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.     

Nitrogen as a key regulator of flowering in Fagus crenata: understanding the physiological mechanism of masting by gene expression analysis

The role of resource availability in determining the incidence of masting has been widely studied, but how floral transition and initiation are regulated by the resource level is unclear. We tested the hypothesis that floral transition is stimulated by high resource availabiltiy in Fagus crenata based on a new technique, the expression analyses of flowering genes. We isolated F. crenata orthologues of FLOWERING LOCUS T, LEAFY and APETALA1, and confirmed their functions using transgenic Arabidopsis thaliana. We monitored the gene expression levels for 5 years and detected a cycle of on and off years, which was correlated with fluctuations of the shoot‐nitrogen concentration. Nitrogen fertilisation resulted in the significantly higher expression of flowering genes than the control, where all of the fertilised trees flowered, whereas the control did not. Our findings identified nitrogen as a key regulator of mast flowering, thereby providing new empirical evidence to support the resource budget model.     

Masting uncoupling: mast seeding does not follow all mast flowering episodes in a dioecious juniper tree

Evolutionary selective forces, like predator satiation and pollination efficiency, are acknowledged to be major causes of masting (the variable, periodic and synchronic production of seeds in a population). However, a number of recent studies indicate that resources might also play an important role on shaping masting patterns. Dioecious masting species offer a privileged framework to study the role of resources on masting variation, since male and female plants often experience different reproductive costs and selective pressures. We followed masting and reproductive investment (RI) of the dioecious tree Juniperus thurifera in two populations along 10 years and studied the different response of males and females to experimentally increased water and nutrient availability in a third population. Juniperus thurifera females invested in reproduction three times more resources than males. Such disparity generated different resource‐use strategies in male and female trees. Tree‐ring growth and water use efficiency (WUE) confirmed that sexes differed in their resource investment temporal pattern, with males using current resources for reproduction and females using resources accumulated during longer periods. Watered and fertilized female trees presented significantly higher flowering reproductive investments than males and experienced an extraordinary mast‐flowering event. However, seeding RI and mast seeding were not affected by the treatment. This suggests that although resource availability affects the reproductive output of this species, there are other major forces regulating masting on J. thurifera. During 10 years, J. thurifera male and female trees presented high and low flowering years more or less synchronously. However, not all mast flowering episodes resulted in mast seeding, leading to masting uncoupling between flowering and seeding. Since flowering costs represent only 1% of females’ total reproductive investments, masting uncoupling could be a beneficial bet‐hedging strategy to maximize reproductive output in spite of unpredictable catastrophic events.     

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.     

Modeling the impact of reproductive mode on masting

Masting is defined as the intermittent highly variable production of seed in a plant population. According to reproductive modes, that is, sexual and asexual reproduction, masting species can be separated into three groups, that is, (1) species, for example, bamboo, flower only once before they die; (2) species, for example, Fagus, reproduce sexually; and (3) species, for example, Stipa tenacissima, reproduce both sexually and asexually. Several theories have been proposed to explore the underlying mechanisms of masting. However, to our knowledge, no theory has been found to explain the mechanism of masting species that reproduce both sexually and asexually. Here we refine the Resource Budget Model by considering a trade‐off between sexual and asexual reproduction. Besides the depletion efficient (i.e., the ratio of the cost of seed setting and the cost of flowering), other factors, such as the annual remaining resource (i.e., the rest of the resource from the photosynthetic activity after allocating to growth and maintenance), the trade‐off between sexual and asexual reproduction, and the reproductive thresholds, also affect masting. Moreover, two potential reproductive strategies are found to explain the mechanisms: (1) When the annual remaining resource is relatively low, plants reproduce asexually and a part of the resource is accumulated as the cost of asexual reproduction is less than the annual remaining resource. Plants flower and set fruits once the accumulated resource exceeds the threshold of sexual reproduction; (2) when the annual remaining resource is relatively high, and the accumulated resource surpasses the threshold of sexual reproduction, masting occurs. Remarkably, under certain depletion efficient, more investigation in sexual reproduction will lead plants to reproduce periodically. Additionally, plants investigate less resource to reproduce periodically when depletion efficient keeps increasing as plants can reproduce efficiently. Overall, our study provides new insights into the interpretation of masting, especially for species that reproduce both sexually and asexually.     

The role of large environmental noise in masting: General model and example from pistachio trees

Masting is synchronous, highly variable reproduction in a plant population, or synchronized boom-bust cycles of reproduction. These pulses of resources have cascading effects through ecosystems, and thus it is important to understand where they come from. How does masting happen and synchronize? In this paper, we suggest a mechanism for this. The mechanism is inspired by data from a pistachio orchard, which suggest that large environmental noise may play a crucial role in inducing masting in plant populations such as pistachio. We test this idea through development and analysis of a mathematical model of plant reproduction. We start with a very simple model, and generalize it based on the current models of plant reproduction and masting. Our results suggest that large environmental noise may indeed be a crucial part of the mechanism of masting in certain types of plant populations, including pistachio. This is a specific example of an important functional consequence of the interactions between stochasticity and nonlinearity.     

