Rodrigo Pereira

• PhD
• University of São Paulo

Understanding tri-trophic interactions and the relationship among plants, herbivores, and their natural enemies is fundamental to advancing theoretical and practical ecology. Parasitoidism is among those interactions where tri-trophic levels are usually developed, with hyperparasitism and kleptoparasitism as examples. This study explores the intera...

In the complex dynamics of plant–insect interactions, the specialized galling of reproductive structures presents unique evolutionary adaptations. This study investigates the parasitic relationship between Arastichus gallicola (Hymenoptera, Eulophidae), an ovary-galling wasp, and the inflorescences of Thaumatophyllum bipinnatifidum (Araceae). We em...

The evolution of host specialization and feeding habits in non‐pollinating fig wasps remains poorly understood. This study investigates these dynamics within the wasp genus Idarnes , which exhibits diverse life strategies and degrees of host specificity. We reconstructed the phylogeny of 57 Idarnes species using four genetic markers—two mitochondri...

Understanding the ecological and evolutionary aspects of mutualistic interactions is essential for predicting species responses to environmental changes. This study aimed to investigate the phenological patterns and reproductive strategies in two closely related fig tree species, Ficus citrifolia and Ficus eximia. We monitored 99 F. citrifolia and...

A female-biased clutch sex ratio is selected under local mate competition since it reduces competition between male sibs and provides extra mating opportunities for sons. Theoretical models predict that the brood sex ratio of fig wasps becomes less female-biased as the number of wasps laying eggs in the same fig increases. Empirical data have demon...

Encounters between flowers and invertebrates are key events for the functioning of tropical forests. Assessing the structure of networks composed of the interactions between those partners leads to a better understanding of ecosystem functioning and the effects of environmental factors on ecological processes. Gathering such data is, however, costl...

Ficus inflorescences host a species-rich chalcid wasp community, including pollinating fig wasps (Agaonidae: Tetrapusinae, Kradibiinae, and Agaoninae) and several species of non-pollinating fig wasps (NPFW), that show several life-history strategies, including gall-inducers, kleptoparasites (i. e. inquilines), and parasitoids. We analyzed the struc...

1. Recent studies have demonstrated that the richness of pollinators in crop systems can improve productivity due to the effect of functional trait differences between species. These findings reinforce the potential effectiveness of integrated management of both Apis and non-Apis bees to ensure global crop yields. 2. Thus, we used meta-analysis tec...

Mutualism is ubiquitous in nature and probably all species in the world are involved in some form of such ecological interaction. The evolution of mutualisms is often envisioned in a framework where individual selection leads to reciprocal exploitation that results in net benefits to all the interacting parties, i.e. in a framework in which individ...

Ficus (figs) and their agaonid wasp pollinators present an ecologically important mutualism that also provides a rich comparative system for studying functional co-diversification throughout its coevolutionary history (~75 million years). We obtained entire nuclear, mitochondrial, and chloroplast genomes for 15 species representing all major clades...

As plantas do gênero Ficus constituem um recurso-chave para o funcionamento de florestas tropicais, pois provêem alimento para animais frugívoros em períodos de escassez de frutos de outras espécies. Além disso, as figueiras apresentam um papel importante na regeneração e recomposição de comunidades vegetais, atraindo animais frugívoros dispersores...

The synstigma is a structure formed by clusters of two to several stigmas, whether in the same or between different flowers. Although rare in angiosperms, synstigmas are found in c. 500 out of the c. 750 Ficus spp. (Moraceae). This floral structure is associated with fig-fig wasp pollinating mutualism. The synstigma structure and pollen tube pathwa...

Background and Aims Moraceae, the family of mulberry and fig trees, displays small homogeneous flowers but extremely diverse inflorescences ranging from simple and branched to complex and condensed. Inflorescences also vary in flower organization in the receptacle, in the degree of flower condensation, and in the receptacle shape. Thus, the objecti...

Despite many attempts in the Sanger sequencing era, the phylogeny of fig trees remains unresolved, which limits our ability to analyze the evolution of key traits that may have contributed to their evolutionary and ecological success. We used restriction-site-associated DNA sequencing (c. 420 kb) and 102 morphological characters to elucidate the re...

The association between ontogenetic processes in plants and phytophagous insects is not traditionally considered in studies of insect-plant interactions. Angiosperm seeds impose important constraints on seed predators; the structural complexity of seeds and the progressive accumulation of resources throughout their development limit the time window...

