Issues Concerning the Eradication or Establishment and Biological Control of the Mediterranean Fruit Fly,Ceratitis capitata(Wiedemann) (Diptera: Tephritidae), in California

Classical biological control is suggested as a tool worth developing now for possible future use in the integrated pest management of the Mediterranean fruit fly (Medfly),Ceratitis capitata(Wiedemann), in California. Three factors that impact broadly on developing and implementing such a biological control program are: (1) the question of Medfly establishment, (2) quarantine considerations, and (3) agricultural and urban concerns. Each of these factors and their combined effects must be considered when discussing biological control of Medfly in California as shaped by historical perspectives on Medfly invasions, methods of Medfly eradication, and past biological control efforts against Medfly. We believe that biological control research should play a foundational role in any future Medfly management programs in California. Development of biological control should involve life history studies of Medfly and its natural enemies in their area of endemicity in sub-Saharan, southeast Africa. Medfly has been studied and should continue to be studied in areas it has invaded, because information derived from such studies provides insights into the potential distribution, abundance, and impact of Medfly populations in California. A plan for a biological research program on Medfly and its relatives and a biological control strategy are presented.     

Reproductive biology of Fopius ceratitivorus (Hymenoptera: Braconidae), an egg–larval parasitoid of the Mediterranean fruit fly, Ceratitis capitata (Diptera: Tephritidae)

The reproductive biology of Fopius ceratitivorus Wharton, a recently discovered African parasitoid, was studied in quarantine in Hawaii to facilitate its mass production for biological control of the Mediterranean fruit fly, Ceratitis capitata. Mean longevity of host-deprived and ovipositing females was 17.3 ± 0.9 d and 16.2 ± 0.5 d, respectively. Ovarian maturation peaked at 61.6 mature eggs per female on the fifth day after eclosion and declined thereafter. Mean number of offspring produced per day by mated females was 5.1 ± 0.4, and realized fecundity expressed as total eggs deposited during the female’s life time was 107.8 ± 12.8. Females were more attracted, to and reproduced significantly more, in fruit substrates containing odors of adult flies and eggs rather than fruit substrates artificially inoculated with fly eggs. Our findings suggest that F. ceratitivorus is a promising new parasitoid for biological control of C. capitata in Hawaii.     

Susceptibility of Ceratitis capitata Wiedemann (Diptera: Tephritidae) to Entomopathogenic Fungi and Their Extracts

The effectiveness of seven strains of entomopathogenic fungi against Ceratitis capitata adults was evaluated in the laboratory. Adults were susceptible to five of seven aqueous suspensions of conidia. Metarhizium anisopliae and strain CG-260 of Paecilomyces fumosoroseus were the most pathogenic fungi, with 10-day LD₅₀ values of 5.1 and 6.1 × 10³ conidia/fly, respectively, when applied topically. Sublethal effects on fecundity and fertility of the fungal-exposed females were also studied. The most effective fungus in reducing fecundity was P. fumosoroseus CECT 2705, with reductions on the order of 65% at 1 × 10⁶ conidia/fly. M. anisopliae and Aspergillus ochraceus also showed significant reductions of fecundity (40–50% for most of the assayed concentrations). Fertility was moderately affected by the fungi. M. anisopliae at 1 × 10⁶ conidia/fly was the most effective fungus, showing egg eclosion reduction of over 50% compared with the control. In addition, culture broth dichloromethane extracts from the entomopathogenic fungi were tested for insecticide activity against C. capitata, including effects on fecundity and fertility. The extract from M. anisopliae was the most toxic, resulting in about 90% mortality at a concentration of 25 mg/g of diet; under these conditions, fecundity and fertility of treated females were reduced by 94 and 53%, respectively, compared with untreated controls.     

Conditional embryonic lethality to improve the sterile insect technique in Ceratitis capitata (Diptera: Tephritidae)

Background  

The sterile insect technique (SIT) is an environment-friendly method used in area-wide pest management of the Mediterranean fruit fly Ceratitis capitata (Wiedemann; Diptera: Tephritidae). Ionizing radiation used to generate reproductive sterility in the mass-reared populations before release leads to reduction of competitiveness.     

