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Scented Males and Choosy Females: Does Male Odor Influence Female Mate Choice in the Mediterranean Fruit Fly?

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Abstract

The Mediterranean fruit fly, Ceratitis capitata (Wiedemann), displays a lek mating system characterized by a high level of female discrimination among potential mates. The basis of female choice is not understood, but recent studies indicate that male exposure to the aroma of certain plant structures or essential oils may increase mating success. In particular, exposure to the aroma of ginger root oil (GRO) enhances male mating frequency, and several sterile-male release programs against C. capitata have incorporated ‘aromatherapy’ (large-scale exposure of pre-release insects to GRO) to increase the effectiveness of control efforts. We investigated the mechanism underlying female preference for GRO-exposed males. Two sets of experiments were conducted. In the first, we monitored female attraction to (1) freshly killed flies, or (2) paper discs that contained hexane extracts from varying treatments. In these tests, females were sighted more often (1) near GRO-exposed than non-exposed males (even when the males were visually concealed) and (2) near extracts from GRO-exposed than non-exposed males. These findings suggest a ‘perfume effect’, whereby female mate choice is mediated by olfactory differences. In the second set, we compared (1) mate choice between intact females and females from which both antennae had been surgically removed, and (2) mating success between intact males and males from which both antennae had been surgically removed before GRO exposure. Intact females preferred GRO-exposed males, whereas females lacking both antennae rarely mated and showed no preference between GRO-exposed and non-exposed males. In the opposite treatment (intact females but surgically altered males), GRO-exposed males lacking both antennae mated as frequently as GRO-exposed intact males. These data suggest that female choice was dependent on olfactory perception of male odor but that male mating success did not depend on olfactory perception of GRO aroma, suggesting, in turn, that GRO conferred a mating advantage through an external phenomenon (possibly alteration of cuticular scent) rather than through internal processing (pheromone synthesis).

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References

  • Amrein, H. 2004. Pheromone perception and behavior in Drosophila. Curr. Opinion Neurobiol 14:435–442.

    Article  CAS  Google Scholar 

  • Andersson, M. 1994. Sexual Selection. Princeton University Press, Princeton, USA.

    Google Scholar 

  • Arita, L. H., and Kaneshiro, K. Y. 1986. Structure and function of the rectal epithelium and anal glands during mating behavior in the Mediterranean fruit fly male. Proc. Hawaiian Entomol. Soc 26:27–30.

    Google Scholar 

  • Bartelt, R. J., Schaner, A. M., and Jackson, L. L. 1988. Aggregation pheromones in Drosophila borealis and Drosophila littoralis. J. Chem. Ecol 14:1319–1327.

    Article  CAS  Google Scholar 

  • Bernays, E. A., and Chapman, R. F. 1994. Host-Plant Selection by Phytophagous Insects. Chapman and Hall, New York.

    Google Scholar 

  • Briceño, D., Eberhard, W. G., and Shelly, T. E. 2007. Male courtship behavior in Ceratitis capitata (Diptera: Tephritidae) that have received aromatherapy with ginger root oil. Fla. Entomol 90:175–179.

    Article  Google Scholar 

  • Carlson, D. A., Reinert, J. F., Bernier, U. R., Sutton, B. D., and Seawright, J. A. 1997. Analysis of the cuticular hydrocarbons among species of the Anopheles quadrimaculatus complex (Diptera: Culicidae). J. Am. Mosq. Control Assoc Suppl.:103–111.

    Google Scholar 

  • Carlson, D. A., and Yocom, S. R. 1986. Cuticular hydrocarbons from six species of fruit flies. Arch. Insect Biochem. Physiol 3:397–412.

    Article  CAS  Google Scholar 

  • Connor, W. F., Eisner, T., Vandermeer, R. K., Guerrero, A., and Meinwald, J. 1981. Precopulatory sexual interaction in an arctiid moth (Utetheisa ornatrix): the role of a pheromone derived from dietary alkaloids. Behav. Ecol. Sociobiol 9:227–235.

    Article  Google Scholar 

  • Coracini, M., Bengtsson, M., Liblikas, I., and Witzgall, P. 2004. Attraction of codling moth males to apple volatiles. Entomol. Exp. Appl 110:1–10.

