First Evidence of Thalassochory in the Ficus Genus: Seed Dispersal Using the Kuroshio Oceanic Current.

AIM: Plants distributed between southern Taiwan and the north of the Philippines are spread among numerous small islands in an area crossed by the powerful Kuroshio current. Oceanic currents can be effective seed-dispersal agents for coastal plant species. Moreover, the Luzon Strait is an area prone to tropical cyclones. The aim of this study is to look at the dispersal capability of an endangered coastal plant species, the Mearns fig (Ficus pedunculosa var. mearnsii), using both experimental and population genetics methods. LOCATION: Southern Taiwan, the Philippines, and the islands between Luzon and Taiwan Island. METHODS: This study combined two types of analysis, i.e., buoyancy experiments on syconia and double digest restriction-associated DNA sequencing (ddRAD), to analyze the population genetics of the Mearns fig. RESULTS: We first discovered that mature Mearns fig syconia could float in seawater. They have a mean float duration of 10 days to a maximum of 21 days. Germination rates varied significantly between Mearns fig seeds that had undergone different durations of flotation treatment. Population genetic analysis shows a high degree of inbreeding among various Mearns fig populations. Moreover, no isolation by distance was found between the populations and individuals. MAIN CONCLUSIONS: From our analysis of the genetic structure of the Mearns fig populations, we can clearly highlight the effect of the Kuroshio oceanic current on the seed dispersal of this fig tree. Comprehensive analysis has shown that Mearns fig seeds are still viable before the mature syconium sinks into the seawater, and so they could use the Kuroshio Current to float to the current population locations in Taiwan.

Parasitism Features of a Fig Wasp of Genus Apocrypta (Pteromalidae: Pteromalinae) Associated with a Host Belonging to Ficus Subgenus Ficus.

Non-pollinating fig wasps (NPFWs), particularly long-ovipositored Sycoryctina wasps, exhibit a high species specificity and exert complex ecological effects on the obligate mutualism between the plant genus Ficus and pollinating fig wasps. Apocrypta is a genus of NPFWs that mostly interacts with the Ficus species under the subgenus Sycomorus, and the symbiosis case between Apocrypta and F. pedunculosa var. mearnsii, a Ficus species under subgenus Ficus, is unique. As fig's internal environments and the wasp communities are distinct between the two subgenera, we addressed the following two questions: (1) Are the parasitism features of the Apocrypta wasp associated with F. pedunculosa var. mearnsii different from those of other congeneric species? (2) Is this Apocrypta species an efficient wasp that lives in its unique host? Our observation revealed that this wasp is an endoparasitic idiobiont parasitoid, as most congeneric species are, but developed a relatively long ovipositor. Furthermore, the relationships of the parasitism rate versus the pollinator number, the fig wall, and the sex ratio of the pollinator, respectively, showed that it possessed a higher parasitism ability than that of other congeners. However, its parasitism rate was low, and thus it was not an efficient wasp in its habitat. This difference between parasitism ability and parasitism rate might be a consequence of its oviposition strategy and the severe habitat conditions. These findings may also provide insights into the mechanism to maintain the interaction between the fig tree and the fig wasp community.

Mediation of a Mutualistic Conflict for Pollination via Fig Phenology and Odor Recognition between Ficus and Fig Wasp.

The vegetative and reproductive growth of plants provide the basic tempo for an ecosystem, and when species are interdependent, phenology becomes crucial to regulating the quantity and quality of the interactions. In plant-insect interactions, the plants signal the beginning of their reproductive period with visual and chemical cues; however, in the case of Ficus mutualism, the cues are strictly chemical. The volatile organic compounds emitted by a fig species are a unique, specific blend that provides a signal to mutualistic wasps that the figs are receptive for pollination. In this study, we studied both the phenological pattern of Ficus septica in Central Taiwan and its emissions of volatile compounds at receptivity. This dioecious fig species displays a pattern of continuous vegetative and reproductive production all through the year with a decrease in winter. In parallel, the odor blends emitted by male and female trees are similar but with seasonal variations; these are minimal during winter and increase with the size of the wasp population during the favorable season. In addition, the pollinating females cannot distinguish between the male and female summer odor blends. The link between odor similarity, pollinators and intersexual conflict is discussed.

