International Journal of Tropical Science Vol. 28, No. 1, pp. 12–18, 2008 DOI: 10.1017/S1742758408901363 q icipe 2008

Age-related responsiveness of male Bactrocera latifrons (Diptera: ) to a-ionol 1 cade oil relative to age of sexual maturity

Grant T. McQuate1*, Aime´ H. Bokonon-Ganta2, Eric B. Jang1 and Russell H. Messing2 1USDA-ARS-PBARC, US Pacific Basin Agricultural Research Center, PO Box 4459, Hilo, HI 96720, USA: 2Department of Plant and Environmental Protection Sciences, College of Tropical Agriculture and Human Resources, University of Hawaii, Honolulu, HI 96822, USA

(Accepted 23 November 2007)

Abstract. Bactrocera latifrons (Hendel) is a tephritid fruit fly of primarily Asian distribution that became established in Hawaii in 1983 and recently invaded Africa, being detected in Tanzania in 2006 and in Kenya in 2007. Although males of the majority of dacine fruit flies respond to either methyl eugenol or cuelure, B. latifrons shows little to no response to these lures. Instead, B. latifrons males respond to a-ionol þ cade oil. Male age-related responsiveness to a-ionol þ cade oil (using wind tunnel bioassays) relative to the age of sexual maturity (assessed through spermathecal dissections) was documented using wild B. latifrons adults. Relative to the peak response observed at day 28, males exceeded 50, 75 and 90% of the peak response at days 7, 14 and 21, respectively. No females younger than 16 days old were mated. Based on a sigmoidal regression of the percentage of inseminated females versus age, 50% of females were inseminated when 18.8 days old, with the percentage increasing to 75 and 90% at 19.8 and 20.9 days of age, respectively. At 24 days and older, 100% of females were mated. The observation that no female B. latifrons were mated by day 14, while 14-day-old male flies achieved over 75% of the peak response to a-ionol þ cade oil, suggests that a-ionol þ cade oil mass trapping has some potential to remove males from the field before they can contribute to increasing field populations through matings, as previously found with the oriental fruit fly, B. dorsalis (Hendel), and its respective male lure, methyl eugenol. The effectiveness of the removal of males before they mate, though, would be expected to be less for B. latifrons than the male annihilation achieved in the use of methyl eugenol with B. dorsalis because the male lure for B. latifrons is weaker overall.

Key words: Bactrocera latifrons, Tephritidae, alpha-ionol, cade oil, mating, male annihilation

