Spatial dynamics of specialist seed predators on synchronized and intermittent seed production of host plants

Masting, the synchronized and intermittent seed production by plant populations, provides highly variable food resources for specialist seed predators. Such a reproductive mode helps minimize seed losses through predator satiation and extinction of seed predator populations. The seed predators can buffer the resource variation through dispersal or extended diapause. We developed a spatially explicit resource-consumer model to understand the effect of masting on specialist seed predators. The masting dynamics were assumed to follow a resource-based model for plant reproduction, and the population dynamics of the predator were represented by a spatially extended Nicholson-Bailey model. The resultant model demonstrated that when host plants reproduce intermittently, seed predator populations go locally extinct, but global persistence of the predator is facilitated by dispersal or extended diapause. Global extinction of the predator resulted when the intermittent reproduction is highly synchronized among plants. An approximate invasion criterion for the predators showed that negative lag-1 autocorrelation in seeding reduces invasibility, and positive lag-1 cross-correlation enhances invasibility. Spatial synchronization in seeding at local scale caused by pollen coupling (or climate forcing) further prevented invasion of the predators. If the predators employed extended diapause, extremely high temporal variability in reproduction was required for plants to evade the predators.     

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.     

Masting,seed dispersal and seed predation in the cycad Macrozamia communis

Summary Little is known about the adaptive value of mast seeding, a common phenomenon in temperate trees and shrubs. Masting is likely to affect both seed dispersal and seed predation. In systems where similar taxa of animals are involved in these two processes, the consequences of mast seeding are likely to be particularly complicated. This study examined the effects of mast seeding in a cycad, Macrozamia communis, on the dispersal of seeds, the pattern of dispersion of seeds and post-dispersal predation on seeds. Dispersal of seeds by possums was poorer from source plants in a masting population than from source plants in an adjacent, non-masting population. This resulted in fewer seeds per seeding female plant in the masting plot being dispersed to favourable sites. We conclude that this is caused by the feeding behaviour and movements of possums in the masting site. The abundance of seeds in this site did not satiate the post-dispersal predators, native rats. In fact, more seeds in this site were eaten than in the nonmasting site. We suggest that the mast seeding observed in M. communis may not be adaptive, but is more likely a consequence of other factors which synchromize flowering within local 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.

     

Empirical models of pollen limitation, resource acquisition, and mast seeding by a bee-pollinated wildflower

Synchronous mast seeding is increasingly recognized as common in plant populations. Recent theoretical models show that synchronous mast seeding could be a consequence of resource allocation and storage within individual plants, coupled by pollen limitation in low-flowering years. We used long-term population and weather data to parameterize models of flowering based on stored resources and pollen limitation in Astragalus scaphoides, a bee-pollinated plant that flowers in alternate years. We used these models to test whether internal resource dynamics could explain mast seeding in A. scaphoides and, if so, whether synchrony was caused by pollen limitation and/or fluctuations in precipitation. We compared predictions of models that included all combinations of three factors: constant versus precipitation-dependent resource gain, uniform versus heterogeneous resource gain (among individual plants), and resource-dependent versus resource- and pollen-limited fruit set. Pollen limitation and heterogeneous resource gain were necessary and sufficient to explain alternate-year flowering, but precipitation increased the quantitative match between model predictions and flowering dynamics. Together, our results support the importance of density-dependent pollen limitation as an ultimate and proximate cause of mast seeding in A. scaphoides. Precipitation does not act as a direct cue for synchrony in this species but might affect long-term resource gain and fruiting dynamics.     

Masting uncoupling: mast seeding does not follow all mast flowering episodes in a dioecious juniper tree

Evolutionary selective forces, like predator satiation and pollination efficiency, are acknowledged to be major causes of masting (the variable, periodic and synchronic production of seeds in a population). However, a number of recent studies indicate that resources might also play an important role on shaping masting patterns. Dioecious masting species offer a privileged framework to study the role of resources on masting variation, since male and female plants often experience different reproductive costs and selective pressures. We followed masting and reproductive investment (RI) of the dioecious tree Juniperus thurifera in two populations along 10 years and studied the different response of males and females to experimentally increased water and nutrient availability in a third population. Juniperus thurifera females invested in reproduction three times more resources than males. Such disparity generated different resource‐use strategies in male and female trees. Tree‐ring growth and water use efficiency (WUE) confirmed that sexes differed in their resource investment temporal pattern, with males using current resources for reproduction and females using resources accumulated during longer periods. Watered and fertilized female trees presented significantly higher flowering reproductive investments than males and experienced an extraordinary mast‐flowering event. However, seeding RI and mast seeding were not affected by the treatment. This suggests that although resource availability affects the reproductive output of this species, there are other major forces regulating masting on J. thurifera. During 10 years, J. thurifera male and female trees presented high and low flowering years more or less synchronously. However, not all mast flowering episodes resulted in mast seeding, leading to masting uncoupling between flowering and seeding. Since flowering costs represent only 1% of females’ total reproductive investments, masting uncoupling could be a beneficial bet‐hedging strategy to maximize reproductive output in spite of unpredictable catastrophic events.     

