Evolutionary origin of a periodical mass‐flowering plant

The evolutionary origin of periodical mass‐flowering plants (shortly periodical plants), exhibiting periodical mass flowering and death immediately after flowering, has not been demonstrated. Within the genus Strobilanthes (Acanthaceae), which includes more than 50 periodical species, Strobilanthes flexicaulis on Okinawa Island, Japan, flowers gregariously every 6 years. We investigated the life history of S. flexicaulis in other regions and that of closely related species together with their molecular phylogeny to reveal the evolutionary origin of periodical mass flowering. S. flexicaulis on Taiwan Island was found to be a polycarpic perennial with no mass flowering and, in the Yaeyama Islands, Japan, a monocarpic perennial with no mass flowering. Molecular phylogenetic analyses indicated that a polycarpic perennial was the ancestral state in this whole group including S. flexicaulis and the closely related species. No distinctive genetic differentiation was found in S. flexicaulis among all three life histories (polycarpic perennial, monocarpic perennial, and periodical plant). These results suggest that among S. flexicaulis, the periodical mass flowering on Okinawa Island had evolved from the polycarpic perennial on Taiwan Island via the monocarpic perennial in the Yaeyama Islands. Thus, the evolution of life histories could have taken at the level of local populations within a species.     

Survivorship after flowering and flowering synchronicity of three cultivated Strobilanthes flexicaulis individuals from Iriomote Island,Japan

Strobilanthes flexicaulis in Iriomote Island, Japan, is a monocarpic perennial plant, which is thought to be an intermediate evolutionary state from a polycarpic perennial plant to a periodical mass-flowering plant. It remains unclear whether the intermediate reproductive traits are altered by cutting propagation or disbudding treatment (flower bud removal). To evaluate whether these traits are affected by such treatments, three individuals of S. flexicaulis from Iriomote Island were cultivated, and their flowering patterns and survivorship were observed. The monocarpic trait seemed to have been altered into a polycarpic trait by cultivation. The disbudding treatment was not related to the survivorship. The initiation of flowering was synchronized, but the termination of the second flowering period was variable among the three individuals and between the treatments. S. flexicaulis on Iriomote Island seemed to have individual variation in reproductive traits. This variation may result in their intermediate evolutionary state.     

Clonal Structure,Seed Set,and Self-Pollination Rate in Mass-Flowering Bamboo Species during Off-Year Flowering Events

Bamboos are typical examples of highly synchronized semelparous species. Their mass-flowering events occur at supra-annual intervals but they sometimes flower on a small scale in off-years. If some bamboo ramets (culms) of a genet flower and die in off-years, whereas other culms of the same genet do not flower synchronously, the genet can still survive blooming in an off-year and could participate in the next mass-flowering event. At genet level, the effect might be similar to that achieved by synchronously reproducing iteroparous plants. In addition, if multiple genets flower simultaneously in off-years, cross-pollination will be promoted. However, it is not known whether all the culms in a genet flower synchronously and whether multiple genets flower in off-years. We determined the clonal structure of three temperate dwarf bamboo species, i.e., Sasa senanensis, S. kurilensis, and S. palmata, at 24 off-year flowering sites and the surrounding areas in northern Japan using seven microsatellite markers. We also estimated seed set at seven of the sites and self-pollination rates at five sites to determine off-year reproductive success. Next, we investigated whether seed sets at the culm level were related to flowering area and/or number of flowering genets, using generalized linear mixed-effect models (GLMMs). Multiple genets flowered at 9/24 flowering sites. We found that 40/96 of the genets identified had some flowering culms. Non-flowering culms were present in 24/40 flowering genets. Seed set was in the range 2.2%–12.5% and the self-pollination rate was 96.3%. In the best GLMM, seed set increased with flowering area. Seeds were produced in off-years, but cross-pollination was rare in off-years. We suggest that some dwarf bamboos may exhibit iteroparity or imperfectly synchronized semelparity at the genet level, a characteristic similar to that of other reproductively synchronous plants. We also found synchronous flowering of a few genets even in off-years.     

