Tephritids (true fruit flies) include a large number of species(Mau et al. 2007; Vayssières et al. 2009a, b). Some of them arerenowned world wide, such as the Mediterranean fruit fly, whileothers are more local (Aluja and Mangan 2008). They are one ofthe most diversified groups of insects and ranked high among theworld’s most serious pests of horticultural crops (Billah 2007;Billah et al. 2006). Tephritidae consists of over 4,000 species ofwhich 700 species belong to Dacinea fruit flies (Dhillon et al.2005). About 200 species are economically important and widelydistributed in the temperate, tropical, and subtropical regions ofthe world (Chen et al. 2006; Duyck et al. 2006). They are dividedinto two groups defined by physiological and ecological charac-

teristics (Steck and McPheron 1996). The first group includesunivoltine species that have diapause and located in temperateregions such as the genera Rhagoletis. The second group such asthe genera Anastrepha, Ceratitis, and Bactrocera are multivoltinespecies distributed in tropical regions (Table 1) and do not havediapause (Chen et al. 2006). The genera Anastrepha are highlypolyphagous, using hosts from 18 families of plants in 29 genera(Zucchi 2000). The wide-ranging distribution of the familyTephritidae as well as the elevated adaptive and colonizingcapacity may be related to its reproductive potential, derivingfrom the morphological characteristics developed in the pre-imaginal stage (Morgante 1991). Meanwhile, the Mediterraneanfruit fly (medfly), Ceratitis capitata (Wiedemann), is a world-wide agricultural threat and a main insect pest for many fruit andvegetable plants (Mau et al. 2007). General characteristics arethat it is very mobile, has a high reproductive potential, and

Fazil Hasan ( )Email: fazilento10@gmail.comTel: +91-9528432455

The Korean Society of Crop Science

J. Crop Sci. Biotech. 2012 (September) 15 (3) : 169 ~ 188

REVIEW ARTICLE

DOI No. 10.1007/s12892-011-0091-6

Threats to Fruit and Vegetable Crops: Fruit Flies(Tephritidae) - Ecology, Behaviour, and Management

M. Shafiq Ansari, Fazil Hasan*, Nadeem Ahmad

D/O Plant Protection, F/O Agricultural Sciences, Aligarh Muslim University, Aligarh, 202002, India

Received: October 27, 2011 / Revised: February 18, 2012 / Accepted: May 7, 2012Ⓒ Korean Society of Crop Science and Springer 2012

Abstract

Approximately 4,000 known/described species of fruit flies (Tephritidae) are distributed in tropical, subtropical, and temperateregions of world, out of which 200 species are economically important and damaging/spoiling not only to fruits but also to a numberof vegetable crops. Despite their tremendous importance, a limited amount of information is available on the ecology and behaviourof fruit flies especially when compared to fruit fly species complex. It is necessary to understand the ecology and behaviour beforethe formulation of management strategy. The present review may serves as a baseline data for scientists engaged in fruit fly manage-ment programs. Key themes include: (1) demography and population dynamics and, (2) behaviour (e.g. sexual, mating, oviposition,and feeding). The excess of literature on monitoring and management of fruit flies are available, which includes male sterilizationand annihilation, mass trapping, chemical baits, mating disruption, and biological control. But few of them are easily adopted byusers and give satisfactory control of fruit flies and rest are not easily adopted or if used does not give effective control, because ofthe lack of knowledge about the ecology and behaviour of fruit flies. If the information on population dynamics, behavior, and therelated ecological factors are not jointly gathered, it is almost impossible to carry out an appropriate pest control at the right time andplace. We hope that this synthesis will lay the groundwork for future ecological and behavioural studies of fruit fly species, popula-tions, communities, and control.

Key words: behavioural ecology, fruit flies, management, species complex, tephritidae

Introduction

169

Fruit Flies (Tephritidae) - Ecology, Behaviour and Management

infests high-value crops. It is a native of the tropical regions ofAfrica but gained its common name when Mediterranean immi-grants inadvertently introduced it in Australia. It is now a cosmo-politan insect found in almost all continents: in host tree or veg-etable plantations from tropical regions to about 45 ~ North andSouth latitudes (Al-Jboory 2007). It is highly polyphagous, with350 host plants species belonging to 65 families (Duyck et al.2006; Mau et al. 2007). It is a quarantine insect and thus exporta-tion of fruit is often depending on effective medfly control andpostharvest fruit disinfestations.

The genus Bactrocera includes the orchard fly, Bactroceradorsalis (Hendel), and is economically important, while the sub-genus Zeugodacus includes another economically importantspecies, namely the melon fly, B. cucurbitae (Coquillett)(Vayssières et al. 2007). The tropical fruit fly complex contains75 described species largely endemic to South East Asia (Clarkeet al. 2005) and causes widespread damage to tropical fruits rang-ing from 2.5 to 59% (White 2006; Vayssières et al. 2009a, b).The melon fruit fly, B. cucurbitae, is widely distributed through-out the world damaging 81 host plants and is a major pest ofcucurbitaceous crops with losses varying between 30 - 100%depending upon the crop and season (Dhillon et al. 2005; Diaz-Fleischer and Aluja 2000). Behaviour of B. cucurbitae in relationto oviposition, feeding, and larval feeding and jumping wasreported by Severin (1914) and Queensland fruit fly, B. tryoni(Froggatt) by Allmann (1940, 1941). Myers (1952) and Munro(1953) studied acoustic signals of B. tryoni and their importancein mating behaviour. Later, Martin et al. (1953) observed theeffect of male sexual maturity on female attraction and matingbehaviour of Olive fruit fly, B. oleae (Rossi). Roan et al. (1954)noted that B. dorsalis produced a typical high pitched buzzingsound associated with mating at dusk. The pioneering work byProkopy in the late sixties has had a significant impact on thenature of fruit fly behavioural research viz., visual and olfactoryorientation (Prokopy 1968), mating and oviposition behaviour(Prokopy and Boller 1971; Prokopy and Bush 1973; Prokopy andHendrichs 1979; Rahman et al. 2003) and feeding behaviour(Prokopy 1976). The importance of visual cues has long beenrecognized and there is increasing evidence of the relevance ofolfactory cues (Dalby-Ball and Meats 2000; Jang and Light1996) but the behaviour of fruit flies is still poorly understood.

Integrated pest management (IPM) relies on the accuracy ofthe technique applied to pest population monitoring. Ecologicalfactors in the environment can be classified as physical (temper-ature and humidity), chemical (chemical composition of thesoil), and biological factors (pathogens and pests) (Jiang et al.2001). The ecological factors are crucial to the quality and pro-ductivity of the crop. Therefore, available information on thefruit fly ecology and behaviour has been reviewed in this manu-script to explore the possibilities for successful management ofthis pest in fruit and vegetable crops.

Ecology

Comparative demography and life historyPopulation biology of fruitflies has been well-studied in some

systems (Ricklefs 1990). The relatively constant population size,delayed reproduction, and high adult survival of the fruit flypopulation (Carey and Vargas 1985) showed more ‘‘K-selected”dynamics as compared to more ‘‘r-selected” populations.

Survivorship and age-specific reproductive patterns

Growth, survivorship, and movement are major considera-tions in demographic studies of populations (McPeek and Kalisz

170

Table 1. Fruit flies subject to control action

Scientific NameAnastrepha spp.A. antunesiA. bistrigataA. distinctaA. grandis

A. ludensA. obliqua

A. striata

A. suspensaBactrocera spp.B. albistrigataB. atrisetosaB. carambolaeB. correcta

B. cucumisB. cucurbitaeB. distinctaB. diversaB. dorsalisB. latifronsB. minaxB. musaeB. oleaeB. papayaB. passifloraeB. tryoni

B. zonataCeratitis spp.C. anonaeC. capitataC. catoariiC. cosyraC. punctataC. rosaC. rubivoraDacus spp.D. bivittatusD. ciliatusD. frontalisD. vertibratusRhagoletis spp.R. cerasiR. novaR. pomonellaR. tomatis

Common Name

Inga fruit flySouth American cucur-bit fruit flyMexican fruit flyWest indian fruit fly

Guava fruit flyCaribbean fruit fly

Carambola fruit flyGuava fruit fly

Cucumber fruit flyMelon fruit fly

Orientalis fruit flySolanum fruit flyChinese citrus flyBanana fruit flyOlive fruit fly

Fijan fruit flyQueensland fruit fly

Peach fruit fly

Mediterranean fruit flyMascarene fruit flyMango fruit fly

Natal fruit flyBlackberry fruit fly

Pumpkin flyEthiopian fruit fly

Jointed pumpkin fly

European cherry fruit fly

Apple megot fly

Principle Host(s)

Guava, hog plum Common guavaMango, star-appleCucumber, pumpkin, watermelon

Citrus, mango, peach, apple, avocadoMango, citrus, pear , tropical fruits Common guava, mango, citrus, tropical fruitsCitrus, apple, guava, loquat, tropical fruit and nuts

Syzygium spp., tropical almondCucumber, pumpkin, tomato, watermelonCarambola, mango, chili, pepper Banana, tropical fruitsCitrus, mango, common guavaCucurbits, tomato, papayaCucurbits, avocado, papaya, peach, citrusBread fruit, star-appleCucurbits, pumpkin, guardApple, mango, pear, peach, banana, tomatoSolanaceous crops, egg plant, tomatoCitrusBanana, common guavaOliveGuava, mango, citrus, star fruitAvocado, citrus, mango, papayaApple, avocado, berries, pepper, grape, citrus, peach, tomato, tropical fruitsPeach, apple, papaya, citrus, common guava

Mango, coffee, tropical almond, guavaTropical and temperate fruits and nutsAvocado, pepper, mango, peach, tomatoMango, orange, guava, avocado, peachTomatoApple, common guava, pear, papayaRubus spp.

Melon, cucumber, squash, pumpkinMelon, cucumber, squash, pumpkinCucumber, pumpkin, melonMelon, cucumber, squash, pumpkin

CherriesPepinoApple, sour cherryTomato

Modified from Smith (2001).

JCSB 2012 (September) 15 (3) : 169 ~ 188

1993). Carey (1993) outlined basic approaches and presentedmany case histories of insect demography. To develop bettermanagement strategies for fruit flies, researchers have adoptedapplied demographic analysis to economically important tephri-tid flies (Carey and Vargas 1985; Vargas and Carey 1990). Lifehistory studies have provided great impetus to development ofmodern evolutionary ecology (Ricklefs 1990).

Effects of temperature on development and survival of imma-ture stages of the four Hawaiian species of fruit flies weredescribed by Vargas et al. (1996). They differed most in dura-tion of the egg stage and least pupal stage. Interspecific (Vargasand Carey 1990) and intraspecific (Yang et al. 1994a, b, c) com-parisons of demographic parameters for C. capitata, B. dorsalis,and B. cucurbitae were summarized by Vargas et al. (1997).Comparative studies of the effects of constant temperature onlaboratory-adapted strains reared on an artificial wheat diet indi-cated that adult survival, longevity, fecundity, and intrinsic rateof increase varied with species and temperature (Vargas et al.1997). All species exhibited reductions in survivorship and netreproductive rates at 35:24°C. B. dorsalis produced no fertileeggs in four cohorts reared at 35:24°C. This may have been theresult of poor mating (Vargas et al. 1997). The optimum temper-ature for all species, on the basis of fecundity, was apparently29:18°C. Preoviposition periods and reproductive values at thisfluctuating temperature were more favorable than at constanttemperature (24°C). Highest net reproductive rates (i.e. produc-tion of newborn females per generation) for all species wereobtained at a constant temperature of 24°C (Vargas et al. 1997).

Life history evolution involves the balance between selectionon fecundity and adult survival (Williams 1966). Different lifehistory adaptations are favored under conditions of high and lowpopulation density relative to the carrying capacity of the envi-ronment (Cody 1966). Two contrasting strategies have becomeknown as r- and K-selected traits, respectively, after the variablesof the logistic equation for population growth (Ricklefs 1990,1997). Life history patterns are often characterized as r- or K-selected (Ricklefs 1990). Pianka (1970) hypothesized r-K contin-uum with organisms positioned on it according to differences intheir evolved characteristics. Common attributes of r-selectedspecies are temperate zone distributions, small body size, earlyreproduction, high fecundity, short life span, and a high intrinsicrate of increase; K-selected species commonly exhibit tropicaldistributions, large body size, late reproduction, low fecundity,long life span, and a low intrinsic rate of increase (Pianka 1970).A necessary condition with respect to the r and K concept is thatit is applied relatively with respect to comparison with anotherorganism or group of organisms. Vargas et al. (2000) comparedthree fruit fly species which showed that C. capitata is relativelyr-selected on the basis of small body size, early onset of oviposi-tion, high fecundity, a comparatively short life span, and a highintrinsic rate of increase. However, B. cucurbitae has a largerbody size, exhibits a late onset of oviposition, much lower fecun-dity, greater longevity, and a lower intrinsic rate of increase; it istherefore relatively K-selected. B. dorsalis, with an intermediatesize, exhibits mixed traits: late onset of oviposition and long lifespan were K-selected, whereas high fecundity and a high intrinsic

rate of increase were r-selected. Previous life history and demo-graphic studies of B. latifrons characterized the species as highlyK-selected, with a fecundity 70% less than B. cucurbitae(Ricklefs 1997). Therefore, it was concluded that reproductivepatterns may be useful characteristics for predicting the geo-graphical range for certain groups of tephritid flies.

Ecological implicationsEcological studies of fruit flies have been used to predict

areas where pest species may survive and reproduce. One of themost valuable applications of the “intrinsic rate of increase”concept is in the delineation of the livable environment of aspecies, whereas the distribution maps reveal a broader latitudi-nal range for C. capitata than for B. cucurbitae or B. dorsalis(CAB International Institute of Entomology 1995). C. capitata isdistributed in almost all tropical and warm temperate areas ofthe world. In addition, C. capitata has multivoltine habit with abroad host range of more than 300 host plants. White and Elson-Harris (1992) suggests that r-selected traits allow C. capitata tomaintain a high r-value over a broad range of temperatureregimes. This tolerance may be a potential reason for establish-ment of C. capitata throughout the world, while the carambolafruit fly B. carambolae has been found outside its Oriental rangein Surinam, in the New World, and considered as a tropical.

Demographic parameters of fruit fly populations reared underdifferent temperature regimes also have implications for exam-ining the dynamics of colonizing or invading species. Populationsizes, growth rates, and structure can be projected in relation toenvironmental conditions. Likewise, survival and adult longevi-ty measured under different temperature regimes are importantto understanding fruit fly invasion biology and overwinteringbehaviour (Papadopoulos et al. 1998). These factors becomeimportant when fruit flies are introduced accidentally into newareas and eradication is desirable.

