Foraging behaviour of a leafminer parasitoid in the field

Abstract. 1. The searching behaviour of the parasitoid Sympiesis sericeicornis Nees (Hymenoptera, Eulophidae) is analysed under field conditions.
2. Females were tracked when flying around the canopy of apple trees infested with the tentiform leafminer Phyllonorycter cydoniella (D. & S.)(Lepidoptera, Gracillariidae) and their behaviour studied at the level of a single mine and at the level of several mines on the same leaf (patch level).
3. The presence of mines is detected during flight. The foraging behaviour at the patch level is efficient: the female is able to distinguish the suitable from the unsuitable hosts and handle the suitable hosts first. Not all mines are visited before departure from the leaf and those left unvisited are exclusively mines without suitable hosts. The patch leaving rule is discussed.
4. An ethogram of the behaviour on the mine is constructed. Selected behavioural categories are analysed for different combinations of mine content and outcome of the visit to the mine. The assessment of the mine content is done in a differential way, quickly and without mistakes.
5. The results are discussed in the context of two environmental factors, wind speed and temperature, which reduce the available time for searching. They are also related to the growing percentage of unsuitable hosts during each host generation. Tentiform mines remain attractive for a long period of time, even after parasitism or emergence of the adult, and their examination reduces the rate of host discovery.     

Parasitoid foraging decisions mediated by artificial vibrations

In any host-parasitoid interaction, the detection of the host in its microhabitat is a crucial step in the interaction that has a major influence on the parasitoid's fitness. We used bioassays to investigate whether the parasitoid Sympiesis sericeicornis (Hymenoptera: Eulophidae) uses the vibrations of its host Phyllonorycter sp. gr. blancardella (Lepidoptera: Gracillariidae) to detect it in the leaf mine. From the large variety of signals produced by the host, we identified a unitary signal that could be reproduced artificially. We then sent this signal into emptied mines to analyse the reaction of the parasitoid. The wasps reacted by increasing both the time spent foraging on the mine and the number of insertions of the ovipositor to detect the ‘virtual’ host. This study is the first to show that parasitoids detect host vibrations.     

An account of the Chalcidoidea (Hymenoptera) parasitising leaf-mining insects of deciduous trees in Britain

Data on the distribution and frequency of hymenopterous parasites of leaf-mining insects on deciduous trees show that Chalcidoidea of the family Eulophidae are the chief component of the parasite faunas. The regular parasite complement of a leaf-mining species is in the order of 10 to 20 species of parasitic Hymenoptera. Many of these are polyphagous, but in almost all instances a preference for a particular type of host is evident. The parasite faunas of tree leaf-mining Lepidoptera, Coleoptera and Hymenoptera are shown to be qualitatively similar, but those of Diptera are rather different. The parasite faunas of tree leaf-miners are different also from those of leaf gall-forming insects on trees and, to a lesser degree, from those of leaf-miners on herbaceous plants. The parasite fauna associated with a tree genus is quantitatively and qualitatively characteristic and, in general, it most resembles that found on allied tree genera. Congeneric leaf miners attacking the same tree species are attacked by very similar parasite faunas, although mine situation and season of development may exert some influence. These latter factors are considered especially in relation to leaf-miners of the genus Phyllonorycter for which most data are available.     

Two forms of egg defence in a chrysomelid beetle: egg clumping and excrement cover

Abstract.

• 1 Field experiments demonstrated that the faecal covering that female Microrhopala vittata (Fabr.) (Coleoptera: Chrysomelidae) place over their egg masses significantly reduces egg mortality.
• 2 The bottom egg in the egg mass, which lies against the leaf of the host plant, suffers significantly higher mortality than the other eggs in the egg mass.
• 3 The parasite Chrysonotomyia sp. (Hymenoptera: Eulophidae) generally parasitizes only the bottom egg in the egg mass, while predators rarely penetrate the faecal covering.
• 4 No significant relationship was found between mortality and the number of egg masses per leaf.
• 5 By placing eggs in masses, females may ensure that at least the upper eggs in any egg mass are effectively protected against virtually all natural enemies likely to pose a threat.

