J Sci (2014) 87:385–405 DOI 10.1007/s10340-014-0577-3

REVIEW

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

Giovanni Benelli • Kent M. Daane • Angelo Canale • Chang-Ying Niu • Russell H. Messing • Roger I. Vargas

Received: 18 October 2013 / Accepted: 7 March 2014 / Published online: 29 March 2014 Ó Springer-Verlag Berlin Heidelberg 2014

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

Communicated by N. Desneux. Keywords Tephritidae Á Courtship Á Lekking mating system Á Male annihilation technique Á Oviposition marking Electronic supplementary material The online version of this article (doi:10.1007/s10340-014-0577-3) contains supplementary pheromone Á Parapheromones Á Sex pheromones Á Sexual material, which is available to authorized users. selection Á Sterile insect technique

G. Benelli (&) Á A. Canale R. H. Messing Insect Behaviour Group, Department of Agriculture, Food and Kauai Agricultural Research Center, University of Hawaii at Environment, University of Pisa, Via del Borghetto 80, Manoa, 7370 Kuamo’o Road, Kapaa, HI 97646, USA 56124 Pisa, Italy e-mail: [email protected]; [email protected] R. I. Vargas U.S. Pacific Basin Agricultural Research Center, USDA, ARS, K. M. Daane Hilo, HI 96720, USA Department of Environmental Science, Policy and Management, University of California, Berkeley, CA 94720-3114, USA

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

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Introduction combat in lekking sites, (ii) physical and chemical cues affecting mate choice dynamics during courtship and mat- The family Tephritidae contains over 4,000 species, many of ing, (iii) fitness-promoting female behaviours that occur at which constitute enormous threats to fruit and vegetable oviposition sites [mainly the use of oviposition marking production throughout the world, causing both quantitative pheromones (OMPs) and the occurrence of female–female and qualitative losses (Ekesi and Billah 2007). Many tephritid fights for single oviposition sites] and (iv) future perspectives species are highly polyphagous, attacking economically and potential contributions of current knowledge about important fruit and vegetable crops including mango, peach, sexual communication to IPM programs for tephritid pests. , pear, citrus, guava, avocado, tomato, pepper and cucurbits (White and Elson-Harris 1992; Liu et al. 2013), whereas others are oligophagous (Daane and Johnson 2010; Methods Dong et al. 2013). Adult female fruit flies can cause direct damage by laying eggs under the skin of fruits and vegetables; A first screening of current knowledge was based on the eggs hatch into larvae that feed in the decaying flesh of the occurrence of papers with the terms ‘Tephritidae mating’ in crop. Infested fruits and vegetables quickly become inedible SCOPUS (as of September 2013): 436 studies were iden- or drop to the ground (Ekesi and Mohamed 2011). Further- tified. Then, bibliographical data were refined through more, due to their susceptibility to invasive tephritid species, further database screenings using terms related to the three many fruit-producing countries have imposed strict quaran- major behavioural areas of this study (studies not focused tine restrictions on the import of products from countries on tephritid species were disregarded): infested with particular fruit fly species, and/or require that – ‘Tephritidae lek’ (49 papers) and ‘Tephritidae aggres- fruits and vegetables undergo quarantine treatment before sion’ (9 papers) for the section ‘Before courtship: their importation is allowed. Thus, suppression or eradication lekking sites and male–male combats’; of fruit flies has often been the goal of control programs (Estes – ‘Tephritidae courtship’ (93 papers), ‘Tephritidae sexual et al. 2012). Chemical control (i.e. cover and bait sprays) communication’ (18 papers) and ‘Tephritidae sex based on conventional insecticides (i.e. organophosphates and pheromone’ (97 papers) for the section ‘Courtship pyrethroids) and biotechnical tools [e.g. sterile insect tech- and mating behaviour: how physical and olfactory cues nique (SIT) and male annihilation technique (MAT)], rather drive mate choice dynamics’; than biological control, have been the main weapons used in – ‘Tephritidae oviposition marking pheromone’ (26 most control programs (Daane and Johnson 2010; Canale and papers) and ‘Tephritidae aggression’ (9 papers) for Benelli 2012; Lauzon and Potter 2012; Beris et al. 2013). the section ‘After copulation: some fitness-promoting Research on courtship and mating behaviour of insects is female tools’. one of the first steps towards a full understanding of their evolutionary behavioural ecology (Kirkendall 1983). The above-mentioned studies are provided in Electronic Investigating mating behavioural sequences could help to Supplementary Material, ESM, ‘Appendix A’. Then, unravel mate assessment and mate choice dynamics both in additional research was considered through cross-refer- agricultural pests (Jime´nez-Pe´rez et al. 2013; Benelli et al. ences found in these papers and checking for the above- 2012a) and in biological control (Benelli and mentioned terms on Google Scholar and Web of Science. Canale 2012a; Benelli et al. 2012b), adding useful infor- Additional information about the sex pheromones of six mation to help build behaviour-based control strategies. In key pests (A. ludens, B. cucurbitae, B. dorsalis, B. oleae, C. this paper, we review current knowledge about sexual capitata and R. pomonella) was found using their Latin communication and related behaviour in Tephritidae, with names as keywords on a dedicated database, www.pher special focus on six key agricultural pests: the Mexican fruit obase.com (El-Sayed 2013). We are aware that our review fly, Anastrepha ludens (Loew), the melon fly, Bactrocera may be biased by the strict use of the above-mentioned cucurbitae (Coquillett), the oriental fruit fly, Bactrocera terms while disregarding other, more general ones (e.g. dorsalis (Hendel), the fruit fly, Bactrocera oleae , life history traits) as well as our omission of non- (Rossi), the Mediterranean fruit fly, Ceratitis capitata (Wi- English literature or older literature or books not included edemann) and the apple maggot, Rhagoletis pomonella in SCOPUS and Web of Science. (Walsh). Furthermore, we provide a critical survey of the current literature concerning two important post-copulation female behaviours: same-sex aggressive interactions and Before courtship: lekking sites and male–male combat oviposition marking behaviour, since both issues have major implications in tephritid Integrated Pest Management (IPM) Tephritidae are lekking species (i.e. they form aggregations programs. Overall, we examine (i) features of male–male in which each male defends a small territory to perform 123 J Pest Sci (2014) 87:385–405 387 courting rituals to court females and mate); they do not rely weakly rely on lek dynamics to mate with females (Dodson on resource-based mating systems (Ho¨glund and Alatalo 1987). 1995). Tephritid lekking sites are focal places in which Among Tephritidae leks, male–male aggression is male–male competition for partners (i.e. intra-sexual characterized by reciprocal wing waving (Fig. 1a) followed selection) and active choice of males by females (i.e. inter- by head butting and/or boxing with forelegs, as described sexual selection) drive the evolution of sexual traits (Fiske in B. oleae (Benelli 2014), C. capitata (Bricen˜o et al. et al. 1998;Caˆmara de Aquino and Joachim-Bravo 2013). 1999), R. indifferens (AliNiazee 1974; Messina and Subler Generally, lekking males initiate sexual behaviour by 1995), R. pomonella (Biggs 1972), R. completa (Boyce releasing long-range pheromones that attract females to 1934), A. trixa, V. dodsoni (Dodson 1987), T. curvicauda behavioural exhibition sites (Landolt and Heath 1988; (Landolt and Hendrichs 1983), A. ludens (Robacker and Landolt et al. 1988; Landolt et al. 1992; Shelly 2001). Hart 1985a) and Procecidochares sp. (Dodson 1986). In Then, females discriminate among lek participants and other tephritids, the sequence of events during male–male copulate with males that perform the best courtship combat is less elaborate. For instance, in B. dorsalis the behaviour sequence, which includes wing movements male simply runs at the other male and drives it off the leaf, combined with olfactory and tactile cues, prior to mounting whereas pouncing followed by head butting is rare (Shelly attempts (Yuval and Hendrichs 2001; Benelli et al. 2012a; and Kaneshiro 1991). In Paracantha gentilis Hering, males Caˆmara de Aquino and Joachim-Bravo 2013). Well docu- display agonistic behaviours composed of wing waving, mented examples include the melon fly, B. cucurbitae chasing and head butting, while boxing has never been (Kuba and Koyama 1985), the olive fruit fly, B. oleae observed (Headrick and Goeden 1990). Male-male combat (Benelli et al. 2012a; Benelli 2014), the Mediterranean fruit has also been reported for Euaresta stigmatica Coquillett, fly, C. capitata (Arita and Kaneshiro 1989; Whittier et al. Euarestoides acutangulus (Thomson), Tephritis stigmatica 1992), the Mexican fruit fly, A. ludens (Robacker and Hart (Coquillett) and R. completa, but detailed information is 1985a), the Western cherry fruit fly, Rhagoletis indifferens not available on the behavioural sequence of these inter- Curran (AliNiazee 1974; Messina and Subler 1995), the actions (Tauber and Toschi 1965a, b; Headrick and Goeden apple maggot, R. pomonella (Biggs 1972), the walnut husk 1994). fly, Rhagoletis completa Cresson and Rhagoletis suavis Interestingly, prior residence at a given site substantially (Loew) (Boyce 1934). In some species, however, aggres- enhances a male’s chances to win a fight within some te- sion between males appears infrequent and unimportant in phritid species, including A. ludens (Burk 1984; Robacker determining male mating success (Whittier et al. 1994; and Hart 1985a), B. oleae (Benelli 2014) and R. completa Segura et al. 2007). (Tadeo et al. 2013). Furthermore, Ramos (1991) noted that The position of lekking sites varies among different fruit in wild Costa Rican C. capitata, resident males won over fly species. Leks can occur on various parts of tephritid 80 % of the aggressive encounters. In contrast, in Hawaiian host , or away from host plants (Aluja and Norrbom C. capitata, male intruders won more than two-thirds of all 2010). For instance, males of the papaya fruit fly, Toxot- aggressive interactions with resident males (Whittier et al. rypana curvicauda Gerstaecker, prefer papaya fruits as 1992). In a further study on Hawaiian medfly males (Shelly lekking sites (Landolt and Hendrichs 1983). Similarly, 2000a), prior residency did not appear to provide any Rhagoletis spp. males usually converge in close proximity advantage; the same was also shown in B. dorsalis males to cherry fruits (Messina and Subler 1995). Olive fruit fly (Shelly and Kaneshiro 1991). males prefer the windward side of olive trees, and perform Through the lek mating system, tephritid females can most male–male aggression behaviours, as well as mating achieve direct benefits (e.g. guaranteed fertility, less risk of interactions, on olive leaves (Benelli 2014). Medfly male copulation interruption, avoidance of predators and leks occur on various parts of their host trees, including reduced probability of acquiring diseases) (Whittier and fruits, leaves and trunks (Arita and Kaneshiro 1989; Shelly Kaneshiro 1995; Shelly 2000b; Kumaran et al. 2013), and and Kaneshiro 1991). In contrast, melon fly males gather also indirect Fisherian benefits associated with the quality mainly around non-host trees or weeds, to which the of the genetic resources to be donated to their offspring (the females are attracted. Males alight on the lower surface of ‘good genes’ hypothesis, or the ‘Fisher’ model) (Whittier tree leaves or weeds, stridulate with their wings and release and Kaneshiro 1995; Reynolds and Gross 1990; Kirkpa- a pheromone. Males on the leaves exclude other males that trick and Ryan 1991; Jones et al. 1998). On the other hand, approach them, and create small individual territories there are some costs to females participating in leks that around themselves (Kuba and Koyama 1985; Koyama et al. should be taken into account. Female flies have a large 2004). Lastly, other species, such as the gall-forming te- number of potential males to evaluate as possible sexual phritid flies Aciurina trixa Curran and Valentibulla dodsoni partners (Janetos 1980). They can have losses of potential Foote, do not maintain individual territories and only mates to competitors and extensive investment of time and 123 388 J Pest Sci (2014) 87:385–405

