamyl alcohol from the rectal glands of male oriental fruit fly, Dacus dorsalis. Chem Express 3:207–210

    CAS  Google Scholar 

  • Nishida R, Tan KH, Serit M, Lajis NH, Sukari AM, Takahashi S, Fukami H (1988b) Accumulation of phenylpropanoids in the rectal glands of males of the oriental fruit fly, Dacus dorsalis. Experientia 44:534–536

    CAS  Google Scholar 

  • Nishida R, Shelly TE, Kaneshiro KY (1997) Acquisition of female-attracting fragrance by males of oriental fruit fly from a Hawaiian lei flower, Fagraea berteriana. J Chem Ecol 23:2275–2285

    CAS  Google Scholar 

  • Ohinata K, Jacobson M, Kobayashi RM, Chambers DL, Fujimoto MS, Higa HH (1982) Oriental fruit fly and melon fly: biological and chemical studies of smoke produced by males. J Environ Sci Health 17:197–216

    Google Scholar 

  • Opp SB, Prokopy RJ (2000) Multiple mating and reproductive success of male and female apple maggot flies, Rhagoletis pomonella (Diptera: Tephritidae). J Insect Behav 13:901–914

    Google Scholar 

  • Papaj DR (1994) Oviposition site guarding by male walnut flies and its possible consequences for mating success. Behav Ecol Sociobiol 34:187–195

    Google Scholar 

  • Papaj DR, Aluja M (1993) Temporal dynamics of host-marking in the tropical tephritid fly: the role of host quality. Behav Ecol 7:235–242

    Google Scholar 

  • Papaj DR, Messing RH (1996) Functional shifts in the use of parasitized hosts by a tephritid fly: the role of host quality. Behav Ecol 3:235–242

    Google Scholar 

  • Papaj DR, Roitberg BD, Opp SB (1989) Serial effects of host infestation on egg allocation in the Mediterranean fruit fly: a rule of thumb and its functional significance. J Anim Entomol 58:955–970

    Google Scholar 

  • Papaj DR, Roitberg BD, Opp SB, Aluja M, Prokopy RJ, Wong TTY (1990) Effect of marking pheromone on clutch size in the Mediterranean fruit fly. Physiol Entomol 15:463–468

    Google Scholar 

  • Papaj DR, Averill AL, Prokopy RJ, Wong TTY (1992) Host-marking pheromone and use of previously established oviposition sites by the Mediterranean fruit fly (Diptera: Tephritidae). J Insect Behav 5:583–598

    Google Scholar 

  • Partridge L, Ewing A, Chandler A (1987) Male size and mating success in Drosophila melanogaster: the roles of male and female behaviour. Anim Behav 35:555–562

    Google Scholar 

  • Pereira R, Sivinski J, Teal PEA (2010a) Influence of a juvenile hormone analog and dietary protein on male Anastrepha suspensa (Diptera: Tephritidae) sexual success. J Econ Entomol 103:40–46

    CAS  PubMed  Google Scholar 

  • Pereira R, Sivinski J, Teal P, Brockmann J (2010b) Enhancing male sexual success in a lekking fly (Anastrepha suspensa Diptera: Tephritidae) through a juvenile hormone analog has no effect on adult mortality. J Insect Physiol 56:1552–1557

    CAS  PubMed  Google Scholar 

  • Pereira R, Yuval B, Liedo P, Teal PEA, Shelly TE, McInnis DO, Hendrichs J (2012) Improving sterile male performance in support of programmes integrating the sterile insect technique against fruit flies. J Appl Entomol 137(Suppl 1):178–190

    Google Scholar 

  • Pérez-Staples D, Prabhu V, Taylor PW (2007) Post-teneral protein feeding enhances sexual performance of Queensland fruit flies. Physiol Entomol 32:225–232

    Google Scholar 

  • Pérez-Staples D, Shelly TE, Yuval B (2012) Female mating failure and the failure of “mating” in sterile insect programs. Entomol Exp Appl 146:66–78

