Fruit of Economic Importance: From Basic to Applied Knowledge Proceedings of the 7th International Symposium on Fruit Flies of Economic Importance 10-15 September 2006, Salvador, Brazil pp. 97-106 Effect of plant chemicals on the behavior of the Mediterranean fruit

Papadopoulos1, N. T., N. A. Kouloussis2, and B. I. Katsoyannos2

1Laboratory of Entomology and Agricultural Zoology, Department of Crop Production and Rural Environment, University of Thessaly ([email protected]) 2University of Thessaloniki, School of Agriculture, 541 24 Thessaloniki, Greece

Key Words: , , sexual behavior, chemical ecology, reproductive beha- vior

Introduction and pheromone emission begin in the pres- ence of plant volatiles, while in other cases Throughout their lives herbivores plant compounds are used as pheromone are trapped between natural enemies and precursors and thus become involved as a deep sea of foliage or fruits of variable nu- behaviour modifying chemicals indirectly. tritional value (Lawton and McNeill, 1979). There are several studies dealing with the To navigate their way through this environ- host finding behavior of tephritids (true ment have developed complicated flies, Diptera: Tephritidae), and the influence physiological and behavioral mechanisms of plant compounds on their reproductive that suit the needs of their chronological success. Among the most studied species is age and physiological requirements. These the Mediterranean fruit fly (medfy) Ceratitis mechanisms drive decision making in in- capitata (Wiedemann), one of the most no- sects and are aimed at maximizing fitness. torious pests of fruit trees. There are several Insect plant interactions have been studied studies on flies of the genusRhagoletis , Bac- extensively trying to give answers to both trocera and Anastrepha (see Robinson and proximate and ultimate questions. Process- Hooper, 1989, and references therein) as ing of visual, chemical and mechanosen- well. Tephritids use both visual and chemi- sory environmental information guide in- cal signals to locate and access habitat, sects to locate host plants, and then feed adult food, oviposition sites and mating re- and oviposit, through a series of steps that sources. Plant chemical cues play a crucial are neatly described by Schoonhoven et al. role in mediating host finding and ovipo- (2005). Besides host finding, feeding and sition (Fletcher and Prokopy, 1991). Soon oviposition, plant chemicals may also influ- after attaining adulthood both males and ence developmental rates and the progress females need to locate food rich in proteins of maturation (both leading to reproductive and carbohydrates. The availability, quality success) since they define the nutritional and quantity of adult food has significant value of the consumed host. Also, in several effect on the ovarian maturation and egg insect species volatiles influence mating development (Carey et al., 1998; Carey et behavior. In some cases sexual signaling al., 2002) but also on the reproductive suc- cess of males (Blay and Yuval, 1997; Field Corresponding author: and Yuval, 1999; Kaspi et al., 2000; Papado- Papadopoulos1 poulos et al., 1998; Shelly et al., 2002a; Yu-

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val et al., 2002). Therefore, both sexes share preference and select the odor emanating the same nutritional interests and may use from host fruits (Jang, 1995). Male accessory similar cues to locate habitats bearing high gland fluids contain compounds responsi- quality food. Sources of food can be locat- ble for the noted change of behavior. Virgin ed on host plants in the form of fruit juice, females injected with male accessory gland and other plant exudates, but also on other fluids switched odor preference likewise to niches such as bird droppings. Neverthe- mated ones. less, the interests of the two sexes might di- Host plant stimuli may substantially influ- verge later in their lives. After attaining ma- ence the physiology of medflies. In other turity and becoming mated, females search fruit flies the physical properties of artificial for suitable oviposition sites, while sexually oviposition devices influence ovarian matu- mature males search for receptive females. ration and egg development (Lachmann At this point in their lives males and females and Papaj, 2001). The presence of chemical employ different cues to maximize fitness. and visual properties of olive fruits affect This results in temporal differences in the egg maturity and oviposition in the olive spatial distribution of the two sexes (Papa- fruit fly Bactrocera oleae (Rossi) (Girolami et dopoulos et al., 2003). As insects age, their al., 1982). Females reabsorb eggs when no response to cues may shift, but this requires such stimuli are available, and they resume further study. egg maturation when fruits reappear. In fruit This paper reviews current information on flies of the genus Anastrepha host odor and the relation between plant chemicals and male pheromone have a significant effect the Mediterranean fruit fly. It addresses the on ovarian development (Aluja et al., 2001). influence of age and adult physiology on The effect of chemical properties of the host the response of medflies to plant chemicals plants, and especially that of fruits, on the and the effect of plant chemicals on med- ovarian dynamics of female medflies is not fly behavior during host finding, mating yet well studied. Preliminary laboratory ob- and oviposition. It also addresses the issue servations indicate a neutral influence of cit- of how plant chemicals may influence the rus odors on ovarian maturation in medflies dispersion patterns and spatial distribution (Ioannou, 2005). of the fly. The effect of aging on the response to plant chemicals remains largely unknown. Differ- ences in response to synthetic attractants of Adult Age and Physiology medfly adults of four different age classes have been discovered. In a field cage study The response to plant cues may vary with the male and female medflies older than 30 physiological condition and age of individual days exhibited reduced responsiveness to insects. Aging may bring about physiological the synthetic compounds of ammonium changes or result in senescent sensory sys- acetate and trimethylamine (BioLure, Or- tems and reduced responsiveness to specific egon) compared to younger flies (N. Kou- stimuli. Major physiological alterations take loussis, N. Papadopoulos and B. Katsoyannos place during reproductive maturation and unpublished). Whether old age attenuates mating. An example of this would be olfac- response to natural plant chemicals simi- tory mediated behaviors of female C. capitata larly with younger flies remains to be inves- after they have mated. Virgin females choose tigated. Studies addressing the behavioral the odor of male pheromone over the odor of adjustments of the older individuals may host fruits; however, after mating they switch shed important light on the role of older in-

