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.     

Fruit fly parasitoids in coffee in Mpumalanga Province,South Africa

Bracon celer, Psyttalia perproxima, Psyttalia humilis (all Hymenoptera: Braconidae) and Tetrastichus giffardianus (Hymenoptera: Eulophidae) were reared from fruit flies (Diptera: Tephritidae) infesting Coffea canephora in Mpumalanga, South Africa. Psyttalia perproxima and T. giffardianus were recorded for the first time from southern Africa. Ceratitis capitata was likely the main tephritid host.     

Predation potential of the earwig Euborellia annulipes on fruit fly larvae and trophic interactions with the parasitoid Diachasmimorpha longicaudata

The earwig Euborellia annulipes (Lucas) (Dermaptera: Anisolabididae), a generalist predator, has been observed in fruits infested with fruit fly larvae, which are frequently parasitized by parasitoid wasps. Neither the capacity of earwigs to predate on fruit flies nor intraguild interactions between earwigs and fruit fly parasitoids have been investigated. Here, we studied in laboratory conditions the predation on the fruit fly Ceratitis capitata (Wiedemann) (Diptera: Tephritidae) by the earwig E. annulipes, and whether parasitism of fruit fly larvae by the parasitoid wasp Diachasmimorpha longicaudata (Ashmead) (Hymenoptera: Braconidae) influences predation by the earwig. We evaluated the predation capacity, functional response and prey preference of E. annulipes for parasitized and non-parasitized fruit fly larvae in choice and no-choice tests. We found that earwigs prey on second- and third-instar larvae and pupae of C. capitata and consumed larger numbers of second-instar larvae, followed by third-instar larvae and pupae. Females prey on larger numbers of fruit flies than did males, regardless of the prey developmental stage, but both sexes exhibited a type II functional response. Interestingly, males killed but did not consume fruit fly larvae more than did females. In no-choice tests, earwig females consumed equal numbers of parasitized and non-parasitized fruit fly larvae. However, in choice tests, the females avoided feeding on parasitized larvae. Subsequent tests with hexane-washed parasitized and non-parasitized larvae showed that putative chemical markings left on fruit flies by parasitoids did not drive the earwig preference towards non-parasitized larvae. These findings suggest that E. annulipes is a potential biological control agent for C. capitata, and that, because the earwig avoids consuming larvae parasitized by D. longicaudata, a combination of the two natural enemies could have an additive effect on pest mortality.     

Biological assessment of Tetrastichus brontispae,a pupal parasitoid of coconut leaf beetle Brontispa longissima

To control coconut leaf beetle, Brontispa longissima (Gestro), the pupal parasitoid Tetrastichus brontispae Ferrière was imported from Taiwan and its biology was studied in quarantine in Hainan, China. The parasitoid development includes an egg, three larval instars and three pupal stages. Its developmental time from egg to adult was 19.5±0.5 days under conditions of 24±2°C and 75±5% relative humidity (RH). Temperature had no effect on the sex ratio of offspring, but significantly affected the parasitism rate and reproduction. The parasitism rates were 98.07, 97.97 and 95.03% at 28, 24 and 20°C, respectively, whereas the parasitism rate was 52.18% at 18°C and 69.48% at 30°C, respectively. Furthermore, the parasitoids reared at 18 and 30°C produced fewer offspring than those at 20, 24 and 28°C, respectively. With the increase in temperature, developmental time decreased linearly from 46.19 days at 18°C to 17.10 days at 28°C. RH significantly influenced development, parasitism rate and the reproduction of T. brontispa. With the decrease of RH, developmental time increased from 22.94 days at 20% RH to 18.84 days at 95% RH. In contrast, parasitism rate and the number of offspring per female increased with the increase of RH. Though emergence rates between 50 and 95% RH were much higher than those between 20 and 35% RH, the sex ratios between 20 and 95% RH were not different. Photoperiod had no effect on parasitism, the number of offspring per female, emergence and the sex ratio of T. brontispae, but developmental time was significantly different for different photoperiods. Sucrose, honey and glucose significantly enhanced adult longevity, parasitism and the number of offspring per female of T. brontispae, but had no effect on the sex ratio and survival. Females of T. brontispae only parasitized fourth to fifth larval instars and 1–5-day-old pupae, but there was a significant difference in the number of offspring per female, development time, emergence and the sex ratio of offspring in different instars. These results showed that 1-day-old pupae, a temperature of 24–28°C and 65–95% RH were optimal for T. brontispae. These findings should be helpful in developing a production system to rear and release T. brontispae in large enough quantities to effectively control coconut leaf beetle.     