    Google Scholar 

  • Perkins MV, Kitching W, Drew RAI, Moore CJ, König WA (1990a) Chemistry of fruit flies: composition of the male rectal gland secretions of some species of South-East Asian Dacinae. Re-examination of Dacus cucurbitae (melon fly). J Chem Soc Perkin Trans 1:1111–1117

    Google Scholar 

  • Perkins MV, Fletcher MT, Kitching W, Drew RAI, Moore CJ (1990b) Chemical studies of rectal gland secretions of some species of Bactrocera dorsalis complex of fruit flies (Diptera: Tephritidae). J Chem Ecol 16:2475–2487

    CAS  PubMed  Google Scholar 

  • Piñero JC, Mau RFL, Vargas RI (2011) A comparative assessment of the response of three fruit fly species (Diptera: Tephritidae) to a spinosad-based bait: effect of ammonium acetate, female age, and protein hunger. Bull Entomol Res 10:373–381

    Google Scholar 

  • Piñero JC, Souder SK, Vargas RI (2013) Residual attractiveness of a spinosad-containing protein-based bait aged under variable condition to Bactrocera dorsalis and B. cucurbitae (Diptera: Tephritidae) wild females in Hawaii. Fla Entomol 96:1077–1083

    Google Scholar 

  • Pitarra K, Katsoyannos BI (1990) Evidence for a host-marking pheromone in Chaetorellia australis. Entomol Exp Appl 54:278–295

    Google Scholar 

  • Poloni YJ, Silva MT (1986) Considerations on the reproductive behavior of Anastrepha pseudoparallela Loew 1873 (Diptera: Tephritidae). In: Fruit flies: II international symposium: proceedings: contributed papers–abstracts, Colymbari, Greece, 1986, Vol. 1. Elsevier, Amsterdam. pp 11–21

  • Poramarcom R (1988) Sexual communication in the Oriental fruit fly, Dacus dorsalis Hendel (Diptera: Tephritidae). PhD Thesis, University of Hawaii, Honolulu

  • Poramarcom R, Boake CRB (1991) Behavioural influences on male mating success in the Oriental fruit fly, Dacus dorsalis Hendel. Anim Behav 42:453–460

    Google Scholar 

  • Pritchard G (1969) The ecology of a natural population of Queensland fruit fly, Dacus tryoni. II. The distribution of eggs and its relation to behaviour. Austr J Zool 17:293–311

    Google Scholar 

  • Prokopy RJ (1972) Evidence for a marking pheromone deterring repeated oviposition in apple maggot flies. Environ Entomol 1:326–332

    Google Scholar 

  • Prokopy RJ (1975a) Oviposition-deterring fruit marking pheromone in Rhagoletis fausta. Environ Entomol 4:298–300

    Google Scholar 

  • Prokopy RJ (1975b) Mating behavior in Rhagoletis pomonella (Diptera: Tephritidae). V. Virgin female attraction to male odor. Can Entomol 107:905–908

    Google Scholar 

  • Prokopy RJ, Bush GL (1972) Mating behavior in Rhagoletis pomonella (Diptera: Tephritidae). III. Male aggregation in response to an arrestant. Can Entomol 104:275–283

    Google Scholar 

  • Prokopy RJ, Bush GL (1973) Mating behavior in Rhagoletis pomonella (Diptera: Tephritidae). IV. Courtship. Can Entomol 105:873–891

    Google Scholar 

  • Prokopy RJ, Koyama J (1982) Oviposition site partitioning in Dacus cucurbitae. Entomol Exp Appl 31:428–432

    Google Scholar 

  • Prokopy RJ, Webster RP (1978) Oviposition-deterring pheromone of Rhagoletis pomonella a kairomone for its parasitoid Opius lectus. J Chem Ecol 4:481–494

    CAS  Google Scholar 

  • Prokopy RJ, Bennett EW, Bush GL (1971) Mating behavior in Rhagoletis pomonella (Diptera: Tephritidae).I. Site of assembly. Can Entomol 103:1405–1409

