Community structure and specialization in fig wasps (Hymenoptera: Chalcidoidea) in a region of Cerrado

ABSTRACT 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 structure and degree of specialization of the fig wasp community associated with Ficus inflorescences in urbanized areas, agroecosystems, and on the edge of forest fragments in the state of Goiás (Brazil). We sampled 34 wasp species in four native Ficus tree species, from which four wasp species occurred in more than one host. Neotropical fig pollinators (Pegoscapus and Tetrapus) were the most abundant species, and they were host-specific, although two pollinator species were associated with Ficus obtusifolia. The Jaccard similarity index was higher in samples of fig wasps collected in the same host, indicating that the community composition was specific to each host species. Community structure indices indicate a specialized structure with low connectance, high bidimensional Shannon H2' and low partner diversity. The communities present a modular web structure in which modules were represented by each host and its associated insect species. These results indicate that the fig wasp communities analyzed are highly specialized, despite a few not strictly host-specific species.

What makes a fig: insights from a comparative analysis of inflorescence morphogenesis in Moraceae.

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 receptacle shape. Thus, the objective of the present study was to compare the inflorescence morphogenesis of Moraceae species, to investigate whether clades with a similar pollination mode share the same patterns of inflorescence development and the developmental stages at which we observe the key changes resulting in the diversified inflorescence architecture that culminates in the Ficus syconium. METHODS: Inflorescences at different developmental stages were sampled from Brosimum gaudichaudii, Castilla elastica, Clarisia ilicifolia, Ficus pertusa, Maclura tinctoria and Morus nigra and processed for surface and anatomical analyses. KEY RESULTS: The inflorescence morphogenesis of the studied species is highly variable. The shape of the inflorescence meristem (bulging, hemispheric or elongated), the initiation order and arrangement of flowers along the receptacle and the occurrence of bracts vary between related species. This diversity originates early during inflorescence development. Brosimum gaudichaudii, C. elastica and F. pertusa have flowers enclosed or immersed within the receptacle, although inflorescences begin their development as flat and open structures, as occurs in the other three study species. CONCLUSION: Comparison of the inflorescence morphogenesis in Moraceae species allows us to infer that evolutionary ontogenetic changes driven by pollinators culminate in the enclosure of flowers inside the receptacle, as occurs in the Ficus syconium.

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.

Atlantic forests to the all Americas: Biogeographical history and divergence times of Neotropical Ficus (Moraceae).

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 diversification of Ficus in the Americas, we produced a dated Bayesian phylogenetic hypothesis of Neotropical Ficus including two thirds of the species sequenced for five nuclear regions (At103, ETS, G3pdh, ITS/5.8S and Tpi). Ancestral range was estimated using all models available in Biogeobears and Binary State Speciation and Extinction analysis was used to evaluate the role of the initial habit and propagule size in diversification. The phylogenetic analyses resolved both Neotropical sections as monophyletic but the internal relationships between species in section Americanae remain unclear. Ficus started their diversification in the Neotropics between the Oligocene and Miocene. The genus experienced two bursts of diversification: in the middle Miocene and the Pliocene. Colonization events from the Amazon to adjacent areas coincide with the end of the Pebas system (10 Mya) and the connection of landmasses. Divergence of endemic species in the Atlantic forest is inferred to have happened after its isolation and the opening and consolidation of the Cerrado. Our results suggest a complex diversification in the Atlantic forest differing between postulated refuges and more instable areas in the South distribution of the forest. Finally the selection for initial hemiepiphytic habit and small to medium propagule size influenced the diversification and current distribution of the species at Neotropical forests marked by the historical instability and long-distance dispersal.

Naturalization of the bodhi fig tree (Ficus religiosa L. - Moraceae) in Brazil / Naturalização da figueira-dos-pagodes (Ficus religiosa L. - Moraceae) no Brasil

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 observing plantlets of F. religiosa growing on buildings in Rio de Janeiro city, Brazil, showing that this species was hosting pollinating wasps and, consequently, undertaking sexual reproduction outside its native range. We observed that Platyscapa quadraticeps Mayr, 1885, the original pollinator in Asia, was occurring in figs of F. religiosa in Brazil. Considering that several non-pollinating fig wasp species are associated with F. religiosa in its native areas, novel occurrences of wasps may be reported in the future in Brazil. The presence of the native pollinator provides conditions for this exotic tree to become naturalized and/or invasive in Brazil, potentially causing considerable damage to buildings and urban trees.

Ficus religiosa L. é uma das figueiras ornamentais mais valorizadas. Nativa da Ásia, é conhecida popularmente como figueira-dos-pagodes. Como as figueiras apresentam um mutualismo especializado com vespas Agaonidae as espécies exóticas geralmente não se reproduzem sexualmente devido a falta dos polinizadores específicos. Desde 2005 nós observamos plantas jovens de F. religiosa crescendo sobre construções na cidade do Rio de Janeiro, Brasil, indicando que esta espécie está interagindo com vespas polinizadoras e, consequentemente, se reproduzindo sexualmente fora de sua área nativa. Observamos que Platyscapa quadraticeps Mayr, 1885, o polinizador original na Ásia, estava ocorrendo em figos dessa espécie no Brasil. Considerando que várias espécies não-polinizadoras de vespas de figo são associadas a F. religiosa em suas áreas nativas, novas ocorrências de vespas podem ser relatadas no futuro no Brasil. A presença do polinizador nativo provem condições para que esta espécie exótica se naturalize e/ou se torne invasiva no Brasil, com grande potencial de causar danos em prédios e árvores urbanos.

An extreme case of plant-insect codiversification: figs and fig-pollinating wasps.

