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.

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.

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.

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.

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'.

Studying the genetic basis of masting.

The mechanisms underlying mast seeding have traditionally been studied by collecting long-term observational data on seed crops and correlating seedfall with environmental variables. Significant progress in ecological genomics will improve our understanding of the evolution of masting by clarifying the genetic basis of masting traits and the role of natural selection in shaping those traits. Here, we summarize three important aspects in studying the evolution of masting at the genetic level: which traits govern masting, whether those traits are genetically regulated, and which taxa show wide variation in these traits. We then introduce recent studies on the molecular mechanisms of masting. Those studies measure seasonal changes in gene expression in natural conditions to quantify how multiple environmental factors combine to regulate floral initiation, which in many masting plant species is the single largest contributor to among-year variation in seed crops. We show that Fagaceae offers exceptional opportunities for evolutionary investigations because of its diversity at both the phenotypic and genetic levels and existing documented genome sequences. This article is part of the theme issue 'The ecology and evolution of synchronized seed production in plants'.

Excluding mammalian predators increases bird densities and seed dispersal in fenced ecosanctuaries.

Islands are epicenters of animal extinctions and population declines. These losses exacerbate biodiversity loss and disrupt ecological services in areas of high endemism. Island defaunation is primarily driven by invasive mammalian predators, and mammal eradications are reversing population declines for some island species. Invasive mammal eradications may also have the capacity to restore ecological interactions, along with the recovery of island fauna. Here we show that invasive mammal eradication in fenced ecosanctuaries results in higher rates of bird foraging on fruit, and higher bird-mediated seed dispersal, than in similar forests without mammal eradication. We further show that higher foraging and seed dispersal is related to higher densities of native bird species, after accounting for natural variation in fruit availability. For the many other systems globally that are under threat from invasive mammals, New Zealand's fenced ecosanctuary model offers a promising tool for restoring biodiversity and ecosystem services.

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.

Recording COVID-19 consultations: review of symptoms, risk factors, and proposed SNOMED CT terms.

BACKGROUND: There is an urgent need for epidemiological research in primary care to develop risk assessment processes for patients presenting with COVID-19, but lack of a standardised approach to data collection is a significant barrier to implementation. AIM: To collate a list of relevant symptoms, assessment items, demographics, and lifestyle and health conditions associated with COVID-19, and match these data items with corresponding SNOMED CT clinical terms to support the development and implementation of consultation templates. DESIGN & SETTING: Published and preprint literature for systematic reviews, meta-analyses, and clinical guidelines describing the symptoms, assessment items, demographics, and/or lifestyle and health conditions associated with COVID-19 and its complications were reviewed. Corresponding clinical concepts from SNOMED CT, a widely used structured clinical vocabulary for electronic primary care health records, were identified. METHOD: Guidelines and published and unpublished reviews (N = 61) were utilised to collate a list of relevant data items for COVID-19 consultations. The NHS Digital SNOMED CT Browser was used to identify concept and descriptive identifiers. Key implementation challenges were conceptualised through a Normalisation Process Theory (NPT) lens. RESULTS: In total, 32 symptoms, eight demographic and lifestyle features, 25 health conditions, and 20 assessment items relevant to COVID-19 were identified, with proposed corresponding SNOMED CT concepts. These data items can be adapted into a consultation template for COVID-19. Key implementation challenges include: 1) engaging with key stakeholders to achieve 'buy in'; and 2) ensuring any template is usable within practice settings. CONCLUSION: Consultation templates for COVID-19 are needed to standardise data collection, facilitate research and learning, and potentially improve quality of care for COVID-19.

Climate Change Strengthens Selection for Mast Seeding in European Beech.

Climate change is altering patterns of seed production worldwide [1-4], but the potential for evolutionary responses to these changes is poorly understood. Masting (synchronous, annually variable seed production by plant populations) is selectively beneficial through economies of scale that decrease the cost of reproduction per surviving offspring [5-7]. Masting is particularly widespread in temperate trees [8, 9] impacting food webs, macronutrient cycling, carbon storage, and human disease risk [10-12], so understanding its response to climate change is important. Here, we analyze inter-individual variability in plant reproductive patterns and two economies of scale-predator satiation and pollination efficiency-and document how natural selection acting upon them favors masting. Four decades of observations for European beech (Fagus sylvatica) show that predator satiation and pollination efficiency select for individuals with higher inter-annual variability of reproduction and higher reproductive synchrony between individuals. This result confirms the long-standing theory that masting, a population-level phenomenon, is generated by selection on individuals. Furthermore, recent climate-driven increases in mean seed production have increased selection pressure from seed predators but not from pollination efficiency. Natural selection is thus acting to restore the fitness benefits of masting, which have previously decreased under a warming climate [13]. However, selection will likely take far longer (centuries) than climate warming (decades), so in the short-term, tree reproduction will be reduced because masting has become less effective at satiating seed predators. Over the long-term, evolutionary responses to climate change could potentially increase inter-annual variability of seed production of masting species.

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.

Early Pandemic Evaluation and Enhanced Surveillance of COVID-19 (EAVE II): protocol for an observational study using linked Scottish national data.

