Gall Inducing Insects

Galls induced by insects develop through a complex series of plant cell responses. Bauhinia ungulata L. (Fabaceae: Caesalpinioideae) has leaf-folding galls, which were studied by means of anatomical and histochemical approaches. These approaches compared the non-galled leaves, non-parasitoidized galls, and parasitoidized galls by addressing two questions: (1) what structural and histochemical changes are caused by the gall inducer in the leaf tissues of the host plant? And (2) is the parasitoid capable of affecting the gall structure? The non-galled leaf is amphistomatic, with anomocytic stomata, and multicellular non-glandular and navicular glandular trichomes. The mesophyll is dorsiventral, and the vascular system is surrounded by a lignified bundle sheath. In the gall, the outer epidermis is derived from the abaxial leaf epidermis. The outer cortex of the gall originates from the chlorophyllian parenchyma, and is homogeneous, with polyhedral cells and few intercellular spaces. Th...

Thysanoptera-induced galls commonly culminate in simple folding or rolling leaf gall morphotypes. Most of these galls are induced by members of the suborder Tubulifera, with only a few species of the suborder Terebrantia being reported as gall inducers. The Terebrantia, as most of the gall inducers, manipulates the host plant cellular communication system, and induces anatomical and biochemical changes in its host plant. In an effort to keep its homeostasis, the host plant reacts to the stimuli of the galling insect and triggers chemical signaling processes. In contrast to free-living herbivores, the signaling processes involving galling herbivores and their host plants are practically unknown. Current investigation was performed into two steps: first, we set the structural profile of non-galled and galled leaves, and looked forward to find potential alterations due to gall induction by an undescribed species of Nexothrips (suborder Terebrantia) on Myrcia splendens. Once oil glands had been altered in size and number, the second step was the investigation of the chemical profile of three tissue samples: (1) non-galled leaves of a control individual, (2) non-galled leaves of galled plants, and (3) galls. This third sample was divided into two groups: (3.1) galls from which the inducing thrips were manually removed and (3.2) galls macerated with the inducing thrips inside. The chemical profile was performed by gas chromatography/ mass spectrometric detector after headspace solid-phase extraction. The galling activity of the Nexothrips sp. on M. splendens culminates in mesophyll compactness interspersed to diminutive hypersensitive spots, development of air cavities, and the increase in size and number of the secretory glands. Seventy-two compounds were completely identified in the volatile profile of the three samples, from which, sesquiterpenes and aldehydes, pertaining to the "green leaf volatile" (GLVs) class, are the most abundant. The rare event of gall induction by a Terebrantia revealed discrete alterations toward leaf rolling, and indicated

Thysanoptera-induced galls commonly culminate in simple folding or rolling leaf gall morphotypes. Most of these galls are induced by members of the suborder Tubulifera, with only a few species of the suborder Terebrantia being reported as gall inducers. The Terebrantia, as most of the gall inducers, manipulates the host plant cellular communication system, and induces anatomical and biochemical changes in its host plant. In an effort to keep its homeostasis, the host plant reacts to the stimuli of the galling insect and triggers chemical signaling processes. In contrast to free-living herbivores, the signaling processes involving galling herbivores and their host plants are practically unknown. Current investigation was performed into two steps: first, we set the structural profile of non-galled and galled leaves, and looked forward to find potential alterations due to gall induction by an undescribed species of Nexothrips (suborder Terebrantia) on Myrcia splendens. Once oil glands had been altered in size and number, the second step was the investigation of the chemical profile of three tissue samples: (1) non-galled leaves of a control individual, (2) non-galled leaves of galled plants, and (3) galls. This third sample was divided into two groups: (3.1) galls from which the inducing thrips were manually removed and (3.2) galls macerated with the inducing thrips inside. The chemical profile was performed by gas chromatography/ mass spectrometric detector after headspace solid-phase extraction. The galling activity of the Nexothrips sp. on M. splendens culminates in mesophyll compactness interspersed to diminutive hypersensitive spots, development of air cavities, and the increase in size and number of the secretory glands. Seventy-two compounds were completely identified in the volatile profile of the three samples, from which, sesquiterpenes and aldehydes, pertaining to the "green leaf volatile" (GLVs) class, are the most abundant. The rare event of gall induction by a Terebrantia revealed discrete alterations toward leaf rolling, and indicated

Aphids can affect the growth or architecture of their host-trees, but rarely challenge their survival. Nonetheless, the woolly poplar aphid, Phloeomyzus passerinii, can kill healthy, mature poplars during outbreaks. Trees fail to open their buds and flush their leaves in the spring following a severe infestation. This insect develops on poplar trunks, where it induces galls which accumulate amino acids and deplete starch content in the bark tissues. Here, we hypothesized that an infestation may then reduce non-structural carbohydrates (NSC) and non-structural nitrogen compounds (NSNC) contents in the bark, and that the reduction would be positively correlated with the infestation duration. This would in turn compromise the spring reactivation of trees. Consequently we also hypothesized that the bark contents of NSC and NSNC could be positively correlated with the amount of branches exhibiting bud break in spring, and the subsequent radial growth. The bark contents of NSC and NSNC were quantified in autumn for poplars exhibiting different levels of infestation and located in two distant stands. In one stand, NSC and NSNC contents in the bark were also quantified in the following spring and the damage level in the crowns were evaluated. In both stands, the infestation dramatically reduced the NSC and NSNC contents in autumn, especially starch and protein contents. While the drop in protein content was not related to infestation duration, the starch content gradually decreased when infestation duration increased. The infestation effect on starch content was still detectible in spring, after reserves had likely been mobilized for the spring reactivation. Starch content in autumn and spring was strongly positively correlated with crown health and radial increment. These results suggest that poplars infested by P. passerinii may die from carbon reserves deficiency, which would be an unprecedented situation for tree-aphid and tree-gall inducing insects interactions. Further experiments monitoring seasonal dynamics of NSC and NSNC reserves in different organs of infested trees should be conducted to validate this hypothesis. The results also suggest that the starch content in the bark of infested trees, in autumn, might be used as a predictor of tree decay by managers.