Fig. 1 An overview of sexual communication and related behaviours returned in the start position (b) (from Benelli et al. 2012a). e–g The in a tephritid pest of worldwide importance, the olive fruit fly, peculiar grooming reaction performed by males during female’s Bactrocera oleae. a Before courtship: wing waving among fighting courtship: e then males vibrate their wings fast; f during wing males competing for lekking leaves (redrawn from Benelli 2014). b–d vibration, it periodically rubs a hind tarsus on the distal tip of the Frontal view of male wing vibration plus stridulation during the abdomen, in close proximity of the anus, in order to imbue the tarsal female’s courtship. When vibration starts, the wings are close to the brush of the 1st tarsomere with the rectal secretion. Subsequently g it abdomen and approximately parallel to the ground (b). Then, the rubs the tarsus on the urotergal area (from Canale et al. 2013a). wings are rapidly raised and rolled on their longitudinal axes (c). h After mating: boxing acts between two females competing for an When the wings are raised in the upper position (d), they are rapidly oviposition site (redrawn from Benelli 2014) metabolic energy in mating activities (Reynolds and Gross (AliNiazee 1974; Messina and Subler 1995; Benelli 2014). 1990). Thus, the evolution of female mate preference Under field conditions, tephritid males may maintain their seems to be shaped by a balance among the above-men- lek sites for far longer, thus gaining more from the success tioned costs and benefits (Anjos-Duarte et al. 2011 and of aggressive interactions. On this point, further field references therein). research is strongly encouraged. In summary, tephritid flies appear to have a non- resource-based lek mating system that strongly differs from the classical lek behaviour of vertebrates (Widemo and Owens 1999) regarding the ephemeral nature of fruit fly lek Courtship and mating behaviour: olfactory sites (Shelly and Kaneshiro 1991), the avoidance of serious and physical cues driving mate choice dynamics injuries during male–male aggression and the low site fidelity of the participating individuals (Ho¨glund and Courtship and mating behaviour: some general rules Lundberg 1987; Benelli 2014). However, even if tephritid leks appear ephemeral compared to those of many verte- Among Tephritidae, the sequence of courtship events brate species that occur at the same site year after year (e.g. leading to copulation is usually divided into three key Bradbury et al. 1989), in some species (e.g. C. capitata), phases: (i) a male defends its small territory against other they have been reported as relatively long-lasting sites, males, then produces olfactory (e.g. sex pheromones), covering a period of at least several weeks (Whittier et al. acoustic (e.g. wing vibrations) and also visual signals to 1992). The low fidelity for individual territories within a attract females; (ii) an individual female flies near the male, lek site could be partially due to high fly density per unit of lands and walks to the male; (iii) the male perceives the area, a common feature of restricted environments, where female and tries one or more copulation attempts (Koyama the majority of these studies have been conducted 1989). This is true for many genera, including Anastrepha

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Table 1 Sex pheromones routing courtship and mating dynamics in cucurbitae, the oriental fruit fly, Bactrocera dorsalis, the olive fruit five tephritid species of huge agricultural importance: the Mexican fly, Bactrocera oleae and the Mediterranean fruit fly, Ceratitis fruit fly, Anastrepha ludens, the melon fruit fly, Bactrocera capitata Tephritid species Semiochemical(s) Behavioural function References