Modeling spatial dynamics of episodic and synchronous reproduction by plant populations: the effect of small-scale pollen coupling and large-scale climate

Many plant species show masting, intermittent and synchronized reproduction at population level. In the present paper, we review the resource-based model providing a theoretically plausible physiological mechanism underlying masting. In the model, a non-linear allocation of energy reserves is considered: plants accumulate photosynthate every year, produce flowers when the energy reserve level exceeds a threshold, and set seeds at a rate limited by pollen availability. The model predicted that individual plants alter their reproductive dynamics from annual to intermittent depending on how heavily the plant invests resource in reproduction. When fruit production is limited by the availability of outcross pollen, a plant population showed diverse reproductive behavior such as completely synchronized or desynchronized reproduction. Spatial scale of reproductive synchrony tended to be a few times larger than the range of direct pollen exchange. Impact of climatic fluctuation correlated at a large spatial scale was also investigated as an alternative synchronizing factor. The variation in annual productivity and the reproductive threshold induced from climatic fluctuation was accounted for by incorporating an additional term in the model. When plants show a 2 year reproductive cycle, highly synchronized reproduction at a regional scale was induced due to correlated environmental forcing, but reproductive synchrony with long intermast periods was realized only when pollen coupling and environmental forcing were at work. These results suggest that distance-dependent processes, such as pollen exchange between nearby trees, induce synchrony at a local scale and external environmental forcing correlated at geographically large scales works to strengthen and maintain such a synchrony.     

Evolutionary ecology of mast-seeding in temperate and tropical oaks (Quercus spp.)

Mast-seeding is the synchronous production of large seed crops within a population or community of species every two or more years. This paper addresses three non-mutually exclusive hypotheses explaining the evolution of mast-seeding in temperate tree species, especially the genus Quercus: (1) mast-seeding is a consequence of mast-flowering which evolves to increased pollination efficiency in mast-flowering years; (2) mast-seeding has evolved as an anti-predator adaptation by which large seed crops during mast years satiate the seed predators and allow survival of some of the seeds; (3) selection on seed size by habitat can indirectly affect the evolution of masting if trees with large seeds require more time to accumulate reserves to mature those seeds. I find support for the pollination hypothesis in several wind-pollinated temperate tree species but not oaks. However, oaks show evidence favoring the predation and seed size hypotheses. I then develop a model to illustrate the relationships among the three hypotheses in their effects on the evolution of masting. Finally, using data from herbaria and Floras, the influence of selection via flowering, fruiting, and seed size in the evolution of masting in tropical oaks is discussed. I conclude that the need for a supra-annual cue to synchronize flowering and fruiting as well as the larger seed size found in many tropical oak species should contribute to the evolution of masting to a greater extent than seen among temperate oaks.     

The evolutionary ecology of mast seeding in trees

The hypothesis that masting by trees is a defensive strategy which satiates seed predators in mast years and starves them in the intervening periods is tested in 59 sets of data on the seed production and pre-dispersal seed-predation of 25 tree species. Twenty-lour of the 59 data-sets support the hypothesis and show a statistically significant positive relationship between the proportion of seeds surviving the pre-dispersal stage and the log₁₀ of the crop size for the same year. Evidence that pre-dispersal seed survival increases with the length of the mast interval is poor.
A positive relationship between the strength of the masting habit and the maxintum observed pre-dispersal seed mortality in a sample of 15 tree species suggests that the masting habit is best developed in predator-prone species. A survey of seed crop frequencies in the woody plant flora of Nortli America shows masting species to be under-represented amongst shrubs and amongst trees which disperse their seeds in fleshy dispersal units. The selection pressures and evolutionary constraints which operate on the evolution of masting plants and their seed predators are discussed.     

