Soil-plant-gall relationships: from gall development to ecological patterns.

The adaptive nature of the galler habit has been tentatively explained by the nutrition, microenvironment, and enemy hypotheses. Soil attributes have direct relationships with these three hypotheses at the cellular and macroecological scales, but their influence has been restricted previously to effects on the nutritional status of the host plant on gall richness and abundance. Herein, we discuss the ionome patterns within gall tissues and their significance for gall development, physiology, structure, and for the nutrition of the gallers. Previous ecological and chemical quantification focused extensively on nitrogen and carbon contents, evoking the carbon-nutrient defence hypothesis as an explanation for establishing the plant-gall interaction. Different elements are involved in cell wall composition dynamics, antioxidant activity, and regulation of plant-gall water dynamics. An overview of the different soil-plant-gall relationships highlights the complexity of the nutritional requirements of gallers, which are strongly influenced by environmental soil traits. Soil and plant chemical profiles interact to determine the outcome of plant-herbivore interactions and need to be addressed by considering not only the soil features and galler nutrition but also the host plant's physiological traits. The quantitative and qualitative results for iron metabolism in gall tissues, as well as the roles of iron as an essential element in the physiology and reproduction of gallers suggest that it may represent a key nutritional resource, aligning with the nutrition hypothesis, and providing an integrative explanation for higher gall diversity in iron-rich soils.

Experimental evidence for a hidden network of higher-order interactions in a diverse arthropod community.

Transcending pairwise interactions in ecological networks remains a challenge.1,2,3,4,5 Higher-order interactions (HOIs), the modulation of a pairwise interaction by a third species,6 are thought to play a particularly important role in stabilizing coexistence and maintaining species diversity.7,8,9,10,11,12 However, HOIs have so far only been demonstrated in models9,10,11,12,13,14 or isolated experimental systems including only a few interacting species.7,8,15 Their ubiquity and importance at a community level in the real world remain unknown. We hypothesized that a complex network of HOIs could be constantly modifying pairwise interactions and shaping ecological communities and that consequently the outcome of pairwise interactions would be a product of many influences from distinct sources. Using field experiments, we tested how multiple interactions within a diverse arthropod community associated with the tropical shrub Baccharis dracunculifolia D.C. (Asteraceae) were modified by the removal of ant species or live or hatched insect galls (a non-trophic engineering effect) of the dominant galler species. We revealed an extensive hidden network of HOIs modifying each other and the "visible" pairwise interactions. Most pairwise interactions were affected indirectly by the manipulation of non-interacting taxonomic groups. The pervasiveness of these interaction modifications challenges pairwise approaches to understanding interaction outcomes and could shift our thinking about the structure and persistence of ecological communities. Investigating coexistence mechanisms involving interaction modulation by HOIs may be key to elucidating the underlying causes of the stability and persistence of ecological communities.

Insect galls from the Serra da Bandeira (Barreiras, Western Bahia, Brazil) / 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.

Resumo Compreender a diversidade de galhas de insetos é fundamental para o estabelecimento de planos de conservação em diferentes ecossistemas brasileiros. Aqui, nós (1) caracterizamos as galhas de insetos encontradas em espécies de plantas hospedeiras, (2) identificamos os insetos indutores de galhas até o nível taxonômico mais baixo possível e (3) registramos a presença de fauna associada a galhas. Nosso estudo foi realizado mensalmente de agosto de 2017 a julho de 2018 ao longo de nove trilhas na Serra da Bandeira, que está localizada em uma área de Cerrado stricto sensu ao longo de um ano. Encontramos 48 morfotipos distintos de galhas, pertencentes a 12 famílias botânicas. Os morfotipos mais comumente encontrados foram globoide (27,1%), lenticular (27,1%) e cilíndrico (25%). Os órgãos vegetais mais afetados pelos insetos galhadores foram as folhas (73%), seguidas do caule (19%), flor (4%), inflorescência (2%) e frutos (2%). As famílias botânicas hospedeiras com maior número de galhas foram Fabaceae (26), Malpighiaceae (5) e Anacardiaceae, Combretaceae e Euphorbiaceae (3). Observamos que o gênero Copaifera Lindl. (Fabaceae) apresentou a maior diversidade de morfotipos de galhas, abrigando 19 morfotipos distribuídos em três espécies que ocorrem simpatriicamente - Copaifera sabulicola J. Costa (Fabaceae), Copaifera depilis Dwyer (Fabaceae) e Copaifera luetzelburgii Harms (Fabaceae). Pela primeira vez no Brasil, registramos a ocorrência de galhas em flores de Manihot caerulescens (Euphorbiaceae), em inflorescências de Mimosa acutistipula (Fabaceae) e em botões florais de Anacardium humile (Anacardiaceae), induzidas por Cecidomyiidae. Indutores da ordem Diptera (Família Cecidomyiidae) foram os mais abundantes, encontrados em 14 morfotipos de galhas. Em relação à fauna associada, encontramos insetos pertencentes principalmente à ordem Hymenoptera, e os identificamos como parasitóides. As informações fornecidas podem ser utilizadas por tomadores de decisão para programas de conservação, bem como em outras estratégias para a conservação da diversidade biológica no Cerrado brasileiro.