    Google Scholar 

  • Prokopy RJ, Bennett EW, Bush GL (1972) Mating behavior in Rhagoletis pomonella (Diptera: Tephritidae). II. Temporal organization. Can Entomol 104:97–104

    Google Scholar 

  • Prokopy RJ, Reissig WH, Moericke V (1976) Marking pheromone deterring repeated oviposition in Rhagoletis flies. Entomol Exp Appl 20:170–178

    Google Scholar 

  • Prokopy RJ, Greany PD, Chambers DL (1977) Oviposition-deterring pheromone in Anastrepha suspensa. Environ Entomol 6:463–465

    Google Scholar 

  • Prokopy RJ, Ziegler JR, Wong TTY (1978) Deterrence of repeated oviposition by fruit marking pheromone in Ceratitis capitata (Diptera: Tephritidae). J Chem Ecol 4:55–63

    CAS  Google Scholar 

  • Prokopy RJ, Malavasi A, Morgante JS (1982) Oviposition-deterring pheromone in Anastrepha fraterculus flies. J Chem Ecol 8:763–771

    CAS  PubMed  Google Scholar 

  • Prokopy RJ, Green TA, Olson WA, Vargas RF, Kaneshia D, Wong TY (1989) Discrimination by Dacus dorsalis females (Diptera: Tephritidae) against larval infested fruit. Fla Entomol 72:319–323

    Google Scholar 

  • Raghu S (2004) Functional significance of phytochemical lures to dacine fruit flies (Diptera: Tephritidae): an ecological and evolutionary synthesis. Bull Entomol Res 94:385–399

    CAS  PubMed  Google Scholar 

  • Raghu S, Clarke AR (2003) Spatial and temporal partitioning of behaviour by adult dacines: direct evidence for methyl eugenol as a mate rendezvous cue for Bactrocera cacuminata. Physiol Entomol 28:175–184

    CAS  Google Scholar 

  • Ramos D (1991) Seleccion y comportamiento de apareamiento de la mosca Mediterranea de la fruta (Ceratitis capitata) en laboratorio y la comparacion con una cepa silvestre bajo condiciones semi-naturales. MS Thesis, Costa Rica University

  • Renou M, Guerrero A (2000) Insect parapheromones in olfaction research and semiochemical-based pest control strategies. Annu Rev Entomol 45:605–630

    CAS  PubMed  Google Scholar 

  • Reynolds JD, Gross MR (1990) Costs and benefits of female mate choice: is there a lek paradox? Am Nat 136:230–243

    Google Scholar 

  • Reynolds AH, Prokopy RJ (1997) Evaluation of odor lures for use with the red sticky spheres to trap apple maggot (Diptera: Tephritidae). J Econ Entomol 90:1655–1660

    CAS  Google Scholar 

  • Robacker DC (1988) Behavioral responses of female Mexican fruit flies, Anastrepha ludens, to components of male-produced sex pheromone. J Chem Ecol 14:1715–1726

    CAS  PubMed  Google Scholar 

  • Robacker DC, Hart WG (1985a) Courtship territoriality of laboratory-reared Mexican fruit flies, Anastrepha ludens (Diptera: Tephritidae), in cages containing host and nonhost trees. Ann Entomol Soc Am 78:488–494

    Google Scholar 

  • Robacker DC, Hart WG (1985b) (Z)-3-nonenol, (Z,Z)-3,6-nonandienol and (S,S)-(-)-epianastrephin: male produced pheromone of the Mexican fruit fly. Entomol Exp Appl 39:103–108

    CAS  Google Scholar 

  • Rocca JR, Nation JL, Strekowski L, Battiste MA (1992) Comparison of volatiles emitted by male Caribbean and Mexican fruit flies. J Chem Ecol 18:223–244

    CAS  PubMed  Google Scholar 

  • Rodriguero MS, Vilardi JC, Vera MT, Cayol JP, Rial E (2002) Morphometric traits and sexual selection in medfly (Diptera: Tephritidae) under field cage conditions. Fla Entomol 85:143–149