    Article  CAS  Google Scholar 

  • Costanzo, K., and Monteiro, A. 2007. The use of chemical and visual cues in female choice in the butterfly Bicyclus anynana. Proc. Roy. Soc. Lond. B 274:845–851.

    Article  Google Scholar 

  • Coyne, J. A., Crittenden, A. P., and Mah, K. 1994. Genetics of a pheromonal difference contributing to reproductive isolation in Drosophila. Science 265:1461–1464.

    Article  PubMed  CAS  Google Scholar 

  • Douglas, M. H., Van Klink, J. W., Smallfield, B. M., Perry, N. B., Anderson, R. E., Johnstone, P., and Weavers, R. T. 2004. Essential oils from New Zealand manuka: triketone and other chemotypes of Leptospermum scoparium. Phytochemistry 65:1255–1264.

    Article  PubMed  CAS  Google Scholar 

  • Dowd, P. F., and Bartelt, R. J. 1991. Host-derived volatiles as attractants and pheromone synergists for dried fruit beetle, Carpophilus hemipterus. J. Chem. Ecol 17:285–308.

    Article  CAS  Google Scholar 

  • Etges, W. J., and Jackson, L. L. 2001. Epicuticular hydrocarbon variation in Drososphila mojavensis cluster species. J. Chem. Ecol 27:2125–2149.

    Article  PubMed  CAS  Google Scholar 

  • Féron, M. 1962. L’instinct de reproduction chez la mouche Mediterranéan des fruits Ceratitis capitata Wied. (Diptera: Trypetidae). Comportement sexuel. Comportement de ponte. Rev. Pathol. Veg. Entomol. Agric. Fr 41:1–129.

    Google Scholar 

  • Flath, R. A., Cunningham, R. T., Mon, T. R., and John, J. O. 1994a. Additional male Mediterranean fruit fly (Ceratitis capitata Wied.) attractants from angelica seed oil (Angelica archangelica L.). J. Chem. Ecol 20:1969–1984.

    Article  CAS  Google Scholar 

  • Flath, R. A., Cunningham, R. T., Mon, T. R., and John, J. O. 1994b. Male lures for Mediterranean fruit fly (Ceratitis capitata Wied.): structural analogues of α-copaene. J. Chem. Ecol 20:2595–2609.

    Article  CAS  Google Scholar 

  • Ginzel, M. D., and Hanks, L. M. 2005. Role of host plant volatiles in mate location for three species of longhorned beetles. J. Chem. Ecol 31:213–217.

    Article  PubMed  CAS  Google Scholar 

  • Greenfield, M. D., Shelly, T. E., and Downum, K. R. 1987. Variation in host plant quality: implications for territoriality in a desert grasshopper. Ecology 68:828–838.

    Article  Google Scholar 

  • Hanks, L. M., Millar, J. G., and Paine, T. D. 1996. Mating behavior of the eucalyptus longhorned borer (Coleoptera: Cerambycidae) and the adaptive significance of long “horns”. J. Insect Behav 9:383–393.

    Article  Google Scholar 

  • Heath, R. R., Landolt, P. J., Tumlinson, J. H., Chambers, D. L., Murphy, R. E., Doolittle, D. E., Dueben, D. B., Sivinski, J., and Calkins, C. O. 1991. Analysis, synthesis, formulation and field testing of the three major components of male Mediterranean fruit fly pheromone. J. Chem. Ecol 17:1925–1940.

    Article  CAS  Google Scholar 

  • Hendrichs, J., and Hendrichs, M. A. 1990. Mediterranean fruit fly (Diptera: Tephritidae) in nature: location and diel pattern of feeding and other activities on fruiting and nonfruiting hosts and nonhosts. Ann. Entomol. Soc. Am 83:632–641.

    Google Scholar 

  • Hoppe, K. L., Dillwith, J. W., Wright, R. E., and Szumlas, D. E. 1990. Identification of horse flies (Diptera: Tabanidae) by analysis of cuticular hydrocarbons. J. Med. Entomol 27:480–486.

    PubMed  CAS  Google Scholar 

  • Hovorka, O., Kindl, J., Kalinova, B., Knížek, M., Vrkočová, and Koutek, B. 2005. The role of beetle and host volatiles in host colonization in the European oak bark beetle, Scolytus intricatus (Ratzeburg) (Col., Scolytidae). J. Appl. Entomol 129:221–226.