Galls are characteristic plant structures formed by cell size enlargement and/or cell proliferation induced by parasitic or pathogenic organisms. Insects are a major inducer of galls, and insect galls can occur on plant leaves, stems, floral buds, flowers, fruits, or roots. Many of these exhibit unique shapes, providing shelter and nutrients to insects. To form unique gall structures, gall-inducing insects are believed to secrete certain effector molecules and hijack host developmental programs. However, the molecular mechanisms of insect gall induction and development remain largely unknown due to the difficulties associated with the study of non-model plants in the wild. Recent advances in next-generation sequencing have allowed us to determine the biological processes in non-model organisms, including gall-inducing insects and their host plants. In this review, we first summarize the adaptive significance of galls for insects and plants. Thereafter, we summarize recent progress r...

Insect galls are unique organs that provide shelter and nutrients to the gall-inducing insects. Although insect galls are fascinating structures for their unique shapes and functions, the process by which gall-inducing insects induce such complex structures is not well understood. Here, we performed RNA-sequencing-based comparative transcriptomic analysis of the early developmental stage of horned gall to elucidate the early gall-inducing process carried out by the aphid, Schlechtendalia chinensis, in the Chinese sumac, Rhus javanica. There was no clear similarity in the global gene expression profiles between the gall tissue and other tissues, and the expression profiles of various biological categories such as phytohormone metabolism and signaling, stress-response pathways, secondary metabolic pathways, photosynthetic reaction, and floral organ development were dramatically altered. Particularly, master transcription factors that regulate meristem, flower, and fruit development, and biotic and abiotic stress-responsive genes were highly upregulated, whereas the expression of genes related to photosynthesis strongly decreased in the early stage of the gall development. In addition, we found that the expression of class-1 KNOX genes, whose ectopic overexpression is known to lead to the formation of de novo meristematic structures in leaf, was increased in the early development stage of gall tissue. These results strengthen the hypothesis that gall-inducing insects convert source tissues into fruit-like sink tissues by regulating the gene expression of host plants and demonstrate that such manipulation begins from the initial process of gall induction.

& Key message For an optimal deployment of poplar resistance to the gall-inducing aphid Phloeomyzus passerinii, a laboratory susceptibility assay has been developed. The nature of aphid-tree interactions during compatible and incompatible situations has been studied in detail. This should help at identifying specific resistance markers and at testing effects of site conditions on tree-pest interactions. & Context P. passerinii is a major pest of poplar plantations in Europe, and the plantation of resistant poplar genotypes is regarded as the best long-term management strategy for this pest. This requires a sound knowledge of the interactions among the pest, its host and their environment. & Aims Here, we review the recent advances aiming at developing an optimal deployment of host resistance versus P. passerinii. & Results Investigations on aphid-host interactions demonstrated that P. passerinii induces pseudogalls within the bark of susceptible hosts. This results in a reduction of starch bark content during aphid outbreaks, which could be involved in tree death. The constitutive level of starch in the bark could be related to the tolerance level of trees. A susceptibility test has been designed for poplar genotypes, discriminating three categories of susceptibility depending on tree's ability to totally or partially inhibit pseudogall induction. The test still has several limitations however. It neither takes into account the large level of individual genetic diversity of the aphid in France, nor the environmental modulation of tree resistance and tolerance, while water deficit and fertilization could potentially affect these parameters. & Conclusion The hypotheses drawn regarding the processes leading to tree death or resistance should help at identifying resistance markers, and at testing effects of site conditions on tree-pest interactions.

Successful plant colonization by parasites requires the circumvention of host defenses, and sometimes a reprogramming of host metabolism, mediated by effector molecules delivered into the host. Using transcriptomic and enzymatic approaches, we characterized salivary glands and saliva of Phloeomyzus passerinii, an aphid exhibiting an atypical feeding strategy. Plant responses to salivary extracts of P. passerinii and Myzus persicae were assessed with poplar protoplasts of a susceptible and a resistant genotype, and in a heterologous Arabidopsis system. We predict that P. passerinii secretes a highly peculiar saliva containing effectors potentially interfering with host defenses, biotic stress signaling and plant metabolism, notably phosphatidylinositol phosphate kinases which seemed specific to P. passerinii. Gene expression profiles indicated that salivary extracts of M. persicae markedly affected host defenses and biotic stress signaling, while salivary extracts of P. passerinii induced only weak responses. The effector-triggered susceptibility was characterized by downregulations of genes involved in cytokinin signaling and auxin homeostasis. This suggests that P. passerinii induces an intracellular accumulation of auxin in susceptible host genotypes, which is supported by histochemical assays in Arabidopsis. This might in turn affect biotic stress signaling and contribute to host tissue manipulation by the aphid.

An insect-induced gall is a highly specialized structure resulting from atypical development of plant tissue induced by a reaction to the presence and activity of an insect. The insect induces a differentiation of tissues with features and functions of an ectopic organ, providing nutrition and protection to the galling insect from natural enemies and environmental stresses. In this anatomical and cytological study, we characterized how the gall-inducing aphid Pemphigus betae reshapes the leaf morphology of the narrow-leaf cottonwood Populus angustifolia to form a leaf fold gall. Young galls displayed a bend on one side of the midvein toward the center of the leaf and back to create a fold on the abaxial side of the leaf. This fold was formed abaxially by periclinal and anticlinal divisions, effectively eliminating intercellular spaces from the spongy parenchyma. Galls at this stage exhibited both cell hypertrophy and tissue hyperplasia. Cells on the adaxial surface were more numerou...

