Gall Maker Research Articles

Galls as habitats: the inquiline communities of insect galls

Gall makers can be considered microhabitat engineers, because their galls provide both a food resource and a habitat that can be exploited by herbivorous and omnivorous organisms that do not feed on the galling insect. We compiled literature data on inquilines of insect-induced galls for 112 galler systems in order to examine physiological, ecological and taxonomic patterns of diversity. We measured inquiline species richness two ways, first as the number of inquiline species/number of natural enemy species + inquiline species for each system in order to attain a measure of relative diversity that was free of sampling bias across different systems, and second as the total number of species. A taxonomic list of gall systems containing inquilines is presented. We conducted quantitative analyses on the following independent variables: host plant architecture, latitude, gall size, gall type and gall maker taxon. Inquiline diversity was significantly correlated only with host plant architecture and latitude; galls on trees support the richest inquiline communities, and inquiline diversity is highest in the temperate zone. However, the relative paucity of inquiline data in the literature is reflected in our results, thus highlighting the need for further study on organisms that are potentially as important a component of galler communities as predators and parasitoids.

Insects on common reed ( Phragmites australis): community structure and the impact of herbivory on shoot growth

In this paper, community structure of endophagous insects attacking common reed ( Phragmites australis (Cav.) Trin ex Steud.) and impact of herbivory on shoot growth was analyzed in south west Germany. All the 26 phytophagous insects were monophagous, i.e. restricted to their host plant P. australis, which appeared to be due to the predictability and apparency of the large and ancient Phragmites stands. Habitat types were clearly separated due to the mean shoot diameter (‘dry’ and ‘wet’ reed) and the mean level of shoot damage (high and low abundance of Archanara shoots). The stem-boring moth Archanara geminipuncta greatly influenced structure of the insect community, due to heavy shoot damage, and could be classified to be the key species of the reed ecosystem. In contrast to common expectations of negative effects, Archanara shoot damage enhanced populations of many insect species, so insect guilds of ‘primary attackers’ (on the main shoot) and ‘secondary attackers’ (on damaged shoots) could be separated. Primary attackers either killed the growing point or attacked the apical, medium or basal internodes, while secondary attackers were facilitated by shoot damage and could also be subdivided in four guilds: Inquilinous species living between the wilting leaves of damaged shoots, attackers of the side shoot growing in response to the destruction of apical meristems, saprophagous species feeding on Archanara droppings, and the successor community of bees and wasps nesting in empty galls or broken shoots. There is a continuum from evident plant damage, e.g. by stem-boring moths and leaf-sucking aphids, to enhanced shoot growth due to the parasitic influence of gall makers, e.g. the significant shoot elongation by the gall midge Giraudiella inclusa. In Europe, conservationists are concerned about the die-back of P. australis, while in North America and Australia, P. australis is considered to be an invasive weed. Classical biological control with the introduction of European insects (like the moth A. geminipuncta) is discussed.

Espécies cecidógenas (Diptera, Cecidomyiidae) e parasitóides (Hymenoptera) associadas a Guapira opposita (Vell.) Reitz: (Nyctaginaceae) na Restinga da Barra de Maricá, Rio de Janeiro

Three different galls of Bruggmannia spp. (Diptera, Cecidomyiidae) on Guapira opposita (Vell.) Reitz. (Nyctaginaceae) were studied at Restinga of Barra de Marica, State of Rio de Janeiro. Thirty parasitoid species are associated to these galls. Most of them is generalist and solitary. Hyperparasitoidism is common. The trophic relations among gall makers and parasitoids are presented.

Insect communities of Phragmites habitats used for sewage purification: Effects of age and area of habitats on species richness and herbivore-parasitoid interactions

In 1994, 28 sewage purification plants based on common reed Phragmites australis were analyzed, to study fragmentation effects on diversity and on food web structure of insect communities. Purification plants differed in age (2 to 11 years) and area (10 to 2,500 m 2). Both age and area were significantly correlated with species richness of herbivores. Populations of the two most abundant herbivores, the gall makers Lipara pullitarsis (Diptera, Chloropidae) and Giraudiella inclusa (Diptera, Cecidomyiidae), increased significantly with age and size of the Phragmites habitats, i.e. the purification plants. Incidence curves showed that only habitats older than 6 years and larger than 100 m 2 have a 50% probability of finding these two most abundant gall makers, and can correspondingly be considered to contribute to insect species conservation. Natural enemies were even more susceptible to habitat fragmentation than their phytophagous hosts or prey, thereby hampering possible biocontrol. Percent parasitism of both the Lipara and Giraudiella gall makers significantly increased with habitat age.

