Exposure To Orange (citrus Sinensis L

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Exposure to Orange (Citrus sinensis L.) Trees, Fruit, and Oil Enhances Mating Success of Male Mediterranean Fruit Flies (Ceratitis capitata [Wiedemann]) Todd Shelly,1−3 Charmian Dang,1 and Susan Kennelly2 Accepted: December 18, 2003; revised January 23, 2004

Previous laboratory tests revealed that exposure to oranges (Citrus sinensis L.) increased the mating success of male Mediterranean fruit flies, Ceratitis capitata (Wiedemann) (medfly). This advantage may have resulted from male exposure to α-copaene (a sesquiterpene hydrocarbon and known male attractant) in the peel, as pure α-copaene has been shown to increase the mating success of male medflies. Working with orange trees as well, we investigated whether male exposure to nonfruiting trees, leaves (also known to contain α-copaene albeit at a lower concentration than fruit), and fruit conferred a mating advantage to wild-like males in field-cage tests. Males exposed to entire nonfruiting trees or leaves had a mating advantage over control males (exposed to a nonhost plant) in trials conducted 1 day but not 3 days after exposure. Males exposed to orange fruits had higher mating success than control males (exposed to apples) in trials conducted 1 and 3 days after exposure. Enhanced mating success was observed only when males were permitted to contact the orange leaves and fruits; aroma alone did not affect male mating success. In addition, we examined whether exposure to commercially available orange oil, which also contains α-copaene, enhanced the mating performance of wild-like and mass-reared sterile males. Heightened mating success was observed in trials conducted 1 and 3 days after exposure for both types of 1USDA-APHIS, 2Center

Waimanalo, Hawaii 96795. for Conservation Research and Training, University of Hawaii, Honolulu, Hawaii

96822. whom correspondence should be addressed at USDA-APHIS, 41-650 Ahiki Street, Waimanalo, Hawaii 96795. e-mail: [email protected].

3To

303 C 2004 Plenum Publishing Corporation 0892-7553/04/0500-0303/0 °

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males, and in this case aroma alone had a positive effect on male mating success. Future research should attempt to identify the behavioral, physiological, or chemical mechanisms underlying the observed increases in male mating success. KEY WORDS: Mediterranean fruit fly; Ceratitis capitata; orange trees; mating success; α-copaene.

INTRODUCTION Host plants affect the mate searching strategy of male phytophagous insects in two main ways. First, host plants may have a strong influence on male spacing. In particular, males may concentrate their mate searching in the vicinity of host plants if females aggregate there in search of food and/or oviposition sites (Mangan, 1979; Greenfield, 1997). In addition, host plants may affect male reproductive behavior via chemical interactions. Particular plant-borne substances ingested by larvae (Lofstedt et al., 1989) or adults (Krasnoff and Dussourd, 1989) may serve as precursors in the synthesis of male sex pheromone. Exposure to host plant volatiles may also trigger pheromone release in males (Jaffe et al., 1993) as well as increase female responsiveness to male pheromones (Phillips et al., 1984). Several recent studies have shown that plant-derived compounds have an important effect on the mating behavior of male tephritids. For example, males of the oriental fruit fly (Bactrocera dorsalis [Coquillett]) that feed on pure methyl eugenol (Shelly and Dewire, 1994; Tan and Nishida, 1996) or natural sources (flowers) of the compound (Shelly, 2000, 2002) have a pronounced mating advantage over methyl eugenol-deprived males. Males that consume methyl eugenol display increased signaling activity and produce a more attractive pheromone (Shelly and Dewire, 1994), presumably resulting from the incorporation of certain metabolites of methyl eugenol in the pheromone (Nishida et al., 1997). Growing evidence (Nishida et al., 1993; Hee and Tan, 1998; Tan and Nishida, 2000) indicates that host plant substances influence male reproductive behavior in other species of Bactrocera as well. Similarly, work on the Mediterranean fruit fly (or medfly; Ceratitis capitata [Wiedemann]), has revealed that feeding on wounded fruits of the orange tree (Citrus sinensis L.) confers a mating advantage in laboratory tests (Papadopoulos et al., 2001). The effect of fruit exposure was quite longlasting: males exposed to wounded oranges for 24 h had a mating advantage over control males for at least 10 days after exposure. Likewise, Shelly and Villalobos (2004) found that male medflies exposed to the bark and fruits of guava trees (Psidium guajava L.) obtained significantly more matings than

