Incidence of the introduced parasitoids Cotesia kazak and Microplitis croceipes (Hymenoptera: Braconidae) from Helicoverpa armigera (Lepidoptera: Noctuidae) in tomatoes,sweet corn,and lucerne in New Zealand

Two parasitoids,Cotesia kazak (Telenga) and Microplitis croceipes (Cresson) have been successfully introduced into New Zealand to improve control of Helicoverpa armigera (Hübner), tomato fruitworm. C. kazak has spread throughout the North Island, but M. croceipes is restricted largely to its release areas in crops in the Gisborne and Hawke’s Bay regions in the East Coast of the North Island and in pine plantations in the central North Island. Rates of mortality of H. armigera from parasitism were studied in processing tomato crops where these parasitoids are a key component of an integrated pest management programme, and in sweet corn, lucerne and soybeans. C. kazak was the dominant parasitoid in tomatoes and soybeans. It emerged from small H. armigera larvae and usually killed the host before it caused major damage to fruit. M. croceipes emerged from larger host larvae than C. kazak. Death rates from parasitism of H. armigera larvae in tomatoes increased from less than 1% caused by native parasitoids prior to parasitoid introductions, to 25–45% in 1988 and 70–80% in 1996 following the establishment of both introduced parasitoids. M. croceipes was the most common parasitoid in lucerne and total mortality from all parasitoids was similar to that in tomatoes. Low rates of parasitism by C. kazak in sweet corn were attributed to the reduced penetration of the adult parasitoid into sweet corn fields and to the protection afforded by sweet corn when H. armigera larvae burrowed into corn cobs. The implementation of an IPM programme based partly on the effectiveness of these parasitoids has contributed to a decrease in insecticide applications to processing tomatoes.     

Predation by Podisus maculiventris (Hemiptera: Pentatomidae) on Plutella xylostella (Lepidoptera: Plutellidae) larvae parasitized by Cotesia plutellae (Hymenoptera: Braconidae) and its impact on cabbage

Biological control offers potentially effective suppression of the diamondback moth (DBM), Plutella xylostella, a serious pest of Brassica crops. Little is known of whether multiple natural enemies have additive, antagonistic, or synergistic effects on DBM populations. No-choice and choice tests were conducted to assess predation by Podisus maculiventris on DBM larvae parasitized by Cotesia plutellae and unparasitized larvae. In no-choice tests, P. maculiventris preyed on greater numbers of parasitized than unparasitized larvae and greater numbers of young larvae than old larvae. In choice tests with early third instar DBM, there was no difference in predation between parasitized or unparasitized larvae. However, in choice tests with older prey, P. maculiventris preyed on more parasitized than unparasitized larvae. Two field studies were conducted to test if this predator and parasitoid have additive, antagonistic or synergistic effects on DBM populations and plant damage in cabbage (Brassica oleracea var. capitata). In 2002, DBM populations were significantly lower in the presence of C. plutellae but not in the presence of P. maculiventris. There was not a significant interaction between the natural enemies. Plant damage was reduced only with C. plutellae. In 2003, DBM populations were significantly lower in the presence of C. plutellae and P. maculiventris, although the combination of natural enemies did not lead to a non-additive interaction. Plant damage was unaffected by the presence of either natural enemy. Because of its greater predation on parasitized larvae, P. maculiventris could be an intraguild predator of C. plutellae. Yet, their overall combined effect in the field was additive rather than antagonistic.     

Suitability of some farmscaping plants as nectar sources for the parasitoid wasp, Microplitis croceipes (Hymenoptera: Braconidae): Effects on longevity and body nutrients

In support of an ongoing study to evaluate potential farmscaping plants for utilization in organic vegetable production systems, we examined the effects of the nectar of three flowering plant species, sweet alyssum (Lobularia maritima), buckwheat (Fagopyrum sagittatum), and licorice mint (Agastache foeniculum), on the lifespan and body nutrient levels of the wasp, Microplitis croceipes (Cresson) (Hymenoptera: Braconidae), a key parasitoid of some caterpillar pests of vegetable crops in the USA. The greatest longevity (～16 days) was recorded for honey-fed wasps (positive control). Buckwheat significantly increased the lifespan of female and male wasps by at least two-fold relative to wasps provided water only (longevity = 3–4 days). Licorice mint significantly increased female longevity and numerically increased male longevity. Sweet alyssum slightly increased longevity of both sexes but this was not significantly different from the water only control. Females had a significantly longer longevity than males on all the diet treatments. The greatest carbohydrate nutrient levels (sugar content and glycogen) were recorded in honey-fed wasps followed by wasps fed buckwheat, whereas very little nutrients were detected in wasps provided sweet alyssum, licorice mint or water only. However, female wasps were observed to attempt to feed on all three flowering plant species. Thus, the low nutrient levels detected in wasps provided sweet alyssum or licorice mint may be because the nectars were not accessible or were of poor quality. Further studies will evaluate the effects of the promising farmscaping plants on the beneficial and pest insect communities in the field.     

