Climate change increases flowering duration, driving phenological reassembly and elevated co-flowering richness.

Changes to flowering phenology are a key response of plants to climate change. However, we know little about how these changes alter temporal patterns of reproductive overlap (i.e. phenological reassembly). We combined long-term field (1937-2012) and herbarium records (1850-2017) of 68 species in a flowering plant community in central North America and used a novel application of Bayesian quantile regression to estimate changes to flowering season length, altered richness and composition of co-flowering assemblages, and whether phenological shifts exhibit seasonal trends. Across the past century, phenological shifts increased species' flowering durations by 11.5 d on average, which resulted in 94% of species experiencing greater flowering overlap at the community level. Increases to co-flowering were particularly pronounced in autumn, driven by a greater tendency of late season species to shift the ending of flowering later and to increase flowering duration. Our results demonstrate that species-level phenological shifts can result in considerable phenological reassembly and highlight changes to flowering duration as a prominent, yet underappreciated, effect of climate change. The emergence of an autumn co-flowering mode emphasizes that these effects may be season-dependent.

Is self-incompatibility a reproductive barrier for hybridization in a sympatric species?

PREMISE: Barriers at different reproductive stages contribute to reproductive isolation. Self-incompatibility (SI) systems that prevent self-pollination could also act to control interspecific pollination and contribute to reproductive isolation, preventing hybridization. Here we evaluated whether SI contributes to reproductive isolation among four co-occurring Opuntia species that flower at similar times and may hybridize with each other. METHODS: We assessed whether Opuntia cantabrigiensis, O. robusta, O. streptacantha, and O. tomentosa, were self-compatible and formed hybrid seeds in five manipulation treatments to achieve self-pollination, intraspecific cross-pollination, open pollination (control), interspecific crosses or apomixis, then recorded flowering phenology and synchrony. RESULTS: All species flowered in the spring with a degree of synchrony, so that two pairs of species were predisposed to interspecific pollination (O. cantabrigiensis with O. robusta, O. streptacantha with O. tomentosa). All species had distinct reproductive systems: Opuntia cantabrigiensis is self-incompatible and did not produce hybrid seeds as an interspecific pollen recipient; O. robusta is a dioecious species, which formed a low proportion of hybrid seeds; O. streptacantha and O. tomentosa are self-compatible and produced hybrid seeds. CONCLUSIONS: Opuntia cantabrigiensis had a strong pollen-pistil barrier, likely due to its self-incompatibility. Opuntia robusta, the dioecious species, is an obligate outcrosser and probably partially lost its ability to prevent interspecific pollen germination. Given that the self-compatible species can set hybrid seeds, we conclude that pollen-pistil interaction and high flowering synchrony represent weak barriers; whether reproductive isolation occurs later in their life cycle (e.g., germination or seedling survival) needs to be determined.

Exploring the molecular regulation of vernalization-induced flowering synchrony in Arabidopsis.

Many plant populations exhibit synchronous flowering, which can be advantageous in plant reproduction. However, molecular mechanisms underlying flowering synchrony remain poorly understood. We studied the role of known vernalization-response and flower-promoting pathways in facilitating synchronized flowering in Arabidopsis thaliana. Using the vernalization-responsive Col-FRI genotype, we experimentally varied germination dates and daylength among individuals to test flowering synchrony in field and controlled environments. We assessed the activity of flowering regulation pathways by measuring gene expression across leaves produced at different time points during development and through a mutant analysis. We observed flowering synchrony across germination cohorts in both environments and discovered a previously unknown process where flower-promoting and repressing signals are differentially regulated between leaves that developed under different environmental conditions. We hypothesized this mechanism may underlie synchronization. However, our experiments demonstrated that signals originating from sources other than leaves must also play a pivotal role in synchronizing flowering time, especially in germination cohorts with prolonged growth before vernalization. Our results suggest flowering synchrony is promoted by a plant-wide integration of flowering signals across leaves and among organs. To summarize our findings, we propose a new conceptual model of vernalization-induced flowering synchrony and provide suggestions for future research in this field.

Among-individual variation in flowering phenology affects flowering synchrony and mating opportunity.