The gall maker Neopelma baccharidis Burck. (Homoptera:Psyllidae) on Baccharis dracunculifolia DC. (Asteraceae): individual, local, and regional patterns

Baccharis dracunculifolia, the host plant of the gall maker Neopelma baccharidis Burck., is locally distributed in delimited patches. The effects of the host plant individual (plant height, crown diameter, and crown volume), local (host plant patch), and regional (locality) characteristics on the number of galls were analyzed, in Viçosa (three patches) and in Rio Doce State Park, Marliéria (two patches), Minas Gerais State (20°45'S, 42°50'W; and 19°50'S, 42°30'W, respectively). The number of galls/individual plant increased homogenousliy with plant dimensions on local and regional scale. Gall load was also homogenous, but the proportion of galled plants differed on a local scale. The differences were related to local plant size differences, and not to host plant patch size. Plants without galls presented different frequency distributions of plant dimensions than galled plants, with greater number of little plants, which indicated a minimum plant size to be gall maker prone. Local factors prevailed over regional factors in determining the number of N. baccharidis galls on 5. dracunculifolia, affecting the size of individual plants and suitability to the gall maker, without modifying the relationship between gall load and plant dimensions.

Gall Makers on Flowers of Cuphea (Lythraceae)

Enlarged or deformed floral tubes of the herbaceous perennial plant genus Cuphea have been noted by many collectors but without knowledge of the causative agent. A survey of herbarium collections of Cuphea found enlarged, thickened or inflated, sometimes exceptionally hairy flowers present in nine species from Mexico, Guatemala, Costa Rica, Panama, and Ecuador. Investigation determined the enlargements were due to two different gall-forming parasites. Cuphea appendiculata, C. cyanea, C. hookeriana, C. llavea, C. nitidula, and C. spectabilis in the dosely related sections Diploptychia, Heterodon, and Leptocalyx are hosts to Asphondylia sp. (Diptera: Cecidomyiidae), a gall midge. Asphondylia is notable for its apparent symbiotic relationship to fungi which grow in the gall. Cuphea bombonasae, C. epilobiifolia, and C. spraguei, of section Heteranthus, are parasitized by Mompha sp. (Lepidoptera: Momphidae), a microlepidopteran that feeds on the reproductive organs of the flower. These are the first records of gall-forming genera parasitizing the Lythraceae and are new host records for the insects. Flowers infected by either parasite produce no seeds. However, the number of infected vs. non-infected plants is relatively low (14% gall midge infection in C. cyanea and 22% Mompha sp. infection in C. epilobiifolia), and among the multi-flowered inflorescences of any plant, at least 80 percent of the flowers remain free of galls, suggesting the gall makers strike a balance in their parasitism that does not excessively threaten the plant species on which it depends.

Chaves para classificação de galhas de Cecidomyiidae (Diptera) em Myrtaceae na Restinga da Barra de Maricá, Rio de Janeiro

Keys to Cecidomyiidae galls occuring on Myrtaceae by genus of the host plant, in alphabetical order, are presented. Data on gall makers, predators and inquilinous species are given, as well as illustrations of the galls.

Fungal endophytes which invade insect galls: insect pathogens, benign saprophytes, or fungal inquilines?

Fungi are frequently found within insect galls. However, the origin of these fungi, whether they are acting as pathogens, saprophytes invading already dead galls, or fungal inquilines which invade the gall but kill the gall maker by indirect means, is rarely investigated. A pathogenic role for these fungi is usually inferred but never tested. I chose the following leaf-galling-insect/host-plant pairs (1) a cynipid which forms two-chambered galls on the veins of Oregon white oak, (2) a cynipid which forms single-chambered galls on California coast live oak, and (3) an aphid which forms galls on narrowleaf cottonwood leaves. All pairs were reported to have fungi associated with dead insects inside the gall. These fungi were cultured and identified. For the two cynipids, all fungi found inside the galls were also present in the leaves as fungal endophytes. The cottonwood leaves examined did not harbor fungal endophytes. For the cynipid on Oregon white oak, the fungal endophyte grows from the leaf into the gall and infects all gall tissue but does not directly kill the gall maker. The insect dies as a result of the gall tissue dying from fungal infection. Therefore, the fungus acts as an inquiline. Approximately 12.5% of these galls die as a result of invasion by the fungal endophyte.