Key messageFor an optimal deployment of poplar resistance to the gall-inducing aphidPhloeomyzus passerinii, a laboratory susceptibility assay has been developed. The nature of aphid–tree interactions during compatible and incompatible situations has been studied in detail. This should help at identifying specific resistance markers and at testing effects of site conditions on tree–pest interactions.ContextP. passeriniiis a major pest of poplar plantations in Europe, and the plantation of resistant poplar genotypes is regarded as the best long-term management strategy for this pest. This requires a sound knowledge of the interactions among the pest, its host and their environment.AimsHere, we review the recent advances aiming at developing an optimal deployment of host resistance versusP. passerinii.ResultsInvestigations on aphid-host interactions demonstrated thatP. passeriniiinduces pseudogalls within the bark of susceptible hosts. This results in a reduction of starch bark content...

The modification of plant structures through hypertrophy and/or hyperplasia leads to the development of galls that can be induced by various biotic agents such as viruses, bacteria, fungi, algae, nematodes, rotifers, copepods, and insects. Galls provide better utilization of underutilized niche, thus they have been reported to be helpful for insect survival and evolutionary processes. Around 13,000 species of gall-inducing insects are known worldwide, representing about 2% of the total number of insect species. These insect- gall inducers belong to different families of Hemiptera, Thysanoptera, Coleoptera, Hymenoptera, Diptera, and Lepidoptera. Even though, their wider distribution throughout the world, they have not yet explored fully. The plant defense – insect offense interaction in the gall- host interaction depends on various factors such as the production of effectors, the release of phytohormones, indirect and direct plant defense mechanisms that need to be studied for better...

The ontogenetic characterization of the leaf galls induced in the internervural region and in the second and third order veins of A. spruceanum Müell Arg. (Apocynaceae) aims to evaluate the distinct levels of cell reaction during the process of gall formation, and the relation between external gall morphology and the oviposition sites. The ground system had the most remarkable alterations, namely, the non differentiation of palisade parenchyma in both leaf sides, the hyperplasia of the spongy parenchyma and the neoformation of fibersclereids, a cell type not observed in non galled leaves. Changes of the feeding sites inside the larval chamber reveal distinct levels of cell competence to respond to the insects stimuli and explain the variations in the shape of the larval chamber.

Interest in studying galls and their arthropods inducers has been growing rapidly in the last two decades. However, the Neotropical region is probably the least studied region for gall-inducing arthropods. A study of the richness and composition of gall-inducing arthropods was carried out at Coiba National Park in the Republic of Panama. Field data come from samples obtained between August 1997 and September 1999, with three (two-week long) more intensive samplings. Seventeen sites, representing the main land habitats of Coiba National Park were surveyed. 4942 galls of 50 insect and 9 mite species inducing galls on 50 vascular plants from 30 botanical families were colleted. 62.7% of the galls were induced by gall midges (Diptera, Cecidomyiidae), 15.3% by mites, Eriophyidae, 8.5% by Homoptera, Psyllidae, 6.8% by Coccidae and 5.1% by Phlaeothripidae (Tysanoptera). The host plant families with the most galls were Myrtaceae with seven, Bignoniaceae with five and Euphorbiaceae, Fabaceae and Melastomataceae with four. Leaf galls accounted for about 93% of collected galls. Most leaf galls were pit/blister galls followed by covering and pouch galls. Gall richness per collecting site was between 1 and 19 species. Coiba's gall diversity is discussed in relation to data available from other tropical sites from continental Panama and the Neotropical region. Our results support the idea that it may be premature to conclude that species richness of gall inducers declines near the equator. Rev.

Two kinds of cecidomyiid galls induced by Daphnephila on Machilus thunbergii Sieb. & Zucc. leaves at various developmental stages, i.e., young, growing, and mature, were analyzed for their biochemical composition of photosynthetic pigment-protein complexes located in thylakoid membranes using the Thornber and MARS electrophoretic fractionation systems. Both kinds of galls were totally deficient in the pigment-protein complexes CP1, and A1, AB1, and AB2 through the whole period of gall formation. Immunoblotting of antibody against light-harvesting complex 2b (LHC2b) apoprotein confirmed this deficiency in gall's lifetime, which never recovered under any condition. Electron microscopy demonstrated that already at the early developmental stage the gall chloroplasts had thylakoid morphology like that in a normal leaf.

Survey was conducted in Eucalyptus nurseries and plantations of TAFCORN at Karaikudi, Aranthangi, Pudukattai, Ariyalur and Sivagangai regions and TNPL farm forestry areas at Thiruvallur, Chengalpet, Mathuranthakam, Kanchipuram, Sriperumputhur, Madapuram, Akaram, Ulunthoorpettai, Thirunelveli, Sivagangai, Kovilpatti, Sattur, Ariyalur, Thiruvannamalai, Krishnagiri, Dharmapuri and Namakkal, covering five Agro-climatic zones of Tamil nadu viz., Cauvery Delta, North Eastern, Western and Southern Zones. Of the nineteen clones planted, clones like C10, C7, C271, T61 and C 283, were found infested with gall insect, Leptocybe invasa, ranging from 80-100%. Clone 413 was planted in all the agro-climatic zones surveyed and found free from gall. The most preferred clones C10, C3 and C7 were infested in all agro-climatic zones of Tamilnadu. Clone C283 and C271 were found to be most susceptible clones in southern, north eastern and north western zones, respectively. The present survey reveals that...

Orange leafhopper Cicadulina bipunctata feeding induces wallaby ear symptoms, namely growth suppression and gall formation characterized by severe swelling of leaf veins, on various Poaceae, thereby leading to low crop yields. Here, we investigated the development of wallaby ear symptoms on rice seedlings due to C. bipunctata feeding. After confirming that C. bipunctata feeding induces growth suppression and gall formation on rice seedlings, we further demonstrated that gall formation score decreased with decreasing levels of nitrogen in the medium and that C. bipunctata feeding induces the expression levels of nitrogen transporter genes. These gene expression changes may participate in the nutrient accumulation observed in galled tissues and in gall formation. In addition, these expression changes should induce growth promotion but the inhibition of gibberellin signaling by C. bipunctata feeding might be the reason why growth is suppressed. Treatment with plant growth regulators di...