The association between ontogenetic processes in plants and phytophagous insects is not traditionally considered in studies of insect-plant interactions. Angiosperm seeds impose important constraints on seed predators; the structural complexity of seeds and the progressive accumulation of resources throughout their development limit the time window...

Eulophidae is a hyper-diverse family of chalcidoid wasps with 324 genera, about 5300 described species and probably thousands of others to be described. Until now, the absence of unequivocal morphological apomorphies and the low resolution provided by the handful of Sanger sequenced genes have hampered the reconstruction of phylogenetic relationshi...

Despite their ecological and evolutionary importance as key components of tropical ecosystems, the phylogeny of fig trees is still unresolved. We use restriction-site-associated DNA (RAD) sequencing (ca 420kb) and 102 morphological characters to elucidate the relationships between 70 species of Ficus representing all known subgenera and sections an...

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 require...

Epiphytes are hyper‐diverse and one of the frequently undervalued life forms in plant surveys and biodiversity inventories. Epiphytes of the Atlantic Forest, one of the most endangered ecosystems in the world, have high endemism and radiated recently in the Pliocene. We aimed to (1) compile an extensive Atlantic Forest data set on vascular, non‐vas...

Biotic invasion in mutualistic communities is of particular interest due to the possible establishment of new relationships with native species. Ficus species are widely cultivated as ornamental plants, and they host specific communities of chalcid wasps that are strictly associated with the fig inflorescences. Some introduced fig species are capab...

Mutualistic relationships are open to exploitation by non-cooperative species that can reduce the fitness of one or both cooperating partners. In addition to their obligate agaonid pollinators, a diverse community of non-pollinating fig wasps (NPFW) also uses the figs as a resource for the development of their broods. Some species of NPFW are gall...

The galling habit represents a complex type of interaction between insects and plants, ranging from antagonism to mutualism. The obligate pollination mutualism between Ficus and fig wasps relies strongly on the induction of galls in Ficus flowers, where wasps' offspring develop. Even though gall induction plays an important role in many insect-plan...

Mass spectra obtained by MALDI-TOF MS (linear positive ion mode) from reservoirs of the galling wasp Pegoscapus sp. Analyses were carried out immediately after dissection (A) and after 6 weeks of storage at 2–6°C (B). (PDF)

Total ion chromatogram of venom reservoirs obtained using GC-MS. Spectra correspond to non-galling wasp Idarnes sp. 1 (A), galling wasp Idarnes sp. 3 (B) and the solvent, which was used as control (C). (PDF)

Total ion chromatogram of venom reservoirs obtained using UPLC-ESI MS in negative ion mode. Spectra correspond to galling wasp Idarnes sp. 3 (A), non-galling wasp Idarnes sp. 1 (B) and the solvent, which was used as control (C). (PDF)

Mass spectra obtained by MALDI-TOF MS (linear positive ion mode) from three different samples (each sample consists of a pool of 10 reservoirs) of the galling wasp Pegoscapus aerumnosus. (PDF)

Mass spectrum obtained by MALDI-TOF (reflector positive ion mode) from reservoirs of the non-galling wasp Sycoryctes aff. trifemmensis. (PDF)

Extracted ion chromatogram of ion m/z 204 obtained using UPLC-ESI MS in positive ion mode. Spectra correspond to venom reservoirs from galling wasp Idarnes sp. 3 (A), venom reservoirs from non-galling wasp Idarnes sp. 1 (B) and the solvent, which was used as control (C). (PDF)

Mass spectrum obtained by MALDI-TOF (linear positive ion mode) from reservoirs of the non-galling wasp Sycoryctes aff. trifemmensis. (PDF)

Partial Least Squares Discriminant Analysis based on the intensity matrix of ions detected by MALDI-TOF MS in the 1–20 KDa range. Samples from pollinating ovary-galling wasps are represented by cubes (Pegoscapus sp. in light blue and Ceratosolen solmsi in pink). Samples from non-pollinating ovary-galling wasps are represented by tetrahedrons (Idarn...

Studied fig wasp species. a- Ceratosolen solmsi (pollinating ovary-galling species); b- Pegoscapus sp. (pollinating ovary-galling species); c- Sycophaga sp. (non—pollinating ovary-galling species); d- Idarnes sp. 3 (non—pollinating ovary-galling species); e- Philotrypesis pilosa (cleptoparasite); f- Idarnes sp. 1 (cleptoparasite); g- Sycoryctes aff...