Spatial Distribution and Climate Warming Impact on Abies kawakamii Forest on a Subtropical Island.

Species distribution modeling (SDM) is currently the primary tool for predicting suitable habitats for species. In this study, we used Abies kawakamii, a species endemic to Taiwan. Being the only Abies species distributed in high mountains, it acts as an ecological indicator on the subtropical island. We analyzed a vegetation map derived from remote sensing and ground surveys using SDM. The actual distribution of A. kawakamii in Taiwan has a total area of 16,857 ha distributed at an altitude of 2700-3600 m, and it often forms a monodominant forest at 3100-3600 m with the higher altitude edge as a forest line. Exploring the potential distribution of A. kawakamii through MaxEnt showed that the suitable habitat was 73,151 ha under the current climate. Under the scenarios of temperature increases of 0.5, 1.0, 1.5, and 2.0 °C, suitable habitat for A. kawakamii will gradually decrease to 70.2%, 47.1%, 30.2%, and 10.0% of this area, respectively, indicating that A. kawakamii will greatly decline under these climate warming scenarios. Fire burning disturbance may be the most significant damage to A. kawakamii at present. Although A. kawakamii has been protected by conservation areas and its natural regeneration is in good condition, it rarely has the opportunity to migrate upwards during climate warming. We suggest that in the future, research on the natural regeneration and artificial restoration of A. kawakamii should be emphasized, especially in the forest line ecotone.

Pollinator sharing, copollination, and speciation by host shifting among six closely related dioecious fig species.

The obligate pollination mutualism between figs (Ficus, Moraceae) and pollinator wasps (Agaonidae, Hymenoptera) is a classic example of cospeciation. However, examples of phylogenetic incongruencies between figs and their pollinators suggest that pollinators may speciate by host shifting. To investigate the mechanism of speciation by host shifting, we examined the phylogenetic relationships and population genetic structures of six closely related fig species and their pollinators from southern China and Taiwan-Ryukyu islands using various molecular markers. The results revealed 1) an extraordinary case of pollinator sharing, in which five distinct fig species share a single pollinator species in southern China; 2) two types of copollination, namely, sympatric copollination by pollinator duplication or pollinator migration, and allopatric copollination by host migration and new pollinator acquisition; 3) fig species from southern China have colonized Taiwan repeatedly and one of these events has been followed by host shifting, reestablishment of host specificity, and pollinator speciation, in order. Based on our results, we propose a model for pollinator speciation by host shifting in which the reestablishment of host-specificity plays a central role in the speciation process. These findings provide important insights into understanding the mechanisms underlying pollinator speciation and host specificity in obligate pollination mutualism.

Leaf epidermal morphology of Asparagaceae of Taiwan and its systematic significance.

The current study analyzed the epidermal morphology of Asparagaceae in detail and assessed its systematic importance. At the familial level, no consistent characteristics were found, but anticlinal wall and stomata morphology provided systematic information of different tribes, especially Ophiopogoneae and Polygonateae. In Ophiopogoneae, Liriope and Ophiopogon had similar epidermis, which implying a close relationship between them, and was also supported by related studies. The leaves of Polygonateae exhibited rounded and undulate anticlinal wall. Polygonatum arisanense var. formosanum had a rounded anticlinal wall, whereas other species exhibited undulate anticlinal walls. Different epidemis of Po. arisanense var. formosanum supported the variety treatment of Po. arisanense. The intergeneric relationship was also interpreted based on the anticlinal wall and stomata. Therefore, the epidermis could provide the systematic value of Asparagaceae. The present study also revealed the linkage of stomata and habitat types, though the adaptative significance of epidermal traits needs further study. RESEARCH HIGHLIGHTS: Anticlinal wall and stomatal morphology had systematic potential on tribal or generic levels of Asparagaceae. Stomatal types of Asparagaceae might be linked to environmental factors.

Cirsiumtaiwanense (Compositae, Cirsiumsect.Onotrophe, subsect. Australicirsium), a new species from Taiwan.

