The biology of Psyllaephagus bliteus Riek (Hymenoptera: Encyrtidae), a parasitoid of the red gum lerp psyllid (Hemiptera: Psylloidea)

The red gum lerp psyllid, Glycaspis brimblecombei Moore (Hemiptera: Psylloidea), is native to Australia, where it feeds upon Eucalyptus species. It first appeared near Los Angeles, California, in 1998, and soon spread throughout the state. A biological control program directed against the psyllid was initiated and Psyllaephagus bliteus Riek (Hymenoptera: Encyrtidae) was imported from Australia and released in California. During quarantine screening, the taxonomic status of Psyllaephagus quadricyclus Riek was assessed by one of us (RLZ) and is proposed here as a new junior synonym for P. bliteus. The experiments discussed herein provide basic biological information on P. bliteus to supplement and improve the control program. We found that P. bliteus can oviposit into psyllid nymphs of any age but prefers third and fourth instars. Observations of host-handling behavior suggest that the large lerps of fifth instar psyllids increase host-handling time, thereby impeding oviposition and providing some protection from parasitism. Female P. bliteus were observed host-feeding on all psyllid nymphal development stages. Adults are relatively long-lived and, at constant temperatures of 17, 21, 23, 26, and 32 °C, longevity is a negative linear function of temperature. Females lived significantly longer than males. Adult females can live for several months, provided with hosts and held under glasshouse conditions (22 ± 3 °C), however, maximum egg deposition occurred within 22 days after adult emergence. Studies of larval development show that P. bliteus is a koinobiont and larval development is not initiated until the host reaches the late fourth or early fifth instar.     

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.     

Intraguild interactions between the predator Macrolophus pygmaeus and the parasitoid Eretmocerus mundus,natural enemies of Bemisia tabaci

The native parasitoid Eretmocerus mundus Mercet and the predator Macrolophus pygmaeus Rambur are widely used to control Bemisia tabaci (Gennadius) in Mediterranean tomato greenhouses. An optimal biological control strategy for B. tabaci should take into account intraguild interactions between these natural enemies. In this study, predator's prey preferences and prey consumption were studied when offered different parasitoid and whitefly stages. The effect of the host plant on the adults of both natural enemies was also examined. M. pygmaeus preferred to consume B. tabaci over E. mundus when immature stages and adults of B. tabaci and E. mundus were offered. They consumed a larger amount of healthy B. tabaci nymphs and adults than of parasitised nymphs or E. mundus adults. The predator M. pygmaeus interfered with the reproduction of E. mundus females on cotton but not on tomato. However, B. tabaci nymphal mortality on tomato associated with parasitoid host feeding was also lower when the adult parasitoids coexisted with the predators. The joint release of M. pygmaeus and E. mundus adults did not increase the control of the whitefly B. tabaci.     

Release and establishment of a biological control agent, Psyllaephagus pilosus for eucalyptus psyllid (Ctenarytaina eucalypti) in Ireland

An Australian parasitoid wasp, Psyllaephagus pilosus, was collected from a previous release site in France and introduced into a commercial eucalyptus foliage plantation in Co. Kerry in the south west of Ireland to control the eucalyptus (blue gum) psyllid Ctenarytaina eucalypti. The first parasitised psyllid nymphs were observed 26 days after the release was made in late May 1998, and 49 days elapsed before a new generation of adult parasitoids was seen. Visually assessed indices of psyllid parasitism and adult wasp incidence were used to quantify the pattern of adult dispersion and establishment. A second generation of adult wasps emerged in late August, initiating a rapid spread of parasitism throughout the release site during September that culminated in a peak rate of almost 100% parasitism by late October. Subsequently by the end of 1998, an apparently random process of dispersion and successful natural colonisation occurred at eight out of ten monitored plantations at distances up to 70 km from the release point. The first colonisers of the other two sites arrived very late in 1998, and consequently failed to establish viable populations by the following summer. Probably this failure was because the small numbers of colonisers had arrived too late in the growing season to effect population establishment before the onset of winter. Assisted introductions were, therefore, made at these sites in June and August 1999, respectively. Once fully established, the parasitoid had no difficulty in surviving winter conditions at all monitored sites and demonstrated excellent potential as a biological control agent.     