Spatial and temporal flowering patterns of the monocarpic dwarf bamboo Sasa veitchii var. hirsuta

In order to clarify spatial and temporal patterns in the flowering process of S. veitchii var. hirsuta, the authors investigated the flowering of the species at a regional level in a mountainous area of Kyoto City, and at population/individual culm levels at experimental forest stations within the same municipal region. S. veitchii var. hirsuta flowered in several separate areas spanning ranges between several and more than 10?km north?Csouth and east?Cwest from 2004 to 2007. Sporadic flowering occurred the year before mass flowering. In the mass-flowering year, 98% of the culms in an S. veitchii var. hirsuta population flowered, and the other 2% or so flowered in the years before and after mass flowering. These results show a spatiotemporal synchronous flowering pattern (with most culms of populations gregariously flowering in a year over a large area) and an asynchronous flowering pattern (with a small percentage of the culms of populations flowering before and after the mass-flowering year) for S. veitchii var. hirsuta. It was also clarified that the year and scale of mass flowering differ by area, and that mass flowering occurs in individual areas in successive years. The survey performed at the individual culm level revealed that the mean numbers of open florets and attached seeds per culm showed two peaks from April to July, suggesting that S. veitchii var. hirsuta flowering events occur twice a year.     

Insect assemblages on flowering patches of 12 bamboo species

Bamboos are known as long-living monocarpic plants that exhibit synchronous flowering at long intervals. It has been reported that florivory has a critical effect on their seed production in bamboos, especially in small scale flowering patches. In this study, we aimed to determine species composition and life history of florivorous insects in multiple bamboo species. We collected the inflorescences of 12 bamboo species from 15 sites in Japan from 2017 to 2019 and recorded insect assemblages found in the flowers. Five different insect species were observed to feed on the flowers of bamboo species. Among these, the larvae of two Dicraeus species were the most widely observed florivorous insects of the bamboo species. The other insects included the larvae of Cecidomyiidae sp., which was frequently observed on Sasa species, and the other two insects were Epuraea submicrurula, and Dimorphopterus japonicus. These insects were oviposited on the florets during the budding period. In addition, predators and parasitoids were found in the bamboo flowers. Our findings suggest that the bamboos flowers were mainly consumed by dipteran larvae. Insect species composition and frequency varied among bamboo species and sites. Comparing the frequency of the florivorous insects among bamboo flowering patches, including mass flowering patches, in different areas is needed in future studies.     

Genets of dwarf bamboo do not die after one flowering event: evidence from genetic structure and flowering pattern

Dwarf bamboos in the genus Sasa are believed to be long-lived, synchronously flowering, and monocarpic plants. However, the monocarpy of dwarf bamboo has not been confirmed, because whether all ramets within one genet flower at the same time cannot be determined without differentiating the genetic structure among ramets. This study aims to evaluate the reproductive traits of Sasa pubiculmis by verifying the monocarpy and physiological integration between flowering ramets and non-flowering ramets during a 4-year flowering period. One genotypically identified genet, which covered an area of approximately 3 ha, had both flowering and non-flowering patches of ramets during the 4-year flowering period (2004–2007). A fraction of the flowering genet remained non-flowering during the 4 years of observation, and did not die after mass flowering. Flowering ramets were physically connected to non-flowering ramets via rhizomes, and assimilated ¹³C was allocated from non-flowering ramets to flowering ramets. Consequently, we clarified that this dwarf bamboo potentially has polycarpic reproductive traits rather than monocarpic, and a genet can keep rhizomes and non-flowering patches alive to sustain the organism after mass flowering.     

Rare nationwide synchronized massive flowering and decline event of <Emphasis Type="Italic">Sasa borealis</Emphasis> (Hack.) Makino in South Korea

