Competition between Diachasmimorpha kraussii and Fopius arisanus in Bactrocera tryoni: does native parasitoid-host association matter?

In Australia Fopius arisanus (Sonan) is an established, but exotic fruit fly egg-larval-pupal parasitoid which co-occurs with Diachasmimorpha kraussii (Fullaway), a native larval-pupal fruit fly parasitoid: both attack the native fruit fly Bactrocera tryoni (Froggatt). In interactions involving evolutionary novel host-parasitoid associations, F. arisanus consistently out-competes other parasitoid species, including D. kraussii. However, in fruit fly-parasitoid systems where there is co-evolutionary history between parasitoids and their hosts, competitive hierarchies can vary. In this study we investigated the outcome of competition between F. arisanus and D. kraussii within B. tryoni, to test whether the close evolutionary relationship between D. kraussii and B. tryoni might circumvent the competitive advantage of F. arisanus. Consistent with previous research, and despite the evolutionary relationship, dissection of multiparasitized B. tryoni larvae showed that D. kraussii was invariably suppressed by F. arisanus. A total of 47% and 74% of the eggs of D. kraussii in presence of F. arisanus were killed within a span of 24 h and 48–72 h, respectively. However, parasitoid emergence from fruit fly hosts exposed sequentially to F. arsianus and D. kraussii suggest that D. kraussii females are able to discriminate hosts already parasitized by F. arisanus. Results show that the co-evolutionary relationship between B. tryoni and D. kraussii does not help overcome the early-acting advantage of the egg parasitoid F. arisanus. Though F. arisanus may not have completely displaced D. kraussii in its native habitat, simultaneous inundative releases of these two parasitoid species (currently under consideration) might not help increase B. tryoni parasitism levels.

     

Intra- and interspecific competition by Fopius arisanus and Diachasmimorpha tryoni (Hymenoptera: Braconidae), parasitoids of tephritid fruit flies

Fopius arisanus (Sonan) and Diachasmimorpha tryoni (Cameron) are two important solitary endoparasitoids of tephritid fruit flies. The former species attacks host eggs while the latter attacks host larvae, and both species emerge as adults from the host puparium. This study investigated intrinsic competition between these two parasitoids, as well as aspects of intraspecific competition within each species in the Mediterranean fruit fly, Ceratitis capitata (Wiedemann). Parasitization by F. arisanus resulted in direct mortality of host eggs and prolonged development of host eggs and larvae. Superparasitism by F. arisanus was uncommon when mean parasitism per host patch was <50%, but increased with rising rates of parasitism. Superparasitism by D. tryoni was more common. In superparasitized hosts, supernumerary individuals of F. arisanus were killed through physiological suppression, while supernumerary larvae of D. tryoni were killed mainly through physical attack. In multiparasitized hosts, dissections showed that 81.6% of D. tryoni eggs in the presence of F. arisanus larvae died within 3 days, indicating physiological inhibition of egg hatch. Rearing results further showed that F. arisanus won almost all competitions against D. tryoni. The ratio of D. tryoni stings to ovipositions was lower in hosts not previously parasitized by F. arisanus than in parasitized hosts, suggesting that D. tryoni can discriminate against parasitized hosts. The mechanism that F. arisanus employs to eliminate D. tryoni is similar to that it uses against all other larval fruit fly parasitoids so far reported. The results are discussed in relation to the competitive superiority of early acting species in fruit fly parasitoids, and to a possible competitive-mediated mechanism underlying host shift by D. tryoni to attack non-target flies following the successful introduction of F. arisanus in Hawaii.     

<Emphasis Type="Italic">Fopius arisanus</Emphasis> oviposition in four <Emphasis Type="Italic">Anastrepha</Emphasis> fruit fly species of economic importance in Mexico