    Google Scholar 

  • Rogers CD, Armsworth CG, Poppy GM (2013) Conspecific transmission of insecticidal adhesive powder through mating in the Mediterranean fruit fly, Ceratitis capitata. J Pest Sci. doi: 10.1007/s10340-013-0545-3

  • Roitberg BD, Lalonde RG (1991) Host marking enhances parasitism risk for a fruit-infesting fly Rhagoletis basiola. Oikos 61:389–393

    Google Scholar 

  • Roitberg BD, van Lenteren JC, van Alaphen JJM, Galis F, Prokopy RJ (1982) Foraging behaviour of Rhagoletis pomonella, a parasite of hawthorn (Crataegus viridis), in nature. J Anim Ecol 51:307–325

    Google Scholar 

  • Roitberg BD, Cairl RS, Prokopy RJ (1984) Oviposition deterring pheromone influences dispersal distance in tephritid fruit flies. Entomol Exp Appl 35:217–220

    Google Scholar 

  • Ruther J, Steiner S (2008) Costs of female odour in males of the parasitic wasp Lariophagus distinguendus (Hymenoptera: Pteromalidae). Naturwissenschaften 95:547–552

    CAS  PubMed  Google Scholar 

  • Segura D, Petit-Marty N, Sciurano R, Vera T, Calcagno G, Allinghi A, Cendra PG, Cladera J, Vilardi J (2007) Lekking behavior of Anastrepha fraterculus (Diptera: Tephritidae). Fla Entomol 90:154–162

    Google Scholar 

  • Selivon D (1991) Alguns aspectos do comportamento de Anastrepha striata Schiner e Anastrepha bistrigata Bezzii (Diptera: Tephritidae). Master Dissertation, University of São Paulo, São Paulo

  • Sharp JL, Webb JC (1977) Flight performance and signaling sound of irradiated or unirradiated Anastrepha suspensa. Proc Hawaii Entomol Soc 22:525–532

    Google Scholar 

  • Shelly TE (1994) Consumption of methyl eugenol by male Bactrocera dorsalis (Diptera: Tephritidae): low incidence of repeat feeding. Fla Entomol 77:201–208

    CAS  Google Scholar 

  • Shelly TE (1999) Defense of oviposition sites by female oriental fruit flies (Diptera: Tephritidae). Fla Entomol 82:339–346

    Google Scholar 

  • Shelly TE (2000a) Aggression between wild and laboratory-reared sterile males of the Mediterranean fruit fly in a natural habitat (Diptera: Tephritidae). Fla Entomol 83:105–108

    Google Scholar 

  • Shelly TE (2000b) Flower-feeding affects mating performance in male oriental fruit flies Bactrocera dorsalis. Ecol Entomol 25:109–114

    Google Scholar 

  • Shelly TE (2000c) Effects of raspberry ketone on the mating success of male melon flies (Diptera: Tephritidae). Proc Hawaii Entomol Soc 34:163–167

    Google Scholar 

  • Shelly TE (2000d) Fecundity of female oriental fruit flies (Diptera: Tephritidae): Effects of methyl eugenol-fed and multiple mates. Ann Entomol Soc Am 93:559–564

    Google Scholar 

  • Shelly TE (2000e) Trapping male oriental fruit flies (Diptera: Tephritidae): does feeding on a natural source of methyl eugenol reduce capture probability? Fla Entomol 83:109–111

    Google Scholar 

  • Shelly TE (2001) Feeding on methyl eugenol and Fagraea berteriana flowers increases long-range female attraction by males of the oriental fruit fly (Diptera: Tephritidae). Fla Entomol 84:634–640

    CAS  Google Scholar 

  • Shelly TE (2006) Aromatherapy and medfly SIT. Fruit flies of economic importance: from basic to applied knowledge. In: Proceedings of the 7th international symposium on fruit flies of economic importance, Salvador, Brazil, 10–15 September 2006, pp 59–69