Mexican fruit fly, (Z)-3-Nonenol Male-borne pheromone Battiste et al. (1983); Stokes et al. Anastrepha ludens (Z,Z)-3,6-Nonandienol (1983); Robacker and Hart (1985b); Robacker (1988); (E)-Hexahydro-(E)-4,7a-dimethyl-4-vinylbenzofuran- Rocca et al. (1992) 2(3H)-one (E,E)-4,8-Dimethyl-3,8-decadien-10-olide (E,E)-3,7,11-Trimethyl-1,3,6,10-dodecatetraene 1-Methyl-4-(6-methylhepta-1,5-dien-2-yl)-cyclohex-1- ene 1-Methyl-4-(1-methylethenyl)-cyclohexene Melon fly, 2,3,5,6-Tetramethylpyrazine Male-borne pheromone Baker et al. (1982a) Bactrocera 2-Methylpyrazine cucurbitae 2,3,5-Trimethylpyrazine 2-Ethoxybenzoic acid Pentacosane Male-borne pheromone Ohinata et al. (1982) Heptacosane Nonacosane (E)-5-(3,6-heptadienyl)-dihydro-2(3H)-furanone N-3-Methylbutylacetamide Female-borne pheromone Baker and Bacon (1985) (E,E)-2,8-Dimethyl-1,7-dioxaspiro[5.5]undecane (Z,E)-2,8-Dimethyl-1,7-dioxaspiro[5.5]undecane Ethyl 4-hydroxybenzoate Male-borne pheromone Perkins et al. (1990a) Propyl 4-hydroxybenzoate Oriental fruit fly, N-2-Methylbutylpropanamide Male-borne pheromone Ohinata et al. (1982) Bactrocera (E,E)-2,8-Dimethyl-1,7-dioxaspiro[5.5]undecane Female-borne pheromone Baker and Bacon (1985) dorsalis (E,E)-8-Ethyl-2-methyl-1,7-dioxaspiro[5.5]undecane (E,E)-8-Methyl-2-propyl-1,7-dioxaspiro[5.5]undecane 2-Allyl-4,5-dimethoxyphenol Male-borne pheromone Nishida et al. (1988a, b) 4-((E)-3-Hydroxyprop-1-enyl)-2-methoxyphenol (Z)-3,4-Dimethoxycinnamyl alcohol (E,E)-2-Ethyl-8-methyl-1,7-dioxaspiro[5.5]undecane Male-borne pheromone Perkins et al. (1990b) 3-Hydroxy-2,8-dimethyl-1,7-dioxaspiro[5.5]undecane Dimethyl butanedioate Trimethyl phosphate N-3-Methylbutylacetamide 2,3,5-Trimethylpyrazine Olive fruit fly, 1,7-Dioxaspiro[5.5]undecane Female-borne pheromone Baker et al. (1980), (1982b), Bactrocera oleae 3-Hydroxy-1,7-dioxaspiro[5.5]undecane Gariboldi et al. (1983), Mazomenos and Haniotakis 4-Hydroxy-1,7-dioxaspiro[5.5]undecane (1985), Levi-Zada et al. (2012), 2,6,6-Trimethylbicyclo[3.1.1]hept-2-ene Canale et al. (2012) Nonanal Ethyl dodecanoate 1,7-Dioxaspiro[5.5]undecane Male-borne pheromone Cavalloro et al. (1983); Fletcher Diethyl 5-oxononanedioate (young males) et al. (1992); Canale et al. (2012); Benelli et al. (2013a) (4S,6S)-4-Hydroxy-1,7-dioxaspiro[5.5]undecane (4R,6S)-4-Hydroxy-1,7-dioxaspiro[5.5]undecane (3R,6S)-3-Hydroxy-1,7-dioxaspiro[5.5]undecane (Z)-9-Tricosene Male-borne pheromone Carpita et al. (2012); Canale et al. (sexually mature males) (2013a)

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Table 1 continued Tephritid species Semiochemical(s) Behavioural function References

Mediterranean fruit Methyl (E)-6-nonenoate Male-borne pheromone Jacobson et al. (1973); Jacobson fly, Ceratitis (E)-6-Nonen-1-ol and Ohinata (1980); Baker et al. capitata (1985); Heath et al. (1991); Jang (1S-exo)-1,3,3-Trimethylbicyclo[2.2.1]heptan-2-ol et al. (1994) 3,4-Dihydro-2H-pyrrole Ethyl (E)-3-octenoate (E)-3,7-Dimethyl-2,6-octadienyl acetate (E,E)-3,7,11-Trimethyl-1,3,6,10-dodecatetraene (E)-2-Hexenoic acid Dihydro-3-methylfuran-2(3H)-one 3,5-Dimethyl-2-ethylpyrazine 2,6-Dimethyl-2,7-octadien-6-ol Ethyl acetate

(Robacker 1988; Rocca et al. 1992; Goncalves et al. 2013), diminish after mating (Canale et al. 2013a and references Ceratitis (Jang et al. 1994), Trupanea (Zunic Kosi et al. therein). 2013) and the majority of Bactrocera species (Perkins et al. 1990a; Poramarcom and Boake 1991). The scent of mating: male- and female-borne sex Several tephritid species show more complex courtship pheromones and mating behaviours. A good example is the C. capitata mating sequence, in which additional courtship acts have In tephritid flies, courtship and mating are influenced by been detected, including male wing buzzing (Bricen˜o et al. both physical and olfactory cues. Olfactory stimuli in 1996), head rocking (Webb et al. 1983; Bricen˜o et al. 1996) particular play a key role during the mate-searching phase. and aristae tapping before the copulation attempt (Miranda It is generally acknowledged that tephritid males produce 2000). Interestingly, males of some species improve the sex pheromones to attract females (Table 1) (El-Sayed dispersion of pheromone signals via peculiar behaviours, 2013). However, there are at least three major exceptions including wing acts (e.g. hamation and evanation, sensu of key importance, in which both sexes produce sex Headrick and Goeden 1994), abdominal pleural distention, pheromones: the melon fly (Baker and Bacon 1985; Perkins dabbing the substrate with the proctiger and leg rubbing et al. 1990a), the oriental fruit fly (Baker and Bacon 1985; movements from the rectal glands to the urotergal ones Perkins et al. 1990b) and the olive fruit fly (Canale et al. (Sivinski et al. 2000 and references therein; Canale et al. 2013a). 2013a). Tephritid males can also provide females with In the olive fruit fly, the perception of both female- and nuptial gifts (i.e. mating trophallaxis). This behaviour is male-borne olfactory cues is crucial during courtship and part of the courtship and mating sequence in at least 15 mating. Virgin females produce a multi-component sex tephritid species, and it may occur shortly before, during or pheromone containing four constituents with a synergistic shortly after copulation. To the best of our knowledge, action: 1,7-dioxaspiro[5.5]undecane (DSU, hereafter) and mating trophallaxis has not been observed in key tephritid methyl dodecanoate are produced in the rectal glands, pests, thus we avoid a detailed analysis of it here (see while a-pinene and nonanal are produced elsewhere in the Sivinski et al. 2000 for a dedicated review). body (Baker et al. 1980; Mazomenos and Haniotakis In general, tephritid males are polygamous and mate 1981, 1985). Gerofotis et al. (2013) recently showed that repeatedly if receptive females are available (Zouros and the exposure of sexually mature male and female olive Krimbas 1970; Zervas 1982; Opp and Prokopy 2000). In flies to the aroma of a-pinene increases subsequent mat- most species, females can mate more than once (China- ing success compared to non-exposed individuals. Possi- jariyawong et al. 2010 and references therein); however, ble physiological mechanisms at the basis of this finding for some species, only a low percentage of females have are still unknown. However, among these compounds, multiple matings (e.g. 5 % in field caught C. capitata DSU is reported as the most abundant component and females: Bonizzoni et al. 2006). In males, the female exhibits the highest biological activity towards males mating status does not usually affect mating preference (Mazomenos and Haniotakis 1981, 1985). Interestingly, (Benelli et al. 2012a); this seems to be correlated with young B. oleae males also produce DSU in the rectal female production of sex attractants that does not cease or glands. In males, the production of DSU starts from the