We studied the oviposition performance of Fopius arisanus (Sonan) (Hymenoptera: Braconidae) attacking eggs of four fruit flies of the genus Anastrepha Schiner (Diptera: Tephritidae) under laboratory conditions. The complete process of oviposition on an individual egg of Anastrepha ludens (Loew) lasts in average 85.4 ± 2.9 s, including a tremor (25.8 ± 1.03 s) observed in the middle of this process related to the egg’s descent. The average parasitism of A. ludens egg was 60.9 ± 7.5%, with only 1.2% of superparasitized eggs. During individual acts of oviposition, we noted that F. arisanus possesses a highly flexible ovipositor that curves easily as it searches for additional suitable eggs, which may be of particular benefit when a female finds large clutches of eggs. The individual oviposition of F. arisanus in host fruits attacked by Anastrepha spp. varies with the egg clutch size of each fruit fly species: A. serpentina laid the biggest egg clutches (21.3 ± 1.4), followed by A. ludens (14.2 ± 0.9), and A. striata (1.0 ± 0.0) (=A. obliqua). The time spent by F. arisanus in individual ovipositions was parallel to these findings, reinforcing the idea that F. arisanus attacks several eggs in each individual insertion of its ovipositor. Neither formal oviposition acts, nor adult emergences of F. arisanus were registered in A. obliqua. We discuss the potential of F. arisanus as natural enemy of fruit flies of the genus Anastrepha, and explore the eventual developing of its mass rearing. Handling Editor: Torsten Meiners.     

Opiine parasitoids (Hymenoptera: Braconidae) and biological control of fruit flies (Diptera: Tephritidae) in Australia: Past,present and future

Opiine braconids are parasitoids of the immature stages of frugivorous tephritids. The female wasp lays her eggs into the eggs or larvae of the fruit fly host, where the immature wasp develops before emerging as a next-generation adult from the now dead host pupal case. In support of a new generation of Australian fruit fly parasitoid research, this paper comprehensively reviews what is known about the Australian fruit fly infesting opiines. Based on the most recent taxonomic revision 11 fruit fly infesting opiine species are documented to occur in Australia, but we consider as doubtful the record for Diachasmimorpha longicaudata and consider the record for Fopius illusorius to be tentative without further collections. We identify that the systematics and taxonomy of the Australian native fruit fly infesting opiines are in urgent need of further work. The history of fruit fly biological control in Australia is comprehensively reviewed, including the export of native Australian opiines for fruit fly control elsewhere in the world. Australia was actively involved in three major classical biological control programmes against fruit flies from the turn of the 1900s until the mid-1960s. Despite the introduction of 11 opiine species, plus numerous other natural enemies, only Fopius arisanus established in eastern Australia, where in South-east Queensland it can now cause between 30 and 40% mean parasitism. In addition to the exotic F. arisanus, the native species Diachasmimorpha kraussii and Diachasmimorpha tryoni also cause fruit fly parasitism in agriculturally important crops: both species have also been liberated widely outside of Australia for fruit fly control. Other Australian opiines have not been reared from flies infesting commercial crops and appear biologically restricted to the fruits and environs of Australian east-coast rainforests. The biology literature for D. tryoni and D. kraussii is comprehensively reviewed, while for F. arisanus, already reviewed elsewhere, key literature only is covered. Forward looking, we consider the potential for inoculative or inundative releases of opiines in areas where they do not currently occur to be good, while conservation biological control may help to increase the impacts of parasitoids in areas where they are already established.     

Natural establishment of a parasitoid complex on Bactrocera latifrons (Diptera: Tephritidae) in Hawaii

Bactrocera latifrons (Hendel) (Diptera: Tephritidae) is the most recent of four tephritid fruit fly species accidentally introduced into Hawaii. Although parasitoids have been released against other tephritid fruit fly species and have shown partial success in Hawaii, no parasitoids were released until 2004 to suppress populations of B. latifrons. The present study was conducted to document the parasitoid complex that has naturally established against B. latifrons in Hawaii and to assess whether there is a need for improving the biological control of this species. Based on ripe turkeyberry (Solanum torvum Sw) fruit collections over three consecutive years B. latifrons was the dominant tephritid fruit fly infestating turkeyberry at all four sites surveyed, across three major islands in Hawaii. The overall percentage parasitism of B. latifrons ranged from a low of 0.8% (Hana, Maui) to a high of 8.8% (Kahaluu, Oahu). Five primary parasitoid species were recovered from individually held B. latifrons puparia: Fopius arisanus (Sonan), Psyttalia incisi (Silvestri), Diachasmimorpha longicaudata (Ashmead), D. tryoni (Cameron), and Tetrastichus giffardianus Silvestri. F. arisanus was the predominant parasitoid at three of the four sites. Low levels of parasitism suggest that there is a need to improve biological control of B. latifrons, to minimize chances of this species causing economic impacts on crop production in Hawaii. We discuss the possibility of improving biological control of B. latifrons through augmentative releases of F. arisanus or introduction and release of specific and efficient new parasitoid species.     