    Article  Google Scholar 

  • Hughes, P. R., and Renwick, J. A. A. 1977. Hormonal and host factors stimulating pheromone synthesis in female western pine beetles Dendroctonus brevicomis. Physiol. Entomol 2:289–292.

    Google Scholar 

  • Jaffe, K., Sanchez, P., Cerda, H., Hernandez, J. A., Jaffe, R., Urdaneta, N., Guerra, G., Martinez, R., and Miras, B. 1993. Chemical ecology of the palm weevil Rhynchophorus palmarum L. (Coleoptera: Curculionidae): attraction to host plants and to a male produced pheromone. J. Chem. Ecol 19:1703–1720.

    Article  CAS  Google Scholar 

  • Jang, E. B., Light, D. M., Binder, R. G., Flath, R. A., and Carvalho, L. A. 1994. Attraction of female Mediterranean fruit flies to the five major components of male-produced pheromone in a laboratory flight tunnel. J. Chem. Ecol 20:9–20.

    Article  CAS  Google Scholar 

  • Jang, E. B., Light, D. M., Flath, R. A., Nagata, J. T., and Mon, T. R. 1989. Electroantennogram responses of the Mediterranean fruit fly, Ceratitis capitata, to identified volatile constituents from calling males. Entomol. Exp. Appl 50:7–19.

    Article  CAS  Google Scholar 

  • Katsoyannos, B. I., Kouloussis, N. A., and Papadopoulos 1997. Response of Ceratitis capitata to citrus chemicals under semi-natural conditions. Entomol. Exp. Appl 82:181–188.

    Article  CAS  Google Scholar 

  • Krasnoff, S. B., and Dussourd, D. E. 1989. Dihydropyrrolizidine attractants for arctiid moths that visit plants containing pyrrolizidine alkaloids. J. Chem. Ecol 15:47–60.

    Article  CAS  Google Scholar 

  • Landolt, P. J., and Phillips, T. W. 1997. Host plant influences on sex pheromone behavior of phytophagous insects. Annu. Rev. Entomol 42:371–391.

    Article  PubMed  CAS  Google Scholar 

  • Landolt, P. J., Heath, R. R., Millar, J. G., Davis-Hernandez, K. M., Dueben, D. B., and Ward, K. E. 1994. Effects of host plant, Gossypium hirsutum L., on sexual attraction of cabbage looper moths, Trichoplusia ni (Hubner) (Lepidoptera: Noctuidae). J. Chem. Ecol 20:2959–2974.

    Article  CAS  Google Scholar 

  • Levinson, H. Z., Levinson, A. R., and Schäfer, K. 1987. Pheromone biology of the Mediterranean fruit fly (Ceratitis capitata Wied.) with emphasis on the functional anatomy of the pheromone glands and antennae as well as mating behaviour. J. Appl. Entomol 104:448–461.

    Article  Google Scholar 

  • Lofstedt, C., Vickers, N. J., Roelofs, W. L., and Baker, T. C. 1989. Diet related courtship success in the Oriental fruit moth, Grapholita molesta (Tortricidae). Oikos 55:402–408.

    Article  Google Scholar 

  • Macleod, A. J., and De Troconis, N. G. 1982. Volatile flavour components of guava. Phytochemistry 21:1339–1342.

    Article  CAS  Google Scholar 

  • Macleod, A. J., Macleod, G., and Subramanian, G. 1988. Volatile aroma constituents of orange. Phytochemistry 27:2185–2188.

    Article  CAS  Google Scholar 

  • Marcillac, F., and Ferveur, J.-F. 2004. A set of female pheromones affects reproduction before, during and after mating in Drosophila. J. Exp. Biol 207:3927–3933.

    Article  PubMed  CAS  Google Scholar 

  • Moore, A. J. 1988. Female preferences, male social status, and sexual selection in Nauphoeta cinerea. Anim. Behav 36:303–305.

    Article  Google Scholar 

  • Nakagawa, S., Farias, G. J., Suda, D., and Chambers, D. L. 1973. Mating behavior of the Mediterranean fruit fly following excision of the antennae. J. Econ. Entomol 66:583–584.

    Google Scholar 

  • Nishida, R., Shelly, T. E., Whittier, T. S., and Kaneshiro, K. Y. 2000. Alpha- copaene, a potential rendezous cue for the Mediterranean fruit fly, Ceratitis capitata?. J. Chem. Ecol 26:87–100.