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1st day after adult emergence, reaches a maximum when gonad maturation is complete, then decreases to 0 by the 11th day (Canale et al. 2012; Levi-Zada et al. 2012). The presence of DSU in young males cannot be considered a case of chemical mimicry (sensu Ruther and Steiner 2008). Indeed, the mating performance of young males is not superior to that of adults (Benelli et al. 2013a). However, young males could benefit indirectly from DSU production, simply by distracting mature males from females. After having reached sexual maturity, the males do not need to produce the female scent and they stop DSU biosynthesis (Benelli et al. 2013a). When olive fruit fly males become sexually mature, they start to produce (Z)-9-tricosene, a compound unique to males, which is able to selectively attract females during the close-range Fig. 2 A pair of Mediterranean fruit flies, Ceratitis capitata,in phase only (Carpita et al. 2012; Canale et al. 2013a). copula. This phase is probably affected by tactile cues (e.g. low Overall, the courtship and mating behaviour of the olive volatile cuticular hydrocarbons) perceived by both sexes, particularly by the males through leg scrubs on the female’s abdomen fruit fly differs from the above-described general sequence of Tephritidae mainly in the first phase. Indeed, in B. oleae the male starts with a mate-searching phase conspecifics of the opposite sex. In this species, Baker and aimed at locating a female, then courts her through Bacon (1985) first demonstrated that female aeration extracts acoustic signals and finally attempts copulation (Benelli attracting males are composed of several spiroacetals, et al. 2012a and references therein). including (E,E)-2,8-dimethyl-1,7-dioxaspiro[5.5]undecane, In the melon fly, both sexes produce volatile compounds (E,E)-8-ethyl-2-methyl-1,7-dioxaspiro[5.5]undecane and (E,E)- showing selective attraction towards the opposite sex. It has 8-methyl-2-propyl-1,7-dioxaspiro[5.5]undecane. Later, Nishida been observed that B. cucurbitae males produce a pheromonal et al. (1988a, b) pointed out that also the B. dorsalis males pro- substance visible as ‘smoke’ at dusk (Sugimoto 1979;Kuba duce several volatiles showing pheromonal activity towards and Sokei 1988) that evokes attraction towards virgin females females, including 2-allyl-4,5-dimethoxyphenol, 4-((E)-3-hy- (Suzuki and Koyama 1980, 1981). The pheromone contains droxyprop-1-enyl)-2-methoxyphenol and (Z)-3,4-dimethoxyc- pentacosane, heptacosane, nonacosane, the lactone (E)-5- innamyl alcohol. Lastly, Perkins et al. (1990a, b) extended the list (3,6-heptadienyl)-dihydro-2(3H)-furanone, together with a of male-borne pheromones, highlighting the presence of some large amount of trisodium phosphate and other phosphorus molecules (e.g. 2,3,5-trimethylpyrazine) that play a similar role salts (Ohinata et al. 1982). Moreover, Baker et al. (1982a, b) also in B. cucurbitae. demonstrated that excised male rectal glands are able to elicit strong responses from female melon flies, and that the volatile Singing on the wing! The role of male wing vibration constituents of male rectal gland secretions contain 2-meth- during courtship oxy-N-3-methylbutyl acetamide together with two other amides, three pyrazine derivatives and 2-ethoxybenzoic acid. Tephritid males court females through wing vibration (i.e. Baker and Bacon (1985) investigated the chemical composi- the male maintains the wings close to the abdomen, tion of aeration extracts from melon fly females, since these vibrating them rapidly in a dorso-ventral fashion and/or latter are attractive towards males, and noted that they contain rolling them on their longitudinal axes), plus stridulation a variety of 2,8-dialkyl-1,7-diaxospiro[5.5]undecanes, toge- behaviour (i.e. during wing vibration, the posterior portion ther with N-3-methylbutylacetamide. Lastly, Perkins et al. of the male wing repeatedly contacts the abdomen, rubbing (1990a, b) re-examined melon fly sexual chemoecology, and the cubital microtrichia on the abdominal pecten) (Fig. 1b– found that the major component in the rectal gland secretion of d) (Keiser et al. 1973; Benelli et al. 2012a). Wing vibration males is ethyl 4-hydroxybenzoate rather than 2-ethoxyben- and/or stridulation behaviour has been analysed in many zoic acid. However, no further information is available on the tephritid species of economic importance, including A. temporal production pattern of sex pheromones in the melon suspensa (Webb et al. 1984), B. cucurbitae (Kanmiya fly. It would be interesting to know if melon fly males are able 1988; Kanmiya et al. 1987a, b, c), B. dorsalis (Poramarcom to produce the female scent when they are young, as noted for 1988; Poramarcom and Boake 1991), B. oleae (von Rolli the olive fruit fly (Benelli et al. 2013a). 1976; Benelli et al. 2012a) and C. capitata (Bricen˜o and The oriental fruit fly is the third peculiar example of te- Eberhard 2000a, 2002; Bricen˜o et al. 2002, 2007). How- phritid in which both sexes release molecules that attract ever, in several cases it is unclear if these signals are 123 392 J Pest Sci (2014) 87:385–405 triggered by air-borne mechanical particle displacement may serve as further courtship behaviour (i.e. to placate the due to wing vibration, by stridulation or by both mecha- female), or to maintain the male’s balance while he posi- nisms (see also Benelli et al. 2012a). tions himself for copulation (Zapien et al. 1983; Bricen˜o Feron and Andriew (1962) interpreted tephritid wing et al. 1996; Benelli et al. 2012a). In addition, copulation vibration as a mating stimulus that may serve to test the outcomes are probably also affected by tactile cues (e.g. female’s willingness to copulate. In some species (e.g. A. low volatile cuticular hydrocarbons) perceived by both suspensa, B. oleae), the male’s performance of wing sexes, particularly by the male through leg scrubs on the vibration (e.g. the frequency and pulse duration) affects the female’s abdomen (Fig. 2). female’s decision during courtship (Webb et al. 1984; Lastly, tephritid wings are often marked with bands and Benelli et al. 2012a). For instance, in C. capitata it was spots. These characters are visual cues that, particularly observed that mounts by wild males that failed to copulate when sexually dimorphic, could play a role in courtship and were preceded by significantly shorter courtships than were mating sequences of several species (Burk 1981; Sivinski mounts by successful males (Bricen˜o and Eberhard 2000a). et al. 2000). This is true also for other body parts that are In B. dorsalis, females were less attracted to those males brightly coloured and/or patterned, such as eyes and legs that that spent less time performing wing vibrations, and a could have communicative functions in sexual behaviour. A male’s ability to produce continuous wing vibration signals good example is the lifting of black mid-femora marked over an extended period was important in determining with yellow tips in males of Eutreta diana (Osten Sacken) mating success (wing vibration duration in successful during courtship (Sivinski et al. 2000 and references males was from 1 to 9 min; in unsuccessful males: 30 s) therein). Visual cues may also be found in male ornaments. (Poramarcom and Boake 1991). Some features (e.g. fre- Indeed, in some tephritid species, males bear peculiar quency and pulse duration) of male wing vibrations were structures that may function as sexual signals. Examples higher before successful matings than before unsuccessful include the antlers in Phytalmia species (that also commu- ones, and when the males’ wings were removed the prob- nicate male size to foes during agonistic approaches), the ability of successful mating was strongly reduced (Benelli row of enlarged bristles on the head of Chetostoma curvi- et al. 2012a). The association between peculiar wing nerve Rondani, the forward-jutting projections on the front vibration performances and mating success appears due of Stemonocora cornuta (Scopoli), the pedicel sticking out mainly to female preference. This could allow the females like a bristled horn in Carajocera ceratocera Hendel, the to improve their reproductive success by selecting the best broadened and concave front basitarsi of Euphranta macu- male, indicated by the male that is able to produce strong lifemur (Meijere), the mid-legs ‘feathered’ with long setae wing vibrations reflective of vigour and health. on the tibia or on the tibia plus femur in some Ceratitis Wing sexual dimorphism has been detected in several species and the mass of strong yellowish bristles along the tephritids (Keiser et al. 1973; Benelli et al. 2012a). Wings fifth tergite of the abdomen in Trupanea bruneipennis Hardy are broader in males than in females for both B. oleae (see Sivinski et al. 2000 for a dedicated review). However, (Benelli et al. 2012a) and C. capitata (Bricen˜o and Eber- few studies have elucidated the exact behavioural role of hard 2000b). Wing sexual dimorphism could reflect an these visual cues in courtship and mating behaviour and adaptation for acoustic cue production (Bricen˜o and Eb- further research on this point is required. erhard 2000b). Furthermore, the enlarged posterior portion of the male’s wing may enhance the dissemination of Just vision? The peculiar mating system of the apple olfactory cues during wing vibration. For instance, B. oleae maggot fly males transfer (Z)-9-tricosene from their rectal glands to urotergal ones, through a peculiar leg-rubbing behaviour While in the majority of tephritid species courtship and (Fig. 1e–g), while performing wing vibration, thus dis- mating behaviour are guided by a combination of physical seminating pheromonal signals towards potential mates and chemical cues, in at least one species, the apple maggot (Canale et al. 2013a). Similarly, in A. suspensa and C. fly (R. pomonella), mating behaviour is triggered by visual capitata, wing vibrations are performed in connection with cues only (Prokopy and Bush 1973). Results of laboratory pheromone emission to attract females (Webb et al. 1976; and field observations revealed that the site for mating Bricen˜o et al. 1996). For some Bactrocera species, Keiser assembly of sexually mature R. pomonella is exclusively et al. (1973) speculated that males may display wing on the fruit (Prokopy et al. 1971), predominantly during the vibration as a territorial behaviour during mating. How- afternoon and at dusk (Prokopy et al. 1972). When the ever, no further evidence has been provided to validate this environmental conditions are favourable, sexually mature hypothesis. flies fly to the host fruit. Both sexes may initiate the flight. Male wing vibrations usually continue during the cop- Such flights by males are often evoked by the visual cues ulation attempt phase as well. Wing vibrations at this time from females moving on a fruit, while such flights by 123 J Pest Sci (2014) 87:385–405 393 females seem to be primarily in response to the fruit as a ones (Bricen˜o and Eberhard 1998, 2000a). Also in A. lu- potential oviposition site (Prokopy et al. 1971; Prokopy and dens, crowding in early