The Bionomics ofCoptera Haywardi(Ogloblin) (Hymenoptera: Diapriidae) and Other Pupal Parasitoids of Tephritid Fruit Flies (Diptera)

The endoparasitoidCoptera haywardi(Ogloblin) (Diapriidae) was discovered in Mexico attacking the pupae of the Mexican fruit fly,Anastrepha ludens(Loew). Typically, parasitoids of Diptera Cychlorrhapha pupae develop as ectoparasitoids and are generalists that attack hosts in a number of families. Aspects of the bionomics ofC. haywardiwere compared to those of two chalcidoid ectoparasitoids,Dirhinus himalayanusWestwood andSpalangia geminaBoucek.C. haywardideveloped in three genera of Tephritidae, but not in species of other families. The two species of chalcidoids developed in all the calypterate and acalypterate hosts to which they were exposed. In an olfactometerC. haywardipreferredAnastrepha suspensa(Loew) pupae, while the chalcidoids preferred the pupae ofMusca domestica L.This preference inS. geminawas diminished in insects that had been reared onA. suspensa. C. haywardioviposited in theA. suspensapupae that had been previously parasitized by the braconidDiachasmimorpha longicaudata(Ashmead). However, it completed development only in unparasitized pupae. Mortality of the primary parasitoid due toD. himalayanuswas approximately two-thirds the mortality inflicted on the host fly.S. geminadid not discriminate between parasitized and unparasitized pupae ofA. suspensaand developed in both.C. haywardiappears to have a more restricted host range relative to chalcidoid pupal parasitoids and this may be due to its endoparasitic development.     

Biological Control of Anastrepha spp. (Diptera: Tephritidae) in Mango Orchards through Augmentative Releases of Diachasmimorpha longicaudata (Ashmead) (Hymenoptera: Braconidae)

Diachasmimorpha longicaudata (Ashmead) parasitoids were released by air on a weekly basis over 1600 ha of commercial mango orchards, backyard orchards, and patches of native vegetation, at a density of ca. 940 parasitoids/ha. Releases were made during 2 consecutive years, beginning at flower onset and lasting until the end of the production cycle. Two areas, 7 km apart, were compared. In one area parasitoids were released, whereas the other area was used as a control. During the 2nd year treatments were reversed. Fruit was sampled in commercial mango orchards and in backyard orchards to assess levels of parasitism in fruit fly larvae. Highly significant differences in percentage parasitism were found in release and control zones in backyard orchards. Furthermore, trapping results indicated that D. longicaudata releases were associated with ca. 2.7-fold suppression of Anastrepha spp. populations in backyard orchards. Results suggest that suppression might be affected by environmental conditions and by the parasitoid:fly ratio achieved. Anastrepha obliqua McQuart populations were suppressed more effectively by use of parasitoids than those of Anastrepha ludens Loew, perhaps due to the type of host fruits used by each species. Augmentative parasitoid releases in marginal areas surrounding commercial orchards (backyard orchards, wild vegetation) can substantially suppress fly populations. Through this approach, the number of flies that later move into commercial orchards can be significantly reduced. Such a strategy, when combined with sound orchard management schemes, can allow growers to produce clean fruit without the need to resort to the widespread use of insecticides.     

The Distributions of Parasitoids (Hymenoptera) of Anastrepha Fruit Flies (Diptera: Tephritidae) along an Altitudinal Gradient in Veracruz, Mexico