Sexually dimorphic galls induced on leaflets of Matayba guianensis (Sapindaceae): a rare phenomenon occurring in Diptera (Cecidomyiidae).

In a general way, galling insects can induce only one gall morphotype on the host plant species. However, some taxa of galling insects such as Eriococcidae can induce sexually dimorphic galls on the same host. In the present study, Lopesia mataybae (Diptera: Cecidomyiidae) induced two gall morphotypes on the leaflets of Matayba guianensis (Sapindaceae), a rare evidence of sexual dimorphism in galls induced by Cecidomyiidae. We investigated the adult emergence of galling insects and the morphological, histological, and histochemical attributes of the gall morphotypes. Both gall morphotypes showed the galling insect in the larval or pupal stage, and the insect adult emergence from different morphotypes was sexually distinct. Galls occupied by females (Globoid) were significantly larger (average height = 4.67 mm. S = 0.43/average width = 4.59 mm. S = 0.70) than galls occupied by males (cylindrical) (average height = 2.95 mm. S = 0.46/average width = 2.34 mm. S = 0.45). Both gall types were composed of elongated cells in the inner cortex and rounded cells in the outer cortex of the vessel-like structure. The globoid galls showed 42 cell layers (14 of them cylindrical, S = 3.86; 28 rounded, S = 5.89) and cylindrical galls showed 29 layers. There were no differences between morphotypes in the histochemical compounds detected. We have shown here significant morphological and histological differences between male and female galls possibly due to the different nutritional requirements of Lopesia mataybae sexes. Therefore, the expression of sexual dimorphism in gall morphotypes may be associated with developmental pathway differentiation between the sexes of L. mataybae.

Insect galls associated with Copaifera sabulicola J.A.S Costa & L.P Queiroz (Fabaceae): Characterization and new records

ABSTRACT Among the plant diversity of the Cerrado, the genus Copaifera is commonly associated with galling insects. Here, we expand the knowledge about insect galls on Copaifera sabulicola J.A.S Costa & L.P. Queiroz (Fabaceae) by characterizing their occurrence in a stricto sensu vegetation area of the Brazilian Cerrado, Western Bahia, Brazil throughout the year. We randomly sampled 60 branches (50 cm long) from individuals of C. sabulicola, from April 2015 to March 2016. We found 11 morphotypes for C. sabulicola, of which 5 are new records. Further, we identified six gall-inducing insects, all belonging to Cecidomyiidae family. Regarding other arthropods associated with C. sabulicola, we observed inquilines, successors, and parasitoids, belonging to the orders Collembola, Hemiptera, Hymenoptera and Acari. The parasitoid fauna included three families of the order Hymenoptera: Braconidae, Encyrtidae and Eulophidae.

Insect galls of the Brazilian Cerrado: associated fauna / Galhas de insetos do Cerrado Brasileiro: fauna associada

Abstract: Insect galls host a rich and diverse fauna of secondary dwellers, which compose the associated fauna. In Brazil, many inventories of insect galls in Cerrado areas have recorded secondary dwellers. These records were scattered in several papers. This study gathered literature data to provide an overview of the arthropod fauna associated with insect galls in the Brazilian Cerrado. We searched for scientific publications in online academic databases and retrieved 16 papers with data on the secondary dwellers. We limited our search to the period from 1988 to 2020. We updated the name of plant species and verified endemism and geographic distribution in Flora do Brasil 2020. We provided plant species uses based on the Tropical Useful Plants 2014. We found 163 gall morphotypes with secondary dwellers (16.8% of the total of gall morphotypes of the Brazilian Cerrado) on 94 plant species in 37 families. Asteraceae, Fabaceae, Myrtaceae, and Malpighiaceae exhibited the greatest number of records. These are the richest families in insect galls in the Brazilian Cerrado. Most arthropod fauna were recorded in galls of Cecidomyiidae (Diptera). Most records were in leaf galls, the predominant galled organ. Parasitoids were more frequent than successors, inquilines, and predators. Eulophidae and Eurytomidae were the most frequent parasitoid families. Inquilines were represented by Coleoptera, Diplopoda, Diptera, Hemiptera, Hymenoptera, Lepidoptera, Psocoptera, and Thysanoptera; successors by Acari, Araneae, Cecidomyiidae (Diptera), Coleoptera, Collembola, and Formicidae (Hymenoptera), whereas predators by Pseudoscorpiones and Diptera. Most records were presented in suprageneric categories, showing that the taxonomic knowledge is very deficient. 29 plant species are endemic to Brazil and totaled 45 gall morphotypes with secondary dwellers; 46 plant species are useful and host secondary dwellers in 62 gall morphotypes. These data add ecological and economic importance to these arthropods.