PREMISE: The timing and pattern of a plant's flowering can have important consequences for reproductive success. Variation in flowering phenology may influence the number of prospective mates, the risk of mating with lower quality individuals, and the likelihood of self-pollination. Here we use a common garden experiment to explore within- and among-population variation in phenology. Our work provides new insights into how flowering phenology shapes mating opportunity and flowering synchrony in a self-compatible perennial. METHODS: To quantify variation in flowering phenology we raised progeny from nine populations of Mimulus ringens in a common garden. For each individual, we measured phenological traits including age at flowering onset, daily floral display size, total flower number, and flowering synchrony with other members of the population, and related these traits to mating opportunity. We also tested how individual flowering schedules influence the magnitude of synchrony. RESULTS: Flowering phenology and synchrony varied substantially within and among populations. From day to day, plants often oscillated between large and small daily floral displays. Additionally, flowering schedules of individual plants strongly influenced flowering synchrony and, along with the number of flowering days, markedly affected plants' mating opportunity. CONCLUSIONS: Phenological traits such as flowering synchrony can affect the quantity of mating opportunities and may be important targets of natural selection. Our results highlight the need for studies that quantify flowering patterns of individuals as well as populations.

Floral Aroma and Pollinator Relationships in Two Sympatric Late-Summer-Flowering Mediterranean Asparagus Species.

This research delves into plant-pollinator relationships within the Mediterranean region, focusing on two synchronous and sympatric asparagus species: A. acutifolius and A. albus. For the first time, the floral scents of the genus Asparagus are reported. We investigate the volatile organic compounds (VOCs) present in their floral scents and their impact on pollinator attraction. Captured flower-emitted VOCs underwent solid-phase microextraction of headspace (SPME-HS) and gas chromatography and mass spectrometry (GC-MS) analysis. The investigation confirms distinctive aroma profiles for each species. A. albus predominantly emits benzene derivatives and sesquiterpenes, while A. acutifolius is characterized by carotenoid derivatives, monoterpenes, and sesquiterpenes. The only shared compounds between the two species are the sesquiterpenes (Z,E)-α-farnesene and (E,E)-α-farnesene. A positive correlation links peak floral aroma intensity (benzenoids in A. albus and ionones in A. acutifolius) with a higher pollinator visit frequency, emphasizing the critical role of intense floral scents in pollinator attraction. The study of reproductive aspects reveals almost complete gynodioecy in A. acutifolius, influencing unique dynamics for the two species. These adaptations hold significant importance within the Mediterranean ecosystem, particularly during the late dry summer period, when a limited number of plant species vie for a shared primary pollinator.

Quantification and Qualification of Floral Patterns of Coffea arabica L. in Colombia.

The phenological patterns of coffee flowering in Colombia have typically been studied in a descriptive way, with knowledge from an inferential perspective being scarce. The present study evaluated the effect of geographic location and accession on the floral patterns and phenological descriptors of Coffea arabica L. Fifteen accessions from the Colombian coffee collection (four tall and eleven short) were planted in the departments of Cesar, Caldas, Quindío and Cauca (Colombia). The number of flower buds per branch per plant per evaluated accession was recorded weekly during four flowering semesters. Subsequently, the phenological flowering descriptors, namely synchrony among individuals, intraindividual temporal variability and number of events were calculated. The data were analyzed descriptively, and then the inferential component was conducted using analysis of variance for a two-factor additive model and randomization restriction. The results showed that there are two flowering patterns according to the expression of flowering in the floral cycles, the "annual" class in the department of Cesar and the "continual" class in the departments of Caldas, Quindío and Cauca. The phenological descriptors show differences between the departments according to the coffee zone to which it belongs (northern, central or southern). In turn, the floral pattern of each area can be linked to the latitudinal change in daily sunshine, as well as to the distribution of rainfall and temperature, in a very broad sense and based on the literature. The data did not provide statistical evidence to suggest differences among the accessions or between the tree sizes evaluated.

Dynamics of pollen-generating environment producing impact on society based on the relative humidity of the previous year and flowering synchrony.