In the state of Veracruz, Mexico, fruits from 38 sites at various altitudes were collected monthly over a period of 2 years, and the tephritid fruit flies of the genus Anastrepha and associated parasitoids that emerged from these fruits were identified and counted. Of the 26 species of fruits that contained Anastrepha larvae, 18 species also contained a total of 10 species of Anastrepha parasitoids. These consisted of 4 native and 1 exotic species of opiine braconid larval–pupal parasitoids, 2 native species of eucoilid larval–pupal parasitoids, 1 exotic species of eulophid larval–pupal parasitoid, 1 exotic species of pteromalid pupal parasitoid, and 1 native species of diapriid pupal parasitoid. Overall parasitism (including flies from fruit species that bore no parasitoids) was 6% and was greatest, 16%, at 600–800 m in altitude. The relative contributions of individual parasitoid species to overall parasitism were frequently influenced by both the altitude (and correlated changes in temperature and precipitation) and the species of plant in which the Anastrepha larvae were found. This was particularly the case among the more abundant and widespread Braconidae. To distinguish the role of altitude from that of the distributions of the host plants, these braconids were examined in 4 individual species of fruit that grew over a broad range of altitudes. In guava (Psidium guajava L.) and “jobo” (Spondias mombin L.) the parasitoid Doryctobracon areolatus (Szepligeti) was relatively more common at low altitudes. Its congener, Doryctobracon crawfordi (Viereck), was relatively more abundant at high altitudes in sour orange (Citrus aurantium L.). Utetes anastrephae (Viereck) became relatively more common at higher altitudes in S. mombin, whereas Diachasmimorpha longicaudata (Ashmead) tended to become relatively rare at the highest altitudes in C. aurantium, but increased at high altitudes in P. guajava compared to other braconids. Different altitudinal patterns of abundance in different fruits suggests the importance of both biotic and abiotic factors in parasitoid distributions. We discuss the effect of an expanding agricultural frontier on parasitoid abundance and relate our findings to the design of a fruit fly biological control program that tailors mass releases to parasitoid climate preferences.     

The Effects of Chilling on the Fecundity and Life Span of Mass-reared Parasitoids (Hymenoptera: Braconidae) of the Mediterranean Fruit Fly, Ceratitis capitata (Wiedemann) (Diptera: Tephritidae)

Suppression of Mediterranean fruit fly (medfly), Ceratitis capitata (Wiedemann), populations may be achieved through the mass-rearing and augmentative aerial release of opiine braconid parasitoids. Typically, aerial release techniques require up to one hour of chilling of adult parasitoids at temperatures as low as 3.5°C prior to their dissemination. Such chilling potentially could affect the subsequent performance of the insects. Among three species of the genus Diachasmimorpha longicaudata (Ashmead), tryoni (Cameron), and krausii (Fullaway) there was little or no affect of chilling in the laboratory on female longevity, production of daughters, or offspring sex ratio. This is consistent with previous experiments that found chilling to have no discernable effect on the short-term mortality of D. tryoni or on its ability to take flight immediately after aerial release. While there was little effect of chilling on longevity and fecundity in a species from another opiine genus, Fopius arisanus (Sonan), exposure to low temperatures did result in a significantly more male-biased offspring sex ratio.     

Effect of Two Opiine Parasitoids (Hymenoptera: Braconidae) Introduced for Fruit Fly Control on a Native Hawaiian Tephritid,Trupanea dubautiae(Diptera: Tephritidae)

Diachasmimorpha longicaudata(Ashmead) andPsyttalia fletcheri(Silvestri) are opiine parasitoids introduced into Hawaii for control of the Oriental fruit fly,Bactrocera dorsalis(Hendel) and the melon fly,Bactrocera cucurbitae(Coquillett), respectively. Both species have recently been mass-reared and released for research in augmentative biocontrol programs. Laboratory and field sleeve cage experiments were conducted to investigate the potential impact of mass-producedD. longicaudataandP. fletcherion a native Hawaiian tephritid,Trupanea dubautiae(Bryan), infesting the flowerheads of the native composite shrubDubautia raillardioidesHillebrand. Gravid females ofD. longicaudataandP. fletcheriwere confined with bloomingD. raillardioidesflowerheads infested with late instarT. dubautiae.BothD. longicaudataandP. fletcherilacked positive oviposition responses toT. dubautiaelarvae in infested flowerheads and caused neither parasitism nor mortality to the flies. However, when larvae were removed from the flowerheads and presented in screened dishes containing artificial diet of the parasitoids' normal rearing hosts (B. dorsalisandB. cucurbitae), bothD. longicaudataandP. fletcherireadily oviposited in the test larvae. Oviposition byD. longicaudatadid not significantly affect the percentage pupation ofT. dubautiae,but did reduce the emergence of adult flies. Oviposition byP. fletcherisignificantly reduced both pupation and adult fly emergence. All progeny of both parasitoid species died as eggs or first-instar larvae. Results from our experiments demonstrate that biological control programs targeted against frugivorous tephritid pests byD. longicaudataandP. fletcherihave no harmful impact on flowerhead-infestingT. dubautiae.     

