Relatives reproduce in synchrony: kinship and individual condition shape intraspecific variation in masting phenotype.

Masting (synchronous and interannually variable seed production) is frequently called a reproductive strategy; yet it is unclear whether the reproductive behaviour of individuals has a heritable component. To address this, we used 22 years of annual fruit production data from 110 Sorbus aucuparia L. trees to examine the contributions of genetic factors to the reproductive phenotype of individuals, while controlling for environmental variation. Trees sharing close genetic relationships and experiencing similar habitat conditions exhibited similar levels of reproductive synchrony. Trees of comparable sizes displayed similar levels of year-to-year variation in fruiting, with relatedness contributing to this variation. External factors, such as shading, influenced the time intervals between years with abundant fruit production. The effects of genetic relatedness on the synchrony of reproduction among trees and on interannual variation provide long-awaited evidence that the masting phenotype is heritable, and can respond to natural selection.

How to measure mast seeding?

The periodic production of large seed crops, or masting, is a widespread phenomenon in perennial plants. This behavior can enhance the reproductive efficiency of plants, leading to increased fitness, and produce ripple effects on food webs. While variability from year to year is a defining characteristic of masting, the methods used to quantify this variability are highly debated. The commonly used coefficient of variation lacks the ability to account for the serial dependence in mast data and can be influenced by zeros, making it a less suitable choice for various applications based on individual-level observations, such as phenotypic selection, heritability, and climate change studies, which rely on individual-plant-level datasets that often contain numerous zeros. To address these limitations, we present three case studies and introduce volatility and periodicity, which account for the variance in the frequency domain by emphasizing the significance of long intervals in masting. By utilizing examples of Sorbus aucuparia, Pinus pinea, Quercus robur, Quercus pubescens, and Fagus sylvatica, we demonstrate how volatility captures the effects of variance at both high and low frequencies, even in the presence of zeros, leading to improved ecological interpretations of the results. The growing availability of long-term, individual-plant datasets promises significant advancements in the field, but requires appropriate tools for analysis, which the new metrics provide.

Costs and benefits of masting: economies of scale are not reduced by negative density-dependence in seedling survival in Sorbus aucuparia.

Masting is a widespread reproductive strategy in plants that helps to reduce seed predation and increase pollination. However, masting can involve costs, notably negative density-dependent (NDD) seedling survival caused by concentrating reproduction in intermittent events. Masting benefits have received widespread attention, but the costs are understudied, which precludes understanding why some plant species have evolved intense masting, while others reproduce regularly. We followed seed production, seed predation (both 13 yr), and seedling recruitment and survival (11 yr) in Sorbus aucuparia. We tested whether NDD in seedling survival after mast years can reduce the benefits of pulsed reproduction that come through predator satiation. Seed predation rates were extreme in our population (mean = 75%), but were reduced by masting. The commonly accepted, but untested, assertion that pulsed recruitment is associated with strong NDD was unsupported. Consequently, the proportion of seedlings that survived their first year increased with fruit production. This provides a rare test of economies of scale beyond the seed stage. Our results provide estimation of the costs of mast seeding, and indicate that these may be lower than expected. Low masting costs, if common, may help explain why masting is such a widespread reproductive strategy throughout the plant kingdom.

Seed predation selects for reproductive variability and synchrony in perennial plants.

Annually variable and synchronous seed production by plant populations, or masting, is a widespread reproductive strategy in long-lived plants. Masting is thought to be selectively beneficial because interannual variability and synchrony increase the fitness of plants through economies of scale that decrease the cost of reproduction per surviving offspring. Predator satiation is believed to be a key economy of scale, but whether it can drive phenotypic evolution for masting in plants has been rarely explored. We used data from seven plant species (Quercus humilis, Quercus ilex, Quercus rubra, Quercus alba, Quercus montana, Sorbus aucuparia and Pinus pinea) to determine whether predispersal seed predation selects for plant phenotypes that mast. Predation selected for interannual variability in Mediterranean oaks (Q. humilis and Q. ilex), for synchrony in Q. rubra, and for both interannual variability and reproductive synchrony in S. aucuparia and P. pinea. Predation never selected for negative temporal autocorrelation of seed production. Predation by invertebrates appears to select for only some aspects of masting, most importantly high coefficient of variation, supporting individual-level benefits of the population-level phenomenon of mast seeding. Determining the selective benefits of masting is complex because of interactions with other seed predators, which may impose contradictory selective pressures.

Does masting scale with plant size? High reproductive variability and low synchrony in small and unproductive individuals.