Resumo: As galhas de insetos abrigam uma fauna rica e diversificada de habitantes secundários que compõem a fauna associada. No Brasil, muitos inventários de galhas de insetos em áreas de Cerrado registram habitantes secundários. Estes registros, dispersos em vários artigos, foram reunidos para fornecer uma visão ampla da fauna de artrópodes associados às galhas de insetos no Cerrado brasileiro. Buscamos publicações científicas nas bases de dados acadêmicas virtuais e encontramos 16 artigos com informações de habitantes secundários. Limitamos nossa busca ao período de 1988 a 2020. Atualizamos o nome das espécies botânicas e verificamos sua distribuição geográfica e endemismos no site Flora do Brasil 2020. Fornecemos os usos das espécies vegetais com base no site Tropical Useful Plants 2014. Encontramos 163 morfotipos de galhas com habitantes secundários (16,8% do total de morfotipos de galhas do Cerrado brasileiro) em 94 espécies de plantas de 37 famílias. Asteraceae, Fabaceae, Myrtaceae e Malpighiaceae exibiram o maior número de registros. Estas são as famílias mais ricas em galhas de insetos no Cerrado brasileiro. A maioria da fauna de artrópodes foi assinalada em galhas de Cecidomyiidae (Diptera). A maioria dos registros foi em galhas foliares, órgão vegetal com maior riqueza de galhas. Os parasitoides foram mais frequentes que os sucessores, inquilinos e predadores. Eulophidae e Eurytomidae foram as famílias de parasitoides mais frequentes. Os inquilinos foram representados por Coleoptera, Diplopoda, Diptera, Hemiptera, Hymenoptera, Lepidoptera, Psocoptera, e Thysanoptera; os sucessores por Acari, Araneae, Cecidomyiidae (Diptera), Coleoptera, Collembola e Formicidae (Hymenoptera); enquanto os predadores por Pseudoscorpiones e Diptera. A maioria dos registros foi apresentada em categorias supragenéricas, mostrando que o conhecimento taxonômico é muito deficiente. Vinte e nove plantas são endêmicas do Brasil e totalizam 45 morfotipos de galhas com habitantes secundários; 46 espécies vegetais são úteis e hospedam habitantes secundários em 62 morfotipos de galhas. Estas informações acrescentam importância ecológica e econômica a estes artrópodes.

Gall-Inducing Parasites: Convergent and Conserved Strategies of Plant Manipulation by Insects and Nematodes.

Gall-inducing insects and nematodes engage in sophisticated interactions with their host plants. These parasites can induce major morphological and physiological changes in host roots, leaves, and other tissues. Sedentary endoparasitic nematodes, root-knot and cyst nematodes in particular, as well as gall-inducing and leaf-mining insects, manipulate plant development to form unique organs that provide them with food from feeding cells. Sometimes, infected tissues may undergo a developmental switch resulting in the formation of aberrant and spectacular structures (clubs or galls). We describe here the complex interactions between these plant-reprogramming sedentary endoparasites and their infected hosts, focusing on similarities between strategies of plant manipulation. We highlight progress in our understanding of the host plant response to infection and focus on the nematode and insect molecules secreted in planta. We suggest thatlooking at similarities may identify convergent and conserved strategies and shed light on the promise they hold for the development of new management strategies in agriculture and forestry.

The Role of Baccharis dracunculifolia and its Chemical Profile on Green Propolis Production by Apis mellifera.

The botanical source of Brazilian green propolis (BGP) is Baccharis dracunculifolia DC, which interacts not only with Apis mellifera, but also with galling insects. In the last decade, because of green propolis´ important biologic activities, the international demand for BGP overcame the production capacity, consequently, new approaches are required to increase this production. Hence, the understanding of the chemical ecology interactions of B. dracunculifolia with galls and bees in field conditions may provide insights to increase BGP's production. A "bee pasture" experiment aiming to better understand this plant-insect interaction was therefore performed. For that, 48 B. dracunculifolia individuals, being 24 females and 24 males, were cultivated and investigated for the following parameters: (1) phenolic and volatile compounds in both B. dracunculifolia leaves and green propolis, (2) environmental variables, (3) visiting rate by bees, (4) time of resin collection, and (5) number of galls. Regression analyses by independent linear mixed-effect models were run to correlate phenolic and volatile compounds concentration with the environmental and field variables. Significant differences in chemical profile and field variables were observed between male and female plants. Male plants showed higher infestation by galling insects while female plants showed higher number of visiting bees, time of resin collection and terpenes concentration, contributing to the differences observed in the field. The obtained results suggest that increasing the percentage of female B. dracunculifolia plants in the field may attract more bees and therefore enhance propolis production.

Identification of a cyanidin-3-O-ß-galactoside in gall tissue induced by midges on Japanese beech (Fagus crenata Blume).

Insect gall structures have many characteristic forms and colors, which are distinguishable from host plants. In this study, we identified an anthocyanin from red color insect galls and revealed that the anthocyanin biosynthesis of plants was induced by the gall extracts. The galling insects presumably regulate the anthocyanin biosynthesis of host plants to protect their larvae from environmental stresses.

Superhost Plants Alter the Structure of Plant-Galling Insect Networks in Neotropical Savannas.