Diapause and seasonalityKnowledge about fruit fly species and their respective sea-

sonalities related to host plant phenology is crucial to understandthe population dynamics of these insects. Fruit infestation isinfluenced by its degree of maturation during the fruit fly ovipo-sition period (Messina and Jones 1990). Foraging differencescan be observed as fruit flies make incursions into fruits of a cer-tain developmental stage. Such information can be obtained bybagging and unbagging fruits throughout their development.

Raspi et al. (2002) conducted a laboratory experiment aimingto verify the role of variable photoperiod on eggs maturation inB. oleae, showing markedly different responses as a function oftreatments administered and providing an explanation of thefindings observed in nature. Most experimental work on theinduction of insect diapause has been carried out using constantphotoperiod and the proportion of population entering diapauseis plotted as a function of daylength. Since the majority ofinsects are summer active, the most frequent photoperiodicresponse curve is the long-day type (the insects develop orreproduce in long days but become dormant in short days),while the short-day type of photoperiodic response characterizes

171

a small number of insect species that are spring-autumn or win-ter-active, and pass the summer in an aestival diapause. In arecent review on seasonal development and dormancy of insectfeeding on olive, Tzanakakis (2003) pointed out that the B. oleaeis adapted to develop best in autumn, when its larval food is atits optimal condition for larval growth. Tzanakakis (2003) sug-gested that the lack of ovarian maturation during late spring-early summer and the laboratory induction of reproductive dia-pause under conditions resembling those of that season showsthat B. oleae is a short-day species (Tzanakakis 2003).

Adult food sourcesFruit flies are well known for their association with bacteria

(Behar et al. 2009; Lauzon 2003) and many species evince mor-phological adaptations for housing bacteria in the digestive tract(Mazzon et al. 2008). B. oleae was the first member of this fami-ly in which an association with bacterial symbionts wasdescribed (Behar et al. 2009; Mazzon et al. 2008) and may bethe most specialized in this regard among fruit-infesting mem-bers of Dacinae and Trypetinae. In adult olive flies, a diverticu-lum of the oesophagus accommodates a large and proliferatingpopulation of extracellular bacteria (Behar et al. 2009; Mazzonet al. 2008). This organ periodically releases bacteria into theoesophagus, which inoculate and densely colonize the anteriormidgut (Capuzzo et al. 2005). Alternatively, the intestinalmicrobiota can provide the metabolic capability to generate thenitrogenous components missing from the diet (Estes et al.2009). This may be achieved by fixing atmospheric nitrogen,recycling nitrogenous waste, or by using the existent nitrogen inthe diet (Behar et al. 2005). Amino acids may then be secretedby bacteria and directly assimilated by the fly as demonstrated inother insect-bacteria associations (aphids; Douglas 1998). Whenconditions in the gut support a high rate of bacterial reproduc-tion, the flies may be realizing their need for protein simply bydigesting the excessive bacterial biomass in the gut (Lemos andTerra 1991). The association extends via the egg and continuesin the larval stage where bacteria heavily populate the fourmidgut caeca during the entire larval development within theolive fruit (Behar et al. 2009). Although recent studies haveidentified several species of bacteria in the digestive tract ofwild olive flies (Estes 2009; Kounatidis et al. 2009) and the mostcommon and widespread of these is Candidatus Erwinia dacico-la (Capuzzo et al. 2005; Estes et al. 2009).

Adults of B. oleae are opportunistic feeders that are notrestricted to feeding on one particular diet and exploit varioussubstrates such as honeydew, nectar, fruit and plant exudates,and occasionally bird droppings and pollen (Drew and Yuval2000). The nutritional value of these food sources may varygreatly, however, the ones considered most important (e.g. hon-eydew, nectar, and plant-derived exudates) are generally rich incarbohydrates but relatively poor in amino acids (Lundgren2009; Wackers 2005). Moreover, in some cases the smallamounts of amino acids that are available may be highly unbal-anced in composition and contain mainly those that are consid-ered non-essential (Douglas 2006; Wackers 2005). Thus, despitetheir seemingly varied choice of foodstuffs, these flies rely on

food sources that are poor and unbalanced in their amino acidcomposition. The low nitrogen content of such a diet seems tocontrast with the nutritional demands of adult olive flies which(like many other long-lived tephritid fruit flies) require a contin-uous external supply of protein in order to achieve their repro-ductive potential (Drew and Yuval 2000). This requirement isparticularly important in females, whose fecundity greatlydepends on the nitrogenous contents of their diet. When peptidesor proteins are not available, a source of essential amino acids isobligatory for oogenesis as B. oleae (like other eukaryotes) areunable to synthesize these compounds (Tsiropoulos 1983).Indeed, in the laboratory, females are unable to adequately syn-thesize protein and to mature eggs if maintained on diets lackingessential amino acids (Tsiropoulos 1983). Proliferation of bacte-ria in the gut and the dependence of adults on essential aminoacids suggested that bacteria have a role in nitrogen metabolism.Many investigations aimed to determine the relationshipbetween nutrition, gut bacteria, and fecundity in other fruit fliessuggest that gut bacteria compensate, at least partially, for aminoacid and vitamin deficiencies in the diet (Behar et al. 2009;Douglas 2006; Wackers 2005).

Tephritids, who share a similar nutritional niche, may be asso-ciated with bacteria for the same reason. Thus, by ingesting avaried diet in the wild, fruit flies have the potential for acquiringthe nitrogen needed for reproduction. However, by simultaneous-ly nurturing a beneficial intestinal microbiota, they gain the abili-ty to continuously subsist on food sources such as honeydew thatare more marginal in terms of their nitrogenous composition.

Population dynamicsKnowledge of insect population dynamics is, to a large

degree, based upon studies of temperate and tropical regioninsects. For practical needs of fruit fly control, the distributionand occurrence of fruit fly has received most attention in recentyears, when agricultural production and trade has been increas-ing rapidly. The seasonal occurrence and food quality displaysthe essential characteristics of the fruit fly population in particu-lar geography and climate. In this section we draw on a few casestudies of fruit flies to illustrate the diversity in populationdynamics through temporal and spatial structures.

Temporal abundanceAbiotic factors like temperature, rainfall, humidity, and light

intensity influence the temporal abundance of fruit flies popula-tion. Ye and Liu (2007) concluded that population fluctuations ofthe B. dorsalis were almost identical during the three study years(1997, 2000, and 2003). Adult population of the fly remained at avery low level from November through February and got higherin the rest of the months. Peak of the population was recorded inJune or July depending on the year. The influence of rainfall onB. dorsalis population involves two aspects. Rainfall less than 50mm or more than 200 mm may suppress population growth.When the monthly rainfall gets higher than 250 mm, the fruit flypopulation would decline remarkably. On the other hand, month-ly rainfall from 50 mm to 200 mm is favorable for populationincrease of B. dorsalis. Rainfall influences population of B. dor-

Fruit Flies (Tephritidae) - Ecology, Behaviour and Management172

JCSB 2012 (September) 15 (3) : 169 ~ 188

salis indirectly through soil water content (Jiang et al. 2001).Mziray et al. (2010) have studied the temporal abundance of

B. latifrons by trapping adult flies in the hosts’ fields and by col-lecting host fruits that were cultured in the laboratory in order todetermine the number of emerged adults. Trap catches were lowwithout definite peaks, even at times when solanaceous hostswere available. Low catches of B. latifrons, despite availabilityof ovipositional resources, was also observed by McQuate andPeck (2001). The low number of adults caught in traps wasprobably due to the low power of the attractant used (McQuateand Peck 2001). The population is being regulated below itsbiotic potential due to larval mortality, parasitism, and other fac-tors (McQuate and Peck 2001).

Host fruits are another main factor influencing B. dorsalisinfestation in Kunming region (Ye 2001). Peach was the majorhost fruit of the fly (Zhang et al. 1995). In orchards without pes-ticide treatments, more than 70% of the peach fruits were infest-ed, averaging seven larvae per fruit with a maximum of 15(Zhang et al. 1995). Zhang et al. (1995) noted B. dorsalis-infest-ed apples in Yunnan. However, Ye and Liu (2005) observedonly a few infested apples, suggesting that apple is a less pre-ferred host. Plantings of oranges and grapes were less commonin the Kunming area and generally suffered low infestation ratesby B. dorsalis. Therefore, peach was probably the crucial hostfruit shaping the B. dorsalis population dynamics in this area.However, in Xishuangbanna, both mango and longan are themost important host fruits (Sheng et al. 1997), deciding popula-tion growth of the fruit fly. Peach, pear, orange, etc., are alsoimportant host plants of B. dorsalis population growth (Li andYe 2000). Fruiting periods of these host plants alternately pro-vide a successive food resource for B. dorsalis.

Spatial abundanceSpatial abundance of B. latifrons was determined on different

altitudes by collecting fruits from two locations and foursolanaceaus fruits between February and April 2008 (Ye and Liu2005). The populations of many tephritids increase when hostsare available in abundance (Mwatawala et al. 2006a, b;Vayssières et al. 2005). However, the abundance of B. latifronswas generally low, considering the potential of the pest to reachhigh population levels (McQuate and Peck 2001) as well as thelong term availability of hosts that produce small but numerousfruits. Moisture can directly or indirectly affect the biology ofthe pest through host availability. The population patternobtained by sampling was not discernible. Liquido et al. (1994)sampled a number of hosts of B. latifrons and reported a lowpopulation of the pests without a discernible pattern. In depthstudies of the spatial abundance of fruit flies populations mayimprove the successful management of this pest.

Behaviour

Sexual and mating behaviourStudies were carried out on sexual behaviour of fruit fly

species. Generally, they mate on their host plants, but matingtactics vary, even within some species. Lek formation by males,usually on nonhosts, has been observed in C. capitata andspecies of Dacina, Anastrepha, Rhagoletis, andProcecidochares (Prokopy and Hendrichs 1979). Males of mostspecies of Tephritidae secrete certain sex-attractant chemicals,either by inflating the lateral abdominal membranes or byextruding an anal pouch (Fitt 1989). They disperse thesepheromones by wing fanning, which also produces sounds ofpossible significance in courtship (Nufio and Papaj 2001). Wingfanning is a predominant male sexual behaviour reported in sev-eral Dacines but not observed in B. correcta (Poramarcom andBaimai 1996). Tychsen (1977) suggested how wind directioninfluences lek (settled swarms, similar to aggregation of flyingmales seen in other dipteran) position on host plants with respectto B. tryoni. Wing vibration and pheromone released by malesare important factors in courtship behaviour of the melon fruitfly (Kobayashi et al. 1978; Prokopy et al. 1976; Sugimoto1979). However, wing vibration and posterior abdomen beatingbehaviour in B. cucurbitae were related to pheromone emissionand was exhibited by the males as they approached virginfemales. Males of Bactrocera and Dacus have specialized struc-tures, including a tibial pad, a microtrichose area of the wing,and a row of setae on the abdomen called the pecten, which areused for pheromone dispersal. The pecten has been proposed asa stridulatory organ. Calling behavior includes short loopingflights has been studied in A. robusta (Aluja and Prokopy 1993).Visual stimuli, as well as chemical and auditory stimuli, play animportant role in communication between and among the sexesand with other insects. The body, of fruitfly is often brightly col-ored, and the wings, which are usually patterned and are held ormoved in particular ways are supposed to act as releasers. Malesof some species are also engaged in antagonistic displays orbouts (Nufio and Papaj 2001), including species of Phytalmiawhich have large genal processes used in these bouts.

Generally, mating in B. correcta occurred at dusk(Poramarcom and Baimai 1996). Poramarcom and Baimai(1996) also reported that vision is significant for mating accept-ance by B. correcta females and sound and or pheromone, ifany, may be used for long range attraction. They also reportedthat for both the sexes physical characteristic are important to bedrawn to a mating site. Females of B. dorsalis with advancedstage of ovarian development coincided with mating by females.Further, courtship behaviour of B. dorsalis was found to be simi-lar to those of B. cucurbitae (Suzuki and Koyama 1980).Selection of mating site in B. cacuminata (Hering) may be influ-enced by specific characteristics viz. intermediate light intensity,greater height, and greater food quantity (Raghu et al. 2004).However, sexually mature females of the Ethiopian fruit fly, D.ciliatus were most attractive to orange colour whereas yellowcolour was most attractive to sexually mature males (Nufio andPapaj 2001; Raghu et al. 2004). Mating behaviour of B. tryoniby caging wild, laboratory domesticated, and gamma-irradiatedmales with wild females revealed that mating behaviour ofmass-reared males was different from that of wild males,although the behaviour of wild and sterile males was similar.

173

Mass-reared males engage in mounting the other males more fre-quently than wild and sterile males. Despite differences in behav-iour, the frequency of successful copulation, and mating successwere similar among wild, mass-reared, and sterile males (Weldon2005). Mass rearing has been reported to extend the duration ofmale mating behaviour in B. cucurbitae, a dusk mating fruit fly(Suzuki and Koyama 1980). Pheromone cues may be importantin mate choices in females of B. tryoni and B. cucurbitae(Kobayashi et al. 1978). B. tryoni and B. cucurbitae did notappear to be associated with female choice of partners to mateand when courtship occurred, females have only accepted wildmales to mate (Iwahashi 1996). Tychsen (1977) reported thatmating of B. tryoni was limited to about 30 min as light intensityfell at dusk and sexual activity began about 10 min before sunsetunder natural light conditions. Laboratory studies conducted toassess the effect of the parapheromone cue lure on mating behav-iour in males of B. cucurbitae revealed that for wild flies, malesthat were fed on cue lure on the day or one day prior to testingmated more frequently than males that had no prior exposure tocue lure. However, control and treated males had similar successin tests performed later at 3 or 7 days after treated males wereexposed to cue lure (Shelly and Villalobos 1995). The B. tryonifemale does not become responsive to male pheromone untiltheir ovaries were in the final stage of development (Fletcher andGiannakakis 1973). Earlier sexual maturation has been reportedin B. cucurbitae in the laboratory strain than the wild strain(Soemori et al. 1980). Male aggregation size on female visitationin B. tryoni revealed that the female fly visited the largest aggre-gation more frequently than single males in association withhigher proportion of calling males, but there was no correlationbetween aggregation size and female visitation (Weldon 2007).Further, Weldon (2007) gave has suggested that olfaction is anindispensable sensory modality for mating success of the femalesand olfactory receptors are usually located on antennae. Fieldcage studies with B. cacuminata showed that there are significantdiurnal patterns in the abundance and behaviour and also the fliesphysiological status used resources differently. Sexually matureflies were found to forage for sugars during the day and dusk,and respond strongly to methyl eugenol to mate, while immatureflies spend most of their time foraging the sugar and protein tofacilitate development (Raghu and Clarke 2003). Female-biasedattraction of B. dorsalis to a blend of host fruit volatiles fromTerminalia catappa L. revealed that geranyl acetate and methyleugenol elicited the largest Electo Antennogram Detector (EAD)response (Siderhurst and Jang 2006).

