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.     

Population and individual level of masting in a fleshy-fruited tree

Masting is usually considered as a population phenomenon but it results from individuals?? reproductive patterns. Studies of individual patterns of seed production and their synchrony are essential to an understanding of the mechanisms of masting. The aim of this study was to find the relationship between population and individual levels of masting. We examined individuals?? contribution to masting, considering their endogenous cycles, interannual variability and associated weather cues, as well as inter-individual synchrony of fruit production. We studied masting of Sorbus aucuparia L., which in Europe is one of the most common trees bearing fleshy fruits and is strongly affected by a specialized seed predator. The data are 11-year measurements of fruit production of 250 individuals distributed on a 27-ha area of subalpine forest in the Western Carpathians (Poland). Population- and individual-level interannual variability of fruit production was moderate. Synchrony among individuals was relatively high for all years, but the trees were much less synchronized in heavy crop years than in years of low fruit production. Weak synchrony among trees for heavy production years suggests that the predator satiation hypothesis does not explain the observed masting behavior. Fruit production, both at individual and at population level, was highly correlated with weather conditions. However, the presence of masting cannot be fully explained by the resource-matching hypothesis either. We suggest that adverse weather conditions effectively limit fruit production, causing high inter-individual synchrony in low crop years, whereas the unsynchronized heavy crop years seem to have been affected by individually available resources.     

Reproductive success of individuals with different fruit production patterns. What does it mean for the predator satiation hypothesis?

The predator satiation hypothesis states that synchronous periodic production of seeds is an adaptive strategy evolved to reduce the pressure of seed predators. The seed production pattern is crucial to the predator satiation hypothesis, but there are few studies documenting the success of individuals that are in synchrony and out of synchrony with the whole population. This study is based on long-term data on seed production of Sorbus aucuparia and specialised pre-dispersal seed predation by Argyresthia conjugella, in a subalpine spruce forest in the Western Carpathians (Poland). At the population level, we tested whether functional and numerical responses of predators to the variation of fruit production operate. At the individual level, we tested whether individuals with higher interannual variability in their own seed crops and higher synchrony with the population have higher percentages of uninfested fruits. The intensity of pre-dispersal seed predation was high (average 70 %; range 19–100 %). There were both functional and numerical responses of predators to the variation of fruit production at the population level. We found that individuals that were expected to be preferred under seed predator pressure had higher reproductive success. With increasing synchrony of fruit production between individual trees and the population, the percentage of infested fruits decreased. There was also a negative relationship between the interannual variation in individual fruit production and the percentage of infested fruits. These results confirm selection for individuals with a masting strategy. However, the population does not seem well adapted to strong seed predation pressure and we suggest that this may be a result of prolonged diapause of A. conjugella.     

Mechanisms driving interspecific variation in regional synchrony of trees reproduction

Seed production in many plants is characterized by large interannual variation, which is synchronized at subcontinental scales in some species but local in others. The reproductive synchrony affects animal migrations, trophic responses to resource pulses and the planning of management and conservation. Spatial synchrony of reproduction is typically attributed to the Moran effect, but this alone is unable to explain interspecific differences in synchrony. We show that interspecific differences in the conservation of seed production-weather relationships combine with the Moran effect to explain variation in reproductive synchrony. Conservative timing of weather cues that trigger masting allows populations to be synchronized at distances >1000 km. Conversely, if populations respond to variable weather signals, synchrony cannot be achieved. Our study shows that species vary in the extent to which their weather cueing is spatiotemporally conserved, with important consequences, including an interspecific variation of masting vulnerability to climate change.     