  • Shelly TE (2012) Mate choice by wild and mass-reared females of the Mediterranean fruit fly. J Appl Entomol 136:238–240

    Google Scholar 

  • Shelly TE, Dewire ALM (1994) Chemically mediated mating success in male oriental fruit flies (Diptera: Tephritidae). Ann Entomol Soc Am 87:375–382

    Google Scholar 

  • Shelly TE, Kaneshiro KY (1991) Lek behavior of the Oriental fruit fly, Dacus dorsalis, in Hawaii (Diptera: Tephritidae). J Insect Behav 4:235–241

    Google Scholar 

  • Shelly TE, Nishida R (2004) Larval and adult feeding on methyl eugenol and the mating success of male oriental fruit flies, Bactrocera dorsalis. Entomol Exp Appl 112:155–158

    Google Scholar 

  • Shelly TE, Whittier TS (1996) Mating competitiveness of sterile male Mediterranean fruit flies (Diptera: Tephritidae) in male-only releases. Ann Entomol Soc Am 89:754–758

    Google Scholar 

  • Shelly TE, Whittier TS, Kaneshiro KY (1994) Sterile insect release and the natural mating system of the Mediterranean fruit fly, Ceratitis capitata (Diptera: Tephritidae). Ann Entomol Soc Am 87:470–481

    Google Scholar 

  • Shelly TE, Whittier TS, Villalobos EM (1996) Trimedlure affects mating success and mate attraction in male Mediterranean fruit flies. Entomol Exp Appl 78:181–185

    Google Scholar 

  • Shelly TE, McInnis DO, Pahio E, Edu J (2004) Aromatherapy in the Mediterranean fruit fly (Diptera: Tephritidae): sterile males exposed to ginger root oil in prerelease storage boxes display increased mating competitiveness in field cage trials. J Econ Entomol 97:846–853

    PubMed  Google Scholar 

  • Shelly TE, Rendon P, Moscoso F, Menendez R (2010) Testing the efficacy of aromatherapy at the world’s largest eclosion facility for sterile males of the Mediterranean fruit fly (Diptera: Tephritidae). Proc Hawaii Soc Entomol 42:33–40

    Google Scholar 

  • Shelly T, Edu J, Pahio E (2012) Mate choice by lekking males: evidence from the Mediterranean fruit fly from field cage trials (Diptera: Tephritidae). Ann Entomol Soc Am 105:368–376

    Google Scholar 

  • Silva JG (1991) Biologia e comportamento de Anastrepha grandis (Macquart, 1846) (Diptera: Tephritidae). Master Dissertation, University of São Paulo, São Paulo

  • Silva MA, Bezerra-Silva GCD, Mastrangelo T (2012) The host marking pheromone application on the management of fruit flies—a review. Braz Arch Biol Technol 55:835–842

    CAS  Google Scholar 

  • Simões MH, Polloni YJ, Pauludetti MA (1978) Biología de algunas especies de Anastrepha (Diptera: Tephritidae) en laboratório. In: III Latin-American entomology congress. Proceedings: contributed papers–abstracts, Ilheus

  • Sivinski J, Aluja M, Dodson G, Freidberg A, Headrick D, Kaneshiro K, Landolt P (2000) Topics in the evolution of sexual behavior in the Tephritidae. In: Aluja M, Norrbom AL (eds) Fruit flies (Tephritidae): phylogeny and evolution of behavior. CRC Press, Boca Raton, pp 751–792

    Google Scholar 

  • Smith DC, Prokopy RJ (1980) Mating behavior in Rhagoletis pomonella (Diptera: Tephritidae). VI. Site of early-season encounters. Can Entomol 112:585–590

    Google Scholar 

  • Stelinski LL, Zhang A, Onagbola EO, Meyer WL (2009) Recognition of foreign oviposition marking pheromones is context dependent and determined by preimaginal conditioning. Commun Integr Biol 2:391–393