Host plants may harbor a variable number of galling insect species, with some species being able to harbor a high diversity of these insects, being therefore called superhost plants. In the present study, we tested the hypothesis that the occurrence of superhost plant species of genus Qualea (Vochysiaceae) affects the structure of plant-galling insect ecological networks in Brazilian Cerrado. We sampled a total of 1882 plants grouped in 131 species and 43 families, of which 64 species and 31 families of host plants hosted 112 galling insect species. Our results showed that occurrence of superhosts of genus Qualea increased the linkage density of plant species, number of observed interactions, and the size of plant-galling insect networks and negatively affected the network connectance (but had no effect on the residual connectance). Although the occurrence of Qualea species did not affect the plant species richness, these superhosts increased the species richness and the number of interactions of galling insects. Our study represents a step forward in relation to previous studies that investigated the effects of plant diversity on the plant-insect networks, showing that few superhost plant species alter the structure of plant-herbivore networks, even without having a significant effect on plant diversity.

Interaction engineering: Non-trophic effects modify interactions in an insect galler community.

Theory suggests that non-trophic interactions can be a major mechanism behind community stability and persistence, but community-level empirical data are scarce, particularly for effects on species interactions mediated through changes in the physical environment. Here, we explored how ecosystem engineering effects can feed back to the engineer, not only modulating the engineer's population density (node modulation) but also affecting its interactions with other species (link modulation). Gall induction can be viewed as ecosystem engineering since galls serve as habitat for other species. In a community-level field experiment, we generated treatments with reduced or elevated ecosystem engineering by removing or adding post-emergence galls to different plots of their host plant in the Brazilian Cerrado. We tested the effect of post-emergence galls on the galler, as well as on the galler-parasitoid and galler-aphid interactions. The manipulation of post-emergence galls had little effect on the galler-abundance and survivorship were not affected, and gall volume changed only slightly-but modified interactions involving the galler, parasitoid wasps and inquiline aphids. Aphid inquilines negatively affected density-dependent parasitism rates (interaction modification) likely by killing parasitised galling larvae. Post-emergence galls interfered with aphid inquilinism-likely by the provision of alternative habitat for aphids-and thus interfered with the negative effect of aphids on parasitism (modification of an interaction modification). This work is one of the few studies to demonstrate experimentally the role played by environment-mediated interaction modification at a community level in the field. Moreover, by manipulating a species' ecosystem engineering effect (post-emergence galls) instead of the species itself, we demonstrate the novel result that populations can be regulated by non-trophic effects initiated by their own activities that alter their interaction with other species. This reveals that indirect interactions mediated via the environment offer new pathways of feedback loops for population regulation. Our results indicate that interaction modification has the potential to be a key regulatory mechanism underlying interaction variation in nature, and play a major role in community structure, dynamics and stability.

Phylogenetics of Australasian gall flies (Diptera: Fergusoninidae): Evolutionary patterns of host-shifting and gall morphology.

This study investigated host-specificity and phylogenetic relationships in Australian galling flies, Fergusonina Malloch (Diptera: Fergusoninidae), in order to assess diversity and explore the evolutionary history of host plant affiliation and gall morphology. A DNA barcoding approach using COI data from 203 Fergusonina specimens from 5gall types on 56 host plant species indicated 85 presumptive fly species. These exhibited a high degree of host specificity; of the 40 species with multiple representatives, each fed only on a single host genus, 29 (72.5%) were strictly monophagous, and 11 (27.5%) were reared from multiple closely related hosts. COI variation within species was not correlated with either sample size or geographic distance. However variation was greater within oligophagous species, consistent with expectations of the initial stages of host-associated divergence during speciation. Phylogenetic analysis using both nuclear and mitochondrial genes revealed host genus-restricted clades but also clear evidence of multiple colonizations of both host plant genus and host species. With the exception of unilocular peagalls, evolution of gall type was somewhat constrained, but to a lesser degree than host plant association. Unilocular peagalls arose more often than any other gall type, were primarily located at the tips of the phylogeny, and did not form clades comprising more than a few species. For ecological reasons, species of this gall type are predicted to harbor substantially less genetic variation than others, possibly reducing evolutionary flexibility resulting in reduced diversification in unilocular gallers.

Sink Status and Photosynthetic Rate of the Leaflet Galls Induced by Bystracoccus mataybae (Eriococcidae) on Matayba guianensis (Sapindaceae).

The galling insect Bystracoccus mataybae (Eriococcidae) induces green and intralaminar galls on leaflets of Matayba guianensis (Sapindaceae), and promotes a high oxidative stress in host plant tissues. This biotic stress is assumed by the histochemical detection of hydrogen peroxide, a reactive oxygen species (ROS), whose production alters gall physiology. Thus, we hypothesize that high levels of nutrients are accumulated during gall development in response to a local maintenance of photosynthesis and to the galling insect activity. Moreover, the maintenance of low levels of photosynthesis may guarantee O2 production and CO2 consumption, as well as may avoid hypoxia and hypercarbia in gall tissues. To access the photosynthesis performance, the distribution of chlorophyllous tissues and the photochemical and carboxylation rates in gall tissues were analyzed. In addition, histochemical tests for hydrogen peroxide and phenolic derivatives were performed to confirm the biotic stress, and set the possible sites where stress dissipation occurs. The contents of sugars and nitrogen were evaluated to quantify the gall sink. Currently, we assume that the homeostasis in gall tissues is ruptured by the oxidative stress promoted by the galling insect activity. Thus, to supply the demands of gall metabolism, the levels of water-soluble polysaccharides and starch increase in gall tissues. The low values of maximum quantum efficiency of PSII (Fv/Fm) indicate a low photosynthetic performance in gall tissues. In addition, the decrease of PSII operating efficiency, (F'm-F')/F'm, and Rfd (instantaneous fluorescence decline ratio in light, to measure tissue vitality) demonstrate that the tissues of B. mataybae galls are more susceptible to damage caused by stressors than the non-galled tissues. Thus, the high oxidative stress in gall developmental sites is dissipated not only by the accumulation of phenolic derivatives in the protoplast, but also of lignins in the walls of neoformed sclereids.