An area with the potential of producing high concentrations of airborne pollen is defined as the 'potential pollinosis area'. However, the detailed dynamics of pollen dispersion are not fully understood. Further, studies on the detailed dynamics of the pollen-generating environment are limited. This study aimed to determine the relationship between the dynamics of potential pollinosis areas and annual meteorological factors with high spatiotemporal resolution. We visualised and analysed the dynamics of the potential polliosis area based on 11-year high-spatial-density observation data for the atmospheric concentrations of Cryptomeria japonica pollen. The results showed that the potential pollinosis area headed northeast with repeated expansion and contraction, while the centre of the potential pollinosis area leaped to the north in mid-March. The variance in the fluctuation of the coordinates for the potential pollinosis area before the northward leap was strongly related to the variance in the relative humidity of the previous year. These results indicated that the pollen grains of C. japonica across Japan are distributed based on the meteorological conditions of the previous year until mid-March, after which, the pollen grains are distributed through flowering synchrony. Our results suggest that daily nationwide flowering synchrony has a significant annual impact, and changes in relative humidity caused by, for example, global warming would affect the occurrence and predictability of seasonal changes in the pollen dispersion dynamics of C. japonica and other pollen-producing species. Our study showed that pollen production by C. japonica through flowering synchrony is a major cause of nationwide pollinosis and other allergy-related health problems.

Fire effects on plant reproductive fitness vary among individuals, reflecting pollination-dependent mechanisms.

PREMISE: Fire induces flowering in many plant species worldwide, potentially improving reproductive fitness via greater availability of resources, as evident by flowering effort, and improved pollination outcomes, as evident by seed set. Postfire increases in flowering synchrony, and thus mating opportunities, may improve pollination. However, few studies evaluate fire effects on multiple components of fitness. Consequently, the magnitude and mechanism of fire effects on reproductive fitness remain unclear. METHODS: Over multiple years and prescribed burns in a prairie preserve, we counted flowering stems, flowers, fruits, and seeds of three prairie perennials, Echinacea angustifolia, Liatris aspera, and Solidago speciosa. We used aster life-history models to assess how fire and mating opportunities influenced annual maternal fitness and its components in individual plants. RESULTS: In Echinacea and Liatris, but not in Solidago, fire increased head counts, and both fire and mating opportunities increased maternal fitness. Burned Echinacea and Liatris plants with many flower heads produced many seeds despite low seed set (fertilization rates). In contrast, plants with an average number of flower heads had high seed set and produced many seeds only when mating opportunities were abundant. CONCLUSIONS: Fire increased annual reproductive fitness via resource- and pollination-dependent mechanisms in Echinacea and Liatris but did not affect Solidago fitness. The consistent relationship between synchrony and seed set implies that temporal mating opportunities play an important role in pollination. While fire promotes flowering in many plant species, our results reveal that even closely related species exhibit differential responses to fire, which could impact the broader plant community.

Sex dimorphism in dioecious Palmer amaranth (Amaranthus palmeri) in response to water stress.

MAIN CONCLUSION: Phenological isolation can potentially reduce seed output and may be exploited as a novel tool for ecological management of dioecious weeds. Dioecious plants may benefit from a maximized outcrossing and optimal sex-specific resource allocation; however, this breeding system may also be exploited for weed management. Seed production in dioecious species is contingent upon the co-occurrence and co-flowering of the two genders and can be further disturbed by flowering asynchrony. We explored dimorphism in secondary sex characters in Amaranthus palmeri, and tested if reproductive synchrony can be affected by water stress. We have used seeds of A. palmeri from California, Kansas and Texas, and studied secondary sex characters under natural conditions and in response to water stress. Seeds of A. palmeri from California (CA) and Kansas (KS) were cordially provided by Dr. Anil Shrestha (California State University, Fresno, California) and Dr. Dallas E. Peterson (Kansas State University, Manhattan, Kansas), respectively. Seeds of a third population were collected from mature plants (about 30 plants) from a set-aside field in College Station, Texas. A. palmeri showed no sexual dimorphism with regard to the timing of emergence, plant height, and relative growth rate. While the initiation of flowering occurred earlier in males than females, females preceded males in timing of anthesis. Water stress delayed anthesis in males to a greater extent than females increasing the anthesis mismatch between the two sexes by seven days. Our data provide the first evidence of environment-controlled flowering asynchrony in A. palmeri. From a practical point of view, phenological isolation can potentially reduce seed output and may be exploited as a novel tool for ecological management of dioecious weeds.