    PubMed Central  PubMed  Google Scholar 

  • Stokes JB, Uebel EC, Warthen JD, Jacobson M, Flippen-Anderson JL, Gilardi R, Spishakoff LM, Wilzer KR (1983) Isolation and identification of novel lactones from male Mexican fruit flies. J Agric Food Chem 31:1162–1167

    CAS  Google Scholar 

  • Straw NA (1989) Evidence for an oviposition-deterring pheromone in Tephritis bardanae (Schrank) (Diptera: Tephritidae). Oecologia 78:121–130

    Google Scholar 

  • Suckling DM, Jang EB, Holder P, Carvalho L, Stephens AEA (2008) Evaluation of lure dispensers for fruit fly surveillance in New Zealand. Pest Manag Sci 64:848–856

    CAS  PubMed  Google Scholar 

  • Sugimoto A (1979) Smoke emission by the melon fly, Dacus cucurbitae Coquillett. Jpn J Appl Entomol Zool 23:40–42

    Google Scholar 

  • Suzuki Y, Koyama J (1980) Temporal aspects of mating behavior of the melon fly, Dacus cucurbitae Coquillett (Diptera: Tephritidae): a comparison between laboratory and wild strains. Appl Entomol Zool 15:215–224

    Google Scholar 

  • Suzuki Y, Koyama J (1981) Courtship behavior of the melon fly, Dacus cucurbitae Coquillett (Diptera: Tephritidae). Appl Entomol Zool 16:164–166

    Google Scholar 

  • Tadeo E, Aluja M, Rull J (2013) Alternative mating tactics as potential prezygotic barriers to gene flow between two sister species of frugivorous fruit flies. J Insect Behav 26:708–720

    Google Scholar 

  • Tan KH, Nishida R (1995) Incorporation of raspberry ketone in the rectal glands of males of the Queensland fruit fly, Bactrocera tryoni Froggatt (Diptera: Tephritidae). Appl Entomol Zool 30:494–497

    CAS  Google Scholar 

  • Tan KH, Nishida R (1996) Sex pheromone and mating competition after methyl eugenol consumption in the Bactrocera dorsalis complex. In: McPheron BA, Steck GJ (eds) Fruit fly pests. St. Lucie Press, Delray Beach, pp 147–153

    Google Scholar 

  • Tan KH, Nishida R (2007) Zingerone in the floral synomone of Bulbophyllum baileyi (Orchidaceae) attracts Bactrocera fruit flies during pollination. Biochem System Ecol 35:334–341

    CAS  Google Scholar 

  • Tauber MJ, Toschi CA (1965a) Bionomics of Euleia fratria. I. Life history and mating behavior. Can J Zool 43:369–379

    Google Scholar 

  • Tauber MJ, Toschi CA (1965b) Life history and mating behavior of Tephritis stigmatica. Pan Pac Entomol 41:73–79

    Google Scholar 

  • Taylor PW, Yuval B (1999) Postcopulatory sexual selection in Mediterranean fuit flies: advantages for large and protein-fed males. Anim Behav 58:247–254

    PubMed  Google Scholar 

  • Teal PEA, Pereira R, Segura DF, Haq I, Gomez-Simuta Y, Robinson AS, Hendrichs J (2013) Methoprene and protein supplements accelerate reproductive development and improve mating success of male tephritid flies. J Appl Entomol 137(Suppl 1):91–98

    CAS  Google Scholar 

  • Vargas RI, Stark JD, Kido MH, Ketter HM, Whitehand LC (2000) Methyl eugenol and cue-lure traps for suppression of male oriental fruit flies and melon flies (Diptera: Tephritidae) in Hawaii: effects of lure mixtures and weathering. J Econ Entomol 93:81–87

    CAS  PubMed  Google Scholar 

  • Vargas RI, Miller NW, Stark JD (2003) Field trials of spinosad as a replacement for naled DDVP, and malathion in methyl eugenol and cue-lure bucket traps to attract and kill male oriental fruit flies and melon flies (Diptera: Tephritidae) in Hawaii. J Econ Entomol 96:1780–1785

