Plasticity and diversity of the phenology of dioecious Ficus species in Taiwan

While Ficus present a series of traits often associated with dioecy, the prevalence of dioecy in Ficus is atypical. In Asian floras, dioecious Ficus species generally outnumber monoecious ones. Further this is also true in relatively northerly locations for Ficus such as the island of Taiwan. Ficus are pollinated by species-specific wasps that use fig flowers as breeding sites. In dioecious fig species, pollinators develop only in the inflorescences of male fig trees. In this study, we investigated the reproductive phenology of four dioecious Ficus species with distinct ecologies in several locations in northern and southern Taiwan. The two first species (Ficus erecta and Ficus septica) were investigated in four locations. Reproductive phenology was quite different among sites, even within a single species. For example, F. erecta presented well-defined crops at the population level in its usual high-elevation habitat but continuous fig production at low elevations, especially in South Taiwan. The two other fig species (Ficus pedunculosa var. mearnsii and Ficus tinctoria subsp. swinhoei), are shrubs growing together along seashores in exposed locations on coral reef remnants. These two species presented quite different traits allowing the survival of pollinating wasp populations. Ficus pedunculosa var. mearnsii produced figs continuously so that fresh receptive figs were always available for the pollinating wasps while F. tinctoria subsp. swinhoei extended the period of receptivity of its figs, so that receptive figs that had been waiting for pollinating wasps were almost always available. In summary, dioecious figs in Taiwan showed remarkable variation in their phenology, within species among locations or among species within location. Nevertheless, despite this variation, the phenology of the trees always allowed survival of pollinating wasp populations. Dioecious figs seem to have adopted a differentiated set of strategies which result in high resilience of pollinator populations. This resilience could help explain the atypical prevalence of dioecy in Ficus.     

Daily Rhythm of Mutualistic Pollinator Activity and Scent Emission in Ficus septica: Ecological Differentiation between Co-Occurring Pollinators and Potential Consequences for Chemical Communication and Facilitation of Host Speciation

The mutualistic interaction between Ficus and their pollinating agaonid wasps constitutes an extreme example of plant-insect co-diversification. Most Ficus species are locally associated with a single specific agaonid wasp species. Specificity is ensured by each fig species emitting a distinctive attractive scent. However, cases of widespread coexistence of two agaonid wasp species on the same Ficus species are documented. Here we document the coexistence of two agaonid wasp species in Ficus septica: one yellow-colored and one black-colored. Our results suggest that their coexistence is facilitated by divergent ecological traits. The black species is longer-lived (a few more hours) and is hence active until later in the afternoon. Some traits of the yellow species must compensate for this advantage for their coexistence to be stable. In addition, we show that the composition of the scent emitted by receptive figs changes between sunrise and noon. The two species may therefore be exposed to somewhat different ranges of receptive fig scent composition and may consequently diverge in the way they perceive and/or respond to scents. Whether such situations may lead to host plant speciation is an open question.     

Intra- and interspecific variations in vacuolar flavonoids among Ficus species from the Budongo Forest,Uganda

Leaves of 14 species of Ficus growing in the Budongo Forest, Uganda, were analysed for vacuolar flavonoids. Three to six accessions were studied for each species to see whether there was intraspecific chemical variation. Thirty-nine phenolic compounds were identified or characterised, including 14 flavonol O-glycosides, six flavone O-glycosides and 15 flavone C-glycosides. In some species the flavonoid glycosides were acylated. Ficus thonningii contained in addition four stilbenes including glycosides. Most of the species could be distinguished from each other on the basis of their flavonoid profiles, apart from Ficus sansibarica and Ficus saussureana, which showed a very strong intraspecific variation. However, on the whole flavonoid profiles were sufficiently distinct to help in future identifications.     