Host finding and oviposition behaviourOviposition behavior appears to be much more uniform than

epigamic behaviour that consists of the following stages: a)movement towards and arrival at the oviposition site; b) testingthe site; c) drilling with the ovipositor; and d) oviposition.Oviposition behavioral studies were conducted pertaining to pre-alighting (host search and response visual and olfactory cluesused to find hosts) and post-alighting behaviour (fly behaviourafter landing on host). Pre-alighting behaviour of flies has beenstudied extensively in relation to the visual stimuli (host colour,

shape, and size) (Moericke et al. 1975; Prokopy 1968).Oviposition behaviour has been reported as one of the most limit-ing factor in host use by five Bactrocera species (Fitt 1983).Olfactory stimuli, intra- and interspecific cues used by flies tofind host have also been studied and reviewed (Aluja andProkopy 1992, 1993; Fletcher and Prokorpy 1991). Both visualand olfactory stimuli have also been studied from an appliedangle in relation to the use of traps, pheromones, and baits toimprove management strategies for Bactrocera fruit flies. Openpans baited with 0.1% methyl eugenol in mango orchards attract-ed a significantly higher number of flies (B. dorsali, B. correcta,and B. zonata) as compared to white- and yellow-coloured pansfollowed by green, orange, red, and blue pans (Sarada et al.2001). Species in five genera have been reported to deposit amarking pheromone that deters oviposition by other females(Prokopy et al. 1976). This involves the female dragging heraculeus over the substrate, secreting, and smearing thepheromone. The pheromone of R. cerasi has been identified, syn-thesized, and used in orchards to combat damage to cherries.

Recent reports from China have revealed that for B. dorsalis,UV and green stimuli would enhance the attractiveness of acoloured paper, while blue stimuli would diminish the attractive-ness (Wu 2007). Studies from Taiwan have shown that a greaternumber of females of B. dorsalis were trapped in a mangoorchard using Guava-Sticky-Bag (GSB) traps and plots withoutGSBs had a significantly higher degree of damaged fruits thanthe plots having GSBs (Ho et al. 2003). Post-landing behaviourand selection of oviposition sites may have a direct bearing onthe infestation levels (Pritchard 1969). Host fruit juices can act asoviposition deterrent for B. oleae (Girolami et al. 1981).Abundance and oviposition behaviour B. cacuminata were sig-nificantly influenced by the density of host foliage (wild Solanummauritianum plants) and associated microclimate. The number ofovipositing females was positively influenced by temperature andnegatively by relative humidity (Raghu et al. 2004). Females ofB. dorsalis often use pre-existing punctures made by other tephri-tids to deposit the eggs. In the 12 - 14 day-old laboratory culturedfruit flies of B. dorsalis released in an orchard of host tree, allmating pairs occurred on the fruit itself rather than on foliage orbranches and both sexes were also strongly attracted to the odourof the fruit host. Also, a high amount of male aggregation andmale sexual behaviour were seen on the fruits of the host tree(Prokopy et al. 1995). Pinero et al. (2006) studied the response ofB. cucurbitae females to host-associated visual and olfactorystimuli and reported that a combination of both these stimuli wasneeded to elicit a high level of response as compared to eachstimulus offered alone. This had significant in female monitoringand killing strategies of melon fly in Hawaii. The carambola fruitfly, B. carambolae, in Malaysia laid more (22%) single eggbatches in the field as compared to only 7.5% single egg batchesin the laboratory which is inferred as a survival mechanism toovercome parasitism by potential egg parasitoids (Chua 1994).Effects of food abundance within a tree canopy on the behaviourof wild and cultured B. tryoni have shown that behaviour of fliesdepended not only on fruit abundance but also the sex of the flyand whether the fly was laboratory cultured or from the wild.

Fruit Flies (Tephritidae) - Ecology, Behaviour and Management174

JCSB 2012 (September) 15 (3) : 169 ~ 188

Wild female flies responded to a higher fruit abundance by visit-ing more leaves and spending more time per tree with an increas-ing abundance of fruits while wild male flies could be expectedin the same place that accumulated females (Dalby-Ball andMeats 2000). Aluja and Mangan (2008) suggested that fruit flyoviposition behaviour is influenced by a number of factors andthat can potentially lead a female to lay eggs into a fruit outsideof its natural host range in nature or in experiments under artifi-cial laboratory conditions are host quality, genetics, learning,potential fecundity, ovarian dymanics, aculeus wear, female age,social context, chemical context, and individual variations inoviposition decisions.

Feeding behaviourFeeding behaviour, especially in nature, is a poorly under-

stood aspect of tephritid biology However, it has been widelystudied (Douglas 2006; Kutuk and Ozaslan 2006; Wackers2005) and is essential for survival and reproduction (Diaz-Fleischer and Aluja 2000). Adult nutritional requirements vary,largely depending upon the quality of the larval food and usuallyinclude at least carbohydrates and water, although some gall-forming species do not feed at all (Freidberg and Kugler 1989;Kutuk and Ozaslan 2006) but many species also essentiallyrequired amino acids, sterols, vitamins, and minerals for theirreproduction (Aluja and Prokopy 1993; Wackers 2005). In somespecies, they feed in galls or on seeds (Wackers 2005) femalesare proovigenic, i.e. they emerge with mature eggs and do notrequire protein for egg development, whereas in other speciesprotein is needed for egg development (synovigeny) as well asfor optimal development of male salivary glands and pheromoneproduction (Douglas 2006). Adults may also feed upon plantexudates, including those from oviposition holes or rotting fruit,bird feces, nectar, honeydew, and leachates, microorganisms,pollen and other matters on plant surfaces or in rain drops(Kutuk and Ozaslan 2006; Wackers 2005). Microorganisms mayplay a significant role in the nourishment of some frugivourousspecies (Drew and Lloyd 1987; Estes 2009; Estes et al. 2009).Drew and Fay (1987) found that bacterial odour and ammoniawere strong attractants for B. tryoni. Extensive work has beencarried out on the role of bacteria as a food source for adult fliesand how this influences the behaviour and fitness (Drew andLloyd 1987; Drew et al. 1983). Daily activity rhythm of B. dor-salis showed that feeding mainly occurs in the morning Adultsof Blepharoneura (and probably Baryglossa and Hexaptilona,which have similarly modified labella) are unusual in being ableto rasp and feed on plant tissues (Arakaki et al. 1984). Fruitflies, both males and females, have a significant prematingdevelopment period of a week or more during which they do notmate (Cornelius et al. 2000a, b; Kutuk and Ozaslan 2006) The10 - 12-day-old protein-fed females of both mated and unmatedB. dorsalis were more attracted to fruit odour than to proteinodours. Whereas, mated protein deprived females and unmatedprotein-fed females were equally attracted to fruit and proteinodours. Females of B. dorsalis were most attracted to odour ofsoft and ripe fruits, with the odour of guava being equally attrac-tive as strawberry, guava, orange, and mango (Cornelius et al.

2000a, b). B. cucurbitae flies were more responsive whenstarved for 1 day than non-starved ones to an attractant contain-ing molasses, tryptone, and ethyl acetate. However, this attrac-tiveness decreases when fly density per unit area was too high.

Flight and movementTropical fruit flies are capable of flying long distances as they

are strong fliers (Al-Zaghal and Mustafa 1986; Christonson andFoote 1960). Irradiation doses are negatively correlated with thecapability to fly in B. cucurbitae (Hamada 1980). Pupal handlingduring mass rearing has been reported to influence the flight abil-ity of tephritid fruit flies (Ozaki and Kovayashi 1981). Dalby-Ball and Meats (2000) studied the behaviour of wild and culturedB. tryoni flies and hypothesized that females would respond tocues in such a way as to search a tree more thoroughly if it con-tains acceptable fruits. It would be more advantageous for malesto spend much time in such a tree as it would increase the chanceof encountering females. Verghese et al. (2006) found that windvelocity significantly influenced trap catches of B. dorsalis.

Interspecific Competition

Competition between adultsFemales are being disturbed by other adult tephritids during

egg laying. However, Fitt (1989) felt that this competition mech-anism was largely insignificant, given that the time lapsebetween a female’s arrival on a fruit and egg laying is generallyvery short. Females have been seen to defend their egg-layingsites against females of the same species in B. dorsalis (Shelly1999), and it is likely that this type of behaviour may also affectinterspecific competition. Interference competition may alsooccur via marking pheromones. Host-marking pheromones arechemicals that are deposited by many tephritid species after egglaying, which help to regulate interspecific competition betweenlarvae (Roitberg and Prokopy 1987). Most studies suggest thathost-marking pheromones are only effective against individualsof the same species (Fitt 1989; Nufio and Papaj 2001), but it hasalso been demonstrated in the genus Rhagoletis that there maybe some form of cross recognition between species of a givengroup (Prokopy et al. 1976). No host-marking pheromones haveyet been found in species of the genus Bactrocera, but in twospecies Bactrocera tryoni and Bactrocera jarvisi (Tryon) wherefemales can recognize fruits containing developing larvae, nodoubt as a result of chemical modifications in the fruit (Fitt1989). This recognition is not affected by the species of the lar-vae, and may therefore play a role in interspecific competition.

Competition between larvaeTwo types of competition – interference and exploitation –

undoubtedly both occur, but it is difficult to distinguish betweenthem. Interference between larvae may take the form of physicalattacks, cannibalism, or elimination by fruit deterioration.Whatever the mechanism involved, the first larva to hatch in agiven fruit will have an advantage over subsequent larvae (Fitt

175

1989). The impact of cross-infestation on larva development hasbeen demonstrated in two species that live on the Cucurbitaceae,B. cucurbitae and D. ciliatus (Qureshi et al. 1987), and in C.capitata and B. dorsalis (Keiser et al. 1974). These experimentshave shown that the competitive advantage observed in the wildcan partly be predicted by a better survival of larvae in laborato-ry conditions.

However, both types of competition (exploitation and inter-ference) could work in the same direction provided the speciesthat have superior interference skills also have a K-strategy. Forinstance, a bigger adult size could increase the ability to com-pete by both exploitation and interference.

Management

Local area managementLocal area management means the minimum scale of pest

management over a restricted area such as at field level/croplevel/village level, which has no natural protection against rein-vasion. The aim of local area management is to suppress thepest, rather than eradicate it. Under this management option, anumber of methods such as bagging of fruits, field sanitation,protein baits and cue-lure traps, host plant resistance, biologicalcontrol, and safer insecticides, can be employed to keep the pestpopulation below the economic threshold in a particular cropover a period of time to avoid the crop losses without health andenvironmental hazards, which is the immediate concern of thefarmers.

Bagging of fruitFruits can be easily protected against fruit flies by bagging

them in newspaper bags. The bag provides a physical protectionto the fruit by preventing female flies laying eggs. Bagging hasbeen used for a very long time in Asia by commercial plantersand smallholder farmers. The carambola export industry inMalaysia, worth 10 Million US$ in 1994, protects entireorchards by bagging. This has been successfully practiced forover 70 years. It is also widely practiced to protect mangoes inThailand and Philippines and melons from melon fly in Taiwan.Bagging is inexpensive and easy to apply and guarantees nearlycomplete protection from fruit flies. It is ideal for small scalegrowers who do not use pesticides. Bagging of fruits on the tree(3 to 4 cm long) with two layers of paper bags at 2 to 3-dayintervals minimizes fruit fly infestation and increases the netreturns by 40 to 58% (Fang 1989; Jaiswal et al. 1997).Akhtaruzzaman et al. (1999) suggested cucumber fruits shouldbe bagged at 3 days after anthesis, and the bags should beretained for 5 days for effective control. It is an environmentallysafe method for the management of this pest.

Field sanitation The collection and destruction of infested, fallen, damaged,

over-ripe fruit are extremely important to reduce the population ofthe fruit flies, which otherwise often becomes the important

source for the fruit fly breeding. If field sanitation is practiced atcommunity scale it could be very useful method for reducing fruitfly population. It is the most effective method in melon fruit flymanagement. To break the reproduction cycle and populationincrease, growers need to remove all unharvested fruits or vegeta-bles from a field by completely burying them deep into the soil.Burying damaged fruits 0.46 m deep in the soil prevents adult flyeclosion and reduces population increase (Klungness et al. 2005).

Protein baits and cue-lure trapsFruit flies need sugars and proteinaceous food to survive and

mature. They utilize various sources such as microbes, birddroppings, pollen, etc. (Mazzon et al. 2008). Because of theirinherent needs, fruit flies are highly attracted to high quality pro-tein and sugar baits (Capuzzo et al. 2005; Estes 2009). Proteinbait lures will capture both males and females of most fruit flyspecies but may not be as attract to a given fruit fly species asthe male lure.

The principal of this particular technique is the denial ofresources needed for laying by female flies such as protein food(protein bait control) or parapheromone lures that eliminatemales. There is a positive correlation between cue-lure trapcatches and weather conditions such as minimum temperature,rainfall, and minimum humidity. The sex attractant cue-luretraps are more effective than the food attractant tephritlure trapsfor monitoring the fruitfly. Methyl eugenol and cue-lure trapshave been reported to attract B. cucurbitae males from mid-Julyto mid-November (Liu and Lin, 1993). A leaf extract of Ocimumsanctum, contains eugenol (53.4%), beta-caryophyllene (31.7%),and beta-elemene (6.2%) as the major volatiles, when placed oncotton pads (0.3 mg) attract flies from a distance of 0.8 km(Roomi et al. 1993). Thus, melon fruit fly can also be controlledthrough use of O. sanctum as the border crop sprayed with pro-tein bait (protein derived from corn, wheat, or other sources)containing spinosad as a toxicant. Cue-lure traps have been usedfor monitoring and mass trapping of the fruit flies (Pawar et al.1991; Permalloo et al. 1998; Seewooruthun et al. 2000). A num-ber of commercially produced attractants (Flycide® with 85%cue-lure content; Eugelure® 20%; Eugelure® 8%; Cue-lure® 85%+ naled; Cue-lure® 85% + diazinon; Cue-lure® 95% + naled) areavailable in the market, and have been found to be effective incontrolling this pest (Iwaizumi et al. 1991). Chowdhury et al.(1993) captured 2.36 to 4.57 flies per trap per day in poison baittraps containing trichlorfon in bitter gourd. The use of male lurecearlure B1 (Ethylcis-5-Iodo-trans-2 methylcyclohexane-1- car-boxylate) have been found to be 4 - 9 times more potent thantrimedlure for attracting medfly, C. capitata males (Mau et al.2003) and thus could be tried for male annihilation strategies ofmelon fruit fly areawide control programs. A new protein baitGF-120 Fruit Fly Bait® containing spinosad as a toxicant havebeen found to be effective in the areawide management of melonfruit fly in Hawaii (Prokopy et al. 2003, 2004). The GF-120Fruit Fly Bait® would be highly effective, when applied tosorghum plants surrounding cucumbers against protein-hungrymelon flies, but would be less effective in preventing protein-satiated females from arriving on cucumbers. Maize can also be

Fruit Flies (Tephritidae) - Ecology, Behaviour and Management176

JCSB 2012 (September) 15 (3) : 169 ~ 188

used as a border crop for melon fruit fly attraction through appli-cation of protein bait. Although the protein baits, para-pheromone lures, cue-lures, and baited traps have been success-ful for the monitoring and control of melon fruit fly, there is riskinvolved in the immigration of protein-satiated females whichcould principally be managed by increasing the distance thesesatiated immigrants must travel (Stonehouse et al. 2004).

