Stem galls affect oak foliage with potential consequences for herbivory

Abstract.   1. On two dates, foliar characteristics of pin oak, Quercus palustris , infested with stem galls caused by the horned oak gall, Callirhytis cornigera , were investigated, and the consequences for subsequent herbivory assessed.
2. Second-instar caterpillars of the gypsy moth, Lymantria dispar , preferred foliage from ungalled trees.
3. Ungalled trees broke bud earlier than their galled counterparts.
4. Galled trees produced denser leaves with higher nitrogen and tannin concentrations, but foliar carbohydrates did not differ among galled and ungalled trees.
5. Concentrations of foliar carbohydrates in both galled and ungalled trees increased uniformly between the two assay dates. Nitrogen concentrations were greater in leaves from galled trees, and decreased uniformly in galled and ungalled trees over time. Foliar tannins were also greater in foliage from galled trees early in the season; however, foliar tannins declined seasonally in galled tissue so that by the second assay date there was no difference in tannin concentrations between galled and ungalled foliage.
6. In spite of differences in foliar characteristics, performance of older, fourth instar gypsy moth caterpillars did not differ between galled and ungalled trees.     

Arthropod-induced neoplastic formations on trees change photosynthetic pigment levels and oxidative enzyme activities

Abstract

In order to test the hypothesis that arthropod-induced neoplastic formations on trees affect biochemical characteristics of both the newly formed galls and host plant tissues, biochemical characteristics with a possible adaptive role were determined in nine gall-former–host tree combinations. Photosynthetic pigments, extractable protein content, and oxidative enzyme activities were determined in gall tissues, leaf tissues of galled leaves, and leaves on ungalled tree branches. Neoplastic tissues were characterized by a low content of photosynthetic pigments, decreased chlorophyll a/b ratio, lower extractable protein content, and decreased activities of peroxidase and polyphenol oxidase as compared with ungalled host leaf tissues. In galled leaves or in leaves adjacent to galls, increased level of peroxidase activity was found. In several gall-inducer–host plant combinations, galled host plant tissues contained increased activity of polyphenol oxidase as well. The presented data reflect long-term systemic effects of neoplastic formation on host tree physiology suggesting that gall inducers affect potential adaptive responses of host plants.     

Phytohormones Related to Host Plant Manipulation by a Gall-Inducing Leafhopper

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 (GA₁ and GA₄) than ungalled maize leaves. Leafhopper treatment significantly increased ABA and tZ contents and decreased GA₁ and GA₄ 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.     

Physiological Responses of Gall Tissues on Ivy Tree Leaves Induced by Thrip

In this research, tuber like galls which induced by thrip on ivy tree leaves were chosen as materials, and the physiological responses as well as partitioning of mineral nutrition, soluble protein and saccharide contents in galled and un galled tissues were assayed. Results indicated that compared to the un galled tissues, galling tissues decreased in many physiological indexes including hydrogen peroxide concentration, Peroxidase and phenylnine amonialase activities and the contents of malondialdehyde. Galling tissues decreased in photosynthetic rate but increased in respiratory rate. Galling tissues acted as a nutritive sink that accumulate more nutrition than surrounding un galled tissues. Phytohormones and insects extracts alone can not induce the formation of galls, but cytokinins such as kinetin, 6 BA and Zeatin can induce responses which are similar to the earlier response of thrip feeding.     

Qualitative and Quantitative Evaluation of Gall Induced by <Emphasis Type="Italic">Pseudophacopteron alstonium</Emphasis> Yang et Li 1983 (Hemiptera: Psyllidae: Phacopteronidae) as Plant Parasite,in <Emphasis Type="Italic">Alstonia scholaris</Emphasis> Leaves