This article reports the results of research only. Mention of a proprietary product does not constitute an endorsement or a recommendation by the USDA for its use. *E-mail: [email protected] Age-related response of B. latifrons to male lure 13 Introduction responsiveness to a-ionol þ cade oil relative to their age of sexual maturity. Bactrocera latifrons (Hendel) (Diptera: Tephritidae) is a tephritid fruit fly of primarily Asian distribution (e.g. Pakistan, India, Sri Lanka, Materials and methods Burma, China, Thailand, Laos, Vietnam, Malaysia, Singapore, Taiwan, Brunei; Carroll et al., 2002 Chemicals onwards). Also, it is the most recent alien tephritid a-Ionol (4-(2,6,6-trimethyl-2-cyclohexen-1-yl)-3- fruit fly species to become established in Hawaii, buten-2-ol) was obtained from Bedoukian Research, with the first detection in 1983 (Vargas and Inc. (Danbury, Connecticut, USA). Rectified cade oil Nishida, 1985) and has recently invaded the was obtained from Penta Manufacturing Company continent of Africa, being detected in Tanzania in (West Caldwell, New Jersey, USA). 2006 (Mwatawala et al., 2007) and in Kenya in 2007 (De Meyer et al., 2007; S. Ekesi, ICIPE, personal communication). Following its discovery in Hawaii, it has spread throughout the state (Liquido All B. latifrons adult flies used in this study were et al., 1994). It primarily infests solanaceous fruits recovered from wild turkeyberry Solanum torvum but has also been found to infest some cucurbitac- (Sw.) fruits collected from the vicinity of Haiku eous fruits (Liquido et al., 1994). Although, at on the island of Maui, Hawaii. The fruits were present, little economic damage has been attrib- transported to the laboratories at the Pacific uted to this species in Hawaii, it is considered a Basin Agricultural Research Center on the island quarantine pest resulting in the requirement for of Hawaii and subsequently held in screened costly quarantine treatments for any host fruits buckets with sand on the bottom to serve as a shipped from Hawaii. It has the potential to impact pupation medium. Sand was sieved weekly for the production of solanaceous crops such as peppers recovery of pupariating larvae and pupae, which (Capsicum annuum L. and Capsicum frutescens L.), were then placed in screened-top cups and held in aubergine (Solanum melongena L.) and tomatoes the laboratory at an average (^SEM) temperature (Lycopersicon esculentum Mill.), crops identified for of 22.7 (^0.1) 8C, relative humidity (^SEM) of diversified agriculture in the state. 56.9 ^ 0.4%, and a photoperiod of 12:12 (L:D) h. Although males of the majority of dacine fruit fly emerging on a given day were removed and species respond to either methyl eugenol or cuelure grouped in 1.0-l screened-top containers, 10 females (Drew, 1974; Drew and Hooper, 1981; Cunningham, and 15 males of the same age (for the ‘Age of Sexual 1989; Metcalf, 1990), B. latifrons shows little to no Maturity’ study), or all held in a separate bucket (for response to these lures. Instead, B. latifrons responds the ‘Age-Related Responsiveness to a-ionol þ Cade to a-ionol (Flath et al., 1994), with the response Oil’ study). Adults were fed water, sucrose and a synergistically enhanced by the addition of cade oil ‘protein cake’ (consisting of one part protein yeast (Liquido et al., 2000; McQuate and Peck, 2001; hydrolysate (Enzymatic, United States Biochemical McQuate et al., 2004). Several important aspects Corporation, Cleveland, Ohio, USA), and 0.5 part have yet to be studied for this male attractant. One torula yeast (Lake States Division, Rhinelander is the relationship between male age-related Paper Co., Rhinelander, Wisconsin, USA)) until the responsiveness to a-ionol þ cade oil and the age time of use in the studies. of sexual maturity. Wong et al. (1989) documented that 40–50% of oriental fruit fly, Age of sexual maturity (Hendel), males responded to its male lure, methyl eugenol, before any became sexually mature, The sex ratio used for the ‘Age of Sexual Maturity’ making it possible to remove males from the field study provided an overabundance of males to before they could contribute to increasing field ensure adequate opportunity for mating and populations through matings (‘male annihilation’). permitted up to 50% mortality of females, while By contrast, melon fly, Bactrocera cucurbitae still ensuring the availability of five females for (Coquillett), males respond to their male lure, testing. Co-mingling of males and females is the cuelure, at a later stage in their sexual maturation typical situation in wild flies, and it has been shown than do oriental fruit fly males to methyl eugenol, in some tephritid fruit fly species that the presence allowing males to contribute more to population of males can accelerate sexual maturation in growth before being attracted to the male lure, females (Pritchard, 1970; Pereira et al., 2006). thereby decreasing the potential of male annihil- Spermathecae were removed from five randomly ation to reduce melon fly populations (Wong selected female flies from each bucket and placed et al., 1986, 1991). Here, we report on research on a glass slide with a drop of Hank’s Balanced Salt results that document male B. latifrons age-related Solution (Hanks and Wallace, 1949; prepared 14 G.T. McQuate et al. without MgCl2·H2O, MgSO4·7H2O, CaCl2, NaHCO3 transformation of the percentage data (Sokal and or phenol red). Spermathecae were then smashed Rohlf, 1981), with Tukey’s HSD used for separation of and observed under a compound microscope at means (SAS Institute Inc., 2002). Using regression 40 £ magnification for the presence of live sperm. analysis, both the increase in percentage sexual Flies from five buckets (a total of 25 flies) were maturity with age and the increased male lure tested for ages 14–26 days old, at 2-day intervals. In response with age were fitted to four-parameter this study, we define the age of sexual maturity as sigmoidal curves of the form: the age at which live spermatozoa were recovered from dissected females. This clearly documents a male sexual maturity, but only indicates mating y ¼ y0 þ 1 þ e 2ðage2x0=bÞ status of females because ovarian development was not examined and the presence of mature oocytes in an ovary is regarded as the definitive character for where y is the percentage sexual maturity or female sexual maturity (Kendra et al., 2006). percentage male lure response, and a, b, x0 and y0 However, experience with Bactrocera spp. in Hawaii are all computed parameters. The significance of the has been that when females mate, mature or fit to the curves was tested by ANOVA (SPSS, 2002). very close to mature ovaries are found and females can lay eggs very soon after mating (D.O. McInnis, Results personal communication). Age of sexual maturity Age-related responsiveness to a-ionol þ cade oil The percentage of mated flies, by age, is presented, Male B. latifrons age-related responsiveness to together with the fitted sigmoidal curve, in Fig. 1. a-ionol þ cade oil was determined through the There were significant differences in the percentage use of a rectangular glass flight tunnel as described of mated females among the ages 16, 18, 20 and 24 by Jang and Light (1991) and Jang et al. (1994). days old. The sigmoidal curve generated to relate Twenty male flies of a given age group were the increase in age to the percentage of mated females was highly significant (F ¼ 175.9, df ¼ 3, 6; released between 1300 and 1330 h at the downwind 2 end of the 2.8 £ 0.9 £ 0.9 m tunnel from a platform P ¼ 0.0007), with an r of 0.99. No mated females situated at mid-height of the tunnel (40.5 cm). Each were found younger than 16 days old. Based on the of 14 age groups (ages 2–28 days, in 2-day generated sigmoidal curve, 50% of the females were intervals) was tested. Two Jackson traps, each mated by 18.8 days old, with the percentage holding sticky inserts, were suspended behind increasing to 75 and 90% by 19.8 and 20.9 days (upwind of) Hawaiian chilli pepper C. frutescens old, respectively. At 24 days and older, 100% of the plants placed, side by side, at the upwind end of females were inseminated. the tunnel. Each trap held a 2.5 cm long £ 0.5 cm diameter cotton wick that was baited with 0.15 ml Age-related responsiveness to a-ionol þ cade oil water in one trap (control) and with 0.1 ml a-ionol at one end of the wick and 0.05 ml cade oil at the The average catch of males caught in control other end of the wick in the other trap (treatment). and treatment traps versus fly age is presented in Lighting inside the tunnel averaged 2760 lux using Table 1. The average percentage adjusted catch, eight overhead 60-W fluorescent lights set with a calculated by adjusting the catch by subtracting the photoperiod of 12:12 (L:D) h. The airflow in the control trap catch from the treatment trap catch, tunnel during the light phase was 0.15 m/s, but then dividing that adjusted catch by the number of was stopped over the course of the dark phase. flies released and then multiplying by 100, together Inserts were retrieved after 24 h and the number of with the fitted sigmoidal curve, is presented in trapped flies counted. Total response was calcu- Fig. 2. Because of high variability in response at lated as the difference between flies recovered in most ages, only differences between age 2 and ages the treatment and control traps. Each fly age tested 18, 24 and 26 are significantly different from each was replicated a total of four times, with relative other. However, the trend for increased response position of the treatment and control traps over time is apparent and the sigmoidal curve reversed for half of the replicates. generated to relate the increase in age to the male lure response was significant (F ¼ 9.79, df ¼ 3, 13; P ¼ 0.0025), with an r 2 of 0.75. Peak response of Statistical analysis 45.0% occurred after 28 days. When comparing Significance of differences, by age, in percentage response data from the fitted curve with the peak sexual maturity and percentage response to a-ionol þ response observed at day 28, male response cade oil were tested by ANOVA, following arcsine exceeded 50% of the peak response by day 7 and Age-related response of B. latifrons to male lure 15