BACKGROUND AND AIMS: In a range of plant species, the distribution of individual mean fecundity is skewed and dominated by a few highly fecund individuals. Larger plants produce greater seed crops, but the exact nature of the relationship between size and reproductive patterns is poorly understood. This is especially clear in plants that reproduce by exhibiting synchronized quasi-periodic variation in fruit production, a process called masting. METHODS: We investigated covariation of plant size and fecundity with individual-plant-level masting patterns and seed predation in 12 mast-seeding species: Pinus pinea, Astragalus scaphoides, Sorbus aucuparia, Quercus ilex, Q. humilis, Q. rubra, Q. alba, Q. montana, Chionochloa pallens, C. macra, Celmisia lyallii and Phormium tenax. KEY RESULTS: Fecundity was non-linearly related to masting patterns. Small and unproductive plants frequently failed to produce any seeds, which elevated their annual variation and decreased synchrony. Above a low fecundity threshold, plants had similar variability and synchrony, regardless of their size and productivity. CONCLUSIONS: Our study shows that within-species variation in masting patterns is correlated with variation in fecundity, which in turn is related to plant size. Low synchrony of low-fertility plants shows that the failure years were idiosyncratic to each small plant, which in turn implies that the small plants fail to reproduce because of plant-specific factors (e.g. internal resource limits). Thus, the behaviour of these sub-producers is apparently the result of trade-offs in resource allocation and environmental limits with which the small plants cannot cope. Plant size and especially fecundity and propensity for mast failure years play a major role in determining the variability and synchrony of reproduction in plants.

Environmental Veto Synchronizes Mast Seeding in Four Contrasting Tree Species.

Synchronized and variable reproduction by perennial plants, called mast seeding, is a major reproductive strategy of trees. The need to accumulate sufficient resources after depletion following fruiting (resource budget), the efficiency of mass flowering for outcross pollination (pollen coupling), or the external factors preventing reproduction (environmental veto) could all synchronize masting. We used seed production data for four species (Quercus ilex, Quercus humilis, Sorbus aucuparia, and Pinus albicaulis) to parametrize resource budget models of masting. Based on species life-history characteristics, we hypothesized that pollen coupling should synchronize reproduction in S. aucuparia and P. albicaulis, while in Q. ilex and Q. humilis, environmental veto should be a major factor. Pollen coupling was stronger in S. aucuparia and P. albicaulis than in oaks, while veto was more frequent in the latter. Yet in all species, costs of reproduction were too small to impose a replenishment period. A synchronous environmental veto, in the presence of environmental stochasticity, was sufficient to produce observed variability and synchrony in reproduction. In the past, vetoes like frost events that prevent reproduction have been perceived as negative for plants. In fact, they could be selectively favored as a way to create mast seeding.

Genetic rescue by distant trees mitigates qualitative pollen limitation imposed by fine-scale spatial genetic structure.

Restricted seed dispersal frequently leads to fine-scale spatial genetic structure (i.e., FSGS) within plant populations. Depending on its spatial extent and the mobility of pollinators, this inflated kinship at the immediate neighbourhood can critically impoverish pollen quality. Despite the common occurrence of positive FSGS within plant populations, our knowledge regarding the role of long-distance pollination preventing reproductive failure is still limited. Using microsatellite markers, we examined the existence of positive FSGS in two low-density populations of the tree Pyrus bourgaeana. We also designed controlled crosses among trees differing in their kinship to investigate the effects of increased local kinship on plant reproduction. We used six pollination treatments and fully monitored fruit production, fruit and seed weight, proportion of mature seeds per fruit, and seed germination. Our results revealed positive FSGS in both study populations and lower fruit initiation in flowers pollinated with pollen from highly-genetically related individuals within the neighbourhood, with this trend intensifying as the fruit development progressed. Besides, open-pollinated flowers exhibited lower performance compared to those pollinated by distant pollen donors, suggesting intense qualitative pollen limitation in natural populations. We found positive fine-scale spatial genetic structure is translated into impoverished pollen quality from nearby pollen donors which negatively impacts the reproductive success of trees in low-density populations. Under this scenario of intrapopulation genetic rescue by distant pollen donors, the relevance of highly-mobile pollinators for connecting spatially and genetically distant patches of trees may be crucial to safeguarding population recruitment.

Strong among population variation in frugivory strength by functional diverse frugivores: a 'reciprocal translocation' experiment.