The evolution of the gall-inducing ability in insects and the adaptive significance of the galling habit have been addressed by many studies. Cicadulina bipunctata, the maize orange leafhopper, is an ideal study organism for evaluating these topics because it can be mass-reared and it feeds on model plants such as rice (Oryza sativa) and maize (Zea mays). To reveal differences between gall inductions by C. bipunctata and other gall inducers, we conducted four experiments concerning (a) the relationship between the feeding site and gall-induction sites of C. bipunctata on maize, (b) the effects of leafhopper sex and density, (c) the effects of length of infestation on gall induction, and (d) the effects of continuous infestation. C. bipunctata did not induce galls on the leaves where it fed but induced galls on other leaves situated at more distal positions. The degree of gall induction was significantly correlated with infestation density and length. These results indicate that C. bipunctata induces galls in a dosedependent manner on leaves distant from feeding sites, probably by injecting chemical(s) to the plant during feeding. We suggest that insect galls are induced by a chemical stimulus injected by gall inducers during feeding into the hosts.

The maize orange leafhopper Cicadulina bipunctata (Melichar) is an insect pest of cereal crops in tropical and subtropical regions of the Old World. This leafhopper induces gall symptoms characterized by stunted growth and swollen leaf veins on various Poaceae. Damage by C. bipunctata has been reported from Australia, the Philippines, China, Taiwan, and Japan. In Japan, C. bipunctata occurs in the central and southern parts of Kyushu. Because the leafhopper is a potential pest of various cereal crops, we conducted field surveys in Shikoku and the southern part of the Kii Peninsula (a part of Honshu), where the climate seems to be suitable for the establishment of C. bipunctata. As a result, we found C. bipunctata at some localities in Ehime and Kochi Prefectures. This is the first record of this leafhopper from Shikoku. Our laboratory experiment revealed that a Kochi population of C. bipunctata had a gall inducing ability similar to the Kumamoto population. More attention should be paid to assessing the risk of further expansion of C. bipunctata populations in Shikoku.

The maize orange leafhopper Cicadulina bipunctata (Hemiptera: Cicadellidae) induces galls characterized by growth stunting and severe swelling of leaf veins on various plants of Poaceae. Previous studies revealed that galls are induced not on feeding site but on distant, newly extended leaves during the feeding, and strongly suggested that some chemicals injected by the leafhopper affect at the leaf primordia. To approach the mechanism underlying gall induction by C. bipunctata, we examined physiological response of plants to feeding by the leafhopper. We performed high-throughput and comprehensive plant hormone analyses using LC-ESI-MS/MS. Galled maize leaves contained higher contents of abscisic acid (ABA) and trans-Zeatin (tZ) and lower contents of gibberellins (GA 1 and GA 4) than ungalled maize leaves. Leafhopper treatment significantly increased ABA and tZ contents and decreased GA 1 and GA 4 contents in extending leaves. After the removal of leafhoppers, contents of tZ and gibberellins in extending leaves soon became similar to the control values. ABA content was gradually decreased after the removal of leafhoppers. Such hormonal changes were not observed in leafhopper treatment on leaves of resistant maize variety. Water contents of galled leaves were significantly lower than control leaves, suggesting water stress of galled leaves and possible reason of the increase in ABA content. These results imply that ABA, tZ, and gibberellins are related to gall induction by the leafhopper on susceptible variety of maize.

This study investigates the variation among Eucalyptus clones for incidence of gall wasp (Letocybe invasa) and relative changes in biochemical parameters. The three years, and replicated clonal trial involved 14 clones with monthly observations made on the gall wasp incidence. Significant variation was found among the clones, with maximum incidence being in F-316 and relatively the least incidence in C-413, PE-11, PE-14 and C-72. Gall wasp incidence gradually increased from January to April and declined thereafter. The total soluble sugars and phenol content in the infested leaves were found to increase by 49.2 and 22.8% respectively, whereas the protein content decreases (8.8% decrease).

We investigated insect galls in Rupestrian field and Cerrado vegetation in the municipality of Caetité (BA), Brazil, between August/2015 and June/2016. This is the first study of gall diversity in Rupestrian field vegetation in that state. We encountered 48 different morphotypes of galls, distributed among 17 different plant species belonging to 13 genera and 21 host plant families. The greatest gall richness was observed in Cerrado (n=39) as compared to Rupestrian field (n=9) vegetation. The principal botanical families observed with galls were Leguminosae, Malpighiaceae, and Myrtaceae, with 10, 8 and 4 morphotypes, respectively. The genera showing the greatest gall diversity were Copaifera L. (n=6) (Leguminosae-Detarioideae), Croton L. (n=2) (Euphorbiaceae), Mimosa L. (n=2) (Leguminosae-Caesalpinioideae), Byrsonima Rich. ex Kunth (n=2) (Malpighiaceae), and Eugenia L. (n=2) (Myrtaceae). The super-host species was Copaifera sabulicola J.A.S. Costa & L.P. Queiroz (n= 5). Most galls occurred on leaves, being globoid, glabrous, isolated, and unilocular. Most gall-inducing insect species belong to the Cecidomyiidae family, while the associated fauna was represented by Hymenoptera and Lepidoptera. We recorded here for the first time galls on Ocotea velutina (Mart. ex Ness) Rohwer (Lauraceae) and Miconia alborufescens Naudin (Melastomataceae). The results indicate the need for more studies to understand the dynamics of the insect-induced galls in Rupestrian field.