Sasa borealis, a monocarpic species of dwarf bamboo, is widely distributed throughout Korea. It dominates forest floors, thereby inhibiting mainly the biodiversity. Although it flowers very rarely, examples have recently been observed in multiple locations, providing a good opportunity to study reproduction phenomena, and to aid in biodiversity restoration. Therefore, we investigated the nationwide timing of flowering events by using data collected from a social network service (SNS). We also more closely examined flowering and decline event, focusing at the patch and culm levels on Mt. Jeombong. We then analyzed the main factors affecting flowering. Our SNS and survey results showed that S. borealis is in a current flowering cycle that started in 2013 and continues to the present (83% of all events happening within this period) with a peak in 2015 (48% of the cases occurring in that year). This clearly demonstrated nationwide, synchronized, and massive flowering. Although the culm density in patches was not related to flowering, patches with large culms tended to flower (F = 8.241, p = 0.01). We suspected that this nationwide flowering event was triggered by prolonged drought during the spring months of 2014 and 2015 (F = 5.207, p < 0.05), which led to concurrent, massive flowering in patches mature enough to do so. Because this species prefers a wet habitat, we concluded that severe, prolonged drought induced environmental stress for those plants. After flowering, culms in those particular patches tended to die off within one year. This large-scale synchronized decline should have an enormous effect on the vegetation dynamics of a forest dominated and suppressed by Sasa. Future investigations might incorporate methods of ecological control and manipulation to increase biodiversity there.     

Density-dependent seed set in the Haleakala silversword: evidence for an Allee effect

Plant species may be subject to Allee effects if individuals experience a reduction in pollination services when populations are small or sparse. I examined temporal variation in reproductive success of the monocarpic Haleakala silversword (Argyroxiphium sandwicense subsp. macrocephalum) over five years, to determine if plants flowering out of synchrony with most of the population (i.e., in low flowering years) exhibited lower percent seed set than synchronously-flowering plants (i.e., those flowering in high flowering years). Through two pollination experiments conducted over multiple years, I also measured pollen limitation and self-incompatibility in this species. The number of flowering plants varied greatly among years, as did reproductive success. Percent seed set was significantly correlated with the number of plants flowering annually, such that plants flowering in high flowering years (1997 and 2001) exhibited significantly higher percent seed set than did plants flowering in low flowering years (1998-2000). In the 3-year pollen limitation study, plants flowering asynchronously were pollen-limited, whereas plants flowering synchronously were not. This species is strongly self-incompatible. Results of this study demonstrate that the Haleakala silversword experiences reduced reproductive success in low flowering years, and suggest that this Allee effect is pollinator-mediated. Allee effects in plants are an understudied yet potentially important force with implications for the population dynamics and conservation of rare species.     

Pollination systems in a warm temperate evergreen broad-leaved forest on Yaku Island

Animal pollination in a warm temperate evergreen broad-leaved forest was observed on Yaku-shima Island, south of Kyushu, Japan. Three groups of plants were categorized: canopy-flowering tree species, understory-flowering tree species, and climber and epiphyte species. Each of these formed different pollination systems. The canopy-flowering tree species had shallow, dish-shaped flowers and utilized various types of opportunistic pollinators. Most of the climber and epiphyte species had deep, tube-shaped flowers and specialized pollinators, although some climber species which bloomed in the canopy especially in winter, had opportunistic pollinators. The understory-flowering tree species had large dish- or funnel-shaped flowers and endothermic pollinators able to tolerate the dark and cold conditions under the canopy. The individual trees of canopy-flowering tree species produced large numbers of flowers simultaneously (mass-flowering) and had a well synchronized flowering period. Each canopy-flowering tree species segregated its flowering time from those of the anothers. Climber and epiphyte species and most of the understory-flowering tree species produced small numbers of flowers sequentially (extended flowering) and showed a long flowering period.     

Population age structure and reproductive behavior of the monocarpic perennial Heracleum mantegazzianum (Apiaceae) in its native and invaded distribution ranges

Many invasive species are benign in their native region-are there interactions between their key traits and the new habitats that explain invasion success? The giant perennial herb Heracleum mantegazzianum is a problematic invader in Europe and is also naturalized in North America. We compared its population structure and reproductive behavior in the native (W. Caucasus) and invaded (Czech Republic) areas in managed (pastures) and unmanaged sites. The age structure of the populations and age at flowering were analyzed using herb-chronology, a method based on counting annual rings in the secondary xylem of roots. The species was strictly monocarpic; most plants in unmanaged sites in the invaded range flowered in the third and fourth yr (maximum 12 yr). In unmanaged habitats, plants from the native range flowered later than those from the invaded range. In both ranges, flowering was delayed in managed sites where the population density was higher and most plants flowered around the fifth year. Reproductive output of individual plants was neither related to population density nor to age at flowering. More favorable climatic conditions in the invaded region, together with increased chances for dispersal in a densely colonized central Europe, seemed to allow the massive invasion.     