Experimentally reducing species abundance indirectly affects food web structure and robustness.

Studies on the robustness of ecological communities suggest that the loss or reduction in abundance of individual species can lead to secondary and cascading extinctions. However, most such studies have been simulation-based analyses of the effect of primary extinction on food web structure. In a field experiment we tested the direct and indirect effects of reducing the abundance of a common species, focusing on the diverse and self-contained assemblage of arthropods associated with an abundant Brazilian shrub, Baccharis dracunculifolia D.C. (Asteraceae). Over a 5-month period we experimentally reduced the abundance of Baccharopelma dracunculifoliae (Sternorrhyncha: Psyllidae), the commonest galling species associated with B. dracunculifolia, in 15 replicate plots paired with 15 control plots. We investigated direct effects of the manipulation on parasitoids attacking B. dracunculifoliae, as well as indirect effects (mediated via a third species or through the environment) on 10 other galler species and 50 associated parasitoid species. The experimental manipulation significantly increased parasitism on B. dracunculifoliae in the treatment plots, but did not significantly alter either the species richness or abundance of other galler species. Compared to control plots, food webs in manipulated plots had significantly lower values of weighted connectance, interaction evenness and robustness (measured as simulated tolerance to secondary extinction), even when B. dracunculifoliae was excluded from calculations. Parasitoid species were almost entirely specialized to individual galler species, so the observed effects of the manipulation on food web structure could not have propagated via the documented trophic links. Instead, they must have spread either through trophic links not included in the webs (e.g. shared predators) or non-trophically (e.g. through changes in habitat availability). Our results highlight that the inclusion of both trophic and non-trophic direct and indirect interactions is essential to understand the structure and dynamics of even apparently discrete ecological communities.

Resource allocation in Copaifera langsdorffii (Fabaceae): how supra-annual fruiting affects plant traits and herbivory?

AbstractPlants have limited resources to invest in reproduction, vegetative growth and defense against herbivorous. Trade-off in resources allocation promotes changes in plant traits that may affect higher trophic levels. In this study, we evaluated the trade-off effect between years of high and low fruiting on the investment of resources for growth and defense, and their indirect effects on herbivory in Copaifera langsdorffii. Our questions were: (i) does the resource investment on reproduction causes a depletion in vegetative growth as predicted by the Carbon/Nutrient Balance hypothesis (CNBH), resulting in more availability of resources to be allocated for defense?, (ii) does the variation in resource allocation for growth and defense between years of high and low fruiting leads to indirect changes in herbivory? Thirty-five trees located in a Cerrado area were monitored during 2008 (year of high fruiting) and 2009 (year of no fruiting) to evaluate the differential investment in vegetative traits (biomass, growth and number of ramifications), plant defense (tannin concentration and plant hypersensitivity) and herbivory (galling attack and folivory). According to our first question, we observed that in the fruiting year, woody biomass negatively affected tannin concentration, indicating that fruit production restricted the resources that could be invested both in growth as in defense. In the same way, we observed an inter-annual variation in herbivorous attack, and found that plants with higher leaf biomass and tannin concentration, experienced higher galling attack and hypersensitive reaction, regardless years. These findings suggested that plants’ resistance to herbivory is a good proxy of plant defense and an effective defense strategy for C. langsdorffii, besides the evidence of indirect responses of the third trophic level, as postulated by the second question. In summary, the supra-annual fruiting pattern promoted several changes on plant development, demonstrating the importance of evaluating different plant traits when characterizing the vegetative investment. As expected by theory, the trade-off in resource allocation favored changes in defense compounds production and patterns of herbivory. The understanding of this important element of insect-plant interactions will be fundamental to decipher coevolutionary life histories and interactions between plant species reproduction and herbivory. Besides that, only through long-term studies we will be able to build models and develop more accurate forecasts about the factors that trigger the bottom-up effect on herbivory performance, as well the top-down effect of herbivores on plant trait evolution. Rev. Biol. Trop. 64 (2): 507-520. Epub 2016 June 01.

