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.

A novel TFL1 gene induces flowering in the mast seeding alpine snow tussock, Chionochloa pallens (Poaceae).

Masting, the synchronous, highly variable flowering across years by a population of perennial plants, has been reported to be precipitated by various factors including nitrogen levels, drought conditions, and spring and summer temperatures. However, the molecular mechanism leading to the initiation of flowering in masting plants in particular years remains largely unknown, despite the potential impact of climate change on masting phenology. We studied genes controlling flowering in the alpine snow tussock Chionochloa pallens (Poaceae), a strongly masting perennial grass. We used a range of in situ and manipulated plants to obtain leaf samples from tillers (shoots) which subsequently remained vegetative or flowered. Here, we show that a novel orthologue of TERMINAL FLOWER 1 (TFL1; normally a repressor of flowering in other species) promotes the induction of flowering in C. pallens (hence Anti-TFL1), a conclusion supported by structural, functional and expression analyses. Global transcriptomic analysis indicated differential expression of CpTPS1, CpGA20ox1, CpREF6 and CpHDA6, emphasizing the role of endogenous cues and epigenetic regulation in terms of responsiveness of plants to initiate flowering. Our molecular-based study provides insights into the cellular mechanism of flowering in masting plants and will supplement ecological and statistical models to predict how masting will respond to global climate change.

Molecular control of the floral transition in the mast seeding plant Celmisia lyallii (Asteraceae).

Mast flowering (or masting) is synchronous, highly variable flowering among years in populations of perennial plants. Despite having widespread consequences for seed consumers, endangered fauna and human health, masting is hard to predict. While observational studies show links to various weather patterns in different plant species, the mechanism(s) underpinning the regulation of masting is still not fully explained. We studied floral induction in Celmisia lyallii (Asteraceae), a mast flowering herbaceous alpine perennial, comparing gene expression in flowering and nonflowering plants. We performed translocation experiments to induce the floral transition in C. lyallii plants followed by both global and targeted expression analysis of flowering-pathway genes. Differential expression analysis showed elevated expression of ClSOC1 and ClmiR172 (promoters of flowering) in leaves of plants that subsequently flowered, in contrast to elevated expression of ClAFT and ClTOE1 (repressors of flowering) in leaves of plants that did not flower. The warm summer conditions that promoted flowering led to differential regulation of age and hormonal pathway genes, including ClmiR172 and ClGA20ox2, known to repress the expression of floral repressors and permit flowering. Upregulated expression of epigenetic modifiers of floral promoters also suggests that plants may maintain a novel "summer memory" across years to induce flowering. These results provide a basic mechanistic understanding of floral induction in masting plants and evidence of their ability to imprint various environmental cues to synchronize flowering, allowing us to better predict masting events under climate change.

Climate warming causes mast seeding to break down by reducing sensitivity to weather cues.

Climate change is altering patterns of seed production worldwide with consequences for population recruitment and migration potential. For the many species that regenerate through synchronized, quasiperiodic reproductive events termed masting, these changes include decreases in the synchrony and interannual variation in seed production. This breakdown in the occurrence of masting features harms reproduction by decreasing the efficiency of pollination and increasing seed predation. Changes in masting are often paralleled by warming temperatures, but the underlying proximate mechanisms are unknown. We used a unique 39-year study of 139 European beech (Fagus sylvatica) trees that experienced masting breakdown to track the seed developmental cycle and pinpoint phases where weather effects on seed production have changed over time. A cold followed by warm summer led to large coordinated flowering efforts among plants. However, trees failed to respond to the weather signal as summers warmed and the frequency of reproductive cues changed fivefold. Less synchronous flowering resulted in less efficient pollination that further decreased the synchrony of seed maturation. As global temperatures are expected to increase this century, perennial plants that fine-tune their reproductive schedules based on temperature cues may suffer regeneration failures.

Molecular control of masting: an introduction to an epigenetic summer memory.

BACKGROUND: Mast flowering ('masting') is characterized by mass synchronized flowering at irregular intervals in populations of perennial plants over a wide geographical area, resulting in irregular high seed production. While masting is a global phenomenon, it is particularly prevalent in the alpine flora of New Zealand. Increases in global temperature may alter the masting pattern, affecting wider communities with a potential impact on plant-pollinator interactions, seed set and food availability for seed-consuming species. SCOPE: This review summarizes an ecological temperature model (ΔT) that is being used to predict the intensity of a masting season. We introduce current molecular studies on flowering and the concept of an 'epigenetic summer memory' as a driver of mast flowering. We propose a hypothetical model based on temperature-associated epigenetic modifications of the floral integrator genes FLOWERING LOCUS T, FLOWERING LOCUS C and SUPPRESSOR OF OVEREXPRESSION OF CONSTANS1. CONCLUSIONS: Genome-wide transcriptomic and targeted gene expression analyses are needed to establish the developmental and physiological processes associated with masting. Such analyses may identify changes in gene expression that can be used to predict the intensity of a forthcoming masting season, as well as to determine the extent to which climate change will influence the mass synchronized flowering of masting species, with downstream impacts on their associated communities.

