Morphology and ultrastructure of sense organs on the ovipositor of Trybliographa rapae,a parasitoid of the cabbage root fly

The ovipositor of the parasitoid wasp Trybliographa rapae was examined by scanning and transmission electron microscopy. Characteristic peg-like sensilla with a cuticular ring at the base are found at the tip of the ventral valves, where they occur in a characteristic arrangement of triplets. The unusual basal structure probably protects the sensilla against damage during movement through the substrate and piercing of the host cuticle. These sensilla are each innervated by six dendrites, some of which have lamellated tips, generally considered to be characteristic of thermosensitivity. It is suggested that the remaining dendrites are gustatory, and as such probably respond to factors present in host haemolymph. A second type of peg-like sensillum is found on both the dorsal and the ventral valves. These are set in deep pits so that only the tip of the peg protrudes above the surface of the cuticle. These occur along the length of the ovipositor shaft and ultrastructural studies reveal the pegs to be innervated by a single mechanosensitive dendrite, probably monitoring the movement of the ovipositor through the substrate.     

Structure of female genitalia of glassy-winged sharpshooter, Homalodisca coagulata (Say) (Hemiptera: Cicadellidae)

The functional reproductive morphology of the female glassy-winged sharpshooter, Homalodisca coagulata (Say), is described at both light microscopy and scanning electron microscopy levels. The female has nine abdominal segments; the seventh to the ninth abdominal segments are modified for reproduction; the eighth tergite is reduced to two segments, with the ovipositor partially exposed from the modified ninth segment-the pygofer. The pygofer, covered with trichoid and coeloconic sensilla, almost completely encloses the ovipositor, which consists of three pairs of valvulae and two pairs of valvifers. The first and second valvulae function together for oviposition. The first valvulae are located exterior to the second valvulae, both of which bear many trichoid, campaniform, and coeloconic sensilla. The third valvulae, possessing many coeloconic sensilla, envelope the first and second valvulae. Seven major muscles are found to be associated with the ovipositor and the pygofer. The oviposition process is described with respect to the activity of the valvulae and their associated musculature. The female morphology follows the general pattern of cicadellids as a group.     

Host handling and specificity of the hyperparasitoid wasp, Dendrocerus carpenteri (Curtis) (Hym., Megaspilidae): importance of host age and species

The oviposition behaviour of Dendrocerus carpenteri (Curtis), an ectophagous hyperparasitoid of aphidiine wasps inside mummified aphids was examined. Hyperparasitoids were provided in the laboratory with pea aphids ( Acyrthosiphon pisum ) which had been parasitized by three different species of aphidiine wasps ( Aphidius ervi, Ephedrus californicus and Praon pequodorum ) ranging in physiological age from the late larval stage to the late pupal stage. Females accepted only the hosts inside mummified aphids; they ignored live aphids, and did not accept dead, but not yet mummified aphids, although the latter were sometimes probed with the ovipositor. Female behaviour in handling A. ervi or E. californicus mummies did not change with experience; handling and oviposition times were stereotypic. However, naive females needed experience to locate the cocoon of P. pequodorum and distinguish it from the empty aphid mummy. Host acceptance and specificity were influenced more by the developmental stage than the species of the primary parasitoid. In dichotomous choice tests, hyperparasitoids 'preferred' prepupae over younger pupae of A. ervi , but they did not distinguish between these stages of E. californicus; older pupae were accepted at a low rate. Host preference was not influenced by conditioning on the rearing host. We consider several constraints on the host range of D. carpenteri , and discuss alternative explanations of differential hyperparasitism in the field.     