Earlier spring reduces potential for gene flow via reduced flowering synchrony across an elevational gradient.

PREMISE: One of the best-documented ecological responses to climate warming involves temporal shifts of phenological events. However, we lack an understanding of how phenological responses to climate change vary among populations of the same species. Such variability has the potential to affect flowering synchrony among populations and hence the potential for gene flow. METHODS: To test whether an earlier start of the growing season affects the potential for gene flow among populations, we quantified the distributions of flowering times of two spring-flowering plants (Trillium erectum and Erythronium americanum) over 6 years along an elevational gradient. We developed a novel model-based metric of potential gene flow between pairs of populations to quantify the potential for pollen-mediated gene flow based on flowering phenology. RESULTS: Earlier onset of spring led to greater separation of peak flowering dates across the elevational gradient for both species investigated, but was only associated with a reduction in potential gene flow in T. erectum, not E. americanum. CONCLUSIONS: Our study suggests that climate change could decrease gene flow via phenological separation among populations along climatic gradients. We also provide a novel method for quantifying potential pollen-mediated gene flow using data on flowering phenology, based on a quantitative, more biologically interpretable model than other available metrics.

Flowering synchrony drives reproductive success in a wind-pollinated tree.

Synchronised and quasi-periodic production of seeds by plant populations, known as masting, is implicated in many ecological processes, but how it arises remains poorly understood. Flowering and pollination dynamics are hypothesised to provide the mechanistic link for the observed relationship between weather and population-level seed production. We report the first experimental test of the phenological synchrony hypotheses as a driver of pollen limitation in mast seeding oaks (Quercus ilex). Higher flowering synchrony yielded greater pollination efficiency, which resulted in 2-fold greater seed set in highly synchronised oaks compared to asynchronous individuals. Pollen addition removed the negative effect of asynchronous flowering on seed set. Because phenological synchrony operates through environmental variation, this result suggests that oak masting is synchronised by exogenous rather than endogenous factors. It also points to a mechanism by which changes in flowering phenology can affect plant reproduction of mast-seeding plants, with subsequent implications for community dynamics.

Does sexual dimorphism exist in flowering phenology traits in anemophilous dioecious species? A test with Rumex acetosa.

PREMISE: Sexual dimorphism in flowering phenology traits may have evolved under sexual selection and vector-mediated selection. The conspicuous sexual dimorphism and sex-specific selection pressures in flowering phenology traits have been investigated mainly in entomophilous dioecious plants, whereas little is known about this in anemophilous plants. METHODS: We examined sexual dimorphism in flowering onset, flowering peak, flowering duration, maximum proportion of open flowers per inflorescence branch, maximum proportion of newly opening flowers on a given date per branch, and longevity of individual flowers in natural Rumex acetosa populations. Correlations between flowering phenology traits and the degree of flowering overlap with the opposite sex were examined. We also tested whether the overlap of female flowering with male flowering enhanced seed set in female plants. RESULTS: Little sexual dimorphism was observed in flowering onset, peak, duration, and maximum proportion of newly opening flowers. Females had greater floral longevity and greater maximum proportion of open flowers than males. Flowering overlap with the opposite sex significantly increased with the maximum proportion of newly opening flowers and decreased with temporal deviation in the flowering peak in both sexes. Females with greater flowering overlap with males set more seeds in two of the three study populations. CONCLUSIONS: In wind-pollinated R. acetosa, little sexual dimorphism in phenological traits may have evolved to achieve synchronous flowering with the opposite sex. Our results suggest that, in angiosperms, not only common selection but also anemophily-specific selection may shape little sexual dimorphism in R. acetosa, unlike in entomophilous plants.

Evidence of temporal niche separation via low flowering time overlap in an old-field plant community.