ResumenLas plantas tienen recursos limitados para invertir en reproducción, crecimiento vegetativo y defensa contra herbívoros. El cambio en la distribución de recursos promueve variaciones en rasgos vegetales, que pueden afectar los niveles tróficos superiores. Durante dos años consecutivos de alta y baja inversión reproductiva se evaluó el cambio de recursos entre crecimiento vegetativo y defensa, y su efecto indirecto sobre la herbivoría en Copaifera langsdorffii. Nos preguntamos: i) ¿La inversión de recursos para la reproducción causa reducción del crecimiento vegetativo, como predice la hipótesis de equilibrio carbono/nutrientes, haciendo posible gastar más recursos en defensa? ii) ¿La variación en distribución de recursos para crecimiento y defensa entre años de alta y baja fructificación modifica indirectamente la herbivoría? Se monitorearon treinta y cinco árboles durante 2008 (gran fructificación) y 2009 (sin fructificación) en un área de vegetación de cerrado (Brasil), para evaluar la inversión diferencial en rasgos vegetativos (biomasa, crecimiento y No. de ramificaciones), defensa (concentración de taninos e hipersensibilidad vegetal) y herbivoría. De acuerdo a nuestra primera pregunta, se observó que en el año de fructificación la biomasa leñosa afectó negativamente la concentración de taninos, indicando que la producción de frutos redujo los recursos que podían invertirse en crecimiento y defensa. Además, la resistencia de las plantas y el ataque de agallas fueron influidos positivamente por la concentración de taninos y la biomasa foliar, lo que sugiere que la resistencia de los árboles a la herbivoría es un buen indicador de defensa vegetal y una estrategia efectiva de defensa de C. langsdorffii, además hay evidencia de respuesta trófica indirecta, como se postula en la segunda pregunta. En resumen, el patrón de fructificación supra-anual provoca varios efectos en el desarrollo de las plantas, mostrando la importancia de evaluar diversos rasgos vegetales al caracterizar la inversión de recursos de una especie. Como se esperaba, el cambio en la distribución de recursos modifica la producción de compuestos de defensa y los patrones de herbivoría. El entendimiento de este elemento importante de las interacciones insecto-planta será fundamental para descifrar la historia natural coevolutiva y las interacciones entre reproducción vegetal y ataque herbívoro. Además de eso, solo a través de estudios a largo plazo vamos a ser capaces de construir modelos y desarrollar pronósticos más precisos acerca de los factores que desencadenan el efecto de abajo hacia arriba en el rendimiento de la herbivoría, así el efecto de arriba hacia abajo de los herbívoros sobre la evolución de las plantas.

Ocorrência e caracterização de galhas em fragmento de Floresta Estacional Semidecidual em Telêmaco Borba, Paraná, Brasil / Occurrence and gall characterization in a fragment of Seasonal Semideciduous Forest in Telêmaco Borba, Paraná, Brazil

Levantamentos de galhas no Paraná são escassos e a maioria dos esforços amostrais no Brasil tem se concentrado em áreas de Cerrado. Assim, o presente estudo investigou um fragmento de Floresta Estacional Semidecidualda Fazenda Monte Alegre em Telêmaco Borba, com o intuito de contribuir para o conhecimento das galhas no Estado do Paraná. As coletas foram realizadas em uma trilha de 300m de comprimento e 5m de largura, atravésde busca ativa até dois metros de altura. Foram encontrados 41 morfotipos de galhas, dos quais treze tiveram a planta hospedeira identificada ao nível de espécie, dez ao nível de gênero, dez ao nível de família e oito morfotipos não foram identificados. Entre as famílias identificadas, Solanaceae, Asteraceae, Euphorbiaceae, Bignoniaceae, Melastomataceae e Leguminosae-Fabaceae representaram as maiores riquezas de galhas. A maioria ocorreu em folha (39%); 98,6% são entomógenas; 70,7% são glabras, e quanto à forma, a maioria foi classificada comoglobóide (43,9%). Quanto à forma de agrupamento das galhas nas plantas hospedeiras, 46,3% apresentaram-se deforma isolada, e 53,7% de forma agrupada. Este trabalho contribuiu para o enriquecimento do conhecimento sobre as galhas no Estado do Paraná e para o Bioma Mata Atlântica.

Galls surveys in Paraná are scarce and most sampling efforts in Brazil have still been concentrated on Cerradoregions. In this context, the present study investigated an area of semideciduous forest of Fazenda Monte Alegrein Telêmaco Borba, in order to contribute to the knowledge of galls in the state. Samples were collected on a 300m long track and 5m width, through active search up to two meters high. Fourty-one morphotypes werefound, thirteen of which were identified to the host plant species level, ten according to level of genus, ten tofamily level and eight morphotypes were not identified. Among the identified families, Solanaceae, Asteraceae, Euphorbiaceae, Bignoniaceae, Melastomataceae and Leguminosae-Fabaceae represented the greatest quantityof morphotypes. Most of them occurred on the leaf (39%), 98.6% are entomogenous. 70.7% are glabrous, andas for the shape, most of them were classified as globular (43.9%). As for the way galls grouping on host plants, 46.3% showed up in isolation, and 53.7% in groupings. This study has contributed to enrich the knowledge ongalls in the state of Paraná and for the Atlantic Forest Biome.