Intrinsic inter-specific competition in a guild of tephritid fruit fly parasitoids: Effect of co-evolutionary history on competitive superiority

Tephritid fruit fly parasitoid guilds are dominated by solitary koinobiont species that attack different host stages, but most emerge as adults from host puparia. Previous studies suggest intrinsic competitive superiority by the egg-attacking parasitoid Fopius arisanus (Sonan) against all larval-attacking parasitoids in Hawaii. In this study, we tested the early-acting competitive superiority prediction in relation to the co-evolutionary history of competition between an egg–larval parasitoid (Fopius ceratitivorus Wharton), and each of three larval parasitoids [Psyttalia concolor (Szépligeti), Diachasmimorpha kraussii (Fullaway), and Diachasmimorpha longicaudata (Ashmead)]. F. ceratitivorus and P. concolor share a common origin (eastern Africa), while D. kraussii is an Australian species, and D. longicaudata is from Southeast Asia. The outcomes of intrinsic competition between the egg-attacking parasitoid and each of the three larval-attacking parasitoids within their common host, the Mediterranean fruit fly Ceratitis capitata (Wiedemann) were compared. F. ceratitivorus invariably eliminated the co-evolved P. concolor through physiological suppression of the later-attacking parasitoid’s egg development, providing evidence that supports the early-acting-superiority hypothesis. However, F. ceratitivorus was unable to suppress development of the two non co-evolved larval parasitoids. Instead, the larvae of both later-acting parasitoid species physically killed F. ceratitivorus larvae inside the host. The results suggest that co-evolutionary history influences competitive superiority. The evolution of inter-specific competition and its implications for biological control are discussed.     

Fruit trap: A detection and collection tool for opiine parasitoids (Hym.: Braconidae) of the oriental fruit fly,Bactrocera dorsalis (Dipt.: Tephritidae)

A fruit trap was developed for detection and collection of the opiine parasitoids of the oriental fruit fly,Bactrocera (=Dacus)dorsalis (Hendel). Gravid females ofBiosteres arisanus (Sonan), an egg-larval parasitoid, orDiachasmimorpha longicaudata (Ashmead) andPsytallia incisi (Silvestri), both larval parasitoids, were lured to parasitize the eggs or larvae ofB. dorsalis inoculated in ripe papaya fruits,Carica papaya L. Progenies ofB. arisanus were consistently recovered from papaya fruits inoculated withB. dorsalis eggs (subsequently referred to as egg fruit traps). Except in Moloaa on Kauai (6%), higher percentage ofB. dorsalis parasitization (range=38–43%) was recorded in Hilo, island of Hawaii and Waimanalo and Poamoho, island of Oahu. Progenies ofD. longicaudata and a fewP. incisi were recovered from papaya fruits artificially infested withB. dorsalis larvae (subsequently referred to as larval fruit traps). The recovery of parasitoid progenies from larval fruit traps suspended from papaya trees did not differ significantly from larval fruit traps placed on the ground. In both methods of trap placement, percent parasitization ofB. dorsalis byD. longicaudata (predominant species) ranged from 58–60%. On the other hand, significantly moreB. arisanus thanD. longicaudata andP. incisi adults (larval parasitoids) were recovered from fully ripened to highly deteriorated papaya fruits collected from papaya trees or ground (fallen fruits).     

Oviposition response and development of the egg-pupal parasitoid Fopius arisanus on Bactrocera oleae, a tephritid fruit fly pest of olive in the Mediterranean basin

To date, information is wanting with regard to the use of new exotic parasitoids against olive fruit fly, Bactrocera (=Dacus) oleae (Gmelin) (Diptera: Tephritidae), a serious pest of olives Olea europaea L., in the Mediterranean basin. We investigated the oviposition response and developmental biology on B. oleae of Fopius (=Biosteres) arisanus (Sonan) (=Opius oophilus Fullaway) (Hymenoptera: Braconidae), an egg-pupal parasitoid of tephritid fruit flies, never tested before as a potential parasitoid of this host. Our results showed that olive fruits infested with B. oleae eggs exerted a relevant attraction to gravid F. arisanus and represented a stimulus for oviposition. Nevertheless they were not as attractive to female parasitoids as the Mediterranean fruit fly, Ceratitis capitata Wiedemann (Diptera: Tephritidae), eggs infested papaya fruits (Carica papaya L.). In our experimental conditions, F. arisanus completed development in B. oleae within 33 ± 1.7 days (males) and 35 ± 1.6 (females). Increases in host egg to female parasitoid ratios of 1:1, 5:1, 10:1 and 20:1 corresponded with decreases in the percentage of B. oleae parasitisation and host killing but corresponded also with increases in absolute parasitisation. Our findings are discussed in light of possibilities of utilising F. arisanus for biological control of olive fruit fly.     