The ground beetle Pseudophonus rufipes revealed as predator of Ceratitis capitata in citrus orchards

The Mediterranean fruit fly Ceratitis capitata (Wiedemann) is a major citrus pest in Spain. Although medfly is being controlled chemically, alternative biorational strategies should be developed, like those based on conservation biological control of polyphagous predators. The ground beetle Pseudophonus rufipes (De Geer) is the most abundant carabid inhabiting the ground of citrus orchards in eastern Spain. However, little is known about its activity–density and predatory role against C. capitata in the citrus agroecosystem. Here, we report on its predatory potential on the medfly’s developmental stages that take place in the citrus ground. This carabid species preyed efficiently on C. capitata third instar larvae and especially on pupae but not on teneral adults. Moreover, predation under field conditions was evaluated by detecting C. capitata DNA remains using PCR-based gut-content analysis. Half-life DNA detectability of C. capitata was of 32.33 h. Pseudophonus rufipes specimens were field-collected after C. capitata sterilized pupae were deployed in a commercial citrus orchard. Thereafter, the carabids captured by pitfall traps were analyzed, being DNA-remains of C. capitata detected in 22.2% of them. Data reported here clearly suggest that P. rufipes could play an important role in regulating medfly populations in citrus orchards. This information is particularly useful when biological control conservation strategies are being considered to control this pest.     

The Ability of Coptera haywardi (Ogloblin) (Hymenoptera: Diapriidae) to Locate and Attack the Pupae of the Mediterranean Fruit Fly, Ceratitis capitata (Wiedemann) (Diptera: Tephritidae), under Seminatural Conditions

In Latin America, the diapriid Coptera haywardi (Ogloblin) attacks the pupae of tephritid fruit flies. Anastrepha spp. are among its natural hosts, but in the laboratory it also develops in the exotic Mediterranean fruit fly, Ceratitis capitata (Wiedemann). Field cage tests demonstrated that C. haywardi could locate and parasitize Mediterranean fruit fly pupae under seminatural conditions as found in a Guatemalan coffee plantation. A mean of 18.3% of the pupae buried artificially at depths of 5 mm were parasitized by C. haywardi, while those buried at 15 mm suffered 3.2% parasitism. In a laboratory experiment, larvae that buried themselves to pupate were not significantly more likely to be parasitized than artificially buried pupae, although they may have left a physical or chemical trail that betrayed their presence. Thus, the artificial burial of pupae is unlikely to grossly underestimate C. haywardi efficacy in the field. Another field cage test found that mortality levels due to unsuccessful parasitoid attacks were similar to those resulting from successful parasitism. Thus, the actual effect of a mass-release might be considerably greater than that suggested from parasitism data alone. The results are considered sufficiently positive to encourage further testing of C. haywardi as a biological control agent of the Mediterranean fruit fly.     

Acceptance and suitability of different host stages of Ceratitis capitata (Wiedemann) (Diptera: Tephritidae) and seven other tephritid fruit fly species to Tetrastichus giffardii Silvestri (Hymenoptera: Eulophidae)