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(control) nonexposed males in tests conducted in field cages. Tests with both orange and guava showed that males gained a mating advantage only when they were permitted to contact the fruits (and, for guava, the bark) and that exposure to fruit (or guava bark) aroma alone had no effect on male mating success. In addition to natural substrates, exposure to particular essential oils, namely, angelica seed oil and ginger root oil (Shelly, 2001), has been shown to confer a mating advantage to male medflies. In contrast to the natural substrates, these oils conferred a mating advantage even when males were prohibited from contacting them directly. The chemical basis for these findings is unknown, but evidence suggests that α-copaene, a plant-borne sesquiterpene hydrocarbon and known attractant of male medflies (Flath, 1994a,b), is involved. The substances shown to confer a mating advantage to male medflies all contain this chemical (orange fruit [Teranishi et al., 1987], guava fruit [Oliveros-Belardo et al., 1986], guava bark [F. Webster, personal communication], angelica seed and ginger root oils [Takeoka et al., 1990]). In addition, male medflies exposed to pure α-copaene had a mating advantage over control, nonexposed males (Shelly, 2001). (Although α-copaene is clearly implicated, it should be recognized that many related terpenoids co-occur with α-copaene and may also affect the behavior of male medflies either independently or in combination with α-copaene [Flath, 1994a,b)]. Consequently, any reference to α-copaene is perhaps best considered to include not only that compound, but other sesquiterpenes that may also influence male medflies.) How αcopaene enhances male mating performance is not known, although tests with ginger root oil showed that exposed males signaled more frequently (Shelly, 2001) and mounted females more quickly (i.e., exhibited shorter courtship [Briceno et al., unpublished data]) than control males. Exposure to ginger root oil does not appear to affect the attractiveness of the male sex pheromone (Shelly, 2001). The present study expanded upon that of Papadopoulos et al. (2001) and focused on two main objectives regarding the interaction between orange trees and male medflies. First, we investigated whether male exposure to nonfruiting trees, leaves, and fruit conferred a mating advantage to wildlike males (see below) in field-cage tests. Nishida et al. (2000) reported that α-copaene occurs in the leaves of various citrus plants, including orange, and consequently we investigated whether exposure to entire, nonfruiting trees or leaves only increase male mating success. Second, we examined whether exposure to commercially available orange oil, which also contains the attractant α-copaene, enhanced the mating performance of both wildlike and mass-reared, sterile males. The release of sterile male medflies is an important means of suppressing infestations of this notorious agricultural pest (Hendrichs et al., 2002), and exposure to ginger root oil has been shown

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to increase the mating performance of sterile males relative to wild males (Shelly and McInnis, 2001). Here, we determine whether prerelease exposure to orange oil similarly increases the mating competitiveness of sterile males.

METHODS Study Flies. Wild-like flies were derived from a laboratory colony started with 200–300 adults reared from coffee (Coffea arabica L.) collected near Haleiwa, Oahu. The colony was maintained in a screen cage and provided with ample food (sugar and yeast hydrolysate at a 3:1 volumetric ratio), water, and oviposition substrate (perforated plastic vials containing small sponges soaked in lemon juice). Eggs were placed on standard larval medium (Tanaka et al., 1969) in plastic containers over vermiculite for pupation. Adults used in the mating experiments were separated by sex within 24 h of emergence, well before reaching sexual maturity at 5–7 days of age. When used in this study, the wild-like flies were six to eight generations removed from the wild. Mass-reared males were from the Maui-Med strain produced by the USDA-APHIS Hawaii Fruit Fly Rearing Facility, Waimanalo, HI, since 1996 (i.e., mass-reared for approximately 60 generations prior to this study). Pupae of this mass-reared strain were exposed in air to 15 krad of gamma irradiation from a 137 Cs source 2 days before eclosion and then delivered to the laboratory. Males of this strain were collected within 12 h of emergence (sexual maturity is attained at 2–3 days of age [D. O. McInnis, personal communication]). Both wild-like and mass-reared adults were held in plastic buckets covered with nylon screening (5-liter volume, 100–150 flies per bucket) with ample food and water at 22–25◦ C and 65–85% RH with a photoperiod of 12:12 (L:D) from natural and artificial light. Male Exposure to Orange Trees, Leaves, and Fruit. We ran three experiments that involved wild-like flies exclusively. In the first, we examined whether exposure to nonfruiting orange trees influenced male mating success. We released 150 (treated) males between 0700 and 0730 into nylon-mesh field cages (3-m diameter, 2.5 m high) that contained two potted, nonfruiting orange trees (approximately 2 m tall). The field cages were located at the Agricultural Experiment Station of the University of Hawaii, Waimanalo. Five trees, presented in different combinations, were used for exposing males. Males were collected 4 h later, returned to the laboratory (where food and water were provided), and then tested 1 or 3 days later. Control males were treated in the same manner except that they were released in a field cage containing a nonhost tree (fiddlewood, Citharexylum