Vertebrate Herbivores as Predators of Insect Herbivores: An Asymmetrical Interaction Mediated by Size Differences

We have analysed the effect of wild goat (Capra pyrenaica) on the reproductive success of a chalcid gall maker (Systasis encyrtoides), both species being herbivores of Hormathophylla spinosa, a stunted mediterranean high-mountain shrub. The gall's position on H. spinosa is very specific, reflected in the fact that the gall maker attaches principally to the basal floral buds of the inflorescence, and in the lower sector of the plant. We labelled inflorescences with and without galls in order to quantify goat herbivory and gall predation

Life History and Parasites of Asphondylia borrichiae (Diptera: Cecidomyiidae), a Gall Maker on Borrichia frutescens

We studied the life history, seasonal and spatial abundance, and parasites of Asphondylia borrichiae Rossi and Strong (Diptera: Cecidomyiidae), a newly described gall maker on sea oxeye daisy, Borrichia frutescens (L.) DC. Galls are located on the apical meristem of the host plant, are usually solitary, often prevent flowering, and can kill the host stem. Individual galls may contain from one to eight fly larvae, most commonly one to three. Gall size is greatest in spring. Galls can be found year round, and there are several generations, of which the largest occurs in the summer. Gall densities differ consistently between sites, but the seasonal variation of galls within sites is very similar. Fly larvae in galls are attacked by four species of Hymenoptera, Rileya cecidomyiae and Tenuipetiolus teredon (Eurytomidae), Torymus umbilicatus (Torymidae), and Galeopsomyia haemon (Eulophidae), of which G. haemon causes the most mortality. At least two of the parasites are facultatively hyperparasitic. Parasitism levels are low in the spring but rise quickly to reach 100% in the early summer and late fall.

Survivorship, Life History, and Concealment: A Comparison of Leaf Miners and Gall Formers

During the critical immature stages, folivorous insects exhibit different levels of concealment, which may affect their overall survival and success. I tested this proposition by comparing the survivorship of gall makers with that of leaf miners, which have similar life histories but do not produce galls. Final mortalities did not in fact differ between the two guilds, but the mortality of leaf miners was lower before the mid-larval stage, producing Type I and/or Type II survivorship. Gall formers approached Type III survivorship. Hypotheses are proposed for the divergence. Other life-history traits co-varied with survivorship pattern in the expected manner, except for generation time, which was longer for gall formers. The latter is attributed to constraints arising from the substrate requirements for gall formation and likely contributes to the similar final mortalities in the two guilds. Fast development in leaf miners and galling in the gall formers may be viewed as alternative, roughly equivalent but mutually exclusive strategies for reducing mortality. It is misleading to view one strategy as better than another; rather, each feeding type has its advantages and disadvantages, and the balance of these determines the relative success of that type for a given habitat.

MEASURING SELECTION ON REACTION NORMS: AN EXPLORATION OF THE EUROSTA-SOLIDAGO SYSTEM.

The sensitivity of genotypic expression to the environment can be depicted as the reaction norm, which is defined as the array of phenotypes produced by a single genotype over a range of environments. We studied selection on reaction norms of the gall-inducing insect Eurosta solidaginis (Diptera; Tephritidae), which attacks tall goldenrod Solidago altissima (Compositae). Gall size was treated as a component of insect phenotype and attributes of the host plant as environmental influences on gall development. Genetic differences in the response of gall size to plant lag time (the number of days before a plant responds to the gall maker) were examined. Reaction norms for full-sib families of flies were quantified as linear functions; the elevation of the function denoted gall size produced by the family averaged across all plants, and the function's slope denoted family sensitivity to lag time. Expected fitness of each family was regressed over reaction norm elevation and slope to yield selection gradients on these reaction norm parameters. Directional selection on gall size averaged across environments is four times stronger than selection on sensitivity. Yet, genetic variation for sensitivity contributes more than twice as much to gall phenotypic variance as family mean gall size. Our results suggest that selection on environmental sensitivity will be weak for populations restricted to a narrow segment of an environmental gradient, but strong for broadly distributed species.

Attack by a Stem-Boring Moth Increases Susceptibility of Phragmites Australis to Gall-Making by a Midge: Mechanisms and Effects on Midge Population Dynamics

The role of plant stress and shoot damage in the population dynamics of a grassinhabiting gall maker was assessed in the field. Four generations of Giraudiella inclusa (Diptera, Cecidomyiidae), developing in grain-like galls inside the internodes of common reed Phragmites australis, were sampled from nine habitats in northern West Germany from 1981 to 1984. Thin shoots of dry reed, stressed by water and nutrient deficiency, contained less silicate, caused less mortality of gall-inducing first instar larvae and had higher gall abundance than thick and intact shoots of wet reed. Thick shoots damaged by the stem-boring moth Archanara geminipuncta (Lepidoptera, Noctuidae) developed narrow side shoots that were highly susceptible to attack of the 2nd to 4th midge generation, thereby causing an increase of egg survival and gall abundance. Such facilitation among herbivores is a poorly known type of food web interaction. Differentiation between dry and wet reed and number of side shoots m-2 explained 92% of the variation of midge gall abundance between habitats and years. Availability of susceptible food, easily measurable by shoot characters, was the key factor in midge population dynamics.