Host plant resistanceHost plant resistance is an important component in integrated

pest management programs. It does not cause any adverseeffects on the environment, and no extra cost is incurred to thefarmers. Unfortunately, success in developing high-yielding andfruit fly-resistant varieties has been limited. There is a distinctpossibility of transferring resistance genes in the cultivatedgenotypes from the wild relatives of cucurbits for developingvarieties resistant to melon fruit fly through wide hybridization.

Biological Control

PredatorsA few studies have been evaluated the impact that predators

have on fruit flies (Debouzie 1989). However, pupal mortalitymay be important in regulating the abundance of fruit fly popu-lations in the field. To date, ants, carabidm and staphylinid bee-tles, and spiders have been cited as preying on fruit fly larvaeand pupae (Eskafi and Kolbe 1990; Galli and Rampazzo 1996).As a consequence, ant control is considered fundamental to car-rying out an IPM program based on biological control in Spain(Palacios et al. 1999). On the other hand, they can have a benefi-cial impact by directly consuming pests (DeBach and Rosen1991; Hölldobler and Wilson 1996). Ant preyed larvae andpupae of medfly on the field (Eskafi and Kolbe 1990) Chickensand other fowls eat upon fruit fly larvae present on vegetablesand overripe fruits and sometimes consume fly pupae foundbeneath trees. Other common larval and pupal fruit fly predatorsconsist of predaceous wasps, mites, and crickets. Hummingbirdsare also frequent eaters of fruits that might have fruit fly larvae.In Crete, olive flies (B. oleae) are reduced by birds that eat 81%of infested fruits. In consuming the fruits, predators, unfortu-nately, also consume parasitoids so there is an indirect adverseeffect. In the endemic forest habitat, however, predation by fruit-eating vertebrates, such as birds and primates, results in markedreductions in fruit fly numbers.

ParasitoidsThe use of parasitoids to control fruit flies biologically has

always had wide appeal, but tropical fruit flies have not, in gen-eral, proved to be good targets for biological control. The mostdocumented research on using parasitoids to reduce fruit flypopulations has been in Hawaii, where a large number of specieshave been introduced and released to control oriental fruit fly (B.dorsalis), Mediterranean fruit fly (C. capitata), and melon fly(B. cucurbitae). The parasitoids of the families: Braconidae,Chalcididae, and Eulophidae are important to play a significant

role in suppression of fruit flies. Releases of a range of para-sitoids resulted in up to 95% reductions in populations ofMediterranean and oriental fruit flies. Also, in normally heavilyinfested commercial fruits, the levels of damage caused by fruitflies were reduced to a point where fruits were virtually freefrom infestation. These results were due mainly to the establish-ment of the wasp, Fopius arisanus (Somata et al. 2010) and, to alesser extent, the establishment of F. vandenboschii andDiachasmimorpha longicaudata. More recently, a parasitoid, F.arisanus has also been included in the IPM program of B. cucur-bitae at Hawaii (Somata et al. 2010). F. arisanus apparentlybreeds in seven dacine and trypetine hosts, but by 1966, neitherF. arisanus nor D. longicaudata affected the incidence ofQueensland fruit fly. Both species have now become estab-lished.

By 1968, it was claimed that the oriental fruit fly was nolonger a major pest of a number of fruits, except guava. Thislevel of control, however, has not been sustained. Oriental fruitfly and Mediterranean fruit fly are still very serious pests of awide range of fruits and vegetables. Inundative releases of labo-ratory-reared parasitoids may be an appropriate option and isbeing researched in Hawaii.

With respect to melon fly in Solomon Islands, the parasitoidPsyttalia fletcheri was introduced from Hawaii in 1997, with theaim of reducing its populations to a level that may reduce thepressure on the efficacy of protein bait sprays. The populationsof mango fly (B. frauenfeldi) are extremely high throughout theyear on Pohnpei and Kosrae Islands in the Federated States ofMicronesia. F. arisanus and D. longicaudata were introduced in1997 on Pohnpei and Kosrae Islands. F. arisanus has becomequickly established on Pohnpei, but it is too early to assess itslong term impact on mango fly populations. The establishmentof D. longicaudata on Kosrae is being been confirmed at pres-ent.

Srinivasan (1994) reported Opius fletcheri Silv. to be a domi-nant parasitoid of B. cucurbitae, but the efficacy of this para-sitoid has not been tested under field conditions in India. Theparasitization of B. cucurbitae by O. flatcheri has been reportedto vary from 0.2 to 1.9% in Momordica charantia fields inHonolulu at Hawaii. Similar level of parasitization (< 3%) wasalso reported from Northern India by Nishida (1963). However,Nishida (1955) have reported parasitization at levels of 80, 44,and 37%, respectively, from Hawaii. Thus, there is a need toreevaluate the parasitization potential of O. flatcheri before itsexploitation as biocontrol agent for the management of B. cucur-bitae and other related fruit flies species.

Microbes

Fungal pathogensThe conidial phase (spores) of a large number of strains of

entomopathogenic fungi coming from different geographicregions have been assessed under laboratory conditions for con-trol of fruit fly species and on different life history stages(Castillo et al. 2000; De la Rosa et al. 2002; Ekesi et al. 2002;

177

Lezama-Gutiérrez et al. 2000). Applications of conidia to thesoil have been suggested as a method to use these entomopatho-genic fungi for fruit fly control (Dimbi et al. 2003; Lezama-Gutiérrez et al. 2000). This method has been shown to be aneffective way to infect new-emerged adults (Ekesi et al. 2002)and the entomopathogenic fungi might survive better under soilconditions (Gaugler et al. 1989).

Mortality levels varied with fungal strains and species of fruitflies. Dimbi et al. (2003) found from 7 to 100% mortality inadults of C. capitata and C. rosa treated with Beauveriabassiana. Castillo et al. (2000) reported 100% mortality in C.capitata treated with 1 x 106 con mL-1 of Metarhiziumanisopliae. Other strains of this fungi species have been found tobe virulent to adults and immatures of A. fraterculus (Wied.)(Rodrigues-Destéfano et al. 2005). Muñoz (2000) evaluated 16strains of B. bassiana against C. capitata adults and found mor-tality levels between 20 and 98.7%. Similarly, De la Rosa et al.(2002), tested M. anisopliae and B. bassiana for the control of A.ludens adults reported a mortality range between 82 and 100%.

Sinha (1997) reported that culture filterate of the fungus,Rhizoctonia solani Kuhn, to be an effective bio-agent against B.cucurbitae larvae, while the fungus Gliocladium virens Origenhas been reported to be an effective against B. cucurbitae.Culture filtrates of the fungi R. solani, Trichoderma viridaePers., and G. virens affected the oviposition and development ofB. cucurbitae adversely (Sinha and Saxena 1999).

Therefore, the use of sterile flies as fungal vectors is a feasibleapproach that requires further attention. The amount of conidiarequired and the side effects on non-target organisms will be mini-mized. Performance of sterile males under current sterile insecttechnique (SIT) programs conditions must be compared with theperformance under this new approach, considering effects, sterili-ty induction, and mortality produced by fungal transmission.

Bacterial PathogensDipteran species have been found to be susceptible to

Bacillus thuringiensis (Berliner) var. israelensis: mosquitoes,blackflies, chironomids, tipulids, muscids, sciarids, drosophilids(Itoua-Apoyola et al. 1995), and tephritids: B. oleae (Alberola etal. 1999), A. ludens (Robacker et al. 1996; Toledo et al. 1999),and C. capitata (Hassani and Gaouar Benyelles 2008; Vidal-Quist et al. 2009). Yamvrias and Anagnou (1989) have reporteda mortality > 80% when they used various Bt strains against oldlarvae of the dipteran olive fruit fly, B. oleae. Robacker et al.(1996) tested 55 isolates of Bt on larvae of Mexican fruit fly, A.ludens. Seven isolates were found to be most toxic to larvae ascentrifugation pellets were tested against adult flies as either pel-lets or acetone/lactose precipitates made from resuspended pel-lets. Of 55, five isolates killed 65 - 80% of adults in 10 daysafter feeding on them for 2 days, compared with 2.7% mortalityin controls. Isolates that were most toxic to larvae were not nec-essarily most toxic to adults and vice versa. The toxic principleswere characterized as endotoxins based on their water insolubili-ty and heat lability.

Hassani and Gaouar Benyelles (2008) have tested the effectof the preparation of Bt on wild third instars and adults of C.

capitata isolated from Citrus fruit orchards in Algeria, andobserved toxicity in high doses (100 mg g-1) with a reduction inaverage emergence (84.62%), concluding that the stage L3 andadults are very susceptible at this dose of Bt product. Alberola etal. (1999) studied the Bt activity against 2nd instar of B. oleae lar-vae and newly emerged adults and reported that both spore-crys-tal mixtures (109 per mL) caused 70% mortality for larvae in 72hours and 80% of mortality for adult flies in 6 to 10 days ofapplication.

Entomopathogenic virusesAnagnou-Veroniki et al. (1984) have isolated paraspherical

viral particles, 60 nm in diameter, from adults of the olive fly (B.oleae). The virus actively replicated in midgut epithelial cellsand in advanced infections virions accumulated in microvilli.They were released in the gut lumen and were very abundant infly faeces. The virions exhibited the salient features of reovirus-es, with an external shell and an internal core with a tubular sub-unit protruding at each vertex of the icosahedron. The viralgenome consisted of ten segments of double stranded RNAtotalling 23.4 kbp. Based on its overall properties, this virus canbe considered as a nonoccluded insect reovirus.

The impact of the virus in natural conditions is still unknownbut in laboratory conditions the virus is pathogenic both per osand by inoculation (Anagnou-Veroniki et al. 1984).

Entomopathogenic NematodesUse of entomopathogenic nematodes (EPNs) might be a

viable option in an integrated fruit fly management program.Various fruit fly species including medfly were found to be sus-ceptible to EPN (Toledo et al. 2006; Yee and Lacey 2003).Heterorhabditis bacteriophora, H. zealandica, and Steinernemakhoisanae nfect pupariating larvae, pupae, and adults of C. capi-tata and C. rosa.

Pupariating larvae and adult flies were susceptible to nema-tode infection, with no infection recorded for the pupae.Pupariating larvae of C. capitata were generally more suscepti-ble to infection than those of C. rosa. Significantly more larvaeof C. capitata were infected by H. bacteriophora. For C. rosa,the highest infectivity of larvae was obtained with H.zealandica. In contrast, adults of both species were highlyinfected by S. khoisanae.

A Mexican strain of the nematode, S. carpocapsae (Weiser)has been reported to cause 0 to 86% mortality to B. oleae afteran exposure of 6 days to 5,000 to 5,000,000 nematodes per cupin the laboratory, and an average of 87.1% mortality under fieldconditions when applied at 500 infective juveniles per cm2 soil.Sirjani et al. (2009) tested six entomopathogenic nematodes(EPNs) species against B. oleae similar infection levels wereobserved when third-instar larvae were exposed to infectivejuveniles (IJs) of S. feltiae on a sand-potting soil substrate.When IJs of S. feltiae were sprayed over naturally infested fallenolives, many larvae died within treated olives as well as in thesoil. S. feltiae caused the highest overall mortality of 67.9%.Many larvae died inside treated olives, which indicate that IJswere able to find and infect them before they exited the fruit.

Fruit Flies (Tephritidae) - Ecology, Behaviour and Management178

JCSB 2012 (September) 15 (3) : 169 ~ 188

Nematodes most likely entered feeding canals in the olives viaexit holes, oviposition punctures, or tears on the surfaces of thefruit. Similarly, S. feltiae and S. carpocapsae infectedAnaplophora glabipennis (Motchulsky) (Coleoptera:Cerambycidae) larvae inside tunnels bored in an artificial diet.In addition, LeBeck et al. (1993) demonstrated that S. carpocap-sae entered the leaf mines of Liriomyza trifolii (Burgess)(Diptera: Agromyzidae) larvae via oviposition holes or unnatu-ral openings and subsequently infected them.

In many studies, a number of third instar larvae of B. oleaedied as pupae when exposed to S. feltiae and S. carpocapsae(Yee and Lacey 2003). Also, larvae of C. capitata, B. dorsalis,and B. cucurbitae exposed to S. carpocapsae were infected aslarvae but died after pupating (Lindegren and Vail 1986). S. fel-tiae causing 100% mortality before pupation is surprising andimpressive, since fly larvae pupate within a few hours of leavingthe fruit at 25°C (Sirjani et al. 2009). This may be due to a rela-tively high pathogenicity (”the ability to produce disease”)and/or virulence (Shapiro-Ilan et al. 2005) of S. feltiae against B.oleae larvae specifically and dipterous larvae in general (Lewiset al. 2006). When tested against C. capitata larvae, however, S.feltiae was out-performed by S. riobrave (Gazit et al. 2000).

To determine the optimal time period during the season forfield application of selected EPN species, it is essential to exam-ine the effects of abiotic factors on EPN survival and infectivityduring the potential time period. Temperature is one of themajor factors that may limit EPNs activities (Grewal et al. 1994;Griffin 1993) as it influences development (Kaya 1977), forag-ing behavior (Byers and Poinar 1982), infectivity (Chen et al.2003; Saunders and Webster 1999), and survival (Kung et al.1991) of the nematodes. Suggesting an optimal time periodbetween the EPN application and fruitfly larvae falling to thesoil needs more investigation.

The efficacy of most of these bio-agents is unclear underfield conditions. Therefore, there is a need to evaluate the effica-cy of these bio-agents against fruit fly for practical use in inte-grated pest management programs.

Wide area managementWide area management is not a unitary concept, but incorpo-

rates a number of related but distinct methods including localarea management. The methods used include male-sterile insectrelease, insect transgenesis, and quarantine control techniques incombination with available local area management options. Theaim of wide area management is to coordinate and combine dif-ferent characteristics of an insect eradication program over anentire area within a defensible perimeter. The area must be sub-sequently protected against reinvasion by quarantine controls,for example, by pest eradication on isolated islands. The USDA-ARS areawide IPM programs of melon fruit fly started in 1999in collaboration with the Hawaiian State Department ofAgriculture and University of Hawaii, using the environmentallysound strategies such as field sanitation, male annihilation withmale lures and attractants, protein bait sprays/traps, augmenta-tive releases of biological control agents (F. arisanus and P.fletcheri), and sterile insect release. It has proved to be economi-

cally viable, environmentally sensitive, sustainable, and has sup-pressed fruit flies below economic thresholds with the minimumuse of organophosphate and carbamate insecticides (Klungnesset al. 2005; Mau et al. 2003) An IPM program that used fieldsanitation, protein bait applications, male annihilation, andrelease of sterile flies and parasites reduced fruit fly infestationfrom 30 to 40% to less than 5%, and cut organophosphate pesti-cide use by 75 to 90% (Vargas 2004). The recent wide areamanagement or eradication program of B. cucurbitae inSeychelles demonstrated a three tier model including a) initialpopulation reduction using bait sprays, b) elimination of repro-duction using parapheromone lure blocks to eradicate males andthus prevent oviposition by females, and c) intensive surveyingby traps and fruit inspection, until it can be certain that the pestis entirely eradicated (Mumford 2004). Although, the sterileinsect technique has been successfully used in area-wideapproaches, the wide area management needs more sophisticatedand powerful technologies in their eradication program such asinsect transgenesics, which could be deployed over wide-areaand is less susceptible to immigrants. Above all, the use of thegeographical information system has been used as a tool to marksite-specific locations of traps, host plants roads, land use areas,and fruit fly populations within a specified operational grid(Mau et al. 2003).