Snow tussocks, chaos, and the evolution of mast seeding

One hitherto intractable problem in studying mast seeding (synchronous intermittent heavy flowering by a population of perennial plants) is determining the relative roles of weather, plant reserves, and evolutionary selective pressures such as predator satiation. We parameterize a mechanistic resource-based model for mast seeding in Chionochloa pallens (Poaceae) using a long-term individually structured data set. Each plant's energy reserves were reconstructed using annual inputs (growing degree days), outputs (flowering), and a novel regression technique. This allowed the estimation of the parameters that control internal plant resource dynamics, and thereby allowed different models for masting to be tested against each other. Models based only on plant size, season degree days, and/or climatic cues (warm January temperatures) fail to reproduce the pattern of autocovariation in individual flowering and the high levels of flowering synchrony seen in the field. This shows that resource-matching or simple cue-based models cannot account for this example of mast seeding. In contrast, the resource-based model pulsed by a simple climate cue accurately describes both individual-level and population-level aspects of the data. The fitted resource-based model, in the absence of environmental forcing, has chaotic (but often statistically periodic) dynamics. Environmental forcing synchronizes individual reproduction, and the models predict highly variable seed production in close agreement with the data. An evolutionary model shows that the chaotic internal resource dynamics, as predicted by the fitted model, is selectively advantageous provided that adult mortality is low and seeds survive for more than 1 yr, both of which are true for C. pallens. Highly variable masting and chaotic dynamics appear to be advantageous in this case because they reduce seed losses to specialist seed predators, while balancing the costs of missed reproductive events.     

Modelling the Masting Behaviour of Betula platyphylla var. japonica using the Resource Budget Model

A masting model of Betula platyphylla var. japonica, a majorwind-pollinated tree in Hokkaido, northern Japan, was constructedfrom the perspective of the resource budget model. An 11-yeardata series of pollen dispersal by birch showed marked annualfluctuations in flowering. Although flowering fluctuated widelyamong years, a reciprocal relationship was observed betweentwo consecutive years; very little flowering occurred aftera mast year. This suggests that there is a negative relationshipbetween current fruiting and flower bud induction. There wasa significant positive relationship in flowering between regions,which suggests that weather conditions regulate flowering inbirch. A model that included weather variables and resourceallocation systems among years explained 94·5% of theobserved annual fluctuations in flowering. In the model, warmspring conditions from bud burst to flower bud development andlittle flowering in the previous year (t-1) resulted in increasedflowering in the current year (t), whereas abundant floweringin year t-2 resulted in a decrease in flowering in the currentyear (t). The latter indicates that flowering in year t-2 affectsresource storage after overwintering; the balance is carriedforward to year t-1 and affects the initiation of flower primordiabefore bud burst. In the model, fluctuating weather conditionsin the previous spring strongly affected the masting behaviourof birch. Copyright 2001 Annals of Botany Company Betula platyphylla var. japonica, flowering, masting, modelling, pollen dispersal, resource allocation, resource budget model, weather conditions     

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.     

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.     

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.     

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.     

Costs of reproduction in Nyssa sylvatica: sexual dimorphism in reproductive frequency and nutrient flux

Summary We examined the influence of differential reproductive frequency between the sexes on tertiary (phenotypic) sex ratios in the the dioecious tree Nyssa sylvatica (Nyssaceae). Reproduction was evaluated in relation to sex, size and canopy exposure using flowering data collected from 1229 marked trees over a four year period. For subsets of each population we used data on flower number, fruit crop size, fruit/flower ratios, and individual flower and fruit mass to compare biomass invested in reproductive structures of males and females. We also examined seasonal changes in stem nitrogen and soluble carbohydrate content in relation to flower and fruit production for trees of each sex. Our results indicate that: 1) Male-biased tertiary sex ratios could be explained by more frequent reproduction by male trees; 2) Estimated secondary sex ratios based on sums of all known males and females were not significantly different from 1:1; 3) Flowering frequency of males and females was significantly related to plant size (DBH) and exposure of the canopy to light; 4) Estimtes of reproductive biomass allocation ranged from 1.36 to 10.8 times greater for females relative to males; 5) Flower production was related to stem nutrient status for both sexes, but nutrient depletion and its effect on subsequent flowering was much more pronounced for female trees. We conclude that less frequent flowering by female trees may result from depletion of stored reserves, and that differential flowering frequency in N. sylvatica may ultimately reduce apparent sexual differences in the costs of reproduction.     