Analyses of gall biology and development allow determination of morphogenesis events in host-plant organs that are altered by galling insects. Currently, we assume that there is a correlation between Lopesia sp. instars and the alterations in gall tissues on Mimosa gemmulata that generate the gall shape. The development of Lopesia sp. (three larval instars, pupae and adult) correlates positively with gall growth, especially on the anticlinal axis. First-instar larvae are found in galls at the stage of induction, Instar 2 in galls at early growth and development, Instar 3 in galls at late growth and development, pupae in galls at maturation, and the adult emerges from senescent galls. At induction, the larva stimulates cell differentiation in pinnula and pinna-rachis tissues on M. gemmulata. At early growth and development stages, cell division and expansion are increased, and non-glandular trichomes assist gall closing. Homogenous parenchyma and neoformed vascular bundles characteri...

Aim Figs (Ficus, Moraceae) are exploited by rich communities of often host-specific phytophagous wasps. Among them, gall-inducing Sycophaginae (Hymenoptera, Chalcidoidea) may share a common history with Ficus and their mutualistic pollinators (Agaonidae). We investigate here, for the first time, the phylogeny and biogeographical history of Sycophaginae and compare the timing of radiation and dispersion of major clades with available data on Ficus and fig pollinators. Reconstructing the history of their host colonization and association over space and time is central to understanding how fig wasp communities were assembled. Location Worldwide. Methods Maximum likelihood and Bayesian analyses were conducted on 4267 bp of mitochondrial and nuclear DNA to produce a phylogeny of all genera of Sycophaginae. Two relaxed clock methods with or without rate autocorrelation were used for date estimation. Analyses of ancestral area were also conducted to investigate the geographical origin of the Sycophaginae. Results The phylogeny is well resolved and supported. Our data suggest a post-Gondwanan origin for the Sycophaginae (50-40 Ma) and two independent outof-Australia dispersal events to continental Asia. Given palaeoclimatic and palaeogeographic records, the following scenario appears the most likely. The ancestor of Idarnes+Apocryptophagus migrated to Greater India through the Ninetyeast Ridge (40-30 Ma). The ancestor of Anidarnes+Conidarnes dispersed later via Sundaland (25-20 Ma). Idarnes and Anidarnes subsequently reached the New World via the North Atlantic land bridges during the Late Oligocene Warming Event. Apocryptophagus reached Africa c. 20 Ma via the Arabic corridors and returned to Australasia following the expansion of Sundaland tropical forests (20-10 Ma). Main conclusions Sycophaginae probably invaded the fig microcosm in Australia c. 50-40 Ma after the origin of their host plant. Once associated with figs, they dispersed out of Australia and radiated together with their host fig and associated pollinator through the tropics. We recorded a good coincidence of timing between dispersal events of Sycophaginae and continental connections. Furthermore, fruit pigeons that disperse figs probably spread out of Australasia through the Indian Ocean via the Ninetyeast Ridge c. 38 Ma. Therefore, our study highlights the potential for combining molecular phylogenetics with multiple methods of dating of interacting groups to reconstruct the historical biogeography of plant-herbivore associations.

Galling arthropods represent one of the most specialized herbivore groups. On an evolutionary scale, different taxa of insects and mites have convergently adapted to a galling lifestyle. In this study, we have used a multi-taxonomic approach to analyze the interaction specialization between gall-inducing mites and insects and their host plants in the Nitra City Park (Nitra, Slovakia). We used four ecological descriptors for describe plant-galling interactions: number of host plant species used by each arthropod species, galling specificity on host plant species (specificity), exclusivity of interactions between galling and plant species (specialization) and overlap of the interactions between arthropod species (similarity). We have found 121 species of gall-inducing arthropods, totaling 90 insects and 31 mites occurring on 65 host plant species. Our results reveal that mites have high specialization and low similarity of interactions in comparison to insects. A multiple-taxonomic co...

1Laboratoire d'Écologie, Département de Biologie, Faculté des Sciences, Université de Sherbrooke, 2500 Boulevard Université, Sherbrooke, Québec J1K 2R1, Canada. 2Laboratório de Ecologia, Departamento de Botânica, Centro de Ciências Biológicas, Universidade ...

Aphid feeding behavior and performance on a given host plant are influenced by the plants’ physical and chemical traits, including structural characters such as trichomes and nutritional composition. In this study, we determined the feeding behavior and performance of soybean aphids (Aphis glycines) on the stem, the adaxial (upper), and the abaxial (lower) leaf surfaces during early vegetative growth of soybean plants. Using the electrical penetration graph technique, we found that aphids feeding on the stem took the longest time to begin probing. Once aphids began probing, the sieve elements were more conducive to feeding, as evidenced by less salivation on the stem than either leaf surface. In whole-plant assays, stems harbored higher aphid populations, and aphids had shorter development time on stems than the adaxial and the abaxial leaf surfaces. We compared trichome density and length on the stem, the adaxial, and the abaxial leaf surfaces to investigate whether plant trichomes...

Galls are neoformed structures induced by specific animals, fungi, bacteria, virus or some parasitic plants on their host plant organs. Developmental processes are well known in Agrobacterium tumefasciens galls, but the animal-induced galls have a striking anatomical diversity, concerning several patterns, which were reunited herein. Anatomical traits observed in animal-induced galls involve manipulation of plant morphogenesis in convergent ways. Nematode, mite and insect galls usually contain homogeneous storage parenchyma and develop due to hyperplasia and cell hypertrophy. The development of typical nutritive tissues, giant cells, or hypertrophied vascular bundles may occur. Some other anatomical features may be usually restricted to galls induced by specific taxa, but they may eventually be related to the developmental potentialities of the host plants. The combination of distinct morphogenetic peculiarities in each gall system culminates in extant gall structural diversity. Convergent anatomical traits are observed according to the feeding mode of the gall inducers, representing potentiation or inhibition of similar events of host plant morphogenesis and cell redifferentiation, independent of gall-inducing taxa.