Effects of fruit fly host, fruit species, and host egg to female parasitoid ratio on the laboratory rearing of Biosteres arisanus

The host suitability of the oriental fruit fly, Bactrocera dorsalis (Hendel), for development of Biosteres arisanus (Sonan), a braconid parasitoid, was compared with three other fruit fly species, namely, Mediterranean fruit fly, Ceratitis capitata Weidemann, melon fly, Bactrocera cucurbitae Coquilett, and Malaysian fruit fly, Bactrocera latifrons (Hendel). In addition, effects of five different fruit species, namely, Carica papaya L. (solo papaya), Musa sapientum (L.) O. Ktze. (apple banana), Mangifera indica (L.) (Haden mango), Terminalia catappa (L.) (false kamani), and Citrus aurantiifolia (Christman) Swingle (common lime), on the parasitization rate of B. dorsalis and sex ratio of parasitoid progenies were evaluated. Effects of host egg to female B. arisanus ratios on parasitoid progeny yields were likewise determined. The host suitability of fruit flies for development of B. arisanus was ranked as: B. dorsalis>C. capitata=B. latifrons=B. cucurbitae. Based on percent parasitization of B. dorsalis, preference of B. arisanus females for host eggs varied with fruit species, however, preferential oviposition displayed by female parasitoids did not influence sex ratios of subsequent parasitoid progenies. Increases in host egg to female parasitoid ratios of 5:1, 10:1, 20:1, 25:1, and 30:1 corresponded with increases in parasitoid progeny yield reaching a plateau at 20:1.     

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.     

Implications of host mortality on the economics of Fopius arisanus (Hymenoptera: Braconidae) mass rearing

Fopius (= Biosteres) arisanus (Sonan) (= Opius oophilus Fullaway) is an egg-pupal parasitoid of tephritid fruit flies. Our breakthrough in the development of a laboratory-adapted strain of F. arisanus facilitated insectary rearing of parasitoids in large numbers. First colonized in captivity in 1989, F. arisanus has been reared routinely on the oriental fruit fly, Bactrocera (= Dacus) dorsalis (Hendel), its natural host. Parasitization by F. arisanus results in the latent death of developing hosts. Host mortality data are presented in a life table to estimate cost of parasitization on the economics of F. arisanus mass rearing. Percent kills of 10, 32, and 76% exerted by F. arisanus on the egg, larval, and pupal stages of the rearing hosts, respectively, resulted in a mean parasitoid recovery of 23.6%. The production cost was estimated by integrating life table data with the costs of rearing supplies and materials and personnel-hours requirements. Production of 1 million parasitoid adults requires the exposure of 4.2 million B. dorsalis eggs (= propagation hosts). We estimated the cost of producing 1 million parasitoids to be $2,363.30 and identified the most expensive aspects of F. arisanus rearing. Recommendations for streamlining the rearing process to reduce costs are provided.     

Host species and vegetable fruit suitability and preference by the parasitoid wasp Fopius arisanus

Parasitoids that oviposit in a concealed host inside a plant part need to be able to find both the plant and the host. Egg parasitoids of fruit‐infesting Tephritidae need to assess the oviposition site based both on the host egg and the infested fruit. Infestation by Tephritidae fruit flies threatens fruit and vegetable production. Management methods have been implemented including biological control, using Fopius arisanus Sonan (Hymenoptera: Braconidae). The parasitism by F. arisanus in three Tephritidae flies in vegetable fruits was investigated. Laboratory assays were conducted to assess the parasitoid's preference and survival. Zucchini, sweet pepper, and tomato were artificially infested with eggs of Bactrocera dorsalis Hendel, Ceratitis capitata Wiedemann, and Ceratitis cosyra Walker (all Diptera: Tephritidae), then exposed to mated naïve F. arisanus females in a 20:1 egg:parasitoid ratio. Parasitoid behavioral activities (resting, antennating, probing, ovipositing) were observed on the infested fruits. Parasitism rate was determined by dissection of fruit fly eggs under a stereomicroscope. Behavioral activities of F. arisanus differed between all the fruits when infested with B. dorsalis or C. cosyra eggs but differed only between some of the fruits when infested with C. capitata. Fopius arisanus preferred B. dorsalis over C. capitata and C. cosyra, with a parasitism rate 2× higher on B. dorsalis compared to the Ceratitis species. Preference for fruits was dependent on the infesting fruit fly. The emergence of F. arisanus was higher with B. dorsalis than with Ceratitis spp. Although B. dorsalis completed its development earlier than Ceratitis spp., host fly species did not affect the developmental time of F. arisanus. We discuss the significance of F. arisanus preference in relation to naturally occurring Tephritidae infestations. We also discuss whether some fruits might constitute a refuge for Tephritidae flies and whether this will affect the current biological control efforts against B. dorsalis.     

