Resource partitioning and exploitative competition in stem-galling midges mediated by the host plant

Izeniola obesula Dorchin and Stefaniola defoliata Dorchin (Diptera, Cecidomyiidae) are two cecidomyiid species inducing multichambered galls in young shoots of the salt marsh plant, Suaeda monoica Gmelin (Chenopodiaceae). The purpose of this work was to study the relationship between the two species, which co‐occur in time and space, and may therefore potentially compete for plant resources. Characterization of the resources available to ovipositing females revealed that shoots in apical positions are more vigorous than shoots in basal positions, but that the two species of gall midges react to this variability of resources in different ways, as reflected by the patterns of gall distribution. Izeniola obesula galls were primarily induced in the younger, more rapidly growing shoots, whereas those of S. defoliata were predominantly induced in older, less vigorous shoots. Nevertheless, despite the general partitioning of resources, a certain amount of niche overlap was found, resulting in the occasional induction of an S. defoliata gall proximal to that of I. obesula in the same shoot. Co‐occurrence of the two types of galls in time and space did not have apparent effect on S. defoliata galls, but did have a strong adverse impact on young I. obesula galls, 60% of which were killed without producing adult midges, and the remaining 40% produced a much smaller number of adults. These effects are attributed to asymmetric interspecific competition that is mediated by the plant, resulting from the difference in stem tissues utilized by the larvae of the two species. It is concluded that preponderance of vacant niches, low densities of galls, and small niche overlap between the species do not preclude the occurrence of interspecific exploitative competition in this system, although its role in shaping the populations of the species is limited.     

Skewed sex ratios and multiple founding in galls of the oak apple gall wasp Biorhiza pallida

Abstract. 1. The gall wasp Biorhiza pallida (Hymenoptera: Cynipidae) reproduces by cyclical parthenogenesis. The adults of the sexual generation develop within galls (oak apples) that contain many larval cells.
2. Folliot [(1964) Annales Des Sciences Naturelles: Zoologie, 12, 407–564] found asexual generation females to be of three reproductive types. Androphores produce only sons, gynophores produce only daughters, and gynandrophores produce both sons and daughters. In nature, most oak apples give rise to either only males or only females but a proportion produces both sexes. These mixed‐sex galls could result either from eggs laid by one or more gynandrophores or from eggs laid by androphores and gynophores developing within a single gall (multiple founding).
3. Here the frequency of mixed‐ and single‐sex galls was quantified, and morphological and genetic analyses were carried out on the adults emerging from 10 galls to determine the frequency of multiple founding in B. pallida .
4. Seventy-five per cent of 627 galls yielded only one sex. The majority of the remaining 25% had a highly skewed sex ratio. Low genetic variation in B. pallida limited the application of allozyme-based genetic techniques, however seven of the 10 galls analysed in detail, including mixed-sex galls, appeared to have been multiply founded. Contributions by the different foundresses in multiply founded galls were highly skewed.
5. The significance of multiple founding is discussed in the light of possible adaptive scenarios (reduction of parasitoid-induced mortality, avoidance of local stochastic extinction and inbreeding) and possible competition for oviposition sites.     

Rapid gall midge adaptation to a resistant willow genotype

Abstract 1 We conducted two experiments to investigate why a basket willow Salix viminalis L. genotype, known to be highly resistant to the leaf-roller gall midge Dasineura marginemtorquens (Bremi), should support very high gall densities in a field plantation at Tälle, south Sweden.
2 The first experiment was a field test of the hypothesis of fine-scale host adaptation in the gall midge/willow system. Support for the hypothesis would be established if midges originating from resistant willows and those originating from nearby susceptible willows differed in their abilities to initiate galls and complete development on resistant plants.
3 The objective of the second experiment was to explore whether there was a genetic basis to the trait for virulence in the midge population and to investigate any potential trade-offs this trait may entail.
4 Our results indicate that there was a fine-scaled microgeographic genetic structure to the midge population at Tälle. Midges originating from resistant plants had a heritable trait that enabled them to establish galls on resistant plants.
5 Midges able to initiate galls on the resistant genotype had longer developmental time on the susceptible genotype. This suggests that there is a physiological cost associated with being adapted to the resistant willow genotype.
6 We suggest that driving forces behind the observed host adaptation are selection imposed on the midge population by very strong willow resistance and restricted gene flow in the midge populations due to the special life history features of D. marginemtorquens .     

