Idiobiont Ectoparasitoid Research Articles

Comparative morphology and biology of terminalinstar larvae of someEurytoma(Hymenoptera, Eurytomidae) species parasitoids of gall wasps (Hymenoptera, Cynipidae) in western Europe

Gómez J. F., Nieves-Aldrey J. L., Hernández Nieves M. & Stone G. N. 2011. — Comparative morphology and biology of terminal-instar larvae of some Eurytoma (Hymenoptera, Eurytomidae) species parasitoids of gall wasps (Hymenoptera, Cynipidae) in western Europe. Zoosystema 33 (3): 287-323.We present a taxonomic and biological study of the genus Eurytoma Illiger, 1807 (Hymenoptera, Eurytomidae), based on the morphology and biology of the terminal-instar larvae of 13 species living as parasitoids in the galls of European species of cynipid gall wasps. We provide the first detailed descriptions of the terminal-instar larvae of the studied species, illustrating diagnostic characters for the family and the studied genera with SEM pictures. We also provide a species key for the identification of Eurytoma larvae associated with cynipid galls, based on particular characters associated with the head, mouthparts and mandibles. Although we find only limited informative variation in body shape, the head and mandibles provide many characters of potential taxonomic and phylogenetic value. We summarise the larval biology of the 13 Eurytoma species inhabiting cynipid galls. Eurytoma larvae are usually solitary idiobiont ectoparasitoids of the host larva or of larvae of cynipid inquilines that also often feed on gall tissue.

Behavioral Response of Tamarixia radiata (Waterston) (Hymenoptera: Eulophidae) to Volatiles Emanating from Diaphorina citri Kuwayama (Hemiptera: Psyllidae) and Citrus

Tamarixia radiata Waterston (Hymenoptera: Eulophidae) is an effective idiobiont ectoparasitoid of the psyllid Diaphorina citri Kuwayama (Hemiptera: Psyllidae), vector of the huanglongbing (HLB). We examined the olfactory responses of T. radiata to volatiles emanating from D. citri or plant volatiles using a custom designed T-maze olfactometer and open arena bioassays. We also examined the behavioral response of male and female T. radiata to conspecifics of the opposite sex to determine whether olfactory signals mediate mate location. T. radiata adults exhibited a sexually dimorphic response to volatiles emanating from D. citri and citrus. Female T. radiata responded positively to the odors emanating from D. citri nymphs in both olfactometer and open arena bioassays. However, female wasps showed no response to odors emanating from D. citri adults, D. citri honey dew secretions, intact citrus or orange jasmine leaves. Odors emanating from D. citri damaged citrus were not attractive to T. radiata females but stimulated attraction of wasps to D. citri on damaged plants. T. radiata females were not attracted to D. citri immatures when they were presented as visual cues. Male T. radiata did not show attraction to D. citri nymphs or other putative odors that were attractive to female T. radiata. In olfactometer bioassays, more male T. radiata responded to the odor of female conspecifics than blank controls in the absence of associated citrus host plant volatiles. Odors emanating from female T. radiata were not attractive to male T. radiata. Male or female T. radiata were not attracted to the odors emanating from same sex conspecifics. Both male and female T. radiata adults showed positive phototactic behavior. Collectively, our results provide behavioral evidence that: 1) female T. radiata use volatiles emanating from D. citri nymphs to locate its host and: 2) female T. radiata release a volatile pheromone that attracts male conspecifics.

Developmental and Reproductive Biology of the Ectoparasitoid,Elasmus steffani, in a Substitute Host,Ephestia kuehniella

Elasmus steffani (Viggiani) (Hymenoptera: Elasmidae) is a gregarious idiobiont ectoparasitoid of Prays oleae (Bernard) (Lepidoptera: Plutellidae), an olive crop pest. In the substitute host Ephestia kuehniella (Zeller) (Lepidoptera: Pyralidae), the duration of the developmental stages was approximately 11–15 days. The preoviposition was 8.9 ± 5.0 days, and oviposition lasted 30.4 ± 10.5 days, with a reproduction capacity of 185.5 ± 62.3 eggs per female, for a mean of 5.4 ± 0.9 eggs per day. The oviposition rhythm reached its maximum when the parasitoid was 35 days of age. The lack of food negatively influenced survival of the adults, while those fed on a honey-water mixture lived significantly longer that those that also had access to a host as food. The female parasitoid fed upon 15% of the paralyzed larvae. The virgin female E. steffani exhibits arrhenotokic parthenogenesis.