The evolution of gall parasitism accompanied by a host shift in the gall aphid, Eriosoma yangi (Homoptera: Aphidoidea)

Eriosoma aphids form leaf-roll galls on various elm species. Eriosoma yangi occurring on the Japanese elm is an obligatory “cuckoo” parasite, invading and usurping galls of other Eriosoma species. But another host race of E. yangi induces its own galls on the Chinese elm. Multivariate morphometries show that the two host races differ significantly in quantitative characters. Overwintering eggs of the parasitic form were experimentally transferred to the Chinese elm. The resultant larvae still exhibited a parasitic habit and developed into adults, which multivariate morphometries classified as the parasitic form. This form is considered different enough from the gall maker to be given a species rank. Eriosoma aphids facultatively invade other Eriosoma galls, where they sometimes deposit offspring. It is hypothesized that the parasitic form on the Japanese elm originated from a founder population which had migrated from the Chinese elm. On this new host, only those fundatrices that invade other species' galls will be able to leave offspring, because aphid fundatrices cannot gall plants other than their primary hosts. It is assumed that the parasitic form was established under intense selective pressure following a population bottleneck. This hypothesis was corroborated by field investigations at sites where the two forms occur sympatrically.

Variability of the grass Phragmites australis in relation to the behaviour and mortality of the gall-inducing midge Giraudiella inclusa (Diptera, Cecidomyiidae)

Variability within and between shoots of the grass Phragmites australis proved to be important for both survival (successful gall induction) and reproduction (larval weight) of the gall-inducing midge Giraudiella inclusa. The ovipositing females and the migrating first instar larvae chose a predictable microhabitat within shoots and within internodes characterized by a high nutritional quality (nitrogen, mineral content, sugar, water) and reduced palnt defense properties (silicate). Clutch size increased with the shoot diameter, larval scramble competition could not be detected. Female shoot selection was random, although the chances of successful gall induction greatly differed between shoots. Thick and intact shoots (≥6 mm) led to a high larval mortality. But thick shoots destroyed apically by stem-mining caterpillars (of the noctuid moth Archanara geminipuncta) had on average large gall clusters. Accordingly, the adjustment of the clutch size to the shoot diameter resulted in an advantage for the gall midge females only when shoots were thin and short (i.e. stressed by water and nutrient deficiency) or heavily damage (i.e. stressed) by caterpillars. Thus, the monophagous gall maker G. inclusa did not compensate for all features of intershoot variation of P. australis, although grasses are well-known for their simple plant architecture and their low diversity and low concentration of secondary compounds.

Reactive Plant Tissue Sites and the Population Biology of Gall Makers

Plant galls, one of the great curiosities of the insect world, have fascinated naturalists from the time of Theophrastus (57). A century ago, the debate over natural selection briefly focused on insect-induced galls because, according to Romanes (51), they seemed to be , .. the one and only case in the whole range of organic nature where it can be truly said that we have unequivocal evidence of a structure occurring in one species for the exclusive benefit of another. Earlier, Darwin (18) had admitted that if any such case were uncovered it would annihilate his theory. However, Romanes saw an explana­ tion for galls that was consistent with the emerging evolutionary orthodoxy; although direct selection on the plant cannot lead to the evolution of galls, ... natural selection may operate to this end on the plants indirectly through the insect, viz. by always selecting those individual larvae the character of whose excitatory emanations is such as will best cause the plant to grow the kind of morphological abnormality that is required (51). In the present day it is appreciated that selection acts on gall makers to manipulate host-plant development (19, 37, 63) for nutritiOn and for protection from both the physical environment and some natural enemies (1, 45, 63). The evolution of the plant-gall maker interaction is complicated by the fact that galls are phenotypic entities that develop under the influence of both plant and insect genotypes (Figure 1). From the plant's perspective, the gall is a developmental abnormality, induced by an environmental stimulus, i.e. the insect. When viewed from the insect's perspective, the gall is a phenotypic

Evolution of Host-Plant Manipulation by Gall Makers: Ecological and Genetic Factors in the Solidago-eurosta System