Of mast and mean: differential‐temperature cue makes mast seeding insensitive to climate change

Mast‐seeding plants often produce high seed crops the year after a warm spring or summer, but the warm‐temperature model has inconsistent predictive ability. Here, we show for 26 long‐term data sets from five plant families that the temperature difference between the two previous summers (ΔT) better predicts seed crops. This discovery explains how masting species tailor their flowering patterns to sites across altitudinal temperature gradients; predicts that masting will be unaffected by increasing mean temperatures under climate change; improves prediction of impacts on seed consumers; demonstrates that strongly masting species are hypersensitive to climate; explains the rarity of consecutive high‐seed years without invoking resource constraints; and generates hypotheses about physiological mechanisms in plants and insect seed predators. For plants, ΔT has many attributes of an ideal cue. This temperature‐difference model clarifies our understanding of mast seeding under environmental change, and could also be applied to other cues, such as rainfall.     

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.

     

Masting by Betula-species; applying the resource budget model to north European data sets

Masting, the intermittent production of large crops of flowers by a plant population, is a common feature among trees in boreal and temperate forests. The pollen of many broadleaved trees causes allergic diseases, which are major causes of increasing health-care costs in industrialised countries. As the prevalence and severity of allergic diseases are connected with the concentrations of airborne pollen, an universal model predicting the intensity of the coming flowering would be a valuable tool for pollen information services, and ultimately for allergic people and allergologists. We investigated whether a resource budget model created in Japan explains the fluctuations in the annual pollen sums of Betula-species in north European data sets (10–12 years at 4 sites, 20 years at 10 sites). Using the shorter data sets, the model explained 76–92% of the annual fluctuations at five study sites. Using the 20-year data set, the percentage for southern Finland was much lower, only 48%, compared with the 85% of the 12-year data set. The annual pollen sums have been higher during the 1990s than in the 1980s, which may explain the ineffectiveness of the model, while applied to the 20-year data set. Our results support the resource budget model: the masting of birch species is regulated by weather factors together with the system of resource allocation among years. The model can serve pollen information service. However, only the 10 most recent years should be used to avoid interference from trends in changing vegetation and/or climate.     

Two-year cycles of synchronous acorn and leaf production in biennial-fruiting evergreen oaks of subgenus Cyclobalanopsis (Quercus, Fagaceae)

Many masting species switch resources between vegetative growth and reproduction in mast and non-mast years. Although masting of oak species is well known, there have been few investigations of the relationship between vegetative growth and reproduction based on long-term monitoring data, especially in evergreen oaks of subgenus Cyclobalanopsis. We investigated annual variations over 13?years in acorn and leaf production of three evergreen oak species in subgenus Cyclobalanopsis, genus Quercus (Fagaceae)??Q. acuta, Q. salicina and Q. sessilifolia??in western Japan. In these species, the maturation of acorns occurs in the second autumn after flowering, which is known as a biennial-fruiting habit. We found a pattern of acorn production and masting in alternate years that was synchronized in all three species. Masting was not correlated with temperature and precipitation. Annual leaf-fall also showed 2-year cycle in the three oak species; peak years were synchronized between species and peak leaf-fall alternated with acorn production in all three species. Furthermore, there was a significant negative correlation between acorn and leaf production in all three species. Data showing 2-year cycles of acorn and leaf production and the negative correlation between them supports the hypothesis of resource switching between vegetative growth and reproduction. The 2-year cycle might be the basic, intrinsic rhythm of resource allocation in biennial-fruiting Cyclobalanopsis species.     

Masting in whitebark pine (Pinus albicaulis) depletes stored nutrients

? In masting trees, synchronized, heavy reproductive events are thought to deplete stored resources and to impose a replenishment period before subsequent masting. However, direct evidence of resource depletion in wild, masting trees is very rare. Here, we examined the timing and magnitude (local vs individual-level) of stored nutrient depletion after a heavy mast event in Pinus albicaulis. ? In 2005, the mast year, we compared seasonal changes in leaf and sapwood nitrogen (N) and phosphorus (P) concentrations and leaf photosynthetic rates in cone-bearing branches, branches that never produced cones, and branches with experimentally removed cones. We also compared nutrient concentrations in cone branches and branches that had never had cones between 2005 and 2006, and measured tree ring width and new shoot growth during 2005. ? During the mast year, N or P depletion occurred only in tissue fractions of reproductive branches, where photosynthetic rates were reduced. However, by the end of the following year, nutrients were depleted in all branches, indicating individual-level resource depletion. New shoot and radial growth were not affected by masting. ? We provide direct evidence that mast events in wild trees deplete stored nutrients. Our results highlight the importance of evaluating reproductive costs over time and at the individual level.     

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.     

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.