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.     

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.     

Measuring mast seeding behavior: relationships among population variation,individual variation and synchrony

Mast seeding, or masting, is the variable production of flowers, seeds, or fruit across years more or less synchronously by individuals within a population. A critical issue is the extent to which temporal variation in seed production over a collection of individuals can be viewed as arising from a combination of individual variation and synchrony among individuals. Studies of masting typically quantify such variation in terms of the coefficient of variation (CV). In this paper we examine mathematically how the population CV relates to the mean individual CV and synchrony, concluding that the relationship is a complex one which cannot isolate an overall measure of synchrony, and involves additional factors, principally the number of plants sampled and the mean productivity per plant. Our development suggests some simple approximate relationships of population CV to individual variability, synchrony and the number of individuals. These were found to fit quite well when applied to data from 59 studies which included seed production at the individual level.     

Testing the resource‐matching hypothesis in the mast seeding tree Nothofagus truncata (Fagaceae)

Abstract: The genus Nothofagus in New Zealand and Australia exhibits strong mast seeding (i.e. highly variable seed crops between years). Seed crop variation is synchronized within and between species over large spatial scales, and results in greatly increased wind pollination efficiency which could provide a selective benefit favouring the maintenance of mast seeding. However, the null hypothesis (that plants simply match their reproductive effort to the variable resources available each year) has not been tested in Nothofagus. Here we use a 33‐year dataset on seedfall and wood ring increments for 19 individual Nothofagus truncata trees at Orongorongo, New Zealand, to test for the presence of switching (exaggeration of seedfall variability by diverting resources into, then out of, reproduction). A generalized least squares model explained 40.7% of the variance in standardized ring widths, using six weather variables (absolute minimum temperatures in March (lag 0) April (lag 0 and lag 1), May (lag 0) and rainfall in November and February (lag 0) ) and seedfall. Seedfall had a negative relationship with the current year's ring widths even after controlling for all significant weather variables. This shows that switching is occurring in N. truncata within individuals among years, and therefore that masting in this species is the result of selective forces such as increased wind pollination efficiency. As this result has been demonstrated for very few masting species, we call for this test to be applied more widely.     

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.     

Pollen limitation as a main driver of fruiting dynamics in oak populations

In many perennial wind‐pollinated plants, the dynamics of seed production is commonly known to be highly fluctuating from year to year and synchronised among individuals within populations. The proximate causes of such seeding dynamics, called masting, are still poorly understood in oak species that are widespread in the northern hemisphere, and whose fruiting dynamics dramatically impacts forest regeneration and biodiversity. Combining long‐term surveys of oak airborne pollen amount and acorn production over large‐scale field networks in temperate areas, and a mechanistic modelling approach, we found that the pollen dynamics is the key driver of oak masting. Mechanisms at play involved both internal resource allocation to pollen production synchronised among trees and spring weather conditions affecting the amount of airborne pollen available for reproduction. The sensitivity of airborne pollen to weather conditions might make oak masting and its ecological consequences highly sensitive to climate change.     

Why men matter: mating patterns drive evolution of human lifespan

Evolutionary theory predicts that senescence, a decline in survival rates with age, is the consequence of stronger selection on alleles that affect fertility or mortality earlier rather than later in life. Hamilton quantified this argument by showing that a rare mutation reducing survival is opposed by a selective force that declines with age over reproductive life. He used a female-only demographic model, predicting that female menopause at age ca. 50 yrs should be followed by a sharp increase in mortality, a "wall of death." Human lives obviously do not display such a wall. Explanations of the evolution of lifespan beyond the age of female menopause have proven difficult to describe as explicit genetic models. Here we argue that the inclusion of males and mating patterns extends Hamilton's theory and predicts the pattern of human senescence. We analyze a general two-sex model to show that selection favors survival for as long as men reproduce. Male fertility can only result from matings with fertile females, and we present a range of data showing that males much older than 50 yrs have substantial realized fertility through matings with younger females, a pattern that was likely typical among early humans. Thus old-age male fertility provides a selective force against autosomal deleterious mutations at ages far past female menopause with no sharp upper age limit, eliminating the wall of death. Our findings illustrate the evolutionary importance of males and mating preferences, and show that one-sex demographic models are insufficient to describe the forces that shape human senescence.     