Flowering time is a trait that reflects the timing of specific resource requirements by plants. Consequently, several predictions have been made related to how species are assembled within communities according to flowering time. Strong overlap in flowering time among coexisting species may result from clustered abiotic resources, or contribute to improved pollination success. Conversely, low flowering time overlap (asynchrony) among coexisting species may reduce competition for soil, light, or pollinator resources and alleviate interspecific pollen transfer. Here, we present evidence that coexisting species in an old-field community generally overlap less in flowering time than expected under a commonly used and statistically validated null model. Flowering time asynchrony was more pronounced when abundance data were used (compared to presence-absence data), and when analyses focused on species that share bees as pollinators. Control and herbivore-exclusion plots did not differ in flowering time overlap, providing no evidence of the reduction in overlap expected to result from increased competition. Our results varied with the randomization algorithm used, emphasizing that the choice of algorithm can influence the outcome of null models. Our results varied between 2 years, with patterns being less clear in the second year, when both growing season and flowering times were contracted. Finally, we found evidence that further supports a previous finding that higher plot-level flowering time overlap was associated with higher proportions of introduced species. Reduced flowering time overlap among species in our focal community may promote coexistence via temporal niche differentiation and reduced competition for pollinators and other abiotic resources.

Reproductive consequences of variation in flowering phenology in the dry forest tree Enterolobium cyclocarpum in Guanacaste, Costa Rica.

PREMISE OF THE STUDY: Flowering initiation, duration and magnitude, and degree of flowering synchrony within a population can affect the reproductive fitness of individuals. We examined the flowering phenology within a population of the tropical dry forest Guanacaste tree (Enterolobium cyclocarpum) to gauge the impact of phenological variation among trees on fruit production and progeny vigor. METHODS: We monitored the flowering phenology of 93 trees weekly during 2005, 2006, and 2007, using a scale based on the percentage of the crown with open flowers. We also monitored fruit production for each tree in 2005, 2006, 2007, and 2008. Finally, we evaluated the relationship between phenological variation and progeny performance. KEY RESULTS: Ten measures of flowering phenology and synchrony among flowering trees, based on the number of weeks when anthesis of the crown exceeded 50%, were used to develop four phenological profiles. These profiles were correlated with significant differences in fruit production and progeny vigor. Trees with flowers in >50% of their crown for at least 2 weeks produced more fruits and more vigorous progeny than trees with other profiles. Trees also tended to produce the same phenological profile among years than predicted by chance. CONCLUSIONS: Guanacaste trees vary significantly in the initiation of anthesis, duration and magnitude of flowering, and degree of synchrony among trees. Trees also tend to maintain the same flowering profile among years. Finally, the flowering behavior of E. cyclocarpum leads to significant differences in fruit and seed production, germination, and early progeny growth.

Phenotypic selection varies with pollination intensity across populations of Sabatia angularis.

Pollinators are considered primary selective agents acting on plant traits, and thus variation in the strength of the plant-pollinator interaction might drive variation in the opportunity for selection and selection intensity across plant populations. Here, we examine whether these critical evolutionary parameters covary with pollination intensity across wild populations of the biennial Sabatia angularis. We quantified pollination intensity in each of nine S. angularis populations as mean stigmatic pollen load per population. For female fitness and three components, fruit number, fruit set (proportion of flowers setting fruit) and number of seeds per fruit, we evaluated whether the opportunity for selection varied with pollination intensity. We used phenotypic selection analyses to test for interactions between pollination intensity and selection gradients for five floral traits, including flowering phenology. The opportunity for selection via fruit set and seeds per fruit declined significantly with increasing pollen receipt, as expected. We demonstrated significant directional selection on multiple traits across populations. We also found that selection intensity for all traits depended on pollination intensity. Consistent with general theory about the relationship between biotic interaction strength and the intensity of selection, our study suggests that variation in pollination intensity drives variation in selection across S. angularis populations.

The strength of assortative mating for flowering date and its basis in individual variation in flowering schedule.

Although it has been widely asserted that plants mate assortatively by flowering time, there is virtually no published information on the strength or causes of phenological assortment in natural populations. When strong, assortative mating can accelerate the evolution of plant reproductive phenology through its inflationary effect on genetic variance. We estimated potential assortative mating for flowering date in 31 old-field species in Ontario, Canada. For each species, we constructed a matrix of pairwise mating probabilities from the individual flowering schedules, that is the number of flower deployed on successive dates. The matrix was used to estimate the phenotypic correlation between mates, ρ, for flowering date. We also developed a measure of flowering synchrony within species, S, based upon the eigenstructure of the mating matrix. The mean correlation between pollen recipients and potential donors for flowering date was ρ=0.31 (range: 0.05-0.63). A strong potential for assortative mating was found among species with high variance in flowering date, flowering schedules of short duration and skew towards early flower deployment. Flowering synchrony, S, was negatively correlated with potential assortment (r= -0.49), but we go on to show that although low synchrony is a necessary condition for phenological assortative mating, it may not be sufficient to induce assortment for a given phenological trait. The potential correlation between mates showed no seasonal trend; thus, as climate change imposes selection on phenology through longer growing seasons, spring-flowering species are no more likely to experience an accelerated evolutionary response than summer species.

