Scented males and choosy females: does male odor influence female mate choice in the Mediterranean fruit fly?

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).

Age-dependent variation in mating success of sterile male Mediterranean fruit flies (Diptera: Tephritidae): implications for sterile insect technique.

The sterile insect technique (SIT) is widely used in integrated programs against the Mediterranean fruit fly, Ceratitis capitata (Wiedemann) (Diptera: Tephritidae). Unfortunately, the mass-rearing procedures inherent to the SIT often lead to a reduction in the mating ability of the released males. To counter this deficiency, SIT programs rely upon the production and release of large numbers of sterile males to achieve high overflooding (sterile:wild male) ratios. To ensure a high release volume, emergence facilities release adult males at a young age (2 d old in some cases). The primary objective of this study was to describe age-dependent variation in the mating propensity and competitiveness of sterile males of C. capitata. Males that were 2 or 3 d old had lower mating propensity than males that were > or =4 d old, and 3-d-old males had lower mating competitiveness than males that were > or =4 d old. Given these results, we measured the effect of a longer holding period on male mortality in storage boxes. With delayed food placement, males held in storage boxes for 4 d after emergence showed no higher mortality than males held for only 2 d (the standard interval). Using large field enclosures, we compared the levels of egg sterility attained via releases of 2- versus 4-d-old sterile males at two overflooding ratios (5:1 and 100:1). At the lower ratio, the proportion of unhatched eggs observed for trials involving 2-d-old sterile males was not, on average, significantly higher than that observed for matings between wild flies (33 versus 25%, respectively), whereas the level of egg sterility observed for releases of 4 d old sterile males was 62%. At the 100:1 overflooding ratio, the proportion of unhatched eggs associated with the 2-d-old sterile males was 58%, a level not significantly different from that induced by 4-d-old sterile males at the 5:1 ratio and significantly lower than the level (79%) observed for 4-d-old sterile males at 100:1 overflooding ratio. The implications of these results for SIT are discussed.

Sterile insect technique and Mediterranean fruit fly (Diptera: Tephritidae): assessing the utility of aromatherapy in a Hawaiian coffee field.

The sterile insect technique (SIT) is widely used in integrated programs against tephritid fruit fly pests, particularly the Mediterranean fruit fly, Ceratitis capitata (Wiedemann) (Diptera: Tephritidae). Unfortunately, the mass-rearing procedures inherent to the SIT often lead to a reduction in the mating ability of the released males. One potential solution involves the prerelease exposure of males to particular attractants. In particular, exposure of male Mediterranean fruit flies to ginger, Zingiber officinale Roscoe, root oil (GRO) has been shown to increase mating success in laboratory and field cage trials. Here, we describe a field experiment that compares the level of egg sterility observed in two Hawaiian coffee, Coffea arabica L., plots, with GRO-exposed, sterile males released in one (treated) plot and nonexposed, sterile males released in the other (control) plot. Once per week in both plots over a 13-wk period, sterile males were released, trap captures were scored to estimate relative abundance of sterile and wild males, and coffee berries were collected and dissected in the laboratory to estimate the incidence of unhatched (sterile) eggs. Data on wild fly abundance and the natural rate of egg hatch also were collected in a remote area that received no sterile males. Despite that sterile:wild male ratios were significantly lower in the treated plot than in the control plot, the incidence of sterile eggs was significantly higher in the treated plot than in the control plot. Correspondingly, significantly higher values of Fried's competitiveness index (C) were found, on average, for treated than control sterile males. This study is the first to identify an association between the GRO "status" of sterile males and the incidence of egg sterility in the field and suggests that prerelease, GRO exposure may represent a simple and inexpensive means to increase the effectiveness of Mediterranean fruit fly SIT programs.

Aromatherapy in the Mediterranean fruit fly (Diptera: Tephritidae): sterile males exposed to ginger root oil in prerelease storage boxes display increased mating competitiveness in field-cage trials.

Previous research showed that exposure to ginger root, Zingiber officinale Roscoe, oil increased the mating success of mass-reared, sterile males of the Mediterranean fruit fly, Ceratitis capitata (Wiedemann). This work, however, involved the exposure of small groups of males (n = 25) in small containers (volume 400 ml). Several sterile male release programs use plastic adult rearing containers (so-called PARC boxes; hereafter termed storage boxes; 0.48 by 0.60 by 0.33 m) to hold mature pupae and newly emerged adults before release (approximately = 36,000 flies per box). The objective of the current study was to determine whether the application of ginger root oil to individual storage boxes increases the mating competitiveness of sterile C. capitata males. Irradiated pupae were placed in storage boxes 2 d before adult emergence, and in the initial experiment (adult exposure) ginger root oil was applied 5 d later (i.e., 3 d after peak adult emergence) for 24 h at doses of 0.0625, 0.25, 0.5, 1.0, and 2.0 ml. In a second experiment (pupal-adult exposure), ginger root oil was applied to storage boxes immediately after pupal placement and left for 6 d (i.e., 4 d after peak adult emergence) at doses of 0.25 and 1.0 ml. Using field cages, we conducted mating trials in which ginger root oil-exposed (treated) or nonexposed (control) sterile males competed against wild-like males for copulations with wild-like females. After adult exposure, treated males had significantly higher mating success than control males for all doses of ginger root oil, except 2.0 ml. After pupal-adult exposure, treated males had a significantly higher mating success than control males for the 1.0-ml but not the 0.25-ml dose of ginger root oil. The results suggest that ginger root oil can be used in conjunction with prerelease, storage boxes to increase the effectiveness of sterile insect release programs.