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spinosum L.). A single fiddlewood tree was used for all control males. Air temperature (1 m aboveground in the shade) ranged from 23 to 32◦ C during the exposure period. When released for exposure, treated and control males were 8–11 days old. In the second experiment, treated males were tested after exposure to fresh leaves in the laboratory. Leaves were removed from trees near the laboratory and immediately placed in screen cages (30-cm cubes). Forty leaves were used per cage, and these were placed on chicken-wire screen raised above the cage floor, allowing the males access to both top and bottom leaf surfaces. We then placed 60 males in individual cages at 0800, removed them 3 h later, and held them (with food and water) until tested 1 or 3 days later. Control males were handled in the same manner except that they were exposed to leaves (40 leaves/cage) from a fiddlewood tree (the leaves used were of similar size to orange leaves). When exposed to the leaves, treated and control males were 8–13 days old. Treated and control males were exposed to leaves in separate rooms to avoid inadvertent exposure of orange aroma to the control males (both rooms were isolated from the colony as well). In an additional test, we covered the orange leaves with nylon screening to prevent the males from contacting them. Males treated in this manner were tested 1 day later. Third, treated males were exposed to fruit in the laboratory. Sixty males were placed in screen cages (30 cm cubes) at 0800 with two Valenica oranges, collected 3 h later, and kept in the laboratory (with food and water) until tested 1 or 3 days later. As with leaf exposure, we modified this protocol by placing the two oranges in screen containers that allowed males to detect the fruit odor but prevented them from making direct contact with the fruit. Males treated in this manner were tested 1 day later. Control males were handled in the same manner except that they were presented with two Granny Smith apples (Malus sylvestris Mill.) instead of oranges. Fruit were purchased in a supermarket and then rinsed in water and dried prior to use. Also, before exposure, we made five shallow cuts (2–4 cm long) into the peel of all fruit using a scalpel. When exposed to fruit, treated and control males were 8–10 days old. As with the leaf exposure, treated and control males were exposed to fruit in separate rooms. Male Exposure to Orange Oil. We ran three experiments involving male exposure to orange oil (Oil Orange California Type C.P. FCC; Product code, 15061; Citrus and Allied Essences, Lake Success, NY), containing α-copaene 0.2% (concentration [S. Young, personal communication]). A standard exposure protocol was followed in all experiments. We applied 20 µl of the oil to a small disk of filter paper using a microcapillary pipette. The disk was placed on the bottom of a transparent plastic drinking cup (400-ml volume), 25 males were immediately placed in the cup using an aspirator,

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and the cup was covered with nylon screening. Exposure started at 0700 and continued until 1100. The behavior of the males was not monitored systematically during exposure periods, but in frequent checks males were never observed touching the paper disc (the same observation was made for ginger root oil [Shelly, 2001]). In a given experiment, control males were simply nonexposed males of an age similar to that of treated (exposed) males. Exposure to the oil was always conducted in an isolated room to prevent inadvertent exposure to control males (and the colony as a whole). In the first experiment, we compared the mating success of treated and control wild-like males. Treated males were exposed at 8–10 days of age using the standard method and tested 1 or 5 days later, respectively. In the second experiment, treated and control mass-reared males competed separately (i.e., in separate field cages) against wild-like males. Treated massreared males were exposed at 4–5 days of age to orange oil using the standard protocol and tested 1 or 5 days later, respectively. Wild-like males (9–14 days old when tested) were not exposed to orange oil in this experiment. In the third experiment, treated and control mass-reared males competed directly against one another (i.e., no wild-like males were used). Treated males were exposed to orange oil using the standard protocol or, as with the orange leaves and fruits, were exposed to the aroma only. In both cases, treated males were 4–5 days old when exposed and were tested 1 day later. To present direct contact with the oil, we placed the oil-laden disks in small containers (covered with nylon mesh screening) that were then introduced into the plastic cups. Mating Trials. Mating trials were conducted in Waimanalo, Oahu, at the same University of Hawaii facility noted above. In all experiments (with one exception), groups of 100 treated and 100 control males of the same strain (i.e., wild-like or mass-reared) and 100 wild-like females were released between 0700 and 0730 in field cages that contained a single rooted guava tree. (In the exception, 100 mass-reared and 100 wild-like males were released along with 100 wild-like females in one experiment testing the effect of orange oil exposure. In this case, mass-reared males were either treated or control, and wild-like males were never treated). For a given test, we marked either treated or control males (or mass-reared or wild-like males for the aforementioned exception), alternating the marked group between successive tests. Males were marked 1 day before testing by cooling them for several minutes and placing a dot of enamel paint on the thorax. This procedure had no obvious adverse effects, and males resumed normal activities within minutes of handling. The cages were monitored for 4 h, mating pairs were collected in vials, and the males were identified. Wild-like females (8–14 days old) were used in all tests. All flies were used only once.