A new species of Cirsium, C.taiwanense Y.H.Tseng & Chih Y.Chang from central-northern Taiwan is reported in this article. This species is similar to C.hosokawae Kitam. in having a densely cobwebby abaxial leaf surface, but differs in its yellow (vs. vivid purplish red) corolla and the angle between the midrib and the lateral veins of the leaf, which is acute as opposed to nearly at a right angle in C.hosokawae. Cirsiumtaiwanense has 2n = 32 chromosomes, which is different from the other species in the Taiwanese subsect. Australicirsium Kitam. (2n = 34). An identification key to the Cirsium taxa of Taiwan is presented.

Competition in Abies kawakamii forests at subtropical high mountain in Taiwan.

The spatial patterns of plant species reflect the competitive pressures on individuals. To generate Competition indices (CI), we measured the diameter at breast height (DBH), crown volumes (CV) and the distances between trees. In this study, Abies kawakamii were divided based on the dominant component of the understory (moss or bamboo) to (1) investigate the relationship between the CI and stand structural attributes (SSAs); (2) compare the inter- and intraspecies; CIs as well as living and dead individual CIs; and (3) examine the relationship between the DBH and CI. The current findings indicate that the understory composition affected the CI and SSAs. The interspecies CI was larger than the intraspecies CI when bamboo-dominated the understory. In contrast, the intraspecies CI was larger than the interspecies CI when the understory was dominated by moss. The CI of dead individuals was higher than that of live individuals due to the biological characteristics and regeneration needs of Abies. Additionally, sensitivity to the environment and available resources may exert more pressure on young individuals than mature individuals.

Population Monitoring, Egg Parasitoids, and Genetic Structure of the Invasive Litchi Stink Bug, Tessaratoma papillosa in Taiwan.

Here we assessed population dynamics, natural enemy fauna (with emphasis on egg parasitoid), and population genetic structure (based on mitochondrial DNA) of the invasive litchi stink bug (LSB), Tessaratoma papillosa in Taiwan. Our major findings include: (1) fluctuations of LSB in numbers of adults, mating pairs, and egg masses over a 2-year period in Taiwan generally resemble those in the native populations; (2) Anastatus dexingensis and A. fulloi are among the most dominant LSB egg parasitoids, with the former consistently outnumbering the latter throughout Taiwan; (3) the presence of two genetically distinct clades suggests LSB in Taiwan most likely derived from multiple invasions. All these data practically improve our understanding of this invasive insect pest, particularly its ecological and genetic characteristics in the introduced area, which represents critical baseline information for the design of future integrated pest management strategies.

Cirsiumtatakaense (Compositae), a new species from Taiwan.

A new species of Cirsium, Cirsiumtatakaense Y.H.Tseng & C.Y.Chang, from central-southern Taiwan is described and illustrated. This species is similar to C.kawakamii Hayata in leaf shape, achene and chromosome number (2n = 64), but can be readily distinguished from C.kawakamii by the narrower leaf lobes, usually higher number of florets and phyllaries, the purplish-red corolla (vs. white) and larger pollen grains. A key to the species of Cirsium in Taiwan is also presented.

Tree mortality in response to typhoon-induced floods and mudslides is determined by tree species, size, and position in a riparian Formosan gum forest in subtropical Taiwan.

Global warming-induced extreme climatic changes have increased the frequency of severe typhoons bringing heavy rains; this has considerably affected the stability of the forest ecosystems. Since the Taiwan 921 earthquake occurred in 21 September 1999, the mountain geology of the Island of Taiwan has become unstable and typhoon-induced floods and mudslides have changed the topography and geomorphology of the area; this has further affected the stability and functions of the riparian ecosystem. In this study, the vegetation of the unique Aowanda Formosan gum forest in Central Taiwan was monitored for 3 years after the occurrence of floods and mudslides during 2009-2011. Tree growth and survival, effects of floods and mudslides, and factors influencing tree survival were investigated. We hypothesized that (1) the effects of floods on the survival are significantly different for each tree species; (2) tree diameter at breast height (DBH) affects tree survival-i.e., the larger the DBH, the higher the survival rate; and (3) the relative position of trees affects tree survival after disturbances by floods and mudslides-the farther trees are from the river, the higher is their survival rate. Our results showed that after floods and mudslides, the lifespans of the major tree species varied significantly. Liquidambar formosana displayed the highest flood tolerance, and the trunks of Lagerstoemia subcostata began rooting after disturbances. Multiple regression analysis indicated that factors such as species, DBH, distance from sampled tree to the above boundary of sample plot (far from the riverbank), and distance from the upstream of the river affected the lifespans of trees; the three factors affected each tree species to different degrees. Furthermore, we showed that insect infestation had a critical role in determining tree survival rate. Our 3-year monitoring investigation revealed that severe typhoon-induced floods and mudslides disturbed the riparian vegetation in the Formosan gum forest, replacing the original vegetation and beginning secondary succession. Moreover, flooding provided new habitats for various plants to establish their progeny. By using our results, lifecycles of trees (including death) can be understood in detail, facilitating riparian vegetation engineering in forests severely disturbed by typhoon-induced floods and mudslides.