Diapause strategy in the parasitoid Psyllaephagus pistaciae

The processes involved in the induction and termination of diapause in the parasitoid Psyllaephagus pistaciae Ferrière (Hymenoptera: Encyrtidae) were investigated under controlled laboratory conditions. Results indicated that the parasitoid P. pistaciae is able to overwinter successfully as a pupa within the mummified psyllid host Agonoscena pistaciae Burckhardt and Lauterer (Homoptera: Psylloidea), and the parasitoid clearly responded to a short photoperiod by entering diapause. The incidence of diapause increased significantly with decreasing temperature, indicating the existence of an interaction between low temperature and short‐day photoperiod that resulted in a 100% diapause. However, low temperature alone partly stimulated P. pistaciae to enter diapause. The incidence of diapause was likely to be independent from psyllid nymphal instar and the condition of its mother. This investigation showed that the termination of diapause in the overwintering parasitoid pupae and the duration of diapause completion or adult emergence is photoperiod independent, but dependent on temperature. However, chilling treatment was found to be unnecessary for diapause termination in P. pistaciae, although it decreased the duration of diapause maturation. The positive responses of parasitoids to environmental factors appears to act as a basic strategy to induce diapause in the parasitoid P. pistaciae against extreme climatic conditions.     

Intraguild predation among the predatory mites Amblyseius eharai,Amblyseius cucumeris and Amblyseius barkeri

Predator species with the same prey interact not only by competition for food and space but also by intraguild predation (IGP). The impact of IGP on introduced phytoseiid mites and native species in the context of biological control is a matter of considerable debate. Amblyseius eharai is the dominant native citrus species in central China, while Amblyseius cucumeris and Amblyseius barkeri are candidates for importation. All three species can feed on the spider mite Panonychus citri, which is the main pest in citrus. This study investigated, in the laboratory, possible IGP among these species in the absence and presence of P. citri, respectively. IGP in different densities of shared prey and intraguild (IG) prey was also studied. All three species consumed heterospecific larvae and eggs but not adults, and the IGP rate of larvae was significantly higher than that of eggs in the absence of shared prey. Additionally, the IGP rate of each group was reduced dramatically in the presence of both shared and IG prey when compared to the absence of shared prey. This occurs most likely because the three species prefer to feed on their natural prey P. citri, rather than on IG prey. Our results showed that A. eharai seems to be a more voracious IG predator than A. cucumeris. A. eharai was much more prone to IGP than A. barkeri.     

Intraguild predation and interference by the mealybug predator Cryptolaemus montrouzieri on the parasitoid Leptomastix dactylopii

The compatibility of the encyrtid parasitoid Leptomastix dactylopii with the coccinellid beetle Cryptolaemus montrouzieri against the citrus mealybug, Planococcus citri, is determined by the extent of intraguild predation and interference by the predator. We tested the preference of the adults and fourth-instar larvae of C. montrouzieri for healthy mealybugs and parasitized mealybugs harboring 1-, 4-, 7- and 14-day-old parasitoid larvae. The experiments were conducted in no-choice (only unparasitized mealybugs or parasitized mealybugs of one parasitoid age were offered at one time) and choice (unparasitized and parasitized mealybugs of a specific age were offered simultaneously) tests. Both the adults and larvae of C. montrouzieri fed on unparasitized and parasitized mealybugs but strongly discriminated against the hardened mummies (14 days old). We also investigated the influence of the presence of C. montrouzieri to the foraging effectiveness of L. dactylopii. The level of parasitism by L. dactylopii was reduced from about 13 to 6% when the number of the C. montrouzieri was increased from zero to four. We recommended that the releases of C. montrouzieri should be conducted 14 days after the releases of L. dactylopii to reduce intraguild predation on the parasitized mealybugs and to avoid interference with the foraging parasitoids.     

昆虫群落中的集团内捕食作用

与捕食、竞争等种间关系相比 ,集团内捕食作用是一种更为复杂的种间关系 ,广泛存在于各种生态系中。该文从它的概念、类型、作用特点、与其它种间关系的区别、存在的广泛性、发生强度的影响因素、化学信息调控及其对生物防治效果的影响等几个方面介绍了天敌群落中的这一典型的种间相互关系。根据参与者在集团内捕食作用关系中的利益地位的不同 ,可将集团内捕食作用分为单向性和双向性的 ,也可分成对称性的和不对称性的。参与者的生物学特性和各种环境条件对集团内捕食作用的发生程度和结果起着重要的调控作用。在多种天敌存在的系统中 ,集团内捕食作用影响着目标生物种群动态及其生物防治的效果。深入地研究这一种间关系对增强生物控害的功能有十分重要的意义     