Insect galls of the xeric vegetation of Ilha do Cabo Frio (Arraial do Cabo, RJ, Brazil) / Galhas de insetos da vegetacao xerica da Ilha do Cabo Frio (Arraial do Cabo, RJ, Brasil)

The xeric vegetation of Ilha do Cabo Frio (Arraial do Cabo, RJ) was investigated for insect galls, in May, June and August of 2012, totalizing 24 hours of field work. Forty-five morphotypes of insect galls were found on 29 species of host plant (25 genera and 18 families). Asteraceae and Myrtaceae were the most galled plant families. Leaves were the most galled plant organ, with ca. 62% of the total, followed by stems (ca. 22%). Globoid and fusiform galls were the most frequent with about 29% and 24%, respectively. The majority was glabrous (ca. 91%), and one-chambered (ca. 84%). Gallers of 30 morphotypes were determined. They belong to Diptera (Cecidomyiidae), and Lepidoptera. The former was the most frequent. Larvae of Muscomorpha (Diptera) (probably inquilines) were found in a single gall morphotype; parasitoids (Hymenoptera) in seven (ca. 15% of the total), and predators (pseudoscorpion) in a single one. As there is no previous data of insect galls of Ilha do Cabo Frio, all records presented here are new. The geographic distribution of nine species of gall midges (Diptera, Cecidomyiidae) is widened. For the first time, eleven plant species are recorded as host of galling insects, and 24 gall morphotypes are described.

A vegetação xérica da Ilha do Cabo Frio (Arraial do Cabo, RJ) foi investigada à procura de galhas de insetos em maio, junho e agosto de 2012, totalizando 24 horas de trabalho de campo. Quarenta e cinco morfotipos de galhas foram encontrados em 29 espécies de plantas hospedeiras (25 gêneros e 18 famílias). Asteraceae e Myrtaceae foram as famílias de planta com maior riqueza de galhas. Os órgãos vegetais mais galhados foram folha (cerca de 62% do total) e caule (cerca de 22%). Galhas globóides e fusiformes foram mais frequentes com cerca de 29% e 24%, respectivamente. A maioria era glabra (cerca de 91%) e unilocular (cerca de 84%). Os galhadores de 30 morfotipos foram determinados. Eles pertencem a Diptera (Cecidomyiidae) e Lepidoptera. Os primeiros foram mais frequentes. Larvas de Muscomorpha (Diptera) (provavelmente inquilinas) foram encontradas em um único morfotipo, parasitóides (Hymenoptera) em sete (cerca de 15% do total) e predadores (pseudoscorpiões) em um. Como não havia informação prévia de galhas de insetos na Ilha do Cabo Frio, todos os registros apresentados aqui são novos. A distribuição geográfica de nove espécies de Cecidomyiidae (Diptera) é ampliada. Pela primeira vez, onze espécies de plantas são assinaladas como hospedeiras de galhas e 24 morfotipos de galhas são descritos.

Herbivory among habitats on the Neotropical tree Cnidoscolus quercifolius Pohl. in a seasonally deciduous forest / Herbivoria entre habitats em uma árvore neotropical Cnidoscolus quercifolius Polh. em uma floresta estacional decidual

Our goal was to identify herbivory patterns from two insect guilds associated with Cnidoscolus quercifolius in a tropical deciduous forest in northeastern Brazil. We sampled four different habitats: (1) forest edge, (2) mesic (near to the perennial water source), (3) forest interior and (4) rupestrian fields. Habitat edge had lower leaf damage than rupestrian, mesic and forest interior habitats. Nevertheless, abundance of galls at the edge habitat was higher than at mesic, forest interior and/or rupestrian habitats. There was no difference in gall mortality by natural enemies among the four habitats sampled, demonstrating the absence of any influence of top-down controls related to abundance of galls. Trophic relationships were not related to the patterns of distribution among habitats of two insect herbivorous guilds associated with C. quercifolius. Our results demonstrated that environmental heterogeneity of dry forests can significantly alter important ecological interactions and experimental studies are needed to better understand the mechanisms responsible for differences in herbivory among habitats.

Nosso objetivo foi identificar os padrões de herbivoria de duas guildas de insetos herbívoros associadas à Cnidoscolus quercifolius, em uma floresta estacional seca do nordeste do Brasil. Foram amostrados quatro diferentes habitats: (1) borda florestal; (2) mésico (próximo a uma fonte de água perene); (3) interior florestal, e (4) rupestre. O habitat borda apresentou uma quantidade de dano foliar inferior aos habitats rupestre, mésico e interior florestal. Diferentemente, a abundância de galhas no habitat borda foi superior aos habitats mésico, interior florestal e rupestre. Não houve diferença na mortalidade de galhas por inimigos naturais entre os quatro habitats, o que revela ausência de influência de controles top-down relacionados à abundância de galhas. Relações tróficas não parecem influenciar os padrões de distribuição entre habitats das duas guildas de insetos herbívoros associadas à C. quercifolius. Nossos resultados demonstram que a heterogeneidade ambiental de florestas secas pode alterar significativamente importantes interações ecológicas e que trabalhos experimentais são necessários para uma melhor compreensão dos mecanismos responsáveis pelas diferenças nas taxas de herbivoria entre habitats.

