Apple sawfly Hoplocampa testudinea (Hym., Tenthredinidae) and its parasitoid Lathrolestes ensator in Dutch apple orchards (Hym., Ichneumonidae, Ctenopelmatinae)

Abstract: Changes in population densities of the apple sawfly Hoplocampa testudinea (Klug) and its parasitoid Lathrolestes ensator (Brauns) were monitored in 15 apple orchards for a period of up to 4 years. The parasitoid species was found in all orchards except one, and was more numerous in plantings on sandier soils. Post‐bloom insecticide applications against other pests, and carbaryl for fruit thinning, often decimated both host and parasitoid in integrated pest management orchards. In organic orchards, where synthetic pesticides are banned, and Quassia is the only remedy against sawfly, the pest is more problematic. The low levels of parasitism in all organic orchards, except one, were possibly due to the application of wettable sulphur during the parasitoid flight period. The sawfly usually recovers more quickly than its parasitoid when chemical control is discontinued, because propagation of L. ensator is limited in various ways. The parasitoid is time limited, because suitable second instar host larvae are rarely available for more than a week on a single apple variety. Moreover, parasitism levels stay moderate because the parasitoid females do not avoid superparasitism. Finally, relatively more sawflies than parasitoids emerge after 10 months underground, because the incidence of prolonged diapause is more elevated in L. ensator than in the sawfly. It is suggested that both the high incidence of prolonged diapause and the inability to avoid superparasitism are useful in reducing the risk of local extinction. Elevated sawfly attack in a single early apple variety would reduce exploitation of suitable host larvae in other nearby varieties, in as far as the parasitoid is not able to distinguish fruitlets with accessible second instar host larvae from those with inaccessible older larvae. Although the former are available for a limited time, the latter may keep the parasitoids from moving to the less abundant second instar larvae in late(r) varieties. Reduction of elevated host density in such an early variety by a properly timed application of a short‐lived pesticide, such as Quassia, increases parasitism levels proportionally, and is expected to promote parasitoid movement to host larvae in other varieties nearby.     

Life history of Aptesis nigrocincta (Hymenoptera: Ichneumonidae) a cocoon parasitoid of the apple sawfly, Hoplocampa testudinea (Hymenoptera: Tenthredinidae)

Aptesis nigrocincta: Gravenhorst is a bivoltine ectoparasitoid of apple sawfly cocoons, hosts that must be found and parasitized by females at a depth of 10-25 cm in the soil. Females are significantly smaller than males and nearly wingless. After encountering a host, females needed 29.3 min at 20 degrees C and 19. 9 min at 25 degrees C to deposit an egg on the host. Development from egg to adult took 39.6 days for females and 38.0 days for males at 20 degrees C. This small difference was significant. At 20 degrees C, the longevity of females that had no opportunity to oviposit was on average 72.5 days, significantly higher than male longevity (50.6 days). The longevity of females given access to hosts throughout their lifetime averaged 58.6 days. Females were able to mate immediately after emergence and copulation lasted on average 21.7 s. After a pre-oviposition period averaging 5.8 days, females laid 20.2 eggs during their lifetime, thus less than one egg per day. Neither the fecundity nor longevity of individual females was correlated with body size. If females were deprived of food, longevity as well as lifetime fecundity were drastically reduced. Field studies were carried out in one organically managed apple orchard in Switzerland. Aptesis nigrocincta showed parasitism rates ranging from 12.1 to 39.7 % within single parasitoid generations, thereby constituting the most important mortality factor of apple sawfly cocoons.     