Interactions between the red imported fire ant, the citrus leafminer, and its parasitoid Ageniaspis citricola (Hymenoptera: Encyrtidae): Laboratory and field evaluations

Interactions between the red imported fire ant [Solenopsis invicta (Hymenoptera: Formicidae)], the citrus leafminer [Phyllocnistis citrella (Lepidoptera: Gracillariidae)], and the citrus leafminer endoparasitoid Ageniaspis citricola (Hymenoptera: Encyrtidae) were investigated under laboratory and field conditions in Florida. Previous studies had shown that S. invicta would selectively prey on brown citrus aphids (Toxoptera citricida) parasitized by Lipolexis oregmae and Asian citrus psyllids (Diaphorina citri) parasitized by Tamarixia radiata, which led us to question whether S. invicta would selectively prey on citrus leafminer (CLM) larvae or eggs parasitized by A. citricola. In the laboratory trial, there was no significant difference between the type of CLM larvae preyed on. However, higher predation was observed on parasitized CLM larvae reared on potted plants in a citrus grove. A subsequent citrus grove test revealed slightly, although not significantly, lower levels of parasitism by A. citricola in trees to which ants had access because predation by ants was higher. However, predation by other predators in the trees to which ants had no access resulted in no significant differences in CLM densities in the two treatments. The field data provide, for the first time, the seasonal phenology of the CLM and its parasitoid A. citricola in the Indian River region of Florida in an unsprayed grapefruit block.     

Web-Construction Behavior of Linyphiid Spiders (Araneae,Linyphiidae): Competition and Co-Existence Within a Generalist Predator Guild

The web-construction behavior of three species of linyphiid spider (Erigone autumnalis, Meioneta unimaculata and Bathyphantes pallida) was studied in the laboratory to examine competition and co-existence within predator guilds. Competitive interactions between spiders potentially reduce their role in biological control. We tested the hypothesis that at high densities, intraguild competition for web-sites would occur but spatial separation of microhabitat would reduce interguild competition, thus allowing co-existence. High mortality and reduced web-size were observed at high B. pallida densities but Linyphiinae co-existed with Erigoninae which constructed webs at different strata. Competitive exclusion by larger individuals occurred between species whose microhabitat niche overlapped. The biocontrol potential of spider or arthropod predator guilds could ultimately be enhanced by maximizing the diversity of species whose niche axes vary.     

Compatibility of an entomopathogenic fungus with a predator and a parasitoid in the biological control of greenhouse whitefly

An ongoing debate in biological control consists of whether interference between biological agents can disrupt pest control. This study investigated the outcome of interactions between the entomopathogen Beauveria bassiana with the whitefly predator Dicyphus hesperus and the parasitoid Encarsia formosa, as well as their effect on the control of the greenhouse whitefly Trialeurodes vaporariorum on greenhouse tomato crops. Our objective was to determine whether the generalist B. bassiana would disrupt biological control by interfering with D. hesperus or E. formosa. In experimental greenhouses, whitefly, parasitoid and predator populations were established, and over 27 days, tomato plants were sprayed with three applications of the B. bassiana based product BotaniGard® (5.13×10³ conidia/mm²) or water (control). Populations of greenhouse whitefly and biological control organisms were regularly monitored in control and B. bassiana-treated compartments. Overall, 10.6% of all whiteflies in treated compartments were infected, and 0.98% were both infected and parasitized. There were 31.7 and 22.3% fewer immature and adult whiteflies, respectively, on B. bassiana-treated plants relative to controls. Parasitism by E. formosa and predation by D. hesperus occurred at rates of 7.5 and 2.5%, respectively, in B. bassiana-treated compartments, and 5 and 6%, respectively in control compartments. Our study suggests that applications of B. bassiana for short-term biological control of greenhouse whiteflies are compatible with the concurrent use of E. formosa and D. hesperus on greenhouse tomato crops.     

Intraguild predation of Planococcus ficus parasitoids Anagyrus pseudococci and Leptomastix dactylopii by Nephus kreissli