Tetrastichus giffardii Silvestri is a gregarious eulophid endoparasitoid of several tephritid fruit fly species. Host stage suitability was studied using nine age groups of Ceratitis capitata (Wiedemann) (Diptera: Tephritidae), namely, eggs less than 24 h and between 24 and 48 h old, and 1- to 7-day-old larvae. Life table studies for T. giffardii using C. capitata as host were done at 26 ± 5 °C and 55–60% RH. Egg load in relation to age of the female parasitoid was also assessed as was the effect of host deprivation on adult longevity. Host acceptance and suitability were examined with respect to eight species of tephritids. Potential hosts so tested were five Ceratitis species, the Medfly, C. capitata, the mango fruit fly, Ceratitis cosyra (Walker), the Natal fruit fly, Ceratitis rosa Karsch, Ceratitis fasciventris (Bezzi), and Ceratitis anonae Graham; two Bactrocera species, the melon fruit fly, Bactrocera cucurbitae (Coquillett) and the newly invasive Bactrocera invadens Drew, Tsuruta, and White; and one Dacus species, the lesser pumpkin fly, Dacus ciliatus Loew. No parasitoids were obtained from eggs while all larval stages were suitable though at varying degrees. Parasitism and number of progeny was related to host age in a curvilinear manner with maxima at 4- to 5-day-old larvae. By contrast, development time decreased with age of host larvae while sex ratio was not affected. The intrinsic rate of increase was 0.17 ± 0.01; gross and net reproductive rates were 64.9 ± 4.3 and 44.9 ± 3.8, respectively. Non-ovipositing females lived significantly longer than ovipositing ones. The females accepted all host species tested, but only C. capitata, D. ciliatus and, to a much lesser extent, C. cosyra were suitable. In the remaining host species, most eggs were encapsulated. In C. capitata and D. ciliatus, percent parasitism was similar, but number of progeny was lower and the sex ratio, as the proportion of females, was higher when the parasitoid was reared on D. ciliatus. Progeny per puparium were also similar for the two hosts. In the light of these results it can be concluded that T. giffardii has a narrow host range, but it attacks and successfully develops in larvae representing a wide range of ages.     

Susceptibility of the Mediterranean fruit fly (Ceratitis capitata) and the Natal fruit fly (Ceratitis rosa) to entomopathogenic nematodes

The potential of entomopathogenic nematodes, Heterorhabditis bacteriophora, Heterorhabditis zealandica and Steinernema khoisanae, to infect pupariating larvae, pupae and adults of Ceratitis capitata and Ceratitis rosa was investigated in laboratory bioassays. Pupariating larvae and adult flies were susceptible to nematode infection, with no infection recorded for the pupae. Pupariating larvae of C. capitata were generally more susceptible to infection than those of C. rosa. Significantly more larvae of C. capitata were infected by H. bacteriophora. For C. rosa, highest infectivity of larvae was obtained with H. zealandica. In contrast, adults of both species were highly infected by S. khoisanae.     

Parasites of rice stemborers in Sarawak (Malaysian Borneo)

Observations on parasites were made during a study of the following rice stem-borers in Sarawak (Malaysian Borneo):Tryporyza incertulas (Walker),T. innotata (Walker),Chilo suppressalis (Walker)C. auricilia (Dudgeon), andSeamia inferens (Walker). Egg-parasitism was often high, but that of the larval and pupal stages generally very low. Between 40–80% of theTryporyza eggs were parasitised byTelenomus rowani (Gahan), while 30–50% were attacked byTetrastichus schoenobii Ferrière. About 40–90% of the eggs ofChilo were parasitised byTrichogramma? japonicum Ashmead and 5–26% byTelenomus dignus (Gahan). Only 0.4–3% of theTryporyza larvae were parasitised by a Braconid,Rhaconotus schoenobivorus (Rohwer), whileBracon chinensis Szepligeti attacked 0.2–0.7% of the larvae ofC. suppressalis. Parasitism ofSesamia larvae byApanteles flavipes Cameron was equally low, never exceeding 2%. Pupal parasitism was somewhat higher.Tetrastichus israeli (Mani & Kurian) attacked 8% and 18% of the pupae ofC. suppressalis andS. inferens, respectively, while the Ichneumonid,Xanthopimpla stemmator (Thunberg) attacked up to 3% of the pupae of the former species. The immature stages of some of these parasites are described.     

