Gall-inducing Insects Research Articles

Sun and shade galls of Clinodiplosis profusa (Cecidomyiidae) on Eugenia uniflora (Myrtaceae): Are there differences in their establishment and growth?

Gall-inducing insects stimulate their host plants, leading to the formation of distinct structures, such as the fusiform galls induced by Clinodiplosis profusa Maia, 2001 (Cecidomyiidae) on leaves of Eugenia uniflora L. (Myrtaceae). The influence of different light conditions on infestation rates, establishment, and morphogenesis of galls is little known. We tested if gall infestation is higher in E. uniflora sun plants compared to shade plants, and if the size, anatomical, and histometrical features of the mesophyll and epidermis are distinct between sun and shade leaves and galls. Gall infestation rates are similar in sun and shade plants, although the results indicate a possible difference in life cycle duration between the light conditions. Anatomical data revealed the leaves and galls respond similarly to sun and shade for number of cell layers. In the galls the hyperplasia provoked by C. profusa is influenced by distinct sunlight exposure. Cell hypertrophy and a reduced stomatal index in the galls is remarkable when compared to non-galled leaves. The cell sizes in the mesophyll and epidermis and stomatal densities are similar between the sun and shade galls, but these factors are distinct between the sun and shade leaves. Cell hypertrophy and epidermal differentiation patterns are more influenced by the gall inducer, which inhibits the influence of light on these patterns. In conclusion, gall morphogenesis is strongly influenced by galling stimuli for some developmental processes, but other processes are influenced by abiotic conditions, such as light exposure. This opens a field in gall ecological anatomy and development.

Extreme acidity in a cynipid gall: a potential new defensive strategy against natural enemies.

The morphology of insect-induced galls contributes to defences of the gall-inducing insect species against its natural enemies. In terms of gall chemistry, the only defensive compounds thus far identified in galls are tannins that accumulate in many galls, preventing damage by herbivores. Intrigued by the fruit-like appearance of the translucent oak gall (TOG; Amphibolips nubilipennis, Cynipidae, Hymenoptera) induced on red oak (Quercus rubra), we hypothesized that its chemical composition may deviate from other galls. We found that the pH of the gall is between 2 and 3, making it among the lowest pH levels found in plant tissues. We examined the organic acid content of TOG and compared it to fruits and other galls using high-performance liquid chromatography and gas chromatography-mass spectrometry. Malic acid, an acid with particularly high abundance in apples, represents 66% of the organic acid detected in TOGs. The concentration of malic acid was two times higher than in other galls and in apples. Gall histology showed that the acid-containing cells were enlarged and vacuolized just like fruits mesocarp cells. Accumulation of organic acid in gall tissues is convergent with fruit morphology and may constitute a new defensive strategy against predators and parasitoids.

Ab-GALFA, A bioassay for insect gall formation using the model plant Arabidopsis thaliana

Insect galls are abnormal plant organs formed by gall-inducing insects to provide shelter and nutrients for themselves. Although insect galls are spatialized complex structures with unique shapes and functions, the molecular mechanism of the gall formation and the screening system for the gall inducing effectors remains unknown. Here, we demonstrate that an extract of a gall-inducing aphid, Schlechtendalia chinensis, induces an abnormal structure in the root-tip region of Arabidopsis seedlings. The abnormal structure is composed of stem-like cells, vascular, and protective tissues, as observed in typical insect galls. Furthermore, we confirm similarities in the gene expression profiles between the aphid-treated seedlings and the early developmental stages of Rhus javanica galls formed by S. chinensis. Based on the results, we propose a model system for analyzing the molecular mechanisms of gall formation: the Arabidopsis-based Gall-Forming Assay (Ab-GALFA). Ab-GALFA could be used not only as a model to elucidate the mechanisms underlying gall formation, but also as a bioassay system to isolate insect effector molecules of gall-induction.