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dividuals in nature and provide basic infor- fruit surface. After finding a suitable location mation on aging dynamics of fruit flies and the female uses her ovipositor to lay a group other . of eggs in a perforated cavity. As suggested by Levinson et al. (2003) medfly oviposition is favored by high fruit humidity Host finding and appropriate tactile and optical stimuli, while the odor of fruits plays a secondary role. Visual and chemical stimuli emitted from Though odors from small amounts of orange host plants direct fruit flies to host trees peel oil did not affect oviposition, higher dos- (Katsoyannos, 1989a; Katsoyannos, 1989b). es of orange oil had deterrent effects. Electro- Adult medflies respond to plant derived ol- physiological studies showed that olfactory factory cues and use them to orient towards sensilla on medfly antennae are sensitive to host trees. The distance over which visual orange oils (Hernandez et al., 1996). Under or plant odor stimuli are first detected and natural conditions this sensitivity may mani- elicit a response remains largely unknown fest itself as avoidance by females to lay eggs (Prokopy and Roitberg, 1989). The only doc- on fruits loaded with citrus peel oils. High umented case of attraction were females of doses of citrus oils have toxic allelopathic pomonella that have been shown effects on immature medlies. Therefore, fe- to respond to fruit odor emitted from a dis- males might use the odor from citrus peel as tance of approximately 20 m (Fletcher and a signal to avoid oviposition where offspring Prokopy, 1991). Upon landing on a host tree, survival may be low. However, essential oils the shape, size, and color of the fruits and are not the only odors emitted from mature other visual properties attract female med- fruits and it seems that other chemicals en- flies to fruits suitable for oviposition. Fruit courage oviposition. Guava juice has been density may also play a role. Physical prop- used as oviposition stimulant and prefer- erties of the fruit surface, gustatory and/or ential oviposition on ripe coffee berries has short range olfactory stimuli influence deci- been reported (McInnis, 1989; Vargas et al., sion to accept or reject the specific fruit. The 1995). Jang et al. (1994) reported intensive insect will oviposit or depart respectively. egg-laying in hollow plastic spheres perfo- rated with holes emanating odor from host fruits. Oviposition The extent fruit odors influence the ovipo- sition behavior of medflies became clearer Mature mated medfly females search for from studies utilizing citrus odors. Peel and ripening or ripe fruits for oviposition. Upon pulp odors differ substantially in many landing on a fruit that is suitable for oviposi- fruits, even though some of the compounds tion, a gravid female engages in a series of that constitute them are the same. In citrus steps that define preoviposition behavior fruits, essential oils account for the peel odor, (Levinson et al., 2003). This behavior involves whereas the odor of the pulp comes from examination of the fruit with her proboscis, other compounds. In a field cage study, fe- tarsi, and probably olfactory sensilla. This male medflies did not respond to the odor of process is performed to assess suitability orange peel oil, but responded to the odor of and the possible presence of host marking juice from the pulp; males responded to both pheromone deposited by other females. orange oil and to pulp odors (Katsoyannos et She then locates a suitable spot to oviposit, al., 1997). Both sexes search for food, so pulp preferably a depressed or injured site on the chemicals may direct them to feeding sites.

