Modeling spatial dynamics of episodic and synchronous reproduction by plant populations: the effect of small-scale pollen coupling and large-scale climate

Many plant species show masting, intermittent and synchronized reproduction at population level. In the present paper, we review the resource-based model providing a theoretically plausible physiological mechanism underlying masting. In the model, a non-linear allocation of energy reserves is considered: plants accumulate photosynthate every year, produce flowers when the energy reserve level exceeds a threshold, and set seeds at a rate limited by pollen availability. The model predicted that individual plants alter their reproductive dynamics from annual to intermittent depending on how heavily the plant invests resource in reproduction. When fruit production is limited by the availability of outcross pollen, a plant population showed diverse reproductive behavior such as completely synchronized or desynchronized reproduction. Spatial scale of reproductive synchrony tended to be a few times larger than the range of direct pollen exchange. Impact of climatic fluctuation correlated at a large spatial scale was also investigated as an alternative synchronizing factor. The variation in annual productivity and the reproductive threshold induced from climatic fluctuation was accounted for by incorporating an additional term in the model. When plants show a 2 year reproductive cycle, highly synchronized reproduction at a regional scale was induced due to correlated environmental forcing, but reproductive synchrony with long intermast periods was realized only when pollen coupling and environmental forcing were at work. These results suggest that distance-dependent processes, such as pollen exchange between nearby trees, induce synchrony at a local scale and external environmental forcing correlated at geographically large scales works to strengthen and maintain such a synchrony.     

Dynamics of internal carbon resources during masting behavior in trees

Several proximate factors of masting have been provided. Here, I focus on the role of internal factors, especially the relationship between internal carbon resources and modular structures in trees. I summarize various studies of carbon resource allocation for reproduction during masting events in terms of the proximate factors of masting and discuss the modular structure in which trees accumulate and consume carbon resources as well as the timing when internal carbon resources affect masting since trees have complex resource dynamics among organs. The resource budget model, which provides a simple mechanistic explanation of the masting mechanism, is supported by various study lines. This model assumes decreasing levels of stored photosynthate after flowering and fruiting. According to several studies, however, carbon reserves do not decrease after fruiting in species in which the modules autonomously allocate current photosynthate for fruiting. In addition, it is important to elucidate when carbon resources affect masting events because during their long developmental processes, trees pass through various stages until they produce maturing fruits to create successful masting events. To explore the mechanisms of masting in future studies, it would be important to figure out how and when candidate factors (including nutrients other than carbon) may influence the entire reproduction process, for example, using field manipulation experiments.     

Evolution of masting with intermittence and synchronization under the enhancements of fertility and survival

Mast seeding is a reproductive mode in plants characterized by intermittence and intra- or interspecific synchronization. Several mechanisms have been proposed to explain the evolution of mast seeding, but the relative importance of each is still unclear due to the complex interactions among the various factors involved, i.e., the two components of masting (intermittence and synchronization), two potential advantages of masting (enhancement of fertility and survival), and the intensities of interactions among individuals through enhancement effects. Several masting studies have claimed that independent selective forces may operate to drive the evolution of intermittence and synchrony, although a theoretical framework for the action of these independent selective forces has not yet been established. In the present study, we investigated the relationships among these factors by analyzing a mathematical model and conducting computer simulations. We found that intense interactions among plant individuals, through the enhancement of fertility or survival, promoted synchronous reproduction while concomitantly suppressing evolution of intermittence. We also demonstrated that enhancement of either fertility or survivorship alone may be insufficient for the evolution of masting, whereas a combination of the two effects can significantly promote it. This suggested a complementary relationship between two well-known hypotheses for the origin of masting, namely, the pollen/pollinator hypothesis and the predator satiation hypothesis.     