Biocontrol of the apple sawfly,Hoplocampa testudinea,with entomogenous nematodes

Four types of experiments were conducted to assess the pathogenicity of entomogenous nematodes against the apple sawfly,Hoplocampa testudinea Klug (Hymenoptera: Tenthredinidae). In Petri dish,Steinernema carpocapsae (Weiser) DD 136 strain,S. carpocapsae All strain,S. feltiae (Filipjev) andHeterorhabditis bacteriophora Poinar caused 100% larval mortality 72 h after the treatments. In semi-field conditions under dwarf apple trees, a single treatment with either 40 or 80S. carpocapsae All strain/cm² caused significant (>80%) larval mortality. No significant increase in mortality was obtained with a second application. In 1990, late treatment with 80S. carpocapsae All strain/cm² caused significant (39.1%) pupal mortality. In 50×50 cm quadrats under dwarf apple trees, treatment with 40 and 80S. carpocapsae All strain/cm² were done in spring 1989. In spring 1990, respectively 22 and 25 apple sawfly adults emerged from quadrats treated with 40 and 80S. carpocapsae All strain/cm², whereas 78 adults emerged from untreated quadrats. In a foliar application experiment, a single treatment withS. carpocapsae All strain significantly reduced the percent of fruit showing secondary damage. The possibility of using entomogenous nematodes as part of an integrated pest management in apple orchards is discussed, with particular reference to the integration of programs aimed at managing plum curculio,Conotrachelus nenuphar (Herbst) (Coleoptera: Curculionidae) populations.      

Prediction of flight of apple sawfly, Hoplocampa testudinea, using temperature sums

A method to predict the beginning of the flight of apple sawfly, Hoplocampa testudinea (Klug) (Hymenoptera, Tenthredinidae) is presented. Adults were monitored during 8 years at the experimental orchard De Schuilenburg, Kesteren, The Netherlands, with visual sticky traps. Temperature sums, accumulated until the day of the first capture of sawfly, were calculated for different starting dates of the summations. Beginning on 1 January, variation of the temperature sums, calculated in each of 8 years, decreased when later starting dates for temperature summation were chosen, reaching a minimum on 1 April for soil temperatures (–5 cm). The soil temperature sum, accumulated from 1 April until the first capture, was on average 134 day-degrees above a threshold of 4 °C. So this was the most suitable starting date to predict the beginning of sawfly flight activity. As use of the summation method based on air temperatures is in practice more appropriate for timing of trap installation by extension services and apple growers, trap deployment is recommended at an adapted value of 157 day-degrees from 15 March.     

Soil application of Beauveria bassiana GHA against apple sawfly,Hoplocampa testudinea (Hymenoptera: Tenthredinidae): Field mortality and fungal persistence

Low impact alternatives to synthetic insecticides for the control of apple sawfly (Hoplocampa testudinea Klug) are scarce encumbering pest management in organic apple orchards. We investigated the soil persistence and field efficacy of the entomopathogenic fungus Beauveria bassiana (Balsamo) Vuillemin (BotaniGard) against apple sawfly under common organic orchard practices. We also assessed the efficacy of B. bassiana GHA and Metarhizium brunneum Petch (indigenous strain) against sawfly in the laboratory. Larvae treated with either fungus in the laboratory died faster than control larvae and displayed 49.4%–68.4% mycosis. In the field, B. bassiana density remained high in the week after application, during larval descent to the soil. Fungal density decreased to 25% at 49 d after application and to 0.4% after 55 weeks. Molecular markers revealed that the majority of fungal isolates recovered comprised the applied B. bassiana strain GHA. Larvae pupating in soil cages in the orchard for 49 d displayed 17% mycosis. The high efficacy under laboratory conditions was not seen in the field. B. bassiana application resulted in densities above the upper natural background level during the growing season, but reversion to background levels occurred within a year. It remains to be investigated whether this has a detrimental effect on nontarget organisms. Additional work is needed to bridge the knowledge gap between laboratory and field efficacy in orchards.     

The apple sawfly, Hoplocampa testudinea: a temperature driven model for spring emergence of adults

The effect of temperature on post-diapause development of the apple sawfly Hoplocampa testudinea Klug was studied under controlled conditions. Survival was found to decrease at temperatures higher than 15°C, the lethal temperature being close to 25°C. The lower thermal threshold was 4.5°C; the values for males and females did not differ significantly. However, different values were established for unprotected individuals, in vermiculite and in potting compost respectively. Based on the overall mean and variance of the developmental time and the overall thermal threshold a simple soil temperature driven phenology model was constructed using a time- varying distributed delay. The validation with independent field and semi-field data revealed the model to be a reliable tool to predict apple sawfly phenology and hence to determine the optimal time for the installation of white sticky traps or for control measures such as insecticide treatments.     