Patterns and mechanisms of masting in the large‐seeded southern hemisphere conifer Araucaria araucana

Abstract Masting, the intermittent and synchronous production of large seed crops, may result from either of two major processes: resource matching and economy of scale. Components of cone production in Araucaria araucana were partitioned among populations and trees to ascertain the existence of masting and the processes involved. Cone production data from seven populations were obtained during a 9‐year period and seed gathering data were available for an 18‐year time series from six sites in an area of more than 7600 km². Araucaria araucana showed environmentally triggered, intermittent, moderately fluctuating, and highly regionally synchronous reproduction. The mean pairwise correlations of cones production among populations and seed gathering sites were 0.89 and 0.74, respectively, suggesting synchrony in reproduction. Among trees we observed a mean correlation of 0.74 with values ranging from 0.66 to 0.81 for the analysed populations. The existence of negative autocorrelation in seed production between year 0 and year ?2 at the individual tree level suggests the presence of ‘switching’ or internal resource allocation, thus discarding the Resource Matching hypothesis. Mean coefficient of variation (CV_p) among populations was moderate (0.95) and similar to the modal CV_p values reported in the published reports. Mean CV_i among individual trees was 1.16, suggesting a large number of equally and synchronously fluctuating trees, rather than a few largely fluctuating individuals. These results suggest that pollination efficiency and/or predator satiation hypotheses could be responsible for the masting cycles in this conifer. Ancillary data about limitation of airborne pollen dispersion and temporal variation in the amount of seeds per cone and about seed predator satiation, also support both proposed mechanisms.     

Within-season synchrony of a masting conifer enhances seed escape

Predator satiation resulting from interannual reproductive synchrony has been widely documented in masting plants, but how reproductive synchrony within a year influences seed escape is poorly understood. We evaluated whether the intra-annual reproductive synchrony of individual white spruce trees (Picea glauca) increased seed escape from their primary predispersal seed predator, North American red squirrels (Tamiasciurus hudsonicus). Trees with cones that matured synchronously relative to those of other trees within red squirrel territories were significantly more likely to escape squirrel predation in years with both low and superabundant levels of cone production, generating a significantly positive linear selection differential for increasing intra-annual reproductive synchrony. Thus, this masting plant escapes seed predation in numbers through interannual synchrony in seed production and in time through intra-annual synchrony of seed availability.     

Reproductive collapse in European beech results from declining pollination efficiency in large trees

Climate warming increases tree mortality which will require sufficient reproduction to ensure population viability. However, the response of tree reproduction to climate change remains poorly understood. Warming can reduce synchrony and interannual variability of seed production (“masting breakdown”) which can increase seed predation and decrease pollination efficiency in trees. Here, using 40 years of observations of individual seed production in European beech (Fagus sylvatica), we showed that masting breakdown results in declining viable seed production over time, in contrast to the positive trend apparent in raw seed count data. Furthermore, tree size modulates the consequences of masting breakdown on viable seed production. While seed predation increased over time mainly in small trees, pollination efficiency disproportionately decreased in larger individuals. Consequently, fecundity declined over time across all size classes, but the overall effect was greatest in large trees. Our study showed that a fundamental biological relationship—correlation between tree size and viable seed production—has been reversed as the climate has warmed. That reversal has diverse consequences for forest dynamics; including for stand- and biogeographical-level dynamics of forest regeneration. The tree size effects suggest management options to increase forest resilience under changing climates.     

Latitudinal variation in seed weight and flower number in Prunella vulgaris

Studies of seed-weight variation across altitudinal and latitudinal gradients have led to conflicting hypotheses regarding the selective value of this traint in relation to the length of the growing season. Growing-season length may also influence the evolution of seed number, and population differentiation in seed weight may be constrained by a negative genetic correlation between seed weight and seed number within populations. We examined variation in seed weight and an estimate of seed number (flower number) and the covariance of these traits among populations of Prunella vulgaris at five latitudes between northern Michigan and South Carolina. We measured seed weight and flower number in native habitats and in a common environment to determine the extent to which patterns observed in the field reflect genetic differentiation. We observed no genetically based variation in seed weight across the latitudinal gradient, although genetic variation among populations within a latitude was observed. In contrast to the lack of variation in seed weight, flower number increased clinally from northern Michigan to Tennessee in a common environment. Population mean flowering date in a common environment was successively later from north to south. Later-flowering individuals appear to achieve a larger size before flowering and consequently possess more resources for seed production. This difference may account for the greater flower production of late-flowering, southern populations. Independence of population mean seed weight and flower number across the latitudinal gradient suggests that population differentiation in seed weight has not been constrained by a trade-off between seed size and number within populations.     