Parameterisation and validation of a resource budget model for masting using spatiotemporal flowering data of individual trees

Synchronised and fluctuating reproduction by plant populations, called masting, is widespread in diverse taxonomic groups. Here, we propose a new method to explore the proximate mechanism of masting by combining spatiotemporal flowering data, biochemical analysis of resource allocation and mathematical modelling. Flowering data of 170 trees over 13 years showed the emergence of clustering with trees in a given cluster mutually synchronised in reproduction, which was successfully explained by resource budget models. Analysis of resources invested in the development of reproductive organs showed that parametric values used in the model are significantly different between nitrogen and carbon. Using a fully parameterised model, we showed that the observed flowering pattern is explained only when the interplay between nitrogen dynamics and climatic cues was considered. This result indicates that our approach successfully identified resource type‐specific roles on masting and that the method is suitable for a wide range of plant species.     

Spatial dynamics of specialist seed predators on synchronized and intermittent seed production of host plants

Masting, the synchronized and intermittent seed production by plant populations, provides highly variable food resources for specialist seed predators. Such a reproductive mode helps minimize seed losses through predator satiation and extinction of seed predator populations. The seed predators can buffer the resource variation through dispersal or extended diapause. We developed a spatially explicit resource-consumer model to understand the effect of masting on specialist seed predators. The masting dynamics were assumed to follow a resource-based model for plant reproduction, and the population dynamics of the predator were represented by a spatially extended Nicholson-Bailey model. The resultant model demonstrated that when host plants reproduce intermittently, seed predator populations go locally extinct, but global persistence of the predator is facilitated by dispersal or extended diapause. Global extinction of the predator resulted when the intermittent reproduction is highly synchronized among plants. An approximate invasion criterion for the predators showed that negative lag-1 autocorrelation in seeding reduces invasibility, and positive lag-1 cross-correlation enhances invasibility. Spatial synchronization in seeding at local scale caused by pollen coupling (or climate forcing) further prevented invasion of the predators. If the predators employed extended diapause, extremely high temporal variability in reproduction was required for plants to evade the predators.     

Climate variation,reproductive frequency and acorn yield in English Oaks

Aims Annually variable but synchronous production of large seed crops (‘masting’) is a widespread phenomenon in temperate trees. Mounting concerns about the impacts of anthropogenic climate change (ACC) on plant reproduction gives urgency to our need to understand better the role of climate on tree reproduction, and in particular, mast events. Unlike our understanding of reproductive phenology however, there is little consensus regarding how climate affects plant reproductive effort or indeed the actual environmental triggers that underpin masting behaviour.     

Masting behaviour in a Mediterranean pine tree alters seed predator selection on reproductive output

• Context‐dependency in species interactions is widespread and can produce concomitant patterns of context‐dependent selection. Masting (synchronous production of large seed crops at irregular intervals by a plant population) has been shown to reduce seed predation through satiation (reduction in rates of seed predation with increasing seed cone output) and thus represents an important source of context‐dependency in plant‐animal interactions. However, the evolutionary consequences of such dynamics are not well understood.
• Here we describe masting behaviour in a Mediterranean model pine species (Pinus pinaster) and present a test of the effects of masting on selection by seed predators on reproductive output. We predicted that masting, by enhancing seed predator satiation, could in turn strengthen positive selection by seed predators for larger cone output. For this we collected six‐year data (spanning one mast year and five non‐mast years) on seed cone production and seed cone predation rates in a forest genetic trial composed by 116 P. pinaster genotypes.
• Following our prediction, we found stronger seed predator satiation during the masting year, which in turn led to stronger seed predator selection for increased cone production relative to non‐masting years.
• These findings provide evidence that masting can alter the evolutionary outcome of plant‐seed predator interactions. More broadly, our findings highlight that changes in consumer responses to resource abundance represent a widespread mechanism for predicting and understanding context dependency in plant‐consumer evolutionary dynamics.