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However, gravid females might also use pulp Sexual behavior odor to locate oviposition sites. It is well documented that females exploit natural Medfly males form loose aggregations or artificial peel-penetrating fruit wounds termed leks, usually on host plant leaves, to lay their eggs (Papaj et al., 1989). There- performing sexual signaling by emitting a fore, females may be able to discriminate sexual pheromone and defending territo- between odors from the peel and odors ries (Prokopy and Hendrichs, 1979; Yuval and from the pulp and use them appropriately Hendrichs, 2000). Receptive females visit leks to maximize fitness. High concentrations and choose mates following a process that is of citrus oils might indicate an oviposition not well understood. Males are likely evaluat- site with deleterious properties that would ed and selected as mates on the basis of their result in reduced hatchability of eggs, en- physical characteristics and their courtship hanced mortality of early instar larvae, or performance. Overall male mating success suppression of larval growth (Katsoyannos relies on the ability to establish or join leks, et al., 1997). Conversely, juice volatiles might perform sexual signaling, convince courtship, indicate a highly suitable oviposition site and finally mate and transfer sperm. that would enhance egg hatch and larval Males of C. capitata and other Tephritidae performance. Other workers have reported display a strong attraction for certain plant- juice odors to either increase medfly ovipo- derived substances, such as the essential oils sition (Jang and Light, 1996; McInnis, 1989) contained in the peel of citrus fruits and the or to be neutral (Stark et al., 1991). Recent root of ginger, as well as for certain laborato- laboratory studies that addressed this phe- ry synthesized chemicals, such as trimedlure. nomenon showed that females ovipositing A well studied plant substance is α-copaene, in response to citrus juices are induced to a sesquiterpene hydrocarbon that is found start reproduction at a younger age, remain in a wide range of medfly hosts and in the oviposition-active for a longer proportion of above mentioned oils (Nishida et al., 2000). their lives, and lay more eggs than females Males are attracted to α-copaene from a long ovipositing in response to water (Ioannou, distance and select treated over untreated 2005, N. Kouloussis, B. Katsoyannos, N. Papa- leaves. It has been suggested that α-copaene dopoulos, unpublished data). triggers lek establishment by functioning as Another group of compounds that affects an aggregating stimulus for males (Nishida oviposition of medfly females and other te- et al., 2000). In the same study Nishida et al. phritids is referred to as “green leaf volatiles” showed a short range attraction of female (Jang and Light, 1996). This group comprises medflies to α-copaene sources and reported six-carbon aliphatic aldehydes and alcohols “abnormal” female behaviors. In a field cage and forms the main odor emitted from green study, males, not female medflies, were at- leaves and unripe fruits. Green leaf volatiles tracted to the odor of essential oils emanat- repel medflies from landing on objects ema- ing from peel wounds on oranges (Katsoyan- nating this odor and also deter oviposition. nos et al., 1997). Shelly and Villalobos (2004) Green leaf volatiles provide a cue of poor reported tight aggregations of males on the larval food and may assist females in mak- trunk and branches of specific guava trees ing wiser choices of oviposition sites, thus where natural α-copaene occured. Males in contributing to increased offspring survival. both studies appeared to feed on the odor Other volatiles that deter gravid females source on orange peel wounds or on the bark from oviposition are emitted from ferment- of guava (Katsoyannos et al., 1997; Shelly and ing fruits (Jang and Light, 1996). Villalobos, 2004).

