Entomologia Experimentalis et Applicata 82: 181–188, 1997. 181c 1997 Kluwer Academic Publishers. Printed in Belgium.

Response of Ceratitis capitata to citrus chemicals under semi-naturalconditions

B. I. Katsoyannos, N. A. Kouloussis1 & N. T. PapadopoulosUniversity of Thessaloniki, Department of Agriculture, Laboratory of Applied Zoology and Parasitology, 54 006Thessaloniki, Greece1Technological Educational Institution of Thessaloniki, Department of Plant Production, Laboratory ofEntomology, P.O. Box 14561, 5410 01 Thessaloniki, Greece

Accepted: September 24, 1996

Key words: Ceratitis capitata, Diptera, Tephritidae, fruit flies, host selection, chemical stimuli, citrus

Abstract

Responses of Mediterranean fruit fly Ceratitis capitata (Wiedemann) (Diptera: Tephritidae) adults to chemicalsfrom citrus fruits were quantified in choice tests conducted in large field cages housing naturally planted orangetrees, on the Greek island of Chios. Both sexes responded strongly to chemicals released from artificial cuts madein the pulp of peeled oranges and also to natural or commercial orange juice applied to the surface of yellow7.0 cm diameter spheres. Males also responded strongly to chemicals released from cuts made in the oily regionof the orange peel, or flavedo and less to sour orange and lemon. In contrast, females did not respond to flavedochemicals. Male response to peel chemicals occurred throughout the day and increased as the number of cuts perfruit increased from 2 to 8. Contact of male mouthparts with sap from cuts, and mating attempts between males onor near the cuts were frequently observed. The males also responded to commercial essential orange oils appliedto yellow spheres, but less to essential mandarin oils. The role of citrus chemicals in host finding behaviour ofC. capitata and their potential use for the development of effective traps for monitoring and controlling the fly arediscussed. The experimental method followed in this study can be used as a standard technique for evaluation ofthe quality of flies to be used in sterile insect technique programmes.

Introduction

Resource-finding behaviour in insects is the product ofresponses to an array of sensorial information from theenvironment which interact simultaneously or sequen-tially. Tephritid fruit flies use both olfactory and visualcues to seek and assess habitat, food, and ovipositionalresources (Prokopy & Roitberg, 1984; Prokopy, 1986;Katsoyannos, 1989b). The chemical cues associatedwith host fruits have been well documented to playa crucial role in mediating behavioural steps leadingto host finding and oviposition (Fletcher & Prokopy,1991).

The Mediterranean fruit fly (medfly), Ceratitis cap-itata (Wiedemann), is a polyphagous tephritid thatattacks the ripening fruit of numerous commerciallyimportant fruit crops (Liquido et al., 1991). Because

of this wide host range and an ability to exist in avariety of climates, C. capitata is considered one ofthe world’s most destructive agricultural pests and onethat will continue to expand its range of geographicaldistribution (Carey, 1996). As a consequence, much ofthe research on this insect is aimed at the improvementof control methods and the development of attractantsto be used for population monitoring, quarantine andsurveillance.

The dependence of C. capitata on both olfactoryand visual cues when searching for resources has beenwell documented (Nakagawa et al., 1978; Teranishiet al., 1987; Katsoyannos, 1989a; Light et al., 1992).The role of olfactory cues in resource location hasbeen investigated in numerous studies dealing withthe response of adults to host-plant derived chemicals,including chemicals from various citrus fruits (Steiner

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et al., 1957; Teranishi et al., 1987; McIniss & WarthenJr., 1988; Warthen Jr. & McIniss, 1989), and in extens-ive electroantennogram studies with plant volatiles(Light et al., 1988; Levinson et al., 1990; Light etal., 1992). Despite the wealth of data involving chem-icals, there is a lack of behavioural evidence from fieldstudies and several questions concerning the responseof the medfly to chemicals remain unanswered. Forexample, it is unclear whether chemicals from certainhost fruits elicit similar (Light et al., 1988; 1992) ordifferent responses (Levinson et al., 1990) from thetwo sexes.

