Establishment of Citrostichus phyllocnistoides (Hymenoptera: Eulophidae) as a biological control agent for the citrus leafminer Phyllocnistis citrella (Lepidoptera: Gracillariidae) in Spain

A program of introduction of exotic parasitoids for the biological control of the citrus leafminer Phyllocnistis citrella Stainton (Lepidoptera: Gracillariidae) was carried out in València (Spain) between 1996 and 1999. Eleven species of parasitoids were imported through a total of 37 shipments coming from nine countries. Six species were released in the field, the encyrtid Ageniaspis citricola (Logvinosvskaya), and the eulophids Quadrastichus sp., Semielacher petiolatus (Girault), Galeopsomyia fausta LaSalle, Cirrospilus ingenuus (Gahan), and Citrostichus phyllocnistoides (Narayanan). A. citricola was recovered in summer in many release points, reaching nearly 50% of parasitism and dispersing more than 300 m, but it was not able to overwinter. Quadrastichus sp. and S. petiolatus established temporarily in some sites, but produced little differences in parasitism or density of host population. In 1999, a substantial expansion of C. phyllocnistoides of more than 30 km in all directions was observed from one release point. In 2000 and 2001 this parasitoid expanded to all citrus grown in continental Spain and the Balear Islands, becoming the most abundant parasitoid in all the orchards, and displacing native and other introduced parasitoids. As a consequence, parasitism on second instars increased from less than 16% to 65% and on third instars from 35–38% to 59%. Overall, the mean percentage of parasitism increased from 20–25% to near 60%. Apparently, C. phyllocnistoides reduced by 34% the number of eggs and early instars of the host, and by 72% the number of adults. Damage to citrus foliage decreased by 56%.     

Seasonal variation and infestation incidence by Marmara gulosa (Lepidoptera: Gracillariidae) on grapefruit in the Coachella Valley,California

The population dynamics of citrus peelminer, Marmara gulosa Guillén and Davis, were investigated in 1996-1999 in commercial grapefruit groves in the Coachella Valley, CA. The first generation of the peelminer on new fruit was observed in early June 1998; larval densities of peelminer increased at the beginning of summer and peaked in late July to early August in most years, then decreased, remaining low by the end of the summer and rest of the year. Three parasitoids were identified, with Cirrospilus coachellae Gates in highest numbers in all groves and years. Numbers of larvae parasitized by C. coachellae increased by midsummer in most groves, coinciding with the decline in densities of the citrus peelminer. Miners continued to develop on fruit left from previous harvest in June. Miners preferred the lower half canopy of the trees. Parasitism and availability of fruit for development are major components in the dynamics of the citrus peelminer.     

Host-plant mediated effects of transgenic maize on the insect parasitoid Campoletis sonorensis (Hymenoptera: Ichneumonidae)

Determining the impact of genetically modified (GM) crops on beneficial organisms is an important aspect of the environmental risk assessment of GM crops. In the present study, the impact of Bt maize expressing Cry1Ab on the development and behaviour of the parasitoid Campoletis sonorensis was compared to individuals reared on hosts fed conventionally bred plants partially resistant to the European corn borer (Ostrinia nubilalis Hübner) and on susceptible maize hybrids. Adult parasitoids reared on Bt maize-fed Spodoptera frugiperda larvae were significantly smaller (15–30%) than those reared in hosts fed either of the conventional maize hybrids. The magnitude of this effect was dependent on the size of the host at oviposition and its subsequent growth rate. The development time of C. sonorensis was not affected by the maize treatment. In choice tests, female parasitoids displayed no preference for hosts fed a specific maize hybrid. No Cry1Ab was detected within adult parasitoids.     