Paleoenvironment of Ankilitelo Cave (late Holocene, southwestern Madagascar): implications for the extinction of giant lemurs

Following human arrival, Madagascar suffered well-documented megafaunal extinctions and widespread deforestation. Although humans are widely considered to be the primary cause of the extinctions, the relative contributions of climate change and human activities to this ecological transformation remain uncertain. Reconstructing the habitats of the giant lemurs of Madagascar can provide key information for understanding the evolutionary mechanisms involved in their extinction. In this study, I present a faunal analysis of the subfossil assemblage from Ankilitelo Cave, southwestern Madagascar. This assemblage documents the latest known occurrence of five species of extinct giant lemur, in association with abundant well-preserved small mammal remains. I compared the small mammal fauna at Ankilitelo with 27 extant Malagasy mammal communities spanning the range of Madagascar's habitat types. Similarities in species composition between modern communities and Ankilitelo were assessed using cluster analysis. Ecological similarities were examined by assigning each species to dietary, locomotor, activity pattern, and body size categories. Multiple discriminant analysis was then used to classify Ankilitelo relative to modern habitat types in Madagascar, based on the ecological structure of the subfossil fauna. Results indicate that the habitat surrounding Ankilitelo during the late Holocene was similar to the succulent woodlands of modern southwestern Madagascar. This suggests that approximately 500 yr BP, these semi-arid habitats supported a subfossil lemur community that included the highly-suspensory Palaeopropithecus, and deliberate slow-climber Megaladapis, as well as Archaeolemur, Pachylemur, and Daubentonia robusta. In such environments, these giant lemurs would likely have been highly vulnerable to increasing human pressure in southwestern Madagascar.     

Fine‐scale Population Genetic Structure of Two Dioecious Indian Keystone Species,Ficus hispida and Ficus exasperata (Moraceae)

Although Ficus (Moraceae) is a keystone plant genus in the tropics, providing resources to many frugivorous vertebrates, its population genetic structure, which is an important determinant of its long‐term survival, has rarely been investigated. We examined the population genetic structure of two dioecious fig species (Ficus hispida and Ficus exasperata) in the Indian Western Ghats using co‐dominant nuclear microsatellite markers. We found high levels of microsatellite genetic diversity in both species. The regression slopes between genetic relationship coefficients (f_ij) and spatial distances were significantly negative in both species indicating that, on average, individuals in close spatial proximity were more likely to be related than individuals further apart. Mean parent–offspring distance (σ) calculated using these slopes was about 200 m in both species. This should be contrasted with the very long pollen dispersal distances documented for monoecious Ficus species. Nevertheless, overall population genetic diversity remained large suggesting immigrant gene flow. Further studies will be required to analyze broader scale patterns.     

Geographic and taxonomic distribution of a positive interaction: ant-tended homopterans indirectly benefit figs across southern Africa

Although species pairs and assemblages often occur across geographic regions, ecologists know very little about the outcome of their interactions on such large spatial scales. Here, we assess the geographic distribution and taxonomic diversity of a positive interaction involving ant-tended homopterans and fig trees in the genus Ficus. Previous experimental studies at a few locations in South Africa indicated that Ficus sur indirectly benefited from the presence of a homopteran (Hilda patruelis) because it attracted ants (primarily Pheidole megacephala) that reduced the effects of both pre-dispersal ovule gallers and parasitoids of pollinating wasps. Based on this work, we evaluated three conditions that must be met in order to support the hypothesis that this indirect interaction involves many fig species and occurs throughout much of southern Africa and Madagascar. Data on 429 trees distributed among five countries indicated that 20 of 38 Ficus species, and 46% of all trees sampled, had ants on their figs. Members of the Sycomorus subgenus were significantly more likely to attract ants than those in the Urostigma subgenus, and ant-colonization levels on these species were significantly greater than for Urostigma species. On average, each ant-occupied F.sur tree had 37% of its fig crop colonized by ants, whereas the value was 24% for other Ficus species. H. patruelis was the most common source for attracting ants, although figs were also attacked by a range of other ant-tended homopterans. P. megacephala was significantly more common on figs than other ant species, being present on 58% of sampled trees. Ant densities commonly exceeded 4.5 per fig, which a field experiment indicated was sufficient to provide protection from ovule gallers and parasitoids of pollinators. Forty-nine percent of all colonized F. sur trees sampled had ant densities equal to or greater than 4.5 per fig, whereas this value was 23% for other Ficus species. We conclude that there is considerable evidence to suggest that this indirect interaction occurs across four southern African countries and Madagascar, and involves many Ficus species. Received: 11 December 1997 / Accepted: 6 April 1998     