Behavioural studies on the medfly involving citrusfruits are even more limited. Teranishi et al. (1987)observed male attraction to odour from oranges andsuggested �-copaene as the active compound without,however, supporting these observations with quantit-ative data. In a recent field study, Papaj et al. (1989)showed that medfly females were more likely to landon and attempt to oviposit into oranges that were arti-ficially pricked than into unpricked control oranges.Deep wounds that pierced the fruit pulp and causedthe release of juices elicited more female landings thanshallow ones that pierced only the flavedo. In anotherstudy, Levinson et al. (1990) tested the response of alaboratory strain of medflies to certain fruits, includ-ing Citrus spp., and inferred that fruit volatiles werenot essential for the location of those fruits by theflies. However, in the same study electrophysiologic-al recordings from olfactory sensilla on the antennalfuniculi revealed that essential oils of orange and lem-on fruits provide more olfactory stimuli to females thanto males.

In this study we evaluated behavioural responses ofboth sexes of wild medflies to citrus fruit peel and pulpchemicals under semi-natural conditions.

Materials and methods

Generalities. The study was conducted during thesummers of 1993 and 1994 on the island of Chios,Greece, in a citrus orchard used previously used formedfly studies (Hendrichs et al., 1991; Katsoyannos,1987; 1989a; Papaj et al., 1989). Although citrus fruitsare harvested annually in that orchard, managementpractices are minimal and pesticides have not beenapplied for many years. At the time of experimenta-tion, fruits were unripe or ripening. Fruit used in theexperiments were collected from this orchard.

Field cages. Two cylindrical (2 m high, 2.6 m diam),plastic-screen field cages were used for the experi-ments, each housing a 20-year-old sweet orange tree(Citrus sinensis Osbeck) of 2.2–2.5 m canopy diameter.Leaves of each caged tree were appropriately thinned toallow easy access and observation inside the cage. Alloranges were removed. Wet cotton balls were placedin 3–4 branches of each tree to provide water for theflies. Additional water was sprayed on the trees with ahand atomiser several times per day. A 1–2 mm thicklayer of a semi-liquid food mixture of yeast enzymatichydrolysate and sugar was applied by hand to severalplaces on the tree branches and foliage and allowed todry. A light to moderate northerly wind blew throughthe cages during most days of the study and temperat-ure ranged between 26 and 33 �C.

Flies used. Flies originated from pupae obtainedfrom naturally infested sour oranges (Citrus aurantiumL.) were collected from orchards in the area. Adultswere kept in 40 � 40 � 60 cm organdy gauze netcages with wire frames and provided with water anda piece of cloth soaked in the semi-liquid food mix-ture described above. These cages contained groups of200–300 individuals of one or both sexes. Other exper-iments conducted in the same orchard showed that themajority of females in the wild population started ovi-positing after 8 days, by which time more than 90%of both males and females had mated (Katsoyannos,unpubl.). Thus, adults of 8 or more days old were con-sidered mature in this study. Females of 8 days, cagedwith males since emergence, were considered mated.

All flies used in the experiments were 1–12 daysold. To conduct a test, 200 mated or unmated flies of agiven age and sex were introduced into each field cagethe evening before the initiation of the test. During anexperimental day, the same flies were subjected to upto 8 replicates of various treatments. Most experimentswere replicated more than 10 times.

Response to peel and pulp chemicals. To assessresponse to peel chemicals from the outermost oilyregion of the peel (flavedo), uninfested, ripening souroranges, sweet oranges and lemons (C. limon L.) werewounded by removing a ca. 0.5 mm deep disk of peeltissue at 5 different positions (unless otherwise men-tioned) on each fruit with a sharp razor. Each removeddisk left a fruit surface area of approximately 3 cm2,which contained an average of 240 severed oil glandsin the flavedo (s.d. = 41.3, n=15), provoking the releaseof peel oil components. To assess the response to pulp

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chemicals (the part of the fruit containing the juice ves-icles), ripening oranges were peeled and the peel wasdiscarded. Subsequently, a ca. 2 mm deep disk of pulptissue (surface area approx. 3 cm2) was removed fromfive different positions in each fruit. Each removed diskleft a fruit surface area containing an average of 115severed juice vesicles (s.d.= 21.3, n=15), provoking theexudation of juice and the release of juice components.