Spatial distribution of a spherical gall (Hymenoptera, Eulophidae) on Caryocar brasiliense (Caryocaraceae) / Distribuição espacial da galha esférica (Hymenoptera, Eulophidae) em Caryocar brasiliense (Caryocaraceae)

We obtained the first data on spatial distribution of a spherical galling insect (Hymenoptera, Eulophidae) at the Caryocar brasiliense Camb. (Caryocaraceae) tree level. This work was developed in two pastures in Montes Claros, Minas Gerais State, Brazil. The areas studied were: pasture 1 (in activity) and pasture 2 (abandoned pasture = savanna in recovery). We evaluated the distribution of spherical galls in: foliage orientation (slope), among leaves (border and interior of the tree crown), among leaflets (right, central, left), distal, median, and proximal as well as border, central area, and adjacent to the mid leaf vein of the leaflet, and difference between areas in 10 infested trees per area. The smaller number of spherical gall/leaflet was observed in pasture 1 than in pasture 2. More spherical galls were found on the northern in pasture 1, but in the pasture 2, the lower spherical galls were observed on the northeast than other slopes. The average number of spherical galls did not differ statistically among the three leaflets of C. brasiliense in pasture 2. However, in pasture 1, we observed highest number of spherical galls in the central leaflet. More spherical galls were found in the border than interior of the tree crown. The average number of spherical galls did not differ statistically among the longitudinal region on leaflet of C. brasiliense. The spherical gall insect preferred to colonize the leaf margin than the central portion or near mid vein on transversal regions on a leaflet.

Foi descrito, pela primeira vez, a distribuição espacial da galha esférica (Hymenoptera, Eulophidae) em árvores de Caryocar brasiliense Camb. (Caryocaraceae). Este trabalho foi desenvolvido em duas pastagens em Montes Claros, Estado de Minas Gerais, Brasil. As áreas estudadas foram: pastagem 1 (em atividade) e pastagem 2 (pastagem abandonada = cerrado em recuperação). Foi avaliada a distribuição de galhas esféricas em relação a: orientação das folhas no dossel, entre folhas (na borda ou no interior da copa da árvore), entre folíolos (direito, central, esquerdo), regiões distal, mediano, e proximal bem como na margem, área central e próximo à nervura central dos folíolos, e a diferença entre pastagens em 10 árvores infestadas por área. O menor número de galhas esféricas/folíolo foi observado na pastagem 1 do que na pastagem 2. Mais galhas esféricas foram encontradas na face norte em pastagem 1, mas na pastagem 2, o menor número destas galhas foi observado nesta face (norte). O número médio de galhas esféricas não diferiu estatisticamente entre os folíolos de C. brasiliense na pastagem 2. Entretanto, na pastagem 1, foi observado maior número de galhas esféricas no folíolo central. Mais galhas esféricas foram encontradas na borda do que no interior da copa das árvores. O número médio de galhas esféricas não diferiu estatisticamente entre as regiões longitudinais dos folíolos de C. brasiliense. Entretanto, esse inseto galhador preferiu colonizar a margem dos folíolos à parte central ou próximo da nervura central dos folíolos.

Efeitos da sazonalidade e do tamanho da planta hospedeira na abundância de galhas de Cecidomyiidae (Diptera) em Piper arboreum (Piperaceae) / Effects of seasonality and the size of host plants on abundance of Cecidomyiidae (Diptera) galls on Piper arboreum (Piperaceae)

Este trabalho teve por objetivo verificar se existem efeitos da sazonalidade e do tamanho da planta hospedeira na ocorrência de galhas de Cecidomyiidae (Diptera) em Piper arboreum (Piperaceae). O estudo foi conduzido mensalmente de setembro/2006 a agosto/2007, em uma área remanescente de Mata Mesófila Semidecídua em Goiânia, Goiás, Brasil. Em cada coleta, 10 indivíduos da planta hospedeira foram escolhidos aleatoriamente, e a altura, o número total de folhas, o número de folhas com galhas e o número de galhas por folhas foram estimados. A abundância de galhas variou significativamente durante o período de estudo, sendo que a maior abundância foi encontrada no início da estação chuvosa. A altura da planta hospedeira e o número de folhas por indivíduo também estiveram positivamente e significativamente relacionados com a abundância de galhas, uma vez que, plantas maiores oferecem maior disponibilidade de recursos e sítios de oviposição. Os resultados do presente estudo apontam que a sazonalidade pode ser tão determinante na abundância de galhas quanto os padrões arquitetônicos da planta hospedeira. As mudanças sazonais podem influenciar diretamente o desenvolvimento da planta hospedeira e assim, alterar a quantidade e a qualidade dos nutrientes oferecidos aos insetos galhadores.

The objective of this work was to verify the effects of seasonality and the size of host plants on occurrence of Cecidomyiidae (Diptera) galls on Piper arboreum (Piperaceae). This study was carried out monthly, from September, 2006 to August, 2007, in a remnant area of Semidecidual Forest in Goiânia, Goiás, Brazil. In each survey, 10 individuals of the host plant were chosen randomly, and the height, the total number of leaves, the number of leaves with galls and the number of galls per leaves were estimated. The abundance of galls varied significantly during the study period, being the greatest abundance found at the beginning of the rainy season. The height of the host plant and number of leaves per individual were also positively and significantly related to the abundance of galls, since larger plants offer greater availability of resources and sites of breeding. The results of this study suggest that the seasonality may be decisive in the abundance of galls as well as the architectural patterns of the host plant. The seasonal changes can directly influence the development of the host plant and thus alter the quantity and quality of nutrients offered to insects galling.