Patterns of Annual Seed Production by Northern Hemisphere Trees: A Global Perspective

We tested whether annual seed production (masting or mast fruiting) in Northern Hemisphere trees is an evolved strategy or a consequence of resource tracking by comparing masting patterns with those of annual rainfall and mean summer temperatures, two environmental variables likely to correlate with available resources. There were generally significant negative autocorrelations between the seed crop in year x and year x+1 (year x+2 in species of Quercus requiring 2 yr to mature acorns), as expected if resources are depleted in mast years in part by switching resources from growth to reproduction. Spatial autocorrelation in annual seed production generally declined with distance but was statistically significant over large geographic areas. Variability in annual seed production was relatively high and inversely correlated with latitude and generally not bimodally distributed. Patterns of spatial autocorrelation in annual rainfall and summer temperatures are generally similar to those exhibited by annual seed production, and relative variability in annual rainfall is also inversely correlated with latitude. However, these environmental variables exhibit distinctly different patterns of temporal autocorrelation, are much less variable, and are more normally distributed than annual seed production. Combined with the inverse relationship between growth and reproduction previously documented, these results support the hypothesis that variability in annual seed production is an evolved strategy and that annual seed production is more or less normally distributed rather than an all-or-none phenomenon.     

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.     

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.     

Spatiotemporal dynamics of Floerkea proserpinacoides (Limnanthaceae), an annual plant of the deciduous forest of eastern North America

Because environmental filters are temporally and spatially heterogeneous, there often is a lack of significant relationship between the spatial patterns of successive life stages in plant populations. In this study, we determined the spatiotemporal relationships between different life stages in two populations of an annual plant of the deciduous forests of eastern North America, Floerkea proserpinacoides. Demographic surveys were done over a 4-yr period, and experiments were performed in the field and under controlled conditions to test for the effects of various environmental factors on population dynamics. There was a general lack of relationship between the spatial patterns of seed bank and seedling density, and a lack of similarity between their spatial correlograms. This was related mostly to the effects of spatially variable environmental filters operating on germination and emergence. However, environmental filters acting on plant survival were stable through time and contributed to stabilize the density and spatial patterns of the populations. Despite density-dependent presenescence mortality, spatial patterns of seedlings and mature individuals were similar and their correlograms were alike, suggesting that mortality did not fully compensate for density. Estimated fecundity was negatively correlated with population density over the study period. Although flower production started only 2-3 wk after emergence, seed maturation mostly occurred at the end of the life cycle, just before the onset of plant senescence. Yet, individual fecundity was low for an annual plant, i.e., 3.0 ± 0.5 mature seeds/plant (mean ± 1 SE). Seed predation by vertebrates was not significant. Low soil moisture had little effect on the total number of seeds germinating, although it slowed down the germination process. In quadrats where leaf litter was experimentally doubled, seedling emergence was lower than in control quadrats; in quadrats where leaf litter was completely removed, emergence did not differ from that in control quadrats. Susceptibility to drought stress was higher for seedlings than for mature plants. Although the species does not maintain a long-term persistent soil seed bank, other factors, such as density-dependent fecundity and autogamy, may temper population fluctuations through time and reduce the probability of local extinction.     

Factors contributing to the loss of seed from the seed-bank of Trifolium balansae and Trifolium resupinatum over summer

Abstract The influence of predation, fungi and germination of seed of the annual legumes Trifolium balansae and Trifolium resupinatum was investigated by placing known quantities of seed in bags in the field; combinations of all three factors were imposed. It was found that rainfall was the most important factor contributing to the loss of seed over summer (up to 76%), followed by predation (up to 15%); fungi had only a very small influence (0.1–0.2%). Predation contributed to a larger percentage of loss over summer in T. resupinatum line SA14433 than in T. balansae cv. Paradana, which is attributed to seed size. The effect of summer grazing on the size of the seed-bank was investigated. It was found that summer grazing did not influence the amount of seed present in the seed-bank in March. Removal of all surface material in December resulted in a significant drop in seed reserves compared with the ungrazed or grazed areas. Hardseededness in March was not affected by any of the treatments; the seedling density after regeneration was not affected by summer grazing, but was reduced when all surface material was removed. The data were incorporated in a model to describe seed loss from the seed bank over summer quantitatively; the utility of such models is discussed.     