To conduct a test, fruits and flies were intro-duced into the field cages immediately after fruitswere treated. Fruits were suspended from their stalksby 10 cm long wires in shadowed areas on the treebranches, usually 1–2 m apart, and at a height of about1.5 m above ground and a distance of about 1 m fromthe tree trunk. On each tree were suspended four fruits,of which one or two were untreated (controls). Fif-teen minutes after the introduction of the fruits intothe cages, the numbers of insects on each fruit werecounted. Then, the flies were gently blown away andthe fruits were removed from the cages. Counts ofresponding flies were supplemented by direct observa-tions of fly behaviour made by an observer inside eachcage. Each replicate was initiated at least one hour afterthe termination of the previous one, and the positionsof the treatments were rerandomised. All tests wereconducted between 0900 and 1800 h because prelim-inary tests showed that flies responded to the varioustreatments with similar intensity throughout this peri-od.

Evaluation of essential oils and juices. A 3 cm diam,0.5 cm thick piece of cotton wool was treated with 0.5ml of essential oil from either mandarin (Citrus reticu-lata Blanco), orange or lemon fruit. The oils were pur-chased from the local citrus-juice industry. The cottonwas then gently rubbed onto the surface of a plastic,yellow, 7.0 cm diam hollow sphere and then attached tothe upper part of the sphere. Two such spheres and twountreated controls were suspended from a caged tree bya 10 cm long wire. The experimental procedure follow-ing thereafter is described above. After each replicate,the spheres were thoroughly washed. A similar proced-ure was followed to test responses to juice from freshlysqueezed oranges collected from the study orchard orto orange juice sold at the local market (Amita, Hellen-ic Bottling Company S.A., Maroussi, Greece). One mlof juice was used for each treated sphere per replicate.

Results

Medfly response to citrus peel chemicals

Response to fruits with peel cuts. To test whether fliesrespond to peel chemicals from the flavedo of oranges,males or females were given a choice of oranges withor without five peel cuts. Males were sighted often ontreated oranges and very rarely on controls, exhibitinga statistically significant positive response to chem-icals from the cuts (Table 1). Males were frequentlyobserved lowering their head and contacting the sapfrom the cuts with their mouthparts. Male homosexualactivity (mating attempts) on or near the cuts was alsocommonly observed.

Direct observations revealed none to few males onthe control fruits throughout the 15-min test period.Upon introduction of the fruits, males exhibited anexcited behaviour and several of them landed on thetreated fruits within 1–2 min. After landing on treatedfruits, most individuals remained there throughout the15-min period. Only occasionally would a male departfrom a treated fruit, most often after being disturbedby another male. These observations strongly suggestthat flies were attracted from a distance to propertiesof the treated fruit, and thereafter arrested on it. Sincemost flies responded concurrently and exclusively tothe treated fruits, the possibility that flies responded tothe presence of other flies on the fruits is remote.

In contrast, virgin or mated mature females vis-ited the treated and the control oranges at equal rates,displaying no heightened response to peel chemicals(Table 1). Direct observations showed that none of thefew females recorded on fruits was exploiting the peelcuts for oviposition or other purposes. These resultsdemonstrate a marked disparity between males andfemales in their responses to peel chemicals.

When given a choice of orange, sour orange orlemon, all with peel cuts, sexually immature, unmatedmales responded strongly to chemicals of orange andless to sour orange, whereas mature, mated males werealso slightly sensitive to chemicals of lemon (Table 2).In contrast, immature, mated and unmated femaleswere not responsive to peel chemicals from any fruits.These results further demonstrate a strong differencein responses between the sexes.