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Statistical Analyses. Pairwise comparisons were made using the t-test. Assumptions of normality (tested using the Kolmogorov–Smirnov distribution with the Lillefors correction) and homoscedasticity (tested using Levene’s median test) were met in all cases. Where comparisons involved proportions, values were arcsine transformed. Statistical tests were performed using SigmaStat (Version 2.0).

RESULTS Orange Trees, Leaves, and Fruit. Wild-like males exposed to orange trees obtained significantly more matings than (control) wild-like males exposed to a nonhost tree in tests conducted 1 day following exposure (Table I). However, exposure to orange trees conferred no mating advantage in tests conducted 3 days following exposure. Similar results were obtained when wild-like males were exposed to leaves in laboratory cages: exposure to orange leaves (with contact possible) conferred a mating advantage 1 day but not 3 days after exposure (Table I). When denied contact with the orange leaves, however, no difference in mating success was detected between treated and control males. Wild-like males exposed to orange fruit achieved significantly more matings than (control) wild-like males exposed to apples, and in this instance a mating advantage was evident both 1 and 3 days after

Table I. Mating Success of Treated Versus Control Wild-like Males, Where Treated Males Were Exposed to Nonfruiting Orange Trees in Field Cages (Control Males Were Exposed to a Fiddlewood Tree) or Orange Leaves and Fruit in the Laboratory (Control Males Were Exposed to Fiddlewood Leaves and Apples, Respectively)

Experiment

Exposure treated males

1

Trees

2

Leaves

2

Fruit

Postexposure interval (days)a 1 3 1 3 1(hc) 1 3 1(nc)

Matings per replicate Treated

Control

33.0 (8.3) 24.6 (5.0) 29.9 (7.8) 19.1 (4.7) 17.8 (6.9) 26.9 (7.7) 23.2 (6.7) 23.5 (7.7)

18.8 (6.2) 25.9(7.2) 13.5 (4.3) 15.9 (4.6) 18.9 (8.8) 10.4 (5.3) 11.9 (3.8) 18.0 (9.9)

t 4.1∗∗ 0.4 (NS) 4.9∗∗∗ 1.0 (NS) 0.4 (NS) 5.0∗∗∗ 4.2∗∗∗ 1.2 (NS)

Note. Values represent means (±1 SD) based on nine replicates for tree exposure and eight replicates for both leaf and fruit exposure. See text for details of exposure protocols. a For treated males, days elapsed between exposure and testing; control males were approximately the same age as treated males in all experiments. (HC) No contact of orange leaves or fruit was possible. ∗∗ P < 0.001; ∗∗∗ P < 0.001. NS, not significant, at P = 0.05.

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exposure (Table I). However, treated males accounted, on average, for a slightly higher proportion of the total matings 1 day after exposure than 3 days after exposure (75 versus 66%, respectively; t = 2.4, P < 0.05). The advantage conferred by fruit exposure apparently derived from physical contact with the oranges, because exposure to fruit odor alone did not enhance the mating success of treated males (Table I). Orange Oil. In competition between wild-like males (Table II; Experiments 1a and 1b), individuals exposed to orange oil achieved significantly more matings than nonexposed individuals in tests performed 1 or 5 days after exposure of the treated males. The mating success of mass-reared males relative to wild-like males depended strongly on whether the mass-reared males were exposed to orange oil (Table II; Experiments 2a and 2b). Mass-reared males exposed to orange oil had a mating advantage whether tested 1 or 5 days after exposure, accounting for 70 and 65% of the total matings, respectively (t = 0.3, P > 0.05). In contrast, when neither group was exposed to orange oil, (control) wildlike males outcompeted the (control) mass-reared males associated with both postexposure intervals.