     

Nitrogen storage dynamics are affected by masting events in Fagus crenata

It is generally assumed that the production of a large crop of seeds depletes stores of resources and that these take more than 1 year to replenish; this is accepted, theoretically, as the proximate mechanism of mast seeding (resource budget model). However, direct evidence of resource depletion in masting trees is very rare. Here, we trace seasonal and inter-annual variations in nitrogen (N) concentration and estimate the N storage pool of individuals after full masting of Fagus crenata in two stands. In 2005, a full masting year, the amount of N in fruit litter represented half of the N present in mature leaves in an old stand (age 190–260 years), and was about equivalent to the amount of N in mature leaves in a younger stand (age 83–84 years). Due to this additional burden, both tissue N concentration and individual N storage decreased in 2006; this was followed by significant replenishment in 2007, although a substantial N store remained even after full masting. These results indicate that internal storage may be important and that N may be the limiting factor for fruiting. In the 4 years following full masting, the old stand experienced two moderate masting events separated by 2 years, whilst trees in the younger stand did not fruit. This different fruiting behavior may be related to different “costs of reproduction” in the full masting year 2005, thus providing more evidence that N may limit fruiting. Compared to the non-fruiting stand, individuals in the fruiting stand exhibited an additional increase in N concentrations in roots early in the 2007 growing season, suggesting additional N uptake from the soil to supply resource demand. The enhanced uptake may alleviate the N storage depletion observed in the full masting year. This study suggests that masting affects N cycle dynamics in mature Fagus crenata and N may be one factor limiting fruiting.     

Masting in a temperate tree: Evidence for environmental prediction?

Many plant species produce large fruit crops in some years and then produce few or no fruits in others. Synchronous, inter‐annual variation in plant reproduction is known as ‘masting’ and its adaptive significance has yet to be fully resolved. For 8 consecutive years, I quantified every fruit produced by 22 females of a New Zealand tree species (Dysoxylum spectabile), which has an unusual habit of taking a full calendar year to mature fruits after flowering. Fruit production varied strongly among years and was tightly synchronized among trees. Annual variability in fruit production declined with total reproductive output, indicating trees with lower fecundity exhibited a stronger tendency to mast. Although unrelated to temperature, annual fruit production was positively related to precipitation during annual periods of fruit development, and negatively related to fruit production in the previous year. Seedlings had higher rates of survivorship in a wet, high‐seed year than in a dry, low‐seed year, suggesting that seedlings might be drought sensitive. Therefore, D. spectabile produced large fruit crops during periods of high rainfall prior to fruit maturation, which may enhance survivorship of drought‐intolerant seeds. Results were inconsistent with several hypotheses that are widely believed to be the most likely explanations for masting. Instead, results were consistent with the environmental prediction hypothesis, suggesting that this hypothesis may be more important than previously appreciated.     

Evolutionary jumping and breakthrough in tree masting evolution

Many long-lived plants such as trees show masting or intermittent and synchronized reproduction. In a coupled chaos system describing the dynamics of individual-plant resource budgets, masting occurs when the resource depletion coefficient k (ratio of the reproductive expenditure to the excess resource reserve) is large. Here, we mathematically studied the condition for masting evolution. In an infinitely large population, we obtained a deterministic dynamical system, to which we applied the pairwise invasibility plot and convergence stability of evolutionary singularity analyses. We prove that plants reproducing at the same rate every year are not evolutionarily stable. The resource depletion coefficient k increases, and the system oscillates with a period of 2 years (high and low reproduction) if k<1. Alternatively, k may evolve further and jump to a value >1, resulting in the sudden start of intermittent reproduction. We confirm that a high survivorship of young plants (seedlings) in the light-limited understory favors masting evolution, as previously suggested by computer simulations and field observations. The stochasticity caused by the finiteness of population size also promotes masting evolution.     

Reproductive correlation and mean-variance scaling of reproductive output for a forest model

We analyse the mean-variance scaling of reproductive output for a previously published forest model. The model relates individual reproductive effort and pollen limitation to the degree of synchrony in reproduction throughout a forest. We show that the exponent of Taylor's power law reflects the degree of synchrony of reproduction because it indicates the covariance of reproductive behavior. Further, we are able to relate the three components of masting, individual variability, population variability and synchrony in reproductive output, using Taylor's power law. Therefore Taylor's power law can be used as a synoptic index of masting.     