Male response in relation to the number of peel cuts.When given a choice of oranges with 8, 4, 2 or 0 peelcuts, males exhibited a decreased response as the num-ber of cuts per fruit decreased. The average response

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Table 1. Field cage response of C. capitata to peel chemicals from ripeningoranges bearing five superficial disk cuts in the flavedo (200 males or femaleswere used per replicate; the duration of the bioassay was 15 min)

Exper- Sex, age, No. of Mean no.1 responding

iment mating status replicates to oranges with

Flavedo cuts No cuts

1 Males, 8–12 days 10 34.5a 0.2b

old, mated

2 Females, 8–12 days 10 5.2a 3.8a

old, unmated

3 Females, 8–12 days 14 0.9a 1.4a

old, mated

1Means in each experiment followed by the same letter are not significantlydifferent at the 0.05 level (paired t-test).

Table 2. Field cage, choice response of C. capitata to peel chemicals from different ripening citrusfruits bearing five superficial wounds in the flavedo (200 males or females were used per replicate;the duration of the bioassay was 15 min)

Exper- Sex, age, No. of Mean no.1 of flies responding to:

iment mating status replicates Orange Sour orange Lemon Control2

1 Males, 1–2 days 9 26.1a 5.7ab 1.0b 0.3b

old, unmated

2 Males, 8–12 days 8 23.1a 11.1b 4.7bc 0.3c

old, mated

3 Females, 1–2 days 6 0.5a 1.3a 0.0a 2.3a

old, unmated

4 Females, 8–12 days 6 1.0a 2.5a 0.0a 4.2a

old, mated

1Means in each experiment followed by the same letter are not significantly different at the 0.05level (Tukey’s HSD test). 2Untreated orange.

(number of flies/fruit � s.e.) recorded was 25.8�11.0,12.9�10.8, 6.9�4.6 and 0.4�0.7, respectively (10 rep-licates per treatment using 200 mated males of 8–12days of age per replicate). The differences in responsesto fruits with 8 cuts and fruits with 4, 2 or zero cutswere significant, as were the differences between 4 andzero cuts. This suggests that, within the range tested,attractiveness of oranges was considerably elevated byincreasing the number of cuts (i.e., the quantity ofreleased chemicals).

Male response to peel cuts in relation to fruit ripe-ness. When unripe oranges (dark green colour, ca.4–5.5 cm diam) with cuts in the flavedo were com-

pared to ripening oranges (green to yellow colour, ca.7–8 cm diam, susceptible to oviposition), or over-ripe oranges (still on the trees from the previous crop,orange colour, ca. 7–8 cm diam) with similar cuts,the differences in male responses were not significant.However, males showed a slight tendency to land moreoften and to stay longer on ripening oranges. The aver-age response (number of flies/fruit � s.e.) recordedwas 25.4�9.3 males on ripening oranges, 17.7�11.6on unripe oranges and 17.8�15.3 on overripe oranges(11 replicates per treatment using 200 mated males of3–8 days of age per replicate).

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Table 3. Field cage response of C. capitata to 7.0 cm diam spheres treated with 0.5 ml of peel oil fromdifferent citrus fruits (200 males or females per replicate; the duration of the bioassay was 15 min)

Exper- Sex, age, No. of Mean no.1 of flies responding to spheres treated with:

iment mating status replicates Orange oil Mandarin oil Lemon oil Water

1 Males, 3–8 days 8 14.3a 4.4b 2.4bc 0.0c

old, mated

2 Females, 1–8 days 12 0.1a 0.0a 0.0a 0.3a

old, virgin

3 Females, 8–12 days 12 0.0a 0.0a 0.1a 0.4a

old, mated

1Means in each experiment followed by the same letter are not significantly different at the 0.05 level(Tukey’s HSD test).

Medfly response to commercial essential oils fromcitrus

Response to peel oils. When given a choice of spherestreated with commercial essential peel oils of orange,mandarin, or lemon, the degree of male attractiondiffered significantly. Males were particularly respons-ive to orange oil, less sensitive to mandarin oil andalmost unresponsive to lemon oil (Table 3). Virgin andmated mature females displayed very low responses(approximately zero) to all three oils, even lower thanthe response to control spheres. Direct observationsrevealed that females that landed on a control sphere,either accidentally or attracted by the yellow colour,would tend to remain there. On the contrary, the fewfemales that landed on a treated sphere would fly awayimmediately upon touching it with their tarsi, as ifrepelled by the oil on the sphere surface. These resultsagain support the marked disparity between the sexesin responses to peel chemicals.