Efficacy of inoculative releases of Trichogramma ostriniae (Hymenoptera: Trichogrammatidae) against European corn borer Ostrinia nubilalis (Lepidoptera: Crambidae) in field corn

We evaluated the egg parasitoid Trichogramma ostriniae (Hymenoptera: Trichogrammatidae) to control European corn borer [Lepidoptera: Crambidae: Ostrinia nubilalis (Hübner)] in field corn in 2001 and 2002. Inoculative releases of 75,000 T. ostriniae/ha occurred in New York and Virginia in 5–10 cornfields per state when corn was at mid-whorl. Incidence of egg mass parasitism, number of stalk tunnels, incidence of ear damage, and whole-plant yield were evaluated. Parasitism of European corn borer egg masses ranged from 0 to 75% in release plots and was greater in release plots than in control plots. Individual comparisons between paired release and control plots showed no reductions in either stalk or ear damage. However, when data were combined across both years and fields, stalk and ear damage were significantly reduced in New York. In Virginia, no significant differences were detected using data obtained from one year. There were no differences in yield between release and control plots. Low densities of European corn borer, drought conditions in 1 year, and a larger plant canopy in field corn are possible reasons why T. ostriniae releases provided less control than has been observed in previous trials in sweet corn. Additional research focused on improved timing and frequency and number of releases is warranted.     

Nondevelopment ofCotesia kariyai(Hymenoptera: Braconidae) in Entomopoxvirus-Infected Larvae ofPseudaletia separata(Lepidoptera: Noctuidae)

Interaction between an entomopoxvirus (PsEPV) and a gregarious braconid endoparasitoid,Cotesia kariyai,inPseudaletia separatalarvae showed that infection of larvae with PsEPV was deleterious to the development and survival ofC. kariyai.The survival and development ofC. kariyaiin PsEPV-infectedP. separatalarvae depended on the length of time between parasitization and viral infection. No parasitoid larvae emerged from PsEPV-infected hosts when host larvae were exposed simultaneously to parasitization and PsEPV inoculation whereas more than 80% of the hosts produced parasitoids when PsEPV was administered 5 days postparasitization.C. kariyailarvae in PsEPV-infected hosts showed a retarded development, shrank, and died about 8 days after viral exposure. Virion-free plasma from PsEPV-infectedP. separatalarvae was toxic to the parasitoid larvae even up to a dilution level of 32 when it was injected intrahemocoelically into the host larvae. Development of parasitoids in hosts that were simultaneously parasitized and injected with the virion-free plasm never progressed beyond the egg stage. The parasitizedP. separatalarvae injected with the virion-free plasma did not pupate and died within 30 days after injection.     

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.     

Using the literature to evaluate parasitoid host ranges: a case study of Macrocentrus grandii (Hymenoptera: Braconidae) introduced into North America to control Ostrinia nubilalis (Lepidoptera: Crambidae)

We propose a method for using the literature to evaluate host ranges of parasitoids that are candidates for biological control introductions. Data on the parasitoids that attack a given host species can be used as negative evidence concerning the candidate whose host range is being evaluated. By compiling studies for a variety of host species, one can delineate those taxa unlikely to be attacked by the candidate. Using a retrospective case study of a parasitoid introduced into North America, we describe (1) this approach to using the literature to evaluate host range and (2) how well predictions based on such an evaluation match actual host range. Based on the host range of Macrocentrus grandii in Eurasia as reported in the literature, we predicted that the species in the genus Ostrinia are the most likely hosts. Of native North American species, Ostrinia obumbratalis is the only non-target species likely to be attacked by M. grandii. The predicted host range for North America matched the actual host range found in the field. This suggests that a careful literature review could be used as an important source of data on host range of parasitoid species proposed for introduction into a new environment.     