The effects of parasitism by the ectoparasitoid Bracon hebetor Say (Hymenoptera: Braconidae) on host hemolymph proteins in the Mediterranean flour moth Ephestia kuehniella Zeller (Lepidoptera: Pyralidae)

Parasitism of lepidopteran larvae by braconid wasps has significant effects on host hemolymph proteins and the physiology of the host insect. In this study the post-parasitism effects of a gregarious idiobiont ectoparasitoid (Bracon hebetor) on hemolymph plasma proteins in the final instar larvae of the host (Ephestia kuehniella) were investigated. Hemolymph plasma proteins were analyzed using spectrophotometry and sodium dodecyl sulphate polyacrylamide gel electrophoresis (SDS-PAGE). Total quantity of plasma proteins in the host's hemolymph decreased slightly 24 and 48 h after parasitization; however, SDS-PAGE analysis showed that the quantity of 12 proteins decreased, whereas that of 5 proteins increased in concentration in the hemolymph of parasitized host larvae 24 and 48 h post-parasitism. Therefore, we conclude that host regulation of E. kuehniella by B. hebetor involves only quantitative changes in host plasma proteins and does not lead to upregulation of novel proteins.

Host-seeking behavior and parasitism by Spathius agrili Yang (Hymenoptera: Braconidae), a parasitoid of the emerald ash borer

Spathius agrili Yang (Hymenoptera: Braconidae) is a newly described and important idiobiont ectoparasitoid of the emerald ash borer (EAB) that has excellent potential as a biological control agent against EAB populations in the USA. In order to understand the ecological factors involved in the search and discovery of concealed hosts by S. agrili, we investigated the behavioral responses of adult female wasps to potential semiochemicals from host plants, hosts, and host frass as well as to vibration signals from host feeding and movement. Using a bioassay, we showed that S. agrili first finds the host’s habitats by detecting the volatile compounds emitted by ash. In the second phase of host location and acceptance, the parasitoids detect the mechanical vibrations produced by host feeding and movement under the surface of the bark and then probe to find the EAB larvae. Contact chemicals seem to play little or no role in short-range host finding. Female wasps avoided laying eggs on EAB larvae already parasitized and thus paralyzed. We hypothesized that female wasps were not attracted to these larvae due to their lack of feeding or movement. While an induced paralysis in the host is instrumental in avoiding superparasitism, we cannot rule out that S. agrili females also use an oviposition pheromone to deter conspecific females. Together, these results suggest that vibration and olfactory cues play significant roles in distinct phases of S. agrili host habitat and host location behaviors.

Antennal Sensilla ofTamarixia radiata(Hymenoptera: Eulophidae), a Parasitoid ofDiaphorina citri(Hemiptera: Psyllidae)

AbstractTamarixia radiata (Waterston) (Hymenoptera: Eulophidae) is an effective idiobiont ectoparasitoid of the psyllid Diaphorina citri Kuwayama (Hemiptera: Psyllidae), vector of the huanglongbing (citrus greening disease) pathogen. We examined the external and functional morphology of the antennal sensilla of adult male and female T. radiata by using scanning and transmission electron microscopy, respectively, to gain insights into the behavioral ecology of this parasitoid. The geniculate antennae of male and female T. radiata were composed of a long scapula-shaped scape with a basal radicula, a barrel-shaped pedicel, and a long flagellum with a basal ring-like annulus. Five morphologically distinct sensilla, including two types of aporous trichoid sensilla (AST-1 and AST-2), one multiporous trichoid sensillum (MST), one multiporous placoid sensillum (MPS), and one aporous basiconic capitate peg sensillum were identified on the antennae of both sexes. The antennal structures of T. radiata were sexually dimorphic. Male antennae consisted of four funicular flagellomeres and possessed a greater number of olfactory MST than female antennae, suggesting their possible function in perception of mate-related volatile cues. Female antennae were characterized by three funicular flagellomeres and a greater number of MPS than male antennae, suggesting their possible function in the perception of host-related volatile cues. The results are discussed in relation to plausible roles of the identified sensilla in mate and host location by this important parasitoid species.