INTRODUCTION: Following the emergence of the novel severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) in December 2019 and the ensuing COVID-19 pandemic, population-level surveillance and rapid assessment of the effectiveness of existing or new therapeutic or preventive interventions are required to ensure that interventions are targeted to those at highest risk of serious illness or death from COVID-19. We aim to repurpose and expand an existing pandemic reporting platform to determine the attack rate of SARS-CoV-2, the uptake and effectiveness of any new pandemic vaccine (once available) and any protective effect conferred by existing or new antimicrobial drugs and other therapies. METHODS AND ANALYSIS: A prospective observational cohort will be used to monitor daily/weekly the progress of the COVID-19 epidemic and to evaluate the effectiveness of therapeutic interventions in approximately 5.4 million individuals registered in general practices across Scotland. A national linked dataset of patient-level primary care data, out-of-hours, hospitalisation, mortality and laboratory data will be assembled. The primary outcomes will measure association between: (A) laboratory confirmed SARS-CoV-2 infection, morbidity and mortality, and demographic, socioeconomic and clinical population characteristics; and (B) healthcare burden of COVID-19 and demographic, socioeconomic and clinical population characteristics. The secondary outcomes will estimate: (A) the uptake (for vaccines only); (B) effectiveness; and (C) safety of new or existing therapies, vaccines and antimicrobials against SARS-CoV-2 infection. The association between population characteristics and primary outcomes will be assessed via multivariate logistic regression models. The effectiveness of therapies, vaccines and antimicrobials will be assessed from time-dependent Cox models or Poisson regression models. Self-controlled study designs will be explored to estimate the risk of therapeutic and prophylactic-related adverse events. ETHICS AND DISSEMINATION: We obtained approval from the National Research Ethics Service Committee, Southeast Scotland 02. The study findings will be presented at international conferences and published in peer-reviewed journals.

Climate warming disrupts mast seeding and its fitness benefits in European beech.

Many plants benefit from synchronous year-to-year variation in seed production, called masting. Masting benefits plants because it increases the efficiency of pollination and satiates predators, which reduces seed loss. Here, using a 39-year-long dataset, we show that climate warming over recent decades has increased seed production of European beech but decreased the year-to-year variability of seed production and the reproductive synchrony among individuals. Consequently, the benefit that the plants gained from masting has declined. While climate warming was associated with increased reproductive effort, we demonstrate that less effective pollination and greater losses of seeds to predators offset any benefits to the plants. This shows that an apparently simple benefit of climate warming unravels because of complex ecological interactions. Our results indicate that in masting systems, the main beneficiaries of climate-driven increases in seed production are seed predators, not plants.

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.

Long seed dispersal distances by an inquisitive flightless rail (Gallirallus australis) are reduced by interaction with humans.

Human presence is becoming increasingly ubiquitous, but the influence this has on the seed dispersal services performed by frugivorous animals is largely unknown. The New Zealand weka (Gallirallus australis) is an inquisitive flightless rail that frequently congregates in areas of high human use. Weka are important seed dispersers, yet the seed dispersal services they provide are still poorly understood. We estimated seed dispersal distances of weka for two plant species (Prumnopitys ferruginea and Elaeocarpus dentatus) and tested how human interaction affected these dispersal distances. We estimated weka seed dispersal distances by combining GPS data from 39 weka over three sites with weka seed retention time data in a mechanistic model. The mean seed retention times were extremely long (38-125 h). Weka were highly effective dispersers, dispersing 93-96% of seeds away from parent canopies, and 1% of seeds over 1 km. However, we found evidence of a significant human impact on the seed dispersal distances of weka, with birds occupying areas of high human use performing 34.8-40.9% shorter distances than their more remote counterparts. This represents an example of cryptic function loss, where although weka are still present in the ecosystem, their seed dispersal services are impaired by human interaction.

Introduction of mammalian seed predators and the loss of an endemic flightless bird impair seed dispersal of the New Zealand tree Elaeocarpus dentatus.

Understanding the mutualistic services provided by species is critical when considering both the consequences of their loss or the benefits of their reintroduction. Like many other Pacific islands, New Zealand seed dispersal networks have been changed by both significant losses of large frugivorous birds and the introduction of invasive mammals. These changes are particularly concerning when important dispersers remain unidentified. We tested the impact of frugivore declines and invasive seed predators on seed dispersal for an endemic tree, hinau Elaeocarpus dentatus, by comparing seed dispersal and predation rates on the mainland of New Zealand with offshore sanctuary islands with higher bird and lower mammal numbers. We used cameras and seed traps to measure predation and dispersal from the ground and canopy, respectively. We found that canopy fruit handling rates (an index of dispersal quantity) were poor even on island sanctuaries (only 14% of seeds captured below parent trees on islands had passed through a bird), which suggests that hinau may be adapted for ground-based dispersal by flightless birds. Ground-based dispersal of hinau was low on the New Zealand mainland compared to sanctuary islands (4% of seeds dispersed on the mainland vs. 76% dispersed on islands), due to low frugivore numbers. A flightless endemic rail (Gallirallus australis) conducted the majority of ground-based fruit removal on islands. Despite being threatened, this rail is controversial in restoration projects because of its predatory impacts on native fauna. Our study demonstrates the importance of testing which species perform important mutualistic services, rather than simply relying on logical assumptions.