Predator satiation and extreme mast seeding in 11 species of Chionochloa (Poaceae)

Variation in annual flowering effort is described for 16 long datasets from 11 species of Chionochloa (Poaceae) in New Zealand. All populations exhibited extreme mast seeding. The most variable species was C. crassiuscula (coefficient of variation, CV=3.02) over 26 years at Takahe Valley, Fiordland, which is the highest published CV we know of worldwide. The other populations also had high CVs (lowest CV=1.42, mean CV=1.84) which were higher than for other well‐studied genera such as Picea, Pinus and Quercus. There were also frequent years of zero flowering (mean across all populations was 37.2% zero years; maximum 53% for C. rubra and C. crassiuscula over 19 years) whereas zero years are rare in other published masting datasets.Flowering was highly synchronous among species within a site (mean r=0.886), and also (though significantly less so) among sites. Among sites, synchrony was not significantly higher within‐species (mean r=0.711) than between‐species (r=0.690). Warm summer temperatures led to heavy flowering the following summer. Flowering synchrony increased with increasing synchrony in local deseasonalised summer temperatures, and decreased with increasing distance between sites.Mast seeding has been shown in Chionochloa to reduce losses to specialist flower or seed predators. Among‐species synchrony may be adaptive if species share a common seed predator. Developing seeds of at least 10 Chionochloa species are attacked by larvae of an undescribed cecidomyiid. In Takahe Valley, where masting is most pronounced, cecidomyiids attacked all six Chionochloa species in all four years studied. Mean annual losses were almost constant (10.0 to 13.4%) while flowering effort varied 100‐fold. The invariant losses are consistent with other evidence that the cecidomyiid may have extended diapause, which would make it harder to satiate by mast seeding. We hypothesise that one possible factor favouring such extremely high levels of mast seeding in Chionochloa is that its seed predator is very hard to satiate.     

Masting and trophic cascades: interplay between rowan trees, apple fruit moth, and their parasitoid in southern Norway

We analyzed berry production in rowan, Sorbus aucuparia L., in southern Norway and examined the ramifying effects of rowan masting on the dynamics of the dominant seed predator and its parasitoid. The apple fruit moth, Argyresthia conjugella Zeller, is a pre-dispersal seed predator of rowan. The larva of the apple fruit moth rely on rowan berries, which in turn is attacked by the parasitoid wasp, Microgaster politus Marsh. We found classic masting in rowan: berry production varied across years (the mean coefficient of variation=1.02) and was spatially synchronized at large scale (the averaged correlation coefficient=0.67). Berry production represented a two-year cycle in western but a three-year cycle in eastern Norway. The abundance of the moth and the parasitoid also varied across years and were spatially synchronized. The degree of spatial synchrony decreased and cyclicity became obscure with increasing trophic level. We attempted to assess two different components to the predator satiation, functional and numerical satiations, based on a simple population dynamics model. The observed pattern of seed predation testified that both of functional and numerical satiations were at work in this system. In a comparison at different locations, rowan trees with more variable berry production were more effective in reducing losses to the seed predator. The parasitoids also seemed to experience satiation through the fluctuation in their host abundance. These results show that rowan masting has an adaptive foundation, which impacts the dynamics of higher trophic levels.     