Galhas de insetos da Serra da Bandeira (Barreiras, Oeste da Bahia, Brasil)

Abstract Understanding the diversity of insect galls is pivotal to the establishment of conservation planning in different Brazilian ecosystems. Here, we (1) characterize the insect galls found on plant host species, (2) identify the gall-inducing insects to the lowest possible taxonomic level, and (3) record the presence of gall-associated fauna. Our study was carried out monthly from August, 2017 to July, 2018 along nine trails in Serra da Bandeira, which is located in an area of Cerrado stricto sensu over a year. We found 48 distinct gall morphotypes, belonging to 12 botanical families. The most morphotypes commonly found were globoid (27.1%), lenticular (27.1%) and cylindrical (25%). The plant organs most affected by galling insects were the leaves (73%), followed by the stem (19%), flower (4%), inflorescence (2%) and fruits (2%). The host botanical families holding the highest number of galls were Fabaceae (26), Malpighiaceae (5) and Anacardiaceae, Combretaceae and Euphorbiaceae (3). We observed that the genus Copaifera Lindl. (Fabaceae) had the greatest diversity of gall morphotypes, harboring 19 morphotypes distributed in three species that occur sympatrically - Copaifera sabulicola J. Costa (Fabaceae), Copaifera depilis Dwyer (Fabaceae) and Copaifera luetzelburgii Harms (Fabaceae). For the first time in Brazil, we recorded the occurrence of galls on flowers of Manihot caerulescens (Euphorbiaceae), on inflorescences of Mimosa acutistipula (Fabaceae) and flower buds of Anacardium humile (Anacardiaceae), which were induced by Cecidomyiidae. Inducers of the order Diptera (Family Cecidomyiidae) were the most abundant, found in 14 morphotypes of galls. Regarding the associated fauna, we found insects primarily belonging the order Hymenoptera, and identified them as parasitoids. The information provided can be used highly by decision makers for conservation programs, as well as in other strategies for the conservation of biological diversity in the Brazilian Cerrado.

Insect galls from the Botanical Garden of the Museu Nacional (Rio de Janeiro, RJ, Brazil).

The Botanical Garden of the Museu Nacional/Universidade Federal do Rio de Janeiro (Rio de Janeiro, RJ, Brazil) was investigated monthly from October, 2017 to December, 2019 in a total of 27 collections, each lasting four hours, following the methodology of random walking. Vegetative and reproductive organs of herbs, bushes and trees (up to 2 m high) were examined by two people. Voucher material was deposited in the Entomological Collection of the Museu Nacional (MNRJ)/Universidade Federal do Rio de Janeiro. We found 13 insect gall morphotypes in nine host plant species of four families. All host plants are native of Brazil, except Ficus microcarpa L.f. (Moraceae), which is naturalized. Myrtaceae and Moraceae were the plant families with the greatest richness of gall morphotypes. Eugenia L. (Myrtaceae) and Ficus L. (Moraceae) were the plant genera with the highest number of gall morphotypes. In several inventories in the Atlantic forest, Myrtaceae and Eugenia stand out for harboring a great variety of galls, while Moraceae and Ficus were never stood out for this reason. Most plant species mentioned in the present study were already known as hosts of gall-inducing insects in Brazil. However, for the first time, insect galls are reported on Ficus crocata (Miq.) Miq. (Moraceae). We found two new morphotypes on Eugenia florida DC. (Myrtaceae). Leaves, stems and buds were the galled organs. Cecidomyiidae were the most frequent inducers. Galls of Thysanoptera were also found. Inquilines were observed in leaf galls on Eugenia florida. They promoted differences in gall morphology and killed the gall-inducing larva.

Can Molecularly Engineered Plant Galls Help to Ease the Problem of World Food Shortage (and Our Dependence on Pollinating Insects)?