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Convincing explanations for this affinity or because they emit distinctive close-range between C. capitata males and certain host- olfactory cues (Papadopoulos et al., 2006). derived substances has only recently been The physiological mechanisms underlying provided. Over the past few years a wealth the function of the above two plant chemi- of information have been gathered on the cals have only recently been studied. It has effect of orange peel oil and ginger root oil been hypothesized that (a) males ingest on C. capitata males. Exposure to these oils the responsible chemicals to use them in confers to males a significant mating advan- pheromone biosynthesis, thereby produc- tage over non exposed males (Papadopou- ing pheromone of higher quality; (b) males los et al., 2006; Papadopoulos et al., 2001; perceive volatile chemicals olfactorily from Shelly, 2001; Shelly and McInnis, 2001; Shelly some distance and this triggers production and Kennelly, 2004). Exposure of males to of pheromone of higher quality; (c) volatiles natural sources of α-copaene or/and other from the above two compounds aromatize compounds, emmited by wounded oranges males by interacting with cuticular odor, thus or guava bark, increase mating competitive- rendering these males more attractive to fe- ness as well. The behavioral and physiologi- males. However, topical application of orange cal mechanisms underlying these phenom- or ginger root oil on the wings of males had ena have not been fully elucidated. Both a negligible effect on their mating perfor- orange oil and ginger root oil increase male mance (Papadopoulos et al., 2006). sexual signaling (Papadopoulos et al., 2006; Shelly, 2001), and high signalers mate at higher rates (Shelly, 2000). Part of the expla- Spatial distribution nation may, therefore, rely on the elevated signaling activity of exposed males. Never- The ecological factors selecting for particular theless, the above two oils might also func- spatial patterns rest on the spatiotemporal tion in other ways. In wind tunnel experi- pattern in the distribution of food resources, ments females tended to become arrested climate and probably other critical param- more on objects emitting pheromone from eters (Koenig, 1999). Plant sources and plant males previously exposed to orange oil chemicals are distributed in patches, and than to objects emitting pheromone from there is also a temporal availability of the re- non exposed males. However, in the same spective chemicals. As we discussed above, experimental set up the pheromone emit- plant chemicals affect host finding, oviposi- ted from males exposed to ginger root oil tion, habitat selection and mating behavior did not have such an effect (Papadopoulos of medflies which might affect their tempo- et al., 2006). Female arrestment might pro- ral and spatial distribution. Therefore, adult vide males exposed to orange oil with ex- medflies in specific times of the season will tra courting time and increase their mating be distributed in patches as a result of their probabilities, whereas ginger root oil might response to above plant compounds (Nestel act differently. Video recording of pre-copu- et al., 2004; Papadopoulos et al., 2003). Spatial lation behavior of males exposed to ginger distribution might differ between the two root oil showed that females accept more sexes because of the different ecological and readily males exposed to ginger root oil behavioral needs. In a recent field study that over unexposed males (Briceno et al., 2005). examined the temporal and spatial distribu- These males may be successful in mating tion of medflies in a mixed deciduous fruit or- because they display one or more courtship chard in northern Greece (Papadopoulos et elements in a distinctive form or rate and/ al., 2003), it was found that females exhibit ag-

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Summary diagram

Behavioral responses Medfly physiology and other Plant chemicals elicit to plant chemicals Effects on ecological factors affect responses Medfly behaviors in direct influence parameters to plant chemicals and indirect ways medfly ecology

Mating Volatiles Habitat location Dispersion

Host finding Aging Non volatile chemicals effects Direct Feeding Spatial Distribution Sexual behavior Sex to responses Other factors Nutritional Oviposition and non (host acceptance, oviposition stimulation) nutritional Population Dynamics Qualitative and quantitative effects on effects quantitative and Qualitative compounds Indirect effects (Maturity-Fecundity)

figure 1. Summary diagram of the complex interactions of plant chemicals with medfly behaviors including those factors Fig.affecting 1. Summary the response diagram of medfly of tothe plant complex chemicals interactionsand the ecological of consequencesplant chemicals of these with responses. medfly behaviors includ- ing those factors affecting the response of medfly to plant chemicals and the ecological consequences of these responses.

gregated distributions that are tightly relat- tion may affect female distribution via at- ed to host fruit availability and maturity, and traction to male sex pheromone. Therefore, that low populations tend to be more clus- plant chemicals might directly affect male tered than high populations. Males exhibit spacing and indirectly female spatial distri- aggregated distributions that are not closely bution (Shelly and Villalobos, 2004). Figure related to host fruit maturity and availability, 1 summarizes the complex interactions of and are different from those of females in plant chemicals with medfly behaviors and specific times of the season. A dramatic in- the resulting ecological consequences. crease of the population size, and exhaustion of fruit resources at the end of fruiting season, results in random distribution indicating a Practical implications and dispersion drive. The spatio-temporal disper- Conclusions sion pattern of the medfly populations in an orchard is a dynamic process that might also The successful application of the Sterile In- reflect the individual fly foraging behavior. sect Technique (SIT) for the control of the Essential resources for adults constitute adult Mediterranean fruit fly and other fruit flies food, mating sites, mating partners, oviposi- hinges on the quality of the released males tion sites, and refugia (Prokopy et al., 1994). that has to be comparable with that of wild Differences between the two sexes reflect males. Sterile males should exhibit a battery the differential use and need for resources. of qualities such as adequate mobility and On the other hand, male spatial distribution survival, ability for habitat orientation, mat- might be affected by the patchy availability ing compatibility with wild females, and a of plant chemicals, which may vary between capacity to compete successfully with wild and within plant species and male distribu- males (Katsoyannos et al., 1999a). The im-