Geographical variation in the spatial synchrony of a forest-defoliating insect: isolation of environmental and spatial drivers

Despite the pervasiveness of spatial synchrony of population fluctuations in virtually every taxon, it remains difficult to disentangle its underlying mechanisms, such as environmental perturbations and dispersal. We used multiple regression of distance matrices (MRMs) to statistically partition the importance of several factors potentially synchronizing the dynamics of the gypsy moth, an invasive species in North America, exhibiting outbreaks that are partially synchronized over long distances (approx. 900 km). The factors considered in the MRM were synchrony in weather conditions, spatial proximity and forest-type similarity. We found that the most likely driver of outbreak synchrony is synchronous precipitation. Proximity played no apparent role in influencing outbreak synchrony after accounting for precipitation, suggesting dispersal does not drive outbreak synchrony. Because a previous modelling study indicated weather might indirectly synchronize outbreaks through synchronization of oak masting and generalist predators that feed upon acorns, we also examined the influence of weather and proximity on synchrony of acorn production. As we found for outbreak synchrony, synchrony in oak masting increased with synchrony in precipitation, though it also increased with proximity. We conclude that precipitation could synchronize gypsy moth populations directly, as in a Moran effect, or indirectly, through effects on oak masting, generalist predators or diseases.     

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.     

Tree-to-tree variation in seed size and its consequences for seed dispersal versus predation by rodents

Individual variation in seed size and seed production is high in many plant species. How does this variation affect seed-dispersing animals and, in turn, the fitness of individual plants? In this study, we first surveyed intraspecific variation in seed mass and production in a population of a Chinese white pine, Pinus armandii. For 134 target trees investigated in 2012, there was very high variation in seed size, with mean seed mass varying among trees almost tenfold, from 0.038 to 0.361 g. Furthermore, 30 of the 134 trees produced seeds 2 years later, and for these individuals there was a correlation in seed mass of 0.59 between years, implying consistent differences among individuals. For a subset of 67 trees, we monitored the foraging preferences of scatter-hoarding rodents on a total of 15,301 seeds: 8380 were ignored, 3184 were eaten in situ, 2651 were eaten after being cached, and 395 were successfully dispersed (cached and left intact). At the scale of individual seeds, seed mass affected almost every decision that rodents made to eat, remove, and cache individual seeds. At the level of individual trees, larger seeds had increased probabilities of both predation and successful dispersal: the effects of mean seed size on costs (predation) and benefits (caching) balanced out. Thus, despite seed size affecting rodent decisions, variation among trees in dispersal success associated with mean seed size was small once seeds were harvested. This might explain, at least in part, the maintenance of high variation in mean seed mass among tree individuals.     

Environmental correlates of acorn production by four species of Minnesota oaks

We measured acorn production by four species of oaks in central Minnesota over a 17-year period with the goal of understanding the proximate drivers of masting behavior. All four species exhibited significant annual variation and within-population synchrony of acorn production, although masting behavior was more pronounced in the two species that require 1 year to develop acorns (‘1-year’ species) than the two species that require 2 years (‘2-year’ species). There was also strong synchrony between species that require the same number of years to mature acorns, but not between species requiring different numbers of years. Acorn production by three of the four species correlated with spring or summer conditions, while no significant environmental correlate of acorn production was detected for the fourth species. Acorn production by none of the four species correlated significantly with variables calculated from the differences in weather conditions from 1 year to the next. These results, combined with prior studies of oaks, suggest that environmental conditions during key periods of acorn development frequently correlate with acorn production, as expected if such factors bear a direct mechanistic relationship to seed production. On the other hand, the environmental factors involve vary greatly both among species and even among populations of the same species, a result consistent with the hypothesis that environmental correlates are simply cues used by plants to synchronize reproductive investment. In either case, our results do not support the recent proposition that variables based on differences in environmental conditions from 1 year to the next serve as a general cue for masting behavior.     

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.     