Interactions between density-dependent processes, population dynamics and control of an invasive plant species, Tripleurospermum perforatum (scentless chamomile)

Tripleurospermum perforatum is an invasive weedy species which exhibits strong over-compensating density dependence. Interactions between density-dependent survival, probability of flowering and fecundity were modelled and their impact on the population dynamics were examined. When only fecundity was density-dependent, the dynamics were similar to those observed in the model containing all three density-dependent terms. Density-dependent survival was a stabilizing process when acting in combination with density-dependent fecundity and probability of flowering; removing density-dependent survival from the model produced two-point cycles. The addition of a seed bank was also stabilizing. Simulations of control strategies at different life-history stages indicated that full control would be difficult due to the strong over-compensating density dependence, with severe reductions in fecundity and late season survival necessary in order to reduce equilibrium seed density and biomass.     

Evidence of a component Allee effect driven by predispersal seed predation in a plant (Pedicularis rex,Orobanchaceae)

A small or sparse population may suffer a reduction in fitness owing to Allee effects. Here, we explored effects of plant density on pollination, reproduction and predation in the alpine herb Pedicularis rex over two years. We did not detect a significant difference in the pollination rate or fecundity (fruit set and the initial seed set) before predation between sparse and dense patches in either year, indicating no pollination-driven Allee effect. However, dense patches experienced significantly fewer attacks by predispersal seed predators in both years, resulting in a significantly decreased realized fecundity (final seed set), suggesting a component Allee effect driven by predispersal seed predation. Predation-driven Allee effects have been predicted by many models and demonstrated for a range of animals, but there is scant evidence for such effects in plants. Our study provides strong evidence of a component Allee effect driven by predation in a plant species.     

Masting in a temperate tree: Evidence for environmental prediction?

Many plant species produce large fruit crops in some years and then produce few or no fruits in others. Synchronous, inter‐annual variation in plant reproduction is known as ‘masting’ and its adaptive significance has yet to be fully resolved. For 8 consecutive years, I quantified every fruit produced by 22 females of a New Zealand tree species (Dysoxylum spectabile), which has an unusual habit of taking a full calendar year to mature fruits after flowering. Fruit production varied strongly among years and was tightly synchronized among trees. Annual variability in fruit production declined with total reproductive output, indicating trees with lower fecundity exhibited a stronger tendency to mast. Although unrelated to temperature, annual fruit production was positively related to precipitation during annual periods of fruit development, and negatively related to fruit production in the previous year. Seedlings had higher rates of survivorship in a wet, high‐seed year than in a dry, low‐seed year, suggesting that seedlings might be drought sensitive. Therefore, D. spectabile produced large fruit crops during periods of high rainfall prior to fruit maturation, which may enhance survivorship of drought‐intolerant seeds. Results were inconsistent with several hypotheses that are widely believed to be the most likely explanations for masting. Instead, results were consistent with the environmental prediction hypothesis, suggesting that this hypothesis may be more important than previously appreciated.     

Mast fruiting and seedling survival of the ectomycorrhizal, monodominant Dicymbe corymbosa (Caesalpiniaceae) in Guyana

In Guyana, we investigated seed output, and resulting seedling establishment and survival, during a 'mast' year, by the ectomycorrhizal, monodominant rainforest canopy tree Dicymbe corymbosa (Caesalpiniaceae), a species with high, synchronous seed production at intermittent years. By utilizing seed traps, the mast seed output, predation, carbon and mineral investment, and masting synchrony were quantified in 2003 in primary D. corymbosa forests. Establishment of seedling cohorts was monitored, and climatic conditions associated with masting were assessed. During 2003, D. corymbosa in the Pakaraima Mountains exhibited high, synchronous seed production with low dispersal and predation. Investment in reproductive biomass was large relative to that in other tropical forests. Recent D. corymbosa reproductive events followed El Nino-induced droughts, with little intervening seed production. Over 12 months, 40% of the 2003 seedling cohort survived. Our results suggest that D. corymbosa has a strongly bimodal fruiting pattern that allows the establishment of a large seedling bank, facilitating persistent monodominance. Resource investment in large seed crops may depend on mineral recycling via ectomycorrhizas, coupled with the reallocation of carbon from vegetative maintenance.     

Density-dependent reproductive success among sympatric dipterocarps during a major mast fruiting event

Although masting in Southeast Asia is characterized by the interspecific synchronization of reproduction, little is known about the variation in regeneration strategies among sympatric tree species during major masting events. Herein, we examined the hypothesis that non-abundant species achieve greater seed survival per seed production at the pre- and post-dispersal stages by synchronizing reproduction with abundant species. During the masting event from May to September 2010, we installed seed traps in a primary forest plot of the Deramakot Forest Reserve, Borneo. To identify the possible causes of post-dispersal seed mortality, we conducted a seed-sowing experiment from September 2010 to July 2011 in a primary forest plot with high community-level dipterocarp seed density and two surrounding secondary forests with low seed densities. An abundant species (Shorea multiflora) produced more seeds than other species and exhibited a lower survival rate during the pre-dispersal stage. The ratio of aborted seeds was greater in species with greater seed production, while the ratio of seeds predated by insects was not, suggesting that resource limitations and/or greater inbreeding frequency may explain inefficient seed production. Interspecific variation was rarely observed for post-dispersal seed survival rates. Our study highlights the density-dependent variation in reproductive success between abundant and non-abundant dipterocarp species at the pre-dispersal stage. Non-abundant species achieved greater reproductive success by synchronizing reproduction with the masting of abundant species, which might be an important mechanism for sustainability of rare species populations.     