Alstonia scholaris (Dr C. Alston, 1685–1760) (Family Apocynaceae) (Chattim tree), commonly known as devil tree, is an evergreen tropical tree. The tree is native to India and also found in Sri Lanka, Southern China, throughout Malaysia to northern Australia. This plant is seriously damaged by formation of tumor like galls across the Kolkata city,West Bengal which affects its ornamental and medicinal value. Gall is formed by ovipositing adults of Pseudophacopteron alstonium Yang et Li 1983 (Hemiptera: Psyllidae: Phacopteronidae) and results in destruction of host plant. The nymphal stage undergoes moulting through first instar to third instar to reach the adult within galls. It is observed that highly infested leaves can bear 60–80 galls. The gallmaker Pseudophacopteron sp. stresses the host organ, and the host counters it with physiological activities supplemented by newly differentiated tissues. In infested leaves, chlorophyll and carbohydrate contents decreased sequentially with the age of the gall. There were no significant changes in protein and total amino acid content in gall tissue. But total lipid content was highest in mature galled leaves. Increased phenolic content after psylloid herbivory, which exerted oxidative stress on the host plants, was observed in gall infested leaves as compared to fresh ungalled leaves of Alstonia scholaris. Moisture content was highest in ungalled healthy leaves than the young galled, mature galled and perforated galled leaves.     

Manipulation of food resources by a gall-forming aphid: the physiology of sink-source interactions

Summary We examined the capacity of the galling aphid, Pemphigus betae, to manipulate the sink-source translocation patterns of its host, narrowleaf cottonwood (Populus angustifolia). A series of ¹⁴C-labeling experiments and a biomass allocation experiment showed that P. betae galls functioned as physiologic sinks, drawing in resources from surrounding plant sources. Early gall development was dependent on aphid sinks increasing allocation from storage reserves of the stem, and later development of the progeny within the gall was dependent on resources from the galled leaf blade and from neighboring leaves. Regardless of gall position within a leaf, aphids intercepted ¹⁴C exported from the galled leaf (a non-mobilized source). However, only aphid galls at the most basal site of the leaf were strong sinks for ¹⁴C fixed in neighboring leaves (a mobilized source). Drawing resources from neighboring leaves represents active herbivore manipulation of normal host transport patterns. Neighboring leaves supplied 29% of the ¹⁴C accumulating in aphids in basal galls, while only supplying 7% to aphids in distal galls. This additional resource available to aphids in basal galls can account for the 65% increase in progeny produced in basal galls compared to galls located more distally on the leaf and limited to the galled leaf as a food resource. Developing furits also act as skins and compete with aphid-induced sinks for food supply. Aphid success in producing galls was increased 31% when surrounding female catkins were removed.     

Patterns of gall-forming in Ossaea confertiflora (Melastomataceae) by Lopesia brasiliensis (Diptera: Cecidomyiidae) in an area of Atlantic Rainforest in southeastern Brazil

Patterns of galling by the gall midge Lopesia brasiliensis (Diptera: Cecidomyiidae) were studied in Ossaea confertiflora (Melastomataceae) in an Atlantic forest site at Ilha Grande, RJ. Out of the 81 plants surveyed, 55 (67.9%) bore galls. The number of galls per galled individual ranged from 1 to 261 and 94.4% of the galls were in leaves. The number of galls per galled leaf varied from 1 to 25. Total gall number was positively correlated with plant height. Larger and more ramified plants tended to have a smaller percentage of their leaves with galls and a lower density of galls per leaf than smaller plants. Plants that were close to other individuals of the same species tended to have more galls per leaf than relatively isolated plants. The observed patterns may be linked to strategies of optimization in the use of resources (i.e. oviposition sites) and predation avoidance by the gall midges.     

The effect of galling aphids feeding on photosynthesis photochemistry of elm trees (<Emphasis Type="Italic">Ulmus</Emphasis> sp.)