Development of Asian parasitoids in larvae Of Drosophila Suzukii feeding on blueberry and artificial diet

In just a few years, the Asian fly Drosophila suzukii has invaded several continents and has become a very serious pest of many fruit crops worldwide. Current control methods rely on chemical insecticides or expensive and labour‐intensive cultural practices. Classical biological control through the introduction of Asian parasitoids that have co‐evolved with the pest may provide a sustainable solution on condition that they are sufficiently specific to avoid non‐target effects on local biodiversity. Here, we present the first study on the development of three larval parasitoids from China and Japan, the Braconidae Asobara japonica and the Figitidae Leptopilina japonica and Ganaspis sp., on D. suzukii. The Asian parasitoids were compared with Leptopilina heterotoma, a common parasitoid of several Drosophilidae worldwide. The three Asian species were successfully reared on D. suzukii larvae in both, blueberry and artificial diet, in contrast to L. heterotoma whose eggs and larvae were encapsulated by the host larvae. All parasitoids were able to oviposit one day after emergence. Asobara japonica laid as many eggs in larvae feeding in blueberry as in artificial diet, whereas L. heterotoma oviposited more in larvae on the artificial diet and the Asian Figitidae oviposited more in larvae feeding on blueberry. Ganaspis sp. laid very few eggs in larvae in the artificial diet, suggesting that it may be specialized in Drosophila species living in fresh fruits. These data will be used for the development of a host range testing to assess the suitability of Asian parasitoids as biological control agents in invaded regions.     

Parasitoids of obscure mealybug,Pseudococcus viburni (Hem.: Pseudococcidae) in California: establishment of Pseudaphycus flavidulus (Hym.: Encyrtidae) and discussion of related parasitoid species

To improve natural suppression of the obscure mealybug, Pseudococcus viburni (Signoret), the parasitoids Pseudaphycus flavidulus (Brèthes) and Leptomastix epona (Walker) (Hymenoptera: Encyrtidae) of Chilean origin were released in California's Central Coast vineyards from 1997 to 1999. A survey for parasitoids of P. viburni was conducted in the Edna Valley appellation wine grape region from 2005 to 2007, 6–8 years after classical biological control releases were discontinued. Two survey methods were used. First, field collections of obscure mealybugs from commercial vineyard blocks (2005–2007) and, second, placement of “sentinel mealybugs” on potted (1 L) grape vines (2006 only). From both survey methods, P. flavidulus was recovered, albeit levels of parasitism were low (less than 0.6%). We also placed longtailed mealybug, Pseudococcus longispinus (Targioni Tozzetti), on potted plants concurrent with placement of sentinel obscure mealybugs in the vineyard in order to measure parasitoid activity on this closely-related mealybug species. No P. flavidulus were recovered from P. longispinus. Other encyrtid parasitoids reared from either P. viburni or P. longispinus were Anagyrus pseudococci (Girault), Leptomastix dactylopii Howard, Leptomastidea abnormis (Girault), Coccidoxenoides perminutus Girault, and Tetracnemoidea peregrina (Compere). A hyperparasitoid, Chaetocerus sp., was also reared. The data are discussed with respect to biological control of vineyard mealybugs and newly developed controls for the Argentine ant, Linepithema humile (Mayr) (Hymenoptera: Formicidae). Because Pseudaphycus species reared from mealybugs are superficially very similar a taxonomic key and discussion of host relationships for selected Pseudaphycus species are provided.     

Parasitoids acquired byColeophora parthenica [Lepidoptera: Coleophoridae] ten years after its introduction into southern California for the biological control of Russian thistle

Parasitism of the stem and branch-boring mothColeophora parthenica Meyrick [Lepidoptera: Coleophoridae], introduced into California for the biological control of Russian thistle,Salsola australis R. Brown [Chenopodiaceae] was studied in the Coachella Valley of southern California during 1985–1986. Eight parasitoid species were reared from overwintering larvae ofC. parthenica, but none from the F₁ larvae, and just 2 individuals of one species from the F₂ summer generation. The level of parasitism of overwintering larvae was positively correlated with branch diameter, and ranged from 2% in the primary (main) branches to 45% in the tertiary branches in the spring 1985 sample, and from 2% to 19% in the spring 1986 sample, respectively. Rates of parasitism>20% were only found at sites with higher plant cover and chenopod diversity, but no other plant source or alternate hosts of the parasitoids ofC. parthenica were found. The 2 dominant species, the solitary, hymenopterous ectoparasitoids,Norbanus perplexus (Ashmead) [Pteromalidae] andEurytoma strigosa Bugbee [Eurytomidae], are both congeners of native parasitoids ofC. parthenica in Pakistan. The 2 other species of parasitoids ofC. parthenica in southern California for which other hosts are known are polyphagous and external on the larvae. No specialized endoparasitoid Braconidae, like those which dominate the native parasitoid complex in Pakistan and the U.S.S.R., have transferred toC. parthenica during its first 10 years in southern California.      