Soil properties affect the availability, movement, and virulence of entomopathogenic fungi conidia against puparia of Ceratitis capitata (Diptera: Tephritidae)

The Mediterranean fruit fly, Ceratitis capitata Wiedemann (Diptera: Tephritidae), is the major tephritid pest in the Mediterranean region. This insect may overwinter as pupae inside fruits or in soil. Therefore, infection with entomopathogenic fungi is a potentially useful control technique during the insect’s soil-dwelling stage. Entomopathogenic fungi have an important role in Integrated Pest Management programs as an alternative to conventional chemical control, but they have been usually selected on the basis of laboratory results with little regard to fungal ecology. In this work, we designed several experiments to study the availability and movement of the EF Beauveria bassiana (Balsamo) Vuill. and Metarhizium anisopliae (Metsch.) conidia in 16 soils differing widely in pH, texture, organic matter, and carbonate contents. Experiments of adsorption and drag of conidia by soil particles suspended in CaCl₂ solutions of different ionic strength showed B. bassiana conidia to be retained by clay particles, and this effect disappeared with increasing ionic strength. The availability of M. anisopliae conidia in the suspension tended to be lower for sandy than for clayey soils and was not influenced by ionic strength. Regardless of soil properties, over 90% of the added fungal propagules were recovered from the surface layer of columns of packed soils representing model combinations of texture (sandy or clayey) and pH values (acid or alkaline). However, retention of B. bassiana conidia in the surface layer was higher in clayey than in sandy soils, and the retention of M. anisopliae conidia in the surface layer was higher in sandy than in clayey soils. Finally, neither soil texture nor ionic strength affected the infectivity of conidia of both fungal strains to C. capitata puparia.     

Artificial diets for rearing the coconut hispine beetle,Brontispa longissima (Coleoptera: Chrysomelidae), and their suitability to two specialist parasitoids

The coconut hispine beetle, Brontispa longissima (Gestro), is a serious invasive pest that infests young unopened fronds of coconut palms (Cocos nucifera L.) in Southeast Asia. We previously developed the first artificial diet for rearing B. longissima larvae, which contained a leaf powder of young coconut fronds. Because the fronds are required for healthy growth of coconut palms, it is necessary to reduce their use for rearing the beetles. In this study, we tested two new artificial diets for the beetle larvae, which contained the leaf powders of mature coconut leaves or orchard grass (Dactylis glomerata L.). Brontispa longissima successfully developed from hatching to adulthood on both the mature coconut leaf diet and orchard grass diet. The beetles reared on the mature coconut leaf diet and orchard grass diet developed faster than those reared on the young coconut leaf diet. Fecundity and egg hatchability of beetles did not differ among the three diet treatments. We then examined the suitability of beetle larvae or pupae reared on each diet as hosts for two specialist endoparasitoids, Asecodes hispinarum Boucek and Tetrastichus brontispae Ferriere. The survival rate from oviposition to adult emergence for A. hispinarum was 43.8% in hosts reared on a young coconut leaf diet, 77.1% on a mature coconut leaf diet, and 85.7% on an orchard grass diet. For T. brontispae, the survival rate was 70.0% in hosts reared on the young coconut leaf diet, 38.1% on the mature coconut leaf diet, and 66.7% on the orchard grass diet. Our results indicate these artificial diets can be useful for rearing B. longissima and its two parasitoids, helping to reduce the costs of mass rearing these insects.     

Evaluation of Entomopathogenic Nematodes for the Control of Mediterranean Fruit Fly (Diptera: Tephritidae)