Reproductive biology of Fopius arisanus (Hymenoptera: Braconidae) on Ceratitis capitata and Anastrepha spp. (Diptera: Tephritidae)

The reproduction of the solitary endoparasitoid Fopius arisanus (Sonan) (Hymenoptera: Braconidae) in Anastrepha ludens (Loew), Anastrepha obliqua (Macquart), and Anastrepha serpentina (Wiedemann) was compared with that using Ceratitis capitata (Wiedemann), being the host in which it had been reared previously. Eggs of different ages (<4 h old, 1, 2, and 3 days old for Anastrepha spp., and ⩽4 h, 1 and 2 days old for C. capitata) of each host species were placed in pieces of papaya, exposed to parasitism for 24 h and then reared through to the adult stage. Host species had a marked effect on parasitoid reproduction with consistently higher parasitoid emergence from C. capitata, whereas emergence from A. obliqua was negligible and this host was not studied further. Host age did not significantly affect parasitoid emergence from C. capitata whereas parasitism of A. ludens and A. serpentina was significantly greater in eggs exposed at 3 days old than those exposed at younger ages. Adult parasitoid sex ratio was male biased in all cases. Despite significant differences in host developmental time, host species did not affect parasitoid developmental time. Parasitoid life expectancy at emergence was reduced by >60% for parasitoids that emerged from A. ludens compared to those that emerged from A. serpentina or C. capitata. The reproduction of parasitoid progeny was highest in parasitoids that emerged from and reproduced on C. capitata and lowest for parasitoids reproducing on A. ludens. Parasitoids that emerged from A. ludens were often deformed, but were larger than those that emerged from A. serpentina. Parasitoids that emerged from C. capitata were smaller than those from Anastrepha spp. We conclude that F. arisanus is capable of sustained reproduction in C. capitata and A. serpentina and merits further study as an agent for the control of these fruit flies.     

Pre-release packing and chilling reduce host-searching ability of the parasitoid Diachasmimorpha longicaudata used in the augmentative control of tephritid flies

Diachasmimorpha longicaudata (Ashmead) (Hymenoptera: Braconidae) is a solitary parasitoid used in augmentative releases to control Tephritidae (Diptera) fruit flies of economic importance. Pre-release process includes packing adult parasitoids in cages at high densities and expose them to a temperature of 2 ± 2 °C during 105 min. In this process, females’ antennae may be damaged resulting in a reduction in their host-searching ability and fecundity. Here we measured, for five consecutive days after chilling, the searching ability and fecundity of parasitoids with damaged (D) and undamaged (ND) antennae compared with parasitoids that were not chilled. Female individual responses to fruit infested by Anastrepha spp. was determined in an olfactometer. Latency in the response and latency in making a choice were recorded. Additionally, groups of 30 females were used to measure their ability to find hosts in infested fruit in the laboratory. Fecundity was determined by using artificial oviposition units with Anastrepha ludens (Loew) larvae. In the olfactometer test, ND had lower response than control females during the 1st and 2nd days after chilling. However, no difference in the response was observed between ND and D and the control females on the 5th day. Additionally, chilled females showed a longer latency of response to infested fruit than females of the control treatment when tested in groups. However, after a 24–48 h period, no difference between D and ND and control females was observed. Our results showed similar searching ability and fecundity among parasitoids of the three tested conditions at individual and at group levels. We conclude that pre-release chilling reduces female searching ability only for the first 1–2 days after chilling.     