The world faces numerous problems and two of them are global food shortages and the dwindling number of pollinating insects. Plant products that do not arise from pollination are plant galls, which as in the case of oak apples, can resemble fruits and be the size of a cherry. It is suggested that once research has understood how chemical signals from gall-inducing insects program a plant to produce a gall, it should be possible to mimic and to improve nature and "bioengineer" designer galls of different sizes, colorations and specific contents to serve as food or a source of medicinally useful compounds. To achieve this objective, the genes involved in the formation of the galls need to be identified by RNA-sequencing and confirmed by gene expression analyses and gene slicing. Ultimately the relevant genes need to be transferred to naïve plants, possibly with the aid of plasmids or viruses as practiced in crop productivity increases. There is then even the prospect of engineered plant galls to be produced by plant tissue culture via genetic manipulation without the involvement of insects altogether.

New arthropod-Podostemaceae associations in Central and South America.

Podostemaceae are a unique family of aquatic angiosperms found in river rapids and waterfalls throughout southern Asia, Africa, and the Americas. Podostemaceae are understudied, and consequently, the arthropods associated with these plants are not well known. We sought to expand knowledge of arthropod-Podostemaceae associations to better understand the impact of these plants on aquatic ecosystems and biodiversity. We examined samples of Podostemaceae collected between 1998 and 2007 from Brazil, Costa Rica, Suriname, and Venezuela for arthropods even though these samples were not collected with the intent to investigate arthropod-Podostemaceae associations. We examined 15 samples of Podostemaceae, including 10 species never evaluated for arthropod associations, and found over 9000 arthropods representing 12 different orders. The most abundant orders were Diptera (77.88%), Trichoptera (12.90%), Coleoptera (3.35%), and Lepidoptera (2.42%). We found several arthropods not previously reported from Podostemaceae, including Collembola and Acari, documented several instances of insects boring into plant tissues, and provide the first report of an insect-induced gall on Ceratolacispedunculatum C.T. Philbrick, Novelo & Irgang.

Chemical Arms Race: Occurrence of Chemical Defense and Growth Regulatory Phytochemical Gradients in Insect-Induced Foliar Galls

Chemical Arms Race: Occurrence of Chemical Defense and Growth Regulatory Phytochemical Gradients in Insect-Induced Foliar Galls

Antimicrobial diterpene induced by two gall-inducing adelgids coexisting on Picea koraiensis.

The mechanism by which closely related species can coexist is a central factor in the stability of ecological communities. The larch adelgid (Adelges laricis laricis) and the eastern spruce adelgid (Adelges (Sacchiphantes) abietis) have both been found on the branches of Picea koraiensis in China. These two adelgids exhibit strong infectivity and readily induce the formation of 'fish scale-like' and 'pineapple-like' galls with branch parasitism rates of between 75.01±7.03 and 88.02±4.39%. Interestingly, the gall tissues in which these two gall-inducing insects were found to be coexisting were discovered at a rate of ~0.2% in the studied populations. The weight and number of gall chambers as well as the number of adelgids in the 'fish scale-like' side were higher than those in the 'pineapple-like' side. Furthermore, compared with the normal branches, a diterpene neoabietic acid was found at elevated concentrations in the gall tissues, with especially high concentrations seen in the tissues of the co-occupied galls. Neoabietic acid exhibited strong antibacterial activities against Bacillus spp. isolated from the branches of P. koraiensis, as well as potent antifungal activity against the hyphal growth of Fusarium graminearum JMY-1, which was obtained from the gall tissues. Our result provides evidence that the coexistence of the two closely related species could be explained by alterations of the host tissues by the insects resulting in increased concentrations of the antimicrobial agent.