Topographic effect on the phenology of Ficus pedunculosa var. mearnsii (Mearns fig) in its northern boundary distribution, Taiwan.

Mearns fig grows at the edge of coastal vegetation on uplifted coral reefs, its population and mutualistic-pollinators are susceptible to the influence of extreme weather. To determine the phenology of Mearns fig and the effects of various weather events under small-scale topographic differences, phenology was conducted for 3 years and 7 months. Results showed that Mearns figs had multiple leaf and fig productions year-round. Topographic effects caused population in Frog Rock Trail and Jialeshuei, which are less than 10 km away from each other, to exhibit different phenological patterns after experiencing severe weather events. Northeast monsoons led the Jialeshuei population to show low amounts of leaves and figs in winter and the phenological production was also susceptible to disturbances by typhoons in summer. Fig reproduction in such environment was disadvantageous to maintain pollinators. Besides, topographic complex in microhabitat of Frog Rock Trail protected some individuals from these same events thus safeguard population's survival. The phenology of Mearns fig would respond to the weather events sensitively, which serve as references for estimating the mutualism system, and as indicators of climate change.

Effects of climate change on a mutualistic coastal species: Recovery from typhoon damages and risks of population erosion.

Presently, climate change has increased the frequency of extreme meteorological events such as tropical cyclones. In the western Pacific basin, these cyclones are called typhoons, and in this area, around Taiwan Island, their frequency has almost doubled since 2000. When approaching landmasses, typhoons have devastating effects on coastal vegetation. The increased frequency of these events has challenged the survival of coastal plant species and their posttyphoon recovery. In this study, a population of coastal gynodioecious Ficus pedunculosa var. mearnsii (Mearns fig) was surveyed for two years to investigate its recovery after Typhoon Morakot, which occurred in August 2009. Similar to all the Ficus species, the Mearns fig has an obligate mutualistic association with pollinating fig wasp species, which requires syconia (the closed Ficus inflorescence) to complete its life cycle. Moreover, male gynodioecious fig species produces both pollen and pollen vectors, whereas the female counterpart produces only seeds. The recovery of the Mearns fig was observed to be rapid, with the production of both leaves and syconia. The syconium:leaf ratio was greater for male trees than for female trees, indicating the importance of syconium production for the wasp survival. Pollinating wasps live for approximately 1 day; therefore, receptive syconia are crucial. Every typhoon season, few typhoons pass by the coasts where the Mearns fig grows, destroying all the leaves and syconia. In this paper, we highlight the potential diminution of the fig population that can lead to the extinction of the mutualistic pair of species. The effects of climate change on coastal species warrant wider surveys.

Diversification and spatial structuring in the mutualism between Ficus septica and its pollinating wasps in insular South East Asia.