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.     

The evolutionary ecology of masting: does the environmental prediction hypothesis also have a role in mesic temperate forests?

The evolutionary advantages of mast seeding in mesic temperate forests are reviewed with reference to the whole plants lifecycle. The aim of this article is to give attention to the environmental prediction hypothesis as an evolutionary aspect of closed-forest dynamics that need to be tested in field studies and modelling. It is suggested that the year after a period of water stress (or other suboptimal conditions for growth) trees respond with high seed production. Due to an understory environment favorable for prolific establishment of seedlings (i.e., more light at the forest floor) this may give rise to a pulse of regeneration. Thus, understanding masting may require a multi-faceted approach including the study of the ecology of the trees themselves beyond pollination and seed predation, and including gap ecology and patch dynamics with special attention to patterns of forest regeneration.     

Intra- and inter-specific effects of mast seeding on seed fates of two sympatric <Emphasis Type="Italic">Corylus</Emphasis> species

We released seeds of two sympatric tree species, Corylus mandshurica (seed with thinner seed hull, higher nutrition) and C. heterophylla (seeds with thicker seed hull, lower nutrition) in the masting year of C. mandshurica in 2008, and C. heterophylla in 2009, respectively, to investigate how seed masting of the two sympatric Corylus species affects seed removal and dispersal fitness of the two species differently at both intra- and inter-specific levels. At intra-specific level, the authors found mast seeding of both C. mandshurica and C. heterophylla significantly reduced seed removal, seed consumption, but increased seed dispersal distance and seed dispersal fitness of the released seeds. Mast seeding of C. mandshurica increased seed caching of C. mandshurica. At inter-specific level, the authors found mast seeding of C. mandshurica reduced seed removal of C. heterophylla, but mast seeding of C. heterophylla did not significantly reduce seed removal of C. mandshurica. Mast seeding of C. mandshurica reduced seed consumption of C. heterophylla, while mast seeding of C. heterophylla reduced seed consumption of C. mandshurica. We found mast seeding of C. mandshurica significantly reduced seed dispersal distance of C. heterophylla, while mast seeding of C. heterophylla significantly increased seed dispersal distance of C. mandshurica. We found that mast seeding of C. mandshurica significantly increased seed dispersal fitness of C. heterophylla, while mast seeding of C. heterophylla did not significantly increase seed dispersal fitness of C. mandshurica. More studies are needed to reveal the ecological consequences of mast seeding at inter-specific or community-level. Seed traits may attribute the differences of mast seeding at inter-specific level. Because seeds with thinner seed hull and higher nutrition were more harvested and eaten by rodents, mast seeding of C. mandshurica might have reduced seed removal and seed consumption, but increased dispersal fitness of C. heterophylla (seeds with thicker seed hull, lower nutrition). Therefore, synchrony among species is, or is not, selectively beneficial to the focus species depends on seed traits which determine gains from mast seeding at inter-specific level.     

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

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

Effect of climate change on mast-seeding species: frequency of mass flowering and escape from specialist insect seed predators

Global surface temperatures are expected to increase by several degrees in the next century, with potentially large but poorly understood impacts on ecological interactions. Here we propose potential effects of increased temperatures on ecologically dominant New Zealand grasses (Chionochloa spp.) that mass flower and mast seed. Twenty-two years’ data from five masting Chionochloa species in New Zealand showed that the cue for heavy flowering was unusually high temperature in the summer of the year before flowering. Attack by predispersal insect seed predators was much reduced in mast years, apparently because predator populations were satiated. Increased temperatures would greatly decrease interannual variation in Chionochloa flowering, allowing seed predator populations to increase and potentially to devastate the seed crop annually. Similar responses are likely in masting species worldwide. This previously unrecognized effect of global warming could have widespread impacts on temperate ecosystems.     

Disease resistance in Arabidopsisthaliana increases the competitive ability and the predicted probability of long‐term ecological success under disease pressure

Evidence is mounting that flowering by the mast-fruiting Dipterocarpaceae in Southeast Asia is triggered by ENSO events such that seeds are dispersed at the end of ENSO droughts. These droughts induce substantial defoliation and mortality of canopy trees, producing a favorable environment for seedling recruitment in the forest understory. Therefore, seedling release following droughts may have selected for synchronized, supra-annual fruiting in these rain forests. Currently, mast fruiting in Southeast Asia is generally regarded as an evolutionary response to seed predation by nomadic vertebrates. Separating the two causes for mast fruiting, seedling release and predator satiation, may be difficult if they are coupled in nature by ENSO droughts. Nevertheless, if the cue for masting is environmental, then the post-ENSO seedling environment should be considered a potential cause for masting, and if it operates in conjunction with predator satiation, then it may have provided the initial stimulus for supra-annual synchrony in fruiting.     