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.

An avian seed dispersal paradox: New Zealand's extinct megafaunal birds did not disperse large seeds.

Often the mutualistic roles of extinct species are inferred based on plausible assumptions, but sometimes palaeoecological evidence can overturn such inferences. We present an example from New Zealand, where it has been widely assumed that some of the largest-seeded plants were dispersed by the giant extinct herbivorous moa (Dinornithiformes). The presence of large seeds in preserved moa gizzard contents supported this hypothesis, and five slow-germinating plant species (Elaeocarpus dentatus, E. hookerianus, Prumnopitys ferruginea, P. taxifolia, Vitex lucens) with thick seedcoats prompted speculation about whether these plants were adapted for moa dispersal. However, we demonstrate that all these assumptions are incorrect. While large seeds were present in 48% of moa gizzards analysed, analysis of 152 moa coprolites (subfossil faeces) revealed a very fine-grained consistency unparalleled in extant herbivores, with no intact seeds larger than 3.3 mm diameter. Secondly, prolonged experimental mechanical scarification of E. dentatus and P. ferruginea seeds did not reduce time to germination, providing no experimental support for the hypothesis that present-day slow germination results from the loss of scarification in moa guts. Paradoxically, although moa were New Zealand's largest native herbivores, the only seeds to survive moa gut passage intact were those of small-seeded herbs and shrubs.

Olfactory Cues, Visual Cues, and Semiochemical Diversity Interact During Host Location by Invasive Forest Beetles.

Plant-feeding insects use visual and olfactory cues (shape, color, plant volatiles) for host location, but the relative importance of different cues and interactions with non-host-plant volatiles in ecosystems of varying plant biodiversity is unclear for most species. We studied invasive bark beetles and wood borers associated with pine trees to characterize interactions among color, host and non-host volatiles, by employing traps that mimic tree trunks. Cross-vane flight intercept traps (black, green, red, white, yellow, clear) and black funnel traps were used with and without attractants (α-pinene + ethanol), repellents (non-host green leaf volatiles, 'GLV'), and attractant/repellent combinations in four pine forests in New Zealand. We trapped 274,594 Hylurgus ligniperda, 7842 Hylastes ater, and 16,301 Arhopalus ferus. Trap color, attractant, and color × attractant effects were highly significant. Overall, black and red traps had the highest catches, irrespective of the presence of attractants. Alpha-pinene plus ethanol increased trap catch of H. ligniperda 200-fold but only 6-fold for H. ater and 2-fold for A. ferus. Green leaf volatiles had a substantial repellent effect on trap catch of H. ligniperda but less on H. ater and A. ferus. Attack by H. ligniperda was halved when logs were treated with GLV, and a similar effect was observed when logs were placed among broadleaved understory shrubs emitting GLV. Overall, H. ligniperda was most strongly affected by the olfactory cues used, whereas H. ater and A. ferus were more strongly affected by visual cues. Collectively, the results support the semiochemical diversity hypothesis, indicating that non-host plant volatiles from diverse plant communities or artificial dispensers can contribute to resistance against herbivores by partly disrupting host location.

Mechanisms of mast seeding: resources, weather, cues, and selection.

546 I. 546 II. 547 III. 548 IV. 552 V. 554 VI. 556 VII. 558 VIII. 558 IX. 559 559 References 559 SUMMARY: Mast seeding is a widespread and widely studied phenomenon. However, the physiological mechanisms that mediate masting events and link them to weather and plant resources are still debated. Here, we explore how masting is affected by plant resource budgets, fruit maturation success, and hormonal coordination of cues including weather and resources. There is little empirical support for the commonly stated hypothesis that plants store carbohydrates over several years to expend in a high-seed year. Plants can switch carbohydrates away from growth in high-seed years, and seed crops are more probably limited by nitrogen or phosphorus. Resources are clearly involved in the proximate mechanisms driving masting, but resource budget (RB) models cannot create masting in the absence of selection because some underlying selective benefit is required to set the level of a 'full' seed crop at greater than the annual resource increment. Economies of scale (EOSs) provide the ultimate factor selecting for masting, but EOSs probably always interact with resources, which modify the relationship between weather cues and reproduction. Thus, RB and EOS models are not alternative explanations for masting - both are required. Experiments manipulating processes that affect mast seeding will help clarify the physiological mechanisms that underlie mast seeding.