Sunflower stem weevil and its larval parasitoids in the Central and Northern Plains of the USA

The sunflower stem weevil, Cylindrocopturus adspersus (LeConte) (Coleoptera:Curculionidae), is apest of cultivated sunflower (Helianthusannuus L) from the southern to the northernGreat Plains. The incidence of weevilinfestation in fields from the six differentstates sampled during 1996 and 1997 ranged from33% (Minnesota) to 100% (Kansas, Colorado,Nebraska). Weevil populations in the fieldssampled were statistically greater in thecentral Plains (Colorado, Kansas, Nebraska)with a mean of 12.3 and 19.5 larvae per stalkcompared with the northern Plains (North andSouth Dakota, Minnesota) of 0.7 and 1.3 larvaeper stalk in 1996 and 1997, respectively.Parasitization of weevils varied from field tofield ranging from 1 to 100%, but was usuallyless than 20%. The nine species oflarval parasitoids recovered were allHymenoptera and included: Nealioluscurculionis (Fitch), N. collaris(Brues), Bracon sp. (Braconidae); Neocatolaccus tylodermae (Ashmead), Chlorocytus sp., Pteromalus sp.(Pteromalidae); Quadrastichus ainslieiGahan (Eulophidae), Eurytoma tylodermatisAshmead (Eurytomidae); and Eupelmus sp.(Eupelmidae). Nealiolus curculionis wasthe most prevalent parasitoid reared from C. adspersus, and it was recovered from allstates sampled. Parasitoid species richness wasgreatest in the central Plains. Thereduced number of parasitoid species foundattacking C. adspersus in the northernPlains may be caused by low host populationlevels, slow migration by parasitoids into theregion, or lack of adaptation to climaticconditions. Additional work to understandthe population dynamics of the parasitoidcomplex associated with C. adspersus mayresult in improved biological control of thesunflower stem weevil in cultivatedsunflower.     

Natural enemies for the cabbage webworm,Hellula undalis (Fabr.) (Lepidoptera: Pyralidae) in Malaysia

Four species of larval parasitoids were reared from larvae of the cabbage webworm (CWW),Hellula undalis (Fabr.) (Pyralidae: Glaphyriinae) collected from various cruciferous plants and a capparidaceous weed,Cleome rutidosperma (DC). On cabbage, only two species were recorded,viz, Bassus sp. (Braconidae) andTrathala flavoorbitalis (Cam.) (Ichneumonidae). The other parasitoids were braconids,Chelonus sp. andPhanerotoma sp. Egg or pupal parasitoids were not recorded. The parasitoids were not an important mortality factor of CWW on cabbage because they were usually present at the end of the crop season and their numbers were generally low. On the other hand, predator-exclusion experiments indicated that predators were important in determining the density of CWW on cabbage and the within-generation survival in the field. The major predator was the fire-ant,Solenopsis geminata (F.), which foraged on the prepupae and pupae.     

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.     