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 contemporaneous plant-insect diversification might be expected is the obligate mutualism between fig trees (Ficus species, Moraceae) and their pollinating wasps (Agaonidae, Hymenoptera). The ubiquity and ecological significance of this mutualism in tropical and subtropical ecosystems has long intrigued biologists, but the systematic challenge posed by >750 interacting species pairs has hindered progress toward understanding its evolutionary history. In particular, taxon sampling and analytical tools have been insufficient for large-scale cophylogenetic analyses. Here, we sampled nearly 200 interacting pairs of fig and wasp species from across the globe. Two supermatrices were assembled: on an average, wasps had sequences from 77% of 6 genes (5.6 kb), figs had sequences from 60% of 5 genes (5.5 kb), and overall 850 new DNA sequences were generated for this study. We also developed a new analytical tool, Jane 2, for event-based phylogenetic reconciliation analysis of very large data sets. Separate Bayesian phylogenetic analyses for figs and fig wasps under relaxed molecular clock assumptions indicate Cretaceous diversification of crown groups and contemporaneous divergence for nearly half of all fig and pollinator lineages. Event-based cophylogenetic analyses further support the codiversification hypothesis. Biogeographic analyses indicate that the present-day distribution of fig and pollinator lineages is consistent with a Eurasian origin and subsequent dispersal, rather than with Gondwanan vicariance. Overall, our findings indicate that the fig-pollinator mutualism represents an extreme case among plant-insect interactions of coordinated dispersal and long-term codiversification. [Biogeography; coevolution; cospeciation; host switching; long-branch attraction; phylogeny.].

Transferability and characterization of microsatellite markers in two Neotropical Ficus species.

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 transferred to both of the above species. Eleven loci were polymorphic when tested across 60 F. citrifolia and 60 F. eximia individuals. For F. citrifolia, there were 4 to 15 alleles per locus, whereas expected heterozygosities ranged from 0.31 to 0.91. In the case of F. eximia, this was 2 to 12 alleles per locus and expected heterozygosities from 0.42 to 0.87.

Transferability and characterization of microsatellite markers in two Neotropical Ficus species

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 percent) were successfully transferred to both of the above species. Eleven loci were polymorphic when tested across 60 F. citrifolia and 60 F. eximia individuals. For F. citrifolia, there were 4 to 15 alleles per locus, whereas expected heterozygosities ranged from 0.31 to 0.91. In the case of F. eximia, this was 2 to 12 alleles per locus and expected heterozygosities from 0.42 to 0.87.

Mating strategies and aggressive combat in wingless neotropical fig wasp males

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 injury within-species variables correlate with fig/population features? Consistently higher injury levels were observed in the two species of Idarnes than in the pollinator species. The results suggested that aggressive confrontations were involved in the mating strategies of Idarnes, whereas non-aggressive strategies were shown by males of P. tonduzi. Generally, injury variables in Idarnes spp. correlated positively with the male encounter rate and negatively with the fig size, thus supporting the contest competition theory. The results pointed out that different species under similar local conditions might follow distinct evolutionary histories. Within species, natural-history particularities might have some influence upon quantified injury levels in wingless males.

Estudamos machos ápteros da espécie polinizadora (Pegoscapus tonduzi) e de duas espécies não-polinizadoras, gênero Idarnes, de vespas de figo associadas à Ficus citrifolia no Brasil, para responder as seguintes questões: 1) Os machos ápteros de Idarnes spp. e P. tonduzi apresentam estratégias diferentes de competição entre machos?; e 2) As variáveis associadas às injúrias são correlacionadas às características populacionais de cada espécie? Os níveis de injúrias foram maiores nas duas espécies de Idarnes. Nossos resultados sugerem que combates agressivos fazem parte da estratégia de acasalamento de Idarnes, ao passo que machos de P. tonduzi adotam estratégias não agressivas. Em geral, as variáveis de injúria correlacionaram-se positivamente à taxa de encontros entre machos e negativamente ao tamanho do figo, apoiando a teoria de competição direta. Nossos resultados apontaram que espécies diferentes sob condições similares podem seguir histórias evolutivas distintas. Particularidades da história natural das espécies podem influenciar o nível de injúria quantificado nos machos ápteros.

Components of fecundity and abortion in a tropical tree, Dahlstedtia pentaphylla (Leguminosae)

Studies were conducted on pollination and patterns of fruit and seed production to assess the potential factors causing high fruit and seed abortion in Dahlstedtia pentaphylla (Leguminosae) through analyses of relationships between flower position in the inflorescence and ovules and seeds within ovaries and fruits, and flower, fruit and seed abortion. No differences were found in pollination and fruit set as a function of inflorescence position. There was no relationship, neither between degenerating ovules and their position within the ovary, nor between developing seed and fruit position. Maternal resource limitation related to fruits and embryos, due to the high cost of fruit production and seed maturation, was one of the factors that led to a high abortion rate in D. pentaphylla.

Este trabalho estudou o efeito dos componentes de fecundidade na reprodução de Dahlstedtia pentaphylla, leguminosa neotropical com baixa produção de frutos e sementes. Para tal, foram analisadas as relações das posições das flores na inflorescência e dos óvulos/sementes no ovário/fruto ao aborto de frutos e sementes. Não ocorreram diferenças na deposição de pólen em flores e na formação de frutos em função da posição na inflorescência. Não se encontrou também relação entre aborto de óvulos/sementes e sua posição no ovário/fruto. A limitação dos recursos maternos aos frutos e aos embriões, devido ao alto custo de formação de frutos e maturação das sementes, foi um dos fatores responsáveis pelas altas taxas de aborto nesta espécie.