Seed Set and Natural Regeneration of Dendrocalamus membranaceus Munro after Mass and Sporadic Flowering in Yunnan,China

The flowering periods of woody bamboos, seed set, natural regeneration and death after flowering have been rarely observed and evaluated in the field. Dendrocalamus membranaceus Munro, a tropical woody bamboo mainly distributed in the Yunnan, displayed both sporadic as well as gregarious (mass) flowering and fruited from 2006 to 2013 following severe droughts. The aim of this study is to examine potential differences in seed set and natural regeneration between the two flowering patterns in natural D. membranaceus forests. We investigated and analyzed seed set, seed germination, seedling growth and mortality in both mass and sporadic flowering populations. Observations were made over a period of three years to record changes in bamboo seedling density, height and culm diameter. We observed a low natural seed set ranging from 1.76% to 7.49%, and a relatively high seed germination rate in the nursery from 59.6% to 71.0% for both types of flowering populations. Seeds germinated in 5–7 days after sowing and the germination period lasted 10–15 days. Seed set and germination rates in mass-flowering populations were significantly higher than those of sporadically flowering stands. The seedlings within sporadically flowering populations died within two years. In comparison, seedling mortality in the mass flowering population increased over two periods of observation from 64.92% to 98.89%, yet there was good seedling establishment left over, which showed mean height and mean culm diameter increasing by 1053.25% and 410.71%, respectively, in the second year of observations, and 137.10%, and 217.48%, respectively, in the third year. There are significant differences in seed set, natural regeneration ability and sustainability of bamboo populations between the mass flowering and sporadically flowering populations of D. membranaceus. Sporadic flowering populations failed to produce effective regeneration, while mass flowering populations were able to regenerate successfully. This study provides useful insights for conservation and natural forest management of D. membranaceus. We consider the merits of introducing other genetic provenances towards long-term maintenance of the stand features at sporadically flowering sites; meanwhile, the most economic option for mass flowering stands is to allow natural regeneration to take place through protecting such sites from further disturbance.     

Landscapes with high amounts of mass-flowering fruit crops reduce the reproduction of two solitary bees

The intensification of agriculture and the loss of natural habitat are key drivers of the observed declines in wild bee populations in recent decades. Mass-flowering crops are suggested to provide abundant resources for bees during flowering. However, mass-flowering crops could influence the offspring reproduction of bees after mass-flowering due to a lack of floral resources in the fields after mass-flowering. In our study we quantified the reproductive output of two solitary bee species (Osmia cornuta and O. bicornis) during and after mass-flowering of fruit crops (MFFC, i.e. apple, pear and sweet cherry) by means of trap nests. Ten trap nests were placed in landscapes with independent gradients of semi-natural habitat and MFFC in the surrounding landscapes. In addition, the composition of the collected pollen of both bee species was identified. Despite our relatively small sample size, we do detect a clear effect for both bee species, namely that the number of constructed brood cells after mass-flowering decreased significantly as the proportion of MFFC within 200 m of the surrounding landscape increased. During mass-flowering no effects were found, probably because O. cornuta collects significant amounts of Prunus spp., Malus spp. and Pyrus spp. pollen and because O. bicornis collects Malus spp. pollen to a certain extent. Yet, the negative effect after mass-flowering is clearly limiting the reproduction of O. bicornis, a solitary bee species with a later phenology compared to O. cornuta. The latter might also be a concern for other bee species that are active in late spring or summer. Landscape management needs to focus on providing additional floral resources to sustain viable populations of solitary bees and other pollinating insects after mass-flowering in landscapes with high amounts of MFFC.     