Effects of host size on the sex ratio, clutch size, and size of adult Spathius agrili, an ectoparasitoid of emerald ash borer

The idiobiont ectoparasitoid, Spathius agrili Yang (Hymenoptera: Braconidae), parasitizes the concealed larvae of the emerald ash borer (EAB), Agrilus planipennis Fairmaire (Coleoptera: Buprestidae), which feed on the inner bark of ash trees ( Fraxinus spp.). The objectives of this study were to investigate the effects of host larval size on parasitoid clutch size, offspring sex allocation, and adult body length. Results showed that the number of parasitoid eggs per host was positively correlated with host size as measured by larval weight, pronotum width, body length, and body width. The percentage of emerging parasitoids that were female was greater when eggs were laid on large larvae. More parasitoid progeny successfully developed on large host larvae, and parasitoid progeny survival was slightly higher than on small host larvae. Survival of parasitoid progeny was positively related to the width of the host gallery. There were significant differences among the body lengths of adult parasitoid offspring that developed on different sizes of host larvae, especially for female wasps. Furthermore, females were typically longer than males developing on the same host.

A single origin of gall association in a group of parasitic wasps with disparate morphologies

The braconid wasp subfamily Doryctinae mainly comprises idiobiont ectoparasitoids of other insect larvae. In recent years, however, members of a few genera have been discovered to be associated with galls from various unrelated host plant families, with some of these being gall inducers whereas others are suspected as being predators of gallers. Because of their considerable morphological differences, these gall-associated taxa traditionally have been placed in separate tribes or even in other subfamilies. In this study, we investigate the phylogenetic relationships among representatives of a number of different doryctine genera, including five of its seven gall-associated genera using two genetic markers. Here we analyzed the length-variable 28S sequence data based on secondary structure both excising the unalignable regions and recoding them according to indel length. In addition, multiple alignments were carried out with a range of gap-opening and extension parameters. The combined (28S + CO1) phylogenetic hypotheses obtained, both excluding and recoding the unalignable regions, recover a clade comprising the five gall-associated genera, and most of the analyses using multiple alignments also support this relationship. These results support a scenario in which secondary phytophagy evolves from initially attacking primary gall-forming hosts. The relationships recovered are also more congruent with a model that explains the macroevolution of insect plant association in the Doryctinae as reflecting geographic proximity rather than host plant relationships. Further, our phylogenetic hypotheses consistently show that one of the main morphological features employed in the higher level classification of the Doryctinae is actually highly homoplastic.

Megalyra baltica Poinar and Shaw n. sp. (Hymenoptera: Megalyridae), a long-tailed wasp from Baltic amber

The wasp family Megalyridae includes eight living genera of presumed idiobiont ectoparasitoids, most of which are associated with relict primary tropical forests (Shaw 1990b, 2006). Their biology is poorly known except for a few species. Their behavior and host range appear to be diverse since one Australian species, Megalyra fasciipennis Westwood, parasitizes cerambycid beetle larvae in wood, while the much smaller Australian M. troglodytes Naumann parasitizes sphecid wasp larvae in mud nests on vertical rock faces (Shaw 1990a). The long ovipositor of many Megalyra species, as well as the phylogenetic analysis of Shaw (1990b), suggests that parasitism of immature wood-boring beetles is the ancestral and more generalized behavior for the genus. It is presumed that ancient megalyrids, like many of their modern descendants, would have been attracted to dead and dying beetle-infested trees, where they might become trapped in sap flows, and eventually fossilized as amber inclusions.

