Hsy-Yu Tzeng

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

BackgroundIn 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.ResultsOur 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.ConclusionThis syconium phenological scheme, coupled with the fast-recovery rate of pollinators, may explain the worldwide adaptation and invasion of Ficus microcarpa.

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.

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.

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.

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

BackgroundInterspecific 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.ResultsCeratosolen 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.ConclusionsF. 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.

Heteropolygonatum altelobatum (Asparagaceae), comb. nova

Heteropolygonatum has been considered endemic to China, where most of the species are distributed in the SW region of the country. The genus is characterized by having both terminal and axillary inflorescences, inner and outer stamens of different lengths, and an epiphytic existence. Formerly, a number of the species were included in Polygonatum or Smilacina. Polygonatum altelobatum Hayata is an endemic of Taiwan; however, a review of the literature and field observations confirmed that it should be placed in Heteropolygonatum. Thus, we propose the new combination Heteropolygonatum altelobatum (Hayata) Y.H. Tseng, H.Y. Tzeng & C.T. Chao.

Maianthemum harae (Asparagaceae), a New Species from Taiwan

Maianthemum harae Tseng & Chao, a new species of Asparagaceae from Taiwan, is described and illustrated. This species resembles M. formosanum in the shape and size of flower, but is easily distinguished from the latter by its tuberous rhizome, 9–12 leaves, lanceolate leaves and longer styles.

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.