Evidence for host-associated races in a gall-forming midge: trade-offs in potential fecundity

Abstract. 1. The gall midge, Asphondylia borrichiae , attacks the terminals of three plants in the aster family: Borrichia frutescens , Iva frutescens , and I. imbricata .
2. In the field, Borrichia suffers the highest rate of galling and I. imbricata the lowest. Common garden experiments also revealed highly significant differences in the attack rates of the three host species by Asphondylia . However, these differences depended on the source of the attacking midge population.
3. Midges collected from Borrichia and I. frutescens attacked the host in which they developed almost exclusively, whereas those from I. imbricata attacked both Iva spp.
4. Each Asphondylia larva develops in its own chamber within a gall. Borrichia galls were 2.5–3.5-fold less crowded than those from I. imbricata and I. frutescens , respectively. Consequently, midges that developed in Borrichia were significantly larger and eclosed with 30–40% more eggs than those that developed in I. imbricata and I. frutescens , respectively.
5. Although performance of Asphondylia larvae was lowest on the two Iva spp., especially I. frutescens , these hosts may provide an escape from natural enemies as a trade-off for reduced offspring performance.
6. Differences in host-plant species phenology may reduce gene flow among host-associated populations of Asphondylia , thereby favouring the formation of races at the level of plant genus.     

Gall size determines the structure of the Rabdophaga strobiloides host–parasitoid community

Abstract.  1. The relationship between gall size and mortality of the willow pinecone gall midge Rabdophaga strobiloides (Diptera: Cecidomyiidae) was examined by determining the fate of all galls in a 30-ha area in central Alberta, Canada over 4 years. It was found that gall size has a large effect on the type and intensity of mortality experienced by the gall midge, and consequently this factor has the potential to influence the dynamics of the host–parasitoid interaction through the creation of phenotypic refuges.
2. Total midge mortality ranged from 51% to 78% over the course of the study and was dominated by parasitism by Torymus cecidomyiae (Hymenoptera: Torymidae) and Gastrancistrus sp. (Hymenoptera: Pteromalidae) as well as predation by birds. Gall size had a strong, non-linear effect on the attack rates of each of these natural enemies.
3. Birds attacked the smallest size classes. Torymus cecidomyiae preferentially attacked medium diameter galls and thus avoided predation by birds in smaller galls. Gastrancistrus sp. preferentially attacked the largest galls and consequently suffered lower rates of predation by both T. cecidomyiae and birds.
4. This study emphasises the importance of understanding the interactions among mortality factors in order to describe adequately the susceptibility of R. strobiloides to parasitism and predation, and ultimately its population dynamics.     

Biology of Rhoophilus loewi (Hymenoptera: Cynipoidea: Cynipidae), with implications for the evolution of inquilinism in gall wasps

The sole described indigenous afrotropical cynipid, the South African endemic Rhoophilus loewi , was originally described as a gall inducer. As predicted by phylogenetic relationships, we confirm that R. loewi is instead an inquiline wasp. Although all other cynipid inquilines develop in galls induced by cynipid wasps, or very rarely cecidomyiid midges, R. loewi is the only cynipid inquiline of a lepidopteran gall, inducing secondary inquiline cells in galls induced by a cecidosid moth genus Scyrotis on Rhus species (Anacardiaceae). Rhoophilus is a lethal inquiline; its larval cells expand into the hollow interior of the host gall resulting in death of the gall inducer. Rhoophilus loewi is redescribed and the final-instar larva described for the first time. We describe host-plant associations, the morphology and phenology of gall formation, and the suite of parasitoid Hymenoptera associated with these galls. The community centred on Scyrotis galls is compared with those observed in other hosts of inquiline cynipids. Elucidation of the life history of R. loewi has fundamental implications for understanding the evolution of cynipid wasps.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 90 , 153–172.     