Host Gall Size and Temperature Influence Voltinism in an Exotic Parasitoid

Insect phenology is highly temperature-dependent. Higher temperatures can lead to earlier emergence and lengthening of the active period, which enable many insect groups to complete more generations. Studies on the effects of climate change on insect populations are providing concerning evidence supporting this relationship. These kind of shifts in phenology and voltinism also occur in agricultural and forest insect pests and their natural enemies, with potential implications for biological control. The consequences derived from changing temperature regimes on tritrophic interactions remain poorly studied, particularly in gall-inducing insects and their parasitoids. Here we detail the occurrence of bivoltinism in the exotic parasitoid Torymus sinensis, previously categorized as univoltine, a widely introduced species to fight against the invasive Asian chestnut gall wasp Dryocosmus kuriphilus wherever this pest spread. This plasticity in voltinism has been observed in the southernmost European distribution of D. kuriphilus, and appears to be mediated by both temperature and gall traits, namely size or the number of gall chambers. Bivoltinism was most common at annual mean temperatures around 13.5°C and in galls with more chambers. Through this work, we intend to unravel the factors behind this phenomenon and discern the possible consequences on host-parasitoid interactions.

Cecidomyiidae (Diptera) in the State of Santa Catarina, Brazil

The first checklist of gall midges (Diptera: Cecidomyiidae) in the state of Santa Catarina (SC) is organized based on literature review. Species distribution, discussion regarding endemism, and a list of host plants in the state are provided for the first time. We compare the composition of cecidomyiid species with other states of Brazil. Twenty-three species of gall midges occur in SC, all gall-inducers. They are distributed in 14 genera, being Lopesia Rübsaamen, 1908 and Bruggmannia Tavares, 1906 the best represented. The most speciose genera of Cecidomyiidae in SC are among the most speciose in Brazil, so this result matches the Brazilian pattern. Cecidomyiids are associated with 18 host plant species distributed in 12 families. Although SC comprises a low percentage of the Brazilian fauna of Cecidomyiidae (8.7%), two species are known only from the state. The Sorensen`s index showed that the fauna of SC and São Paulo (SP) are the most similar to each other. The similarity of gall-inducing insects can be related to the host plant composition and phytogeographic domain.

Hidden Diversity-A New Speciose Gall Midge Genus (Diptera: Cecidomyiidae) Associated with Succulent Aizoaceae in South Africa.

Simple SummarySucculent Aizoaceae (often called “mesembs” or ice plants) form a dominant component of the Succulent Karoo in southern Africa, constituting one of the most species-rich families within the Greater Cape Floristic Region (GCFR). Despite the diversity and abundance of these plants, the diversity of insects specialized on them has never been surveyed methodically prior to this study. In a three-year study of the galling insects associated with succulent Aizoaceae in South Africa, we found that they support a rich community of gall midges (Diptera: Cecidomyiidae), virtually all of which are new to science. This is not surprising, given that knowledge of the Afrotropical fauna of gall midges is scarce, with most species described in the 1900s. Here, we describe the new genus Ruschiola with ten species from succulent Aizoaceae in Namaqualand, the Knersvlakte and the Cedarberg regions of South Africa based on morphological, molecular and life history data. The genetic data were particularly important in this study for differentiating taxa, given that Ruschiola species are very similar morphologically. Members of this genus develop in leaf galls or in plant tissues without visible gall formation, and are highly host specific.Aizoaceae (Caryophyllales) constitute one of the major floral components of the unique Greater Cape Floristic Region (GCFR), with more than 1700 species and 70% endemism. Within succulent Aizoaceae, the subfamily Ruschioideae is the most speciose and rapidly diversifying clade, offering potential niches for the diversification of specialized herbivorous insects. Nevertheless, insect diversity on these plants has not been studied to date, and knowledge of gall-inducing insects in the Afrotropics is generally scarce. Our recent observations indicate that succulent Aizoaceae in the GCFR support a rich and largely unstudied community of gall midges (Diptera: Cecidomyiidae). Here, we provide a first report of their diversity with a description of a new genus, Ruschiola Dorchin, and ten new species, based on morphological and molecular analyses of material collected during a three-year targeted survey across major GCFR vegetation types. A high degree of morphological uniformity in Ruschiola suggests recent diversification and necessitated the use of molecular data and laboratory rearing from host plants to verify species boundaries and host ranges.