    CAS  PubMed  Google Scholar 

  • Vargas RI, Stark JD, Mackey B, Bull R (2005) Weathering trials of Amulet Cue-Lure and Amulet Methyl Eugenol ‘‘attract and kill’’ stations with male melon flies and oriental fruit flies (Diptera: Tephritidae) in Hawaii. J Econ Entomol 98:1551–1559

    Google Scholar 

  • Vargas RI, Mau RFL, Jang EB, Faust RM, Wong L (2008) The Hawaii fruit fly area-wide pest management program. In: Koul O, Cuperus GW, Elliott NC (eds) Area wide pest management: theory to implementation. CABI Books, London, pp 300–325

    Google Scholar 

  • Vargas RI, Shelly TE, Leblanc L, Piñero JC (2010) Recent advances in methyl eugenol and cue lure technologies for fruit fly detection, monitoring and control in Hawaii. In: Liwack (ed) Vitamins and hormones, vol 83. Elsevier, Academic Press, Burlington, pp 575–596

    Google Scholar 

  • Vargas RI, Souder SK, Mackey B, Cook P, Morse JG, Stark JD (2012) Field trials of solid triple lure (Trimedlure, Methyl Eugenol, Raspberry Ketone, and DDVP) dispensers for detection and male annihilation of Ceratitis capitata, Bactrocera dorsalis, and Bactrocera cucurbitae (Diptera: Tephritidae) in Hawaii. J Econ Entomol 105:1557–1565

    PubMed  Google Scholar 

  • von Rolli K (1976) Die akustischen Sexualsignale von Ceratitis capitata Wied. und Dacus oleae Gmel. Z Ang Entomol 81:219–223

    Google Scholar 

  • Wang XG, Messing RH (2003) Foraging behavior and patch time allocation by Fopius arisanus, an egg-larval parasitoid of tephritid fruit flies. J Insect Behav 16:593–612

    Google Scholar 

  • Wang XG, Johnson MW, Daane KM, Nadel H (2009a) High summer temperatures affect the survival and reproduction of olive fruit fly (Diptera: Tephritidae). Env Entomol 38:1496–1504

    CAS  Google Scholar 

  • Wang XG, Johnson MW, Daane KM, Opp S (2009b) Combined effects of heat stress and food supply on flight performance of olive fruit fly (Diptera: Tephritidae). Ann Entomol Soc Am 102:727–734

    Google Scholar 

  • Webb JC, Sharp L, Chambers DL, McDow JJ, Benner JC (1976) Analysis and identification of sounds produced by the male Caribbean fruit fly, Anastrepha suspensa. Ann Entomol Soc Am 69:415–420

    Google Scholar 

  • Webb JC, Calkins CO, Chambers DL, Schwienbacher W, Russ K (1983) Acoustical aspects of behaviour of Mediterranean fruit flies, Ceratitis capitata: analysis and identification of courtship sounds. Entomol Exp Appl 33:1–8

    Google Scholar 

  • Webb JC, Sivinski J, Litzkow C (1984) Acoustical behaviour and sexual success in the Caribbean Fruit Fly, Anastrepha suspensa (Loew) (Diptera: Tephritidae). Environ Entomol 13:651–656

    Google Scholar 

  • Wee SL, Tan KH, Nishida R (2007) Pharmacophagy of methyl eugenol by males enhances sexual selection of Bactrocera carambolae. J Chem Ecol 33:1272–1282

    CAS  PubMed  Google Scholar 

  • White IM, Elson-Harris MM (1992) Fruit flies of economic significance: their identification and bionomics. CAB International, Wallingford

    Google Scholar 

  • Whittier TS, Kaneshiro KY (1995) Intersexual selection in the Mediterranean fruit fly: does female choice enhance fitness? Evolution 49:990–996

    Google Scholar 

  • Whittier TS, Kaneshiro KY, Prescott LD (1992) Mating behavior of Mediterranean fruit flies (Diptera: Tephritidae) in a natural environment. Ann Entomol Soc Am 85:214–218