Sexually dimorphic gall structures correspond to differential phytohormone contents in male and female wasp larvae

Sexually dimorphic galls are rare among gall‐inducing insects and the reason for their occurrence is unknown. The pteromalid wasp Trichilogaster acaciaelongifoliae, which induces galls on Acacia longifolia, is one such species. In the present study, the anatomical and physiological attributes of male and female galls of T. acaciaelongifoliae are examined and compared. Histological preparations are used to characterize anatomical differences between male and female gall chambers. Bioassays, high‐performance liquid chromatography‐mass spectrometry and an enzyme immunoassay are used to measure concentrations of auxin and cytokinin in normal buds, galled tissues, and larvae of both sexes. Female chambers are found to be 3.3‐fold larger, and are associated with 1.5‐fold more storage tissue and 3.5‐fold more vascular tissues than male chambers. Tissues from female chambers induce stronger cytokinin‐like bioactivity than tissues from male chambers. Female larvae have considerably higher concentrations of cytokinin free bases, ribosides, glucosides and monophosphates than male larvae; higher auxin‐like bioactivity than in normal or galled plant tissues; and almost twice the concentration of auxin than male larvae. Both male and female larvae contain much higher auxin concentrations than either galled or normal plant tissues. These findings suggest that differing levels of phytohormones are involved in the development of sexual dimorphism of gall structures in this species.     

Testing the nutrition hypothesis for the adaptive nature of insect galls: does a non‐adapted herbivore perform better in galls?

Abstract.  1. The nutrition hypothesis for the adaptive nature of galls states that gall-inducing insects control the nutrient levels in galls to their own benefit. Although the nutrition hypothesis is widely accepted, there have been few empirical tests of this idea.
2. A novel method is presented for testing the nutrition hypothesis that links manipulation of gall nutrient levels by the gall inducer to herbivore performance. The effects of adaptation and nutritional advantage are separated by using a herbivore that is adapted to a host plant susceptible to galling but one which never enters the gall environment.
3.  Hellinsia glenni (Cashatt), a plume moth (Pterophoridae) and one of its host plants provide an excellent system for testing the nutrition hypothesis because H. glenni larvae feed internally on the relatively nutrient-poor stems of a goldenrod, Solidago gigantea , but do not venture into the nutrient-rich galls induced on that plant by a tephritid fly, Eurosta solidaginis . The nutrition hypothesis was tested by transplanting early-instar H. glenni larvae into galls and stems of S. gigantea to determine if the larvae transplanted to galls would perform better compared with those larvae transplanted to stems.
4. The results support the nutrition hypothesis for the adaptive nature of galls. Hellinsia glenni achieved greater final mass in the gall environment compared with the final mass larvae achieved in the stem environment. There was also evidence that the quality of gall tissue is controlled by the gall inducer, which has not been previously demonstrated for mature E. solidaginis galls.     

Host gall size and oviposition success by the parasitoid Eurytoma gigantea

Abstract. 1. Eurytoma gigantea Walsh is a specialist parasitoid of the tephritid gallmaker Eurosta solidaginis (Fitch).
2. In the natural environment the incidence of parasitism by Eurytoma is greater in small galls than in large ones.
3. Laboratory experiments demonstrated that small galls are not more frequently discovered; however, oviposition attempts on small galls were more likely to be successful.
4. Eurytoma spends much time probing galls too big to penetrate; this leads to a decrease in foraging efficiency when many large galls are present.
5. The chance of successfully penetrating a gall depends on the thickness of the gall wall and the length of the parasitoid's ovipositor.
6. A simulation model was constructed which shows that a gallmak-er's chance of being parasitized depends on gall size, the number of parasitoids that discover the gall, and their ovipositor lengths.     