    Article  CAS  Google Scholar 

  • Papadopoulos, N. T., Katsoyannos, B. I., Kouloussis, N. A., and Hendrichs, J. 2001. Effect of orange peel substances on mating competitiveness of male Ceratitis capitata. Entomol. Exp. Appl 99:253–261.

    Article  Google Scholar 

  • Papadopoulos, N. T., Shelly, T. E., Niyazi, N., and Jang, E. B. 2006. Olfactory and behavioral mechanisms underlying enhanced mating competitiveness following exposure to ginger root oil and orange oil in males of the Mediterranean fruit fly, Ceratitis capitata (Diptera: Tephritidae). J. Insect Behav 19:403–418.

    Article  Google Scholar 

  • Pivnick, K. A., Lavoie-Dornik, J., and Mcneil, J. N. 1992. The role of the androconia in the mating behaviour of the European skipper, Thymelicus lineola, and evidence for a male sex pheromone. Physiol. Entomol 17:260–268.

    Google Scholar 

  • Pliske, T. E. 1975. Courtship behavior and use of chemical communication by males of certain species of ithomiinae butterflies (Nymphalidae: Lepidoptera). Ann. Entomol. Soc. Am 68:935–942.

    Google Scholar 

  • Prokopy, R. J., and Hendrichs, J. 1979. Mating behavior of Ceratitis capitata in field cages on host trees. Ann. Entomol. Soc. Am 72:642–648.

    Google Scholar 

  • Quiroz, A., Ortega, F., Ramírez, C. C., Wadhams, L. J., and Pinilla, K. 2005. Response of the beetle Hylastinus obscurus Marsham (Coleoptera: Scolytidae) to red clover (Trifolium pretense L.) volatiles in a laboratory olfactometer. Environ. Entomol 34:690–595.

    Article  Google Scholar 

  • Rantala, M. J., Jokinen, I., Kortet, R., Vainikka, A., and Suhonen 2002. Do pheromones reveal male immunocompetence? Proc. Roy. Soc. Lond. B 269:1681–1685.

    Article  Google Scholar 

  • Shanbhag, S., Muller, B., and Steinbrecht, A. 1999. Atlas of olfactory organs of Drosophila melanogaster. 1. Types, external organization, innervation and distribution of olfactory sensilla. Int. J. Insect Morphol. Embryol 28:377–397.

    Article  Google Scholar 

  • Shelly, T. E. 2001. Exposure to α-copaene and α-copaene-containing oils enhances the mating success of male Mediterranean fruit flies (Diptera: Tephritidae). Ann. Entomol. Soc. Am 94:497–502.

    Article  CAS  Google Scholar 

  • Shelly, T. E. 2005. Does mating with ginger root oil-exposed males confer fitness benefits to female Mediterranean fruit flies, Ceratitis capitata (Diptera: Tephritidae)? Proc. Hawaiian Entomol. Soc 37:65–71.

    Google Scholar 

  • Shelly, T. E., and Villalobos, E. 2004. Host plant influence on the mating success of male Mediterranean fruit flies: variable effects within and between individual plants. Anim. Behav 68:417–426.

    Article  Google Scholar 

  • Shelly, T. E., and Kennelly, S. 2007. Settlement patterns of Mediterranean fruit flies in the tree canopy: an experimental analysis. J. Insect Behav 20:453–472.

    Article  Google Scholar 

  • Shelly, T. E., Edu, J., Smith, E., Hoffman, K., War, M., Santos, R., Favela, A., Garagliano, R., Ibewiro, B., and Mcinnis, D. O. 2007a. Aromatherapy on a large scale: exposing entire holding rooms to ginger root oil increases the mating competitiveness of sterile males of the Mediterranean fruit fly. Entomol. Exp. Appl 123:193–201.

    Article  Google Scholar 

  • Shelly, T. E., Cowan, A. N., Edu, J., and Pahio, E. 2007b. Mating success of male Mediterranean fruit flies following exposure to two sources of α-copaene, manuka oil and mango. Fla. Entomol. (in press) .

  • Shelly, T. E., Dang, C., and Kennelly, S. 2004a. Exposure to orange (Citrus sinensis L.) trees, fruit, and oil enhances mating success of male Mediterranean fruit flies (Ceratitis capitata [Wiedemann]). J. Insect Behav 17:303–315.