Resource quality and spatial variation in sex ratios of a free-living solitary sawfly,Dineura virididorsata (Hym., Tenthredinidae)

The sex ratio in final-instar larvae of a birch-feeding, free-living solitary sawfly, Dineura virididorsata, was investigated in Finnish Lapland. The prepupal proportion of females, pooled over ten sites, was 56%, and at four individual sites the sex ratio was significantly female-biased. Larval survival from egg to prepupae did not differ between the sexes. This suggests a femalebiased primary sex ratio in the field. The sex ratio varied among the sites but not among host trees within sites. Contrary to previous results with hymenopterans, we did not find that differences in the sex ratio depended on forage quality: site-specific or tree-specific sex ratios did not correlate with the average prepupal weight. A literature search indicated that female-biased sex ratios are also common in other free-living sawflies. We are unable to explain sex ratios of Dineura virididorsata or other free-living sawflies with existing general models.     

Impact of males on the progeny sex ratio of Campoletis chlorideae (Hym., Ichneumonidae), a parasitoid of Helicoverpa armigera (Hübner) (Lep., Noctuidae)

Abstract: The endoparasitoid Campoletis chlorideae and its host Helicoverpa armigera were reared in the laboratory to determine the progeny sex ratio of C. chlorideae in the presence and absence of male parasitoids. It was observed that the presence of male parasitoids affects the progeny sex ratio by decreasing the number of females in the offspring population, i.e. a significant increase in the proportion of males was observed in united sexes. Therefore, while constructing the life table of the parasitoid, the effect of presence of male parasitoids, should be considered together with other factors, which decreases the efficiency of the parasitoid.     

Egg limitation and the functional response of the parasitoid Campoletis grioti (Hym: Ichneumonidae)

The hypothesis that mature egg availability during a parasitoid's lifetime affects the functional response, as well as a parasitoid's handling time and searching efficiency, was tested. Campoletis grioti Blanchard (Hym: Ichneumonidae) female parasitoids and Spodoptera frugiperda Smith (Lep: Noctuidae) host larvae were used as an example. Each female of C. grioti was confined with different host densities (6, 10, 30, 50, 80, 120 and 160 larvae/day) of first and second S. frugiperda instars until the female died. We found that C. grioti showed a type II functional response, with a reduction in the number of parasitized hosts in relation to female ageing. Handling time and searching efficiency increased over time. When we standardized the data simulating unlimited egg supply, the functional response, handling time and searching efficiency became constant throughout the parasitoid's life. We discuss the relationship between egg availability and functional response and its associated parameters, and its consequence on biological control programs.     

Influence of crucifer cropping system on the parasitism ofPlutella xylostella (Lep., Yponomeutidae) byCotesia plutellae (Hym., Braconidae) andDiadegma semiclausum (Hym., Ichneumonidae)

Field experiments were conducted to study the influence of cabbage monoculture and mixed cropping on the parasitism of diamondback moth,Plutella xylostella (L.), a destructive pest of all crucifers, by 2 larval parasites,Diadegma semiclausum Hellén andCotesia plutellae Kurdjumov. There was no significant difference in parasitism by either species whether cabbage was planted in insecticide-free monoculture or in mixed cropping with 8 noncrucifers which were sprayed twice a week with chemical insecticides mevinphos, methamidophos and permethrin. Population ofP. xylostella increased as the cabbage plants grew older. Parasitism byC. plutellae was higher soon after cabbage transplanting but decreased as the plants grew older. Parasitism byD. semiclausum was very low soon after cabbage planting but increased as the plants grew older. A significant negative correlation was found betwen parasitism byC. plutellae andD. semiclausum. In a caged field study where only one parasite species was used in an individual cage, parasitism ofP. xylostella by both species decreased as theP. xylostella population increased. This is believed to be due to the absence of competition between the two parasites inside the cage. There was no relationship between host-plant age and parasitism ofP. xylostella larvae by either parasite species.     