Phenolic substances and cyanogenesis in galled and non-galled tissue of the fern species Microgramma vacciniifolia.

Galls, neo-formed plant structures that can occur in different organs, are generated by species-specific interaction with an inducing organism. Inducers manipulate the metabolism of its host. Microgramma vacciniifolia (Langsd. & Fisch.) Copel. is a Neotropical epiphytic fern that hosted two stem galls, one induced by a midge species (Diptera) and other by a micromoth species (Lepidoptera). The aim of this study was to evaluate the impact of these two gall-inducing insects on the biochemistry of phenolic acids and the cyanogenesis in galls, stems and leaves of M. vacciniifolia. High performance liquid chromatography (HPLC) indicated a total of 14 phenol derivatives, including caffeic and coumaric acid. Principal Coordinates Analysis (PCoA) of the phenolic substances indicated three groups consisting (1) non-galled stems and micromoth-induced galls; (2) midge-induced galls; (3) midge-induced galls with parasitoids. Regarding the frequency of cyanogenesis assessed by the picrate paper test, the chi-squared test showed significant difference between fertile leaves (8.3%), sterile leaves (27.7%), non-galled stems (0%) and galls. Among galls, only the midge-induced galls analyzed were cyanogenic (15%). Our results indicated that the different gall-inducers (midge and micromoth) promote species-specific alterations to the phenolic substance composition of the host fern.

Leaf Galls with the Same Morphology Induced on the Same Plant Species by Two Species of Latuspina (Hymenoptera: Cynipidae), with a Description of a New Species

A new species in the genus Latuspina (Hymenoptera: Cynipidae) that induces galls on the leaves of Quercus variabilis Blume (Fagaceae) in China is described here as Latuspina jinzhaiensis Abe, Ide, Su, and Zhu, new species. The sexual generation gall of the new species is indistinguishable from that produced by L. abemakiphila Ide and Abe, which is induced on leaves of the same oak species in Japan. However, these two cynipid species can be distinguished based on the morphological characteristics of the propodeum of adult wasps. Moreover, differences in the partial sequence of the mitochondrial cytochrome c oxidase subunit I (COI) gene (18–19 of 658 bp) supports the morphological distinction between these two species. Although congeneric gall-inducing cynipids, as well as other gall-inducing insects such as gall midges, can typically be distinguished based solely on gall characteristics (e.g., shape and position on the plant) and host plant species, these two Latuspina species are an exception. Since the asexual generations of both species are currently unknown, finding asexual generation galls and adults in the future is considered necessary.

Soils and seasonality influence the richness of gall-inducing insects and their host plants in a tropical dry forest

The richness of specialized herbivores and their host plants in a Brazilian dry forest was inventoried to evaluate if soil types and seasonality are important factors determining the composition of gall-inducing insects and their host plants in Caatinga environments on a local scale. This study recorded 12 different morphotypes of gall distributed among eight host species belonging to five botanical families. Both soils and seasonality influenced the number of species and individuals of host plant, and the richness of gall-inducing insect. The greatest richness of gall-inducing insects and their host plants was observed during the rainy season in the Caatinga vegetation on soils of sedimentary origin, which is considered to have low fertility as regards phosphorus content. Our results corroborate the hypothesis of soil fertility which predicts that the richness of gall-inducing insects will be higher on infertile soils and demonstrate the importance of substrate and seasonality for the richness of gall-inducing insects in Caatinga on a local scale.

Contribution to the knowledge of gall-inducing insects from Biskra province, Algeria

Contribution to the knowledge of gall-inducing insects from Biskra province, Algeria

Recent Progress Regarding the Molecular Aspects of Insect Gall Formation.

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 regarding the molecular aspects of insect gall formation.