Changes of chlorophyll (Chl) a fluorescence and photosynthetic pigment contents were analysed in galled leaves (visibly damaged and undamaged parts) and intact leaves. The values of minimal fluorescence of the dark-adapted state, maximal quantum yield of PSII photochemistry, effective quantum yield of PSII photochemical conversion, and photochemical quenching coefficient decreased in Ulmus pumila L. leaves galled by Tetraneura ulmi (L.) and in U. glabra Huds. galled by Eriosoma ulmi (L.). Colopha compressa (Koch.) feeding affected these parameters only in damaged parts of U. laevis Pall. galled leaves. The increasing number of T. ulmi galls progressively decreased photosynthetic performance. In gall tissues of all analysed aphid species, the lowest photosynthetic pigment content was found, indicating that the photosynthetic capacity must have been low in galls. Significant reduction of Chl and carotenoid contents were observed in damaged and undamaged portions of galled leaves only in the case of T. ulmi feeding.     

The number of cecidomyiid insect galls affects the photosynthesis of Machilus thunbergii host leaves

Previous studies of the impacts of galls on host leaf photosynthesis do not suggest any general trends, with a reported range of effects from negative to positive. In this study, photosynthetic characteristics such as chlorophyll fluorescence (Fv/Fm), photosynthetic capacity, and stomata conductance were determined in two types of fruit-like galls (red ovoid and green obovate galls) induced by Daphnephila taiwanensis and Daphnephila sueyenae, respectively, in order to investigate whether the number of galls affects the photosynthesis of galled leaves of Machilus thunbergii. In 2008, chlorophyll fluorescence and photosynthetic capacity were negatively correlated with gall numbers, non-significantly and significantly, respectively, whereas stomata conductance was positively but non-significantly correlated with gall numbers. In 2009, photosynthesis capacity and stomata conductance were negatively, but non-significantly, correlated with gall numbers. Results imply that photosynthesis in M. thunbergii leaves is slightly affected by the number of cecidomyiid insect galls, and that the higher the gall number, the greater the negative effect that galls have on host leaf photosynthesis and subsequent infection.     

Effect of gall formation by a cynipid wasp, Andricus symbioticus, on the development of the leaves and shoots of Quercus dentata

The sexual generation of a cynipid wasp, Andricus symbioticus Kovalev, forms its leaf galls most frequently near and on the leaf petiole of Quercus trees. I examined the effect of gall formation by A. symbioticus on the leaf development of a host plant, Quercus dentata Thunberg, by comparing the size and shape of galled and ungalled leaves. I also examined the effect of gall formation on shoot development by comparing the length of shoots with and without galled leaves. Three of seven Q. dentata trees surveyed were heavily infested with A. symbioticus. Leaf size did not differ between galled and ungalled leaves. However, the ratio of leaf width to length was greater in galled leaves, which is regarded to be a result of gall formation by A. symbioticus inhibiting the growth in length of Q. dentata leaves. Shoot length did not differ significantly between shoots with and without galled leaves. These results suggest that galls of A. symbioticus act as a sink that competes with leaves for reserved photoassimilates.     

Histocytological aspects of four types of ambrosia galls on Machilus zuihoensis Hayata (Lauraceae)

Four types of prosoplasmatic galls induced by Daphnephila midges are found on leaves of Machilus zuihoensis, a species endemic to Taiwan: urn- and small urn-shaped, obovate, and hairy oblong galls. In addition to containing nutritive tissues, these galls are lined with fungal hyphae. The objective of this study was to describe and compare the structural organization of the various gall morphologies and to examine the ultrastructure of the nutritive and fungal cells lining the gall chambers. The morphology and ultrastructure of mature-stage galls were examined by light, scanning electron, and transmission electron microscopy. Diverse epidermal cell shapes and wax textures were observed in the leaves and galls of M. zuihoensis. In small urn-shaped, obovate, and hairy oblong galls vascular bundles extend from the gall base to near the centre of the gall top. In contrast, vascular bundles in urn-shaped galls are distributed in the gall wall and extend to close to the outer gall top. Trichomes were present only abaxially on leaves and on hairy oblong gall surfaces. Starch granules, tannins, and mucilage were distributed differently among the four gall types. Further, fungal mycelia spread in the interior gall wall and partially passed through the intercellular spaces of nutritive cells and reached the sclerenchyma. Histological analyses revealed that the surface structure of galls differs from that of the leaf and that the epidermal organization differs among the four gall types. Different types of leaf galls on the same plant have different patterns of tissue stratification and contain different ergastic substances. The results of this study will contribute to the understanding of tritrophic relationships and the complex interactions among parasitic gall-inducing insects, mutualistic fungi, and host plants.     