Host specialization in habitat specialists and generalists

Generalists and specialists use different cues to find their habitat and essential resources. While generalists have the advantage of exploiting a wider range of resources, they are predicted to be less efficient in using one particular resource compared to specialists. The level of specialization of parasitoids can be either at the habitat or at the host level; strategies used by either type are expected to differ. We examined interactions between three aphid parasitoid species that are a habitat specialist Aphidius rhopalosiphi, a habitat generalist Aphidius ervi, and a host generalist Praon volucre on three cereal aphids, Sitobion avenae, Metopolophium dirhodum and Rhopalosiphum padi. We compared total parasitism rate across behavioral and physiological variation in a non-choice test. Next, we addressed total parasitism in two phases to examine: (1) the response of parasitoids to different hosts through the behavioral sequence from antennation through oviposition, and (2) the physiological suitability of different hosts for oviposition and larval development. Parasitization typically involved the following behavioral steps: (1) antennal contact, (2) abdominal bending, and (3) ovipositor insertion (acceptance). A. rhopalosiphi had the same number of antennal contacts with the three aphids but showed fewer instances of abdominal bending towards R. padi. Pre-contact host preference was found for A. ervi but it did not correspond to the level of acceptance. The number of antennal contacts by P. volucre corresponded to the parasitization level of the aphid species but more mummies were produced on M. dirhodum than on R. padi. These results suggest that parasitoid species that are habitat specialists react similarly to the different host species present in the same habitat, whereas generalist species exhibit clear preferences during host selection. Preferences were, however, not always related to host suitability.     

Oviposition behaviour and the sensilla of the ovipositor of Chilo partellus and Spodoptera littoralis (Lepidoptera: Noctuidae).

Observations of oviposition behaviour by Chilo partellus revealed that antennae, ovipositor tip and possibly tarsi were all involved in the choice of oviposition site. Among a very large number of typical mechanoreceptor hairs on the tip of the ovipositor valves, two pairs of stouter, blunt-tipped hairs were discovered. These hairs alone took up silver nitrate stain and transmission electron microscope sections revealed that the hair shaft had a hollow lumen within which ran a group of four or five dendrites. It is concluded that these sensilla are contact chemoreceptors and they are positioned in such a way that, with the placing of each egg, they would contact the oviposition substrate. Similar hairs were found on the ovipositor of Spodoptera littoralis . It is suggested that the hairs may prevent oviposition on surfaces directly chemically harmful to the eggs.     

Foraging behaviour and sequential multisensory orientation in the aphid parasitoid, Pauesia picta (Hym., Aphidiidae) at different spatial scales

Abstract: Foraging females of Pauesia picta, a parasitoid of the conifer aphid Cinara pinea on pine, used a variety of host plant or host-borne cues to find and recognize its aphid hosts. For long-range detection, females rely mainly on secondary plant compounds to locate potential host plants. In the medium-range (i.e. on a given host plant), females detected the presence of hosts by encounters with honeydew-collecting workers of the ant Formica polyctena and by perceiving host-borne cues. For short-range detection, after the discovery of an aphid colony, P. picta females recognize hosts visually. Subsequent antennal tapping, a tactile stimulus, prevents dispersal of aphids and increases the oviposition success of the parasitoid. The final host acceptance is obviously triggered by signals located in the epicuticle of the host. The results demonstrate the importance of sequential multisensory foraging that correspond to a diminishing distance between the parasitoid and the host.     

两种小菜蛾寄生蜂产卵器感器的形态和超微结构

半闭弯尾姬蜂和菜蛾盘绒茧蜂是两种重要的小菜蛾寄生蜂.采用扫描电镜对该两种寄生蜂雌蜂产卵器上的感受器的形态和超微结构进行了观察和研究,结果显示半闭弯尾姬蜂和菜蛾盘绒茧蜂的产卵器形态结构基本相同,都是由两个独立的腹产卵瓣和两个愈合在一起的背产卵瓣包围形成产卵道,与其它种类的寄生蜂相似.借背产卵瓣上的脊与腹产卵瓣的沟连锁在一起,腹产卵瓣可以沿背产卵瓣上的脊前后相对滑动.在半闭弯尾姬蜂产卵器上观察到1种钟形感器、2种腔锥感器、浅凹状感器和分泌毛孔.在菜蛾盘绒茧蜂产卵器上同样观察到了这几种感器,但菜蛾盘绒茧蜂产卵器端部的钟形感器突起较狭长,顶部开有气孔.此外菜蛾盘绒茧蜂产卵器上还存在第3种腔锥感器,其中央突起较低而长,表面有网孔.对各种感受器的形态和分布进行了描述,并对其功能进行了探讨,认为半闭弯尾姬蜂的产卵器较细长,且刺突部位有6个倒钩状突起,背、腹产卵瓣上分布更多的感受器,显示出更强的寄主搜寻定位和产卵寄生能力.     