Ranking of the ten most important discriminant peaks in the partial least squares discriminant analysis. Analysis was based on the intensity matrix of ions detected from venom reservoir samples by MALDI-TOF MS in the 1–20 KDa range. (PDF)

Extracted ion chromatogram of ion m/z 174 [M-H]- (relative to indole-3-acetic acid) obtained using UPLC-ESI MS in negative ion mode. Spectra correspond to venom reservoirs from galling wasp Idarnes sp. 3 (A), venom reservoirs from non-galling wasp Idarnes sp. 1 (B) and the solvent, which was used as control (C). (PDF)

Extracted ion chromatogram of ion m/z 220 [M+H]+ obtained using UPLC-ESI MS in positive ion mode. Spectra correspond to venom reservoirs from galling wasp Idarnes sp. 3 (A), venom reservoirs from non-galling wasp Idarnes sp. 1 (B) and the solvent, which was used as control (C). (PDF)

Extracted ion chromatogram of ion m/z 336 obtained using UPLC-ESI MS in positive ion mode. Spectra correspond to venom reservoirs from galling wasp Idarnes sp. 3 (A), venom reservoirs from non-galling wasp Idarnes sp. 1 (B) and the solvent, which was used as control (C). (PDF)

Insects show a multitude of symbiotic interactions that may vary in degree of specialization and structure. Gall-inducing insects and their parasitoids are thought to be relatively specialized organisms, but despite their ecological importance, the organization and structure of the interactions they establish with their hosts has seldom been invest...

Hymenopteran insects have meroistic polytrophic ovaries characterised by trophocytes associated with oocytes inside the follicles. In pro-ovigenic species, all oocytes mature before emergence and no trace of oogenesis is visible in adult females. Pro-ovigeny is a rare condition among Hymenoptera, but common in pollinating fig wasps. In the present...

We used recent taxonomic revisions of extra-Amazonian Brazil and material deposited in herbaria to compile the checklist of Ficus for Mato Grosso do Sul state. Twelve species of Ficus are listed for the state (10 from the section Americanae and 2 from the section Pharmacosycea). We highlight the occurrence of an endemic species to the Pantanal (F....

The stigma plays several roles such as pollen hydration and selection, and pollen tube nutrition. In the Ficus-fig wasp mutualism, stigmata have an additional, almost unknown, function by representing a physical interface for both plant and wasp reproduction. We used light and electron microscopy to compare the detailed morphology of the stigmata o...

Ficus (Moraceae) is well diversified in the Neotropics with two lineages inhabiting the wet forests of this region. The hemiepiphytes of section Americanae are the most diversified with c. 120 species, whereas section Pharmacosycea includes about 20 species mostly with a terrestrial habit. To reconstruct the biogeographical history and diversificat...

The high adaptive success of parasitic Hymenoptera might be related to the use of different oviposition sites, allowing niche partitioning among co-occurring species resulting in life history specialization and diversification. In this scenario, evolutionary changes in life history and resources for oviposition can be associated with changes in ovi...

Although in Moraceae the presence of laticifers is considered to be a synapomorphy, little is known about the distribution and morphology of this type of secretory structure in the reproductive organs of its species. Ficus, the largest genus of Moraceae, is characterized by an inflorescence known as syconium and by an obligate mutualistic interacti...

The two seminal papers by Galil and Eisikowitch describing the development of Ficus flowers and their sycophilous wasps (i.e., phases A-E) have been adopted in several ecological and evolutionary studies on a wide range of fig tree-insect interactions. Their classification, however, is not inclusive enough to encompass all the diversity of insects...

We investigated spatial genetic structuring in two vicariant Ficus spp. (F. insipida and F. adhatodifolia), occurring in the Amazon Forest and the Atlantic Forest, respectively. We explain this structuring in a phylogeographical framework of variation in the extent and location of favourable habitats for the two species during climatic oscillations...

Ficus religiosa L. is one of the most valued cultivated ornamental fig trees. Native to Asia, it is known as Bodhi tree. Since fig trees are involved in a highly species-specific pollination mutualism with agaonid wasps, exotic fig species usually fail to produce seeds due to the lack of the specific pollinating wasps. Since 2005 we have been obser...