The compounding effects of high pollen limitation, selfing rates and inbreeding depression leave a New Zealand tree with few viable offspring.

BACKGROUND AND AIMS: Interactions between species are especially sensitive to environmental changes. The interaction between plants and pollinators is of particular interest given the potential current global decline in pollinators. Reduced pollinator services can be compensated for in some plant species by self-pollination. However, if inbreeding depression is high, selfed progeny could die prior to reaching adulthood, leading to cryptic recruitment failure. METHODS: To examine this scenario, pollinator abundance, pollen limitation, selfing rates and inbreeding depression were examined in 12 populations of varying disturbance levels in Sophora microphylla (Fabaceae), an endemic New Zealand tree species. KEY RESULTS: High pollen limitation was found in all populations (average of 58 % reduction in seed production, nine populations), together with high selfing rates (61 % of offspring selfed, six populations) and high inbreeding depression (selfed offspring 86 % less fit, six populations). Pollen limitation was associated with lower visitation rates by the two endemic bird pollinators. CONCLUSIONS: The results suggest that for these populations, over half of the seeds produced are genetically doomed. This reduction in the fitness of progeny due to reduced pollinator service is probably important to population dynamics of other New Zealand species. More broadly, the results suggest that measures of seed production or seedling densities may be a gross overestimate of the effective offspring production. This could lead to cryptic recruitment failure, i.e. a decline in successful reproduction despite high progeny production. Given the global extent of pollinator declines, cryptic recruitment failure may be widespread.

CiteAb: a searchable antibody database that ranks antibodies by the number of times they have been cited.

BACKGROUND: Research antibodies are used by thousands of scientists working in diverse disciplines, but it is common to hear concerns about antibody quality. This means that researchers need to carefully choose the antibodies they use to avoid wasting time and money. A well accepted way of selecting a research antibody is to identify one which has been used previously, where the associated data has been peer-reviewed and the results published. DESCRIPTION: CiteAb is a searchable database which ranks antibodies by the number of times they have been cited. This allows researchers to easily find antibodies that have been used in peer-reviewed publications and the accompanying citations are listed, so users can check the data contained within the publications. This makes CiteAb a useful resource for identifying antibodies for experiments and also for finding information to demonstrate antibody validation. The database currently contains 1,400,000 antibodies which are from 90 suppliers, including 87 commercial companies and 3 academic resources. Associated with these antibodies are 140,000 publications which provide 306,000 antibody citations. In addition to searching, users can also browse through the antibodies and add their own publications to the CiteAb database. CONCLUSIONS: CiteAb provides a new way for researchers to find research antibodies that have been used successfully in peer-reviewed publications. It aims to assist these researchers and will hopefully help promote progress in many areas of life science research.

Unrecognized impact of a biocontrol agent on the spread rate of an invasive thistle.

Herbivores may significantly reduce plant populations by reducing seed set; however, we know little of their impact on seed movement. We show for the first time that the receptacle-feeding weevil Rhinocyllus conicus not only reduces seed production by the invasive thistle Carduus nutans but also inhibits release and subsequent wind dispersal of seeds. These effects generate large, though different, impacts on spatial spread and local abundance in two populations with differing demography, located in the United States and New Zealand. Furthermore, the mechanism is context dependent, with the largest effects through increased terminal velocity in the United States but through reduced seed production in New Zealand. Our results show that the benefit of biocontrol programs may have been underestimated; screenings of potential biocontrol agents should examine effects on pest dispersal and spread, as well as on abundance.

Summer solstice orchestrates the subcontinental-scale synchrony of mast seeding.

High interannual variation in seed production in perennial plants can be synchronized at subcontinental scales with wide consequences for ecosystem functioning, but how such synchrony is generated is unclear1-3. We investigated the factors contributing to masting synchrony in European beech (Fagus sylvatica), which extends to a geographic range of 2,000 km. Maximizing masting synchrony via spatial weather coordination, known as the Moran effect, requires a simultaneous response to weather conditions across distant populations. A celestial cue that occurs simultaneously across the entire hemisphere is the longest day (the summer solstice). We show that European beech abruptly opens its temperature-sensing window on the solstice, and hence widely separated populations all start responding to weather signals in the same week. This celestial 'starting gun' generates ecological events with high spatial synchrony across the continent.