Gall-inducing Aphididae may feed directly on phloem, whereas Eriophyidae and Nematoda feed on cells lining the gall chambers. We assume that a variation in structural complexity will occur within galls induced by each taxon, and that the complexity of the galls could be related to the types of storage tissue they have. Histological, histometric, and histochemical analyses were used to compare six gall systems with different levels of complexity. Such levels are not taxon-related, even though eriophyid galls are usually simpler than nematode and aphid galls. The histological features of galls allowed the classification of storage tissues into three types: typical nutritive tissues (TNT), common storage tissues (CST), and nutritive-like tissues (NLT). The TNT and NLT have cells with dense cytoplasm and a prominent nucleus. The CST cells are vacuolated, and may store starch and other energy-rich molecules, as do the NLT cells. In contrast to NLT or CST, the TNT serves as a direct food ...

Galls induced by insects develop through a complex series of plant cell responses. Bauhinia ungulata L. (Fabaceae: Caesalpinioideae) has leaf-folding galls, which were studied by means of anatomical and histochemical approaches. These approaches compared the non-galled leaves, non-parasitoidized galls, and parasitoidized galls by addressing two questions: (1) what structural and histochemical changes are caused by the gall inducer in the leaf tissues of the host plant? And (2) is the parasitoid capable of affecting the gall structure? The non-galled leaf is amphistomatic, with anomocytic stomata, and multicellular non-glandular and navicular glandular trichomes. The mesophyll is dorsiventral, and the vascular system is surrounded by a lignified bundle sheath. In the gall, the outer epidermis is derived from the abaxial leaf epidermis. The outer cortex of the gall originates from the chlorophyllian parenchyma, and is homogeneous, with polyhedral cells and few intercellular spaces. Th...

The galls induced by Cecidomyiidae, Diptera, are very diverse, with conspicuous evidence of tissue manipulation by the galling herbivores. Bud galls, as those induced by an unidentified Cecidomyiidae species on Marcetia taxifolia, Melastomataceae, can be considered as one of the most complex type of prosoplasma galls. The gall-inducer manipulate the axillary meristem of the plant in a way that gall morphogenesis may present both vegetative and reproductive features of the host plant. Herein, we analyzed traces of determinate and indeterminate growth in the bud gall of M. taxifolia, looking for parallels between the features of the leaves and flowers, natural fates of the meristematic cells. The bud galls are induced by the cecidomyiid fly, and are formed by the connation of eight leaf primordia, a common process in ovary morphogenesis. The bud gall corresponds to a pistil-shaped gall morphotype, with anatomical features similar to those of an hypanthium and sepals. The gall mimics an ovary, which has protective barriers at the apex, and a nutritive tissue (with storage of lipids and proteins) or a placenta, respectively, at the basal portion. The redifferentiation of the promeristem into a nutritive tissue at the base of the gall confers a determinate destiny to the axillary bud. Comparatively, the gradients of cell expansion and of accumulation of primary metabolites also indicate that the gall and the ovary are convergent structures. Some constraints of the host plant cells, such as the absence of lignification, and the accumulation of polyphenols, lipids and terpenoids, are not altered and may confer chemical protection for plant tissues and the larva against oxidative stress. 2014 Elsevier GmbH. All rights reserved.

One of the galling herbivores associated to the superhost Schinus polygamus (Cav.) Cabrera (Anacardiaceae) is Calophya duvauae Scott (Hemiptera: Calophyidae). The galls are located on the adaxial surface of leaves and vary from red to green. The levels of their pigments were herein investigated in relation to age. Samples were collected between June 2008 and March 2009, in a population of S. polygamus at Canguçu municipality, Rio Grande do Sul, Brazil. Galls were separated by color, measured, dissected, and the instar of the inducer was determined. The levels of photosynthetic (chlorophyll a and b, total chlorophylls, and carotenoids) and protective pigments (anthocyanins) were also evaluated. Red galls were more numerous than the green ones, and the induction should occur preferentially on young leaves, but may also occur on mature leaves. Immature stages of C. duvauae were observed in all samples throughout the year, characterizing its life cycle as multivoltine. There was a significant correlation between the instar of the inducer and the size of the gall (r ¼ 0.675, p < 0.001), with larger galls corresponding to more advanced instars. The ratio between red and green galls varied over the samples, with the highest (96%) and lowest (38%) frequency of red galls observed in September, and December 2008, respectively. The average amounts of chlorophyll b and total chlorophylls were 70% lower in the gall tissues when compared to non-galled portions of galled leaves. There is a notable reduction in the contents of all pigments in the galls when compared to non-galled leaves, especially for total anthocyanins in green galls. The red galls presumably had the constant stimuli of healthy gall inducers, whereas in green galls they died prematurely, due to the interference of parasitoids and inquilines. The alterations in gall structure and color were related to the gradual decreasing in galling stimuli.

The only genus of the tribe Fordini (Aphididae; Eriosomatinae) that is endemic in the American continent and that is hosted by plants of the genus Pistacia is Geopemphigus. Galls induced by the species G. morral, G. torsus and G. blackmani on Pistacia mexicana, a member of the Anacardiaceae family, were studied microscopically. The study shows characteristics shared by the three galls and specific differences, lending support to the notion that galls are the extended phenotype of gallicolous aphids. Of the three galls, G. morral shows the smallest degree of modification and the lowest cellularity, followed by G. torsus. The gall G. blackmani presents the most severe modification. On the other hand, the three galls have in common that they are not closed galls and have a multiseriate epidermis-lumen with cuticle, an interior surface without dimples, and a single vascular bundle in the wall (phloem-xylem). These common microscopic characteristics show that the genus Geopemphigus is closer to the genera Forda and Paracletus than to Baizongia.