Fig. 1. Average percentage (^SEM) of mated female Bactrocera latifrons by fly age, with sigmoidal regression line of the observed response (r 2 ¼ 0.99, P ¼ 0.0007). Points with different letters are significantly different by Tukey’s HSD (P ¼ 0.05) exceeded 75 and 90% by days 14 and 21, before they can contribute to increasing field respectively. populations through matings, as is the case with methyl eugenol and oriental fruit fly (Wong et al., Discussion 1989). Although attraction to methyl eugenol in the B. dorsalis Although no female B. latifrons were found to complex (e.g. (Drew and Hancock), B. dorsalis (Hendel), Bactrocera opiliae be mated by 14 days old, 14-day-old male (Drew and Hardy), Bactrocera papayae (Drew and flies achieved over 75% of the peak response to Hancock)) has been found to be strongly correlated a-ionol þ cade oil. These results suggest that with the onset of sexual maturity (Umeya et al., a-ionol þ cade oil trapping has some potential to 1973; Fitt, 1981; Wong et al., 1986, 1989; Wee and Tan, remove significant numbers of males from the field 2000), with a significant level of response before full sexual maturity, we are not aware of any tests conducted for other methyl eugenol-responding Table 1. Average catch (^SEM) of Bactrocera species outside of the B. dorsalis complex. The latifrons males in control traps and traps treated effectiveness of this as a suppression technique for with a-ionol þ cade oil at ages ranging from 2 to 28 B. latifrons populations, however, is unlikely to days old. Each average is based on four replicates match that of methyl eugenol-based trapping Average (SEM) male catch (‘male annihilation’) for suppression of oriental fruit fly populations because the strength of age Control traps Treated traps response of male B. latifrons to a-ionol þ cade oil 2 1.00 (0.41) 2.00 (0.91) is considerably less than the response of male 4 1.00 (0.71) 5.50 (2.33) oriental fruit flies to methyl eugenol. 6 2.00 (0.91) 3.50 (0.96) Based on the data generated in outdoor screened 8 1.00 (0.41) 6.50 (0.65) cages, wild oriental fruit fly (Wong et al., 1989) and 10 1.50 (0.87) 8.25 (1.65) wild melon fly (Wong et al., 1991) did not reach 50% 12 0.75 (0.48) 7.50 (0.29) of their peak male lure response until over 12 and 13 14 1.00 (0.00) 5.25 (1.89) days old, respectively. The response of B. latifrons to 16 1.75 (0.75) 8.00 (1.00) a-ionol þ cade oil in our study seems to develop at 18 0.75 (0.25) 9.25 (0.85) a younger age than does the comparable response 20 1.00 (0.41) 8.75 (1.55) of B. dorsalis to methyl eugenol and B. cucurbitae to 22 1.50 (0.50) 8.50 (1.66) cuelure. We found over 50% of the peak response 24 0.50 (0.50) 9.00 (2.80) for B. latifrons when 7 days old. The respective 26 0.50 (0.29) 9.00 (1.29) responses, however, became more similar for the 28 0.25 (0.25) 9.25 (2.17) higher percentages of peak response, with 75% of 16 G.T. McQuate et al.