Chemical ecology and managementThe chemical ecology of fruit flies is of great interest, mainly

due to the possibilities of its application in area-wide controlprojects (Jones and Casagrande 2000). In this context, semio-chemicals have been effectively used to control pests. Threetypes of control systems using attractants have been developedand applied during the last decades: mating disruption, masstrapping, and lure and kill. While mating disruption has beenmainly used against lepidopteran pests (Jones and Casagrande2000), mass trapping and lure and kill were, and are, mainlyapplied in the control of fruit flies (Aluja 1996; Hendrichs1996). C. capitata has been controlled in the citrus sector forover 40 years by an area-wide coordinated effort in whichmalathion combined with a protein hydrolyzate lure is applied,over orchards, as strips from the air (Hendrichs 1996). Similarly,effective eradications of several species of fruit flies have beenattained by using methods in which semiochemicals have beenan important element of the strategy (Kuba et al. 1996;Seewooruthun et al. 2000). Mass trapping, that combines bothpheromones and food lures has also been effectively (e.g. eco-nomically) practiced against the B. oleae (Broumas et al. 1998;Nestel et al. 2000). The large theoretical possibilities rising fromthe application of olfactory attractants to the control of fruit flieshas lead to important developments in the study of the chemicalecology of these flies (Metcalf 1990). Olfactory attractants forfruit flies can be divided into three types: (a) plant kairomonesor parapheromones that can be volatiles derived from host ornon-host plant species; (b) food lures which are usually proteinhydrolyzate derivatives; and (c) sex pheromones.Parapheromones (e.g. attractants derived from non-host plantsthat mimic a pheromonal mechanism) are widely used in the

179

management of tephritids. Most common products includeTrimedlure, which specifically attracts males of C. capitata, andmethyl eugenol, which is highly attractive to males of manyBactrocera species (Jang and Light 1996; Metcalf 1990).Parapheromones, such as Trimedlure, are mainly used as moni-toring tools in area-wide control programs. However, some para-pheromones have shown particular characteristics in their abilityto strongly attract, arrest, and kill large male populations of afruit fly species decimating the population capacity to repro-duce. Such capacity has been exploited as a control strategy (e.g.male annihilation technique) and used against severalBactrocera species, e.g. the use of methyl eugenol in eradicationcampaigns against B. dorsalis in the Okinawa islands of Japan(Yoshizawa 1997) and in the island of Mauritius (Seewooruthunet al. 2000), and the use of cue-lure, a synthetic derivative ofraspberry ketone, in projects of male annihilation of B. cucur-bitae (Wong et al. 1991). Regarding fruit fly attractants derivedfrom host-plants, few advances have taken place in this area.The two most important discoveries relate to an apple multiple-blend, which has been found useful for the attraction of R.pomonella and a fermented chapote blend that attracts A. ludens(Jang and Light 1996). Protein hydrolysates of corn, soybean,and yeast have been used to monitor fruit flies and as attractantsfor bait sprays (Metcalf 1990). The attractiveness of thesehydrolysates, however, seems to be affected by the rate ofammonium release, which appears to be a function of concentra-tion, type of ammonium salt, and pH (Jang and Light 1996).During the last few years, synthetic derivatives of proteinhy-drolyzate breakdown products (e.g. Ammonium Acetate,Trimethylamine, and Putrescine) have been tested and success-fully used for monitoring tephritids (Heath et al. 1997). A fewattractive pheromones from Tephritidae have been isolated andcharacterized. Evidence of attractive pheromones has beendemonstrated in A. ludens, A. suspense, B. dorsalis, B. oleae, C.capitata, R. pomonella, and R. cerasi (Landolt and Averill1999). Of all these pheromones, however, the only useful one interms of field applications has been the pheromone of B. oleae,which is unusual within the tephritid flies due to the fact ofbeing a female produced pheromone attractive to male flies. Thepheromone of B. oleae is used in area-wide control as a monitor-ing tool, and as a component of the mass-trapping techniquedeveloped for this fly species (Broumas et al. 1998). Host andnon-host plants form the focal point for all fruit fly activities, inparticular feeding, lekking, mating, and egg laying. Most ofthese activities are mediated by semiochemicals (Tan 2000). Inparticular, attraction of fruit flies to its host is usually guided byvolatile phytochemicals (Aluja and Mangan 2008). These chem-icals are expected to serve as good candidates for fruit fly attrac-tants, especially in species exhibiting hosts specificity such asoligophagous D. ciliatus.

Male-sterile techniqueSterile males are released in the field for mating with the wild

females. Sterilization is accomplished through irradiation,chemo-sterilization, or by genetic manipulation. Sterility or ster-ile insect refers to the transmission of dominant lethal mutations

that kill the progeny. The females either do not lay eggs or laysterile eggs. Ultimately, the pest population can be eradicated bymaintaining a barrier of sterile flies. Sterile insect technique(SIT) has been used successfully and developed as a controlmethod for C. capitata, A. ludens, B. carambolae, and B. oleae.SIT may be used as a component of an overall detection and pre-vention strategy, or it may be used as a component of suppres-sion or eradication programs. In practice, if the sterile insects arereleased often enough and in sufficient numbers, a feral popula-tion will decline and can eventually be eradicated.

Chemical bait sprays include malathion that are considerednecessary in eradication programs to eliminate gravid femalefruit flies and reduce the population density to a low level beforeSIT is employed. Increasing the ratio of sterile male fruit flies toferal males improves the effectiveness of the technique. Currentdata indicate that sterile female fruit flies do not contribute tothe suppression of the target pest and that releases of predomi-nantly male flies work much better. This is the force driving thechange to predominantly male release programs against theMedfly and the effort to develop genetic sexing strains for otherfruit flies under mass production. Used in integrated programs,SIT also affords continuing effectiveness on adults that emergefrom the ground where they were not affected by earlier chemi-cal bait sprays.

A sterile insect program is species specific, and is consideredan ecologically safe procedure and has been successfully used inarea-wide approaches to suppress or eradicate pest insects inentire regions such as the pink bollworm, Pectinophora gossyp-iella, in California (Walters et al. 2000), the tsetse fly, Glossinaausteni, in Zanzibar (Vreysen 2001), the New World screwworm,Cochliomyia hominivorax, in North and Central America (Wyss2000), and various tephritid fruit fly species in different parts ofseveral continents (Klassen et al. 1994). Chemo-sterilization (byexposing the flies to 0.5 g tepa in drinking water for 24 h) andgamma irradiation are the only widely tested and accepted male-sterile techniques against melon fly (Odani et al. 1991).Nakamori et al. (1993) found in Okinawa that frequent and inten-sive release of sterile flies did not increase the ratio of sterile towild flies in some areas, suggesting that it is important to identifysuch areas for eradication of this pest. Eradication of this pest hasalready been achieved through sterile-male release in KikaijmaIslands in 1985, Amami-oshima in 1987, Tokunoshima, and theOkierabu-jima and Yoron-jima Islands in 1989 (Yoshizawa1997). Release of sterile males of C. capitata increased the effec-tiveness of the sterile insect program. Male-sterile and male anni-hilation techniques have successfully eradicated the melon flyfrom Japan for over 24 years (Liu 1993). However, the suppres-sion of B. cucurbitae reproduction through male annihilationwith cue-lure may be problematic. Matsui et al. (1990) reportedthat no wild tephritids were caught with cue-lure traps after inten-sification of distribution of cue-lure strings, but the mating ratesof mature females did not decrease as compared to those on con-trol islands. Conventional sterilization based on ionizing radia-tion causes chromosome fragmentation without centromeres,where the chromosome fragments will not be transmitted correct-ly to the progeny, and can have adverse effects on viability and

Fruit Flies (Tephritidae) - Ecology, Behaviour and Management180

JCSB 2012 (September) 15 (3) : 169 ~ 188

sperm quality, resulting in reduced competitiveness of sterilizedindividuals (Cayol et al. 1999; Mayer et al. 1998).

QuarantineThe import and export of infested plant material from one

area or country to other non-infested places is the major mode ofthe spread of insect-pests. The spread of the fruit fly can beblocked through tight quarantine and treatment of fruits at theimport/export ports. Cold treatment at 1.1 ± 0.6°C for 12 daysdisinfested Hawaiian starfruit, Averrhoa carambola, of tephritideggs and larvae (Armstrong et al. 1995). Heat treatment of avo-cado fruits infested with eggs and larvae of B. cucurbitae for40°C for 24 h reduced the estimated surviving population by99.5 to 100% (Yang 1996). Import controls carried out in air-ports in France since 1993 on tropical fruits have revealed thepresence of 12 non-European and one European species ofTephritidae (Bayart et al. 1997).

Conclusions

Keeping in view the importance of fruit flies, their wide hostranges, ability to become established or more widespread, theirpotential economic impacts, and potential ecological impact(direct and indirect), they have been the subject of strict quaran-tines and comprehensive control programs.

Fruit fly can be managed or suppressed locally at the grow-er’s fields using any of the option combinations availableincluding, bagging of fruits, field sanitation, cue-lure traps,spray of protein baits with toxicants, growing fruit fly-resistantgenotypes, augmentative release of biological control agents,and safer insecticides. On the other hand, the incorporation of anumber of different techniques including sterile insect tech-nique, transgene based and quarantine, in addition to the avail-able local area management options, could be exploited for bet-ter results in wide area management of fruit fly. The local areamanagement aims mainly at suppression, rather than eradication.Use of wide area management to coordinate and combine differ-ent parts of an insect eradication program over an entire area,within a defensible perimeter, can subsequently protect againstreinvasion by quarantine controls. The use of a geographicalinformation system could also be used as an IPM tool to marksite-specific locations of traps, host plants roads, land use areas,and fruit fly populations within a specified operational region.Although sterile insect programs have been successfully used inarea-wide approaches, more sophisticated and powerful tech-nologies should be used in their eradication program such asinsect transgenesis, which could be deployed over wide areas.

References

Akhtaruzzaman M, Alam MZ, Ali-Sardar MM. 1999. Suppressing fruit fly infestation by bagging cucumber at dif-ferent days after anthesis. Bang. J. Entomol. 9: 103-112

Alberola TM, Aptosoglou S, arsenakis M, Bel Y, Delrio Get al. 1999. Insecticidal activity of strains of Bacillus thuringiensis on larvae and adults of Bactrocera oleae Gmelin (Dipt. Tephritidae). J. Invert. Pathol. 74: 127-136

Al-Jboory I. 2007. New record of Mediterranean fruit fly in Iraq. Arab and Near East Plant Protection Newsletter, Published by the Arab Society for Plant Protection and Near East Regional Office of the FAO, pp 36-37

Allmann SL. 1940. The Queensland fruit-fly. Observations on breeding and development. NSW Agric. Gaz. 50: 499-501

Allmann SL. 1941. Observations on various species of fruit flies. J. Aust. Inst. Agric. Sci. 7: 155-156

Aluja M. 1996. Future trends in fruit fly management. In BA McPheron, GJ Steck, Eds, Fruit Fly Pests: A world assess-ment of their biology and management. St. Lucie Press, Delray Beach, pp 309-320

Aluja M, Mangan RL. 2008. Fruit fly (Diptera: Tephritidae) Host status determination: Critical conceptual, methodologi-cal and regulatory considerations. Annu. Rev. Entomol. 53: 473-502

Aluja M, Prokopy RJ. 1992. Host search behaviour by Rhagoletis pomonella flies: Inter-tree movement patterns in response to wind-borne fruit volatiles under field conditions. Physiol. Entomol. 17: 1-8

Aluja M, Prokopy RJ. 1993. Host odour and visual stimulus interaction during intra-tree host finding behaviour of Rhagoletis pomonella flies. J. Chem. Ecol. 19: 2671-2695

Al-Zaghal K, Mustafa T. 1986. Flight activity of olive fruit fly (Dacus oleae Gmel.) (Diptera: Tephritidae) in Jordan. J. Appl. Entomol. 103: 452-456

Anagnou-Veroniki M, Bergoin M, Veyrunes JC. 1984. Research on the viral infection of Dacus oleae (Gmel). In R Cavalloro, A Piavaux, Eds, Agriculture. CEC Programme on Integrated and Biological Control. EUR. 8689, pp 201-207

Arakaki N, Kuba H, Soemori H. 1984. Mating behavior of the oriental fruit fly, Dacus dorsalis Hendel (Diptera: Tephritidae). Appl. Entomol. Zool. 19: 42-51

Armstrong JW, Silva ST, Shishido VM. 1995. Quarantine cold treatment for Hawaiian carambola fruit infested with Mediterranean fruit fly, melon fly, or oriental fruit fly (Diptera: Tephritidae) eggs and larvae. J. Econ. Entomol. 88: 683-687

Bayart JD, Phalip M, Lemonnier R, Gueudre F. 1997. Fruit flies. Results of four years of import control on fruits in France. Phytoma 49: 20-25

Behar A, Ben-Yosef M, Lauzon CR, Yuval B, Jurkevitch E. 2009. Structure and function of the bacterial community asso-ciated with the Mediterranean fruit fly. In K Bourtzis, TA Miller, eds, Insect Symbiosis , Boca Raton, CRC Press pp 251-272

Behar A, Yuval B, Jurkevitch E. 2005. Enterobacteriamediated nitrogen fixation in natural populations of the fruit fly Ceratitis capitata. Mol. Ecol. 14: 2637-2643

Billah MK. 2007. ECOWAS fruit fly scoping study and regional action programme. Evaluation of the fruit fly problem in Ghana. A report on Ghana, pp 47

181

Billah MK, Wilson DD, Cobblah MA, Lux SA, Tumfo JA. 2006. Detection and preliminary survey of the invasive fruit fly, (Diptera: Tephritidae) in Ghana, J. Ghana Sci. Assoc. 2: 38-14

Broumas T, Haniotakis G, Liaropoulos C, Tomazou T, Ragousis N. 1998. Effect of attractant, density and deployment of traps on the efficacy of the mass trapping method against the olive fruit fly, Bactrocera oleae (Diptera: Tephritidae). Ann. Inst. Phytopathol. Benaki 18: 67-80

Byers JA, Poinar Jr GO. 1982. Location of insect host by nema-tode, Neoaplectana carpocapsae, in response to temperature. Behaviour 79: 1-10

CAB International Institute of Entomology. 1995. Distribution maps of pests. Reviews of Applied Entomology Series A (Agriculture), Map No. 64. CAB, London

Capuzzo C, Firrao G, Mazzon L, Squartini A, Girolami V. 2005. Candidatus Erwinia dacicola, a coevolved symbiotic bacteri-um of the olive fly Bactrocera oleae (Gmelin). Int. J. Syst. Evol. Microbiol. 55: 1641-1647

Carey JR. 1993. Applied Demography for Biologists with Special Emphasis on Insects, Oxford University Press, New York

Carey JR, Vargas RI. 1985. Demographic analysis of insect mass rearing: A case study of three tephritids. J. Econ. Entomol. 78: 523-527

Castillo MA, Moya P, Hernández E, Primo-Yúfera E. 2000. Susceptibility of Ceratitis capitata Wiedemann (Diptera: Tephritidae) to entomopathogenic fungi and their extracts. Biol. Control 19: 274-282

Cayol JP, Vilardi J, Rial E, Vera MT. 1999. New indices and method to measure the sexual compatibility and mating per-formance of Ceratitis capitata (Diptera: Tephritidae) laborato-ry-reared strains under field cage conditions. J. Econ. Entomol. 92: 140-145

Chen S, Li J, Han X, Moens M. 2003. Effect of temperature on the pathogenicity of entomopathogenic nematodes (Steinernema and Heterorhabditis spp.) to Delia radicum.BioControl 48: 713-724

Chen P, Ye H, Liu J. 2006. Population dynamics of Bactrocera dorsalis (Diptera Tephritidae) and analysis of the factors influencing the population in Ruili, Yunna Province, China. Acta Ecol. Sini 26: 2801-2808

Chowdhury MK, Malapert JC, Hosanna MN. 1993. Efficiency of poison bait trap in controlling fruit fly, Dacus cucurbitaein bitter gourd. Bangladesh Journal of Entomology 3: 91-92.