Host Suitability of Four Cereal Stem Borers (Lepidoptera: Crambidae, Noctuidae) for Different Geographic Populations of Cotesia sesamiae (Cameron) (Hymenoptera: Braconidae) in Kenya

This study focused on the suitability of four species of cereal stem borers for the development of five geographic populations of Cotesia sesamiae (Cameron). C. sesamiae, an indigenous larval parasitoid of gramineous stem borers, is widespread in Africa. Four stem borers, Chilo partellus (Swinhoe), Chilo orichalcociliellus Strand (Lepidoptera: Crambidae), Busseola fusca Fuller, and Sesamia calamistis Hampson (Lepidoptera: Noctuidae), were offered to C. sesamiae for oviposition. Parasitoid individuals originated from five locations in Kenya. Biological parameters such as developmental time, percentage parasitism, progeny production, mortality of immature parasitoids, and proportion of female progeny were compared across host species. The two populations from western Kenya developed well on B. fusca. However, populations from the coast and the Eastern Province could not successfully parasitize B. fusca. With the exception of B. fusca, the percentage of hosts successfully parasitized by the different C. sesamiae populations was not different. The size of the host appeared to be an important factor influencing the development and reproductive potential of the parasitoid. We conclude that the different parasitoid populations were adapted to location-specific characteristics. Parasitoid–host compatibility must be evaluated before release for better establishment and colonization.     

Dynamic expansion in recently introduced populations of fire ant parasitoids (Diptera: Phoridae)

Combating invasive species requires a detailed, mechanistic understanding of the manner and speed with which organisms expand their ranges. Biological control efforts provide an opportunity to study the process of species invasions and range expansions under known initial conditions. This study examines the rate, pattern and mechanisms of spread for two populations of the biological control agent Pseudacteon tricuspis, phorid-fly parasitoids of imported fire ants. We employ a trap-based survey method that detects phorid flies in low-density populations, and provides data on abundance. This technique allows us to differentiate between continuous population spread and effective long-distance dispersal and to examine density gradients of phorid flies across the expanding population front. We find that occupied sites in front of the leading edge of continuous populations were common; forming small populations we refer to as satellite populations. Satellite populations are tens of kilometers from the nearest possible source. Wind governs the dynamics of spread in these two central Texas populations. Population edges expanding with the wind exhibited a higher frequency of effective long-distance dispersal than did populations expanding into the wind. This enhanced effective long-distance dispersal rate translated into a five times faster rate of spread for population edges traveling with the wind. This planned invasion shares many characteristics in common with unplanned species invasions including: protracted establishment phase during which densities were below detection thresholds, and slow initial spread immediately after establishment followed by rapid, accelerating spread rates as population sizes grew.     

Olfactory responses of Cotesia flavipes (Hymenoptera: Braconidae) to target and non-target Lepidoptera and their host plants

The attraction of Cotesia flavipes Cameron to volatiles from a range of non-target lepidopteran larvae and their host plants (grasses and trees) or food substrate (honeycomb) was evaluated using a Y-tube olfactometer. The non-target host larvae used in the study included Galleria mellonella (L.), Charaxes cithaeron Felder, Bombyx mori L., and Eldana saccharina Walker. The target insects, Chilo partellus (Swinhoe) and Chilo orichalcociliellus (Strand), were used as controls. Host plants included Afzelia quanzensis Welw., Morus alba L., Cyperus papyrus L., Pennisetum purpureum Schumach, and Zea mays L. The response of C. flavipes to volatiles from the non-target larvae and their food was variable. Attraction to uninfested maize was not significantly different from uninfested plants of non-target hosts or honeycomb. Only maize and honeycomb were preferred over clean air. C. partellus infested maize plants were significantly more attractive than M. alba, A. quanzensis, and honeycomb infested with their herbivores. Infested maize and C. papyrus were more attractive than uninfested ones. When odors from naked larvae were tested, C. flavipes preferred odors from C. partellus larvae over those of E. saccharina and C. cithaeron and larvae of C. partellus and G. mellonella were preferred to clean air. The implications of these findings for biological control and its effect on non-target organisms are discussed.     

Susceptibility of Helicoverpa zea and Heliothis virescens (Lepidoptera: Noctuidae) to Vip3A insecticidal protein expressed in VipCot™ cotton

Susceptibility of laboratory and field colonies of Helicoverpa zea (Boddie) and Heliothis virescens F. to Vip3A insecticidal protein was studied in diet incorporation and diet overlay assays from 2004 to 2008. Responses of field populations were compared to paired responses of University of Arkansas laboratory susceptible H. zea (LabZA) and H. virescens (LabVR) colonies. After 7 d of exposure, observations were made on number of dead larvae (M) and the number of larvae alive but remaining as first instars (L1). Regression estimates using M (LC₅₀) and M plus L1 (MIC₅₀) data were developed for laboratory and field populations. Susceptibility of laboratory and field populations exposed to Vip3A varied among different batches of protein used over the study period. Within the same batch of Vip3A protein, susceptibilities of laboratory colonies of both species (LabZA and LabVR) were similar. Field colonies were significantly more susceptible to Vip3A than the respective reference colonies of both species. Within field populations, susceptibility to Vip3A varied up to 75-fold in H. zea and 132-fold in H. virescens in LC₅₀ estimates. Variabilities in MIC₅₀s were up to 59- and 11-fold for H. zea and H. virescens, respectively.     