The chemical composition of plant galls: are levels of nutrients and secondary compounds controlled by the gall-former?

The chemical composition of galled and ungalled plant tissue was compared in a series of experiments. Gall and adjacent plant tissue was analysed for 20 species of gall-former on 11 different plant species. There were clear differences between galled and ungalled tissue in levels of nutrients and secondary compounds. Gall tissue generally contained lower levels of nitrogen and higher levels of phenolic compounds than ungalled plant tissue. The gall tissue produced by the same plant in response to different species of gall-former differed in chemical composition, as did the gall-tissue from young and mature galls of the same species. The chemical differences between gall and plant tissues were studied in more detail in two field manipulations. Firstly, the seasonal changes in phenolic biosynthesis in Pontania proxima and P. pedunculi (Hymenoptera: Tenthredinidae) gall tissue were compared to those of their host plants, Salix alba and S. caprea. In both types of gall tissue, phenolic levels declined as the season progressed, but levels in the surrounding plant tissue increased. When the gall insects were killed with insecticide, phenolic levels in the galled tissue dropped to the same level as those in adjacent plant tissue. Secondly, the density of Cynips divisa (Hymenoptera: Cynipidae) galls on Quercus robur leaves was reduced by removing half the galls present, either those from the central region of the leaf or those from the edge. Decreasing gall density increased the size of the remaining galls and the weight of the insects, but these effects were most marked when the galls remaining were growing centrally on the leaf, i.e. when the galls from the edge had been removed. Decreasing gall density increased the nitrogen content of the remaining galls, again to a greater extent in galls growing centrally on the leaf. The results of these studies suggest that the levels of nutrients and secondary compounds in gall tissue are usually markedly different to those of surrounding plant tissue, and that gall-formers may produce species-specific and temporally variable changes in the chemical composition of gall tissue. Received: 7 July 1997 / Accepted: 29 September 1997     

Factors Affecting the Prolongation of NMR Relaxation Times of Water Protons in Leaves of Woody Plants Affected by Formation of Insect Galls

Changes in NMR relaxation times (T₁) of water protons and watercontents of leaves of woody plants affected by formation ofinsect galls were studied in Machilus, Zelkova and Cinnamomumparasitized with a gall-midge, an aphid and two different Triozinepsyllids, respectively. The presence of galls in Machilus leavesincreased both T₁ and water contents in the galled leaf tissues,while such tissues in Zelkova showed only increases in T₁. Similartrends for both parameters were also observed in gall-bearingleaf tissues of Machilus and Cinnamomum, with galls caused bytwo different psyllids. It seems that it is the particular characteristicsof leaf tissues of the host plant that determine whether thesystemic effect of the presence of galls is reflected both inT₁ and in water content, or only in T₁. Histologic features,including the presence of tannins in and leakage of electrolytesfrom these materials, were compared with those of normal (ungalled)leaves to determine possible causative factors involved in theprolongation of T₁ relaxation times that were associated withthe presence of insect galls. The eco-physiological implicationof tannins with respect to the host-parasite relationship isalso discussed. (Received October 27, 1989; Accepted April 24, 1990)     

Aphid galls accumulate high concentrations of amino acids: a support for the nutrition hypothesis for gall formation