adulthood results in lower mating Bush 1973). Once on the same fruit, a male and a female success; it has been hypothesized that the decrease in locate one another apparently primarily through vision, sexual competitiveness may result from the higher level of particularly movement. Besides vision, other chemical male–male interactions and/or to pheromone depletion, (Prokopy and Bush 1972), acoustical and tactile (Prokopy since both mechanisms may increase the chances of a and Bush 1973) cues may also be involved in the mating male’s rejection by females (Dı´az-Fleischer et al. 2009). behaviour of R. pomonella. However, no sex pheromones Among morphological factors that influence mating, have been identified in R. pomonella sexual communica- there have been contradictory results studying the role of tion (Prokopy 1975a, b; El-Sayed 2013). Most successful male body size in affecting male reproductive outcomes. copulation attempts are initiated while the female is For instance, larger A. suspensa males were more suc- engaged in some phase of oviposition behaviour. In many cessful in mating than smaller ones (Burk 1983; Burk and cases, it suggests that matings on fruit may often be forced Webb 1983), while other research noted that male size had matings with unreceptive females (Smith and Prokopy no relation to mating success in this species (Pereira et al. 1980). R. pomonella mating occurs predominantly on apple 2010a and references therein), nor in A. fraterculus (Segura fruit, and is evoked by visual stimuli. That is why red et al. 2007). For C. capitata, male mating success was sticky traps, mimicking red , are efficient in moni- shown by some to be unrelated to male size (Arita and toring and control of wild R. pomonella populations Kaneshiro 1988; Whittier et al. 1994; Whittier and (Reynolds and Prokopy 1997). Kaneshiro 1995), while other research demonstrated that larger medfly males were more successful in mating than Other factors affecting mating behaviour in tephritid flies smaller ones, in both laboratory (Churchill-Stanland et al. 1986; Taylor and Yuval 1999;Caˆmara de Aquino and The courtship and mating behavioural sequences of Joachim-Bravo 2013) and field studies (Kaspi et al. 2000; Tephritidae are affected by numerous environmental (Dı´az- Rodriguero et al. 2002). In B. oleae, larger males were Fleischer and Arredondo 2011), ecological (Leftwich et al. more successful in mating than smaller ones (Benelli, 2012), physiological (Gavriel et al. 2009; Anjos-Duarte unpublished data). Most likely, large males are able to et al. 2011;Pe´rez-Staples et al. 2012; Shelly et al. 2012) achieve greater mating success than smaller males because and morphological factors (Keiser et al. 1973; Miranda they can produce higher quality acoustic sexual signals 2000; Harwood et al. 2013). Particularly, post-teneral diet (e.g. wing vibration plus stridulation, higher volume of is crucial for male reproductive success (Drew and Yuval courtship song, shorter interpulse intervals and/or higher 2000). In several tephritid species, protein-rich diets have number of buzzes for each courtship) (Bricen˜o et al. 2002; been shown to improve male ability to copulate with Bricen˜o and Eberhard 2002; Burk and Webb 1983; Webb females (Faria et al. 2008; Pereira et al. 2012;Pe´rez-Sta- et al. 1984). This could affect the female’s behaviour ples et al. 2012). In some species (e.g. the olive fruit fly), through two distinct mechanisms. First, the male’s distance housed in their digestive tract contribute to adult from the female often varies consistently during courtship fitness in a diet-dependent fashion. For instance, if flies are and this could allow larger males (and their acoustic sexual fed on a diet containing non-essential amino acids as the signals) to be perceived by females for a greater amount of sole source of amino nitrogen, their fitness improves when time (Partridge et al. 1987). Second, particular wing bacteria are present, supporting the hypothesis that bacteria vibration characteristics from differently sized males may compensate for the skewed amino acid composition of the affect the female’s decision (Moradian and Walker 2008). fly’s diet and may be indispensable for flies that subsist However, the higher mating success rate of large males mainly on nitrogen-poor resources (e.g. honeydew and may also be due to their superior fighting ability against plant exudates) (Ben-Yosef et al. 2010 and references smaller ones (Benelli 2014), and/or their ability to over- therein). come female resistance by force when mounting them Female mate selection varies with age, and affects the (Taylor and Yuval 1999). likelihood that they will accept or reject a sterile male (Liedo et al. 2002; see also Pe´rez-Staples et al. 2012 and Tephritid parapheromones: their biological role references therein). Also, density effects due to crowded in an evolutionary perspective conditions in mass-rearing can affect male courtship per- formance and, therefore, their success in mating. For There are additional chemicals (i.e. parapheromones) that instance, lower durations of courtship, wing vibrations and can physiologically or behaviourally affect Tephritidae head rocks, and subsequent lower success in mating were communication systems, evoking a response similar to that found in mass-reared C. capitata males compared to wild of a ‘true’ pheromone (Renou and Guerrero 2000). Indeed, 123 394 J Pest Sci (2014) 87:385–405 tephritid males are strongly attracted to several phenyl enhanced mating success of males seems to be due to an propanoids (PPs), a category of compounds based on a C6– increased production of sexual signals (e.g. ME-fed males C3 skeleton which either occur naturally in plants or are spend more time in wing vibrations: Shelly and Dewire artificially synthesized as analogues of plant-borne mole- 1994) as well as increased signal attractiveness to females cules (for a recent review see Vargas et al. 2010). One of (e.g. more female visits to ME- and CL-fed males: Shelly the widely recognised compounds belonging to the PPs and Dewire 1994; Khoo and Tan 2000; Shelly 2001). category is methyl eugenol (ME), 4-allyl-1,2-dimethox- Furthermore, in several tephritid species (e.g. C. capitata), ybenzene-carboxylate, which has proved an attractant to at exposure of males to the aroma of ginger root oil (GRO), a least 91 species of Tephritidae (87 in Dacini and 4 in natural substance rich in PPs constituents, increases their Ceratitini) (El-Sayed 2013). Cue-lure (CL), 4-(p-acetoxy- mating competitiveness, both in the laboratory and field phenyl)-2-butanone has not been isolated as a natural (Shelly et al. 2004; Shelly et al. 2010;Pe´rez-Staples et al. product, but it is rapidly hydrolyzed to form 4-(p- 2012). Trimedlure (TML), t-Butyl-2-methyl-4-chlor- hydroxyphenyl)-2-butanone, also known as raspberry ocyclohexanecarboxylate, also attracts C. capitata males, ketone (RK), a natural plant constituent found in orchids, and exposure to TML increases their mating success raspberries and cranberries. CL is widely recognized as a (Shelly et al. 1996). However, C. capitata males exposed to strong male-specific lure for B. cucurbitae (Fletcher 1987). TML do not feed on TML, but simply rest in close prox- To the best of our knowledge, no tephritid species responds imity to the odour source. Although TML is widely used in to both ME and CL (Vargas et al. 2010). However, there survey and detection programs, the biological significance are other natural compounds able to attract both ME- and of the C. capitata/TML association is poorly understood CL-responding species. A good example is zingerone, a (see Shelly 2006 for a dedicated review). major component of the fruity odour of the orchid Bulbo- For a long time, no fitness benefits (e.g. increase in egg phyllum baileyi, attractive to males of several Bactrocera hatch rate, improved total fecundity and/or longevity) were species. Interestingly, B. dorsalis males feeding on B. reported for females that had mated with lure-fed males baileyi flowers sequester zingerol (a reduced form of (Shelly 2000d). Recently, however, Kumaran et al. (2013) zingerone) in the body, suggesting its role as a possible proved that B. tryoni females benefit from mating with component of sex pheromones used to attract females zingerone- and CL-fed males, producing more eggs than during courtship (Tan and Nishida 2007). females mated with unfed males. However, females mated Two main theories have been proposed to explain the with lure-fed males died sooner than females mated with biological function of male lures in dacine fruit flies: the unfed males, and their remating propensity was also ‘ancestral host hypothesis’ and the ‘sexual selection reduced (Kumaran et al. 2013). hypothesis’. The first proposed that lures originated as Vargas et al. (2010) proposed two hypotheses to explain plant kairomones serving as rendezvous stimulants to the female preference for ME-fed males. First, the female promote mating, while the second theory suggests that the preference may be a case of runaway selection, whereby the lures served as male pheromone precursors and play an presence of ME metabolites in the male signal could high- important role in affecting female choice of mates (Raghu light a greater ability to locate natural ME sources in the wild. 2004). Several lines of evidence support the sexual selec- The females that select ‘ME-scented’ males could increase tion hypothesis: (1) PPs are male-specific attractants their chances to produce offspring with a high ability to (Raghu and Clarke 2003); (2) males feed on PPs (Khoo and locate wild ME sources. The second hypothesis is that male Tan 2005); (3) after feeding, ME has been detected in the pheromone containing ME metabolites is more attractive fly’s hemolymph (Hee and Tan 2004) and in rectal gland because it mimics other key resources crucial for females, secretions (Nishida et al. 1997) and RK has been detected such as food or an oviposition substrate. In this context, ME- in rectal gland secretions (Tan and Nishida 1995); (4) ME enriched pheromone may represent a sort of ‘sensory trap’, metabolites have been detected in volatiles emitted by thus evoking a strong, pre-existing sensory bias, evolved in a males (Nishida and Fukami 1990); (5) females are attracted nonsexual framework. Overall, the adaptive basis of female to ME metabolites (Tan and Nishida 1996) and prefer the preference for lure-fed males remains poorly known and pheromone of ME-fed males over non-ME-fed males (Wee further research on possible female benefits of choosing lure- et al. 2007). fed males is strongly encouraged. Lure feeding of adult males is correlated with higher mating success, both in ME- (Shelly and Dewire 1994; Wee et al. 2007) and CL/RK-responding tephritid species After copulation: some fitness-promoting female tools (Shelly 2000b, c). In contrast, larval feeding on ME-enri- ched diet had no effect on the mating performance of newly Tephritid females have two main behavioural tools to emerged adult males (Shelly and Nishida 2004). The maintain single oviposition sites, thus increasing the 123 J Pest Sci (2014) 87:385–405 395