Christonson LD, Foote RH. 1960. Biology of fruit flies. Annu. Rev. Entomol. 5:171-192

Chua TH. 1994. Egg batch size of the carambola fruit fly, Bactrocera sp. (Malaysian) (Diptera: Tephritidae). Pertanika J. Trop. Agric. Sci. 17: 107-109

Clarke AR, Armstrong KF, Carmichael AE, Milne JR, Raghu S, Roderick GK, Yeates DK. 2005. Invasive phytophagous pests arising throughrecent tropical evolutionary radiation: the Bactrocera dorsalis Complex of fruit flies. Annu. Rev. Entomol. 50: 293-319

Cody ML. 1966. A general theory of clutch size. Evolution 20:

174-184 Cornelius ML, Duan JJ, Messing RH. 2000a. Volatile hosts fruit

odors as attractants for the oriental fruit fly (Diptera: Tephritidae). J. Econ. Entomol. 93: 93-100

Cornelius ML, Nergel L, Duan JJ, Messing RH. 2000b. Response of femaleoriental fruit flies (Diptera: Tephritidae) to protein and host fruit odors in fieldcage and open field tests. Environ. Entomol. 29: 14-19

Dalby-Ball G, Meats A. 2000. Effect of fruit abundance within a tree canopy on the behaviour of wild and cultured Queensland fruit-fly Bactrocera tryoni (Froggatt) (Diptera: Tephritidae). Aust. J. Entomol. 39: 201-207

DeBach P, Rosen D. 1991. Biological Control by Natural Enemies. 2nd edn, Cambridge University Press, Cambridge

Debouzie D. 1989. Biotic mortality factors in tephritid popula-tions. In AS Robinson, G Hooper, eds, World Crop Pests, Vol. 3B, Fruit Flies, Elsevier, New York, pp 221-227

De la Rosa W, López FL, Liedo P. 2002. Beauveria bassiana as a pathogen of the Mexican fruit fly (Diptera: Tephritidae) under laboratory conditions. J. Econ. Entomol. 95: 36-43

Dhillon MK, Naresh JS, Ram Singh, Sharma, NK. 2005. Influence of physico-chemical traits of bitter gourd, Momordica charantia L. on larval density and resistance to melon fruit fly, Bactrocera cucurbitae (Coquillett). J. Appl. Entomol. 129: 393-399

Diaz-Fleischer F, Aluja M. 2000. Behavior of Tephritid flies: A historical perspective. In M Aluja, AL Norrbom, eds, Fruit Flies (Tephritidae): Phylogeny and Evolution of Behavior, pp 944

Dimbi S, Maniania NK, Lux AS, Ekesi S, Mueke KJ. 2003. Pathogenicity of Metarhizium anisopliae (Metsch.) Sorokin and Beauveria bassiana (Balsamo) Vuillemin, to three adult fruit fly species: Ceratitis capitata (Wiedemann), C. rosa var. Fasciventris Karsch and C. cosyra (Walker) (Diptera: Tephritidae). Mycopathology 156: 375-382

Douglas AE. 1998. Nutritional interactions in insect-microbial symbioses: aphids and their symbiotic bacteria Buchnera. Ann. Rev. Entomol. 43: 17-37

Douglas AE. 2006. Phloem-sap feeding by animals: Problems and solutions. J. Exp. Bot. 57: 747-754

Drew RAI, Courtice AC, Teakle DS. 1983. Bacteria as natural source of food for adult flies Dacus tryoni (Diptera:Tephri-tidae). Oecologia (Berlin) 60: 279-284

Drew RAI, Fay HA. 1987. Comparison of the roles of ammonia and bacteriain the attraction of Dacus tryoni (Froggatt) (Queensland fruit fly) to proteinaceous suspensions. J. Plant Protec. Trop. 5: 127-130

Drew RAI, Lloyd AC. 1987. Relationship of fruit flies (Diptera: Tephritidae) and their bacteria to their host plants. Ann. Entomol. Soc. Am. 80: 629-636

Drew RAI, Yuval B. 2000. The evolution of fruit fly feeding behaviour. In M Aluja, AL Norrbom, eds, Fruit Flies: phy-logeny and evolution of behavior, Boca Raton, CRC Press, pp 731-749

Duyck PF, David P, Quilici S. 2006. Climatic niche partitioning following successive invasions by fruit flies in La Réunion. J.

Fruit Flies (Tephritidae) - Ecology, Behaviour and Management182

JCSB 2012 (September) 15 (3) : 169 ~ 188

Anim. Ecol. 75: 518-526 Ekesi S, Maniania NK, Lux SA. 2002. Mortality in three African

tephritid fruit fly puparia and adults caused by the ento-mopathogenic fungi Metarhizium anisopliae and Beauveria bassiana. Biocontrol. Sci. Technol. 12: 7-17

Eskafi FM, Kolbe MM. 1990. Predation on larval and pupal Ceratitis capitata (Diptera: Tephritidae) by the ant Solenopsis germinata (Hymenoptera: Phormicidae) and other predators in Guatemala. Environ. Entomol. 19: 148-153

Estes AM. 2009. Life in a fly: The ecology and evolution of the olive fly endosymbiont. In Candidatus Erwinia dacicola. PhD thesis, University of Arizona

Estes AM, Hearn DJ, Bronstein JL, Pierson EA. 2009. The olive fly endosymbiont, ‘Candidatus Erwinia dacicola,’ switches from an intracellular existence to an extracellular existence during host insect development. App. Environ. Microbiol. 75: 7097-7106

Fang MN. 1989. Studies on using different bagging materials for controlling melon fly on bitter gourd and sponge gourd. Bull. Taichung District Agric. Improve Station 25: 3-12

Fitt GP. 1983. Factors limiting host range of tephritid fruit flies, with particular emphasis on the influence of Dacus tryoni onthe distribution and abundance of Dacus jarvisi. PhD Thesis, University of Sydney, Australia. pp 291

Fitt GP. 1989. The role of interspecific interactions in the dynamics of tephritid populations. In AS Robinson, G Hooper, eds, Fruit Flies, Their Biology, Natural Enemies and Control. World Crop Pests, Elsevier, Amsterdam, pp 281-300

Fletcher BS, Giannakakis A. 1973. Factors limiting the response of female’s of the Queensland fruit fly, Bactrocera Tryoni. To the sex pheromone of the male. J. Insect Physiol. 19: 1147-1155

Fletcher BS, Prokopy RJ. 1991. Host location and oviposition in tephritid fruitflies. In WJ Bailey, J Ridsdill-Smith, eds, Reproductive Behavior of Insects. Individuals and popula-tions, Chapman & Hall, London, pp 139-171

Freidberg A, Kugler J. 1989. Fauna Palaestina. Insecta IV. Diptera: Tephritidae. Israel Academy of Sciences and Humanities, Jerusalem, pp 212

Galli JC, Rampazzo EF. 1996. Enemigos naturales predadores de Anastrepha (Diptera, Tephritidae) capturados con trampas de gravedad de suelo en huertos de Psidium guajava L. Bol. San. Veg. Plagas 22: 297-300

Gaugler R, Costa SD, Lashomb J. 1989. Stability and efficacy of Beauveria bassiana soil inoculations. Environ. Entomol. 18: 412-417

Gazit Y, Rossler Y, Glazer I. 2000. Evaluation of entomopathogenic nematodes for the control of Mediterranean fruit fly (Diptera: Tephritidae). Biocontrol Sci. Technol. 10: 157-164

Girolami VA, Vianello A, Strapazzon A, Ragazzi E, Veronese E. 1981. Ovipositional deterrents in Dacus oleae. Entomol. Exp. Appl. 29: 177-188

Grewal PS, Selvan S, Gaugler R. 1994. Thermal adaptation of entomopathogenic nematodes: niche breath for infection, establishment and reproduction. J. Thermal Biol. 19: 245-253

Griffin CT. 1993. Temperature responses of entomopathogenic

nematodes: implication for the success of biological control programmes. In R Bedding, R Akhurst, H Kaya. eds, Nematodes and the biological control of insect pests. East Melbourne, Victoria 3002. pp 115–126

Hamad R. 1980. Studies on the dispersal behaviour of melon flies, Dacus cucurbitae Coquillet. (Diptera: Tephritidae) and the influence of gamm-irradiation on dispersal. Appl. Entomol. Zool. 15: 363-371

Hassani F, Gaouar Benyelles N. 2008. Application of Bacillus thuringiensis (Bti) struggling microbiological control of the fruit fly Ceratitis capitata (wied) (Diptera: Tephritidae). IB Scientific J. Sci. 3: 10-13

Heath RR, Epsky MD, Dueben BD, Rizzo J, Jeronimo F. 1997. Adding methylsubstituted ammonia and a food based synthet-ic attractant on captures of Mediterranean and Mexican fruit flies (Diptera: Tephritidae). J. Econ. Entomol. 90: 1584-1589

Hendrichs J. 1996. Action programs against fruit flies of eco-nomic importance: Session overview. In BA McPheron, GJ Steck, eds, Fruit Fly Pests: A world assessment of their biolo-gy and management, St. Lucie Press, Delray Beach, pp 513-519

Ho KY, Lee HJ, Horng SB, Chen CC. 2003. Comparison of the effectiveness of different materials for attracting the Oriental fruit fly, Bactrocera dorsalis (Diptera: Tephritidae). Plant Protect. Bull. 45: 117-126

Hölldobler B, Wilson EO. 1996. Viaje a las hormigas. Una his-toria de exploración científica. Crítica Grijalbo Mondadori, Barcelona 270

Itoua-Apoyolo C, Drif L, Vassal JM, DeBarjac H, Bossy JP, Leclant F, Frutos R. 1995. Isolation of Multiple Subspecies of Bacillus thuringiensis from a Population of the European Sunflower Moth, Homoeosoma nebulella. Appl. Environ. Microbiol. 61: 4343-4347

Iwahashi O. 1996. Problems encountered during long-term SIT program in Japan. In BA McPheron, GJ Steck, eds, Fruit Fly Pests: A world assessment of their biology and management, St Lucie press, pp 392-398

Iwaizumi R, Sawaki M, Kobayashi K, Maeda C, Toyokawa Z, Ito M, Kawakami T, Matsui M. 1991. A comparative experi-ment on the attractiveness of the several kinds of the cue-lure toxicants to the melon fly, Dacus cucurbitae (Coquillett). Res. Bull. Plant Prot. Serv. Jpn. 27: 75-78

Jaiswal JP, Gurung TB, Pandey RR. 1997. Findings of melon fruit fly control survey and its integrated management, Kashi, Nepal. Lumle Agriculture Research Centre Working Paper. pp 1-12

Jang EB, Light DM. 1996. Olfactory semiochemicals of tephritids. In BA McPheron, GS Steck, eds, Fruit Fly Pests, A World Assessment of their Biology and Management, St. Lucie Press, Delray Beach, pp 73-90

Jiang XL, He WZ, Xiao S. 2001. Study on the biology and sur-vival of Bactrocera dorsalis in the border region of Yunnan. J. Southwest Agric. Univ. 23: 510-517

Jones OT, Casagrande ED. 2000. The use of semiochemical-based devices and formulations in the area-wide programmes: A commercial perspective. In KH Tan, eds, Area-Wide

183

Control of Fruit Flies and Other Insect Pests. Penerbit Universiti Sains, Malaysia, Penang, pp 285-293

Kaya HK. 1977. Development of the DD-136 strain of Neoaplectana carpocapsae at constant temperature. J. Nematol. 9: 346-349

Keiser I, Kobayashi RM, Miyashita DH, Harris EJ, Schneider EJ, Chambers DL. 1974. Suppression of Mediterranean fruit flies by Oriental fruit flies in mixed infestations in guava. J. Econ. Entomol. 67: 355-360

Klassen W, Lindquist DA, Buyckx EJ. 1994. Overview of the joint FAO/IAEA Division's involvement in fruit fly sterile insect technique programs, In CO Calkins, W Klassen, P Liedo, eds, Fruit Flies and the Sterile Insect Technique, CRC Press, Boca Raton, pp 3-26

Klungness LM, Jang EB, Mau RFL, Vargas RI, Sugano JS, Fujitani E. 2005. New approaches to sanitation in a cropping system susceptible to tephritid fruit flies (Diptera: Tephritidae) in Hawaii. J. Appl. Sci. Environ. Manag. 9: 5-15

Kobayashi RM, Ohinata K, Hambers DL, Fujimoto MS. 1978. Sex pheromones of the oriental fruit fly and the melon fly: mating behavior, bioassay method and attraction of females by live males and by suspected pheromone glands of males. Environ. Entomol. 7: 107-112

Kounatidis I, Crotti E, Sapountzis P, Sacchi L, Rizzi A, Chouaia B, Bandi C, Alma A, Daffonchio D, Mavragani-Tsipidou P. 2009. Acetobacter tropicalis is a major symbiont of the olive fruit fly (Bactrocera oleae). Appl. Environ. Microbiol. 75: 3281-3288