Different ontogenetic processes promote dicliny in Ficus L. (Moraceae)

The absence of reproductive organs in flowers may ontogenetically arise from inception or by abortion during development. Ficus L., a species-rich genus of angiosperms, is an interesting model for floral developmental studies because of the diversity of sexual systems it contains. This study compares the floral morphology of Ficus citrifolia (monoecious), Ficus religiosa (monoecious), Ficus racemosa (secondarily monoecious), and Ficus hispida (gynodioecious) across development to establish the ontogenetic pathways that result in diclinous flowers. Figs were collected at various developmental stages and were prepared for surface (scanning electron microscopy) and histological (light microscopy) analyses. Dicliny in Ficus is defined by stamen absence from inception in pistillate flowers and either pistil absence from inception (F. citrifolia, F. racemosa and F. religiosa) or by abortion (F. hispida) in staminate flowers. The perianth is formed by a single whorl of sepals, as found in other families related to Moraceae. The gynoecium is tubular during development, a condition that may be related with pseudomonomery. The staminate and neutral flowers in F. hispida develop by similar mechanisms. The diversity in the sexual systems in Ficus results from combinations of different floral morphs (dicliny), which originate from both previously established ontogenetic mechanisms (loss of reproductive organ function by abortion or from inception). These mechanisms act independently of phylogenetic proximity or mechanisms of sex system evolution in Ficus. Other aspects of floral development observed in Ficus are discussed in relation to their systematic position and reproductive biology.     

Living on the edge: Fig tree phenology at the northern range limit of monoecious Ficus in China

Fig trees (Ficus) are a species-rich group of mainly tropical and subtropical plants that are of ecological importance because of the large numbers of vertebrates that utilise their figs for food. Factors limiting their distributions to warmer regions are still poorly understood, but are likely to include factors linked to their specialised pollination biology, because each Ficus species is dependent on one or a small number of host-specific fig wasps (Agaonidae) for pollination. Adult fig wasps are short-lived, but some species are capable of dispersing extremely long distances to pollinate their hosts. Close to its northern range limit we investigated the phenology of Ficus virens, the monoecious fig tree that reaches furthest north in China. Relatively few trees produced any figs, and very few retained figs throughout the winter. Despite this, new crops produced in spring were pollinated, with seasonally migrant pollinators from plants growing further south the most likely pollen vectors. An inability to initiate new crops at low temperatures may limit the distribution of monoecious fig trees to warmer areas.     

Geographic structuring into vicariant species-pairs in a wide-ranging,high-dispersal plant–insect mutualism: the case of <Emphasis Type="Italic">Ficus racemosa</Emphasis> and its pollinating wasps

Ficus and their mutualistic pollinating wasps provide a unique model to investigate joint diversification in a high dispersal system. We investigate genetic structuring in an extremely wide-ranging Ficus species, Ficus racemosa, and its pollinating wasp throughout their range, which extends from India to Australia. Our samples were structured into four large, vicariant populations of figs and wasps which may correspond to distinct (sub)species, located in India, China-Thailand, Borneo, and Australia. However, the genetically most divergent group was the Indian population for the figs and the China-Thailand population for the wasps, suggesting different evolutionary histories of populations. Molecular dating for the wasps shows that diversification of the pollinator clade is surprisingly old, beginning about 13.6 Ma. Data on both the host fig species and its pollinating wasps suggest that strong genetic flow within biogeographic groups over several hundreds of kilometers has limited genetic and morphological differentiation and, potentially, local adaptation. This is probably due to long-distance dispersal of pollinating wasps. The genetic clustering into large geographic units observed in F. racemosa and its pollinators is reminiscent of what can be observed in some other high-dispersal organisms characterized by morphology that varies little over huge distances. The implications of strong gene flow for diversification processes and adaptation to different ecological conditions in Ficus and their pollinating wasps are just beginning to emerge.     