A new species of Bracon (Hymenoptera: Braconidae) parasitic on alien sweetpotato weevils in the south‐west islands of Japan

AbstractA new species of braconid, Bracon yasudai Maeto et Uesato sp. nov., is described here from the south‐west islands of Japan. It is a solitary idiobiont ectoparasitoid of the larvae of the West Indian sweetpotato weevil, Euscepes postfasciatus (Curculionidae), and the sweetpotato weevil, Cylas formicarius (Brentidae), both feeding on Ipomoea batatas (L.) (Convolvulaceae). The percentage parasitism of the braconid on E. postfasciatus in the vines of I. batatas was 19.9–40.7% in the field. Bracon cylasovorus (Rohwer) reared from C. formicarius in the Philippines is also described.

Taxonomic notes on Old World Stephanidae (Hymenoptera): description of Parastephanellus matsumotoi sp. n. from Japan, redescription of Commatopus xanthocephalus (Cameron) and keys to the genera Profoenatopus van Achterberg and Megischus Brullé

mopolitan family, members of which occur mainly in subtropical and tropical forests. The species are usually medium-sized to large: length of the fore wing ranging from 2 to 20 mm, the length of the body of the largest species reach (including ovipositor) up to 75 mm (in the genera Megischus Brulle, 1846, and Profoenatopus van Achterberg, 2002). Up to now 325 extant species are known, including the species in this paper (Aguiar 2004, Achterberg & Yang 2004). Stephanids are conspicuous in having a ‘crown’ or ‘corona’ on the head (figs. 6, 15), the pronotum being more or less modified (figs. 2, 4, 12, 13), the propodeal spiracle slit-like and situated subapically next to the condylus of the first tergite, and the hind femur and tibia modified (figs. 7, 8). Nearly all species known from forested habitats are black or dark brown, frequently with some parts (especially of head and legs) yellowish-, orangeor reddish-brown. Small parts of the body may be ivory and often the ovipositor sheath has a silvery white or ivory subapical band. The scanty biological information indicates that Stephanidae are idiobiont ectoparasitoids of wood boring larvae (van Achterberg 2002). Stephanids are often found around tree trunks or branches of trees that are dead for about one year, inhabited by beetle larvae and not yet heavily infested by fungi. Stephanidae are nearly always reported as parasitoids

First Recorded Parasitoid from China of <I>Agrilus planipennis</I>: A New Species of <I>Spathius</I> (Hymenoptera: Braconidae: Doryctinae)

Abstract The first reported parasitoid reared from Agrilus planipennis Fairmaire, Spathius agrili n. sp., is described from China. S. agrili was reared from A. planipennis in China attacking a Fraxinus species native to North America, Fraxinus velutina Torr., and one endemic to the region, Fraxinus mandshurica Rupr. Life history observations of S. agrili in the field and laboratory indicate it is a gregarious idiobiont ectoparasitoid and has up to four generations per year. Parasitism rates in the field ranged from 30 to 90%, with one to 35 S. agrili eggs associated with a single host. From a host larva 1–18 adult wasps (average of 8.4) were reared. Based on laboratory rearings, the emerging adult female to male ratio is 3:1.

Food Resource Use of Hyperparasitoid <I>Trichomalopsis apanteloctena</I> (Hymenoptera: Pteromalidae), an Idiobiotic Ectoparasitoid

The hyperparasitoid Trichomalopsis apanteloctena (Crawford) is an idiobiont ectoparasitoid that uses the prepupa or pupa of the primary parasitoid Cotesia kariyai (Watanabe), which is paralyzed by venom at parasitization. Changes in nutrient quality of the primary parasitoid were evaluated during its development. The primary parasitoid C. kariyai was available as a host for 5 d, because C. kariyai eclosed at 5 d after emergence. The lipid contents of the primary parasitoid decreased during these 5 d. The size of individual T. apanteloctena progeny paralleled the available nutritional resources of these primary parasitoids. A decrease in body mass, that is, the change in the quality of the fat body in the primary parasitoid development affected the adult size and sex ratio of the hyperparasitoid. The hyperparasitoid had no preference of developmental stage of the primary parasitoid. However, adult sizes of the individual progeny that parasitized at 4 d after pupation were smaller and the sex ratio was male biased.