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portance of specific host trees for the sexual method relies on collecting wild females from behavior of medflies has been documented. the field using female specific traps, keeping In field studies, most of the leks were estab- them individually, and having them lay eggs lished on fruiting Citrus trees and most mat- in artificial oviposition devices (Katsoyannos ings were observed in the foliage of these et al., 1999b). The use of host juice or other trees (Hendrichs et al., 1991; Prokopy and host fruit chemicals that stimulate oviposi- Hendrichs, 1979). Therefore, to be competi- tion promotes quick adaptation to artificial tive sterilized released males need to be re- oviposition devices and could save time and sponsive to plant odors that would drive labor while providing important data for the them to specific trees to ensure mating suc- fertility of the captured females that is direct- cess and survival. Host location and response ly related to the success of a SIT Program. to plant chemicals should be included to the The mating-enhancing properties of orange routine quality control tests for mass-reared peel oil and ginger root oil (Papadopoulos sterilized males. In field cage tests conducted et al., 2006; Papadopoulos et al., 2001; Shelly, in a green house mass-reared males of the 2001; Shelly and Kennelly, 2004) could be put genetic sexing strain Vienna-42 performed into use to increase mating success of the sexual signaling and mating on Citrus trees sterilized flies in Sterile Insect Release Pro- and not on other plants (Katsoyannos et al., grams. The exposure of sterile males to gin- 1999a). Also, in field cage tests conducted ger root oil has been implemented recently in a citrus orchard sterile males of the same with success. Sterilized, mass reared males strain responded similarly to wild males to were exposed to ginger oil and acquired a odor emanating from several citrus fruits mating advantage over wild non exposed that were wounded on the peel. The above males (Shelly and McInnis, 2001; Shelly et al., findings showed that mass-reared males that 2004; Shelly et al., 2002b; Shelly et al., 2003). had been held in the laboratory for more that Exposure to ginger root oil not only increases 150 generations and had undergone artificial the efficacy of the SIT programs but may also selection, still maintained a clear preference result in substantial decrease of the cost of for citrus foliage and volatiles. these programs. Exposure to ginger root oil Host fruit chemicals reduce preoviposition increases mating competitiveness; therefore, period and increase oviposition rates (Ioan- lower numbers of males need to be released nou 2005). Wild flies accept artificial oviposi- to achieve the same result (Barry et al., 2003). tion devices easier when host fruit chemicals Here we attempted to present a review of are present to stimulate oviposition. Therefore the recent advances on the influence of plant fruit chemicals could be used to (a) increase chemicals on the behavior of the Mediter- production in laboratory rearing of medflies, ranean fruit fly and to highlight the practi- (b) increase production in mass rearing facili- cal implications of the acquired knowledge. ties, and most importantly, (c) avoid bottle- Before concluding we should point out that neck effects during new introductions of wild despite the progress made in understand- strains to laboratory conditions. ing the complex interactions between plants Host fruit chemicals could be also used to and the Mediterranean fruit fly behavior, assess the fertility of wild females in Sterile there are still plenty of challenging questions Insect Release Programs (Katsoyannos et al., to answer. For example it would be very inter- 1999b; McInnis, 1989). So far this has been esting to chemically identify the exact com- done with indirect labor intensive methods, pounds responsible for attracting medflies such as with sampling of wild hosts and ex- or eliciting various responses. Such chemicals amining them for medfly eggs. An alternative could be used to develop more powerful at-