Sycophaginae is a group of non-pollinating fig wasps considered closely related to the fig pollinators (Agaoninae, Tetrapusiinae, and Kradibiinae) in the most recent phylogenetic analyses. They occur in all tropical regions and are associated with Ficus subgenera Urostigma and Sycomorus. There are six described genera of Sycophaginae, and two are n...

GenBank assession numbers and sampling information Sampling information and GenBank assession numbers for Idarnes incertus sp. gp species and outgroups

Lucid key Idarnes incertus sp. g Multi-entry taxonomic key for Idarnes incertus species-group. The kay is assembled in Lucid: http://www.lucidcentral.com

Measurements Measurements for Idarnes incertus sp. g. species in mm

Species re-descriptions and additional images Idarnes incertus sp. gp. Species re-descriptions and additional images.

MrBayes file and alignment Nexus file with alignment and MrBayes block with parameters for phylogenetic analysis.

Fig trees and their pollinating fig wasps arose about 75 million years ago in the Cretaceous period. Several other groups of chalcid wasps also utilize figs for larval development, including sycophagines, the putative sister group to pollinating fig wasps. Whereas stone and amber fossil pollinators are known, no fossils representing non-pollinating...

An updated inventory of Brazilian seed plants is presented and offers important insights into the country’s biodiversity. This work started in 2010, with the publication of the Plants and Fungi Catalogue, and has been updated since by more than 430 specialists working online. Brazil is home to 32,086 native Angiosperms and 23 native Gymnosperms, sh...

An updated inventory of Brazilian seed plants is presented and offers important insights into the country’s biodiversity. This work started in 2010, with the publication of the Plants and Fungi Catalogue, and has been updated since by more than 430 specialists working online. Brazil is home to 32,086 native Angiosperms and 23 native Gymnosperms, sh...

Premise of the study: Fig trees (Moraceae) have remarkable enclosed inflorescences called figs or syconia. The flowers are pollinated by host-specific fig wasps that enter the fig to lay their eggs. This nursery pollination system is one of the most studied of tropical mutualism interactions, but the source of the volatiles that attract fig wasps...

1. The transportation of plants and insects between countries often has negative consequences, but also provides opportunities to study community processes. Fig trees are a species-rich group of largely tropical and subtropical plants, characterised by their unusual inflorescences (figs). 2. Ficus microcarpa is a native of Asia and Australasia and...

Aggressive contests between animals are common but rarely result in death because the benefits of winning a fight rarely exceed the cost of losing. Lethal combat can evolve, however, when the contested resource translates to much of the future reproductive success of each combatant. Female agaonid fig wasps pollinate and lay their eggs in the flowe...

This chapter discusses the role of wasps as pollinators, placing them in the general context of insect pollination. Information available in the literature was used to classify wasps into generalist pollinators, pollinators specialized in plants without resources (pollination by mistake) and pollinators specialized in plants with resources. Althoug...

Astract Ecological theory predicts that communities using the same resources should have similar structure, but evolutionary constraints on colonisation and niche shifts may hamper such convergence. Multitrophic communities of wasps exploiting fig fruits, which first evolved about 75 MYA , do not show long‐term ‘inheritance’ of taxonomic (lineage)...

ABstrACt. Paracrias strii Schauff, 1985 and P. ceratophaga Palmieri & Hansson sp. nov. are first record in Brazil and both are associated with Ceratopus Schoenherr larvae (Coleoptera, Curculionidae) reared from syconia of two species of fig-trees. Both Paracrias species are diagnosed and illustrated. Males of P. ceratophaga sp. nov. are described....

In this analysis, we attempt to understand how monoecy and dioecy drive spatial genetic structure (SGS) in plant populations. For this purpose, plants of the genus Ficus were used as a comparative model due to their particular characteristics, including high species diversity, variation in life histories, and sexual systems. One of the main issues...

Besides the pollinators (Agaonidae), several chalcidoid lineages of non-pollinating fig wasps are strictly dependent on Ficus (Moraceae) for reproduction. Overall, non-pollinating fig wasps have not received much consideration. Reliable phylogenetic and taxonomic frameworks are lacking for most groups, which hampers progress in our understanding of...

Recent studies on the obligate interaction between fig trees and their pollinating agaonid wasps have focused on population aspects and wasp–seed exploitation at the level of the inflorescence. Detailed studies on larval and gall development are required to more fully understand how resources are exploited and adaptations fine-tuned by each partner...