Associational resistance mediated by natural enemies

Abstract.  1. Associational resistance theory suggests that the association of herbivore-susceptible plant species with herbivore-resistant plant species can reduce herbivore density on the susceptible plant species. Several casual mechanisms are possible but none has so far invoked natural enemies. Associational resistance mediated by natural enemies was tested for by examining densities of a gall fly, Asphondylia borrichiae (Diptera: Cecidomyiidae), and levels of parasitism on two closely related seaside plants, Borrichia frutescens and Iva frutescens , when alone and when co-occurring.
2. Both Borrichia and Iva grow alone or together on small offshore islands in Florida. Each host plant species has its own associated race of fly, but both races of fly are attacked by the same four species of parasitoids. Borrichia normally has a higher density of galls than Iva , and galls are larger on Borrichia than on Iva .
3. Gall size, gall abundance, parasitism levels, and parasitoid community composition were quantified on both Borrichia and Iva on islands where each species grew alone or together. Some islands were then manipulated by adding Borrichia to islands supporting only Iva , and by adding Iva to islands supporting only Borrichia . Subsequent gall densities and gall parasitism levels on the original native species were then examined.
4. On both natural and experimentally manipulated islands, gall densities on Iva were significantly lowered by the presence of Borrichia . This is because bigger parasitoid species that were common on Borrichia galls, which are bigger, spilled over and attacked the smaller Iva galls. Thus, parasitism rates on Iva were higher on islands where Borrichia co-occurred than on islands where Borrichia were absent. Most parasitoids from Iva were too small to successfully attack the large Borrichia galls and so gall density on Borrichia was unaffected by the presence of Iva .     

Abundance of Gall Midges on Poulsenia armata (Moraceae): Importance of Host Plant Size and Light Environment in Tropical Rain Forests1

We studied the effects of contrasting light environments on the relationship between the host plant size of Poulsenia armata and the abundance of two gall midges in a tropical rain forest in Veracruz, Mexico. The number and density of two gall morphs (i.e., laminar and vein‐petiole galls) were positively correlated with plant size only in trees found in the forest but not in gaps. The availability of foliar area of P. armata trees was greater in forest gaps than in the forest. The foliar area was positively correlated with the abundance of laminar galls in trees in forest sites, but not with vein‐petiole galls. We concluded that the abundance of two morphs of gall midges on P. armata was associated with host plant size only in the forest trees. Larger plants had more galls than small plants, although this relationship was affected by local light environments.     

Influence of tree growth rate, shoot size and foliar chemistry on the abundance and performance of a galling adelgid

1. The abundance and performance of the Eastern Spruce Gall Adelgid, Adelges abietis , was evaluated on young, open-grown trees of White Spruce, Picea glauca , whose growth rates had been increased through fertilization or decreased through root-pruning.
2. In general, gall densities were highest on control trees and on mid-crown branches. Reduced galling success on fertilized trees was largely due to higher overwintering mortality of first-generation nymphs. Foliar magnesium, total tannin and total phenol contents were positively, and nitrogen and total monoterpene contents negatively, related to gall density and/or galling success.
3. Although short shoots were more abundant, shoot length was parabolically related to gall density. There was a non-significant parabolic trend between shoot size and galling success and volume. The number and average size of A. abietis females emerging from galls were positively related to gall volume, and realized fecundity was positively correlated to female size. Consequently, fitness was approximately twice as high for nymphs colonizing intermediate-sized than small or large shoots.
4. These results do not support the plant vigour or plant stress hypotheses. The results do, however, agree with predictions of the modified plant stress hypothesis for sucking insects. It is speculated that Adelges abietis lacks the necessary resources for successful gall formation on small shoots and is unable to produce a stimulus large enough to induce gall formation on large shoots.     