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tractants for monitoring and managing the Carey, J.R., P. Liedo, H.G. Muller, J.L. Wang, and J.W. Vau- medfly, as has been attempted for the con- pel. 1998. Dual modes of aging in Mediterranean trol of the maggot fly using fruit blends fruit fly females. Science 281:996-998. Carey, J.R., P. Liedo, L. Harshman, X. Liu, H.G. Muller, and other attractants (Prokopy et al., 2001; L. Partridge, and J.L. Wang. 2002. Food pulses in- Reynolds et al., 1998; Rull and Prokopy, 2001). crease longevity and induce cyclical egg produc- Basic research aimed at investigating the tion in Mediterranean fruit flies. Functional Ecology evolutionary mechanisms and the response 16:313-325. of medflies to chemicals should also be con- Field, S.A., and B. Yuval. 1999. Nutritional status affects copula duration in the Mediterranean fruit fly, Cera- ducted (Papadopoulos et al., 2006). It would titis capitata (Insecta Tephritidae). Ethology Ecology also be challenging to know the function of & Evolution 11:61-70. these compounds within the plants produc- Fletcher, B.S., and R.J. Prokopy. 1991. Host location and ing them. Alpha copaene, for example, might oviposition in tephritid fruit flies, p. 140-171, In W. serve a defensive role against plant herbi- J. Bailey and J. Ridsdill-Smith, eds. Reproductive Be- vores by attracting predators (Shelly and Vil- haviour of Insects. Chapmann & Hall. Girolami, V., A. Strapazzon, and P.F.D. Gerloni. 1982. In- lalobos, 2004), but this has not been proven. sect/plant repationships in olive flies: General as- Plant compounds that are ingested by te- pects and new findings, p. 258-267, In R. Cavalloro, phritids of the genus Bactrocera increase ed. Fruit Flies of Economic Importance. Balkema/ male mating success but also confer to these Roterdam, Athens, Greece. species partial defense against herbivores Hendrichs, J., B.I. Katsoyannos, D.R. Papaj, and R.J. Proko- py. 1991. Sex-differences in movement between (Tan and Nishida, 1998). They also attract pol- natural feeding and mating sites and tradeoffs linators to plants serving as synomones that between food consumption, mating success and directly benefit both the plant and the fruit predator evasion in Mediterranean fruit flies (Dip- fly (Tan and Nishida, 2000). The investigation tera, Tephritidae). Oecologia 86:223-231. of other roles that plant compounds involved Hernandez, M.M., I. Sanz, M. Adelantado, S. Ballach, and with the behavior of the medfly might play is E. Primo. 1996. Electroantennogram activity from antennae of Ceratitis capitata (Wied) to fresh or- definitely a worthy subject. ange airborne volatiles. Journal of Chemical Ecol- ogy 22:1607-1619. Ioannou, C.S. 2005. Effect of olfactory compounds from References Cited oranges on the oviposition and other biological pa- rameters of the Mediterranean fruit flyCeratitis cap- itata (Diptera: Tephritidae). Masters, Aristotle Uni- Aluja, A., F. Diaz-Fleischer, D.R. Papaj, G. Lagunes, and J. versity of Thessaloniki, Thessaloniki, Greece, Master Sivinski. 2001. Effects of age, diet, female density, Thesis (in Greek with English summary). and the host resource on egg load in Anastrepha Jang, E.B. 1995. Effects of mating and accessory gland ludens and Anastrepha obliqua (Diptera : Tephriti- injections on olfactory mediated behavior in the fe- dae). Journal of Insect Physiology 47:975-988. maleMediterranean fruit fly, Ceratitis capitata. Jour- Barry, J.D., T.E. Shelly, D.O. McInnis, and J.G. Morse. 2003. nal of Insect Physiology 41:705-710. Potential for reducing overflooding ratios of ster- Jang, E.B., and D.M. Light. 1996. Olfactory semiochemi- ile Mediterranean fruit flies (Diptera : Tephritidae) cals of Tephritids, p. 73-89, In E. B. McPheron and G. with the use of ginger root oil. Florida Entomologist J. Steck, eds. Fruit Fly Pests: A World Assessment of 86:29-33. their Biology and Management. St. Lucie Press. Blay, S., and B. Yuval. 1997. Nutritional correlates of re- Jang, E.B., D.M. Light, R.G. Binder, R.A. Flath, and L.A. productive success of male Mediterranean fruit flies Carvalho. 1994. Attraction of female Mediterranean (Diptera: Tephritidae). Behaviour 54:59-66. fruit flies to the 5 major components of male pro- Briceno, R.D., W.G. Eberhard, and T.E. Shelly. 2005. Male duced pheromone in a laboratory flight tunnel. courtship behavior in medflies that have received Journal of Chemical Ecology 20:9-20. aromatherapy (Diptera: Tephritidae: Ceratitis capi- Kaspi, R., P.W. Taylor, and B. Yuval. 2000. Diet and size tata). Florida Entomologist (in press). influence sexual advertisement and copulatory

Book Fruit Flies.indb 104 28/10/2008 08:26:49 105 From Basic to Applied Knowledge Plant chemicals and Ceratitis capitata behavior