Plant galls are growth deformities that feed and house the larvae of specialized insect species and other organisms (nematodes, bacteria, fungi, etc.). The benefits derived by the insect from its interaction with the host plant suggest that gall-making ability is an adaptive trait of the insect subject to modification by natural selection. Our findings, that variation in gall phenotype influences insect fitness and that gall phenotypic variation is affected by genetic variation in the insect population, support this interpretation. Our study of the goldenrod gall fly, Eurosta solidaginis, shows that gall size variation results from genetic variation among flies despite selective pressures by natural enemies. Eurosta larvae that produce small galls are vulnerable to the attack of parasitoid wasps, whereas those producing large galls are more prone to attack by avian predators. In this study population, parasitoid attack was more intense; hence, a net upward selective pressure was exerted. Quantitative-genetic methods were used in a greenhouse experiment to evaluate the contribution of insect genetic variance to phenotypic variation in gall size. Significant differences in gall diameter were found among full-sib families of gall makers. Gall dimensions were genetically correlated with one another at most developmental stages. Observations of galls growing on goldenrod clones in both the field and the greenhouse suggest that plant genotype also influences gall phenotype, and thus affects gall-maker vulnerability to natural enemies.

Potential Selective Pressures by Parasitoids on a Plant‐Herbivore Interaction

The potential role of the third trophic level in the evolution of plant—herbivore relationships was examined in the case of the goldenrod Solidago altissima, and the fly Eurosta solidaginis, which forms a round stem gall. Previous observation had shown that galls attacked by parasites are significantly smaller than those in which the gall maker survives. Two different mechanisms could cause such as pattern: parasite attack could occur before galls reach full size and the attacks could cause early cessation of growth, or attack could occur after galls reach their mature size, but with inherently small galls being more prone to attack. In the first instance, parasite attack would diminish the cost of the gall to the plant, and thus favor plant genotypes that facilitate parasites. In the second instance, parasites would exert selection pressure on the gall marker to induce larger galls. Monitoring of marked plants in the field, and field experiments in which parasites were excluded from gall—bearing plants except during controlled periods, showed that parasite attack does not stop gall growth. The parasitoid wasp Eurytoma gigantea is limited to attacking small galls because of the limited reach of its ovipositor. This created a selection intensity of 0.50, favoring Eurosta that induce larger galls. Evolutionary response to selection could be realized directly through change in the gall marker's stimulus ability, or less directly through phenological changes. Plant activity to the gall marker declined with plant age, so that late—starting galls were more vulnerable to parasite attack.

On the developmental morphology of the rosette galls ofAcacia leucophloea Willd., (Mimosaceae) induced byThilakothrips hablu Ramk. (Thysanoptera: Insecta)

Thilakothrips babuli induces rosette (artichoke) galls on the axillary buds ofAcacia leucophloea. As a result of feeding by the building populations of thrips, axillary shoot meristems are destroyed, and primordial palisade tissues of the leaflets and cortical tissues of the shoot axis are transformed into nutritive cells of specialised morphology. Very similar to the galls induced by mites, midges, chalcids, and chloropids,Thilakothrips-inducedAcacia galls also have a characteristic morphology, involving the inhibition of elongation of the shoot axis and crowding of maldeveloped leaflets. While describing the cecidogenesis in relation to the biology of the gall maker, an attempt has been made to discuss the morphological convergence among shoot apex galls.

The Diversity of Overwintering Strategies Utilized by Separate Populations of Gall Insects

The variability of overwintering strategies of four insect species occupying identical hibernacula are compared over two climatic regions. Stepwise acclimation was accomplished over a 12-week "seasonal" cycle between 5, -40, and 20 C. The ball gall hibernaculum of Solidago sp. provides a minimal thermal buffer to its inhabitants. Separate populations of the gall maker Eurosta solidagensis demonstrate markedly different adaptive strategies during acclimation. Low temperature exposure results in an elevation of supercooling points (SCPs) in northern populations so that early freezing occurs. Southern populations depress the SCP upon similar exposures to avoid tissue-freezing encounters. The SCPs become synchronous between populations when ambient temperatures are reduced below the supercooling limit (-20 C). Warm acclimation is characterized by a major depression in the SCP in both populations. However, the temperature trigger has been shifted to higher temperatures in northern species (>5-< 20 C vs. >0-< 5 C for southern groups). Three other species overwinter in the gall: Mordellistena unicolor, a coinhabitant with E. solidagensis, and Eurytoma obtusiventris and Eurytoma gigantea, two predators. Each of these species have distinct overwintering strategies.