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.

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.

Mast seeding: Study of oak mechanisms carries wider lessons.

Variable acorn crops in oaks were thought to reflect variable pollination success, but a new study shows local climates determine whether pollination or flower production drives acorn crops. This affects forest regeneration under climate change, and cautions against dichotomous summaries of biological phenomena.

Frugivore loss limits recruitment of large-seeded trees.

Although global declines in frugivores may disrupt seed dispersal mutualisms and inhibit plant recruitment, quantifying the likely reduction in plant regeneration has been difficult and rarely attempted. We use a manipulative factorial experiment to quantify dependence of recruitment on dispersal (i.e. fruit pulp removal and movement of seed away from parental area) in two large-seeded New Zealand tree species. Complete dispersal failure would cause a 66 to 81 per cent reduction in recruitment to the 2-year-old seedling stage, and synergistic interactions with introduced mammalian seed and seedling predators increase the reduction to 92 to 94 per cent. Dispersal failure reduced regeneration through effects on seed predation, germination and (especially) seedling survival, including distance- and density-dependent (Janzen-Connell) effects. Dispersal of both species is currently largely dependent on a single frugivore, and many fruits today remain uneaten. Present-day levels of frugivore loss and mammal seed and seedling predators result in 57 to 84 per cent fewer seedlings after 2 years. Our study demonstrates the importance of seed dispersal for local plant population persistence, and validates concerns about the community consequences of frugivore declines.

Importance of individual and environmental variation for invasive species spread: a spatial integral projection model.

Plant survival, growth, and flowering are size dependent in many plant populations but also vary among individuals of the same size. This individual variation, along with variation in dispersal caused by differences in, e.g., seed release height, seed characteristics, and wind speed, is a key determinant of the spread rate of species through homogeneous landscapes. Here we develop spatial integral projection models (SIPMs) that include both demography and dispersal with continuous state variables. The advantage of this novel approach over discrete-stage spread models is that the effect of variation in plant size and size-dependent vital rates can be studied at much higher resolution. Comparing Neubert-Caswell matrix models to SIPMs allowed us to assess the importance of including individual variation in the models. As a test case we parameterized a SIPM with previously published data on the invasive monocarpic thistle Carduus nutans in New Zealand. Spread rate (c*) estimates were 34% lower than for standard spatial matrix models and stabilized with as few as seven evenly distributed size classes. The SIPM allowed us to calculate spread rate elasticities over the range of plant sizes, showing the size range of seedlings that contributed most to c* through their survival, growth and reproduction. The annual transitions of these seedlings were also the most important ones for local population growth (lambda). However, seedlings that reproduced within a year contributed relatively more to c* than to lambda. In contrast, plants that grow over several years to reach a large size and produce many more seeds, contributed relatively more to lambda than to c*. We show that matrix models pick up some of these details, while other details disappear within wide size classes. Our results show that SIPMs integrate various sources of variation much better than discrete-stage matrix models. Simpler, heuristic models, however, remain very valuable in studies where the main goal is to investigate the general impact of a life history stage on population dynamics. We conclude with a discussion of future extensions of SIPMs, including incorporation of continuous time and environmental drivers.

Delayed fertilization facilitates flowering time diversity in Fagaceae.

Fagaceae includes typical masting species that exhibit highly synchronized and fluctuating acorn production. Fagaceae shows an interesting feature in that fertilization is delayed by several weeks to more than 1 year after pollination. Although delayed fertilization was recorded over a century ago, the evolutionary advantage of delayed fertilization is still poorly understood. Here, we present a new hypothesis that delayed fertilization facilitates temporal niche differentiation via non-overlapping flowering times among species. Comparing flowering and fruiting times in 228 species from five genera in Fagaceae, we first show that there is a close association between a wider spread of flowering times and the likelihood of a 2-year fruiting habit in which there is a long delay from pollination to fertilization. To study the coevolution of flowering time and delayed fertilization, we developed a mathematical model that incorporates the effects of competition for pollinators, seed predator satiation and unfavourable season for reproduction on fitness. The model shows that delayed fertilization facilitates the diversification of flowering time in a population, which is advantageous for animal-pollinated trees that compete over pollinators. Our new hypothesis about the coevolution of delayed fertilization and flowering time will provide new insight into the evolution of masting. This article is part of the theme issue 'The ecology and evolution of synchronized seed production in plants'.