Dynamics of mineral nutrient storage for mast reproduction in the tropical emergent tree Dryobalanops aromatica

Limitations in resources are considered to be important in mass-fruiting trees, based on the speculation that they need to consume a large amount of stored resources in a very short period. To test this hypothesis, we studied the total reproductive costs per individual of the tree Dryobalanops aromatica (Dipterocarpaceae), and the dynamics of stored mineral nutrients, specifically nitrogen, phosphorus, and potassium; we then estimated the contribution of each of the stored resources to reproduction in a lowland dipterocarp forest in Sarawak, Malaysia. D. aromatica is an emergent and masting tree species, and it produced a large amount of mature fruit in a masting period running 2001–2002. The dynamics patterns were markedly different for each of the stored nutrients. The phosphorus concentration clearly decreased in the branch, stem and root during reproduction, but nitrogen fluctuated by only a small amount in any organ during this period. The potassium concentration fell in all organs during flowering, but even increased during fruit development. Stored phosphorus accounted for 67.7% of the total phosphorus requirements for reproduction, but nitrogen accounted for only 19.7%. Stored potassium did not appear to contribute anything, at least to fruit production. Our results suggest that D. aromatica supplies phosphorus needed for reproduction mainly from stored resources in the tree, unlike nitrogen or potassium. The accumulation of phosphorus could be the decisive factor in the occurrence and frequency of mast reproduction in the relatively poor soil conditions prevailing in the tropical rain forests of Southeast Asia.     

The evolutionary ecology of mast seeding

The past seven years have seen a revolution in understanding the causes of mast seeding In perennial plants. Before 1987, the two main theories were resource matching (i.e. plants vary their reproductive output to match variable resources) and predator satiation (i.e. losses to predators are reduced by varying the seed crop). Today, resource matching is restricted to a proximate role, and predator satiation is only one of many theories for the ultimate advantage of masting. Wind pollination, prediction of favourable years for seedling establishment, animal pollination, animal dispersal of fruits, high accessory costs of reproduction and large seed size have all been advanced as possible causes of masting. Of these, wind pollination, predator satiation and environmental prediction are important in a number of species, but the other theories have less support. In future, Important advances seem likely from quantifying synchrony within a population, and examining species with very constant reproduction between years.     

Direct and indirect effects of masting on rodent populations and tree seed survival

Many plant species are thought to benefit from mast seeding as a result of increased seed survival through predator satiation. However, in communities with many different masting species, lack of synchrony in seed production among species may decrease seed survival by maintaining seed predator populations through the intermast cycle. Similarly, masting by different plant species may have different effects on the seed predator community. We conducted a three-year study in a northeastern USA temperate deciduous forest to determine if production of large seed crops by several tree species was synchronous, and if they had similar effects on all small mammal species. We found that red oak mast crops resulted in increased densities of Peromyscus leucopus and P. maniculatus , but had no effect on Clethrionomys gapperi abundance. Conversely, C. gapperi populations, but not Peromyscus populations, appeared to increase in response to a large red maple seed crop. Differences in small mammal abundance resulted in changes in species-specific seed survival: in the year of abundant C. gapperi , experimentally placed red oak acorns had significantly higher survival than in the year of high Peromyscus abundance. Red oak acorn removal was positively correlated with Peromyscus abundance, while red maple seed removal was significantly higher with increased C. gapperi abundance. Thus, species-specific seed production had differential effects on subsequent small mammal abundance, which in turn affected seed survival. We suggest that at the level of the community, even short-term lack of synchrony in production of large seed crops can cause variation in postdispersal seed survival, through differential effects on the community of small mammal seed predators.     