Masting behaviour in a Mediterranean pine tree alters seed predator selection on reproductive output

• Context‐dependency in species interactions is widespread and can produce concomitant patterns of context‐dependent selection. Masting (synchronous production of large seed crops at irregular intervals by a plant population) has been shown to reduce seed predation through satiation (reduction in rates of seed predation with increasing seed cone output) and thus represents an important source of context‐dependency in plant‐animal interactions. However, the evolutionary consequences of such dynamics are not well understood.
• Here we describe masting behaviour in a Mediterranean model pine species (Pinus pinaster) and present a test of the effects of masting on selection by seed predators on reproductive output. We predicted that masting, by enhancing seed predator satiation, could in turn strengthen positive selection by seed predators for larger cone output. For this we collected six‐year data (spanning one mast year and five non‐mast years) on seed cone production and seed cone predation rates in a forest genetic trial composed by 116 P. pinaster genotypes.
• Following our prediction, we found stronger seed predator satiation during the masting year, which in turn led to stronger seed predator selection for increased cone production relative to non‐masting years.
• These findings provide evidence that masting can alter the evolutionary outcome of plant‐seed predator interactions. More broadly, our findings highlight that changes in consumer responses to resource abundance represent a widespread mechanism for predicting and understanding context dependency in plant‐consumer evolutionary dynamics.

     

Seed survival on experimental dishes in a central European old‐growth mixed‐species forest – effects of predator guilds,tree masting and small mammal population dynamics

Predation of tree seeds can be a major factor structuring plant communities. We present a three year study on tree seed survival on experimental dishes in an old‐growth forest in central Europe in Austria. We addressed species specific, spatial and temporal aspects of post‐dispersal seed predation. Seeds of Norway spruce Picea abies, European beech Fagus sylvatica, and silver fir Abies alba were exposed on dishes in different types of exclosures which allowed access only to specific guilds of seed predators. Removal experiments were carried out in two old‐growth forests and a managed forest (macro‐sites), including micro‐sites with and without cover of ground vegetation. We conducted the experiment in three consecutive years with a mast year of beech and spruce before the first year of the study. The seed removal experiments were combined with live trapping of small mammals being potential seed predators. Our experiments showed a distinctly different impact of different predator guilds on seed survival on the dishes with highest removal rates of seeds from dishes accessible for small mammals. We observed differing preferences of small mammals for the different tree species. Seed survival in different macro‐ and micro‐habitats were highly variable with lower seed survival in old growth forests. In contrast to our assumption, and in contrast to the satiation hypothesis which assumes higher seed survival in and directly after mast years, seed survival was lower in the year following the mast year of beech when a population peak of small mammals occurred and higher in intermast periods when subsequently small mammal population crashed. This suggests a higher importance of sporadic masting shortly after mast years in intermast periods for establishment of forest trees provided that pollination efficiency is high enough in such years. Combined with the high seed mortality observed after the mast year, this corroborates the important role of seed predation for forest dynamics. An altered synchrony or asynchrony of masting of different tree species and changed masting frequencies through climate change may thus lead to strong and non‐linear effects on forest dynamics.     

土壤种子库的结构与动态

土壤种子库的结构与动态班勇（中国林业科学院林业研究所,北京１０００９１）ＳｔｒｕｃｔｕｒｅａｎｄＤｙｎａｍｉｃｓｏｆＳｅｅｄｓＢａｎｋｓｉｎＳｏｉｌ．￥ＢａｎＹｏｎｇ（ＲｅｓｅａｒｃｈＩｎｓｔｉｔｕｔｅｏｆＦｏｒｅｓｔｒｙ,ＣｈｉｎｅｓｅＡｃａｄｅｍ...     