Sugar secretion and ant protection in Ficus benguetensis: Toward a general trend of fig–ant interactions

The relationship between plants and ants is often mediated by the presence of extrafloral nectaries (EFNs) that attract ants and provide rewards by protecting plants from herbivores or parasites. Ficus trees (Moraceae) and their pollinators (Hymenoptera: Agaonidae) are parasitized by many nonpollinating fig wasp species (Hymenoptera: Chalcidoidea) that decrease the reproductive output of the mutualistic partners. Previous studies have shown that ants living on and patrolling Ficus species can efficiently deter parasitic wasps. The aim of this study was to verify the presence of EFNs on figs of Ficus benguetensis and test the hypothetical protection service provided by ants. Figs in different developmental stages were collected from Fu-Yang Eco Park, Taipei, Taiwan. Sugars on the fig surface were collected and analyzed through high-performance anion-exchange chromatography. Moreover, ants were excluded from the figs to determine the effect of ants on the nonpollinating fig wasps. We identified three oligosaccharides whose relative proportions varied with the fig developmental phase. In addition, results showed that the ant-excluded figs were heavily parasitized and produced three times less pollinators than did the control figs. Finally, the specific interactions of Ficus benguetensis with ants and the relationship between figs and ants in general are discussed.     

Weak genetic divergence suggests extensive gene flow at the northeastern range limit of a dioecious Ficus species

Genus Ficus (Moraceae) plays a critical role in the sustainability and biodiversity in tropical and subtropical ecosystems. Ficus species and their host specific pollinating fig wasps (Agaonidae) represent a classic example of obligate mutualism. The genetic consequence of range expansion and range shift is still under investigation, but extensive gene flow and subsequently low level of genetic divergence may be expected to occur among the populations at the poleward range limit of some Ficus species due to long distance gene flow in the genus. In the present study, we focused on populations of F. sarmentosa var. henryi at its northeastern range limit in southeast China to test whether edge populations were genetically fragile. Consistent with our hypothesis, high level of genetic diversity and weak genetic structure were revealed in Ficus sarmentosa var. henryi populations, suggesting extensive gene flow at the plant's range limit. Long-distance movements of both pollinators and frugivorous birds were likely to be frequent and thereby predominantly contributed to the extensive gene flow at large scale despite of some magnificent landscape elements like huge mountains.     

Histological Comparisons of Parasitism by Schistonchus spp. (Nemata: Aphelenchoididae) in Neotropical Ficus spp.

Syconia (enclosed infructescences) infested with host-specific species of Schistonchus (Aphelenchoididae) were collected from six species of Ficus (Moraceae) native to Florida or Panama. They were sectioned and histologically examined to assess the effects of parasitism. Parasitism by Schistonchus spp. was associated with hypertrophied cells, tissue necrosis, and the presence of an exudate in all species. Occasional hypertrophy of the outer epidermal cells occurred on seed florets, wasp florets, and on the endothecial cells of male florets in F. aurea (subgenus Urostigma) from Florida. Aberrations of the inner mesocarp occurred under the hypertrophied cells on seed florets. In F. laevigata (subgenus Urostigma) from Florida, Schistonchus sp. infested immature male florets and was associated with hypertrophy of endothecial cells, epidermal cells of the anther filaments, and anthers. Schistonchus sp. also caused aberrations of the anther filament, anthers, and pollen. Ficus poponoei (subgenus Urostigma) and F. glabrata (subgenus Pharmacosycea), both from Panama, had hypertrophied outer epidermal cells on seed florets. Ficus poponoei also had Schistonchus sp. within the pedicel of an aborted floret, with hypertrophy of the cortical parenchyma. Ficus trigonata (subgenus Urostigma) from Panama had hypertrophy of the outer epidermis of seed florets. When the outer epidermis on these florets was missing, the inner mesocarp was hypertrophied. Ficus maxima (subgenus Pharmacosycea) from Panama had hypertrophy on the outer epidermis of seed and aborted florets. Schistonchus spp. were not found in wasp larvae or pupae in any of the Ficus spp. examined. Hypertrophy was never observed in the absence of Schistonchus spp.     