Say it with flowers: flowering acceleration by root communication.

The timing of reproduction is a critical determinant of fitness, especially in organisms inhabiting seasonal environments. Increasing evidence suggests that inter-plant communication plays important roles in plant functioning. Here, we tested the hypothesis that flowering coordination can involve communication between neighboring plants. We show that soil leachates from Brassica rapa plants growing under long-day conditions accelerated flowering and decreased allocation to vegetative organs in target plants growing under non-inductive short-day conditions. The results suggest that besides endogenous signaling and external abiotic cues, flowering timing may involve inter-plant communication, mediated by root exudates. The study of flowering communication is expected to illuminate neglected aspects of plant reproductive interactions and to provide novel opportunities for controlling the timing of plant reproduction in agricultural settings.

Relationship between capitulum size and pre-dispersal seed predation by insect larvae in common Asteraceae.

The evolution of a showy floral display as an advertisement to pollinators could simultaneously advertise the availability of resources to pre-dispersal seed-predators. The hypotheses tested here are that the incidence of seed predation by bud-infesting insect larvae in capitula of Asteraceae is positively related to (1) capitulum size among species, (2) capitulum size within species, (3) capitulum lifespan, and (4) the degree of flowering asynchrony on individual plants. Three populations of each of 20 common herbaceous species of Asteraceae from disturbed ground and grassland habitats were monitored for the presence of pre-dispersal, seed-eating insect larvae. Mean capitulum size (receptacle width) of each species was measured. In a sub-set of eight species, individual capitula were tagged to determine their flowering phenology and lifespan (from anthesis to seed shedding). From these data an index of flowering synchrony on individual plants was derived. Among species, the incidence of larval infestation increased with capitulum size. Small-flowered species such as Achillea millefolium were largely free of bud-infesting larvae, whilst large-flowered species such as Arctium minus were heavily infested. In three cases investigated in greater detail, bud infestation was found to increase with capitulum size within species, suggesting a potential for natural selection to favour smaller capitula. No relationship was found between infestation levels and either capitulum lifespan or degree of flowering synchrony, and there was no evidence that the relationship between capitulum size and infestation was confounded by correlations with these other features. The results support hypotheses 1 and 2, but not 3 and 4. It is suggested that the characteristic capitulum size of each species may represent a trade-off between the opposing selection pressures of pollinators and pre-dispersal seed predators.

Consequences of variation in flowering phenology for seed head herbivory and reproductive success in Erigeron glaucus (Compositae).

We examined the relationship between flowering phenology, reproductive success (seed production only), and seed head herbivory for 20 similarly sized clones of Erigeron glaucus growing at Bodega Bay Reserve, northern California, USA. Although clones tended to reach peak flowering on the same date, they differed in the proportion of their total flowers produced around that date (flowering synchrony). Clones also differed in the number and density of flower heads presented at any one time to pollinators and herbivores (floral display). Both of these characteristics had consequences for herbivory and plant reproductive success. The proportion of flower heads damaged by insect herbivores was greater for clones that concentrated flowering activity during the main flowering period for the population as a whole (high synchrony) compared to clones that spread flowering out temporally. The primary reason for this result was that clones with low flowering synchrony produced a significant proportion of their flower heads during the fall and therefore, escaped attack by the tephritid fly, Tephritis ovatipennis. Clones with intermediate synchrony had lower seed success (total number of viable seeds produced over the year) than clones with either low or high synchrony. The proportion of flower heads damaged by insect herbivores and number of tephritid flies reared from flower heads were both negatively correlated to floral display while seed head mass and germination rates were positively related to display. Thus, clones which produced dense floral displays were favored both in terms of reduced herbivory and increased successful seed production.