     

Host location by a parasitoid using leafminer vibrations: characterizing the vibrational signals produced by the leafmining host

Abstract. The aim of this study was to characterize the vibrations produced by the apple tentiform leafminer Phyllonorycter malella (Ger.) (Lepidoptera, Gracillariidae). Host location using vibrations by one of its parasitoids Sympiesis sericeicornis Nees (Hymenoptera, Eulophidae) was postulated by Casas (1989) on the basis of detailed quantitative behavioural observations and has also been suggested by other authors on similar systems. Both host and parasitoid send and may receive vibratory signals; consequently we first attempted to characterize and classify the signals, one of the first steps required in the design of an adequate vibrational biotest. In this respect, our approach differs fundamentally from the familiar setting of host location via semiochemicals and is best framed within the context of vibratory communication. Vibrational signals produced by a moving larva and pupa were measured on several spots on the leaf using a laser vibrometer. The emitted signals were characterized by their temporal patterns of change in amplitude and frequency spectra. The vibrational patterns released by a moving larva were different from those released by a wriggling larva and a wriggling pupa in the time as well as in the frequency domains. Wriggling larvae and wriggling pupae triggered vibrations that were similar in frequency, but differed in their temporal pattern. Frequencies up to 15 kHz could be identified. The amplitudes and frequencies of the signals both decreased significantly from the tip to the base of the leaf. A wriggling pupa and a wriggling larva produced stronger signals than a foraging larva. All calculated parameters (displacement, velocity, acceleration, and duration of the signal components) of the vibrational signals were found to be in a range comparable with others used for well-known arthropod communication systems. The vibrations produced by the host displayed distinct characteristics: they could usually be distinguished easily from background noise; could be perceived anywhere on the leaf; and were specific for a certain host stage and activity. Our findings support the hypothesis that vibration signals represent a reliable source of information to foraging parasitoids and, therefore, explain certain behavioural patterns observed in a population of S. sericeicornis females foraging in the field.     

Diglyphus isaea (Hymenoptera: Eulophidae): a probable complex of cryptic species that forms an important biological control agent of agromyzid leaf miners

Diglyphus isaea ( Walker 1838 ) (Hymenoptera: Eulophidae) is a primary parasitoid of agromyzid leaf miners (Diptera: Agromyzidae) and has been commercialized as a biological control agent. Diglyphus isaea occurs throughout much of the world and different populations are morphologically identical. Using nuclear ribosomal internal transcribed spacer 1 (ITS1) sequences, we examined variation among Chinese populations of D. isaea . Phylogenetic analyses combined with an analysis of sympatry indicated that D. isaea consists of at least four species in mainland China. The results imply that ITS1 is an efficient marker for identifying congeneric species of parasitic waSPS, and that cryptic species could be common in temperate and subtropical regions.     

Phylogenetic relationships of egg parasitoids (Hymenoptera: Eulophidae) and correlated life history characteristics of their Neotropical Cassidinae hosts (Coleoptera, Chrysomelidae)

Egg parasitoids in the family Eulophidae (Hymenoptera) are an important part of the community of insects attacking neotropical leaf beetles in the subfamily Cassidinae. We present a phylogeny of 24 species of oophagous Eulophidae, using the 28S rDNA, the ITS2 rDNA and the cytochrome b genes, applying the NJ, MP, ML and Bayesian tree reconstruction methods on each data set. We ask whether the phylogenetic relationships of the parasitoids are linked with the life history characteristics of their beetle hosts. We show that cladogenesis in the oophagous Eulophidae does correlate with ovipositional behaviour and, to a lesser extent, diet and tribal affinities of their hosts. Additionally using two methods of simultaneous analysis of several gene sets: the Total Evidence method, and the construction of a "supertree" by Matrix Representation Parsimony (MRP), we substantiate the same major phylogenetic relationships within the Eulophidae.     