    Article  Google Scholar 

  • Shelly, T. E., Mcinnis, D. O., Pahio, E., and Edu, J. 2004b. Aromatherapy in the Mediterranean fruit fly (Diptera: Tephritidae): sterile males exposed to ginger root oil in pre-release, storage boxes display increased mating competitiveness in field-cage trials. J. Econ. Entomol 97:846–853.

    Article  PubMed  Google Scholar 

  • Sivinski, J., Calkins, C. O., and Webb, J. C. 1989. Comparisons of acoustic courtship signals in wild and laboratory reared Mediterranean fruit fly Ceratitis capitata. Fla. Entomol 72:212–214.

    Article  Google Scholar 

  • Sutton, B. D., and Steck, G. J. 1994. Disrimination of Caribbean and Mediterranean fruit fly larvae (Diptera: Tephritidae) by cuticular hydrocarbon analysis. Fla. Entomol 77:231–237.

    Article  CAS  Google Scholar 

  • Suvanto, L., Liimatainen, J. O., Tregenza, T., and Hoikkala, A. 2000. Courtship signals and mate choice of the flies of inbred Drosophila montana strains. J. Evol. Biol 13:583–592.

    Article  Google Scholar 

  • Takeoka, G., Flath, R. A., Mon, T. R., Buttery, R. G., Teranishi, R., Guntert, M., Lautamo, R., and Szejtli, J. 1990. Further applications of permethylated β-cyclodextrin capillary gas chromatographic columns. J. High Resol. Chromatogr 13:202–206.

    Article  CAS  Google Scholar 

  • Tanaka, N., Steiner, L. F., Ohinata, K., and Okamoto, R. 1969. Low-cost larval rearing medium for mass-production of oriental and Mediterranean fruit flies. J. Econ. Entomol 62:967–968.

    Google Scholar 

  • Thornhill, R. 1991. Female preference for the pheromone of males with low fluctuating asymmetry in the Japanese scorpionfly (Panorpa japonica: Mecoptera). Behav. Ecol 3:277–282.

    Article  Google Scholar 

  • Thornhill, R., and Alcock, J. 1983. The Evolution of Insect Mating Systems. Harvard University Press, Cambridge, USA.

    Google Scholar 

  • Uebel, E. C., Sonnet, P. E., Menzer, R. E., Miller, R. W., and Lusby, W. R. 1977. Mating-stimulant pheromone and cuticular lipid constituents of the little house fly, Fannia canicularis (L.). J. Chem. Ecol 3:269–278.

    Article  CAS  Google Scholar 

  • Vogt, R. G. 2005. Molecular basis of pheromone detection in insects, pp. 753–804, in L. I. Gilbert, K. Iatro, and S. Gill (eds.). Comprehensive Insect Physiology, Biochemistry, Pharmacology, and Molecular Biology. Vol. 3: EndocrinologyElsevier, London.

    Google Scholar 

  • Warthen, J. D., and Mcinnis, D. O. 1989. Isolation and identification of male medfly attractive components in Litchi chinensis stems and Ficus spp. stem exudates. J. Chem. Ecol 15:1931–1946.

    Article  CAS  Google Scholar 

  • Whittier, T. S., Nam, F. Y., Shelly, T. E., and Kaneshiro, K. Y. 1994. Male courtship success and female discrimination in the Mediterranean fruit fly (Diptera: Tephritidae). J. Insect Behav 7:159–170.

    Article  Google Scholar 

  • Whittier, T. S., Kaneshiro, K. Y., and Prescott, L. D. 1992. Mating behavior of Mediterranean fruit flies (Diptera: Tephritidae) in a natural environment. Ann. Entomol. Soc. Am 85:214–218.

    Google Scholar 

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Acknowledgments

We thank Eric Jang, Jocelyn Millar, David Robacker, and Keng-Hong Tan for technical advice. Sylvia Young of Citrus and Allied Essences Ltd. supplied information regarding the chemical composition of ginger root oil. Eric Jang, Jocelyn Millar, and Boaz Yuval provided comments on an earlier draft.

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Shelly, T.E., Edu, J., Pahio, E. et al. Scented Males and Choosy Females: Does Male Odor Influence Female Mate Choice in the Mediterranean Fruit Fly?. J Chem Ecol 33, 2308–2324 (2007). https://doi.org/10.1007/s10886-007-9394-y

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