Variation in Encardia (Hym., Ichneumonidae) with a key to the species

The Ethiopian genus Encardia Tosquinet is redefined and a key is given to the two species, picta Tosquinet and rufantennata Benoit, now recognised. Type data are given for the twelve nominal taxa now included in E. picta together with data on the three variations found in wing colour pattern.     

Review of the sawfly genus Empria (Hymenoptera, Tenthredinidae) in Japan

The following eleven Empria species are reported from Japan: Empria candidata (Fallén, 1808), Empria japonica Heidemaa & Prous, 2011, Empria liturata (Gmelin, 1790), Empria loktini Ermolenko, 1971, Empria plana (Jakowlew, 1891), Empria quadrimaculata Takeuchi, 1952, Empria rubicola Ermolenko, 1971, Empria tridens (Konow, 1896), Empria tridentis Lee & Ryu, 1996, Empria honshuana Prous & Heidemaa, sp. n., and Empria takeuchii Prous & Heidemaa, sp. n. The lectotypes of Poecilosoma pallipes Matsumura, 1912, Empria itelmena Malaise, 1931, Tenthredo candidata Fallén, 1808, and Tenthredo (Poecilostoma) hybrida Erichson, 1851 are designated. Empria itelmena Malaise, 1931, syn. n. is synonymized with Empria plana (Jakowlew, 1891). Poecilosoma pallipes Matsumura, 1912, previously assigned to Empria, is transferred to Monsoma, creating Monsoma pallipes (Matsumura, 1912), comb. n. Results of phylogenetic analyses using mitochondrial (COI) and nuclear (ITS1 and ITS2) sequences are also provided.     

Influence of different sugars on the longevity of Bathyplectes curculionis (Hym., Ichneumonidae)

Abstract:  Floral nectars, homopteran honeydews and honey are known to increase parasitoid longevity. However, these foods are composed of several sugars which may differentially affect longevity. We tested the effects of individual sugars and mixtures on the longevity of Bathyplectes curculionis Thomson (Hym., Ichenumonidae), a natural enemy of the alfalfa weevil. There was a significant difference in the longevity of female wasps on the various diets. Glucose or fructose alone appeared to have the most benefits while trehalose and melezitose were not as useful for increasing wasp longevity. Suitability of these sugars for provisioning food for parasitoids in the field is discussed.     

Effects of two neem insecticide formulations on the attractiveness, acceptability and suitability of diamondback moth larvae to the parasitoid, Diadegma mollipla (Holmgren) (Hym., Ichneumonidae)

Abstract:  Behavioural responses of female Diadegma mollipla to volatiles from cabbage plants and host-infested [ Plutella xylostella (L.)] cabbage plants sprayed with two neem insecticide formulations were investigated in a Y-tube olfactometer. Parasitoids were significantly more attracted to volatiles from cabbage and host-infested cabbage sprayed with the powder formulation than to clean air. In contrast, parasitoid response to volatiles from cabbage and host-infested cabbage sprayed with the oil formulation was not significantly different from clean air. In choice tests between infested plants sprayed with water (control) or the powder formulation, parasitoids showed no preference for volatiles from either of the treatments. In similar tests with the oil formulation, parasitoids showed a preference for volatiles from control plants over plants sprayed with the oil formulation. In host acceptance and suitability tests, parasitism rates in the neem- and water-sprayed hosts were, with one exception, not significantly different. However, the neem-sprayed larvae died earlier than control larvae and were therefore not able to support parasitoid development. The implication of these findings for the combined use of neem insecticides and parasitoids in the management of P. xylostella is discussed.     