A comparison of artificial diets for mass rearing Brontispa longissima (Coleoptera: Chrysomelidae) as hosts for the larval and the pupal parasitoids

The coconut hispine beetle, Brontispa longissima (Gestro) (Coleoptera: Chrysomelidae) is a serious pest of coconut palm. In this study, we developed an artificial diet for B. longissima so that the beetle could be used as a host for rearing two of its parasitoids, Asecodes hispinarum Boucek (Hymenoptera: Eulophidae) and Tetrastichus brontispae Ferrière (Hymenoptera: Eulophidae). The new artificial diet represents an improvement of our previous diet, which we used as a control. When beetle larvae were reared on the new diet, which contains cysteine but not cellulose powder and has twice as much coconut leaf powder as in the control, the adult emergence was 71% (approximately 2 times that in the control). We also examined the suitability of beetles fed on the new diet as hosts for the larval parasitoid A. hispinarum and the pupal parasitoid T. brontispae. The percentage of wasps that emerged from hosts that were fed the new diet was higher than that from the control-fed hosts. The new diet allowed both A. hispinarum and T. brontispae to produce adult wasps of the next generation, whereas the control only allowed T. brontispae to produce the next generation. These results suggest that the new diet is suitable for B. longissima and will facilitate mass-rearing of A. hispinarum and T. brontispae.     

Reaction of parasitoids of the paper wasp Polistes dominulus (Christ) (Hymenoptera, Vespidae, Polistinae) to the host distribution

The specific features of spatio-temporal organization of the parasitoid-host system in a heterogeneous environment was analyzed. The spatial distribution of ectoparasitoids in different habitat types of their host Polistes dominulus (Christ) (Hymenoptera, Vespidae) was found to be non-uniform. Latibulus argiolus (Rossi) (Hymenoptera, Ichneumonidae) prevailed in the host nests located in shelters, while Elasmus schmitti Ruschka (Hymenoptera, Eulophidae) prevailed in the nests attached to plants.     

Choosy egg parasitoids: Specificity of oviposition-induced pine volatiles exploited by an egg parasitoid of pine sawflies

Generalist parasitoids are well‐known to be able to cope with the high genotypic and phenotypic plasticity of plant volatiles by learning odours during their host encounters. In contrast, specialised parasitoids often respond innately to host‐specific cues. Previous studies have shown that females of the specialised egg parasitoid Chrysonotomyia ruforum Krausse (Hymenoptera: Eulophidae) are attracted to volatiles from Pinus sylvestris L. induced by the egg deposition of its host Diprion pini L. (Hymenoptera: Diprionidae), when they have previously experienced pine twigs with host eggs. In this study we investigated by olfactometer bioassays how specifically C. ruforum responded to oviposition‐induced plant volatiles. Furthermore, we studied whether parasitoids show an innate response to oviposition‐induced pine volatiles. Naïve parasitoids were not attracted to oviposition‐induced pine volatiles. The attractiveness of volatiles from pines carrying eggs was shown to be specific for the pine and herbivore species, respectively (species specificity). We also tested whether not only oviposition, but also larval feeding, induces attractive volatiles (developmental stage specificity). The feeding of D. pini larvae did not induce the emission of P. sylvestris volatiles attractive to the egg parasitoid. Our results show that a specialist egg parasitoid does not innately show a positive response to oviposition‐induced plant volatiles, but needs to learn them. Furthermore, the results show that C. ruforum as a specialist does not learn a wide range of volatiles as some generalists do, but instead learns only a very specific oviposition‐induced plant volatile pattern, i.e., a pattern induced by the most preferred host species laying eggs on the most preferred food plant.     

Matching host reactions to parasitoid wasp vibrations.

The sensory ecology of predator detection by prey has been little studied for any arthropod prey predator system, in contrast to the sensory ecology of prey finding by predators. The aim of this study was to quantify the foraging signals produced by the parasitoid Sympiesis sericeicornis (Hymenoptera: Eulophidae) and the sensory ecology of enemy detection and the avoidance behaviour of the leaf-mining host, Phyllonorycter spp. (Lepidoptera: Gracillariidae). We used synthetic vibrations approximating the signals generated by ovipositor insertions to stimulate the host in its mine. Tothe authors' knowledge, this is the first manipulative study to describe a match in the frequency range between a parasitoid foraging stimulus and a host behavioural response. We discuss our findings in relation to other predator-prey systems for which a coevolution between prey sensitivity and predator signal has been described.     