Mass flowering and parental death in the regeneration of Cerberiopsis candelabra (Apocynaceae), a long-lived monocarpic tree in New Caledonia1

Monocarpy is rare among forest trees, and the selective conditions allowing this life history to evolve are poorly known. Here we examined the regeneration dynamics of a New Caledonian monocarpic tree species, Cerberiopsis candelabra, to better understand how postreproductive mortality and mass flowering might contribute to the success of this strategy. We investigated population size structures and seedling establishment patterns in 18 stands following the 2003 flowering event. We found little evidence of recent recruitment. Instead, population size structures suggested a history of one or more substantial recruitment events followed by recruitment failure, despite multiple flowering events in most populations. The canopy gap created by death of an individual parent appeared generally insufficient to allow seedling establishment, but mass flowering and consequent death of many adults appeared to enhance seedling recruitment by opening more of the canopy. Site means of seedling density below dead parents correlated strongly with light availability and with the proportional density of flowering trees. Therefore, we suggest that mass flowering and gregariousness may have been necessary preconditions for the evolution of monocarpy in this species. However, the degree to which regeneration relies on synchronous flowering and gregariousness vs. infrequent catastrophic disturbances remains uncertain.     

Resource Partitioning between Highly Eusocial Bees and Possible Impact of the Introduced Africanized Honey Bee on Native Stingless Bees in the Brazilian Atlantic Rainforest

The highly eusocial bee community of the neotropical Atlantic Rainforest was studied at Boracéia Biological Station in the state of São Paulo, Brazil. In this reserve, 17 species of stingless bees and the introduced Africanized honey bee were found, the latter being the most abundant flower visitor. Of all flowering plants, Asteraceae and Myrtaceae were particularly important as resources for bees. Trophic niche overlap between the various species of stingless bees is evident, and it was generally larger within the tribes Meliponini and Trigonini than between members of different tribes. Nevertheless, in the stingless bee community the competitive pressure is rather uniformly spread. The trophic niche of the Africanized honey bee can be positioned between those of Meliponini and Trigonini. Today this introduced species represents the main competitor in this bee community. However, its impact on native stingless bee populations is apparently buffered by mass-flowering trees which are the most important food plants of the indigenous highly eusocial bees.     

Flowering requirements of Polymnia canadensis (Asteraceae) and their influence on its life history variation

The purpose of this study is to determine the flowering requirements of Polymnia canadensis and how they correspond to the occurrence of winter annuals, biennials, and short-lived monocarpic perennials in this species. Polymnia canadensis has a vernalization requirement for flowering, and even very small plants (i.e., those with one pair of leaves) can be vernalized. Vernalized plants can flower under both long- and short days. However, to flower plants must attain a minimum postvernalization size. Plants of this primarily monocarpic species that do not die after they flower once require another period of vernalization to flower a second time (i.e., to be dicarpic). Vernalized plants exposed to high temperatures can be devernalized; these must be re-vernalized in order to flower.     

Density regulation during the regeneration of two monocarpic bamboos: self-thinning or intraclonal regulation?

Abstract. The population dynamics of two monocarpic bamboos, Sasa kurilensis and S. tsuboiana, were studied for more than 10 years after establishment following mass flowering. Both species show vigorous rhizomatous vegetative reproduction after growing up to maturity, but horizontal expansion in the seedling stage was much more vigorous in S. tsuboiana than in S. kurilensis. The pattern of changes in culm density in the two species was strikingly similar: culm densities of both species increased until they reached full-density states, after which they decreased in accordance with seedling growth. However, the mode of regulation in culm density was different. S. kurilensis seedlings were composed of only a few culms and scarcely extended their rhizomes during the observation period. Such poor lateral expansion resulted in asymmetric competition as observed in many non-clonal plants, and consequently their culm density decreased as a result of the mortality of genets due to self-thinning. In S. tsuboiana seedlings, the number of culms per genet increased considerably by frequent tillering and sprouting from rhizomes. However, after reaching full density state, the Bud Utility Ratio (BUR), (the proportion of the rhizome nodes with culms to the total number of rhizome nodes), decreased drastically. In this manner, S. tsuboiana regulated culm density intraclonally as is observed in the stable states of many clonal plants. Hence it is important for the understanding of the regeneration process in clonal species to clarify when and how their seedlings extend rhizomes during their growth.     