Interactions Between Figs and Gall-Inducing Fig Wasps: Adaptations, Constraints, and Unanswered Questions

The ancient interaction between figs (Ficus, Moraceae) and their pollinating fig wasps is an unusual example of a mutualism between plants and gall-inducing insects. This review intends to offer fresh perspectives into the relationship between figs and the diversity of gall-inducing sycophiles which inhabit their enclosed globular inflorescences that function as microcosms. Besides gall-inducing pollinators, fig inflorescences are also inhabited by other gall-inducing wasps. This review evaluates the state of current knowledge on gall-induction by fig wasps and exposes the many lacunae in this area. This review makes connections between fig and gall-inducing wasp traits, and suggests relatively unexplored research avenues. This manuscript calls for an integrated approach that incorporates such diverse fields as life-history theory, plant mate choice, wasp sexual selection and local mate competition, plant embryology as well as seed and fruit dispersal. It calls for collaboration between researchers such as plant developmental biologists, insect physiologists, chemical ecologists and sensory biologists to jointly solve the many valuable questions that can be addressed in community ecology, co-evolution and species interaction biology using the fig inflorescence microcosm, that is inhabited by gall-inducing mutualistic and parasitic wasps, as a model system.

A new galling insect model enhances photosynthetic activity in an obligate holoparasitic plant

Insect-induced galls are microhabitats distinct from the outer environment that support inhabitants by providing improved nutrients, defence against enemies, and other unique features. It is intriguing as to how insects reprogram and modify plant morphogenesis. Because most of the gall systems are formed on trees, it is difficult to maintain them in laboratories and to comprehend the mechanisms operative in them through experimental manipulations. Herein, we propose a new model insect, Smicronyx madaranus, for studying the mechanisms of gall formation. This weevil forms spherical galls on the shoots of Cuscuta campestris, an obligate parasitic plant. We established a stable system for breeding and maintaining this ecologically intriguing insect in the laboratory, and succeeded in detailed analyses of the gall-forming behaviour, gall formation process, and histochemical and physiological features. Parasitic C. campestris depends on host plants for its nutrients, and usually shows low chlorophyll content and photosynthetic activity. We demonstrate that S. madaranus-induced galls have significantly increased CO2 absorbance. Moreover, chloroplasts and starch accumulated in gall tissues at locations inhabited by the weevil larvae. These results suggest that the gall-inducing weevils enhance the photosynthetic activity in C. campestris, and modify the plant tissue to a nutrient-rich shelter for them.

Sensory gene identification in the transcriptome of the ectoparasitoid Quadrastichus mendeli

Sensory genes play a key role in the host location of parasitoids. To date, the sensory genes that regulate parasitoids to locate gall-inducing insects have not been uncovered. An obligate ectoparasitoid, Quadrastichus mendeli Kim & La Salle (Hymenoptera: Eulophidae: Tetrastichinae), is one of the most important parasitoids of Leptocybe invasa, which is a global gall-making pest in eucalyptus plantations. Interestingly, Q. mendeli can precisely locate the larva of L. invasa, which induces tumor-like growth on the eucalyptus leaves and stems. Therefore, Q. mendeli–L. invasa provides an ideal system to study the way that parasitoids use sensory genes in gall-making pests. In this study, we present the transcriptome of Q. mendeli using high-throughput sequencing. In total, 31,820 transcripts were obtained and assembled into 26,925 unigenes in Q. mendeli. Then, the major sensory genes were identified, and phylogenetic analyses were performed with these genes from Q. mendeli and other model insect species. Three chemosensory proteins (CSPs), 10 gustatory receptors (GRs), 21 ionotropic receptors (IRs), 58 odorant binding proteins (OBPs), 30 odorant receptors (ORs) and 2 sensory neuron membrane proteins (SNMPs) were identified in Q. mendeli by bioinformatics analysis. Our report is the first to obtain abundant biological information on the transcriptome of Q. mendeli that provided valuable information regarding the molecular basis of Q. mendeli perception, and it may help to understand the host location of parasitoids of gall-making pests.