Processes Driving Ontogenetic Succession of Galls in a Canopy Tree1

Herbivores can be associated with distinct ontogenetic stages of their host in a nonseasonal, directional, and continuous pattern of colonization and extinction of species populations called ontogenetic succession, but the processes behind this pattern are still largely unknown. We used plants of Cryptocarya aschersoniana Mez (Lauraceae) belonging to different ontogenetic stages, to examine how the density of different gall‐inducing insects varies along the ontogeny of the host, and how gall density is influenced by mechanisms associated with host quality (plant height, plant shape, leaf area, specific leaf area, and hypersensitivity), and by mechanisms associated with their natural enemies (parasitoids, pathogens, and predators). In a remnant of Araucaria Forest, located in the São Francisco de Paula National Forest (Brazil), gall density (ind./100 g of leaf ) was obtained for 42 plants of C. aschersoniana divided into three height classes. Two galling species were recorded, showing quite distinct density patterns among height classes of C. aschersoniana. While Hymenoptera gall density decreased almost 50 times from small plants to canopy trees, Hemiptera gall density increased almost 10 times. Path analyses showed that Hymenoptera density was higher in smaller plants, independent of other host traits, while Hemiptera density was higher in plants exhibiting smaller leaves. Natural enemies were not detected in the Hemiptera population, and mortality rates due to predators, parasitoids, and pathogens did not affect Hymenoptera density. Processes associated with plant quality play the main role in generating the observed ontogenetic succession pattern.     

Parasitoid vibrations as potential releasing stimulus of evasive behaviour in a leafminer

Abstract. The aim of this study was to characterize the vibratory signals produced by the parasitoid Sympiesis sericeicornis Nees (Hymenoptera: Eulophidae) while foraging on apple leaves infested by one of its hosts, the spotted tentiform leafminer Phyllonorycter malella (Ger.) (Lepidoptera: Gracillariidae).This leafminer changes its behaviour as a function of the parasitoid's behaviour to escape parasitization.We propose that the leafminer uses vibrations triggered by the parasitoid to detect the presence of its enemy.We measured vibrations produced by a foraging parasitoid on a mine with a laser vibrometer.By recording concurrently the behaviour of the parasitoid on video, vibrations could be assigned to particular behaviours.Subsequently, vibrations were characterized by their dominant frequencies and intensities.The behaviours Landing and Take-off both produced strong impact-like vibrations characterized by an initial irregular phase during which frequencies up to 25 kHz occurred followed by a slow decaying regular phase.Vibrations elicited by Moving, Standing and Probing showed no clear temporal pattern.During Probing , dominant frequencies of up to 5.6 kHz were observed frequently at intensities well above the background noise (>10 dB).During Moving and Standing , vibrations were more scarce and of lower frequencies and intensities.Due to their impact-like nature, vibrations produced by Landing and Take-off are probably not specific to the parasitoid.Vibrations produced by Moving and Standing are difficult to detect and not reliable because of their non-specificity.Therefore, only Probing provides a reliable and detectable source of information for the host.The vibrations elicited during Probing could account for the evasive behaviour that is observed in this and other leafminers.     

First report of a hymenopteran parasitoid complex on jackfruit shoot and fruit borer Diaphania caesalis (Lepidoptera: Crambidae) from India

ABSTRACT

A survey of the species composition and relative abundance of Diaphania caesalis Walker (Lepidoptera: Crambidae) in plantations of jackfruit (Artocarpus heterophyllus Lam.) in three southern states along India’s western coast recorded thirteen species of primary parasitoids and one species of a hyperparasitoid, namely Tetrastichus pantnagerensis Khan (Hymenoptera: Eulophidae). Apanteles stantoni Ashmead (Hymenoptera: Braconidae) was the most dominant parasitoid and found in 35% of the parasitised host larvae in Karnataka, 38.5% in Kerala, and 33.1% in Tamil Nadu whereas the overall level of parasitisation, involving all the different parasitoids recorded, was approximately 41%–45% and did not vary significantly with location.     