Table 2 An overview about the Diet Tephritid species Oviposition Reference occurrence of the oviposition marking marking behaviour in tephritid behaviour flies F Anastrepha suspensa Yes Prokopy et al. (1977) F Anastrepha sorocula Yes Simo˜es et al. (1978) F Anastrepha fraterculus Yes Prokopy et al. (1982) F Anastrepha pseudoparallela Yes Poloni and Silva (1986) F Anastrepha bistrigata Yes Selivon (1991) F Anastrepha grandis Yes Silva (1991) F Anastrepha ludens Yes Papaj and Aluja (1993), Edmunds et al. (2010) F Anastrepha striata Yes Aluja et al. (1993) F Anastrepha obliqua Yes Aluja and Dı´az-Fleischer (2006) F Anastrepha serpentina Yes Aluja and Dı´az-Fleischer (2006) F Bactrocera oleae Yes (plant-borne?) Cirio (1971), Girolami et al. (1981) F Bactrocera cucurbitae No Prokopy and Koyama (1982) F Bactrocera jarvisi No Fitt (1984) F Bactrocera tryoni No Fitt (1984) F Bactrocera dorsalis No Prokopy et al. (1989) F Ceratitis capitata Yes Prokopy et al. (1978) NF Chaetorellia australis Yes Pitarra and Katsoyannos (1990) F Rhagoletis completa Yes Cı´rio (1972) F Rhagoletis pomonella Yes Prokopy (1972) F Rhagoletis cerasi Yes Katsoyannos (1975) F Rhagoletis fausta Yes Prokopy (1975a, b) F Rhagoletis cingulata Yes Prokopy et al. (1976) F Rhagoletis cornivora Yes Prokopy et al. (1976) F Rhagoletis indifferens Yes Prokopy et al. (1976) F Yes Prokopy et al. (1976) F Rhagoletis tabellaria Yes Prokopy et al. (1976) F Rhagoletis basiola Yes Averill and Prokopy (1989) F Rhagoletis zephyria Yes Averill and Prokopy (1989) NF Rhagoletis alternata Yes Bauer (1986) F Rhagoletis suavis Occasional Papaj (1994) F frugivorous species, NF non- NF Tephritis bardanae Yes Straw (1989) frugivorous species (modified NF Terellia ruficauda Yes Lalonde and Roitberg (1992) from Silva et al. 2012) chances of their eggs developing successfully. Here, we withdrawing the after egg deposition in fruit first review evidence about the role of OMPs, both in occurs without apparent deposition of OMPs (Prokopy and frugivorous and non-frugivorous species, with particular Koyama 1982; Fitt 1984; Prokopy et al. 1989). Among reference to their potential usefulness in IPM programs. Bactrocera species, B. oleae seems to be an exception. An We then examine the role of female–female combat that unusual host-marking procedure has been noted in the olive sometimes occurs at oviposition sites. fruit fly. Following oviposition, the female uses her label- In fruit flies, the use of OMPs following oviposition is a lum to spread olive juice exudate from the oviposition crucial signal to indicate an occupied, thus sub-optimal puncture over the fruit surface and this juice appears to act resource (Edmunds et al. 2010). To the best of our as a deterrent to subsequent oviposition (Table 2) (Cirio knowledge, the occurrence of host marking behaviour has 1971; Girolami et al. 1981). However, under very crowded been detected in at least 23 frugivorous species and 4 non- conditions, this peculiar marking behaviour has little effect frugivorous species of Tephritidae (Table 2) (Silva et al. (Canale and Benelli, pers. observ.). Many tephritid species 2012 and references therein). In other tephritids, all deposit eggs in small fruits that provided a limited food belonging to the genus Bactrocera [e.g. B. cucurbitae, B. resource for their offspring. On this basis, conspecific dorsalis, B. tryoni (Froggatt) and B. jarvisi (Tryon)], females recognize OMPs and usually make oviposition