Effect of host diet and adult parasitoid diet on egg load dynamics and egg size of braconid parasitoids attacking Anastrepha ludens

The quantity and quality of host nutrients can affect fitness‐related traits in hymenopteran parasitoids, including oogenesis. The present study tested the prediction that a high host quality will influence oogenesis‐related traits positively in synovigenic parasitoids, and that a high‐quality adult parasitoid diet can positively affect the same parameters, potentially compensating for development on low‐quality hosts. Four braconid parasitoid species with contrasting life histories are reared on a low‐quality diet [Anastrepha ludens Loew (Diptera: Tephritidae) larvae reared on mango] or a high‐quality (artificial) diet. Adult parasitoids are provided with a high‐quality (honey ad libitum), moderate‐quality (honey every other day) or low‐quality (guava pulp) diet. Generalist species that encounter high variation in host quality naturally are predicted to be more flexible in dealing with nutrient shortfalls than specialist species. By contrast to the predictions, low‐quality hosts yield parasitoids with higher egg loads in two species: Opius hirtus Fisher and Diachasmimorpha longicaudata Ashmead. However, as predicted, a high‐quality adult diet exerts a positive effect on egg load (Utetes anastrephae Viereck), egg size (Doryctobracon crawfordi Viereck) and egg maturation rate (D. longicaudata, O. hirtus and U. anastrephae). The generalist D. longicaudata varies in egg load and maturation rate depending on host quality and adult diet, respectively. Evidence of the combined effect of both factors on parasitoid fertility is presented for the specialist O. hirtus. The theoretical and practical implications of these findings are discussed.     

Competitor‐free space mediates non‐target impact of an introduced biological control agent

Abstract 1. Enemy‐free space has been shown to mediate host shifts in herbivores, but this has not previously been documented in parasitoids. Also, natural enemies shown to maintain host shifts have always been from higher trophic levels, rather than competitors. 2. In Hawaii, an Australian parasitoid (Diachasmimorpha tryoni) of medflies that loses competition contests to a subsequently introduced Asian parasitoid (Fopius arisanus) has shifted its realised host range to attack non‐target gall flies on lantana. 3. The present study demonstrates experimentally that D. tryoni reproduction is: (i) lower on medflies in coffee when F. arisanus is present than when it is absent; (ii) higher in gall flies on lantana than on medflies in coffee, when F. arisanus is present; and (iii) higher in medflies on coffee than in gall flies on lantana, when F. arisanus is absent. This meets Berdegue et al.’s (Ecological Entomology, 21 , 203–217, 1996) three conditions to confirm the importance of enemy‐free space. 4. In the field, F. arisanus is abundant on medflies, whereas D. tryoni is rare on medflies, but is the dominant parasitoid of lantana gall flies. 5. Competitor‐free space is thus shown to be a key mechanism maintaining an apparent host shift by an introduced biocontrol agent onto a non‐target species.     

An Optimized Protocol for Rearing Fopius arisanus, a Parasitoid of Tephritid Fruit Flies

Fopius arisanus (Sonan) is an important parasitoid of Tephritid fruit flies for at least two reasons. First, it is the one of only three opiine parasitoids known to infect the host during the egg stage¹. Second, it has a wide range of potential fruit fly hosts. Perhaps due to its life history, F. arisanus has been a successfully used for biological control of fruit flies in multiple tropical regions^2-4. One impediment to the wide use of F. arisanus for fruit fly control is that it is difficult to establish a stable laboratory colony^5-9. Despite this difficulty, in the 1990s USDA researchers developed a reliable method to maintain laboratory populations of F. arisanus^10-12. There is significant interest in F. arisanus biology^13,14, especially regarding its ability to colonize a wide variety of Tephritid hosts^14-17; interest is especially driven by the alarming spread of Bactrocera fruit fly pests to new continents in the last decade¹⁸. Further research on F. arisanus and additional deployments of this species as a biological control agent will benefit from optimizations and improvements of rearing methods. In this protocol and associated video article we describe an optimized method for rearing F. arisanus based on a previously described approach¹². The method we describe here allows rearing of F. arisanus in a small scale without the use of fruit, using materials available in tropical regions around the world and with relatively low manual labor requirements.     