How two different host species influence the performance of a gregarious parasitoid: host size is not equal to host quality

1. Hyssopus pallidus Askew (Hymenoptera, Eulophidae) is a gregarious ectoparasitoid of the two tortricid moths species Cydia molesta Busck and C. pomonella L. (Lepidoptera, Tortricidae). It paralyses and parasitizes different larval instars of both species inside the apple fruit, which leads to the death of the caterpillar. 2. We assessed the influence of host species characteristics and host food on the performance of the parasitoid female in terms of clutch size decisions and fitness of the F(1) generation. 3. A comparison of clutch size revealed that female parasitoids deposited similar numbers of eggs on the comparatively smaller C. molesta hosts as on the larger C. pomonella hosts. The number of parasitoid offspring produced per weight unit of host larva was significantly higher in C. molesta than in C. pomonella, which is contrary to the general prediction that smaller hosts yield less parasitoid offspring. However, the sex ratio was not influenced by host species that differed considerably in size. 4. Despite the fact that less host resources were available per parasitoid larva feeding on C. molesta caterpillars, the mean weight of emerging female wasps was higher in the parasitoids reared on C. molesta. Furthermore, longevity of these female wasps was neither influenced by host species nor by the food their host had consumed. In addition we did not find a positive relationship between adult female weight and longevity. 5. Parasitoid females proved to be able to assess accurately the nutritional quality of an encountered host and adjust clutch size accordingly. These findings indicate that host size is not equal to host quality. Thus host size is not the only parameter to explain the nutritional quality of a given host and to predict fitness gain in the subsequent generation.     

Testing for host‐associated differentiation in two egg parasitoids of a forest herbivore

Several studies underline the importance of ecological barriers and differential selection in driving sympatric speciation. Host‐associated differentiation (HAD) has been proposed as one of the mechanisms leading to sympatric speciation. However, it is still unclear how common HAD is or which are the factors that could promote it. In particular, not much is known about HAD in predators and parasitoids of herbivorous insects. One of the characteristics postulated to pre‐dispose insects to HAD is parthenogenesis as it may favour adaptive responses to particular environments, amplifying selected gene complexes. In this study, we used amplified fragment length polymorphism (AFLP) markers to determine whether HAD is present in two parthenogenetic egg parasitoids attacking the same herbivore species – the pine processionary moth, Thaumetopoea pityocampa (Denis & Schiffermüller) (Lepidoptera: Notodontidae) – on two host Pinus species. A total of 100 loci for 59 individuals sampled in four populations of Baryscapus servadeii (Domenichini) (Hymenoptera: Eulophidae), a specialist parasitoid, and 106 loci for 117 individuals sampled in six populations of Ooencyrtus pityocampae Mercet (Hymenoptera: Encyrtidae), a generalist parasitoid, were analysed. Levels of genetic differentiation were also assessed with an outlier analysis, checking for alleles associated to host plants. No evidence of HAD was detected in any of the two parasitoid species. We hypothesize that both the lack of strict parthenogenetic reproduction and the ectophagous nature of the insect host could explain the absence of HAD. The genetic variation observed in the generalist parasitoid responded to a pattern of local adaptation, whereas no relationship with either host or geography was found in the specialist parasitoid.     