Patterns of resource distribution among conspecific larvae in two fruit fly species: Anastrepha fraterculus and Ceratitis capitata (Diptera: Tephritidae)

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Field parasitism of Ceratitis capitata larvae by Aganaspis daci in Chios, Greece

High parasitism rates were recorded in the Mediterranean fruit fly, Ceratitis capitata (Wiedemann) (Diptera: Tephritidae) in pupae derived from field infested figs, on the Greek island of Chios in 1999 and 2000. Adult parasitoids were identified as Aganaspis daci (Weld) (Hymenoptera:Eucoilidae), previously known as Trybliographa daci (Weld). Approximately 45%of C. capitata pupae yielded adultparasitoid in both years and the totalmortality of pupae due to the parasitoid was62–65%. Development of male A. daci at25°C, reared on 3rd instar larvaeof C. capitata, was shorter than that of the female (34 and 37 days respectively). Average adultmale longevity was 4–5 days longer than female(16–17 to 11–12 days, respectively) and almostidentical in wild and F₁ parasitoids ofboth sexes. We suggest that A. daci maybe an efficient form of biological control ofC. capitata in the Mediterranean regionand probably in other areas.     

Parasitism by Coptera haywardi and Diachasmimorpha longicaudata on Anastrepha flies with different fruits under laboratory and field cage conditions

Larvae of Anastrepha ludens and A. serpentina that developed in mango and sapodilla fruits, respectively, were exposed to Diachasmimorpha longicaudata (Ashmead) (Hymenoptera: Braconidae) and sequentially exposed as pupae to Coptera haywardi (Oglobin) (Hymenoptera: Diapriidae). Sequential exposure to both parasitoid species contributed to a decrease in fruit fly emergence due to higher levels of parasitism, which varied according to fruit type. In creole mango, D. longicaudata represented the highest percentage of parasitism. C. haywardi parasitism was greater in pupae from Ataulfo mangos and sapodilla, where the pulp size and volume may have acted as a refuge, allowing fly larvae to escape and leaving a greater number of unparasitised pupae available to C. haywardi. Similar results were obtained under field cage conditions, but the level of parasitism by C. haywardi was lower, suggesting that its effectiveness has some limitations under natural conditions. Our results suggest that both species can exert complementary parasitism, which represents an alternative worth to investigate under open field conditions.     

Low Temperature Storage of <Emphasis Type="Italic">Telenomus remus</Emphasis> (Nixon) (Hymenoptera: Platygastridae) and its Factitious Host <Emphasis Type="Italic">Corcyra cephalonica</Emphasis> (Stainton) (Lepidoptera: Pyralidae)

We conducted three bioassays to evaluate the effect of low-temperature storage of eggs (host) and pupae and adults (parasitoid) on the biology and parasitism capacity of the egg parasitoid Telenomus remus (Nixon) (Hymenoptera: Platygastridae). Viable stored Corcyra cephalonica (Stainton) (Lepidoptera: Pyralidae) eggs were parasitized to the same degree or even higher than fresh eggs when stored until 14 days at 5°C or until 21 days at 10°C. In contrast, the percentage of parasitized sterilized eggs was equal to the control only when stored for 7 and 14 days. Survival of T. remus pupae declined with storage time at both studied temperatures (5 and 10°C). However, after 7 days of storage, survival of pupae was still 86.3 and 64.9% at 10 and 5°C, respectively. The number of adult male survivors remained similar until the fourth storage day at both 5 and 10°C. In contrast, female survival did not differ until day 8 at 10°C or day 6 at 5°C. Parasitism capacity of stored adults was not altered by storage compared with the control. Therefore, we conclude that the maximal storage time at 10°C is 21 days for viable C. cephalonica eggs and 7 days for T. remus pupae, while parasitoid adults should not be stored for more than 4 days at either 5 or 10°C.     

Variation of superoxide dismutases during the development of the fruit fly Ceratitis capitata L.