Interactions of two idiobiont parasitoids (Hymenoptera: Ichneumonidae) of codling moth (Lepidoptera: Tortricidae) with the entomopathogenic nematode Steinernema carpocapsae (Rhabditida: Steinernematidae)

Simultaneous use of parasitoids and entomopathogenic nematodes for codling moth (CM) control could produce an antagonistic interaction between the two groups resulting in death of the parasitoid larvae. Two ectoparasitic ichneumonid species, Mastrus ridibundus and Liotryphon caudatus, imported for classical biological control of cocooned CM larvae were studied regarding their interactions with Steinernema carpocapsae. Exposure of M. ridibundus and L. caudatus developing larvae to infective juveniles (IJs) of S. carpocapsae (10 IJs/cm2; approximately LC(80-90) for CM larvae) within CM cocoons resulted in 70.7 and 85.2% mortality, respectively. However, diapausing full grown parasitoid larvae were almost completely protected from nematode penetration within their own tightly woven cocoons. M. ridibundus and L. caudatus females were able to detect and avoid ovipositing on nematode-infected cocooned CM moth larvae as early as 12h after treatment of the host with IJs. When given the choice between cardboard substrates containing untreated cocooned CM larvae and those treated with an approximate LC95 of S. carpocapsae IJs (25 IJs/cm2) 12, 24, or 48h earlier, ovipositing parasitoids demonstrated a significant preference for untreated larvae. The ability of these parasitoids to avoid nematode-treated larvae and to seek out and kill cocooned CM larvae that survive nematode treatments enhances the complementarity of entomopathogenic nematodes and M. ridibundus and L. caudatus.     

Suitability ofBusseola fuscaandSesamia calamistis(Lepidoptera: Noctuidae) for the Development of Two Populations ofCotesia sesamiae(Hymenoptera: Braconidae) in Kenya

The suitability ofSesamia calamistisHampson andBusseola fusca(Fuller) for the development of two geographical populations ofCotesia sesamiae(Cameron) was examined in the laboratory. One population of the parasitoid was collected from the coast of Kenya and the other from the inland. Both populations of the parasitoid could develop onS. calamistis.OnB. fusca,the inland population ofC. sesamiaewas able to develop, while the population from the coastal area of Kenya was encapsulated. Mating studies revealed that the two parasitoid populations were partially reproductively isolated. Unidirectional incompatibility, possibly caused by theWolbachiainfection, was observed when males from the infected coastal population were mated with females from the uninfected inland population.     

Influences of plant species on life history traits of Cotesia rubecula (Hymenoptera: Braconidae) and its host Pieris rapae (Lepidotera: Pieridae)

The relative suitability of four plants was studied for larvae of Pieris rapae L. and its parasitoid Cotesia rubecula (Marshall). For unparasitized P. rapae, pupal dry weight and egg-pupa growth rate were higher on cabbage, radish and nasturtium than on Indian hedge mustard. Larval developmental rate and size were greatest for C. rubecula when its host was feeding on nasturtium. Wasp survival was not affected by the host insect/plant combination in which the parasitoid developed. These results indicate that the plant on which host larvae feed is an important factor in development of the parasitoid.     

Potential of Haplothrips brevitubus (Karny) (Thysanoptera: Phlaeothripidae) as a predator of mulberry thrips Pseudodendrothrips mori (Niwa) (Thysanoptera: Thripidae)

The predation potential of Haplothrips brevitubus (Karny) for thrips was evaluated in the laboratory. When second stage larvae of Pseudodendrothrips mori (Niwa) were presented to an adult H. brevitubus at densities of 10, 20, 30, and 40 larvae per cage at 25 °C over 24 h, the number of larvae consumed per day increased with an increasing density up to 30. Predation of H. brevitubus exhibited the type II functional response. The mean development time of the egg, larva, and pupa of H. brevitubus were 4.5, 9.6, and 4.8 days, respectively, at 25 °C. The survival rate from egg to adult emergence was 94.7%. One H. brevitubus larva consumed 41.6 P. mori larvae on average during the total larval period. Adult longevity was 35.2 days in females and 34.6 days in males. The pre-oviposition period was 2.7 days and the oviposition period was 31.5 days. The lifetime fecundity was 120.1 eggs and the mean daily oviposition rate was 3.6 eggs. Calculated mean generation time (T) was 29.5 days, intrinsic rate of natural increase (r_m) was 0.162, and net reproductive rate (R₀) was 56.5. The r_m value of H. brevitubus was higher than that of Thrips palmi Karny and almost equal to that of Frankliniella occidentalis (Pergande). These results indicate that H. brevitubus has good potential as a predator of P. mori and is likely to be useful for controlling thrips.     