The role of sexual and vegetative reproduction in the population maintenance of a monocarpic perennial herb,Cardiocrinum cordatum var. glehnii

Because monocarpic perennial plants have only one reproductive opportunity in their entire life, they need to ensure offspring production. Some plants reproduce both sexually and vegetatively, and vegetative reproduction could possibly compensate for seed production. Therefore, the role and significance of these reproductive modes is likely to differ between monocarps and polycarps, which can reproduce many times. Cardiocrinum cordatum var. glehnii is a monocarpic perennial that reproduces both sexually and vegetatively (bulblet formation). Here, we investigated the characteristics and contribution to population maintenance of sexual and vegetative reproduction to reveal the significance of these two reproductive modes in this species. First, we found that bulblet formation occurred in plants after the three‐leaved rosette stage. Second, resource allocation experiments revealed that although resources were mainly invested in fruit maturation after the flowering season, resource allocation was switched from sexual reproduction to vegetative reproduction if seed production was insufficient. Third, the outcrossing rate in this species varied greatly according to the environment surrounding the population. However, reproductive assurance by selfing kept seed production stable even if flowers did not receive sufficient pollen for full seed set via outcross pollination, and moreover, there was no intensive inbreeding depression. Finally, genotypic identification of ramets suggested that daughter ramets derived from vegetative reproduction received the space that the mother flowering ramet had occupied until the previous year.     

Variation in reproductive modes and population genetic structures of a monocarpic perennial herb,Cardiocrinum cordatum,in relation to habitat fragmentation

Reproductive systems are recognized as having a profound influence on the extent and structure of genetic variation in plant populations. To investigate the spatiotemporal variation in the reproductive modes (sexual and vegetative reproduction) and population genetic structures of a monocarpic perennial herb, Cardiocrinum cordatum (liliaceae), we selected a variety of habitats (e.g. large forested area including primeval forest, small fragmented secondary forest, and so on) around Sapporo City, Japan. We conducted breeding experiments, monitored the fate and growth of marked individuals for 3 years, and also analyzed the spatiotemporal genetic variation of flowering plants within the populations using allozyme variation. Plants emasculated prior to anthesis produced mature fruits in all populations examined. However, seed production was significantly lower in the small fragmented populations, possibly because of the low availability of pollinators and subsequent pollen limitation. In these fragmented populations, the mature flowering plants tended to be more dependent on vegetative reproduction for their recruitment, because they can only produce flowers once in their lifetime. Genetic diversity using samples from mature flowering plants in each population was lower in the small fragmented populations than in the large populations. In addition, although genotypic compositions in the fragmented populations were more or less similar during the 3 years of the study, the dominant genotypes changed temporally and spatially every year in the large populations. The present study demonstrated that the reproductive features of C. cordatum can be altered in various environmental conditions, such as habitat fragmentation, and these changes considerably affected the population genetic structures and vice versa.     

Extremely long-lived stigmas allow extended cross-pollination opportunities in a high Andean plant

High-elevation ecosystems are traditionally viewed as environments in which predominantly autogamous breeding systems should be selected because of the limited pollinator availability. Chaetanthera renifolia (Asteraceae) is an endemic monocarpic triennial herb restricted to a narrow altitudinal range within the high Andes of central Chile (3300-3500 m a.s.l.), just below the vegetation limit. This species displays one of the larger capitulum within the genus. Under the reproductive assurance hypothesis, and considering its short longevity (monocarpic triennial), an autogamous breeding system and low levels of pollen limitation would be predicted for C. renifolia. In contrast, considering its large floral size, a xenogamous breeding system, and significant levels of pollen limitation could be expected. In addition, the increased pollination probability hypothesis predicts prolonged stigma longevity for high alpine plants. We tested these alternative predictions by performing experimental crossings in the field to establish the breeding system and to measure the magnitude of pollen limitation in two populations of C. renifolia. In addition, we measured the stigma longevity in unpollinated and open pollinated capitula, and pollinator visitation rates in the field. We found low levels of self-compatibility and significant levels of pollen limitation in C. renifolia. Pollinator visitation rates were moderate (0.047-0.079 visits per capitulum per 30 min). Although pollinator visitation rate significantly differed between populations, they were not translated into differences in achene output. Finally, C. renifolia stigma longevity of unpollinated plants was extremely long and significantly higher than that of open pollinated plants (26.3±2.8 days vs. 10.1±2.2, respectively), which gives support to the increased pollination probability hypothesis for high-elevation flowering plants. Our results add to a growing number of studies that show that xenogamous breeding systems and mechanisms to increase pollination opportunities can be selected in high-elevation ecosystems.