Male response to various dosages of orange oil. Toevaluate male response to various dosages of orangepeel oil, males were given a choice of 4 spheres treatedeither with 0, 0.1, 0.5, or 1.0 ml of orange oil. Theaverage response (number of flies/sphere � s.e.) was11.3�6.5 males at the 1.0 ml treatment compared to10.8�4.3 at the 0.5 ml treatment, 13.5�7.3 at the 0.1ml treatment, and 0.2�0.5 at the control (8 replicatesper treatment using 200 mated males of 3–8 days old).Although attraction clearly increased with dosages, nosignificant difference between dosages was detected.

Response to citrus pulp chemicals

Response to oranges with pulp cuts. When given achoice of peeled oranges with or without cuts in thepulp, both males and females displayed a strong, pos-itive response (Table 4). Although not directly com-parable, these results suggest that the mature, matedfemales were particularly sensitive, while the mature,unmated ones were less sensitive and the immature,unmated ones were the least sensitive. Direct observa-tions revealed that both sexes would alight on the fruitswith cuts almost immediately and most would remainon the wounds throughout the 15-min period.

Response to orange juice. When given a choice ofspheres treated with natural commercial orange juiceor untreated spheres, both males and females exhibiteda strong preference for the treated spheres (Table 5).Although not directly comparable, the results suggestthat mature, mated females responded in greater num-bers to spheres treated with natural orange juice thandid immature, unmated females. Mouthpart contact byboth males and females with the surface of the treatedspheres was often observed.

Discussion

The present study provides clear evidence that C. cap-itata males respond strongly to chemicals in theflavedo of citrus fruits (especially oranges) and thatthese chemicals elicit no response from females. Thismarked disparity probably reflects differences in eco-logical needs for host-fruit recognition between the

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Table 4. Field cage response of C. capitata to pulp chemicals from peeledripening oranges bearing five superficial wounds in the pulp (200 males orfemales per replicate; duration of the bioassay was 15 min)

Exper- Sex, age, No. of Mean no.1 responding

iment mating status replicates Treatment Control

1 Males, 8–12 days 12 9.3a 2.0b

old, mated

2 Females, 3 days 11 6.0a 0.2b

old, unmated

3 Females, 8–12 days 10 8.7a 1.9b

old, unmated

4 Females, 8–12 days 13 12.2a 1.7b

old, mated

1Means in each experiment followed by the same letter are not significantlydifferent at the 0.05 level (paired t-test).

Table 5. Field cage response of C. capitata to 7 cm diam plastic spheres treated with juicefrom freshly squeezed ripening oranges or commercial orange juice (200 females per replicate;duration of the bioassay was 15 min)

Expe- Juice Sex, age, No. of Mean no.1 responding

riment tested mating status replicates Treatment Control

1 Juice from Males, 8–12 days 12 10.5a 0.8b

squeezed oranges old, mated

2 Commercial Males, 8–12 days 12 14.3a 0.5b

orange juice old, mated

3 Juice from Females, 3–4 days 11 6.0a 0.2b

squeezed oranges old, virgin

4 Juice from Females, 8–12 days 10 12.1a 0.6b

squeezed oranges old, mated

5 Commercial Females, 8-12 days 12 14.8a 0.5b

orange juice old, mated

1Means in each experimenot followed by the same letter are not significantly different at the0.05 level (paired t-test).

sexes. Levinson et al. (1990) recorded electroanten-nograms and found the opposite situation, i.e., thatfemales of C. capitata display more sensitivity thanmales to olfactory stimuli from the essential oils ofcertain fruits, including orange and lemon. This dis-crepancy illustrates the need for caution in interpretingelectroantennogram responses in the absence of beha-vioural data. Although other workers have reportedsimilarities of both sexes in response to various com-

pounds (Light et al., 1988, 1992; Jang et al., 1989),yet dissimilarities were also evident in their resultsin certain cases. For example, Light et al. (1988)recorded electroantennograms from wild C. capitatain response to a range of volatiles, some of which wereknown from leaves and fruits, and observed a stronguniformity in male and female responses. However, 8out of 70 compounds tested elicited significantly higher

187

electroantennogram responses from female than maleantennae.