Parameterisation and validation of a resource budget model for masting using spatiotemporal flowering data of individual trees

Synchronised and fluctuating reproduction by plant populations, called masting, is widespread in diverse taxonomic groups. Here, we propose a new method to explore the proximate mechanism of masting by combining spatiotemporal flowering data, biochemical analysis of resource allocation and mathematical modelling. Flowering data of 170 trees over 13 years showed the emergence of clustering with trees in a given cluster mutually synchronised in reproduction, which was successfully explained by resource budget models. Analysis of resources invested in the development of reproductive organs showed that parametric values used in the model are significantly different between nitrogen and carbon. Using a fully parameterised model, we showed that the observed flowering pattern is explained only when the interplay between nitrogen dynamics and climatic cues was considered. This result indicates that our approach successfully identified resource type‐specific roles on masting and that the method is suitable for a wide range of plant species.     

Climate variation,reproductive frequency and acorn yield in English Oaks

Aims Annually variable but synchronous production of large seed crops (‘masting’) is a widespread phenomenon in temperate trees. Mounting concerns about the impacts of anthropogenic climate change (ACC) on plant reproduction gives urgency to our need to understand better the role of climate on tree reproduction, and in particular, mast events. Unlike our understanding of reproductive phenology however, there is little consensus regarding how climate affects plant reproductive effort or indeed the actual environmental triggers that underpin masting behaviour.     

Seedling bank dynamics of Fagus grandifolia var. mexicana before and after a mast year in a Mexican cloud forest

Abstract. Fagus grandifolia var. mexicana seedling dynamics were studied in a relict forest inside the crater of a volcano where it is the only canopy tree species. The objectives of the study were (1) to determine changes in seedling density before and after a mast year, as well as to monitor seedling recruitment, mortality and growth rate in relation to the micro‐environment, and (2) to discuss the impact of masting on seedling dynamics of the population. Before masting, seedling density was 8.8 seedlings m^–2, afterwards seedling density peaked at 51.5 seedlings m^–2, then decreased by 50% in 3 months and by 85% after 8 months, down to levels of before the mast year (9.9 seedlings m^–2) after 16 months. Seedlings in the forest floor before the mast‐seeding event showed a low relative growth rate – 0.14 mm mm^–1 mo^–1 against 1.27 mm mm^–1 mo^–1 for seedlings that emerged immediately after masting. Seed germination was high (83%) and rapid (L₅₀= 7 days) following masting. Seedling growth was positively correlated with soil water content but not with temperatures and relative humidity. Data suggested that seed production in mast years is important in maintaining the seedling bank, and thus the viability of relict Fagus populations.     

Direct and indirect effects of masting on rodent populations and tree seed survival

Many plant species are thought to benefit from mast seeding as a result of increased seed survival through predator satiation. However, in communities with many different masting species, lack of synchrony in seed production among species may decrease seed survival by maintaining seed predator populations through the intermast cycle. Similarly, masting by different plant species may have different effects on the seed predator community. We conducted a three-year study in a northeastern USA temperate deciduous forest to determine if production of large seed crops by several tree species was synchronous, and if they had similar effects on all small mammal species. We found that red oak mast crops resulted in increased densities of Peromyscus leucopus and P. maniculatus , but had no effect on Clethrionomys gapperi abundance. Conversely, C. gapperi populations, but not Peromyscus populations, appeared to increase in response to a large red maple seed crop. Differences in small mammal abundance resulted in changes in species-specific seed survival: in the year of abundant C. gapperi , experimentally placed red oak acorns had significantly higher survival than in the year of high Peromyscus abundance. Red oak acorn removal was positively correlated with Peromyscus abundance, while red maple seed removal was significantly higher with increased C. gapperi abundance. Thus, species-specific seed production had differential effects on subsequent small mammal abundance, which in turn affected seed survival. We suggest that at the level of the community, even short-term lack of synchrony in production of large seed crops can cause variation in postdispersal seed survival, through differential effects on the community of small mammal seed predators.