Geographic and between-generation variation in the parasitoid communities associated with an invading gallwasp,Andricus quercuscalicis (Hymenoptera: Cynipidae)

The knopper gallwasp Andricus quercuscalicis Burgsdorf 1783 (Hymenoptera: Cynipidae) has invaded western and northern Europe from southern and eastern Europe over the last 400 years. A. quercuscalicis has two alternating generations, which differ in phenology, structure, and host oak species. This study describes geographic variation in the community in the tiny catkin galls of the sexual generation on Turkey oak, Quercus cerris, and compares the patterns obtained with those in the community attacking the alternate agamic generation. As predicted from considerations of parasitoid recruitment to the communities of invading phytophagous insects (Cornell and Hawkins 1993), in its native range the sexual generation shows (1) higher parasitoid community species richness, (2) higher total mortality due to parasitoid attack and (3) a higher ratio of specialist to generalist parasitoid species than is evident in the invaded range. Counter to predictions, there is no indication that parasitoid community richness in the invaded range has increased with time since the arrival of the new host. Higher host mortality in the native range is due principally to a single specialist, Aulogymnus obscuripes Mayr 1877 (Hymenoptera: Eulophidae), and is not distributed evenly among parasitoid species which attack the gall-former only in this area. This contrasts with the community in Britain, where three principal generalist parasitoids cause approximately equal mortalities. The agamic gall contains a taxonomically and structurally diverse guild of parasitoid and inquiline species, associated with the changing resource provided by a large, long-lived, complex gall. In contrast, the sexual community includes a taxonomically and structurally narrow guild, associated with a resource which is structurally simple, small in size and short-lived. No parasitoid species attacks the gall-former in both generations. Surprisingly, in spite of these differences in the nature of the gall resource in the two generations, over their entire range (native and invaded) the parasitoid guilds of the two are equally species rich.     

Non-native gall-inducing insects on forest trees: a global review

Gall-inducing insects cause the development of specialised plant tissues (galls) that provide them with nutrition and some measure of protection from physical and biotic stresses. Their interaction with the plant is the most intimate metabolically of any herbivore group and is often associated with high host specificity. We survey the gall inducers that have become invasive pests of forest trees, most of which belong to just four insect families in three orders: Hemiptera (Adelgidae), Diptera (Cecidomyiidae) and Hymenoptera (Cynipidae and Eulophidae). Most are associated with introduction of plants on which they are specialists, but some have also shifted from introduced to native plant hosts. No formal comparative analysis of traits associated with success of establishment and subsequent range expansion has yet been made, and it is often hard to identify why one species has become a major range-expanding pest, while closely related and biologically very similar species have not. We provide an overview of biological traits likely to facilitate gall inducer range expansion, and highlight the importance of natural enemies in community impacts and biological control. Increasing global trade is likely to result in further range expansions by economically damaging species. The effects of climate change on the direction, frequency, and impact of gall inducer range expansions are likely to be complex and probably species-specific.     

Perspectives for the biological control of Cameraria ohridella

The horse chestnut leaf-miner, Cameraria ohridella Deschka et Dimic (Lepidoptera, Gracillariidae) is a serious invasive pest of Aesculus hippocastanum in Europe. The larvae of this species feed on leaf parenchyma and can reduce the tree growth. We studied the impact of parasitoids on C. ohridella in the Czech Republic and also searched for entomopathogenic fungi associated with this pest. The results showed that the rate of parasitism varied between 5% and 15% in most cases. The most parasitized stages of C. ohridella were spinning stages and especially pupae. The most abundant parasitoid species were Minotetrastichus frontalis, Pnigalio sp. and Pediobius saulius (Hymenoptera, Eulophidae). All species are polyphagous. Using the Galleria-bait method we isolated many strains of entomopathogenic fungi. Dominant species were Paecilomyces fumosoroseus, Paecilomyces farinosus and Beauveria bassiana. The perspectives of fungal bioagents in control of C. ohridella is discussed.     

The discovery of a new species of Ceranisus from southwestern Turkey

An explorative trip was made to southwesternTurkey in April 1995 in search of pear thrips,Taeniothrips inconsequens (Uzel)(Thysanoptera: Thripidae), and its naturalenemies. Forty-three females and 13 males of apreviously undescribed species of the genusCeranisus Walker (Hymenoptera:Eulophidae) were found, mainly in floweringArbutus andrachne L. Although theparasitoid was found in association withseveral thrips species, but especially T.inconsequens adults and larvae, its host orhosts were not determined. The parasitoid isdescribed and given the name Ceranisusantalyacus S. Triapitsyn.