Superoxide dismutase levels were estimated in eggs, larvae and pupae of the fruit fly $\text{Ceratitis capitata}$, as well as in adult flies. No changes occur in the first three stages, but development of the adult fly is accompanied by a large increase in mitochondrial superoxide dismutase per gm of material, and a much smaller relative increase in the cytoplasmic enzyme.     

Life history and life table of the host-feeding parasitoid <Emphasis Type="Italic">Hemiptarsenus varicornis</Emphasis> (Hymenoptera: Eulophidae)

Hemiptarsenus varicornis (Girault), a destructive host-feeding wasp, is an important biocontrol agent/larval ectoparasitoid of agromyzid leafminers worldwide. In the present study, the life history and life table of H. varicornis reared with Liriomyza trifolii (Burgess) were studied at a constant 27 °C. The developmental durations of female and male eggs, larvae, prepupae, pupae and total immature wasps were 1.00 and 1.00, 2.57 and 2.62, 0.45 and 0.37, 3.88 and 3.52, and 7.90 and 7.52 days, respectively. This wasp showed three types of host-killing behavior: reproductive parasitization (parasitism), non-reproductive host feeding (host feeding), and host stinging without oviposition or feeding (host stinging), resulting in 133.9, 303.8, and 84.2, respectively, killed host larvae. We confirm that H. varicornis is a strong synovigenic parasitoid, with an ovigeny index of 0.003. The number of host-feeding events was strongly correlated with parasitism, host-stinging events, longevity and total host mortality. The intrinsic rate of increase, the finite rate of increase, the net reproductive rate, the gross reproduction rate, and the mean length of a generation of H. varicornis were 0.3011/day, 1.3624/day, 66.22 offspring/individual, 168.33 offspring/individual, and 13.56 days, respectively. These results could contribute to a better understanding of the biocontrol efficiency of this destructive host feeder.     

Selectivity evaluation of insecticides used to control tomato pests to Trichogramma pretiosum

The effects of the insecticides abamectin, acetamiprid, cartap and chlorpyrifos on larvae, pupae (within the host egg) and adults of the egg parasitoid Trichogramma pretiosum Riley (Hym.: Trichogrammatidae) were evaluated under laboratory conditions, using three standard tests described by IOBC. When sprayed on the immature stages of this parasitoid, cartap and chlorpyrifos proved to be the most harmful insecticides, affecting both the emergence success and parasitism capacity of this parasitoid, whereas abamectin and acetamiprid were selective. Abamectin was harmful to adults (residue test on glass plates), slightly harmful to larvae, and moderately harmful to pupae (sprayed on the immature stages within host eggs Anagasta kuehniella (Zeller)); acetamiprid was moderately harmful to adults, harmless to larvae, and slightly harmful to pupae; cartap was harmful to adults, moderately harmful to larvae and harmful to pupae; chlorpyrifos to adults, harmless to larvae and harmful to pupae.     

Development of Microplitis bicoloratus on Spodoptera litura and implications for biological control

Microplitis bicoloratus Chen (Hymenoptera:Braconidae:Microgastrinae), a new species of Microplitis Förster from China, is a solitary endoparasitoid of the larvae of the cotton leafworm, Spodoptera litura (Fabricius) (Lepidoptera: Noctuidae). This parasitoid is the first to be successfully reared and evaluated in the laboratory as a potential agent for the biological control of S. litura in China. Oviposition, immature development, and the effects of parasitism on the development of S. litura were studied. In long-term oviposition trials, females laid eggs on S. litura larvae for up to 10 days; oviposition was heavily skewed toward the first few days, with approximately one third of the eggs laid on day 1 and over 50% laid by day 3. This rapid oviposition rate increases the potential for biological suppression of host populations because the likelihood of mortality for the parasites from exposure to detrimental environmental factors or generalist predators increases with time. Immature development of the parasitoid in its host only required 7 days: eggs hatched within 24 h, the first instar larva required 2 days, the second instar larva needed 3 days, and the third instar larvae exited the host and pupated in 1 day, at 27±1°C, 60–80% relative humidity and a 12:12-h (long day) photoperiod. The development of the parasitized hosts was disrupted. When the parasitoid larvae finished development, the body weights of host larvae were significantly reduced regardless of which host instar was parasitized. Our results suggest that M. bicoloratus has considerable potential as a biological control agent for S. litura.     