Intraguild predation of the mealybug parasitoids Anagyrus pseudococci (Girault), and Leptomastix dactylopii Howard (Hymenoptera: Encrytidae) by Nephus kreissli Fürsch & Uygun (Coleoptera: Coccinellidae) was studied. The latter is a native predator of the important pest Planococcus ficus (Signoret) (Hemiptera: Pseudococcidae) on grapevines in Turkey. For this purpose, P. ficus of different ages parasitised by A. pseudococci or L. dactylopii, or by both A. pseudococci and L. dactylopii, were served to fourth instars and adults of N. kreissli as food. Experiments were conducted using two different treatments: no-choice (served unparasitised or only one stage of parasitised mealybug) and choice (served unparasitised and only one age of parasitised mealybug together), under controlled environmental conditions. Both fourth instars and adult predators were fed on two- and four-day-old mealybugs parasitised by A. pseudococci or on two-, four- and six-day-old mealybugs parasitised by L. dactylopii or by either A. pseudococci or L. dactylopii. The predators could not consume six-day-old mealybugs parasitised by A. pseudococci, eight-day-old mealybugs parasitised by L. dactylopii, or those parasitised by either of these parasitoids which had become mummified. While it was found that the adult predators preferred parasitised mealybugs to unparasitised, the larvae did not show a pronounced preference between parasitised and unparasitised mealybugs (except for mealybugs parasitised by A. pseudococci).     

Intraguild interactions and aphid predators: biological efficiency of Harmonia axyridis and Episyrphus balteatus

Introductions of the harlequin ladybird Harmonia axyridis into Belgium for aphid biological control have been followed by declines in native aphid natural enemies. We first examined, in laboratory and field conditions, the impact of larval mobility of either H. axyridis or Episyrphus balteatus, the most abundant native hoverfly in central Europe, on aphid suppression. The hoverfly larvae consumed more aphids (Megoura viciae) in a short term, whereas the ladybird ones were more efficient in a long term. We second investigated the intraguild interactions between H. axyridis and E. balteatus larvae and adults. In larva pairings between the two species in laboratory microcosms containing aphid (M. viciae) infested broad bean (Vicia faba) plants, H. axyridis had an intraguild predation (IGP) advantage over the hoverfly. When conspecific larvae were paired together on aphid‐infested plants, no cannibalism between them was detected. The presence of either H. axyridis or E. balteatus larvae on aphid‐infested plants negatively influenced the ovipositional behaviour of H. axyridis and E. balteatus females; lower numbers of laid eggs were recorded compared to control treatment. Moreover, eggs laid by E. balteatus females were also dropped as victims of predation mainly by H. axyridis larvae. Our results suggest that while the exotic ladybird was more efficient in aphid biological control, larvae and eggs of the native hoverfly species face increased IGP by H. axyridis, which would contribute, as a consequence, to the decline in E. balteatus population following invasion.     

Suitability of the tomato borer Tuta absoluta as prey for Macrolophus pygmaeus and Nesidiocoris tenuis

The tomato borer, Tuta absoluta (Meyrick) (Lep.: Gelechiidae), is an important tomato pest native to South America, which appeared in eastern Spain at the end of 2006. Prey suitability of T. absoluta eggs and larval instars was examined under laboratory conditions to evaluate whether two indigenous predators, Macrolophus pygmaeus (Rambur) and Nesidiocoris tenuis Reuter (Hem.: Miridae), can adapt to this invasive pest. Both predators preyed actively on T. absoluta eggs and all larval stages, although they preferred first‐instar larvae. Our results demonstrate that both mirids can adapt to this invasive pest, contributing to their value as biological control agents in tomato crops.     

When good bugs go bad: intraguild predation by Jalysus wickhami on the parasitoid, Cotesia congregata

We report a case of direct intraguild predation involving an insect predator and parasitoid in an agricultural system. The spined stilt bug, Jalysus wickhami Van Duzee, feeds on eggs of the tobacco hornworm, Manduca sexta L., and also on prepupal and pupal stages of the gregarious hornworm parasitoid, Cotesia congregata (Say). In two separate trials, mean mortality of attached parasitoids was significantly lower (66%, 73%) than that of their detached siblings (97%, 96%) after a 3 day exposure to stilt bugs, demonstrating that attachment to the host offered some protection against predation. In no-choice experiments, prepupal parasitoids suffered greater mortality (0 day-old=61%, 1 day-old=65%) than pupal parasitoids (2 day-old=50%, 3 day-old=14%). When offered in combination with 0 or 2 day-old hornworm eggs, respective mortality of 0, 1, 2 and 3-day-old pupal parasitoids showed a similar pattern (67%, 63%, 33% and 23%). In another experiment, mortality of 0-day-old pupal parasitoids (64%) was greater than that of 3 day-old pupal parasitoids (38%). Mortality of pupal parasitoids was not affected by the availability of hornworm eggs, a highly acceptable food. Younger pupal parasitoids (=prepupae) probably suffered greater mortality because they were more easily fed on by stily bugs than older (pupated) ones. Because C. congregata overwinters in the prepupal stage, it may be particularly vulnerable to attack late in the season when stilt bug populations are large and hornworm eggs are relatively uncommon.     