The virulence of various entomopathogenic nematode (EPN) strains was evaluated against the Mediterranean fruit fly, C. capitata . The selected nematodes were assessed for their infectivity for the final larval stage of the insect host and under varying environmental conditions. Among 12 EPN strains tested, Steinernema riobrave Texas ( Sr TX) and Heterorhabditis sp. IS-5 (H IS-5), showed high activity and induced >80% mortality. Six EPN strains showed limited activity (>30% mortality), and four strains had no effect (<20% mortality). Sr TX was more effective than H IS-5. Mature C. capitata larvae were most susceptible to nematode infection during the first 4h after they began to emerge from their diet to pupate. Activity of the two nematode strains at a constant inoculation rate was dependent on insect larval density. The highest activity was recorded at 1.88 larvae cm -2 and decreased at higher larval densities. EPN activity was also directly related to nematode density. Maximal activity was shown at a density of 150 infective juveniles cm -2 . A similar activity pattern was also recorded with Sr TX in four different soil types. The persistence of this EPN in the soil extended over 5 days but there was no activity after 14 days. Except for a lower activity under cool conditions (17°C), temperatures ranging between 22 and 41°C, or moisture levels in the treated soil ranging between 3 and 20%, had no significant effect on nematode activity. Our results suggest that application of Sr TX against C. capitata may have potential for controlling C. capitata .     

Release of Sterile Mediterranean Fruit Flies, Ceratitis capitata (Wiedemann) (Diptera: Tephritidae), Using an Automated Ground Release Vehicle

A trial was conducted in Tampa, Florida to test an automated ground release machine as an alternative to aerial methods for release of sterile Mediterranean fruit flies, Ceratitis capitata (Wiedemann). Twenty-four Jackson traps baited with trimedlure at three release sites yielded lower than expected numbers of ground released Medflies. Recaptures per trap ranged from 2.8 (±0.7 S.E.) to 6.8 (±1.7 S.E.). Average recovery of sterile flies at each site for all releases combined (144 observations) was similar, 3.4 (±0.5 S.E.), 4.4 (±0.5 S.E.), 4.5 (±0.5 S.E.) for sites 1, 2 and 3 respectively. There was a significant reduction in flight ability from 67.5 (±2.1 S.E.) to 53.6 (±2.9 S.E.)%, from the time of pre-chilling to when immobilized flies were released after 2.5 h in the release container. Further tests are needed to determine what mortality factors may influence recovery and how the automated ground release machine compares to the aerial release method.     

Scent Marking by Males of the Mediterranean Fruit Fly, Ceratitis capitata (Diptera: Tephritidae)

Males of the Mediterranean fruit fly, Ceratitis capitata (medfly), defend individual leaves as mating territories. While perching, males release an air-borne pheromone (known to attract females) from everted rectal epithelium at the tip of the abdomen. Males also occasionally touch the substrate with the tip of their abdomen. The main objective of the present study was to determine whether such abdomen dipping was a form of intersexual signaling, i.e., whether this action resulted in increased female visitation to the territory. Following observations on the frequency of pheromone calling and abdomen dipping of individually marked males, I ran a standard set of experiments using leaves from four different plant species. Leaves were exposed to varying numbers of (mature) males and females, respectively, for varying durations, and female settlement was compared on exposed versus nonexposed leaves in laboratory cages. Exposing leaves to females had no, or little, influence on female distribution for any of the four plant species. Exposing leaves to males had little influence on subsequent female settlement for orange, coffee, or macadamia trees. However, leaves of the fig tree Ficus bejamina that were exposed to males were much more attractive to females than nonexposed leaves. I then conducted a series of additional tests using fig leaves and found that i) leaf exposure to immature males had no effect on female distribution, ii) leaf exposure to mature males for as little as 90 min increased leaf attractiveness to females, iii) prohibiting males direct contact with the leaf during exposure eliminated any effect on female settlement, and iv) females discriminated between exposed and nonexposed leaves even in physically complex environments (i.e., potted plants). The possible role of abdomen dipping in sexual advertisement of male medflies is discussed.     