BACKGROUND: Interspecific interactions have long been assumed to play an important role in diversification. Mutualistic interactions, such as nursery pollination mutualisms, have been proposed as good candidates for diversification through co-speciation because of their intricate nature. However, little is known about how speciation and diversification proceeds in emblematic nursery pollination systems such as figs and fig wasps. Here, we analyse diversification in connection with spatial structuring in the obligate mutualistic association between Ficus septica and its pollinating wasps throughout the Philippines and Taiwan. RESULTS: Ceratosolen wasps pollinating F. septica are structured into a set of three vicariant black coloured species, and a fourth yellow coloured species whose distribution overlaps with those of the black species. However, two black pollinator species were found to co-occur on Lanyu island. Microsatellite data on F. septica indicates the presence of three gene pools that broadly mirrors the distribution of the three black clades. Moreover, receptive fig odours, the specific message used by pollinating wasps to locate their host tree, varied among locations. CONCLUSIONS: F. septica and its black pollinator clades exhibited similar geographic structuring. This could be due originally to geographic barriers leading to isolation, local adaptation, and finally co-structuring. Nevertheless, the co-occurrence of two black pollinator species on Lanyu island suggests that the parapatric distribution of the black clades is now maintained by the inability of migrating individuals of black pollinators to establish populations outside their range. On the other hand, the distribution of the yellow clade strongly suggests an initial case of character displacement followed by subsequent range extension: in our study system, phenotypic or microevolutionary plasticity has allowed the yellow clade to colonise hosts presenting distinct odours. Hence, while variation in receptive fig odours allows specificity in the interaction, this variation does not necessarily lead to coevolutionary plant-insect diversification. Globally, our results evidence evolutionary plasticity in the fig-fig wasp mutualism. This is the first documentation of the presence of two distinct processes in pollinating fig wasp diversification on a host species: the formation of vicariant species and the co-occurrence of other species over large parts of their ranges probably made possible by character displacement.

Genome-wide sequence data suggest the possibility of pollinator sharing by host shift in dioecious figs (Moraceae, Ficus).

The obligate mutualism of figs and fig-pollinating wasps has been one of the classic models used for testing theories of co-evolution and cospeciation due to the high species-specificity of these relationships. To investigate the species-specificity between figs and fig pollinators and to further understand the speciation process in obligate mutualisms, we examined the genetic differentiation and phylogenetic relationships of four closely related fig-pollinating wasp species (Blastophaga nipponica, Blastophaga taiwanensis, Blastophaga tannoensis and Blastophaga yeni) in Japan and Taiwan using genome-wide sequence data, including mitochondrial DNA sequences. In addition, population structure was analysed for the fig wasps and their host species using microsatellite data. The results suggest that the three Taiwanese fig wasp species are a single panmictic population that pollinates three dioecious fig species, which are sympatrically distributed, have large differences in morphology and ecology and are also genetically differentiated. Our results illustrate the first case of pollinator sharing by host shift in the subgenus Ficus. On the other hand, there are strict genetic codivergences between allopatric populations of the two host-pollinator pairs. The possible processes that produce these pollinator-sharing events are discussed based on the level and pattern of genetic differentiation in these figs and fig wasps.

Ficus (Moraceae) and fig wasps (Hymenoptera: Chalcidoidea) in Taiwan.

Although Ficus-associated wasp fauna have been extensively researched in Australasia, information on these fauna in Taiwan is not well accessible to scientists worldwide. In this study, we compiled records on the Ficus flora of Taiwan and its associated wasp fauna. Initial agronomic research reports on Ficus were published in Japanese in 1917, followed by reports on applied biochemistry, taxonomy, and phenology in Chinese. On the basis of the phenological knowledge of 15 species of the Ficus flora of Taiwan, recent research has examined the pollinating and nonpollinating agaonid and chalcid wasps (Hymenoptera: Chalcidoidea). Updating records according to the current nomenclature revealed that there are 30 taxa (27 species) of native or naturalized Ficus with an unusually high proportion of dioecious species (78%). Four species were observed to exhibit mutualism with more than one pollinating wasp species, and 18 of the 27 Ficus species were reported with nonpollinating wasp species. The number of nonpollinating wasp species associated with specific Ficus species ranges from zero (F. pumila) to 24 (F. microcarpa). Approximately half of the Taiwanese fig tree species have been studied with basic information on phenology and biology described in peer-reviewed journals or theses. This review provides a solid basis for future in-depth comparative studies. This summary of knowledge will encourage and facilitate continuing research on the pollination dynamics of Ficus and the associated insect fauna in Taiwan.

Genetic and physiological data suggest demographic and adaptive responses in complex interactions between populations of figs (Ficus pumila) and their pollinating wasps (Wiebesia pumilae).