An 'artificial aphid' for Aphidius ervi (Hym., Braconidae)

Abstract:  An artificial aphid was developed by making parafilm^® bubbles filled with aphid haemolymph and its suitability for parasitoid oviposition was tested. Aphidius ervi accepted the parafilm^® aphid and laid eggs on it. By stretching, the thickness of the parafilm could be changed. The thicker the parafilm, the higher was the mean number of ovipositional stings and the lower the mean number of eggs released by A. ervi .     

Nature's Swiss Army knives: ovipositor structure mirrors ecology in a multitrophic fig wasp community

Background

Resource partitioning is facilitated by adaptations along niche dimensions that range from morphology to behaviour. The exploitation of hidden resources may require specially adapted morphological or sensory tools for resource location and utilisation. Differences in tool diversity and complexity can determine not only how many species can utilize these hidden resources but also how they do so.

Methodology and Principal Findings

The sclerotisation, gross morphology and ultrastructure of the ovipositors of a seven-member community of parasitic wasps comprising of gallers and parasitoids developing within the globular syconia (closed inflorescences) of Ficus racemosa (Moraceae) was investigated. These wasps also differ in their parasitism mode (external versus internal oviposition) and their timing of oviposition into the expanding syconium during its development. The number and diversity of sensilla, as well as ovipositor teeth, increased from internally ovipositing to externally ovipositing species and from gallers to parasitoids. The extent of sclerotisation of the ovipositor tip matched the force required to penetrate the syconium at the time of oviposition of each species. The internally ovipositing pollinator had only one type of sensillum and a single notch on the ovipositor tip. Externally ovipositing species had multiple sensilla types and teeth on their ovipositors. Chemosensilla were most concentrated at ovipositor tips while mechanoreceptors were more widely distributed, facilitating the precise location of hidden hosts in these wasps which lack larval host-seeking behaviour. Ovipositor traits of one parasitoid differed from those of its syntopic galler congeners and clustered with those of parasitoids within a different wasp subfamily. Thus ovipositor tools can show lability based on adaptive necessity, and are not constrained by phylogeny.

Conclusions/Significance

Ovipositor structure mirrored the increasingly complex trophic ecology and requirements for host accessibility in this parasite community. Ovipositor structure could be a useful surrogate for predicting the biology of parasites in other communities.     

Neuroanatomical and electrophysiological studies of identified contact chemoreceptors on the ventral ovipositor valve of 3rd instar larvae of lubber grasshoppers (Taeniopoda eques)

A large number of contact chemoreceptors are located on the ovipositor valves of adult female grasshoppers. These receptors play an important role in many aspects of grasshopper life such as detecting the chemical composition of the soil before and during oviposition. It is surprising, however, to find these types of receptors on the ovipositor valves of instar larvae which are not able to oviposit. Thus, these receptors may serve functions other than to search for a suitable site for egg laying. Observation under the scanning electron microscope revealed the presence of uniporous basiconic contact chemoreceptors in addition to different types of trichoid mechanoreceptors on the ovipositor valve of lubber grasshopper 3rd instar larvae. Neuroanatomical studies have shown that these sensilla are multiply innervated, containing one mechanosensory neuron and four chemosensory neurons that project locally and intersegmentally. The tip recording technique from single basiconic sensilla demonstrated mechanosensory responses to deflections of the sensillum as well as gustatory activity when in contact with different chemical solutions. The electrophysiological studies have shown that these sensilla serve as contact chemoreceptors and not as olfactory receptors.     

The role of physical cues in the regulation of host recognition and acceptance behavior ofAphidius ervi Haliday (Hymenoptera: Braconidae)

The role of color and shape in the host recognition and acceptance behavior ofAphidius ervi Haliday was studied. A quantitative analysis of the oviposition behavior ofA. ervi was carried out with a computer-aided analysis of 150 video-recorded oviposition sequences on its natural host,Acyrthosiphon pisum (Harris). The importance of visual stimuli was assessed in a choice condition bioassay, observing the behavioral reaction of female parasitoids to various test materials flame-sealed into glass capillaries. Glass beads 2 and 6 mm in diameter and a flat arena were coated with cornicle secretion ofA. pisum, and their acceptance rates by both naive and experienced female parasitoids were assessed under no-choice conditions. In most cases,A. ervi females switched from random searching to attack position when the host was within a range of 1 cm, suggesting that host recognition is regulated in part by cues acting before physical contact. The glass capillary bioassay indicated that visual cues are important factors in the host recognition and acceptance phases. Pea aphid color alone can elicit the oviposition response of naiveA. ervi females, and this response is enhanced when color is combined with aphid shape. The cornicle secretion ofA. pisum stimulated an oviposition response which was stronger in naive females ofA. ervi than in experienced ones and was not significantly affected by the glass bead size or flat surface. These results, along with those from previous studies, suggest that manipulation of the oviposition behavior ofA. ervi is feasible under laboratory conditions.     