Masting in Buxus balearica: assessing fruiting patterns and processes at a large spatial scale

Masting consists of the synchronous highly variable seed production among years by a plant population. We studied spatiotemporal variation in fruit production in ten populations of Buxus balearica (six in the Balearic Islands and four in the Iberian Peninsula) from 2001 to 2004 in the light of masting. In some of them we assessed, by means of both observational and experimental data, the relationship between fruit production and some abiotic variables, the role of previous reproduction, the "pollination efficiency" and the "predator satiation" hypotheses, as well as the consequences for seedling density and survival. Fruit production in B. balearica showed substantial between-year variation, especially in island compared to mainland populations. Correlative evidence indicated that this variation and its geographic pattern were related to differences between regions in rainfall variability, cost of reproduction and the degree of ambophily. We found no indication of predator satiation. However, experimental tests failed to support many of our results, namely a negative effect of previous reproduction on future flowering in island populations and lower pollen limitation with increasing flower production. We therefore warn against exclusive reliance on correlations when testing hypotheses related to masting. In addition, seedling recruitment increased after some episodes of high fruit production but probably additional factors had a role in recruitment, suggesting that mast events not always translate into increased reproductive success. Although a limited time series only allows considering B. balearica as showing 'putative' masting, weather and pollination-related processes are good candidates for further exploration of fruiting patterns and processes at a large spatial scale.     

Density-dependent reproductive success among sympatric dipterocarps during a major mast fruiting event

Although masting in Southeast Asia is characterized by the interspecific synchronization of reproduction, little is known about the variation in regeneration strategies among sympatric tree species during major masting events. Herein, we examined the hypothesis that non-abundant species achieve greater seed survival per seed production at the pre- and post-dispersal stages by synchronizing reproduction with abundant species. During the masting event from May to September 2010, we installed seed traps in a primary forest plot of the Deramakot Forest Reserve, Borneo. To identify the possible causes of post-dispersal seed mortality, we conducted a seed-sowing experiment from September 2010 to July 2011 in a primary forest plot with high community-level dipterocarp seed density and two surrounding secondary forests with low seed densities. An abundant species (Shorea multiflora) produced more seeds than other species and exhibited a lower survival rate during the pre-dispersal stage. The ratio of aborted seeds was greater in species with greater seed production, while the ratio of seeds predated by insects was not, suggesting that resource limitations and/or greater inbreeding frequency may explain inefficient seed production. Interspecific variation was rarely observed for post-dispersal seed survival rates. Our study highlights the density-dependent variation in reproductive success between abundant and non-abundant dipterocarp species at the pre-dispersal stage. Non-abundant species achieved greater reproductive success by synchronizing reproduction with the masting of abundant species, which might be an important mechanism for sustainability of rare species populations.     

Variable timing of reproduction in unpredictable environments: adaption of flood plain plants

We study the evolutionarily stable reproductive timing of annual plants that face unpredictable environmental disturbances. Plants living in a riverbed often experience a disturbance before they reproduce, suffering major fitness loss. Plants reproducing prior to the flood season are free from the risk of lost reproduction, but a small flowering plant can produce only a few numbers of seeds. If the date of disturbance is unpredictable, a mixed strategy of reproductive timing may evolve in which individuals of the same genotype have different reproductive dates. We calculate the evolutionarily stable phenotype distribution analytically. Depending on parameters, the ESS distribution is either (1) a timid strategy-the plant reproduces when small, prior to the major disturbance season; (2) a bold strategy-the plant reproduces only when it is fully grown; (3) a mixture of early and late reproduction; or (4) dates of reproduction spread over a wide interval. We also examine the effects of developmental and environmental noises that make realized flowering dates deviate from that programmed by the genotype, which follows the ESS distribution. In the presence of noise, the ESS distribution of programmed timing of reproduction is discrete.     