Experimental tests of the mechanism for ant-enhanced growth in an ant-tended lycaenid butterfly

In a previous laboratory study, larvae of the ant-tended lycaenid butterfly Hemiargus isola developed into larger adults when reared with the ant Formica perpilosa than when reared without ants. Ants neither fed butterfly larvae nor significantly delayed developmental duration. We investigated two non-exclusive hypotheses for the mechanism of this effect: larvae tended by F. perpilosa (1) consume more food, and (2) digest the food they consume more efficiently, than those reared without ants. Larvae reared in the laboratory with F. perpilosa ants became significantly heavier adults but produced a significantly lighter fecal mass than their untended counterparts, suggesting that greater food consumption was not the primary mechanism for the higher growth rates of ant-tended larvae. Tended and untended larvae were equally proficient at digesting the contents of pollen (a major natural food source) throughout the tended portion of the life cycle. Taken together, the results suggest that neither greater consumption nor higher assimilation accounts for the larger size of F. perpilosa-tended larvae. We propose that tended larvae may expend less energy than their untended counterparts. Received: 3 January 1997 / Accepted: 18 June 1997     

Mass production of Diglyphus isaea (Hymenoptera: Eulophidae), a biological control agent of a Korean population of potato leaf miner Liriomyza huidobrensis (Blanchard) (Diptera: Agromyzidae)

The potato leaf miner, Liriomyza huidobrensis (Blanchard), is an important pest of potato throughout the world, including Korea. A method was developed for mass rearing the parasitoid Diglyphus isaea (Walker) using faba bean, Vicia faba L. (Fabaceae), as the host‐plant and L. huidobrensis as the insect host. Faba bean plants were planted in pots and maintained in a greenhouse for about 15 d. Pots were then exposed to adult leaf miners in oviposition cages for 4 h. Plants containing late second to early third instar larvae were exposed to adult D. isaea in parasitoid cages for 24 h. The leaf area per pot after 15 d was 597.9 cm², which produced 103.33 larvae per pot. The number of adult parasitoids emerging per pot was 72.5; about 41% of these were female. The daily cost of parasitoid production was USD20.95 per 1000 individual parasitoids. The methodology developed for D. isaea could be used to rear other ectoparasitoids such as Hemiptarsenus spp. and Pnigalio sp. with different insect hosts like L. trifolii. This is why this mass‐rearing information is important for securing test insect materials for ecological and biological study of Liriomyza species, and also for developing a biological control for Liriomyza species other than L. huidobrensis by mass production of associated natural enemies. We are facing rapid agro‐ecosystem changes including pest systems. Continuous monitoring of Liriomyza in solanaceous crops is needed.     

Importation,colonization and establishment ofAnagyrus indicus [Hym.: Encyrtidae] onNipaecoccus viridis [Hom.: Pseudococcidae] in Jordan

Anagyrus indicus Shafeeet al. was collected on the island of Guam and released in the Jordan River Valley of Jordan in order to regulateNipaecoccus viridis (Newstead) on citrus.A. indicus was originally released in February 1984 and became colonized by April of the same year. It also dispersed by natural means up to 61 km following the original release and colonized that same year on infestedZizyphus sp. By spring of 1985 it became the dominant parasitoid attackingN. viridis. Another parasitoid,Anagyrus kamali Moursi, was collected in Jordan in June of 1985 for the first time. This latter parasitoid apparently moved into the Jordan River Valley by means of natural dispersal from a neighboring country. Infestations ofN. viridis have been greatly reduced in areas whereA. indicus became established. This paper reports the results of research only. Mention of a proprietary product does not constitute an endorsement for its use by USDA.     

Parasitism of the apple maggot,Rhagoletis pomonella,infesting hawthorns in Washington

Five species of larval parasitoids were reared fromRhagoletis pomonella (Walsh) infested fruit of hawthorn,Crataegus, collected from several locations in southwest Washington over a four year period. A braconid,Biosteres melleus (Gahan), parasitized larvae infesting fruits of a native hawthorn species,Crataegus douglasii Lindl. Another braconid,Opius downesi Gahan, emerged exclusively fromR. pomonella pupae reared from fruits of an introduced species of hawthorn,Crataegus monogyna Jacq. A pteromalid,Pteromalus sp., and two eulophids,Tetrastichus spp., attackedR. pomonella larvae infesting fruits of both hawthorn species. No parasitoids emerged from a total of 4385 pupae reared from apple. Percent parasitism ofR. pomonella was higher inC. monogyna compared toC. douglasii fruits. The highest average levels of parasitism ofR. pomonella inC. monogyna andC. douglasii fruits were 90% and 23% respectively. The kinds of parasitoids, their relative abundances and timing of parasitization on the two hawthorns was related to differences in fruit ripening patterns and its effect on the development ofR. pomonella on these two hosts. Parasitization ofR. pomonella byTetrastichus spp. is a new host record. The detection of these species andPteromalus sp. in southwest Washington are the first records of ectoparasitoids attacking this tephritid.     