Individual size variation reduces spatial variation in abundance of tree community assemblage,not of tree populations

Research on individual trait variation has gained much attention because of its implication for ecosystem functions and community ecology. The effect of individual variation on population and community abundance (number of individuals) variation remains scarcely tested. Using two established ecological scaling laws (Taylor's law and abundance–size relationship), we derived a new scaling relationship between the individual size variation and spatial variation of abundance. Tested against multi‐plot tree data from Diaoluo Mountain tropical forest in Hainan, China, the new scaling relationship showed that individual size variation reduced the spatial variation of community assemblage abundance, but not of taxon‐specific population abundance. The different responses of community and population to individual variation were reflected by the validity of the abundance–size relationship. We tested and confirmed this scaling framework using two measures of individual tree size: aboveground biomass and diameter at breast height. Using delta method and height‐diameter allometry, we derived the analytic relation of scaling exponents estimated under different individual size measures. In addition, we used multiple regression models to analyze the effect of taxon richness on the relationship between individual size variation and spatial variation of population or community abundance, for taxon‐specific and taxon‐mixed data, respectively. This work offers empirical evidence and a scaling framework for the negative effect of individual trait variation on spatial variation of plant community. It has implications for forest ecosystem and management where the role of individual variation in regulating population or community spatial variation is important but understudied.     

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.     

Phenological variation in fruit characteristics in vertebrate-dispersed plants

Summary We investigated inter-specific variation in fruit characteristics — fruit size, seed number per fruit, seed weight, nutritional content, fruit persistence, and fruit synchronization — in relation to flowering and fruiting phenology in 34 species of fleshy fruited plants. Except for aspects of fruit synchrony and persistence, the results in general were inconsistent with previous suggestions about adaptive variation in phenologically related fruit traits. The main results were as follows: (1) Late flowering, late fruiting, lengthy development time from flower to fruit, and highly persistent fruits constitute a complex of correlated characteristics among the species. (2) Synchronization of fruiting within individuals increased from early ripening fruits to late ripening fruits. Fruiting synchrony was more pronounced in species with a small crop size than in species with a large fruit crop, whereas synchrony was not significantly related to flowering synchronization, nor to life form. (3) Nitrogen and carbohydrate content of fruit pulp did not vary in relation to phenology, whereas lipid content decreased from early to late ripening fruits. (4) No seasonal trends were found for variation in seed size or seed number per fruit. (5) Interactions with flowering phenology and developmental constraints are important in phenological fruiting patterns. Temporal variation in start of fruiting was partly (36%) explained by variation in flowering time. Seed weight variation explained 17% of variation in development time from flower to fruit. (6) Despite constraints from flowering and seed development, some adaptive adjustment in fruiting phenology is likely to be allowed for among the investigated species. Such an adaptive variation in fruiting phenology was suggested by intra-generic comparisons of Prunus and Vaccinium species.     

Aridity drives spatiotemporal patterns of masting across the latitudinal range of a dryland conifer

Masting, or the synchronous and irregular production of seed crops, is controlled by environmental conditions and resource budgets. Increasing temperatures and shifting precipitation regimes may alter the frequency and magnitude of masting, especially in species that experience chronic resource stress. Yet the effects of a changing climate on seed production are unlikely to be uniform across populations, particularly those that span broad abiotic gradients. In this study, we assessed the spatiotemporal patterns of masting across the latitudinal distribution of a widely distributed dryland conifer species, piñon pine Pinus edulis. We quantified seed cone production from 2004 to 2017 using cone abscission scars in 187 trees from 28 sites along an 1100 km latitudinal gradient to investigate the spatiotemporal drivers of seed cone production and synchrony across populations. Populations from chronically hot and dry areas (greater climatic water deficits and less monsoonal precipitation) tended to have greater interannual variability in seed cone production and smaller crop sizes. Mast years generally followed years with low vapor pressure deficits and high precipitation during key periods of the reproductive process, but the strength of these relationships varied across the region. Populations that received greater monsoonal precipitation were less sensitive to late summer vapor pressure deficits during seed cone initiation yet more sensitive to spring vapor pressure deficits during pollination. Spatially correlated patterns of vapor pressure deficit better predicted synchrony in seed cone production than geographic distance, and these patterns were conserved at distances up to 500 km. These results demonstrate that aridity drives spatiotemporal variability in seed cone production. As a result, projected increases in aridity are likely to decrease the frequency and magnitude of masting in these dry forests and woodlands. Declines in seed production may compound climatic limitations to recruitment and impede tree regeneration, with cascading effects for numerous wildlife species.