The use of visual cues in host evaluation by aphidiid wasps I. Comparison between threeAphidius parasitoids of the pea aphid

Host evaluation behaviour was examined in three species of aphid parasitoids,Aphidius ervi haliday,A. pisivorus Smith, andA. smithi Sharma & Subba Rao (Hymenoptera: Aphidiidae). Parasitoids were provided under laboratory conditions with three kinds of hosts representing two aphid species: (green) pea aphid,Acyrthosiphon pisum (Harris), and green and pink colour morphs of the alfalfa aphid,Macrosiphum creelii Davis. Females of all threeAphidius species distinguished between aphids on the basis of colour, movement, and host species. Patterns of host acceptance by parasitoids were species-specific. InA. ervi, host preference was the same in light and dark conditions: pea aphid>green alfalfa aphid≫pink alfalfa aphid. In contrast,A. pisivorus attacked and accepted pea aphid and green alfalfa aphid equally in the light and preferred both of these over pink alfalfa aphid; however, it made no distinction between pea aphid and pink alfalfa aphid in the dark. Females ofA. smithi attacked all three kinds of hosts (pea aphid>green alfalfa aphid≫pink alfalfa aphid) but apparently laid eggs only in pea aphid. The frequencies of attack and oviposition by all wasps were higher on ‘normal’ pea aphids than on those anaesthetized with CO₂. Host recognition is confirmed by chemical cues in the aphid cuticle that are detected during antennation, and host acceptance is dependent on an assessment of host quality during ovipositor probing.     

Behavioural evidence for hygro- and mechanoreception by ovipositor sensilla of Dacus tryoni (Diptera: Tephritidae)

ABSTRACT. Gravid female Queensland fruit flies Dacus tryoni (Froggatt) readily oviposit when the ovipositor sensilla are stimulated either by a relatively thick (≥2 mm) surface layer, or by moisture under a relatively thin (<0.5 mm) or thick surface layer. A single layer of Parafilm over dry air elicits almost no oviposition; significantly more oviposition occurs when the underside of the Parafilm is coated with a 2 mm thick layer of petroleum jelly; even more oviposition occurs when the Parafilm is floated on liquid paraffin; greatest oviposition is elicited when moist media (agar gel, water or moist air) are presented under the Parafilm. Hollowed-out domes of apple skin elicit significant oviposition only when sealed basally, to give high internal concentrations of water vapour. The previously identified groove sensilla on the tephritid ovipositor are inferred as being a source of mechanical and chemical information used by the fly in such ovipositional decisions. The ovipositor also has two other types of tactile sensilla. The three types of ovipositor sensilla of tephritids are considered to play roles analogous to those of certain labial receptors of flies with piercing mouthparts.     

Functional analysis of a fatty acid binding protein produced by Aphidius ervi teratocytes

Aphidius ervi (Hymenoptera, Braconidae) is an endophagous parasitoid of various aphid species, including Acyrthosiphon pisum (Homoptera, Aphididae), the model host used in the present study. Parasitized hosts show a marked increase of their nutritional suitability for the developing parasitoid larvae. This alteration of the biochemical and metabolic profile is due to a castration process mediated by the combined action of the venom, injected at the oviposition, and of the teratocytes, cells deriving from the dissociation of the embryonic membrane. Teratocytes produce and release in the host haemocoel two parasitism-specific proteins, which are of crucial importance for the development of their sister larvae. One of the proteins is a fatty acid binding protein (Ae-FABP), which shows a high affinity for C14-C18 saturated fatty acids (FAs) and for oleic and arachidonic acids. To better define the possible nutritional role of this protein, we have studied its immunolocalization profile in vivo and the impact on FA uptake by the epidermal and midgut epithelia of A. ervi larvae. During the exponential growth of A. ervi larvae, Ae-FABP is distributed around discrete lipid particles, which are abundantly present in the haemocoel of parasitized host aphids and in the midgut lumen of parasitoid larvae. Moreover, a strong immunodetection signal is evident on the surface of the two larval epithelia involved in nutrient absorption: the parasitoid midgut epithelium and the external epidermal layer. These two epithelia can effectively absorb radiolabelled myristic acid, but the FA transport rates are not affected by the presence in the medium of Ae-FABP. The protein appears to act essentially as a vector in the host haemolymph, transferring FAs from the digestion sites of host lipids to the growing parasitoid larvae. These data indicate that the proteins produced by A. ervi teratocytes may play complementary roles in the nutritional exploitation of the host.     