Table II. Mating Success of Wild-like and Mass-Reared Males, Where Treated Males Were Exposed to Orange Oil (Control Males Were Not Exposed) Experiment

Male type

1a

Wild-like, treated Wild-like, control Wild-like, treated Wild-like, control Mass-reared, treated Wild-like, control Mass-reared, control Wild-like, control Mass-reared, treated Wild-like, control Mass-reared, control Wild-like, control Mass-reared, treated Mass-reared, control Mass-reared, treated Mass-reared, control

1b 2a

2b

3a 3b

Postexposure interval (days)a 1 5 1

5

1 1 (nc)

Mating per replicate

t

35.7 (10.4) 15.4 (6.5) 30.2 (6.9) 18.6 (7.3) 27.2 (9.4) 11.5 (6.6) 14.5 (7.6) 35.1 (11.2) 30.0 (10.2) 16.0 (7.4) 11.6 (6.6) 24.9 (8.8) 33.6 (8.1) 14.0 (8.0) 32.8 (7.2) 16.7 (7.7)

4.7∗∗∗ 4.1∗∗∗ 4.8∗∗∗ 3.9∗∗ 3.8∗∗ 4.2∗∗∗ 4.9∗∗∗ 4.3∗∗∗

Note. Values represent means (±1 SD) based on eight replicates for all experiments. See text for details of exposure protocol. a For treated males, days elapsed between exposure and testing; control males were approximately the same age as treated males in all experiments. (nc) No contact with orange oilcontaining disk possible. ∗∗ P < 0.001; ∗∗∗ P < 0.001.

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Consistent with the preceding experiment, treated mass-reared males had a pronounced mating advantage over control mass-reared males in direct competition, and this pattern was evident regardless of whether the treated males were able to contact the oil-containing disk (Table II; Experiment 3). On average, the proportion of matings obtained by treated males able to contact the disk was similar to that for treated males denied contact (70 and 66%, respectively; t = 0.2, P > 0.05).

DISCUSSION Consistent with earlier data (Papadopolous et al., 2001), the present study shows that (1) exposure to orange fruit conferred a mating advantage to male Mediterranean fruit flies, (2) this advantage lasted several days after exposure, and (3) direct contact with fruit was required for mating enhancement, i.e., exposure to fruit odor alone had no effect. Similar effects were obtained following male exposure to guava fruit as well (Shelly and Villalobos, 2004). The present study also demonstrated that male exposure to entire nonfruiting orange trees and leaves alone increased male mating success. In contrast to fruit exposure, however, the positive effect on male mating was short-lived, and there was no significant difference between control and treated males in tests conducted 3 days after treated males were exposed to orange trees or leaves. This difference between fruit and leaf exposure may reflect a difference in the concentration of α-copaene in these structures: orange peels contain approximately 0.7 µg/g of α-copaene (R. Nishida, personal communication), compared to only 0.3–0.4 µg/g leaf for orange leaves (Nishida et al., 2000; comparable data are not available for guava). The present findings for orange (along with those for guava [Shelly and Villalobos, 2004]) suggest that chemical interactions between males and host plants may influence the distribution of male mating aggregations (leks) in the environment. Although field data on spacing of male and female medflies are scant, evidence (summarized by Field et al., 2002) indicates that males tend to cluster at sites of high female traffic (or hotspots [Bradbury and Gibson, 1983]). According to this idea, medfly leks generally from on particular host trees, because females are attracted there for oviposition. Thus, although males do not control access to fruit, they perch nearby to increase encounter rates with receptive females requiring sperm prior to oviposition. While female response to oviposition sites undoubtedly affects male distribution, the present study suggests that chemical interactions between males and host plants may also influence male spacing independently of female movement.