Fruit-frugivore interactions are critical for the dynamics and evolution of many plant communities. The strength of the interactions between a given plant species and different frugivore guilds (e.g., seed dispersers, seed predators) often vary in space due to changes in plant extrinsic factors (e.g., frugivore abundances) and plant traits (e.g., fruit size and reward). By reciprocally translocating Pyrus bourgaeana ripe fruits representative of five Mediterranean localities during 2 consecutive years, we experimentally quantified guild-specific variations among populations in frugivory strength, while accounted for plant-intrinsic and- extrinsic factors. Though overall fruit removal did not differ among localities, there were strong guild-specific differences in fruit removal strength. Fruit removal by pulp feeders, seed dispersers, and fruit predators varied among populations up to 8.5-, 5.6-, and 4.0-folds, respectively. These strong variations seemed mediated by changes in frugivore relative abundances rather than on availability of alternative fruits. As expected, all fruit traits considered (e.g., fruit size, pulp amount) markedly varied among tree populations. However, no frugivore guild showed preference for fruits from any locality, suggesting that fruit traits did not contribute much to differences in frugivory strength among populations. Since the functional diverse frugivore guilds played contrasting roles in P. bourgaeana dynamics (e.g., seed dispersal vs. seed predation), our study highlights the importance of accounting for functional diversity in frugivore guilds when estimating spatial variations in the strenght of seed dispersal. This investigation also illustrates a neglected but widely applicable experimental approach to identify the relative importance of extrinsic factors and fruit traits in mediating fruit-frugivore interactions.

Evolutionary ecology of masting: mechanisms, models, and climate change.

Many perennial plants show mast seeding, characterized by synchronous and highly variable reproduction across years. We propose a general model of masting, integrating proximate factors (environmental variation, weather cues, and resource budgets) with ultimate drivers (predator satiation and pollination efficiency). This general model shows how the relationships between masting and weather shape the diverse responses of species to climate warming, ranging from no change to lower interannual variation or reproductive failure. The role of environmental prediction as a masting driver is being reassessed; future studies need to estimate prediction accuracy and the benefits acquired. Since reproduction is central to plant adaptation to climate change, understanding how masting adapts to shifting environmental conditions is now a central question.

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.

Thieves or mutualists? Pulp feeders enhance endozoochore local recruitment.

The persistence of mutualisms despite the strong incidence of exploiters could be explained if exploiters deny one or more services (i.e., cheat) while eventually supplying some subtler but critical services. Pulp feeders usually ingest fruit reward without dispersing seeds and thus are considered to be mainly cheaters or thieves of seed-disperser mutualisms. By consuming the fruit pulp, however, they could release seeds from pulp inhibitory effect, enhancing germination and, potentially, subsequent seedling emergence, growth, survival, and thus local recruitment. We evaluated such a largely neglected hypothesis by considering the interaction between Pyrus bourgaeana and its pulp feeders. We experimentally showed that pericarp removal had a consistent strong positive effect on seed performance (e.g., lower rotting and higher germination percentages) and seedling fate (greater emergence, growth, and survival to two years old). Interestingly, these relatively large positive effects of depulpation on plant fitness persisted for a surprisingly long time. Though seedlings experienced higher mortality under fruiting conspecifics, the benefits of depulpation were not overridden by high propagule mortality beneath fruiting trees or in adverse microhabitats after two years of monitoring. Specifically, the cumulative probability of establishment for depulped seeds was 4-25 times higher than for seeds in whole ripe fruits. Thus, under some circumstances, pulp feeders can provide essential services to endozoochorous plants. Our study contributes to clarifying the apparent paradox of plant-frugivore mutualisms that persist in the face of exploitation by pulp feeders. Because "thieves" and "mutualists" refer to the extremes of a complex continuum, and because organisms displaying concurrent cheating and honest behaviors during different host stages are likely prevalent, the persistent language of mutualists vs. thieves, cheaters, or exploiters might be misleading.

Microgeographical, inter-individual, and intra-individual variation in the flower characters of Iberian pear Pyrus bourgaeana (Rosaceae).

Flower characteristics have been traditionally considered relatively constant within species. However, there are an increasing number of examples of variation in flower characteristics. In this study, we examined the variation in attracting and rewarding flower characters at several ecological levels in a metapopulation of Pyrus bourgaeana in the Doñana area (SW Spain). We answered the following questions: what are the variances of morphological and nectar characters of flowers? How important are intra-individual and inter-individual variance in flower characters? Are there microgeographical differences in flower characters? And if so, are they consistent between years? In 2008 and 2009, we sampled flowers of 72 trees from five localities. For six flower morphological and two nectar characteristics, we calculated coefficients of variation (CV). The partitioning of total variation among-localities, among-individuals, and within-individuals was estimated. To analyze differences among localities and their consistency between years, we conducted generalized linear mixed models. The CVs of nectar characters were always higher than those of morphological characters. As expected, inter-individual variation was the main source of variation of flower morphology, but nectar characters had significant variation at both intra- and inter-individual levels. For most floral traits, there were no differences among localities. Our study documents that variation is a scale-dependent phenomenon and that it is essential to consider intra- and inter-individual variance when investigating the causes and consequences of variation. It also shows that single year studies of floral characters should be viewed with caution.