Geographic variation of fruit scents in a dispersion mutualism,the case of Ficus lutea

Chemical mediation is often involved in interactions between plants and animals, as in pollination and in seed dispersion mutualisms. Extensive investigation has been done in floral scents and on their interspecific and intraspecific variations, but similar research on fruit scent remains poorly explored and only focused on interspecific variations. We investigated in this study the intraspecific variations of volatile bouquet emitted by mature fruits of Ficus lutea, in two sites within its wide distribution range, i.e. in South Africa and in Madagascar. We demonstrated a clear geographic variation in the volatile bouquet emitted by ripe figs in these two study sites, especially due to the presence of sesquiterpenes in Madagascan bouquets, while scents present at both sites high amounts of fatty acid derivatives. We discuss here different possible explanations for such variations in fruit scents, potentially resulting from insular and/or geographic isolation. This novel result of an intraspecific variation linked to fig seed dispersion serves to increase our knowledge of the role of scents in seed dispersal mutualisms.     

Differential responses of photosystems I and II to seasonal drought in two Ficus species

Hemiepiphytic Ficus species exhibit more conservative water use strategy and are more drought-tolerant compared with their non-hemiepiphytic congeners, but a difference in the response of photosystem I (PSI) and photosystem II (PSII) to drought stress has not been documented to date. The enhancement of non-photochemical quenching (NPQ) and cyclic electron flow (CEF) have been identified as important mechanisms that protect the photosystems under drought conditions. Using the hemiepiphytic Ficus tinctoria and the non-hemiepiphytic Ficus racemosa, we studied the water status and the electron fluxes through PSI and PSII under seasonal water stress. Our results clearly indicated that the decline in the leaf predawn water potential (ψ_pd), the maximum photosynthetic rate (A_max) and the predawn maximum quantum yield of PSII (F_v/F_m) were more pronounced in F. racemosa than in F. tinctoria at peak drought. The F_v/F_m of F. racemosa was reduced to 0.69, indicating net photoinhibition of PSII. Concomitantly, the maximal photo-oxidizable P700 (P_m) decreased significantly in F. racemosa but remained stable in F. tinctoria. The fraction of non-photochemical quenching [Y(NPQ)] and the ratio of effective quantum yield of PSI to PSII [Y(I)/Y(II)] increased for both Ficus species at peak drought, with a stronger increase in F. racemosa. These results indicated that the enhancement of NPQ and the activation of CEF contributed to the photoprotection of PSI and PSII for both Ficus species under seasonal drought, particularly for F. racemosa.     

Interspecific Variation in Compensatory Regrowth to Herbivory Associated with Soil Nutrients in Three Ficus (Moraceae) Saplings

Plant compensatory regrowth is an induced process that enhances plant tolerance to herbivory. Plant behavior against herbivores differs between species and depends on resource availability, thus making general predictions related to plant compensatory regrowth difficult. To understand how soil nutrients determine the degree of compensatory regrowth for different plant species, we selected saplings of three Ficus species and treated with herbivore insects and artificial injury in both glasshouse conditions and in the field at two soil nutrient levels. Compensatory regrowth was calculated by biomass, relative growth rate and photosynthetic characteristics. A similar pattern was found in both the glasshouse and in the field for species F. hispida, where overcompensatory regrowth was triggered only under fertile conditions, and full compensatory regrowth occurred under infertile conditions. For F. auriculata, overcompensatory regrowth was stimulated only under infertile conditions and full compensatory regrowth occurred under fertile conditions. Ficus racemosa displayed full compensatory regrowth in both soil nutrient levels, but without overcompensatory regrowth following any of the treatments. The three Ficus species differed in biomass allocation following herbivore damage and artificial injury. The root/shoot ratio of F. hispida decreased largely following herbivore damage and artificial injury, while the root/shoot ratio for F. auriculata increased against damage treatments. The increase of shoot and root size for F. hispida and F. auriculata, respectively, appeared to be caused by a significant increase in photosynthesis. The results indicated that shifts in biomass allocation and increased photosynthesis are two of the mechanisms underlying compensatory regrowth. Contrasting patterns among the three Ficus species suggest that further theoretical and empirical work is necessary to better understand the complexity of the plant responses to herbivore damage.     