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Moreover, because the nature of these male-plant interactions varies among different host plant species, there may be corresponding variation in the degree of congruence between male and female responses to a given host plant. In the case of orange, for example, the presence of fruits is likely to attract both sexes strongly, because males gain a longer-lasting mating benefit from fruit than leaves, and females require fruit for oviposition. In the case of guava, however, males gain equal mating benefits through contact with ripe fruit or patches of bark rich in α-copaene (Shelly and Villalobos, 2004). Thus, while fruiting guava trees might attract both sexes, nonfruiting trees may still be attractive to males (if these contains high levels of α-copaene) but not, per se, to females (i.e., independent of male presence). Because of the complex interplay between host plant chemistry and medfly behavior, experimental studies that manipulate the distribution of oviposition sites and α-copaene sources independently may be required to evaluate the relative importance of these two resources on lek distribution. Like ginger root oil (Shelly, 2001), exposure to orange oil greatly increased the mating success of male medflies. In fact, orange oil reversed the outcome of mating competition between wild-like and mass-reared, sterile males. Without exposure to orange oil, mass-reared males achieved about one-third of the total matings, whereas after exposure they obtained approximately two-thirds of all matings. Also, increased mating success was evident even when males were prohibited from contacting the orange oil (the same result was found for ginger root oil [Shelly, 2001]). These findings suggest that, like ginger root oil (Shelly and McInnis, 2001), orange oil could potentially be used to increase the mating competitiveness of sterile males in control programs against the medfly. To further investigate this possibility, the effectiveness of orange oil should be examined at large-scale exposure. Specifically, sterile male release programs against medfly often hold newly emerged flies for 3–4 days in large holding boxes (so-called PARC boxes), each of which holds approximately 40,000 males. The entire box could be exposed to orange oil (by placing oil-laden filter paper on a screened opening on the top of the box), and the mating success of these treated males could be compared to control males from unexposed boxes. Preliminary evidence suggests that, like their wild counterparts, massreared males of C. capitata gain a mating advantage through contact with guava and orange fruits. Thus, sterile males may receive a competitive boost independent of any prerelease exposure regime. Even so, of course, prerelease exposure to orange (or ginger root) oil eliminates the “need” for sterile males to locate chemical sources in the environment (thereby eliminating time and energy costs associated with searching) and guarantees that sterile males benefit fully from exposure to a performance-enhancing oil.

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Future work should focus on identifying the mechanism underlying increased male mating success. Field (Shelly, 2001) and laboratory (Papadopoulous and Shelly, unpublished data) experiments using ginger root oil revealed no difference in long-range female attraction to exposed versus nonexposed males. A chemical perspective also argues against a role for α-copaene (or metabolites) in pheromone synthesis, because no compound similar in structure to α-copaene has been recorded in maleproduced volatiles (Millar, 1995). One possibility is that medfly males alter the pheromonal composition during courtship (i.e., following female arrival) and that α-copaene plays a role in this short-range communication (W. G. Eberhard, personal communication). Data (Briceno et al., unpublished data) showing quick female acceptance of ginger root oil–exposed males are consistent with this idea. Comparing the mating success of exposed and nonexposed males when courting normal females versus females whose ability to sense pheromones has been altered would offer rigorous evaluation of this hypothesis.

ACKNOWLEDGMENTS We thank Roger Coralis for permission to conduct fieldwork at the agricultural station, Erik Rutka and Mindy Teruya for assistance in the laboratory and field, James Duke, Ritsuo Nishida, Guadalupe Rojas, Fran Webster, and Silvia Young for information on α-copaene, and Bill Eberhard, Don McInnis, and Nikos Papadopoulos for helpful discussions. This research was supported in part by a grant from the Binational Agricultural Research and Development (BARD Project No. US-3256-01) to B. Yuval and T.E.S.

REFERENCES Bradbury, J. W., and Gibson, R. M. (1983). Leks and mate choice. In Bateson, P. (ed.), Mate Choice, Cambridge University Press, Cambridge, pp. 109–138. Field, S. A., Kaspi, R., and Yuval, B. (2002). Why do calling medflies (Diptera: Tephritidae) cluster? Assessing the empirical evidence for models of medfly lek evolution. Fla. Entomol. 85: 63–72. Flath, R. A., Cunningham, R. T., Mon, T. R., and John, J. O. (1994a). Males lures for Mediterranean fruit fly (Ceratitis capitata Wied.): Attractants from angelica seed oil (Angelica archangelica L.). J. Chem. Ecol. 20: 1969–1984. Flath, R. A., Cunningham, R. T., Mon, T. R., and John, J. A. (1994b). Males lures for Mediterranean fruit fly (Ceratitis capitata Wied.): Structural analogues of α-copaene. J. Chem. Ecol. 20: 2595–2609. Greenfield, M. D. (1997). Sexual selection in resource defense polygyny: Lessons from territorial grasshoppers. In Choe, J. C., and Crespi, B. J. (eds.), The Evolution of Mating Systems in Insects and Arachnids, Cambridge University Press, Cambridge, pp. 75–88.

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