The mechanoreceptors on the endophytic ovipositor of the dragonfly Aeshna cyanea (Odonata,Aeshnidae)

This study investigates the mechanoreceptors located on the cutting valvulae of the ovipositor of the dragonfly Aeshna cyanea (Aeshnidae), using both SEM and TEM, with the aim of providing an overview of the sensory equipment of an odonatan endophytic ovipositor. Four kinds of sensilla have been described. Notwithstanding their different external and internal morphology, they show features typical of mechanoreceptors. Three of them are evident along the external surface of the two cutting valvulae in the form of sub-spherical pegs, pit organs type 1 (holes) and pit organs type 2 (depressions), these last are similar to amphinematic scolopidia, while the fourth type is represented by subintegumental mononematic scolopidia having no direct relationship with the cuticle. In spite of their structural differences, the morphology of the described mechanoreceptors is consistent with performing a main role in allowing the perception of compression/stretching of the thick cuticle of the valvulae and their bending due to the pressure acting on the distal end of the ovipositor during substrate penetration. Such an organization is coherent with the need of endophytic Odonata to be able to evaluate the stiffness of the plant where to lay eggs.     

Host location and oviposition in a basal group of parasitic wasps: the subgenual organ, ovipositor apparatus and associated structures in the Orussidae (Hymenoptera, Insecta)

Anatomical studies and behavioural observations indicate that representatives of the Orussidae use vibrational sounding to detect suitable oviposition sites. During host location, vibrations generated by tapping the tips of the antennae against the wood are picked up by the fore legs through the basitarsal spurs, transmitted along the basitarsi to thin-walled areas on the tibiae and through haemolymph to the subgenual organs, where they are transduced into nerve impulses. The apical antennomeres are distinctly shaped and have the cuticle thickened distally. The fore basitarsi have weakly sclerotised basitarsal lines proximally and membranous basitarsal spurs distally. The external wall of the fore tibiae have thin-walled areas distally on their posterior parts. Internally, large subgenual organs are situated opposite the thin-walled areas and each organ consists of 300–400 scolopidial units suspended between a lateral cuticular spine, a ventral sheet and a median ridge. The ovipositor is several times the length of the body of the wasp. When at rest, it extends all the way into the prothorax, where it is coiled before extending posteriorly to lie between the third valvulae distally. The ovipositor lies in a membranous ovipositor sac attached posteriorly to the proximal parts of the ovipositor apparatus and the posterior margin of sternum 7. In the ovipositor apparatus, the anterior parts of the second valvifers are displaced and expanded anterodorsally, inverting the first valvifers and the base of the ovipositor. When in use, the ovipositor is extended and retracted by median apodemes situated on the anterior margins of abdominal sterna 3–7. Longitudinal muscles between the apodemes allow the latter to grip the ovipositor in troughs between them. The ovipositor extends from the abdomen at the tip of sternum 7, and an internal trough on sternum 7 serves to guide the ovipositor into the wood. Despite the alterations observed in the ovipositor apparatus in the Orussidae, the musculature is almost complete and the mode of operation presumably not much different from that of other representatives of the Hymenoptera. The different ways parasitic wasps with very long ovipositors handle and accommodate these and the implications for the evolutionary history of Hymenoptera are discussed. Accepted: 14 March 2001     

Quality of different aphids species as hosts for the parasitoid Aphidius ervi Haliday (Hymenoptera: Braconidae: Aphidiinae)