The nutrition hypothesis for the adaptive significance of insect gall formation postulates that galls accumulate higher concentrations of nutritive compounds than uninfested plant tissue, resulting in a high performance of the gall former. This hypothesis has been supported by some taxa of gall insects, but not by taxa such as cynipid wasps. Aphid galls are expected to require higher levels of nitrogen than other insects’ galls with a single inhabitant, because aphid galls are required to sustain a number of aphids reproducing parthenogenetically over two generations. The present study tested this hypothesis by evaluating aphid performance and amino acid concentration in phloem sap, using the aphid Rhopalosiphum insertum (Walker) (Homoptera: Aphididae), which establishes colonies on leaves of Sorbus commixta Hedlund or in galls of the aphid Sorbaphis chaetosiphon Shaposhnikov (Homoptera: Aphididae). We prepared the gall and non‐gall treatments on trees of S. commixta, in which R. insertum fundatrices were reared and allowed to reproduce. In S. chaetosiphon galls, R. insertum colonies propagated more rapidly, and the second generation grew larger and more fecund than on ungalled leaves. The amount of amino acids exuding from cut galled leaves was fivefold that in ungalled leaves; however, there was no significant difference in the amino acid composition between galled and ungalled leaves. In the intact leaves, total amino acid concentration in the phloem sap declined rapidly from late April to late May; however, the galls retained this high amino acid concentration in developing leaves for 1 month. These results indicate that the improved performance in R. insertum is ascribed to the increased concentration of amino acids in galled leaves. We suggest that S. chaetosiphon galls function to promote the breakdown of leaf protein, leading to an increased performance of gall‐inhabiting aphids.     

Impact of whole-canopy and systemic insecticidal treatments on Callirhytis cornigera (Hymenoptera: Cynipidae) and associated parasitoids on pin oak

The gall wasp Callirhytis cornigera (Osten Sacken) is a cynipid with alternating generations that produce large, woody stem galls and tiny blister-like leaf galls on pin oak, Quercus palustris Muenchhausen, in the United States. We tested 3 approaches to control the leaf-galling generation, and determined their impact on associated parasitoids and effectiveness in reducing numbers of new stem galls. First, trees were sprayed with bifenthrin or chlorpyrifos in late March to kill females emerging from stem galls before they oviposited into buds. Second, concentrated solutions of abamectin, imidacloprid, or bidrin were injected from pressurized containers into tree sapwood to control larvae developing in young leaf galls. Finally, systemic insecticides (acephate, abamectin, dimethoate, or imidacloprid) were sprayed at early leaf expansion (2 May) or to young, expanded leaves (17 May) to target larvae in leaf galls. Parasitoids, mostly eulophids, accounted for approximately 70% mortality of leaf-galling C. cornigera larvae on untreated trees. Whole-canopy sprays during C. cornigera emergence from stem galls reduced overall numbers of galled leaves and leaf galls. Trunk injections of bidrin or abamectin resulted in significant mortality of gall inhabitants, including parasitoids. However, neither of the aforementioned approaches significantly reduced numbers of new stem galls. Sprays of abamectin, dimethoate, or imidacloprid applied on 2 May caused high mortality of all gall inhabitants. There was no net benefit, however, because parasitism caused a similar reduction in C. cornigera survival on unsprayed shoots. Sprays applied later in leaf expansion had little impact on gall inhabitants. Of the treatments tested, bifenthrin sprays at bud break provided the greatest reduction in new leaf galls, whereas bidrin injections provided the greatest reduction in gall wasps emerging from galled leaves. This study suggests that gall wasp outbreaks are unlikely to be controlled by a single treatment, regardless of application method.     

蓟马诱导的鹅掌柴叶片虫瘿组织的生理生化响应

以蓟马诱导的鹅掌柴叶片管状虫瘿为材料,分析了虫瘿和非虫瘿组织的抗氧化活性及其它生理响应以及营养物质的含量、分配等。结果发现虫瘿组织中许多生理指标如过氧化氢浓度、过氧化物酶和苯丙氨酸解氨酶活性以及丙二醛含量都比非虫瘿组织低。虫瘿组织比非虫瘿组织光合速率下降而呼吸速率增强,虫瘿组织转变为一个营养库能够富集较多的营养物质。仅仅使用植物激素和蓟马萃取物不能诱导虫瘿的形成,但是,细胞分裂素类植物生长调节物可以引起类似蓟马诱导虫瘿的早期反应。     

Leaf Production and Morphology in the Artichoke Gall of Yew (Taxus baccata L.)