Ecological and morphological characteristics of endoparasitoids on Elcysma westwoodii (Vollenhoven) (Lepidoptera: Zygaenidae)

Six species of insect endoparasitoids were identified from Elcysma westwoodii, which is the most damaging lepidopteran pest of Prunus yedoensis. From Hymenoptera, two species were identified: a species in Braconidae and Charops striatus in Ichneumonidae. From Diptera, there were four species in Tachinidae: Compsilura concinnata, Exorista sp., Pales sp. and Tachinidae spp. The parasitic ratio was 4.86% (45 of 926 larvae). The hymenopterans were parasitic on 31 individuals of E. westwoodii (68.9%) and the dipterans were parasitic on 14 individuals (31.1%). It was found that parasitoids from the larvae of E. westwoodii were all either endoparasitoids or larval parasitoids. However, Exorista sp. of Tachinidae was found to be either a larval parasitoid or larval-pupal parasitoid. Additionally, all the identified parasitoids were solitary parasitoids, as only one parasite occurred in a larva of E. westwoodii. Because the larva of E. westwoodii eats and molts after it is parasitized, all the parasitoids were identified as koinobionts. There were no big differences in morphological characteristics and life histories between C. striatus and C. concinnata. However, for Exorista sp. and Pales sp., males took 3–5 days longer to emerge from their pupae and had remarkably longer body lengths than females.     

Field parasitism levels of Ceratitis capitata larvae (Diptera: Tephritidae) by Aganaspis daci on different host fruit species in the coastal region of Tartous,Syria

The Mediterranean fruit fly, Ceratitis capitata (Wiedemann) (Diptera: Tephritidae), is a key pest of fruit trees in Syria and is attacked by the larval-pupal parasitoid, Aganaspis daci (Weld) (Hymenoptera: Figitidae). The seasonal population dynamics and distribution of A. daci were studied in surveys of orchards [Citrus reticulatum (clementine), Citrus sinensis (maourdi blood orange), Citrus paradise (grapefruit), C. sinensis (sweet orange), Eriobotrya japonica (loquat), Prunus persica (peach), Prunus domestica (plum), Malus domestica (apple), Figus carica (fig) and Psidium guajava (guava)] at eight locations along the coastal region of Syria, between November 2013 and November 2014. A total of 69.4?kg of infested fruits were sampled, yielding 4274 puparia. From these, 3173 emerged as C. capitata adults, 351 as hymenopteran parasitoids and 750 did not eclose. The parasitoids were identified as A. daci (Hymenoptera: Figitidae) and Psyttalia sp. (Szépligeti) (Hymenoptera: Braconidae). The predominant species was A. daci comprising 348 (99.1%) of the total number of parasitoids collected. Populations of A. daci were present from May 2014 to September 2014, and numbers increased with increasing temperature to peak at 32.05% and 34.01% parasitism in June and August 2014, respectively. Parasitoids were only retrieved from larvae reared from loquat, grapefruit, peach and guava with parasitism levels of 1.68%, 30.76%, 18.28% and 16.15%, respectively. These results are important because they suggest that populations of A. daci have potential to be used for biological control in integrated pest management programmes for C. capitata in the coastal region of Syria.     

The effect of host size on the sex ratio of Syngaster lepidus, a parasitoid of Eucalyptus longhorned borers (Phoracantha spp.)