垂叶榕果内寄生瘿蚊的发生规律

在云南西双版纳热带地区,一种还未被描述属和种的瘿蚊寄生于垂叶榕果内的雌花子房里,并膨大形成虫瘿,靠取食花胚组织完成发育.通过2010年定时定点的系统观察和研究瘿蚊的发生规律,结果发现:该种瘿蚊在垂叶榕上发生频率较高,抽样的18批果有17批被瘿蚊寄生,其中有13批果的寄生比率超过了60％,部分甚至达到100％.瘿蚊寄生雌花的平均比率不超过6％,平均每个榕果内有瘿蚊1～40只不等.瘿蚊寄生不仅降低了垂叶榕的种子数,还致命性地影响着传粉榕小蜂的繁殖.在对瘿蚊的羽化、交配行为及其成虫的活动规律观察中,结果显示:寄生在一个榕果里瘿蚊需要5～7d才能羽化完,其羽化高峰期出现在第2～3天;一天内羽化的高峰出现在上午8:00-10:00及晚上20:00-0:00;而羽化后瘿蚊活动高峰期出现在上午8:00-11:00.雄蚊会帮助雌蚊离开榕果并优先获得交配权,雌蚊交配后飞离繁殖自身的榕树,去寻找适合产卵的榕果繁殖后代,雄蚊不离开羽化树,而死在繁殖自身的榕树附近.这些结果为深入研究瘿蚊的防治技术提供了科学依据.     

Fungal diversity in galls of baldcypress trees

The baldcypress midge (Taxodiomyia cupressi and Taxodiomyia cupressiananassa) forms a gall that originates from leaf tissue. Female insects may inoculate galls with fungi during oviposition, or endophytes from the leaf tissue may grow into the gall interior. We investigated fungal diversity inside of baldcypress galls, comparing the gall communities to leaves and comparing fungal communities in galls that had successful emergence versus no emergence of midges or parasitoids. Galls of midges that successfully emerged were associated with diverse gall fungal communities, some of which were the same as the fungi found in surrounding leaves. Galls with no insect emergence were characterized by relatively low fungal diversity.     

Does constrained oviposition influence offspring sex ratio in the solitary parasitoid wasp Venturia canescens?

Abstract.  1. In haplodiploid organisms, virgin or sperm-depleted females can reproduce but are constrained to produce only male progeny. According to Godfray's constrained model, when p , the proportion of females constrained to produce only male progeny, is not null in a panmictic population, unconstrained females should bias their sex allocation towards females to compensate for the excess of males. These unconstrained females should be able to adjust the sex ratio in response to local variation of p .
2. In this paper an experimental approach is used to test the hypotheses of this model in the solitary endoparasitoid Venturia canescens under both field and laboratory conditions. Specifically, it is tested whether unconstrained females use their encounters with conspecifics (either male or female) to estimate p and then adjust their sex ratio accordingly.
3. As assumed by Godfray's model, constrained females actively search for host patches in the field and under laboratory conditions produce the same number of offspring during their lifetime as unconstrained females. As predicted by the model, unconstrained females produce a sex ratio biased towards females both in the laboratory and in the field.
4. The results show that this bias is not a response to encounters with conspecifics previous to oviposition. The hypothesis that the bias is due to differential mortality between sexes during ontogeny is also rejected. The proportions of constrained ovipositions estimated in two natural populations explain only a small fraction of the sex ratio bias observed in V. canescens.     

The gall-inducing habit has evolved multiple times among the eriococcid scale insects (Sternorrhyncha: Coccoidea: Eriococcidae)

The habit of inducing plant galls has evolved multiple times among insects but most species diversity occurs in only a few groups, such as gall midges and gall wasps. This phylogenetic clustering may reflect adaptive radiations in insect groups in which the trait has evolved. Alternatively, multiple independent origins of galling may suggest a selective advantage to the habit. We use DNA sequence data to examine the origins of galling among the most speciose group of gall-inducing scale insects, the eriococcids. We determine that the galling habit has evolved multiple times, including four times in Australian taxa, suggesting that there has been a selective advantage to galling in Australia. Additionally, although most gall-inducing eriococcid species occur on Myrtaceae, we found that lineages feeding on Myrtaceae are no more likely to have evolved the galling habit than those feeding on other plant groups. However, most gall-inducing species-richness is clustered in only two clades ( Apiomorpha and Lachnodius  +  Opisthoscelis ), all of which occur exclusively on Eucalyptus s.s . The Eriococcidae and the large genus Eriococcus were determined to be non-monophyletic and each will require revision.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 83 , 441–452.     