Density-dependent effects on physical condition and reproduction in North American elk: an experimental test

Density dependence plays a key role in life-history characteristics and population ecology of large, herbivorous mammals. We designed a manipulative experiment to test hypotheses relating effects of density-dependent mechanisms on physical condition and fecundity of North American elk (Cervus elaphus) by creating populations at low and high density. We hypothesized that if density-dependent effects were manifested principally through intraspecific competition, body condition and fecundity of females would be lower in an area of high population density than in a low-density area. Thus, we collected data on physical condition and rates of pregnancy in each experimental population. Our manipulative experiment indicated that density-dependent feedbacks affected physical condition and reproduction of adult female elk. Age-specific pregnancy rates were lower in the high-density area, although there were no differences in pregnancy of yearlings or in age at peak reproduction between areas. Age-specific rates of pregnancy began to diverge at 2 years of age between the two populations and peaked at 6 years old. Pregnancy rates were most affected by body condition and mass, although successful reproduction the previous year also reduced pregnancy rates during the current year. Our results indicated that while holding effects of winter constant, density-dependent mechanisms had a much greater effect on physical condition and fecundity than density-independent factors (e.g., precipitation and temperature). Moreover, our results demonstrated effects of differing nutrition resulting from population density during summer on body condition and reproduction. Thus, summer is a critical period for accumulation of body stores to buffer animals against winter; more emphasis should be placed on the role of spring and summer nutrition on population regulation in large, northern herbivores.     

The storage effect due to frequency-dependent predation in multispecies plant communities

Frequency-dependent seed predation (FDP) has been shown to be a powerful coexistence mechanism in models of annual plant communities. However, FDP undermines the competition-based coexistence mechanism called the storage effect (SEc), which relies on temporal environmental fluctuations that drive fluctuations in competition. Although environmental fluctuations also drive fluctuations in predation, a storage effect due to predation (SEp) may not arise due to a time lag between a change in the environment and the resulting change in the predation rate. Here we show how SEp can arise with multispecies FDP, and in a two-species setting with density-dependent frequency-dependence, partially compensating for the reduction in SEc, in the presence of predation. These outcomes occur when predatory behavior is flexible, and can accommodate to changes in prey abundances on a within-year time scale, leading to changes in predator preferences in response to prey abundances in a given year. When predator preferences are determined by average prey abundances over several years, FDP is still a strong coexistence mechanism but undermines SEc without creating SEp.     

Processes organizing open-nesting bird assemblages: competition or nest predation?

Summary The addition of nest predation as a major process to current theories of space utilization and coexistence of open-nesting bird species adds predictive power to hypotheses of resource partitioning and organization of species assemblages. Nest predation can influence the organization of assemblages if predators respond to nests in a density-dependent manner and if predators specialize on nest types. Evidence shows that nest predation is commonly density-dependent and that predators can specialize on nest types. Consequently, nest predation can select for coexistence of bird species that nest at different heights and in different microhabitats (i.e. partitioning of nesting space) to minimize density-dependent responses of predators to the accumulating densities of species within similar nest sites. I establish a series of predicted patterns (1) to test whether predation is operating to influence partitioning of space and coexistence of species, (2) to distinguish effects of nest predation from competition, and (3) to determine the mechanism by which nest predation acts to organize assemblages. Using published and unpublished data to test the predictions, nest predation is seen as a process that we can no longer afford to ignore.     

What makes a good neighborhood? Interaction of spatial scale and fruit density in the predator satiation dynamics of a masting juniper tree

Spatio-temporal variability in fruit production (masting) has been regarded as a key mechanism to increase plant fitness by reducing seed predation. However, considerably more effort has been devoted into understanding the consequences of temporal rather than spatial variations in fruit crop for plant fitness. In order to simultaneously evaluate both components, we quantify fruit production and pre-dispersal damage by three arthropod species (mites, chalcid wasps and moths) in the Spanish juniper (Juniperus thurifera) during 3 years in a spatially explicit context. Our aims were to assess (1) the interaction between fruit production and pre-dispersal fruit damage by arthropods, (2) the potential interference or competition between arthropods, and (3) the form of the phenotypic selection exerted by arthropods on fruit traits considering the spatial context. Arthropods damaged a substantial fraction of fruits produced by Spanish juniper with levels of damage showing sharp inter-annual variations. Fruit damage by mites was negatively related to yearly fruit crop and positively correlated at individual trees fruiting in consecutive years. Increased interspecific interference was an additional consequence of reduced fruit availability during small crop years. During a masting year, fruit damage by less mobile species such as mites was negatively affected by tree crop size, and no spatial structure was observed for mite damage. The incidence of chalcid wasps was low, so the spatial pattern of seed predation was unclear, and no preferences for fruit or seed traits were detected. Conversely, moths selected larger fruits and their incidence on trees was spatially aggregated up to 20 m, with predation levels being negatively affected by fruit abundance at the patch level, suggesting a positive density-dependent effect of neighbors on fruit output. These results highlight the importance of including the spatial component to understand complex species interactions at local scales.     