Introduction,establishment, and impact of Lathrolestes thomsoni (Hymenoptera: Ichneumonidae) for biological control of the ambermarked birch leafminer,Profenusa thomsoni (Hymenoptera: Tenthredinidae), in Alaska

The ambermarked birch leafminer, Profenusa thomsoni Konow (Hymenoptera: Tenthredinidae), was first discovered in Alaska in 1991 but was not correctly identified until 1996 when it invaded Anchorage and became a widespread and damaging pest to forest and urban birches. In 2003, the parasitoid wasp, Lathrolestes thomsoni Reshchikov (Hymenoptera: Ichneumonidae), was selected as a candidate for a classical biological control program against P. thomsoni. Parasitized leafminer larvae were collected from the Northwest Territories and Alberta, Canada, where it was previously introduced and causing injury to Betula spp., and transferred to Alaska in soil as pre-pupae for emergence. From 2004 to 2008, 3636 adult L. thomsoni adults were released in birch stands in Alaska. Parasitoids were later recovered at all six release sites in Anchorage and the Kenai Peninsula. While percent leaves mined declined by 30–40% at parasitoid release sites over the period of this study, a similar decline was also observed at paired, non-release long-term monitoring sites. Therefore, the decline in the pest density cannot be ascribed entirely to L. thomsoni.     

Adult size and reproduction in the ectoparasitoid Agrothereutes lanceolatus Walker (Hym., Ichneumonidae)

The effects of adult male and female size on reproductive performance in Agrothereutes lanceolatus Walker, a solitary ectoparasitoid of mature larvae and pupae of several pyralids and tortricids, were investigated. Females had a longer mean lifetime than males. Larger females lived longer, whereas the size of males did not influence the longevity. The number of ovarioles per female did not differ among females of different sizes but larger females carried a greater number of mature and immature eggs. When presented with host cocoons, large females parasitized a higher percentage of hosts than small females. This was due to the fact that larger females accepted more hosts for oviposition whereas smaller ones rejected more hosts. Small and large females used equal numbers of hosts for host-feeding, suggesting that large females removed a greater amount of materials from single hosts through host-feeding.     

Molecular phylogeny of the sawfly subfamily Nematinae (Hymenoptera: Tenthredinidae)

Abstract.  Nematinae is one of the largest subfamilies in the sawfly family Tenthredinidae, but internal relationships are unknown in the absence of any formal phylogenetic analysis. To understand the internal phylogeny of Nematinae, we sequenced a portion of the mitochondrial cytochrome oxidase I gene and the nuclear elongation factor-1α gene from thirteen outgroup taxa and sixty-eight nematine species, the ingroup taxa of which represent all major genera and subgenera within the subfamily. Maximum parsimony and Bayesian phylogenetic analyses of the DNA sequence data show that: (1) Nematinae are monophyletic in a broad sense which includes Hoplocampa , Susana and the tribe Cladiini, which have been classified often into separate subfamilies; together with Craterocercus , these taxa form a paraphyletic basal grade with respect to the remaining Nematinae, but among-group relationships within the grade remain weakly resolved; (2) the remainder of the ingroup, Nematinae s. str, is monophyletic in all combined-data analyses; (3) within Nematinae s. str, the 'Higher' Nematinae is divided into three groups, Mesoneura and the large tribes Nematini and Pristiphorini; (4) although the traditional classifications at the tribal level are largely upheld, some of the largest tribes and genera are obviously para- or polyphyletic; (5) according to rate-smoothed phylogenies dated with two fossil calibration points, Nematinae originated 50–120 million years ago. In addition, the results from all Bayesian analyses provide strong and consistent support for the monophyly of Tenthredinidae, which has been difficult to demonstrate in previous parsimony analyses of morphological and molecular data.     

Role of the cocoon ofAcrolepiopsis assectella (Lep., Hyponomeutoidae) in host recognition by the parasitoidDiadromus pulchellus (Hym., Ichneumonidae)