The solitary larval ectoparasitoid, Syngaster lepidus Brullé, parasitizes the cryptic larvae of two wood-boring beetles, Phoracantha recurva Newman and Phoracantha semipunctata F. The objective of this study was to determine how the female parasitoids allocated the sex of progeny when presented with larval hosts of uniform size classes. Host size was directly correlated with age of the Phoracantha larval hosts. Groups of Phoracantha larvae of a single age class (2-, 3-, 4-, or 5-week-old) were exposed to parasitoids, and sex ratios of the resulting parasitoid progeny from each host age class were determined. A significant relationship was observed among the sizes of P. recurva and P. semipunctata hosts and the sex ratio of emerging parasitoids. Parasitized 2-week-old beetle larvae of both Phoracantha spp. produced only male S. lepidus progeny, whereas older larval hosts produced increasing proportions of female parasitoids (up to 80% females from 5-week-old hosts). Two-week-old Phoracantha larvae of both species produced fewer parasitoids than host larvae 3–5-week-old. The size of parasitoid progeny consistently increased with host larval age (size), and female parasitoids were larger than males across all host size classes. Male S. lepidus developed in approximately 25 days from 2-week-old hosts, and 19–21 days in 3–5-week-old hosts. Female S. lepidus developed in 22–25 days, with developmental time increasing with host size.     

Indigenous Natural Enemies Associated with Phyllocnistis citrella (Lepidoptera: Gracillariidae) in Eastern Spain

The incidence of generalist indigenous natural enemies of the citrus leafminer (CLM), Phyllocnistis citrella Stainton (Lepidoptera; Gracillariidae), was monitored during three growing seasons at two different orchards located in the major citrus-growing area of Spain. Composition of the parasitoid complex changed during the study period. However, the eulophids Cirrospilus near lyncus Walker and Pnigalio pectinicornis L. were consistently the predominant species. Despite the varying composition of the parasitoid complex, oviposition, host feeding, and predatory preferences of the natural enemies of the CLM clearly centered on third instar larvae. Incidence of beneficial fauna increased as the season progressed, reaching maximal values up to 70% of susceptible leafminers (mature larvae) at the end of the summer. Parasitism was significantly related to relative host density. However, predation showed no relationship to host availability but did so to flushing in one of the orchards. Incidence of indigenous natural enemies of the CLM should not be ignored when planning any introduction of exotic parasitoids, and their conservation should be taken into account when planning any citrus IPM strategy.     

Does host determine short‐range flight capacity of trichogrammatids?

Biological traits, such as body size, fecundity and fertility, of egg parasitoids are strongly influenced by host species, and the use of a single‐host species for consecutive generations has been showed to be detrimental for egg parasitoid biology. Besides biological traits, behaviour of egg parasitoids is also an important parameter for implying their performance in the field, but information about the effect of host on the behaviour of egg parasitoids is still scarce. Thus, this work aimed at determining the influence of host species on the short‐range flight capacity of three egg parasitoids Trichogrammatoidea annulata De Santis, Trichogramma atopovirilia Oatman and Platner and Trichogramma bruni Nagajara reared on Anagasta kuehniella (Zeller), Corcyra cephalonica (Stainton) and Sitotroga cerealella (Olivier), for first, 10 and 28 consecutive generations. Trichogrammatids emerged inside a tubular dark flight chamber, under controlled conditions, and short‐range flying response was based on the proportions of adults trapped to the sticky top of the chamber and the ones found on the bottom, which were checked for defective wings. Our data clearly demonstrate that trichogrammatid short‐range flight depends on the fasctidious host species. All three egg parasitoids had their flight capacity significantly reduced when emerged from S. cerealella. The highest flying capacity of T. annulata was registered when reared on C. cephalonica, while for T. atopovirilia was on A. kuehniella and T. bruni on both C. cephalonica and A. kuehniella. Parasitoid flight capacity is affected when reared on the same host over generations; however, it was not possible to define a pattern for any of the trichogrammatids. Our findings are of great relevance for quality control of mass‐reared egg parasitoids because measuring only behavioural traits with use of flight chambers can be more practical and less time‐consuming than assessing biological parameters.