Rodent seed predation: effects on seed survival, recruitment, abundance, and dispersion of bird-dispersed tropical trees

Tropical tree species vary widely in their pattern of spatial dispersion. We focus on how seed predation may modify seed deposition patterns and affect the abundance and dispersion of adult trees in a tropical forest in India. Using plots across a range of seed densities, we examined whether seed predation levels by terrestrial rodents varied across six large-seeded, bird-dispersed tree species. Since inter-specific variation in density-dependent seed mortality may have downstream effects on recruitment and adult tree stages, we determined recruitment patterns close to and away from parent trees, along with adult tree abundance and dispersion patterns. Four species (Canarium resiniferum, Dysoxylum binectariferum, Horsfieldia kingii, and Prunus ceylanica) showed high predation levels (78.5-98.7%) and increased mortality with increasing seed density, while two species, Chisocheton cumingianus and Polyalthia simiarum, showed significantly lower seed predation levels and weak density-dependent mortality. The latter two species also had the highest recruitment near parent trees, with most abundant and aggregated adults. The four species that had high seed mortality had low recruitment under parent trees, were rare, and had more spaced adult tree dispersion. Biotic dispersal may be vital for species that suffer density-dependent mortality factors under parent trees. In tropical forests where large vertebrate seed dispersers but not seed predators are hunted, differences in seed vulnerability to rodent seed predation and density-dependent mortality can affect forest structure and composition.     

Seasonal variation in the seed bank of a Patagonian grassland in relation to grazing and topography

Abstract. The germinable seed bank of Festuca spp., Carex patagonica, and other annuals and perennials in a semiarid Patagonian grassland was analyzed every three months. The effects of grazing, topography and microsites with respect to established grass tussocks on the germinable-seed bank were also analyzed. The total germinable-seed bank was larger in summer after seed rain. At this time of the year most of the seeds were from annuals and perennial dicots. Seeds of the dominant Festuca spp. were the main components of the graminoid seed bank, which was homogeneously distributed in patches of bare soil. In spring, i.e. some months after the seed rain, the germinable-seed bank of most of the species was greatly reduced, while the seed bank of Carex patagonica did not change significantly. At this time of the year, the graminoid seed bank was heterogeneously distributed in space, with the seeds accumulating in wind-protected microsites. In the grazing treatments, the seed bank of the perennial grasses was reduced proportionally to the decrease of the plant cover. On the other hand, the germinable-seed bank of C. patagonica increased with the grazing treatments, in relation to the increase of vegetation cover. Topographical position had two types of effect on the seed bank of perennial grasses. One was the increase of the germinable-seed bank, after the seed rain, on the relatively warmer northeast facing slopes, which was related to a higher seed rain in these places. The other was an increased seed loss on slopes. The different seed-bank strategies observed in this grassland are compared and discussed in relation to strategies described for other grasslands.     

Seedling establishment in a masting desert shrub parallels the pattern for forest trees

The masting phenomenon along with its accompanying suite of seedling adaptive traits has been well studied in forest trees but has rarely been examined in desert shrubs. Blackbrush (Coleogyne ramosissima) is a regionally dominant North American desert shrub whose seeds are produced in mast events and scatter-hoarded by rodents. We followed the fate of seedlings in intact stands vs. small-scale disturbances at four contrasting sites for nine growing seasons following emergence after a mast year. The primary cause of first-year mortality was post-emergence cache excavation and seedling predation, with contrasting impacts at sites with different heteromyid rodent seed predators. Long-term establishment patterns were strongly affected by rodent activity in the weeks following emergence. Survivorship curves generally showed decreased mortality risk with age but differed among sites even after the first year. There were no detectable effects of inter-annual precipitation variability or site climatic differences on survival. Intraspecific competition from conspecific adults had strong impacts on survival and growth, both of which were higher on small-scale disturbances, but similar in openings and under shrub crowns in intact stands. This suggests that adult plants preempted soil resources in the interspaces. Aside from effects on seedling predation, there was little evidence for facilitation or interference beneath adult plant crowns. Plants in intact stands were still small and clearly juvenile after nine years, showing that blackbrush forms cohorts of suppressed plants similar to the seedling banks of closed forests. Seedling banks function in the absence of a persistent seed bank in replacement after adult plant death (gap formation), which is temporally uncoupled from masting and associated recruitment events. This study demonstrates that the seedling establishment syndrome associated with masting has evolved in desert shrublands as well as in forests.