Kuba H, Kohama T, Kakinohana H, Yamagishi M, Kinjo K, Sokei Y, Nakasone T, Nakamoto Y. 1996. The successful eradication programs of the melon fly in Okinawa. In BA McPheron, GJ Steck, eds, Fruit Fly Pests: A world assess-ment of their biology and management, St. Lucie Press, Delray Beach, pp 543-550

Kung SP, Gaugler R, Kaya HK. 1991. Effects of soil tempera-ture, moisture, and relative humidity on entomopathogenic nematode persistence. J. Invert. Pathol. 57: 242-249

Kutuk M, Ozasalan M. 2006. Faunistical and systematical stud-ies on the Trypetinae (diptera: tephritidae) in the Turkey along with a new record to Turkish fauna. Mun. Ent. Zool. 1: 173-178

Landolt PJ, Averill A. 1999. Fruit flies. In J Hardie, AK Minks, eds, Pheromones of Non-Lepidopteran Insects Associated with Agricultural Plants, CAB International, pp 3-2

Lauzon CR. 2003. Symbiotic relationships of Tephritids. In K Bourtzis, TA Miller, eds, Insect Symbiosis , Boca Raton, CRC Press, pp 115-129

LeBeck, L.M. , Gaugler R., Kaya H.K., Hara A.H., Johnson M.W. (1993) Host stage suitability of the leafminerLiriomyza trifolii (Diptera: Agromyzidae) to the entomopa-thogenic nematode Steinernema carpocapsae (Rhabditida: Steinernematidae) Journal of Invertebrate Pathology, 62, 58–63

Lemos FJA, Terra WR. 1991. Digestion of bacteria and the role of midgut lysozyme in some insect larvae. Comp. Biochem. Phys. B. 100: 265-268

Lewis EE, Campbell J, Griffin C, Kaya H, Peters A. 2006. Behavioral ecology of entomopathogenic nematodes. Bio. Control 38: 66-79

Lezama-Gutiérrez R, Trujillo-de la Luz A, Molina-Ochoa J, Rebolledo-Domínguez O, Pescador AR, López-Edwards M, Aluja M. 2000. Virulence of Metarhizium anisopliae(Deuteromycotina: Hyphomycetes) on Anastrepha ludens (Diptera: Tephritidae): Laboratory and field trials. J. Econ. Entomol. 93: 1080-1084

Li HX, Ye H .2000. Infestation and distribution of the Oriental fruit fly (Diptera: Tephritidae) in Yunnan province. J Yunnan Univ, 22: 473-475 (in Chinese)

Lindegren JE, Vail PV. 1986. Susceptibility of Mediterranean fruit fly, melon fly, and oriental fruit fly (Diptera: Tephritidae) to the entomogenous nematode Steinernema fel-tiae in laboratory tests. Environ. Entomol. 15: 465-468

Liquido NJ, Harris EJ, Dekker LA. 1994. Ecology of Bactrocera latifrons (Diptera: Tephritidae) populations: host plants, natu-ral enemies, distribution and abundance. Ann. Entomol. Soc. Am. 87: 71-84

Liu YC. 1993. Pre-harvest control of Oriental fruit fly and melon fly. Plant Quarantine in Asia and the Pacific, Report of APO Study Meeting, 17-26 March 1992, Taipei, Taiwan Republic of China, pp 73-76

Liu YC, Cheng SK. 1995. Development of food attractants for melon flies Dacus cucurbitae Coq. Plant Protect. Bull. 37: 189-199

Liu YC, Lin JS. 1993. The response of melon fly, Dacus cucur-bitae Coquillett to the attraction of 10% MC. Plant Prot. Bull. Taipei 35: 79-88

Lundgren JG. 2009. Relationships of natural enemies and nonprey foods. Progress in biological control. Dordrecht, The Netherlands, Springer

Martin H, Geigy JR, Bales SA. 1953. Observations biologiques et essais de traitements contre la Mouche de I’olive (Dacus oleae Rossi) dans la province de Tarragone (Espagne) de 1946 a 1948. Rev. Pathol. Veg. Entomol. Agric. Fr. 21: 361-402

Matsui M, Nakamori H, Kohama T, Nagamine Y. 1990. The effect of male annihilation on a population of wild melon flies, Dacus cucurbitae Coquillett (Diptera: Tephritidae) in Northern Okinawa. Jpn. J. Appl. Entomol. Zoo.l 34: 315-317

Mau R, Martin Kessing JL, Diez JM. 2007. Ceratitis capitata(Wiedemann). University of Hawaii Crop Knowledge Master. Available at http://www.extento.hawaii.edu/kbase/crop/Type/ceratiti.htm (21 June 2010)

Mau RFL, Sugano JS, Jang EB. 2003. Farmer education and organization in the Hawaii areawide fruit fly pest manage-ment program. Recent Trends on Sterile Insect Technique and Area-wide Integrated Pest Management: Economic Feasibility, Control Projects, Farmer Organization and Dorsalis Complex Control Study, Research Institute of Subtropics, Okinawa, Japan. pp 47-57

Mayer DG, Atzeni MG, Stuart MA, Anaman KA, Butler DG. 1998. Mating competitiveness of irradiated flies for screw-worm fly eradication campaigns. Prev. Vet. Med. 36: 1-9

Fruit Flies (Tephritidae) - Ecology, Behaviour and Management184

JCSB 2012 (September) 15 (3) : 169 ~ 188

Mazzon L, Piscedda A, Simonato M, Martinez-Sanudo I, Squartin A, Girolami V. 2008. Presence of specific symbiotic bacteria in flies of the subfamily Tephritinae (Diptera Tephritidae) and their phylogenetic relationships: proposal of ‘Candidatus Stammerula tephritidis’. Int. J. Syst. Evol. Microbiol. 58: 1277-1287

McPeek MA, Kalisz S. 1993. Population sampling and boot-strapping in complex designs: Demographic analysis. In SM Scheiner, J Gurevitch, eds, Design and analysis of ecological experiments, Chapman & Hall, New York, pp 232-252

McQuate GT, Peck SL. 2001. Enhancement of attraction of alpha-ionol to male Bactrocera latifrons (Diptera: Tephritidae) by addition of a synergist, cade oil. J. Econ. Entomol. 97: 862-870

Messina FJ, Jones VP. 1990. Relationship between fruit phenol-ogy and infestation by the apple maggot (Diptera: Tephritidae) in Utah. Ann. Entomol. Soc. Am. 83: 742-752

Metcalf RL. 1990. Chemical ecology of Dacinae fruit flies (Diptera: Tephritidae). Ann. Entomol. Soc. Am. 83: 1017-1030

Miyazaki S, Boush GM, Baerwald RJ. 1968. Amino acid syn-thesis by Pseudomonas melophthora, bacterial symbiote of Rhagoletis pomonella (Diptera). J. Insect Physiol. 14: 513-518

Moericke V, Prokopy RJ, Berlocher S, Bush GL. 1975. Visual stimuli associated with attraction of Rhagoletis pomonellaflies to trees. Entomol. Exp. Appl. 18: 497-507

Morgante JS. 1991. Mosca-das-frutas (Tephritidae): característi-cas biológicas, detecção e controle. Boletim Técnico de Recomendações para os Perímetros Irrigados do Vale do São Francisco, Brasília 2: 19

Mumford JD. 2004. Economic analysis of area-wide fruit fly management. In B Barnes, M Addison, eds, Proceedings of the 6th International Symposium on Fruit Flies of Economic Importance, Stellenbosch, South Africa, 6-10 May 2002. Infruitec Press, Stellenbosch, South Africa

Muñoz RJA. 2000. Patogenicidad de Beauveria bassiana (Bals.) Bullí. sobre la mosca del mediterráneo, Ceratitis capitata (Wied.) en condiciones de laboratorio. Tesis de Licenciatura. Facultad de Ciencias Agrícolas. Univ. Aut. de Chiapas. Huehuetán, Chis, México. p 55

Munro J. 1953. Stridulation in the Queensland fruit-fly Dacus (Strumeta) tryoni (Frogg.). Aust. J. Sci. 16: 60-62

Mwatawala MW, De Meyer M, Makundi RH, Maerere AP. 2006a. Biodiversity of fruit flies (Diptera: Tephritidae) in orchards in different agro-ecological zones of the Morogoro region, Tanzania. Fruits 61: 321-332

Mwatawala MW, De Meyer M, Makundi RH, Maerere AP. 2006b. Seasonality and host utilization of the invasive Bactrocera invadens (Diptera: Tephritidae) in Central Tanzania. J. Appl. Entomol. 130: 530-537

Myers K. 1952. Oviposition and mating behaviour of the Queensland fruit-fly (Dacus (Strumeta) cacuminatus Hering). Aust. J. Sci. Res. Series B, Biol. Sci. 5: 264-281

Mziray, HA, Makundi, RH, Mwatawalaa M, Maerere A, De Meyer M. 2010. Spatial and temporalabundance of the

solanum fruitfly, Bactrocera latifrons (Hendel), in Morogoro, Tanzania. Crop Protection. 29: 454–461

Nakamori H, Shiga M, Kinjo K. 1993. Characteristics of hot spots of melon fly, Bactrocera (Dacus) cucurbitae Coquillett (Diptera: Tephritidae) in sterile fly release areas in Okinawa Island. Jpn. J. Appl. Entomol. Zool. 37: 123-128

Nestel D, Saidan S, Nemny-Lavi E. 2000. Mass Trapping of the olive fly as an alternative strategy of control. Alon. Hanoteah 54: 302-307

Nishida T. 1955. Natural enemies of the melon fly, Dacus cucur-bitae Coq. in Hawaii. J. Econ. Entomol. 48: 171-178

Nishida T. 1963. Zoogeographical and ecological studies of Dacus cucurbitae (Diptera: Tephritidae) in India. Technical Bulletin No. 54. Hawaiian Agricultural Station, University of Hawaii, Hawaii

Nufio CR, Papaj DR. 2001. Host marking behavior in phy-tophagous insects and parasitoids. Entomol. Exp. Appl. 99: 273-293

Odani Y, Sakurai H, Teruya T, Ito Y, Takeda S. 1991. Sterilizing mechanism of gamma-radiation in the melon fly, Dacus cucurbitae. Res. Bull. Faculty Agric. Gifu Univ. 56: 51-57

Ozaki ET, Kovayashi RM. 1981. Effect of pupal handling during laboratory rearing on adult eclosion and flight capability in three tephritid species. J. Econ. Entomol. 74: 520-525

Palacios R, Martínez-Ferrer MT, Cerda X. 1999. Composición, abundancia y fenologí a de las hormigas (Hymenoptera: Formicidae) en campos de cítricos de Tarragona. Bol. San. Veg. Plagas 25: 229-240

Papadopoulos NT, Katsoyannos BI, Carey JR. 1998. Temporal changes in the composition of the overwintering larval popu-lation of the Mediterranean fruit fly (Diptera: Tephritidae) in Northern Greece. Ann. Entomol. Soc. Am. 91: 430-434

Pawar DB, Mote UN, Lawande KE. 1991. Monitoring of fruit fly population in bitter gourd crop with the help of lure trap. J. Res. Maharashtra Agric. Univ. 16: 281

Permalloo S, Seewooruthun SI, Joomaye A, Soonnoo AR, Gungah B, Unmole L, Boodram R. 1998. An area wide con-trol of fruit flies in Mauritius. In JA Lalouette, DY Bachraz, N Sukurdeep, BD Seebaluck, eds, Proceedings of the Second Annual Meeting of Agricultural Scientists, pp 12-13

Pianka ER. 1970. On r- and K-selection. Am. Nat. 104: 592-597 Pinero JC, Jácome I, Vargas R, Prokopy RJ. 2006. Response of

female melon fly, Bactrocera cucurbitae, to host-associated visual and olfactory stimuli. Entomol. Exp. Appl. 121: 261-269

Poramarcom R, Baimai V. 1996. Sexual behavior and signals used for mating of Bactrocera correcta. Fruit Fly Pests: A world assessment of their biology and management. Delray Beach, St. Lucie Press, pp 51-58

Pritchard G. 1969. The ecology of the natural population of the Queensland fruit fly, Dacus tryoni. II. The distribution of eggs in relation to behavior. Aust. J. Zool. 17: 923-311

Prokopy RJ. 1968. Visual response of apple maggot flies Rhagoletis pomonell: Orchard studies. Entomol. Exp. Appl. 49: 25-36

185

Prokopy RJ. 1976. Feeding, mating and oviposition activities of Rhagoletis fausta flies in nature. Annu. Entomol Soc. Am. 69: 899-904

Prokopy RJ, Boller EF. 1971. Stimuli eliciting oviposition of the European cherry fruit flies, Rhagoletis cerasi (Diptera: Tephritidae), into inanimate objects. Entomol. Exp. Appl. 14: 1-14

Prokopy RJ, Bush GL. 1973. Ovipositional responses to differ-ent sizes of artificial fruit by flies of Rhagoletis pomonella species group. Annu. Entomol. Soc. Am. 66: 927-929

Prokopy RJ, Hendrichs J. 1979. Mating behaviour of Ceratitis capitata on a field-caged host tree. Annu. Entomol. Soc. Am. 72: 642-648

Prokopy RJ, Miller NW, Pinero JC, Barry JD, Tran LC, Oride LK, Vargas RI. 2003. Effectiveness of GF-120 Fruit Fly Bait spray applied to border area plants for control of melon flies (Diptera: Tephritidae) Journal of Economic Entomology.96:1485–1493

Prokopy RJ, Miller NW, Pinero JC, Oride L, Perez N, Revis HC, Vargas RI. 2004. How effective is GF-120 fruit fly bait spray applied to border area sorghum plants for control of melon flies (Diptera: Tephritidae) Florida Entomologist.87:354–360

Prokopy RJ, Poramarcom R, Sutantawong M, Dokmaihom R, Hendrichs J. 1995. Localization of mating behavior of released Bactrocera dorsalis flies on host fruit in an orchard J. Insect Behav. 9: 133-142

Prokopy RJ, Reissig WH, Moericke V. 1976. Marking pheromones deterring repeated oviposition in Rhagoletis flies. Entomol. Exp. Appl. 20: 170-178

Qureshi ZA, Hussain T, Siddiqui QH 1987. Interspecific compe-tition of Dacus cucurbitae Coq. and Dacus ciliatus Loew in mixed infestation of cucurbits. J. Appl. Entomol. 104: 429-432

Raghu S, Clarke AR 2003. Spatial and temporal partitioning of behaviour by adult dacines: Diect evidence for methyl eugenol as a mate rendezvous site for Bactrocera cacuminata.Physiol. Entomol. 28: 175-18

Raghu S, Drew RAI, Clarke AR. 2004. Influence of host plant structure and microclimate on the abundance and behaviour of a tephritid fly. J. Insect Behav. 17: 179-190