Blue Gum Chalcid (BGC), Leptocybe invasa Fisher and La Salle (Hymenoptera: Eulophidae), causes high damages on Eucalyptus camaldulensis Dehnh in many countries including Ethiopia. This study aimed to determine the damage, damage severity and distribution of the BGC on Eucalyptus camaldulensis plantations in Eastern Amhara, Ethiopia. The assessment was conducted at Tehuledere (South Wollo zone), Habru (North Wollo Zone) and Dawa Chefa (Oromia adminstration zone) districts. These districts were selected purposively for continuous infestation. Three sites per district with a total of nine sites were selected. Assessments were done from four coppiced and five plantations. A minimum of 0.25 ha and five trees per site were assessed in a monthly interval. The assessment result revealed that BGC was found in all the three districts of the three zones. During the assessment, it was found that from five trees the damage severity were 20% nil, 15.6% low, 20% medim, 22.2 high, and 22.2% high. S...

Mediterranean representatives of the galling aphid tribe Fordini (Hemiptera: Aphididae: Eriosomatinae) are usually grouped under the subtribe term Fordina. Aphids within Fordina display two-year life cycles, alternating between Pistacia shrubs, where they induce conspicuous galls, and roots of Poaceae species. The high number of morphs present in a given species, the lack of knowledge of the complete cycle in some species, and the similarity between homologous morphs observed in different species pose many taxonomic problems in this group. We present results of a survey to elucidate the phylogenetic relationships among Fordini species present in the Iberian Peninsula and the Canary Islands. Sequences from the nuclear long-wavelength opsin (LWO) and translation elongation factor 1a (EF-1a) genes and from a region of the mitochondrial DNA containing the genes encoding the subunits six and eight of the F-ATPase were used to infer relationships among 10 Fordina species, namely Smynthurodes betae, Aploneura lentisci, Baizongia pistaciae, two Geoica species (G. utricularia and G. setulosa), three species of Forda and two of Paracletus. Relationships between and within representatives of the genera Forda and Paracletus, both exemplifying taxonomic and ecological problems, were investigated in greater depth through extensive sampling and morphometric analysis. A total of eight, six and six samples from F. formicaria, F. marginata and F. riccobonii, respectively, were included in the survey, along with 40 and 4 samples classified initially as P. cimiciformis and P. donisthorpei, respectively. Our results are relevant to current studies on the evolution of host selection by aphids and on the evolution of gall morphology. Our phylogeny suggests that the group can be divided into two main clades. One clade is composed of aphids inducing small, low-capacity galls on either P. atlantica or P. terebinthus (Smynthurodes betae and genera Forda and Paracletus). The second clade is composed of species inducing larger galls on P. lentiscus and P. terebinthus (Aploneura lentisci, Baizongia pistaciae and Geoica species). Our results suggest that revision of diagnostic characters used in the taxonomy of Paracletus is needed, and suggest Forda rotunda as a new synonym of Paracletus cimiciformis syn.n.

Forestry expertise and plantations managers are struggling to find cheaper and sustainable solutions to contain the losses caused by Leptocybe invasa in the last nine years on the forest stands in Mozambique. Aiming to help find a solution in the control of L. invasa early in the nursery, we conducted an experimental trial at the Niassa Forestry company nursery, located in the Niassa province, northern Mozambique in February 2015. Three insecticides: Acetamiprid, Thiamethoxam, Imidacloprid, with and without adherent and pH regulator were tested. The experiment had seven treatments including the control. The number of seedlings infested by the gall wasp were assessed 15, 30, 45 and 60 days after the seeds were sown in the nursery. Data were analysed in R package. Normality and homogeneity of variances were tested through Shapiro-Wilk and Bartlett&#39;s tests respectively. Analysis of Variance (ANOVA) and parametric means test (Tukey-HSD), were used to assess whether there was differe...

The resource concentration hypothesis states that the concentration or dispersion of host resources has a direct influence on herbivore insect populations. Plant consumers tend to concentrate at places in which the plant resources are abundant and easy to find. Results with Schinus polygamus (Cav.) Cabr. (Anacardiaceae), a shrub showing high leveis of attack by different herbivorous insects, suggest that the concentration of resources influences the level of attack by galling insects, but not in the case of folivorous insects. This difference could be related with the biological features of the species involved, such as size, searching behaviour and flight capacity. Different degrees of specialization could also explain the differences between attack of galling and folivorous insects.

One of the galling herbivores associated to the superhost Schinus polygamus (Cav.) Cabrera (Anacardiaceae) is Calophya duvauae Scott (Hemiptera: Calophyidae). The galls are located on the adaxial surface of leaves and vary from red to green. The levels of their pigments were herein investigated in relation to age. Samples were collected between June 2008 and March 2009, in a population of S. polygamus at Canguçu municipality, Rio Grande do Sul, Brazil. Galls were separated by color, measured, dissected, and the instar of the inducer was determined. The levels of photosynthetic (chlorophyll a and b, total chlorophylls, and carotenoids) and protective pigments (anthocyanins) were also evaluated. Red galls were more numerous than the green ones, and the induction should occur preferentially on young leaves, but may also occur on mature leaves. Immature stages of C. duvauae were observed in all samples throughout the year, characterizing its life cycle as multivoltine. There was a significant correlation between the instar of the inducer and the size of the gall (r ¼ 0.675, p < 0.001), with larger galls corresponding to more advanced instars. The ratio between red and green galls varied over the samples, with the highest (96%) and lowest (38%) frequency of red galls observed in September, and December 2008, respectively. The average amounts of chlorophyll b and total chlorophylls were 70% lower in the gall tissues when compared to non-galled portions of galled leaves. There is a notable reduction in the contents of all pigments in the galls when compared to non-galled leaves, especially for total anthocyanins in green galls. The red galls presumably had the constant stimuli of healthy gall inducers, whereas in green galls they died prematurely, due to the interference of parasitoids and inquilines. The alterations in gall structure and color were related to the gradual decreasing in galling stimuli.