Distinguishing adults ofBracon cephi and Bracon lissogaster(Hymenoptera: Braconidae), parasitoids of the wheat stem sawfly (Hymenoptera: Cephidae)

The wheat stem sawfly,Cephus cinctusNorton (Hymenoptera: Cephidae), has been the most economically important insect pest of wheat in the northern Great Plains since cultivation began (Weiss and Morrill 1992). The wheat stem sawfly was first reported from wild grasses where populations were often highly parasitized by a number of parasitoids, includingBracon (= Microbracon) cephi(Gahan) (Hymenoptera: Braconidae) (Criddle 1923; Ainslie 1929). A similar species,Bracon lissogasterMuesebeck, was later reported to also attackC. cinctuslarvae (Muesebeck 1953; Somsen and Luginbill 1956). These parasitoids are now prevalent in wheat in some regions of Montana (Morrillet al.1994, 1998; Morrill 1997). The life histories and phenologies of these sympatric idiobiont ectoparasitoids are similar. The ability to distinguishB. cephifromB. lissogasteris essential in elucidating their effects on populations ofC. cinctus. We examined 159 females and 123 males ofB. cephifrom Chouteau, Hill, Stillwater, Teton, and Toole counties in Montana; Burke, Burleigh, Rolette, and Williams counties in North Dakota; Rock County in Minnesota; and southem Alberta (Rockyford and Consort). The 254 females and 215 males ofB. lissogasterexamined were from Chouteau, Hill, Teton, and Toole counties in Montana. Holotypes were compared to verify identifications.

Influence of host size on oviposition behaviour and fitness of Elachertus cacoeciae attacking a low‐density population of spruce budworm Choristoneura fumiferana larvae

Summary1. Oviposition behaviour and host size − fitness relationships of a gregarious, idiobiont ectoparasitoid, Elachertus cacoeciae (Howard) (Hymenoptera: Eulophidae), were studied by implanting one fourth‐, fifth‐, and sixth‐instar spruce budworm Choristoneura fumiferana (Clemens) (Lepidoptera: Tortricidae) larva per tree in a stand where the density of the wild C. fumiferana population was low.2. Development time of E. cacoeciae larvae was quickest on fifth‐instar C. fumiferana larvae, which were the preferred hosts for oviposition.3. Brood sex ratio (proportion of females) was related positively to increasing C. fumiferana instar, indicating that more females were laid on larger hosts.4. Parasitoid offspring size increased with increasing C. fumiferana instar and decreased with increasing brood size on smaller hosts. Female but not male size was related positively to increasing brood sex ratio (proportion of females).5. Under laboratory conditions, parasitoid longevity was related positively to parasitoid size and realised lifetime fecundity, and clutch size was related positively to host size.6. These results suggest that selection of intermediate‐sized C. fumiferana larvae may be adaptive for E. cacoeciae.

The developmental strategy of an idiobiont ectoparasitoid, Dendrocerus carpenteri : influence of variations in host quality on offspring growth and fitness.

Dendrocerus carpenteri (Curtis) (Hymenoptera: Megaspilidae) is a solitary hyperparasitoid, which attacks prepupal and pupal stages of hymenopteran parasitoids inside mummified aphids. The larva feeds externally on the host, which is envenomed by the female at oviposition. To evaluate the influence of variations in host quality on the growth, development and fitness of D. carpenteri, we varied the size and developmental stage of the primary parasitoid host (Aphidius ervi Haliday), which was reared on different instars of pea aphid [Acyrthosiphon pisum (Harris)] and English grain aphid [Sitobion avenae (F.)]. Within each kind of host, females eclosed from the relatively larger mummies, while males eclosed from the smaller mummies. Host size and hyperparasitoid size were correlated, and females were larger than males. In hyperparasitoids developing on prepupal and pupal hosts, development time from oviposition to adult eclosion was proportional to size; females required more time for development than males. The mean relative growth rate was the same in males and females and increased with host quality, as predicted by the growth model of Mackauer and Sequeira (1993) for idiobiont parasitoids. Larvae developing on late-pupal stages and pharate adults of A. ervi were unable to consume sclerotized host tissues; they were smaller and needed more time for development. The average number of mature eggs at eclosion was six, except in females developing on suboptimal hosts, which contained only one egg or none. Egg volume was correlated with female size, possibly reflecting differences in larval ontogeny. We provide equations describing the relationship between host quality as indexed by hind-tibia length of the mummified aphid and adult body size in terms of dry mass, development time and mean relative growth rate of D. carpenteri. We discuss the usefulness of host size as a proxy of host quality for idiobiont parasitoids, and provide examples of exceptions.