Rahman AKMZ, Alam MZ, Islam MN, Hossain MM. 2003. Studies on the behavior of adult fruit fly (Bactrocera cucur-bitae Coquillett) after emergence from pupae. Bull. Inst. Trop. Agric. Kyushu Univ. 26: 1-9

Raspi A, Iacono E, Canale A, 2002. Variable photoperiod and presence of mature eggs in olive fly, Bactrocera oleae (Rossi) (Diptera Tephritidae). Redia 85: 111-119

Ricklefs RE. 1990. Ecology. Freeman, New York Ricklefs RE. 1997. Comparative demography of new world pop-

ulations of thrushes (Turdus spp.). Ecol. Monogr. 67: 23-43 Roan CC, Flitters NE, Davis CJ. 1954. Light intensity and tem-

perature as factors limiting the mating of the oriental fruit fly. Annu. Entomol. Soc. Am.47: 593-594

Robacker DC, Martínez AJ, García JA, Díaz M, Romero C. 1996. Toxicity of Bacillus thuringiensis to Mexican Fruit Fly

(Diptera: Tephritidae). J. Econ. Entomol. 89: 104-110 Rodrigues-Destéfano RH, Bechara IJ, Messias CL, Piedrabuena

AE. 2005. Effectiveness of Metarhizium anisopliae against immature stages of Anastrepha fraterculus fruitfly (Diptera: Tephritidae). Braz. J. Microbiol. 36: 94-99

Roitberg BD, Prokopy RJ. 1987. Insects that mark host plants. Bioscience 37: 400-406

Roomi MW, Abbas T, Shah AH, Robina S, Qureshi AA, Hussain SS, Nasir KA. 1993. Control of fruit flies (Dacus spp.) by attractants of plant origin. Anzeiger fur Schadling-skunde, Aflanzenschutz, Umwdtschutz 66: 155-7

Sarada G, Maheswari TU, Purushotham K. 2001. Effect of trap colour, height and placement around trees in capture of mango fruit flies. J. Appl. Zool. Res. 12: 108-110

Saunders JE, Webster JM. 1999. Temperature effects on Heterorhabditis megidis and Steinernema carpocapsae infec-tivity to Galleria mellonella. J. Nematol. 31: 299-304

Seewooruthun SI, Permalloo S, Gungah B, Soonnoo AR, Alleck M. 2000. Eradication of an exotic fruit fly from Mauritius. In KH Tan, Area-Wide Control of Fruit Flies and Other Insect Pests. Penerbit Universiti Sains, Malaysia, Penang, pp 389-394

Seewooruthun SI, Sookar P, Permalloo S, Joomaye A, Alleck M, Gungah B, Soonnoo AR. 1998. An attempt to the eradica-tion of the Oriental fruit fly, Bactrocera dorsalis (Hendel) from Mauritius. In JA Lalouette, DY Bachraz, N Sukurdeep, BD Seebaluck, eds, Proceedings of the Second Annual Meeting of Agricultural Scientists, 12-13 August 1997, pp 181-187

Severin, HP, Severin HC, Hartung WH. 1914. The ravages, life history, weights of stages, natural enemies, and methods of control of the melon fly. Ann. Entomol. Soc. Am. 7: 177-207.

Shapiro-Ilan DI, Fuxa JR, Lacey LA, Onstad DW, Kaya HK. 2005. Definitions of pathogenicity and virulence in inverte-brate pathology. J. Invert. Pathol. 88: 1-7

Shelly TE. 1999. Defense of oviposition sites by female oriental fruit flies (Diptera: Tephritidae). Florida Entomol. 82:.339-346

Shelly TE, Villalobos EM. 1995. Cue lure and the mating behaviour of male melon flies (Diptera: Tephritidae). Florida Entomol. 78: 473-482

Sheng FR, Zhou YS, Zhao HP. 1997. The biological characteris-tics and control of Dacus dorsalis Hendel. J Southwest Forestry College, 12: 85–89

Siderhurst MS, Jang EB. 2006. Female-biased attraction of ori-ental fruit fly, B. dorsalis (Hendel), to a blend of host fruit volatiles from Termanalia catappa L. J. Chem. Ecol. 32: 2513-2524

Sinha P. 1997. Effects of culture filtrates of fungi on mortality of larvae of Dacus cucurbitae. J. Environ. Biol. 18: 245-248

Sinha P, Saxena SK. 1998. Effects of culture filtrates of three fungi in different combinations on the development of Dacus cucurbitae in vitro. Ind. Phytopathol. 51: 361-362

Sinha P, Saxena SK. 1999. Effect of culture filtrates of three fungi in different combinations on the development of the fruit fly, Dacus cucurbitae Coq. Ann. Plant Protect. Serv. 7:

Fruit Flies (Tephritidae) - Ecology, Behaviour and Management186

JCSB 2012 (September) 15 (3) : 169 ~ 188

96-9 Sirjani FO, Edwin EL, Harry KK. 2009. Evaluation of ento-

mopathogenicnematodesagainst the olive fruit fly,Bactrocera oleae (Diptera: Tephritidae). Biological Control. 48, 274–280

Smith HT. 2001. Fruit flies Cooperative control program, Final environmental impact statement. USDA, p385

Soemori H, Tsukaguchi S, Nakamori H. 1980. Comparison of mating ability and mating competitiveness between mass-reared and wild strains of the melon fly Dacus cucurbitaeCoquillet. (Diptera: Tephritidae). Jpn. J. Appl. Entomol. Zool. 24: 246-250

Somata C, Winotai A, Ooi PAC. 2010. Fruit flies reared from Terminalis catappa in Thailand. J. Asia-Pacific Entomol. 13: 27-30

Srinivasan K. 1994. Recent trends in insect pest management in vegetable crops. In GS Dhaliwal, R Arora, eds, Trends Agric. Insect Pest Manag. Christenson pp 345-372

Steck GJ, McPheron BA. 1996. Fruit Fly Pests: A World Assessment of Their Biology and Management. St. Lucie Press, Delray Beach, pp 596

Stonehouse JM, Mumford JD, Verghese A. 2004. Returns to scale in pest suppression and eradication: Issues for the wide-area management of fruit flies in India. In B Subramanyam, VV Ramamurthy, VS Singh, eds, Proceedings of the National Symposium on Frontier Areas of Entomological Research, November 5-7 2003. Indian Agricultural Research Institute, New Delhi, pp 151-158

Sugimoto A. 1979. Smoke emission by the melon fly Dacus cucurbitae Coquillet. Jpn. J. Appl. Entomol. Zool. 23: 40-42

Suzuki Y, Koyama J. 1980. Temporal aspects of mating behav-iour of the melon fly, Dacus cucurbitae Coquillet (Diptera: Tephritidae): A comparison laboratory and wild strains. Appl. Entomol. Zool. 15: 215-224

Tan KH. 2000. Sex pheromone components in defense of melon fly, Bactrocera cucurbitae against Asian house Gecko, Hemidactylus frenatus. J. Chem. Ecol. 26: 697-704

Toledo J, Liedo P, Williams T, Ibarra J. 1999. Toxicity of Bacillus thuringiensis β‚-Exotoxin to Three Species of Fruit Flies (Diptera: Tephritidae). J. Econ. Entomol. 92: 1052-1056

Toledo J, Rasgado MA, Ibarra JE, Gòmez A, Liedo P, Williams T. 2006. Infection of Anastrepha ludens following soil appli-cations of Heterorhabditis bacteriophora in a mango orchard. Entomol. Exp. Appl. 119: 155-162

Tsiropoulos GJ. 1983. The importance of dietary aminoacids on the reproduction and longevity of adult Dacus oleae (Gmelin) (Diptera Tephritidae). Arch. Int. Physiol. Biochim. Biophys. 91: 159-164

Tychsen PH. 1977. Mating behaviour of the Queensland fruit fly, Dacus tryoni (Diptera: Tephritidae) in field cages. J. Aust. Entomol. Soc. 16: 459-465

Tzanakakis ME. 2003. Seasonal development and dormancy of insects and mites feeding on olive: a review. Netherlands. J. Zool. 52: 87-224

Vargas RI. 2003. Effectiveness of GF-120 Fruit Fly Bait spray applied to border area plants for control of melon flies

(Diptera: Tephritidae). J. Econ. Entomol. 96: 1485-1493 Vargas RI. 2004. Hoe effective is GF-120 fruit fly bait spray

applied to border area sorghum plants for control of melon flies (Diptera: Tephritidae). Florida Entomol. 87: 354-360

Vargas RI, Carey JR. 1990. Comparative survival and demographic statistics for wild oriental fruit fly, Mediterranean fruit fly, and melon fly (Diptera: Tephritidae) on papaya. J. Econ. Entomol. 83: 1344-1349

Vargas RI, Walsh WA, Jang EB, Armstrong JW, Kanehisa DT. 1996. Survival and development of the immature stages of four Hawaiian fruit flies (Diptera: Tephritidae) reared at five constant temperatures. Ann. Entomol. Soc. Am. 89: 64-69

Vargas RI, Walsh WA, Kanehira D, Jang EB, Armstrong JW. 1997. Demography of four Hawaiian fruit flies (Diptera: Tephritidae) reared at five constant temperatures. Ann. Entomol. Soc. Am. 90: 162-168

Vargas RI, Walsh WA, Kanehisa D, Stark JD, Nishida T. 2000. Comparative Demography of Three Hawaiian Fruit Flies (Diptera: Tephritidae) at Alternating Temperatures. Ann. Entomol. Soc. Am. 93: 75-81

Vayssières J, Goergen G, Lokossou O, Dossa P, Akponson C. 2005. A new Bactrocera species in Benin among mango fruit fly (Diptera: Tephritidae) species. Fruits 60: 371-377

Vayssières JF, Rey JY, Traore L. 2007. Distribution and host plants of Bactrocera cucurbitae in West and Central Africa. Fruits 62: 391-396

Vayssières JF, Sinzogan A, Adandonon A. 2009a. Range of cultivated and wild host plants of the main mango fruit fly species in Benin. Regional Fruit Fly Control Project in West Africa leaflet

Vayssières JF, Sinzogan A, Korie S, Ouagoussounon I, Thomas-Odjo A. 2009b. Effectiveness of spinosad bait sprays (GF-120) in controlling mango-infesting fruit flies (Diptera: Tephritidae) in Benin. J. Econ. Entomol. 102: 515-521

Verghese A, Knagaraju D, Madhura HS, Kamala Jayanthi PD, Sreedevi K. 2006. Wind speed as an independent variable to forecast the trap catch of the fruit fly, Bactrocera dorsalis.Ind. J. Agric. Sci. 76: 172-175

Vidal-Quist JC, Castañera P, González-Cabrera J. 2009. Diversity of Bacillus thuringiensis Strains Isolated from Citrus Orchards in Spain and Evaluation of Their Insecticidal Activity against Ceratitis capitata. J. Microbiol. Biotechnol. 19: 749-759

Vreysen MJ. 2001. Principles of area-wide integrated tsetse fly control using the sterile insect technique. Medicine for Tropics 61: 397-411

Wackers FL. 2005. Suitability of (extra-) floral nectar, pollen, and honeydew as insect food sources. Plantprovided food for carnivorous insects: protective mutualism and its applica-tions, Cambridge, Cambridge University Press. pp 17-74

Walters ML, Staten RT, Roberson RC. 2000. Pink bollworm integrated management using sterile insects under field trial conditions, Imperial Valley, California. In KH Tan KH, eds, Area-Wide Control of Fruit Flies and Other Insect Pests. Penerbit Universiti Sains Malaysia, Penang, pp 201-206

Weldon C. 2007. Influence of male aggregation size on female

187

visitation in B. tryoni (Froggatt) (Diptera: Tephritidae). Aust. J. Entomol. 46: 29- 34

Weldon CW. 2005. Mass-rearing and sterilization alter mating behaviour of male Queensland fruit fly, Bactrocera tryoni (Froggatt) (Diptera: Tephritidae). Aust. J. Entomol. 44: 158-163

White IM. 2006. Taxonomy of the Dacina (Diptera: Tephritidae) of African and the Middle East. African Entomology Memoir 2:1-156

White IM, Elson-Harris MM. 1992. Dacus (Didacus) ciliatus Loew. In Fruit Flies of Economic Significance: Their identifi-cation and Bionomics, CAB International, Wallingford, UK, pp 329-331

Williams GC. 1966. Adaptation and natural selection. Princeton University Press, Princeton, NJ.

Wong TTY, McInnis DO, Ramadan MM, Nishimoto JI. 1991. Age related response of male melon flies Dacus cucurbitae(Diptera: Tephritidae) to Cue- Lure. J. Chem. Ecol. 17: 2481-2487

Wu WY, Chen YP, Nyang EC. 2007. Chromatic cues to trap the oriental fruit fly, Bactrocera dorsalis. J. Insect Physiol. 53: 509-516

Wyss JH. 2000. Screwworm eradication in the Americas-overview. In KH Tan, eds, Area-Wide Control of Fruit Flies and Other Insect Pests, Penerbit Universiti Sains Malaysia, Penang, pp 79-86

Yang P, Carey JR, Dowell RV. 1994a. Temperature inßuences on the development and demography of Bactrocera dorsalis (Diptera: Tephritidae) in China. Environ. Entomol. 23:971-974

Yang P, Zhou C, Liang G, Dowell RV, Carey JR. 1994b. Temperature studies on a Chinese strain of Bactrocera cucur-bitae (Coquillett) (Diptera: Tephritidae). Pan-Pac Entomol. 70: 269-275

Yang PJ, Carey JR, Dowell RV. 1994c. Tephritid fruit flies in China: Historical background and current status. Pan-Pacific Entomologist 70: 159-167

Ye H. 2001. Distribution of the oriental fruit fly (Diptera: Tephritidae) in Yunnan province. Entomol. Sinic 8: 175-182

Ye H, Liu J. 2005. Population dynamics of the oriental fruit fly, Bactrocera dorsalis (Diptera: Tephritidae) in the Kunming area, southwestern China Insect Sci. 12: 387

Yee WL, Lacey LA. 2003. Stage-specific mortality of Rhagoletis indifferens (Diptera: Tephritidae) exposed to three species of Steinernema nematodes. Biol. Control 27: 349-356

Yoshizawa O. 1997. Successful eradication programs on fruit flies in Japan. Res. Bull. Plant Prot. Serv.Jpn. 33: 10

Zhang ZY, He DY, She YP. 1995. On the population dynamics of oriental fruit fly in Yunnan Province. Acta Phytop. Sinic 22: 210-216

Zucchi RA. 2000. Espécies de Anastrepha, Sinonímias, Plantas Hospedeiras e Parasitóides. In A Malavasi, RA Zucchi, eds, Moscas-das-frutas de Importância Econômica no Brasil. Holos Editora, Ribeirão Preto, pp 41-54

Fruit Flies (Tephritidae) - Ecology, Behaviour and Management188