The suitability of Macrosiphum euphorbiae (Thomas), Aulacorthum solani (Kaltenbach) and Acyrthosiphon kondoi Shinji (Hemiptera: Aphididae) as hosts for the aphid parasitoid Aphidius ervi Haliday was evaluated by assessing host size, host preference, and host quality. Tests were carried out in an environmental chamber at 22±1oC, 70±10% RH and 12h photophase. Replicates (11) consisted of one 24h-old mated female of A. ervi without a previous oviposition experience. Female was released into a Petri dish (5 cm) with 20 2nd and 3rd instars of one of each aphid species tested on a leaf disc of the host plant onto a 1% water-agar layer. Parasitoid emergency was lower in A. kondoi (78.7%) compared to M. euphorbiae (92.2%) and A. solani (91.7%). Acyrthosiphon kondoi (0.36 mm) was the smallest host. The parasitoid showed preference (74.0% parasitism) for M. euphorbiae, the largest host (hind tibia length=0.73 mm), which in turn yielded larger A. ervi females (0.75 mm).     

Complex interactions between a plant pathogen and insect parasitoid via the shared vector-host: consequences for host plant infection

Plant viruses modify the development of their aphid vectors by inducing physiological changes in the shared host plant. The performance of hymenopterous parasitoids exploiting these aphids can also be modified by the presence of the plant pathogen. We used laboratory and glasshouse microcosms containing beans (Vicia faba) as the host plant to examine the interactions between a plant virus (pea enation mosaic virus; PEMV) and a hymenopterous parasitoid (Aphidius ervi) that share the aphid vector/host Acyrthosiphon pisum. Neither PEMV-infection of V. faba, nor the carriage of PEMV virions by A. pisum, affected the growth or morphology of the aphid, or the oviposition behaviour and development of A. ervi. The presence of developing Aphidius ervi larvae within Acyrthosiphon pisum did not affect the ability of the aphids to transmit PEMV. However, by reducing their longevity, parasitism ultimately decreased the time viruliferous aphids were able to inoculate plants. In terms of virus dispersal, parasitized aphids exhibited more movement around experimental arenas than unparasitized controls, causing a slight increase in the proportion of beans infected with PEMV. Exposure to adult Aphidius ervi caused Acyrthosiphon pisum to rapidly drop off bean plants and disperse to new hosts, resulting in considerably higher plant infection rates (70%) than that seen in control arenas (25%). The results of this investigation demonstrate that when parasitoids are added to a plant-pathogen-vector system, benefits to the host plant due to reduced herbivore infestation must be balanced against the consequences of parasitoid-induced aphid dispersal and a subsequent increase in the level of plant infection.     

Sensory receptors of the ovipositor ofTrichogramma maidis [Hym.:Trichogrammatidae]

Sensory receptors of the ovipositor ofTrichogramma maidis are described. Sense organs are found on the 2^nd valvifers (1 type), on the tip of the 3^rd valvulae (2 types) and on the 1^st valvulae (4 types). The nature and possible functions of these sensilla are discussed.      

Ovicide in the whitefly parasitoid, Encarsia formosa

The oviposition decisions made by insect parasitoids when encountering hosts of variable quality have been the subject of extensive theoretical and experimental investigation. For parasitoids that lay their eggs inside the host, the possible outcomes of encounters with parasitized hosts have been assumed to include only oviposition (superparasitism), rejection, or in some cases feeding on host haemolymph. We document another outcome in Encarsia formosa Gahan (Hymenoptera: Aphelinidae), a species that has been a model system for the study of oviposition behaviour. In E. formosa, females may kill eggs previously laid within the host by jabbing them with their ovipositor before ovipositing themselves. (1) Our observations indicated that jabbed eggs were indeed killed. (2) In experimental arenas in the laboratory, ovicide occurred in the majority of encounters with parasitized hosts and at highest frequency in encounters resulting in oviposition. (3) There was no significant difference in the handling time associated with oviposition+ovicide in parasitized hosts in comparison with oviposition alone, suggesting that there is no time cost to ovicide. (4) Ovicide did not appear to be incidental to normal probing within a host. Radial analysis of the direction of ovipositor movement with respect to the centre of the previously laid egg within the host showed that females engaged in ovicidal bouts probed most often in the direction of the egg. This is the first well-documented study of ovicide in an endoparasitoid. We suggest ovicide may be under-reported in other endoparasitoid species due to the difficulty of observing it. Copyright 2000 The Association for the Study of Animal Behaviour.