Assessment of Ceratitis capitata (Diptera,Tephritidae) pupae killed by heat or cold as hosts for rearing Spalangia cameroni (Hymenoptera: Pteromalidae)

In this work, we study the suitability of using dead medfly Ceratitis capitata pupae, killed by heat- or cold-shock, for the mass rearing of Spalangia cameroni, a pupal parasitoid of key pests. 100% mortality of medfly pupae could be accomplished with cold-shock at –20°C for 60 min or with heat-shock at 55°C for 30 min. Neither parasitism percentage nor sex ratio of the offspring differed significantly among heat-shocked, cold-shocked and untreated pupae. In addition, there was no significant difference in the percentage of parasitoids that aborted (♂♂ or ♀♀) among pupal treatments. Some of the pupae were covered with peat because the third larval instar of the medfly buries itself before pupation. However, the buried pupae were not parasitised at a greater or lesser rate than those not covered with peat. The percentage of parasitism was also unaffected by whether the pupae had been killed recently or had been stored at between 4°C and 6°C over 15 or 30 days. The use of dead hosts and later storage permitted the following: (a) the use of hosts over long periods of time; (b) a rapid increase in parasitoid numbers and (c) the availability of pupae killed at the most suitable postpupation times for the production of parasitoids. Furthermore, in biological control projects, the use of dead parasitised pupae in the field avoids the risk of enhancing the pest and allows an increase in parasitism in the field through the use of pupae treated with cold- or heat-shock.     

Effects of temperature on the development and survival of an endangered butterfly,Lycaeides argyrognomon (Lepidoptera: Lycaenidae) with estimation of optimal and threshold temperatures using linear and nonlinear models

The effects of temperature on the development and survival of Lycaeides argyrognomon were examined in the laboratory. The eggs, larvae and pupae were reared at temperatures of 15, 17.5, 20, 25, 30 and 33°C under a long‐day photoperiod of 16‐h light and 8‐h darkness. The survival rates of the first–third instars ranged from 40.0 to 82.4%. The mortalities of the fourth instar were lower than those of the first–third instars. The development time of the overall immature stage decreased from 78.33 days at 15°C to 21.07 days at 30°C, and then increased to 24.33 days at 33°C. The common linear model and the Ikemoto–Takai model were used to estimate the thermal constant (K) and the developmental zero (T₀). The values of T₀ and K for the overall immature stages were 10.50°C and 418.83 degree‐days, and 9.71°C and 451.68 degree‐days by the common model and the Ikemoto–Takai model, respectively. The upper temperature thresholds (T_max) and the optimal temperatures (T_opt) of the egg, the first–third instars and the overall immature stages were estimated by the three nonlinear models. The ranges of T_opt estimated were from 30.33°C to 32.46°C in the overall immature stages and the estimates of T_max of the overall immature stages by the Briere‐1 and the Briere‐2 models were 37.18°C and 33.00°C, respectively. The method to predict the developmental period of L. argyrognomon using the nonlinear models was discussed based on the data of the average temperature per hour.     

Parasitism of Western Corn Rootworm Larvae and Pupae by Steinernema carpocapsae

Virulence and development of the insect-parasitic nematode, Steinernema carpocapsae (Weiser) (Mexican strain), were evaluated for the immature stages of the western corn rootworm, Diabrotica virgifera virgifera LeConte. Third instar rootworm larvae were five times more susceptible to nematode infection than second instar larvae and 75 times more susceptible than first instar larvae and pupae, based on laboratory bioassays. Rootworm eggs were not susceptible. Nematode development was observed in all susceptible rootworm stages, but a complete life cycle was observed only in second and third instar larvae and pupae. Nematode size was affected by rootworm stage; the smallest infective-stage nematodes were recovered from second instar rootworm larvae. Results of this study suggest that S. carpocapsae should be applied when second and third instar rootworm larvae are predominant in the field.