Structure,biochemistry and ecology of entomogenous galls in Selaginella Pal. Beauv. (Selaginellaceae) from India

Abstract

We studied the structure of newly found entomogenous galls in three Indian species of Selaginella, and the biochemical changes during gall development as well as their seasonal abundances in 10 squares of 1.5 m² under two differing habitat conditions, open and covered. Adult wasps (Cynipidae) initiate two types of gall formation by oviposition, spherical galls on vegetative shoots and elongated, club-shaped strobilar galls on reproductive shoots. Galls are anatomically and biochemically different from the unaffected shoots. Vegetative shoot apices bear more galls (84.6%) than reproductive shoot apices (15.4%). Gall frequency is significantly higher in covered (94.8%) than in open habitat (5.2%), and its seasonal peak occurs earlier in the former (43.1% during the rainy season) than in latter habitat (52.8% in autumn). We discuss the relationship between relative species density and gall seasonality as well as the possible role of certain environmental factors that make covered habitats more favorable to the gall inducer.     

Direct and indirect interactions involving ants, insect herbivores, parasitoids, and the host plant Baccharis dracunculifolia (Asteraceae)

Abstract.  1. The relative importance of direct and indirect interactions in controlling organism abundance is still an unresolved question. This study investigated the role of the direct and indirect interactions involving ants, aphids, parasitoids, and the host plant Baccharis dracunculifolia (Asteraceae) on a galling herbivore Baccharopelma dracunculifoliae (Homoptera: Psyllidae).
2. The effects of these interactions on the galling herbivore's performance were evaluated by an exclusion experiment during two consecutive generations of the galling insect.
3. Ants had a direct negative effect on the performance of the galling herbivore by reducing the number of nymphs per gall. In contrast, ants had no indirect effects on gall mortality through the associated parasitoids.
4. Aphids negatively affected gall development, suggesting that galls and aphids might be partitioning photoassimilates and nutrients moving throughout host-plant tissues.
5. In addition, galls that developed during the rainy season were heavier, indicating that variation in the host plant, due to weather changes, can affect the development of B. dracunculifoliae galls. However, variation in the development of B. dracunculifoliae galls due to presence of aphids or the weather changes did not affect parasitoid attack.
6. These results suggest that direct interactions between ants and galls influenced galling insect abundance, whereas numerical indirect effects involving galling insects, ants, aphids, and host plants were less conspicuous.     

The functional resource of a gall-forming adelgid

Interactions among shoots within plant modules could allow gall-insects to acquire resources from other plant parts near the feeding sites. As a result, nearby plant parts may act as a functional resource, or extended resource base. We tested for functional interconections between galls and adjacent ungalled shoots in Adelges cooleyi Gil. (Homoptera: Adelgidae) on Picea engelmanni, Engelmann spruce. Observations of gall and surrounding shoot weights showed that gall weights were twice normal shoot weights, but that surrounding shoot weights were unaffected. Reducing photosynthate availability by covering galls or surrounding shoots with opaque cloth suggested that functional interconnections exist among them; covering galls reduced surrounding current-year ungalled shoot weight, and covering surrounding shoots reduced their weight even further, but neither covering treatment affected gall or gall-insect weight. These patterns suggest that surrounding shoots constitute an extended and flexibly utilized resource base for adelgid galls. Resources made available via functional interconnections appeared to be equally available throughout adelgid galls. No differences were found in gall-insect performance in parts of the gall closer to connections with surrounding shoots compared to more distantly-located gall-insects. Further studies are required to examine patterns of resource movement among unmanipulated galls and shoots. Functional resources may be common features of plant/gall-insect interactions, potentially playing an important role in gall-insect reproductive success and habitat selection.