    Google Scholar 

  • Whittier TS, Nam FY, Shelly TE, Kaneshiro KY (1994) Male courtship success and female discrimination in the Mediterranean fruit fly (Diptera: Tephritidae). J Insect Behav 7:159–170

    Google Scholar 

  • Widemo F, Owens IPF (1999) Size and stability of vertebrate leks. Anim Behav 58:1217–1221

    PubMed  Google Scholar 

  • Yuval B, Hendrichs J (2001) Behavior of flies in the genus Ceratitis (Dacinae: Ceratitidini). In: Aluja M, Norrbom AL (eds) Fruit flies (Tephritidae): phylogeny and evolution of behavior. CRC Press, Boca Raton, pp 429–457

    Google Scholar 

  • Zapien G, Hendrichs J, Liedo P, Cisneros A (1983) Comparative mating behaviour of wild and mass-reared sterile medfly Ceratitis capitata (Wied.) on a field caged host tree. II. Female mate choice. In: Cavalloro R (ed) Fruit flies of economic importance. A.A. Balkema, Rotterdam, pp 397–409

    Google Scholar 

  • Zervas GA (1982) Reproductive physiology of Dacus oleae (Gmel.) (Diptera: Trypetidae). Comparison of a wild and artificially reared flies. Geoponica 282:10–14

    Google Scholar 

  • Zouros E, Krimbas CB (1970) Frequency of male bigamy in natural population of the olive fruit fly Dacus oleae as found by using enzyme polymorphism. Entomol Exp Appl 13:1–9

    Google Scholar 

  • Zunic Kosi A, Chinta SP, Headrick D, Cokl A, Millar JG (2013) Do chemical signals mediate reproductive behavior of Trupanea vicina, an emerging pest of ornamental marigold production in California? Entomol Exp Appl 149:44–56

    CAS  Google Scholar 

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Acknowledgments

We thank Nicolas Desneux for his kind invitation to write this review and three anonymous reviewers for their comments on an earlier version of the manuscript. We are grateful to Adriano Carpita and Alfio Raspi for helpful discussion about Tephritidae chemoecology, Paolo Giannotti and Francesco Lanzo for artwork, Gabriella Bonsignori and Giulia Giunti for their help during manuscript preparation. Giovanni Benelli is particularly grateful to Mark G. Wright, Kenneth Kaneshiro and Luc LeBlanc for constructive discussions on evolutionary biology and sexual communication during a stay at the University of Hawaii at Manoa.

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Authors and Affiliations

  1. Insect Behaviour Group, Department of Agriculture, Food and Environment, University of Pisa, Via del Borghetto 80, 56124, Pisa, Italy

    Giovanni Benelli & Angelo Canale

  2. Department of Environmental Science, Policy and Management, University of California, Berkeley, CA, 94720-3114, USA

    Kent M. Daane

  3. Hubei Key Laboratory of Utilization of Insect Resources and Sustainable Control of Pests, College of Plant Science and Technology, Huazhong Agricultural University, Shizi Mountain Road, Wuhan, 430070, China

    Chang-Ying Niu

  4. Kauai Agricultural Research Center, University of Hawaii at Manoa, 7370 Kuamo’o Road, Kapaa, HI, 97646, USA

    Russell H. Messing

  5. U.S. Pacific Basin Agricultural Research Center, USDA, ARS, Hilo, HI, 96720, USA

    Roger I. Vargas

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  1. Giovanni Benelli
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  2. Kent M. Daane
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  3. Angelo Canale
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  4. Chang-Ying Niu
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  6. Roger I. Vargas
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Correspondence to Giovanni Benelli.

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Communicated by N. Desneux.

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Benelli, G., Daane, K.M., Canale, A. et al. Sexual communication and related behaviours in Tephritidae: current knowledge and potential applications for Integrated Pest Management. J Pest Sci 87, 385–405 (2014). https://doi.org/10.1007/s10340-014-0577-3

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