In the experiments involving flavedo cuts, maleswere often observed lowering their head and contact-ing the wound and the exuding oil with their proboscis.Although males were apparently ingesting exudates, itis very doubtful that they fed on them given that thefield cages were provided with ample food and thatthis behaviour was absent in females. If not for feed-ing, peel substance metabolites could possibly be usedin sex pheromone biosynthesis, as has been impliedby studies on other fruit flies (Nishida et al., 1988;Shelly, 1995). Apart from leaves, males are known toemploy the fruit surface as an alternative site for court-ship and mating (Feron, 1962; Prokopy & Hendrichs,1979; Prokopy & Roitberg, 1984), and it is thus con-ceivable that peel chemicals provide cues for the abovebehaviour as well. The active compounds responsiblefor the above behaviour, as well as for the possibleformation of the sex pheromone, may be related tothe substance �-copaene, which occurs at high levelsin the oil of several plant species, including orange(Teranishi et al., 1987). This compound has power-ful male attractive properties and is considered to bea parapheromone for medflies (Teranishi et al., 1987;Cunningham, 1989).

Lack of female response to chemicals emanatingfrom superficial cuts in the peel may be due to the factthat the essential oils in the flavedo region of citrushave allelopathic effects on the larvae (Greany et al.,1983). Attraction to shallow wounds and use of thesewounds for oviposition increases exposure of offspringto the oils, resulting in reduced hatchability of eggs,enhanced mortality of early instar larvae, and sup-pression of larval growth (Back & Pemberton, 1918;Greany et al., 1983; Carey, 1984). Conversely, ovipos-ition into peel-penetrating wounds enhance egg hatchand larval performance; if larvae are placed directly onthe non-oily pulp of the fruit survival is relatively high(Back & Pemberton, 1918; Carey, 1984). Analogousconclusions were drawn from a field study carried outby Papaj et al. (1989) in the same orchard as the presentstudy. Papaj et al. found that the depth of wounds inoranges, artificially wounded with an insect pin, posit-ively influenced female tendency to land on the fruits.Significantly more wild females were sighted on fruitswith deep pulp-piercing wounds which provoked thesecretion of a small quantity of sap than on fruits withshallow wounds, not piercing the pulp. This finding, aswell as our results, suggest that the positive response offemales to sap may be a significant component of the

behaviour leading to selection of oviposition sites. Innature, females may associate the odour from orangesap with wounds that penetrate the peel and which areconductive to egg and larval survival. Feeding stimuliconcerning both sexes may also be involved.

Trapping experiments, conducted at the sameorchard (Katsoyannos, Kouloussis & Papadopoulos,unpubl.), clearly show that the commercial juice oforange, used as bait in plastic McPhail traps (AgriSenseLtd.), is just as effective in attracting similar numbersof C. capitata males and females as a standard solutionof 9% Nulure (a hydrolysed corn protein), 3% sodiumborate and 88% water. These results suggest that theactive compounds of orange juice, if isolated, identi-fied and synthesised, may prove useful as a monitoringor control tool for C. capitata.

The successful implementation of the sterile insecttechnique against C. capitata requires mass-rearedsterile males that are comparable in behaviour to wildmales and have adequate ability to orient to appro-priate habitats and essential resources (Calkins et al.,1982). The field-cage method of bioassaying chemic-als, described in this paper, is a useful test for monit-oring the behavioural effects of host plants on sterileC. capitata males (Katsoyannos, unpubl.).

Acknowledgements

This research was supported by FAO/IAEA grant7651/RB, EC-AIR3 grant CT92-0300 and the Califor-nia Citrus Reasearch Board. We are grateful to Prof. M.E. Tzanakakis, Prof. J. R. Carey and Ms C. Gruenfeld-er for critically reviewing the manuscript. Also, to DrJ. Hendrichs (IAEA, Vienna) for fruitful discussionsand for providing field cages.

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