Comparative leaf production rates and leaf morphology studiesfor galled and normal shoots of yew trees have been obtainedthroughout the life cycle of the causative agent, the gall midge,Taxomyia taxi. Normal and galled shoot leaf numbers have beenrelated to those of their parent shoots. It was found that whereasthe annual leaf production of normal shoots was positively relatedto that of the parent shoots, galled shoot leaf production remainedconstant regardless of parent shoot vigour showing leaf stimulationby the midge to be a special case. The midge larva appears tobe determining the rate of leaf production in galled shoots.In galls leaf production continues throughout the winter monthswith no dormant period. From morphological evidence, alternationof leaves and cataphylls is continued in galled buds.     

Phenotypic plasticity and similarity among gall morphotypes on a superhost,Baccharis reticularia (Asteraceae)

Understanding factors that modulate plant development is still a challenging task in plant biology. Although research has highlighted the role of abiotic and biotic factors in determining final plant structure, we know little of how these factors combine to produce specific developmental patterns. Here, we studied patterns of cell and tissue organisation in galled and non‐galled organs of Baccharis reticularia, a Neotropical shrub that hosts over ten species of galling insects. We employed qualitative and quantitative approaches to understand patterns of growth and differentiation in its four most abundant gall morphotypes. We compared two leaf galls induced by sap‐sucking Hemiptera and stem galls induced by a Lepidopteran and a Dipteran, Cecidomyiidae. The hypotheses tested were: (i) the more complex the galls, the more distinct they are from their non‐galled host; (ii) galls induced on less plastic host organs, e.g. stems, develop under more morphogenetic constraints and, therefore, should be more similar among themselves than galls induced on more plastic organs. We also evaluated the plant sex preference of gall‐inducing insects for oviposition. Simple galls were qualitative and quantitatively more similar to non‐galled organs than complex galls, thereby supporting the first hypothesis. Unexpectedly, stem galls had more similarities between them than to their host organ, hence only partially supporting the second hypothesis. Similarity among stem galls may be caused by the restrictive pattern of host stems. The opposite trend was observed for host leaves, which generate either similar or distinct gall morphotypes due to their higher phenotypic plasticity. The Relative Distance of Plasticity Index for non‐galled stems and stem galls ranged from 0.02 to 0.42. Our results strongly suggest that both tissue plasticity and gall inducer identity interact to determine plant developmental patterns, and therefore, final gall structure.     

Characterisation of the effects of leaf galls of Clusiamyia nitida (Cecidomyiidae) on Clusia lanceolata Cambess. (Clusiaceae): Anatomical aspects and chemical analysis of essential oil

Galls develop in different plant organs and are induced by the activity of various organisms. Some studies have investigated the ecological interactions between species of Clusia and gall-inducing insects. The goal of our study is to characterise changes in leaf anatomy caused by the activity of gall insects in Clusia lanceolata. Additionally, we also investigated the chemical composition of volatile compounds of normal leaves and those with galls to detect possible effects on the host plants. For anatomical studies, we used botanical material fixed in FAA₅₀. Transversal sections of the leaf blade were obtained from samples of leaves located on the third and fourth nodes from both male and female individuals. Material was studied from both sexes both with unaffected leaves and leaves containing galls. Fresh leaves of C. lanceolata were used for the extraction of volatile compounds, which were submitted to stem distillation using a modified Clevenger apparatus determining the oil yields subsequently (w/w). The unaffected leaves of female and male individuals of C. lanceolata exhibit similar anatomical structures. However, galls on leaves of both sexes show anatomical differences. The activity of the gall insect Clusiamyia nitida induces several changes in the foliar anatomy and the distribution of metabolic compounds in new tissues during gall development. However, the larvae are not able to induce significant changes in the volatile compounds of inflected leaves from male and female individuals.     

Why do the galls induced by Calophya duvauae Scott on Schinus polygamus (Cav.) Cabrera (Anacardiaceae) change colors?

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 = 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.