success of males in Mediterranean fruit fly leks. Nishida, R., T.E. Shelly, T.S. Whittier, and K.Y. Kaneshi- Ecological Entomology 25:279-284. ro. 2000. alpha-copaene, a potential rendezvous Katsoyannos, B.I. 1989a. Response to shape, size and cue for the mediterranean fruit fly, Ceratitis capi- color, p. 307-324, In A. S. Robinson and G. Hooper, tata? Journal of Chemical Ecology 26:87-100. eds. World Crop Pests, Vol. 3a. Elsevier, Amster- Papadopoulos, N., T. Shelly, N. Niyazi, and E. Jang. dam, The Netherlands. 2006. Olfactory and Behavioral Mechanisms Katsoyannos, B.I. 1989b. Field responses of Medi- Underlying Enhanced Mating Competitiveness terranean fruit flies to spheres of different color Following Exposure to Ginger Root Oil and Or- patterns and to yellow crossed panels, p. 393- ange Oil in Males of the Mediterranean Fruit Fly, 400, In R. Cavalloro, ed. Fruit flies of economic Ceratitis capitata (Diptera: Tephritidae). Journal of importance 87. A.A. Balkema, Rome, Italy. Insect Behavior:1-16. Katsoyannos, B.I., N.A. Kouloussis, and N.T. Papa- Papadopoulos, N.T., B.I. Katsoyannos, and J.R. Carey. dopoulos. 1997. Response of Ceratitis capitata 1998. Temporal changes in the composition to citrus chemicals under semi- natural condi- of the overwintering larval population of the tions. Entomologia Experimentalis Et Applicata Mediterranean fruit fly (Diptera : Tephritidae) in 82:181-188. northern Greece. Annals of the Entomological Katsoyannos, B.I., N.T. Papadopoulos, J. Hendrichs, Society of America 91:430-434. and V. Wornoayporn. 1999a. Comparative re- Papadopoulos, N.T., B.I. Katsoyannos, and D. Nes- sponse to citrus foliage and citrus fruit odour tel. 2003. Spatial autocorrelation analysis of a by wild and mass-reared sterile Mediterranean Ceratitis capitata (Diptera : Tephritidae) adult fruit fly males of a genetic sexing strain. Journal population in a mixed deciduous fruit orchard of Applied Entomology 123:139-143. in northern Greece. Environmental Entomology Katsoyannos, B.I., N.T. Papadopoulos, N.A. Koulous- 32:319-326. sis, R. Heath, and J. Hendrichs. 1999b. Method of Papadopoulos, N.T., B.I. Katsoyannos, N.A. Koulous- assessing the fertility of wild Ceratitis capitata sis, and J. Hendrichs. 2001. Effect of orange peel (Diptera: Tephritidae) females for use in ster- substances on mating competitiveness of male ile insect technique programs. J econ entomol Ceratitis capitata. Entomologia Experimentalis et 92:590-597. Applicata 99:253-261. Koenig, W.D. 1999. Spatial autocorrelation of eco- Papaj, D.R., B.I. Katsoyannos, and J. Hendrichs. 1989. logical phenomena. Trends in Ecology and Evo- Use of fruit wounds in oviposition by Mediter- lution 14:22-26. ranean fruit flies. Entomologia Experimentalis et Lachmann, A.D., and D.R. Papaj. 2001. Effect of host Applicata 53:203-209. stimuli on ovariole development in the walnut Prokopy, R.J., and J. Hendrichs. 1979. Mating behav- fly, Rhagoletis juglandis (Diptera, Tephritidae). ior of Ceratitis capitata (Diptera, Tephritidae) on Physiological Entomology 26:38-48. a field caged host tree. Annals of the Entomo- Lawton, J.H., and S. McNeill. 1979. Between the devil logical Society of America 72:642-648. and the deep blue sea: on the problems of being Prokopy, R.J., and B.D. Roitberg. 1989. Fruit fly forag- a herbivore, p. 223 - 244, In R. M. Anderson, et al., ing behavior, p. 293-306, In A. S. Robinson and G. eds. Population dynamics. Blackwell, Oxford. Hooper, eds. World Crop Pests, Vol. 3A. Elsevier, Levinson, H., A. Levinson, and E. Osterried. 2003. Amsterdam, The Netherlands. Orange-derived stimuli regulating oviposition Prokopy, R.J., S.E. Wright, J.L. Black, and J. Rull. 2001. in the Mediterranean fruit fly. Journal of Applied Size of orchard trees as a factor affecting be- Entomology 127:269-275. havioural control of apple maggot flies (Dipt, McInnis, D.O. 1989. Artificial oviposition spheres for Tephritidae) by traps. Journal of Applied Ento- Mediterranean Fruit Flies (Diptera, Tephritidae) mology 125:371-375. in field cages. Journal of Economic Entomology Prokopy, R.J., S.S. Cooley, J.J. Prokopy, Q. Quan, and 82:1382-1385. J.P. Buonaccorsi. 1994. Interactive effects of re- Nestel, D., B. Katsoyannos, E. Nemni-Lavy, Z. Mendel, source abundance and state of adults on resi- and N.T. Papadopoulos. 2004. Spatial analysis dence of apple maggot (Diptera, Tephritidae) of medfly populations in heterogeneous land- flies in host tree patches. Environmental Ento- scapes, p. 35-43, In B. Barnes, ed. 6th International mology 23:304-315. Symposium on Fruit Flies of Economic Impor- Reynolds, A.H., A.M. Kaknes, and R.J. Prokopy. 1998. tance, Stellenbosch, South Africa. Evaluation of two trap deployment methods to