It is thought that speciation in phytophagous insects is often due to colonization of novel host plants, because radiations of plant and insect lineages are typically asynchronous. Recent phylogenetic comparisons have supported this model of diversification for both insect herbivores and specialized pollinators. An exceptional case where contempora...

Mutualisms such as the fig–fig wasp mutualism are generally exploited by parasites. We demonstrate that amongst nonpollinating fig wasps (NPFWs) parasitic on Ficus citrifolia, a species of Idarnes galls flowers and another species feeds on galls induced by other wasps killing their larvae. The galling wasp inserts its ovipositor through the fig wal...

At least three classic systems of nursery pollination mutualism are known: the fig (Ficus, Moraceae) – agaonid (Hymenoptera, Chalcidoidea) association (Cook and Rasplus 2003), the yucca (Yucca, Hesperoyucca; Agavaceae) – yucca moths (Tegeticula, Parategeticula; Lepidoptera, Prodoxidae) association (Pellmyr 2003) and the Glodichion (Phyllanthaceae)...

Lifetime reproductive success in female insects is often egg-or time-limited. For instance in pro-ovigenic species, when oviposition sites are abundant, females may quickly become devoid of eggs. Conversely, in the absence of suitable oviposition sites, females may die before laying all of their eggs. In pollinating fig wasps (Hymenoptera: Agaonida...

Table S1. List of Sycophaginae and outgroup species included in this study. Voucher numbers, taxonomic information, host Ficus species, locality data and GenBank accession numbers for each sequenced fragment. More information is available from the authors upon request.

Non-pollinating Sycophaginae (Hymenoptera, Chalcidoidea) form small communities within Urostigma and Sycomorus fig trees. The species show differences in galling habits and exhibit apterous, winged or dimorphic males. The large gall inducers oviposit early in syconium development and lay few eggs; the small gall inducers lay more eggs soon after po...

Arthropods are sexually dimorphic. An arthropod individual usually diff erentiates into a male or a female. With very low frequencies, however, individuals with both male and female morphological characters have repeatedly been found in natural and laboratory populations of arthropods. Gynandromorphs (i.e., sexual mosaics) are genetically chimeric...

Muitas espécies de Ficus desempenham um importante papel como fonte de recursos alimentares para a fauna silvestre, tendo, portanto, potencial de utilização em projetos de recuperação de ambientes degradados. Desta forma o estudo da fenologia de espécies de Ficus permitirá estabelecer estratégias para o seu manejo em unidades de conservação. Com o...

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Ficus microcarpa is an Asian fig tree that is ornamentally cultivated. The specific pollinator, Eupristina verticillata Waterston, and the non-pollinators Walkerella microcarpae Boucek and Philotrypesis emeryi Grandi, have been reported associated to F. microcarpa in Brazil. In here we report for the first time the occurrence of Odontofroggatia ish...

Microsatellite markers were transferred and characterized for two Neotropical fig tree species, Ficus citrifolia and Ficus eximia. Our study demonstrated that microsatellite markers developed from different subgenera of Ficus can be transferred to related species. In the present case, 12 of the 15 primer pairs tested (80%) were successfully transfe...

The aim of this work was to study the wingless males of pollinating (Pegoscapus tonduzi) and two nonpollinating fig wasp species, genus Idarnes, associated with figs (Ficus citrifolia) in Brazil to answer the following questions: 1) Do wingless males of Idarnes spp. and P. tonduzi show different male-male competition strategies?; and, 2) Do the inj...

Mutualisms, such as the fig-agaonid wasp association, are susceptible to colonization by parasitic species, which exploit the resources involved therein. In most cases, they oviposit into the figs from outside without providing any pollination service. In this study, we used several different methods (adhesive traps and direct standardized field ob...

Males of pollinating and some non-pollinating fig wasps are wingless and quite dissimilar to their co-specific females. Due to the accentuated sexual dimorphism, males and females of some fig wasp species were described in different genera. We used morphological sperm features obtained from male seminal vesicles and female spermathecas to associate...

The interaction between Ficus (Moraceae) and fig wasps is considered one of the most extreme examples of plant-insect mutualism. In the present study, we reported the fig wasp fauna associated with five Ficus species in the Central Amazon, Brazil, and considered some aspects of the pollination mode found in Ficus (Urostigma) cremersii, Ficus (Urost...