123 396 J Pest Sci (2014) 87:385–405 decisions to avoid marked sites. OMPs can exert various behaviours are not only performed between conspecifics behavioural responses in conspecific females, including (1) and in some species, the females also display wing waving, suppression of oviposition behaviour (Averill and Prokopy pouncing and boxing acts against other arthropods such as 1989), (2) disruption of oviposition (Papaj et al. 1989, co-evolved wasps [e.g. after oviposition, B. 1992), (3) emigration from highly infested areas (Roitberg dorsalis versus the egg-attacking braconid Fopius arisanus et al. 1982, 1984) and (4) reduction of the number of eggs (Sonan) (Messing, pers. comm.)], or other tephritid species laid (Papaj et al. 1989, 1990). Overall, the perception of feeding on the same host plant [e.g. Bactrocera invadens OMPs allows females to reduce competition among their Drew, Tsuruta and White versus Ceratitis cosyra (Walker) offspring, and thereby optimize fitness outcomes for their on mango (Mangifera indica L.)] (Ekesi et al. 2009). progeny (Stelinski et al. 2009; see also Silva et al. 2012 for Overall, tephritid females could benefit from displaying a dedicated review). aggressive behaviour, because it allows them to gain and Concerning the applications of OMPs, to date there have maintain single oviposition sites. Particularly for small been three outstanding cases of field application of OMPs fruits, more than one oviposition event per fruit may lead to that achieved noticeable reductions of tephritid pest dam- larval competition for resources, thus reducing larval sur- age (Silva et al. 2012). The three cases concern Anastrepha vival and growth rate (AliNiazee 1974; Debouzie 1989). On obliqua (Macquart) (e.g. 1994: field application of A. lu- this basis, female aggressive behaviour towards a conspe- dens faeces extract with OMP over Spondias purpurea L. cific could increase its fitness (see also Dukas et al. 2001). fruits reduced A. obliqua infestation; 1997: a constituent of the OMP, anastrephamide, exerted a reduction of infesta- tion of S. purpurea by 77 %) (Aluja et al. 2009), C. capi- Towards a future scenario: can knowledge about sexual tata (e.g. treatment of coffee plantations with raw signalling help in Integrated Pest Management methanolic extract of C. capitata faeces resulted in 84 % programs? reduction in medfly infestation) (Arredondo and Dı´az- Fleischer 2006) and Rhagoletis cerasi (Linnaeus) (e.g. Basic knowledge about tephritid sexual communication may application of OMP reduced R. cerasi infestation up to contribute to the development of novel control tools to be 100 % in cherry fields of different regions of Switzerland) used in IPM programs. Knowledge of sexual selection pro- (Katsoyannos and Boller 1976, 1980; Aluja and Boller cesses in the Tephritidae may be useful for successful 1992a; Boller and Hurther 1998). However, a major con- implementation of the SIT (Burk and Calkins 1983). A major cern to be taken into account during OMP applications in concern of SIT programs is the production of males with IPM programs is the risk of habituation by tephritid pests to lower mating ability than wild ones, due to mass-rearing OMPs (Cook et al. 2007; Silva et al. 2012). Indeed, it has procedures as well as to damage/stress occurring in sterili- been observed that after prolonged and continuous expo- zation, shipping and release (Pe´rez-Staples et al. 2012). Low sure to a given OMP, female flies again oviposit into OMP- mating ability of sterile males is an overarching concern in treated fruits (Aluja and Boller 1992b; Papaj and Aluja species such as tephritid flies that have complex mating 1993). To avoid this risk, Silva et al. (2012) outlined an systems due to the presence of leks and choosy females alternative strategy, suggesting that OMPs be applied in (Lance and McInnis 2005). In general, sterile males released those commercial orchards where fruit fly populations are in SIT programs are rejected by females at higher rates than not resident or present in high densities. In this way, low- wild males (Shelly and Whittier 1996; Lance et al. 2000; Lux density populations can be suppressed rapidly, and at the et al. 2002). In some cases, this is due to behavioural changes same time this program reduces the risk of habituation to in courtship and mating of sterile males (Bricen˜o and Eber- OMPs in high-density fly populations. hard 2000a; Shelly 2012), particularly to lower quality Tephritid females also fight for single oviposition sites, olfactory (Moreno et al. 1991; Kraaijeveld and Chapman displaying agonistic behaviour towards conspecifics. For 2004) and vibrational (Sharp and Webb 1977; Mankin et al. instance, in Trupanea bisetosa (Coquillett), the ovipositing 2008) sexual signals than wild ones (for a dedicated review female will not allow other females on its sunflower head, see Pe´rez-Staples et al. 2012). However, it has been dem- and fights them off with wing waving and boxing (Cavender onstrated that sterile C. capitata males have low mating and Goeden 1982; Landolt and Hendrichs 1983). Compa- success with wild females even if they successfully join rable female–female agonistic behaviour has been also natural leks and signal (i.e. perform pheromone-calling described for B. oleae (Benelli 2014) (Fig. 1h), B. dorsalis behaviour) as frequently as wild males, produce a phero- (Shelly 1999), B. tryoni (Pritchard 1969), C. capitata (Papaj monal signal as attractive to females as that produced by wild and Messing 1996; Bricen˜o et al. 1999), A. ludens (Ro- males (Shelly et al. 1994; Shelly and Whittier 1996), and win backer and Hart 1985a), P. gentilis (Headrick and Goeden same-sex aggressive interactions in a comparable proportion 1990) and R. indifferens (AliNiazee 1974). Aggressive to wild males (Shelly 2000a). 123 J Pest Sci (2014) 87:385–405 397