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manage the apple maggot fly (Dipt., Tephritidae). ginger root oil in prerelease storage boxes dis- Journal of Applied Entomology 122:255-258. play increased mating competitiveness in field- Robinson, A.S., and G. Hooper. 1989. Fruit Flies their cage trials. Journal of Economic Entomology Biology, Natural Enemies and Control Elsevier, 97:846-853. Amsterdam. Shelly, T.E., A.S. Robinson, C. Careres, V. Wornoayporn, Rull, J., and R.J. Prokopy. 2001. Effect of apple-or- and A. Islam. 2002b. Exposure to ginger oil en- chard structure on interception of Rhagoletis hance mating success of male Mediterranean pomonella (Diptera : Tephritidae) flies by odor- fruit flies (Diptera: Tepritidae) from a genetic sex- baited traps. Canadian Entomologist 133:355- ing strain. Florida Entomologist 85:440-445. 363. Shelly, T.E., P. Rendon, E. Hernandez, S. Salgado, D. Schoonhoven, L.M., J.J.A. van Loon, and M. Dicke. McInnis, E. Villalobos, and P. Liedo. 2003. Effects 2005. Insect - Plant Biology. 2nd ed. Oxford Uni- of diet, ginger root oil, and elevation on the mat- versity Press, Oxford. ing competitiveness of male Mediterranean fruit Shelly, T.E. 2000. Male signalling and lek attractive- flies (Diptera : Tephritidae) from a mass-reared, ness in the Mediterranean fruit fly. Animal Be- genetic sexing strain in Guatemala. Journal of haviour 60:245-251. Economic Entomology 96:1132-1141. Shelly, T.E. 2001. Exposure to alpha-copaene and Stark, J.D., R.I. Vargas, and R.K. Thalman. 1991. Di- alpha-copaene-containing oils enhances mat- versity and Abundance of Oriental Fruit-Fly ing success of male Mediterranean fruit flies Parasitoids (Hymenoptera, ) in Guava (Diptera : Tephritidae). Annals of the Entomo- Orchards in Kauai, Hawaii. Journal of Economic logical Society of America 94:497-502. Entomology 84:1460-1467. Shelly, T.E., and D.O. McInnis. 2001. Exposure to gin- Tan, K.H., and R. Nishida. 1998. Ecological signifi- ger oil enchance mating success of irradiated, cance of male attractant in the defence and mass-reared males of Mediterranean fruit fly mating strategies of the fruit fly, Bactrocera pa- (Diptera: Tepritidae). Journal of Economic Ento- pyae. Entomologia Experimentalis et Applicata mology 94:1413-1418. 89:155-158. Shelly, T.E., and E.M. Villalobos. 2004. Host plant Tan, K.H., and R. Nishida. 2000. Mutual reproductive influence on the mating success of male Medi- benefits between a wild orchid, Bulbophyllum terranean fruit flies: variable effects within and patens, and Bactrocera fruit flies via a floral syn- between individual plants. Animal Behaviour omone. Journal of Chemical Ecology 26:533-546. 68:417-426. Vargas, R.I., W.A. Walsh, and T. Nishida. 1995. Coloniza- Shelly, T.E., and S. Kennelly. 2004. Exposure to or- tion of Newly Planted Coffee Fields - Dominance ange (Citrus sinensis L.) trees, fruit, and oil en- of Mediterranean Fruit-Fly Over Oriental Fruit-Fly hance mating success of male Mediterranean (Diptera, Tephritidae). Journal of Economic Ento- fruit flies (Ceratitis capitata [Wiedemann]). mology 88:620-627. Journal of Insect Behavior 17:303 - 315. Yuval, B., and J. Hendrichs. 2000. Behavior of flies in Shelly, T.E., S.S. Kennelly, and D.O. McInnis. 2002a. the genus Ceratitis (Dacinae: Ceratitidini). p. 429- Effect of adult diet on signaling activity, mate 457, In M. Aluja and A. Norrbom, eds. Fruit Flies attraction, and mating success in male mediter- (Tephritidae): Phylogeny and Evolution of Behav- ranean fruit flies (Diptera : Tephritidae). Florida ior. CRC Press, Boca Raton, Florida, USA. Entomologist 85:150-155. Yuval, B., R. Kaspi, S.A. Field, S. Blay, and P. Taylor. 2002. Shelly, T.E., D.O. McInnis, E. Pahio, and J. Edu. 2004. Effects of post-teneral nutrition on reproductive Aromatherapy in the Mediterranean fruit fly success of male mediterranean fruit flies (Diptera: (Diptera: Tephritidae): Sterile males exposed to Tephritidae). Florida Entomologist 85:165-170.

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