The study of various behavioural criteria of femaleDiadromus pulchellus parasitoids in the presence of theirAcrolepiopsis assectella hosts has shown the essentially chemical nature of the stimulant determining host recognition. The physical stimuli of the cocoon seem not to be implicated. Thus cocoons whose original texture has been completely altered, either mechanically or chemically, as well as the silk excreted by the host caterpillars significantly stimulates the female parasitoids. The cocoon contact kairomones are detected in testing the aqueous extracts ofA. assectella which provoke a positive behavioural response from the females in a threshold concentration of 1 cocoon-equivalent. The comparison of aqueous extracts ofA. assectella host cocoons, and of non-host species:Bombyx mori, Ephestia kuehniella andCacoecimorpha pronubana demonstrate the kairomone specificity of the silk, the extracts of non-host cocoons being ignored by the parasitoid, as were the silk threads left byE. kuehniella caterpillars. Finally the contact kairomones linked to the silk seem to be independent of the host plant and of the nutrient diet of the host caterpillars. The cocoons spun by the caterpillars reared on leeks or on artificial diets with or without powdered leek provoke similar responses in the parasitoids.     

Host behaviour and its influence on foraging and acceptance by the solitary parasitoid wasp,Venturia canescens (Hym: Ichneumonidae)

Behavioural interactions between the solitary koinobiont parasitoid,Venturia canescens, and two of its hosts,Plodia interpunctella andCorcyra cephalonica, were investigated. The response of both hosts to simulated antennation using a two-haired brush was examined over instars 3 (L3) to 5 (L5). YoungP. interpunctella larvae predominantly adopted escape tactics (writhe, trash) whereas L5P. interpunctella usually froze after the stimulus was applied. L3C. cephalonica larvae were more aggressive (headrear, flick) thanP. interpunctella in response to the application of the stimulus, but olderC. cephalonica responded less aggressively than in earlier instars. AlthoughV. canescens readily jabbed its ovipositor at both hosts after antennation,P. interpunctella was considerably more susceptible to parasitoid attack thanC. cephalonica, irrespective of size in the final (L5) instar.C. cephalonica, the larger, more aggressive host, actively resisted parasitism whereasP. interpunctella responded much more passively after parasitoid contact. Parasitoids examined and jabbed their ovipositors at dead hosts, but this behaviour was not sustained, implying that host movement stimulates parasitoid attack. On patches containingV. canescens, L5C. cephalonica andP. interpunctella, mostP. interpunctella larvae responded by freezing after parasitoid contact.P. interpunctella that froze usually avoided parasitism, whereas larvae that attempted to escape by crawling were pursued with vigour byV. canescens and usually parasitized. Irrespective of behaviour after parasitoid contact,C. cephalonia displayed more aggressive behaviour and had much greater success in warding off parasitoid attack. Host acceptance byV. canescens is clearly affected by the size and species of the host it attacks. The influence of host defensive behaviour is discussed in relation to the evolution of parasitoid counter-defences and oviposition strategies.     

Evidence for the importance of odour-perception in the parasitoid Rhopalicus tutela (Walker) (Hym., Pteromalidae)

Possible host location mechanisms in the chalcid wasp Rhopalicus tutela (Walker) (Hym., Pteromalidae), a parasitoid of the eight-spined spruce bark beetle, Ips typographus (L.) (Col., Scolytidae), were examined. This was carried out in order to repeat and complement former studies on parallel parasitoid–scolytid systems that had contradictory results. Morphological examinations of the parasitoid antennae were made using both scanning and transmission electron microscopy. Possible functions of the sensilla placodea (multiporous plate sensillum), and other sensilla present on the antennae, have been indicated. For the first time, the placoid sensilla in a pteromalid parasitoid have shown porous walls and numerous innervations, which are typical characteristics for chemoreceptors. Previously the placoid sensilla have been suggested to be an infrared receptor. In order to test the chemoreceptive ability of R. tutela females and males, a synthetic reference blend was analysed by combined gas chromatography and electroantennographic detector (GC-EAD). Their sensitivity to host-related volatiles (such as certain pheromone components and oxygenated monoterpenes) was significantly greater than that for host-tree-related compounds (monoterpene hydrocarbons). Employing an infrared thermo-scanner, the current study failed to detect 'hot spots' associated with susceptible hosts beneath the bark. Results from electrophysiology and electron microscopy revealed clear odour-perceptive functions of the parasitoid antennae. These results strongly support the major importance of volatiles in host location by the bark beetle parasitoid R. tutela .