To study interactions between host figs and their pollinating wasps and the influence of climatic change on their genetic structures, we sequenced cytoplasmic and nuclear genes and genotyped nuclear microsatellite loci from two varieties of Ficus pumila, the widespread creeping fig and endemic jelly fig, and from their pollinating wasps, Wiebesia pumilae, found in Taiwan and on nearby offshore islands. Great divergence in the mitochondrial cytochrome c oxidase subunit I (mtCOI) with no genetic admixture in nuclear markers indicated that creeping- and jelly-fig wasps are genetically distinct. Compared with creeping-fig wasps, jelly-fig wasps also showed better resistance under cold (20 °C) than warm (25 and 30 °C) conditions in a survival test, indicating their adaptation to a cold environment, which may have facilitated population expansion during the ice age as shown by a nuclear intron and 10 microsatellite loci. An excess of amino acid divergence and a pattern of too many rare mtCOI variants of jelly-fig wasps as revealed by computer simulations and neutrality tests implied the effect of positive selection, which we hypothesize was associated with the cold-adaptation process. Chloroplast DNA of the two fig plants was completely segregated, with signs of genetic admixture in nuclear markers. As creeping- and jelly-fig wasps can pollinate creeping figs, occasional gene flow between the two figs is thus possible. Therefore, it is suggested that pollinating wasps may be playing an active role in driving introgression between different types of host fig.

Phenology and pollinating wasp dynamics of Ficus microcarpa L.f.: adaptation to seasonality.

BACKGROUND: In the obligate plant/pollinator mutualism, pollinator abundance is conditioned by the host resource. In order to investigate the population fluctuation of pollinating wasps and the phenological processes involved, this study examined the dual dynamics of the pollinator and the syconium phenology of a seasonal fruited fig tree population, Ficus microparpa, in Taipei, Taiwan. RESULTS: Our results revealed three seasons in the annual phenology: spring crop, summer-fall crop and winter trough seasons. The syconium quantity was correlated most significantly with temperature based on the generalized linear model with the meteorological data transformed by a principal component analysis. The pollinator population showed an increasing trend in spring, reached the maximum abundance in summer, and then declined drastically in winter, consistent with the syconium production fluctuation. With the small amount of local pollinators from the winter syconia and potential immigrating foundresses from other populations, the pollinator population size can increase very quickly from almost zero to over 40,000 wasps for this 29-tree local population within a season. CONCLUSION: This syconium phenological scheme, coupled with the fast-recovery rate of pollinators, may explain the worldwide adaptation and invasion of Ficus microcarpa.

Portable microsatellite primers for Ficus (Moraceae).

PREMISE OF THE STUDY: Highly portable microsatellite primers were developed for Ficus to facilitate investigation of genetic structure of complete regional floras using a single set of markers. METHODS AND RESULTS: Pyrosequencing of five species of Ficus produced a library of 5723 potential primers. Potential primers found in at least two species and presenting identical annealing temperatures were tested on a set of five additional Ficus species. A set of 20 primer pairs producing well-defined and easily readable peaks was retained and tests showed their potential utility for analyzing population genetic structure of 24 Ficus species from Taiwan. Numbers of alleles per locus ranged from one to six in the least variable species and from one to 17 in the most variable species. CONCLUSIONS: The results indicate that our set of primers can be used to analyze polymorphism and compare levels of polymorphism among Ficus species.

Phylogenetic analyses suggest a hybrid origin of the figs (Moraceae: Ficus) that are endemic to the Ogasawara (Bonin) Islands, Japan.

The Ogasawara Islands are oceanic islands and harbor a unique endemic flora. There are three fig species (Ficus boninsimae, F. nishimurae and F. iidaiana) endemic to the Ogasawara Islands, and these species have been considered to be closely related to Ficus erecta, and to have diverged within the islands. However, this hypothesis remains uncertain. To investigate this issue, we assessed the phylogenetic relationships of the Ogasawara figs and their close relatives occurring in Japan, Taiwan and South China based on six plastid genome regions, nuclear ITS region and two nuclear genes. The plastid genome-based tree indicated a close relationship between the Ogasawara figs and F. erecta, whereas some of the nuclear gene-based trees suggested this relationship was not so close. In addition, the phylogenetic analyses of the pollinating wasps associated with these fig species based on the nuclear 28S rRNA and mitochondrial cytB genes suggested that the fig-pollinating wasps of F. erecta are not sister to those of the Ogasawara figs These results suggest the occurrence of an early hybridization event(s) in the lineage leading to the Ogasawara figs.