Masting in ponderosa pine: comparisons of pollen and seed over space and time

Many plant species exhibit variable and synchronized reproduction, or masting, but less is known of the spatial scale of synchrony, effects of climate, or differences between patterns of pollen and seed production. We monitored pollen and seed cone production for seven Pinus ponderosa populations (607 trees) separated by up to 28?km and 1,350?m in elevation in Boulder County, Colorado, USA for periods of 4?C31?years for a mean per site of 8.7?years for pollen and 12.1 for seed cone production. We also analyzed climate data and a published dataset on 21?years of seed production for an eighth population (Manitou) 100?km away. Individual trees showed high inter-annual variation in reproduction. Synchrony was high within populations, but quickly became asynchronous among populations with a combination of increasing distance and elevational difference. Inter-annual variation in temperature and precipitation had differing influences on seed production for Boulder County and Manitou. We speculate that geographically variable effects of climate on reproduction arise from environmental heterogeneity and population genetic differentiation, which in turn result in localized synchrony. Although individual pines produce pollen and seed, only one-third of the covariation within trees was shared. As compared to seed cones, pollen had lower inter-annual variation at the level of the individual tree and was more synchronous. However, pollen and seed production were similar with respect to inter-annual variation at the population level, spatial scales of synchrony and associations with climate. Our results show that strong masting can occur at a localized scale, and that reproductive patterns can differ between pollen and seed cone production in a hermaphroditic plant.     

Life history evolution of seed-bank annuals in response to seed predation

Summary We present a model of life history evolution for seed-bank annuals in temporally varying environments in which both the seed bank and the distribution of fecundity across year types evolve in response to seed predation. The fecundity distribution refers to the expected reproductive success of germinating seeds across a range of different year types. We assume that it is a function of traits pertaining to growth and survival under different environmental circumstances. Such traits are assumed to result in a trade-off between reproduction in favourable and less favourable years. The model is used to explore how seed predation selects for changes in the seed bank and fecundity distribution and how changes in each of these further select for changes in the other. The direction of selection is contingent upon: whether or not a seed bank exists; whether predation has a greater effect on fresh or buried seed; whether the predation rate differs in different year types, and if so, if it is positively or negatively density-dependent; whether or not predation rate is sensitive to individual variation in seed yield, and if so, whether and how such dependency varies in different kinds of year. Under a variety of predation regimes, seed predators select for a temporal clumping of reproduction; i.e. a specialisation on a favourable subset of year types. This effect usually requires negatively density-dependent seed predation of the sort created by predator satiation. In fact, the classic scenario favouring masting in perennials creates the strongest such effect in our model. Yet unlike the masting of perennial plants, this effect is favoured in a seed-bank annual. It can even occur in a strict annual without a seed bank, and it can occur in a seed-bank annual even if seed predation is density-independent.     

Synchronized expression of FLOWERING LOCUS T between branches underlies mass flowering in Fagus crenata

Masting is the intermittent and synchronized production of a large amount of flower and seed in plant populations. This population-level phenomenon is caused by individual-level variability in reproduction and its synchrony between individuals. The variability at the individual level is induced by synchronized reproduction between branches within an individual because a tree is an assemblage of branches that are considered as semiautonomous units. However, there have been no empirical studies that quantify the degree of reproductive synchrony at the branch level within the same tree in masting species. Here, we evaluated the reproductive synchrony within individuals by monitoring flowering dynamics and expression level of a flowering-time gene at the branch-level in a typical masting species, Fagus crenata Blume. The 4-year census showed that the branch-level gene expression was highly variable between years and was strongly synchronized between branches. The branch-level synchrony in flowering-time gene expression was followed by coherent flowering cycle at the whole individual. To examine the causal relationship between gene expression and climatic factors, we performed a nonlinear statistical analysis called convergent cross-mapping using the time course data of gene expression and environmental variables. Our results indicated that the observed gene expression pattern was well cross-mapped by temperature or precipitation. However, this cross-mapping skill was lower than that of randomly generated seasonal dynamics, implying a combination of internal and external environmental signals is more likely to regulate gene expression dynamics in F. crenata. Our results provide the first empirical evidence that synchronized expression of a flowering-time gene between branches underlies integrated flowering behavior at the individual level.