Evaluation of the efficacy of Trichogramma evanescens Westwood (Hym., Trichogrammatidae) inundative releases for the control of Maruca vitrata F. (Lep., Pyralidae)

Abstract: The bean podborer, Maruca vitrata (F.), is a serious pest on leguminous crops in the tropics. There are several natural enemies of M. vitrata present in the Philippines, but none of them suppress pest populations naturally below an economic threshold. The egg parasite Trichogramma evanescens Westwood is commercially available for augmentative biological control and a known parasite of podborer eggs. The objective of the present study was to evaluate the efficacy of inundative releases of the egg parasite T. evanescens for controlling M. vitrata in the Philippines. In 1999 and 2000, controlled releases of T. evanescens were made in fields of yardlong bean, Vigna unguiculata, during the dry and rainy seasons in Central Luzon, Philippines. Adult populations of M. vitrata were monitored using light traps. Population density of M. vitrata was found to be positively correlated with rainfall and was subsequently higher during the rainy season, relative to that in the dry season. In quality control experiments, emergence of locally available T. evanescens was found to be highly variable between years, 72% in 1999 and 58% in 2000. The percentage of female parasites was 54% in both years. Survival of T. evanescens in the laboratory after 7 days was found to be only 29 and 21% in 1999 and 2000, respectively. Four parasite releases (each 150 000 wasps per hectare) spaced 7 days apart during the reproductive stage of V. unguiculata were made in three 5 × 5 m plots. Host finding efficacy was identified by exposing M. vitrata eggs laid on cowpea leaves in rearing chambers for 24 h in the fields. Percentage parasitism was higher during the dry season, relative to that in the rainy seasons. In release plots, parasitism increased by 53% during dry and by 43% during rainy season compared with control plots. Despite significant reductions in larval numbers during the dry season, no difference in percentages of pods damaged was found. In the rainy season, the number of larvae per plant and the percentage of pods damaged by M. vitrata larvae were not reduced by T. evanescens releases. The experimental results are critically discussed as a possible part of an integrated pest management system.     

Improvement of quality control methods for augmentative releases of the fruit fly parasitoids,Diachasmimorpha longicaudata and Psyttalia fletcheri (Hymenoptera: Braconidae)

Criteria were established to improve quality control methods for augmentative releases of the opiine parasitoids, Diachasmimorpha longicaudata (Ashmead) and Psyttalia fletcheri (Silvestri). These included correlating puparial weight with adult emergence and sex ratio at the Honolulu rearing facility, and determining the effect of air shipments and field releases on parasitoid emergence and subsequent mortality. There was a positive relationship between the weight of 7–10‐day‐old host puparia and percentage of emergence for both D. longicaudata and P. fletcheri. Standardization of shipping methods included placement of ice blocks in the top levels of the ice chests, prompt shipment and pick‐up of samples, and cooling of puparia before shipment to minimize metabolic heat generated in the samples, and to delay emergence of samples. Before standardization, emergence losses of up to 58% were observed for D. longicaudata and 18% for P. fletcheri. When shipping methods were standardized, emergence was no longer reduced. In addition, low emergence rates were associated with reduced flight propensity of D. longicaudata (R_s = ‐ 0.45 at Kilauea and ‐ 0.54 at Kealia). At the two release sites, 88–95% of adult D. longicaudata that did not escape the release containers were males.     

Response of Three Hymenopteran Parasitoids Introduced for Fruit Fly Control to a Gall-Forming Tephritid,Procecidochares alani(Diptera: Tephritidae)

The response of three larval–pupal parasitoids,Diachasmimorpha longicaudata(Ashmead),Diachasmimorpha tryoni(Cameron), andTetrastichus giffardianusSilvestri, to the Hamakua pamakani gall fly,Procecidochares alaniL., was determined in the laboratory. We also observed responses of these parasitoids to their normal rearing hosts,Bactrocera dorsalis(Hendel) andCeratitis capitata(Weidemann).D. tryonilanded on pamakani galls or on dishes containingP. alanilarvae as frequently as on dishes containingC. capitata.In contrast,D. longicaudataonly rarely landed on the galls.D. tryoniandD. longicaudataoviposited in galls in fewer than 1% of our observations.D. longicaudataprobedP. alanilarvae as frequently asB. dorsalislarvae, but no parasitoid offspring were observed.D. tryonioviposited more frequently inC. capitatathanP. alani.NoD. tryonideveloped inP. alanilarvae.T. giffardianuslanded on pamakani galls andP. alanilarvae more frequently than any other host substrate. In contrast,T. giffardianusentered galls with artificially opened windows one time in 10 observations. We observed 12% parasitism ofP. alanilarvae dissected from the galls and 20% of parasitismP. alaniin the windowed galls. We discuss the implications of our results for future augmentative or classical biological control studies.