Ants as predators of the egg parasitoid Trichogramma cacoeciae (Hymenoptera: Trichogrammatidae) applied for biological control of the olive moth,Prays oleae (Lepidoptera: Plutellidae) in Portugal

The detrimental effect of predators on Trichogramma cacoeciae March. releases to control the olive moth, Prays oleae Bern., in the Trás-os-Montes region (Northeast of Portugal), was evaluated during three releases against the flower generation of the pest in 2002. At 1 and 3 h and at 1, 3, 7 and 14 days after each release, 30 Trichogramma releasing cards were examined in the field and predators were collected and identified. Furthermore, at 1, 3, 7 and 14 days after each release, the percentage of egg predation on the cards was also determined. Formicidae were the most abundant group of predators at 99.1% of the total individuals collected. Ten species were identified, Camponotus aethiops, C. lateralis, C. piceus, C. truncatus, Crematogaster auberti, C. scutellaris, Lasius niger, Leptotorax angustulus, Plagiolephis pygmaea and Tapinoma nigerrimum. T. nigerrimum was the most abundant species, both in total numbers as well as in the number of occupied cards. One day after release, the percentage of predation was 24.0% in the first release, 59.4% in the second and 38.0% in the third. Three days after release, the percentage of predation varied from 60.2 to 83.4% during the three release events. Seven days after release, the percentage of predation increased to 97.8% of the total eggs on cards.     

Increased parasitization of California red scale in the field after exposing its parasitoid, Aphytis melinus, to a synthetic kairomone

The introduced parasitoid, Aphytis melinus DeBach (Hymenoptera: Aphelinidae), utilizes a kairomone, O-caffeoyltyrosine, to recognize California red scale, Aonidiella aurantii (Maskell) (Homoptera: Diaspididae). Wasps used in augmentative release programs for California red scale on California citrus are reared on oleander scale, Aspidiotus nerii Bouché (Homoptera: Diaspididae), themselves reared on squash. Previous laboratory studies demonstrated that wasps reared on oleander scale but exposed to O-caffeoyltyrosine before bioassay more readily accepted California red scale covers for probing than wasps reared similarly but not exposed to O-caffeoyltyrosine. The goal of this study was to determine if wasps reared on oleander scale but exposed to O-caffeoyltyrosine actually parasitized a greater number of field-reared California red scale than unconditioned wasps. In order to distinguish between progeny of conditioned and unconditioned wasps in the field, we utilized two A.melinus strains that carried different electrophoretically distinguishable alleles. In half of the releases, Strain A was conditioned to O-caffeoyltyrosine and Strain B served as the control, while this pattern of conditioning was reversed for the remaining releases. Although there were differences in the rates of population growth of the two strains, whichever strain was the conditioned strain left a greater than expected number of progeny compared to the control strain in all comparisons. Exposure of A. melinus reared in commercial insectaries to O-caffeoyltyrosine prior to release may be a means to improve the effectiveness of such wasps in augmentative release programs to control California red scale.     

Intraguild predation by the generalist predator Dicyphus hesperus on the parasitoid Encarsia formosa

Predation was measured in the laboratory by Dicyphus hesperus females on patches of greenhouse whitefly (Trialeurodes vaporariorum) pupae. The patches contained different proportions of unparasitized pupae and those parastisized as nymphs by Encarsia formosa. Dicyphus hesperus fed readily on parasitized pupae and the number of parasitized pupae consumed increased with the proportion available indicating a capacity for intraguild predation. However, D. hesperus females did not display a preference for feeding on parasitized pupae versus unparasitized pupae. Dicyphus hesperus adults were released at three densities into greenhouse enclosures containing tomato plants harbouring greenhouse whitefly and immature E. formosa. Numbers of killed and parasitized whitefly nymphs and pupae and the total number of healthy whitefly were compared among Dicyphus density treatments. On upper leaves, the amount of predation on whitefly nymphs was higher at the highest predator density than at the lower density or in enclosures where D. hesperus was not released. On lower leaves, the number of parasitized pupae was lowest with the highest predator density indicating a negative effect of intraguild predation by D. hesperus on E. formosa. Despite this, Dicyphus density did not affect the density of whitefly in the presence of E. formosa. The results are discussed as they relate to concurrent use of D. hesperus and E. formosa for regulation of greenhouse whitefly populations.