Several tools have been proposed to improve the mating powerful tools to improve reduced-risk detection and performance of sterile males used in SIT programs. For monitoring dispensers. Particularly, PPs co-formulated instance, pre-exposure of males to PPs, GRO and TML can with insecticides in solid matrixes [e.g. ME cones, CL help to overcome the reduction of mating competitiveness plugs, ME wafers, with 2,2-dichlorovinyl dimethyl phos- due to mass rearing procedures (Shelly et al. 2004; Shelly phate (DDVP) strips] have proven to be safer for workers, et al. 2010; McInnis et al. 2011). However, pre-release more convenient to handle and may be used in place of exposure of sterile males to PPs may complicate evaluation several individual lure and trap systems, thus reducing efforts if the reared males are subsequently less likely to be costs of large survey and detection programs (Suckling captured in PPs-baited traps (Chambers et al. 1974; Fitt et al. 2008; Vargas et al. 2008; Vargas et al. 2012; Chang 1981; Shelly 1994; Vargas et al. 2010). The mating per- et al. 2013). Similarly, MAT with a sprayable Specialized formances of sterile males can be enhanced by the appli- Pheromone and Lure Application Technology (SPLAT), in cation and/or consumption of the juvenile hormone combination with ME or CL/RK and the low-risk insecti- analogue methoprene, since it accelerates sexual matura- cide spinosad, has been proved effective for area-wide tion and, in some cases, improves male mating success suppression of fruit flies (Vargas et al. 2003; Vargas et al. (Pereira et al. 2010b; Haq et al. 2013; Teal et al. 2013). 2010). The most common MAT carriers are fibreboard Male mating ability can also be improved by adult dietary blocks, cotton wicks, Min-U-Gel and moulded filter paper protein (Haq and Hendrichs 2013), especially pre-release (Vargas et al. 2000, 2005). Usually, they are impregnated feeding on hydrolysed yeast, since it increases male sexual or treated with PPs and organophosphate insecticides performance (Faria et al. 2008) and also promotes lon- (primarily malathion and naled). On this point our next gevity (Pe´rez-Staples et al. 2007; Fanson et al. 2012). goal should be the reduction of synthetic toxicants. This Knowledge on how sexual selection works, particularly on could be achieved through (1) replacement with natural sexually selected traits (e.g. male calling performance) molecules able to exert ingestion and contact toxicity acting as indicators of male fitness, may represent a key towards tephritid pests (Pin˜ero et al. 2011; Benelli et al. tool to select fly genotypes with high reproductive success 2012c; Canale et al. 2013b; Pin˜ero et al. 2013), with little and to promote sexually selected male phenotypes through toxic effects on non-target arthropods (Benelli et al. 2013c) mass-rearing optimization, thus improving success of SIT or (2) the development of traps not requiring insecticides programs (Whittier and Kaneshiro 1995; McInnis et al. (Vargas et al. 2010). Moreover, further research is needed 2002; Rodriguero et al. 2002). In the mass-rearing phase, to define the lekking site location for individual fruit fly particular attention should be dedicated to the avoidance of species. This may help us develop recommendations for the crowded conditions, in order to minimize detrimental optimal location of dedicated traps and bait sprays. A good effects on male courtship and mating success (Bricen˜o and example is the approach to control melon fly, B. cucurbi- Eberhard 1998, 2000a;Dı´az-Fleischer et al. 2009). In tae, with bait applied to planted border crops/non-host trees addition, quality control of sterile males in the mass-rear- adjacent to the cucurbit fields (Koyama et al. 2004 and ing phase should include mating tests between the labora- references therein). tory reared and wild flies. The effect of lure feeding on subsequent responsiveness Contacts occurring among tephritid flies during sexual to the lure also has serious implications for the manage- interactions can also aid the dissemination of insecticides ment of fruit fly pests, especially Bactrocera species. MAT co-formulated with adhesive powders (e.g. spinosad programs may be hindered if males visit natural lure insecticide plus EntostatTM) used in insecticidal auto-dis- sources, thus becoming less responsive to lure-baited traps. semination control systems (Rogers et al. 2013), thus On the other hand, for B. dorsalis, it has been noted that providing a valuable alternative to the indiscriminate dis- feeding on ME-bearing flowers does not reduce subsequent tribution and quantity of the killing agent (see also Arms- capture probability. This could be due to the higher ME worth et al. 2006, 2008). content of traps than natural sources (Shelly 2000e). PPs- Sex pheromones and OMPs are key instruments against based detection and monitoring tools, as well as MAT tephritid pests. New and valuable results may be achieved programs, have very low side effects on non-target insects, through research on long-lasting controlled-release dis- such as pollinators (bees and hoverflies), natural enemies pensers for male- and female-borne pheromones that could (parasitoid wasps) and endangered endemics (e.g. Hawai- improve mass-trapping and population monitoring assays ian Drosophila spp.) (Vargas et al. 2010 and references (Gil-Ortiz 2012). This can be particularly applicable for therein). those tephritid species for which other sustainable tools Semiochemicals that influence courtship and mating have yielded few results (e.g. parasitoids of the olive fruit behaviours (e.g. sex pheromones formulated in long-lasting fly) (Daane and Johnson 2010; Benelli and Canale 2012b; dispensers) might also be used to improve IPM programs Benelli et al. 2013b). Among parapheromones, PPs are by reducing adult tephritid dispersal, longevity and/or 123 398 J Pest Sci (2014) 87:385–405 fecundity. For many mating disruption programs, mating is References not prevented, only delayed. Any additional expenditure of energy and resources by the female to locate a mate or AliNiazee MT (1974) The Western cherry fruit fly, Rhagoletis oviposition site, or increased female–female competition indifferens (Diptera: Tephritidae): 2. Aggressive behavior. Can Entomol 106:1201–1204 might lower her longevity and fecundity. For example, in Aluja M, Boller EF (1992a) Host-marking pheromone of Rhagoletis laboratory flight mill studies adult female B. oleae had a cerasi: field development of synthetic pheromone as a novel long flight period when fed, but a significantly shorter flight cherry fly management strategy. Entomol Exp Appl 65:141–147 period when provided only water or no food resource Aluja M, Boller EF (1992b) Host-marking pheromone of Rhagoletis cerasi: foraging behavior in response to synthetic pheromonal (Wang et al. 2009a). Other adult female B. oleae stressors isomers. J Chem Ecol 18:1299–1311 include high summer temperature diurnal regimes that Aluja M, Dı´az-Fleischer F (2006) Foraging behavior of Anastrepha could result in reduced adult longevity and egg production ludens, A. obliqua and A. serpentina in response to feces extracts (Wang et al. 2009b). Therefore, using semiochemicals that containing host marking pheromone. J Chem Ecol 32:367–389 Aluja M, Norrbom A (2010) Fruit flies (Tephritidae): phylogeny and result in adult females spending additional time in court- evolution of behavior. CRC Press, Boca Raton ship and mating behaviours, and/or host location, could Aluja M, Jacome I, Birke A, Lozada N, Quintero G (1993) Basic patterns reduce adult longevity, fecundity and dispersal to new host of behavior in Anastrepha striata (Diptera, Tephritidae) flies under locations. field-cage conditions. Ann Entomol Soc Am 86:776–793 Aluja M, Diaz-Fleischer F, Boller EF, Hurter J, Edmunds AJF, As a final point, we emphasize that further research is Hagmanna L et al (2009) Application of feces extracts and needed on the role of OMPs. Even if OMPs contribute to a synthetic analogues of the host marking pheromone of Anastre- noticeable reduction of damage in some species, thus pha ludens significantly reduces fruit infestation by A. obliqua in offering an eco-friendly strategy in IPM programs (Boller tropical plum and mango backyard orchards. J Econ Entomol 102:2268–2278 and Hurther 1998; Arredondo and Dı´az-Fleischer 2006; Anjos-Duarte CS, Moreira Costa A, Joachim-Bravo IS (2011) Aluja et al. 2009), their presence and role remain largely Influence of female age on variation of mate choice behavior unknown in many other tephritid pests of economic in Mediterranean fruit fly (Diptera: Tephritidae). J Insect Behav importance. The application of OMPs to reduce Tephriti- 24:11–21 Arita LH, Kaneshiro KY (1988) Body size and differential mating dae oviposition rates in IPM programs should be careful to success between males of two populations of the Mediterranean avoid antagonistic effects on parasitoid guilds. Further- fruit fly. Pac Sci 42:173–177 more, valuable synergies between OMPs and biological Arita LH, Kaneshiro KY (1989) Sexual selection and lek behavior in control tools should be taken into account. For instance, it the Mediterranean fruit fly, Ceratitis capitata (Diptera: Tephri- tidae). Pac Sci 43:135–143 has been shown that the perception of tephritid OMPs (i.e. Armsworth CG, Baxter IH, Barton LE, Poppy GM, Nansen C (2006) from R. pomonella and R. basiola) by their parasitoids [i.e. Effects of adhesive powders on the mating and flight behavior of Opius lectus Gahan (: ) and Mediterranean fruit fly (Diptera: Tephritidae). J Econ Entomol Halticoptera rosae Burks (Hymenoptera: ), 99:1194–1202 Armsworth CG, Rogers CD, Barton LE, Soares C, Poppy GM (2008) respectively] can increase the wasps’ chances of successful Uptake of adhesive powders from lure stations by Mediterranean host searching and/or can elicit wasp oviposition behaviour fruit fly (Diptera: Tephritidae). J Appl Entomol 132:45–53 (Prokopy and Webster 1978; Roitberg and Lalonde 1991; Arredondo J, Dı´az-Fleischer F (2006) Oviposition deterrents for the Hoffmeister et al. 2000; Wang and Messing 2003). Since Mediterranean fruit fly, Ceratitis capitata (Diptera: Tephritidae) from fly faeces extracts. Bull Entomol Res 96:35–42 parasitoid wasps are able to learn host-borne olfactory cues Averill AL, Prokopy RJ (1989) Host-marking pheromones. In: (Ngumbi et al. 2012) and experience on given host-borne Robinson AS, Hooper G (eds) Fruit flies: their biology, natural cues can speed-up host searching performance (Canale and enemies and control. Elsevier, Amsterdam, pp 207–219 Benelli 2012), we believe that mass-reared tephritid para- Baker R, Bacon AJ (1985) The identification of spiroacetals in the volatile secretions of two species of fruit fly (Dacus dorsalis, sitoids may be sensitised or trained on OMPs during the Dacus cucurbitae). Experientia 41:1484–1485 pre-release phase, thus improving their post-release per- Baker R, Herbert RH, Howse PE, Jones OT, Francke W, Reith W formance in the field. (1980) Identification and synthesis of the major sex pheromone of the olive fly, Dacus oleae. J Chem Soc Chem Commun 1:52–54 Acknowledgments We thank Nicolas Desneux for his kind invita- Baker R, Herbert RH, Lomer RA (1982a) Chemical components of tion to write this review and three anonymous reviewers for their the rectal gland secretions of male Dacus cucurbitae, the melon comments on an earlier version of the manuscript. We are grateful to fly. Experientia 38:232–233 Adriano Carpita and Alfio Raspi for helpful discussion about Teph- Baker R, Herbert RH, Parton AH (1982b) Isolation and synthesis of 3- ritidae chemoecology, Paolo Giannotti and Francesco Lanzo for art- and 4-hydroxy-1,7dioxaspiro[5.5]undecanes from the olive fly work, Gabriella Bonsignori and Giulia Giunti for their help during (Dacus oleae). J Chem Soc Chem Commun 1982:601–603 manuscript preparation. Giovanni Benelli is particularly grateful to Baker R, Herbert RH, Grant GG (1985) Isolation and identification of Mark G. Wright, Kenneth Kaneshiro and Luc LeBlanc for construc- the sex pheromone of the Mediterranean fruit fly, Ceratitis tive discussions on evolutionary biology and sexual communication capitata (Wied). J Chem Soc Chem Commun 1985:824–825 during a stay at the University of Hawaii at Manoa.

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