Superparasitism in mass reared Diachasmimorpha longicaudata (Ashmead) (Hymenoptera: Braconidae), a parasitoid of fruit flies (Diptera: Tephritidae)

Superparasitism frequency and its effects on the quality of mass-reared Diachasmimorpha longicaudata (Ashmead) parasitoids were investigated under laboratory conditions. Percentage of adult emergence, sex ratio, survival, fecundity and flight ability of adult parasitoids that emerged from Anastrepha ludens (Loew) pupae with different levels of superparasitism were determined. A high prevalence of superparasitism was observed. The number of scars per pupa, produced by insertion of the parasitoid ovipositor, ranged from 1 to 30, with an average (±SD) of 8.3 ± 6.2. Adult parasitoid emergence decreased as the level of superparasitism increased. However, the fraction of females rose with increasing superparasitism and the flight ability was lower in adults emerging from pupae with only one scar, compared with adults emerging from superparasitized hosts. Female longevity and fecundity were not affected by superparasitism. Our results support the hypothesis that superparasitism in D. longicaudata might be adaptive, since adults emerging from hosts with moderate levels of superparasitism showed the highest percentage of emergence and there were no significant differences in the other quality control parameters tested. Our findings are relevant to the mass rearing process, where the ratio of hosts to parasitoids can be optimized as well as the distribution of eggs deposited in host larvae. This contributes to efficient mass rearing methods for augmentative biological control programs.     

X-ray doses to safely release the parasitoid Diachasmimorpha longicaudata (Hymenoptera: Braconidae) reared on Anastrepha fraterculus larvae (Diptera: Tephritidae)

Diachasmimorpha longicaudata is a koinobiont larval parasitoid that is currently used to control fruit flies of the genera Anastrepha, Ceratitis and Bactrocera. In the rearing process, a fraction of the host larvae that are exposed to parasitoids escape from parasitism and develop into viable and fertile flies. This creates the need to eliminate emerging flies before the parasitoids are shipped for release, increasing costs due to additional handling steps. Exposure of fly eggs or larvae to gamma-irradiation before they are parasitised has been used to reproductively sterilise hosts, or even inhibit their emergence. Our aim was to determine whether X-ray radiation applied to Anastrepha fraterculus third instar larvae before they are exposed to parasitoids, inhibits fly emergence in non-parasitised larvae without affecting the performance of the parasitoids that emerge from parasitised larvae. Three X-ray doses: 6250.2 R, 8333.6 R and 10417 R (equivalent to 60, 80 and 100 Gy, respectively) and one γ-ray dose (100 Gy) were tested. Fly emergence decreased with increasing doses of radiation, showing null values for the higher X-ray dose and the dose of 100 Gy. Irradiation showed either no impact or a positive effect on parasitism rate and fecundity. Sex rate was biased towards females in almost every dose. We conclude that the two types of radiation evaluated here were equally effective in suppressing fly emergence with no detrimental effects on the biological quality of the produced parasitoids. X-rays offer an alternative method of irradiation than the conventional radiation source, i.e. γ-rays. These results represent a significant improvement in the development of a biological control programme against A. fraterculus.     

Superparasitism strategies by a native and an exotic parasitoid species attacking the Mexican fruit fly,Anastrepha ludens (Diptera: Tephritidae)

Superparasitism refers to the action of parasitoids ovipositing eggs in hosts that are already parasitized; this inevitably results in the elimination of supernumerary larvae in solitary parasitoids. Here, we investigated superparasitism performed by two species of solitary parasitoids on the larvae of Anastrepha ludens (Loew; Diptera: Tephritidae): a native species, Doryctobracon crawfordi (Viereck; Hymenoptera: Braconidae), and an exotic species, Diachasmimorpha tryoni (Cameron; Hymenoptera: Braconidae). Tests were conducted under laboratory conditions evaluating the behaviour of females acting alone (self-superparasitism) or in groups (conspecific superparasitism). Parasitism strategies were different between these two species. In D. crawfordi, the number of first instar larvae found in each dissected host pupa was never greater than two, regardless of the number of oviposition scars observed per pupa. In contrast, there was a positive correlation between the number of oviposition scars and the number of first instar larvae in D. tryoni. The survival and fecundity of D. crawfordi females emerging from pupae with one scar was higher than in females emerging from pupae with more scars. In D. tryoni, the number of oviposition scars did not show deleterious effects on life history traits and was positively correlated with the proportion of emerging females. An understanding of the superparasitism strategy adopted by parasitoid species could be of great interest to augmentative biological control programmes because the mass rearing of natural enemies could be negatively or positively affected by this condition.