Structural refuges in two stem‐boring weevils onRumex crispus

Abstract.Differences in feeding positions, parasitoid complexes and parasitization rates of the two dominant insect species in stems ofRumex crispuswere investigated.Apion miniatum(inhabiting the lower 10% of the stem) andApion violaceum(occurring all along the stem) exploited distinctly different feeding positions, partly due to differences in time of oviposition.A.miniatumsuffered less parasitization thanA.violaceum, measured both by number of parasitoid species and parasitization rates. Its feeding position constitutes a refuge.Parasitization ofA.violaceumwas least in individuals feeding in basal, thick parts of the stem. There is a trend that the developed refuge increases with increasing stem diameter.The refuge ofA.violaceumin basal positions only affected idiobiont ectoparasitoids, because koinobiont endoparasitoids attack the weevils before they enter the stem. Moreover, the koinobiont did benefit from the refuge itself by avoiding hyperparasitism.Densities ofA.violaceumincreased with plant size, whereas percentage parasitism did not differ. Its three most abundant parasitoid species showed small‐scale density‐independent patterns of attack over all plants. Therefore a constant proportion of weevil larvae mine within the refuge independent of its potential size.Synchronization between weevils and plants, as well as between parasitoids and hosts, appears to be the dominant factor for the spatial community structure of the stem borersof Rumex crispusand their enemies.

Evolutionary patterns of host utilization by ichneumonoid parasitoids (Hymenoptera: Ichneumonidae and Braconidae)*

The four major biological strategies of ichneumonoid parasitoids, koinobiont and idiobiont, ecto-and endoparasitism, are discussed and the evolutionary radiations of the two families Ichneumonidae and Braconidae compared in an attempt to relate differences in patterns of host utilization to differences in evolutionary history. The most primitive members of both families are idiobiont ectoparasitoids of hosts concealed in plant tissue. Idiobiont ectoparasitic braconids are all still primarily associated with such hosts, but idiobiont ectoparasitic ichneumonids have radiated to attack hosts in other situations, such as in aculeate nests or in cocoons. A shift in emphasis between the behavioural steps, host habitat location and host location, is envisaged as being important in such evolutionary change. Idiobiont endoparasitism is postulated as having arisen amongst ectoparasitoids attacking cocooned hosts, as an adaptation that allows them to exploit pupae and puparia in relatively exposed positions; it is a fairly common strategy in the Ichneumonidae, but virtually unknown in the Braconidae. Koinobiosis is perceived as having evolved in association with hosts which feed in a relatively weakly concealed position, but pupate in a more secluded and safe location. The strategy is advantageous as it allows a parasitoid to oviposit on an easily discoverable host, but to use the host's pupation concealment to complete its own development. The evolution of koinobiosis has allowed parasitoids to exploit hosts that feed in exposed positions, and to attack hosts at a younger and numerically more common stage in the host's life cycle. Koinobiont ectoparasitism is envisaged, in some braconid and ichneumonid groups, to occupy an evolutionary transitional position between idiobiosis and endoparasitic koinobiosis; only in the Ichneumonidae have large radiations of koinobiont ectoparasitoids occurred. Endoparasitic koinobiosis is hypothesized as having arisen in the Braconidae in association with lepidopterous/coleopterous hosts, whilst in the major lineage of endoparasitic koinobiont ichneumonids, this habit is hypothesized as having arisen in association with symphytan hosts. The great majority of braconids are koinobiont endoparasitoids, but only about 50% of the Ichneumonidae have this habit. Very few koinobiont braconids develop as endoparasitoids of hymenopterous hosts, although many endoparasitic ichneumonids attack Hymenoptera. However, lineages of the Braconidae have radiated to exploit adult insects and exopterygote nymphs; ichneumonids do not utilize such hosts.