Several species of Ficus present leaf galls and the goal of this research is to study the structural alterations involved in the formation of leaf galls caused by Gynaikothrips ficorum on F. microcarpa, an ornamental plant. The galls of young and mature leaves were separated into two developmental stages based on the presence of lesions on leaf lamina and the degree of leaf folding. Swellings of the lamina were observed in young and mature leaves during gall development which coincided with the areas of cellular hypertrophy and tissue hyperplasia. Swellings were detected in a greater amount and more precociously on young leaves when compared to mature ones. In young leaves, the cecidogenetic responses were quicker and led to further structural differences because younger cells are not completely differentiated. Cell hypertrophy and tissue hyperplasia were striking processes involved in the ontogenesis of the studied gall, similar to other galls induced by thrips. Nevertheless, in sp...

The investigation was comprised of 14 Eucalyptus clones and two Eucalyptus species of fifteen months age planted in complete randomized block design with 3 replications each in 2m × 2m spacing. Among all the Eucalyptus entries E. torellina was found resistant (free of gall). Eucalyptus entries P-411, P-413, P-2136, ERK-04, P-526 and E. pellita were found highly tolerant (GDI: &gt;0-1); P-286, JK-04, B-2153 and SRO-16 were found moderately tolerant (GDI: &gt;1-25); JK-08 and JK-02 were found moderately susceptible (GDI: &gt;25-200) and P-2049, P-2155 and P-405 were found highly susceptible (GDI: &gt;200). Gall wasp damage had significant and negative correlation with growth parameters (height, DBH and volume growth). With respect to growth performance, highest average height (11.42 m) was obtained in P-411 (highly tolerant) and followed by P-413 (10.77 m), P-2136 (10.33m), P-526 (11.19 m), B-2153 (10.58 m) and SRO-16 (10.27 m). The highest average DBH (85.64 mm), average volume (2259...

Plant populations frequently maintain submaximal levels of resistance to natural enemies, even in the presence of substantial genetic variation for resistance. Identifying constraints on the evolution of increased resistance has been a major goal of researchers of plant-herbivore interactions. In a glasshouse study, we measured relative costs and benefits of resistance of tall goldenrod (Solidago altissima) to the gall-inducing tephritid Eurosta solidaginis. We exposed multiple ramets of 26 goldenrod genets to nutrient or shade stress and to oviposition by E. solidaginis. The presence of a gall cost a ramet an average of 1743 seeds, but the cost differed 10-fold across environments. Plant genets varied widely for an induced &#39;hypersensitive&#39; response in which meristem cells become necrotic and kill E. solidaginis hatchlings before gall induction. There was no evidence that this highly effective resistance trait carried an allocation cost. However, the response carried a risk ...

A survey was conducted at Oruc:binga refugee settlement in Mbarara district, Uganda in November 2003 to dttermine the cause, incidence and severity of a gatl damage on Eucalyptus spKies in nursery and woodlots. Leptocybe invasa (Hymenoptera: Eulophidae), a tiny black wasp commonly kuown as blue gum chalcid, was found to be the cause of the gall damage on EucolyptNs. The wasp at1acked field planted seedlings and saplings, but not seedlings in the nursery. The lncide~~a and severity of the wasp attacks were markedly higher on Eucalyptus grandis than E. saflgna. Resurdr is UrJently oeeded to develop Integrated Pest Management (IPM) strategies against the new Eucalyptus pest.

A survey of Northern India was carried out from 2010 to 2014 in different Eucalyptus growing areas of Uttarakhand, Uttar Pradesh, Haryana and Punjab. Gall wasp infestation was observed in both young plantations and nurseries. Observations revealed that in northern India Eucalyptus growing areas were under threat of attack by gall wasp, Leptocybe invasa. Biological control of Leptocybe invasa has been applied in Punjab, from 2012 to 2016, where infestation of gall wasp was regularly decreased and came below 10 % by April 2016.

In this investigation, biological control of eucalyptus Gall wasp, Leptocybe invasa Fisher & La Salle (Hymenoptera: Eulophidae) in Punjab, India was investigated. The genus Leptocybe Fisher & La Salle (Hymenoptera: Eulophidae) was founded with its type species, L. invasa from Israel in 2004. Adult wasps of L. invasa   induce galls on the shoots and midribs of leaves of Eucalyptus sp. and also damage nursery seedlings and young plantations. In the present study, survey was carried out from the year 2012 to 2014, on gall wasp infestation in different eucalyptus growing areas of Punjab. Observations  revealed  that  eucalyptus  growing  areas  in  Punjab were  under  the threat  of  attack  by  gall  wasp,  L. invasa.  During the present study, biological control agents Megastimus viggianii and Quadrastichus mendeli have been successfully applied in the gall infested areas of Punjab, from 2012 to 2017, where infestation of gall wasp was regularly decreased and came below 10 % by July, ...

The Bemisia tabaci species complex (whitefly) causes enormous agricultural losses. These phloem-feeding insects induce feeding damage and transmit a wide range of dangerous plant viruses. Whiteflies colonize a broad range of plant species that appear to be poorly defended against these insects. Substantial research has begun to unravel how phloem feeders modulate plant processes, such as defense pathways, and the central roles of effector proteins, which are deposited into the plant along with the saliva during feeding. Here, we review the current literature on whitefly effectors in light of what is known about the effectors of phloem-feeding insects in general. Further analysis of these effectors may improve our understanding of how these insects establish compatible interactions with plants, whereas the subsequent identification of plant defense processes could lead to improved crop resistance to insects. We focus on the core concepts that define the effectors of phloem-feeding in...