Fig. 2. Average adjusted percentage male Bactrocera latifrons response (^SEM), by age, to Jackson traps holding a cotton wick baited with 0.1 ml a-ionol and 0.05 ml cade oil, with sigmoidal regression line of the observed response (r 2 ¼ 0.75, P ¼ 0.0025). Catch adjusted by subtracting control catch from treatment catch. Points withP different letters are significantly 4 different by Tukey’s HSD (P ¼ 0.05). Average adjusted percentage male response is i¼1100ðxti 2 xciÞ=20 =4, where xt is the number of flies caught in the treatment trap and xc is the number of flies caught in the control trap peak response reached by 17 days for both B. females, and/or the possibility of multiple insemi- dorsalis and B. cucurbitae (compared with 14 days for nations by early maturing males, apply to studies B. latifrons) and over 90% of peak response reached published for other Bactrocera spp. as well, because by 21 days by B. dorsalis and by 20 days by B. the assessments of age-related responsiveness of cucurbitae (compared with 21 days for B. latifrons). males versus age of sexual maturity for B. dorsalis In order to confirm the results presented here, it (Wong et al., 1989) and B. cucurbitae (Wong et al., would be helpful to repeat the age of sexual 1986) were also based on group pairings of male maturity study using single pairs of males (of and female flies of the same age. varying ages) with females of age known to be One issue that remains to be tested is whether mature and receptive. This would permit assessing female B. latifrons will respond to a-ionol þ cade oil the age of sexual maturity under conditions where when males become scarce, as has been observed the males could mate whenever they become for oriental fruit fly females in response to methyl sexually mature, even if they become sexually eugenol (Christenson, 1963; Steiner et al., 1965) mature before the females. If males do become and Mediterranean fruit fly Ceratitis capitata sexually mature at a younger age than females, then (Wiedemann) females in response to trimedlure the results presented here may underestimate the (Nakagawa et al., 1970, 1981), but not for melon fly percentage of males mating. The amount of under- females in response to cuelure (Wong et al., 1991). estimation, if any, is unknown for the different ages However, since the male lure response of B. latifrons tested. By conducting repeat tests with single male– is more similar to that of oriental fruit fly than female pairs, it would also eliminate the possibility melon fly, based on the presence of eugenol as that insemination of females was because of an active ingredient in cade oil (McQuate et al., multiple matings with only the first several males 2004), as well as in the results presented here, we to become sexually mature. If multiple matings by hypothesize that female B. latifrons may behave only a limited number of males led to the observed similarly to female oriental fruit flies under condi- insemination, then the results reported here would tions of male scarcity. overestimate the percentage of males mating. In any case, the results presented here do provide a Conclusion measure of female receptiveness within a small population of male and female flies. It should be Relative to the peak response to a-ionol þ cade oil noted, though, that the concerns for the possibility observed at 28 days old, adult wild male B. latifrons that males may become sexually mature before response exceeded 50 and 75% of the peak response Age-related response of B. latifrons to male lure 17 at 7 and 14 days old, respectively, while no wild Flath R. A., Cunningham R. T., Liquido N. J. and females younger than 16 days old were mated. The McGovern T. P. (1994) Alpha-ionol as attractant for observation that no female B. latifrons were mated trapping Bactrocera latifrons (Diptera: Tephritidae). by day 14, while 14-day-old male flies achieved Journal of Economic Entomology 87, 1470–1476. over 75% of the peak response to a-ionol þ cade oil, Hanks J. H. and Wallace R. E. (1949) Relation of oxygen suggests that a-ionol þ cade oil mass trapping and temperature in the preservation of tissues by has some potential to remove males from the refrigeration. 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