Development and characterization of microsatellite markers for a monoecious Ficus species,Ficus insipida,and cross‐species amplification among different sections of Ficus

The animal‐mediated pollination and seed‐dispersal mutualisms of Ficus species give them key roles in tropical ecosystems, but may make them vulnerable to habitat fragmentation. The development of highly polymorphic markers is needed to analyse their genetic diversity and investigate the effects of fragmentation on gene flow. Of thirteen microsatellite loci isolated from Ficus insipida, a monoecious species in French Guiana, eleven were polymorphic (two to six alleles each). High levels of variation were found among loci; expected heterozygosities ranged from 0.151 to 0.715. All markers revealed a broad cross‐species affinity when tested in 23 other Ficus species.     

Are Protected Areas Required to Maintain Functional Diversity in Human-Modified Landscapes?

The conversion of forest to agriculture across the world’s tropics, and the limited space for protected areas, has increased the need to identify effective conservation strategies in human-modified landscapes. Isolated trees are believed to conserve elements of ecological structure, providing micro-sites for conservation in matrix landscapes, and facilitating seed dispersal and forest restoration. Here we investigate the role of isolated Ficus trees, which are of critical importance to tropical forest ecosystems, in conserving frugivore composition and function in a human-modified landscape in Assam, India. We surveyed the frugivorous birds feeding at 122 isolated Ficus trees, 33 fruit trees, and 31 other large trees across a range of 32 km from the nearest intact forest. We found that Ficus trees attracted richer and more abundant assemblages of frugivores than the other tree categories. However, incidence function estimates revealed that forest specialist species decreased dramatically within the first kilometre of the forest edge. Despite this, species richness and functional diversity remained consistent across the human-modified landscape, as habitat generalists replaced forest-dependent frugivores, and accounted for most of the ecological function found in Ficus trees near the forest edge. We recommend that isolated Ficus trees are awarded greater conservation status, and suggest that their conservation can support ecologically functional networks of frugivorous bird communities.     

Chaos of Wolbachia Sequences Inside the Compact Fig Syconia of Ficus benjamina (Ficus: Moraceae)

Figs and fig wasps form a peculiar closed community in which the Ficus tree provides a compact syconium (inflorescence) habitat for the lives of a complex assemblage of Chalcidoid insects. These diverse fig wasp species have intimate ecological relationships within the closed world of the fig syconia. Previous surveys of Wolbachia, maternally inherited endosymbiotic bacteria that infect vast numbers of arthropod hosts, showed that fig wasps have some of the highest known incidences of Wolbachia amongst all insects. We ask whether the evolutionary patterns of Wolbachia sequences in this closed syconium community are different from those in the outside world. In the present study, we sampled all 17 fig wasp species living on Ficus benjamina, covering 4 families, 6 subfamilies, and 8 genera of wasps. We made a thorough survey of Wolbachia infection patterns and studied evolutionary patterns in wsp (Wolbachia Surface Protein) sequences. We find evidence for high infection incidences, frequent recombination between Wolbachia strains, and considerable horizontal transfer, suggesting rapid evolution of Wolbachia sequences within the syconium community. Though the fig wasps have relatively limited contact with outside world, Wolbachia may be introduced to the syconium community via horizontal transmission by fig wasps species that have winged males and visit the syconia earlier.