Effect of habitat complexity on biological control by the red imported fire ant (Hymenoptera: Formicidae) in collards

A potentially important and understudied biological control agent in US agroecosystems is the red imported fire ant, Solenopsis invicta Buren. Red imported fire ants may be particularly important biological control agents because we can manipulate their abundance with changes in habitat complexity. The effect of habitat complexity on biological control by fire ants was determined using plots of collards intercropped with white clover (complex habitat) and simple collard monocrops. The most economically significant pests of collards are larvae of the diamondback moth (DBM), Plutella xylostella (L.). Predation of DBM larvae by fire ants was more rapid and efficient in the intercrop than the monocrop. Red imported fire ants were 23% less abundant in the intercrop than the monocrop, however, suggesting that fire ants had a greater per capita effect on DBM survival in the complex habitat. Red imported fire ant predation of DBM larvae was significantly affected by larval density. Red imported fire ants also reduced the survival of leaf beetles, another economically significant pest taxa, by 45%. Furthermore, collard leaf damage tended to be inversely related to fire ant density and fire ants were more effective at reducing crop damage in the complex intercrop. Our study indicates the ability of red imported fire ants to be effective biological control agents and suggests that increasing habitat complexity can enhance red imported fire ant efficacy and herbivore control.     

Aphelinus albipodus(Hymenoptera: Aphelinidae) andDiaeretiella rapae(Hymenoptera: Braconidae) Parasitism onDiuraphis noxia(Homoptera: Aphididae) Infesting Barley Plants Differing in Plant Resistance to Aphids

Russian wheat aphid,Diuraphis noxia(Mordvilko), as a pest of small grains, has prompted research into biological control and host plant resistance. In the presence of Russian wheat aphid, leaves of a susceptible barley (Morex) are curled and chlorotic and sustain large densities of this aphid, while leaves of a resistant barley (STARS-9301B) remain flat and green and sustain fewer aphids. Might parasitism of Russian wheat aphid byAphelinus albipodusHayat & Fatima andDiaeretiella rapaeMcIntosh be affected differently by these plant types? When presented the plants separately and based on parasitism rate relative to aphid density, the largerD. rapaewas more effective in parasitizing relatively high densities of aphids within curled leaves of Morex than relatively low densities of aphids on uncurled leaves of STARS-9301B. Parasitism byA. albipodusdid not significantly differ among the plants. When given a choice of plants, approximately equal rates of parasitism occurred on the two plant lines for both parasitoid species, and parasitism byD. rapaewas greater thanA. albipodus.These data indicate that using parasitoid size as an indicator of success in a physically restricted environment may be misleading, when considered in a plant environment responsive in several manners to aphids (chlorosis, curling, and ability to sustain Russian wheat aphid). We expect that use of resistant barley will result in decreased parasitoid abundance as aphid densities decrease. However, parasitism rates are expected to be approximately equal on resistant and susceptible barley. In this system, plant resistance and biocontrol are compatible management strategies.     

Intraguild interactions between generalist predators and an introduced parasitoid of Glycaspis brimblecombei (Homoptera: Psylloidea)

Studies were conducted to evaluate potential impacts of generalist predators on the biological control of Glycaspis brimblecombei Moore (Homoptera: Psylloidea), a pest of eucalyptus trees in California, and its introduced parasitoid Psyllaephagus bliteus (Hymenoptera: Encyrtidae). Based on the results of the monitoring populations of G. brimblecombei and their natural enemies in inland and coastal California in the field, P. bliteus or Anthocoris nemoralis (Fabricius) (Heteroptera: Anthocoridae), alone or both species together were released into cages with G. brimblecombei to simulate predatory interference on the introduced parasitoid in the laboratory. Although coastal sites had higher densities of natural enemies as were percent parasitism and predation, the mean number of G. brimblecombei did not vary between inland and coastal sites. P. bliteus or A. nemoralis significantly reduced the psyllid densities in cages. However, when both species were together, the presence of A. nemoralis increased the parasitoid mortality relative to the mortality observed in the parasitoid-alone treatment. Moreover, the increase in parasitoid mortality was followed by the decrease in mortality of the psyllids. The current study also indicated that predation risk of parasitized hosts varies depending on the developmental stages of the psyllids.