Dynamics of internal carbon resources during masting behavior in trees

Several proximate factors of masting have been provided. Here, I focus on the role of internal factors, especially the relationship between internal carbon resources and modular structures in trees. I summarize various studies of carbon resource allocation for reproduction during masting events in terms of the proximate factors of masting and discuss the modular structure in which trees accumulate and consume carbon resources as well as the timing when internal carbon resources affect masting since trees have complex resource dynamics among organs. The resource budget model, which provides a simple mechanistic explanation of the masting mechanism, is supported by various study lines. This model assumes decreasing levels of stored photosynthate after flowering and fruiting. According to several studies, however, carbon reserves do not decrease after fruiting in species in which the modules autonomously allocate current photosynthate for fruiting. In addition, it is important to elucidate when carbon resources affect masting events because during their long developmental processes, trees pass through various stages until they produce maturing fruits to create successful masting events. To explore the mechanisms of masting in future studies, it would be important to figure out how and when candidate factors (including nutrients other than carbon) may influence the entire reproduction process, for example, using field manipulation experiments.     

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.     

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.     

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.     

Social structure and winter survival in acorn ants

Fluctuating selection is a major theme in the evolutionary and ecological literature, yet attempts to measure how differential selection across time or space affects long-term change in life history traits or behaviors are still rare. Social evolution among the insects has been broadly studied with respect to how key parameters such as queen number and relatedness vary to influence colony fitness. However, a primary focus on fertility selection in the warm months must be complemented by parallel investigations on survivorship selection during the cold months. Here we provide the first assessment of social structure and overwintering survivorship in the field. We studied the acorn ant, which stays aboveground throughout the cold winters in North America, by varying queen number and colony size over two consecutive winters. We found that winter survival was quite low but unconnected to variable colony structure. Therefore previous studies on how social structure affects fertility selection in acorn ants have not been confounded by countervailing selection during the cold months. Our data support the assumption of the larger literature that selective forces molding social behavior in ants act primarily on fertility selection during the reproductive season.     

Disruptive viability selection on adult exploratory behaviour in eastern chipmunks

Heterogeneous forces of selection associated with fluctuating environments are recognized as important factors involved in the maintenance of inter‐individual phenotypic variance within populations. Consistent behavioural differences over time and across situations (e.g. personality) are increasingly cited as examples of individual variation observed within populations. However, the suggestion that heterogeneous selective pressures target different animal personalities remains largely untested in the wild. In this 5‐year study, we investigated the dynamics of viability selection on a personality trait, exploration, in a population of eastern chipmunks (Tamias striatus) experiencing substantial seasonal variations in weather conditions and food availability associated with masting trees. Contrary to our expectations, we found no evidence of fluctuating selection on exploration. Instead, we found strong disruptive viability selection on adult exploration behaviour, independent of seasonal variations. Individuals with either low or high exploration scores were almost twice as likely to survive over a 6‐month period compared with individuals with intermediate scores. We found no evidence of viability selection on juvenile exploration. Our results highlight that disruptive selection might play an important role in the maintenance of phenotypic variance of wild populations through its effect on different personality types across temporally varying environmental conditions.     

Geographical variation in the spatial synchrony of a forest-defoliating insect: isolation of environmental and spatial drivers

Despite the pervasiveness of spatial synchrony of population fluctuations in virtually every taxon, it remains difficult to disentangle its underlying mechanisms, such as environmental perturbations and dispersal. We used multiple regression of distance matrices (MRMs) to statistically partition the importance of several factors potentially synchronizing the dynamics of the gypsy moth, an invasive species in North America, exhibiting outbreaks that are partially synchronized over long distances (approx. 900 km). The factors considered in the MRM were synchrony in weather conditions, spatial proximity and forest-type similarity. We found that the most likely driver of outbreak synchrony is synchronous precipitation. Proximity played no apparent role in influencing outbreak synchrony after accounting for precipitation, suggesting dispersal does not drive outbreak synchrony. Because a previous modelling study indicated weather might indirectly synchronize outbreaks through synchronization of oak masting and generalist predators that feed upon acorns, we also examined the influence of weather and proximity on synchrony of acorn production. As we found for outbreak synchrony, synchrony in oak masting increased with synchrony in precipitation, though it also increased with proximity. We conclude that precipitation could synchronize gypsy moth populations directly, as in a Moran effect, or indirectly, through effects on oak masting, generalist predators or diseases.     

Fertility of exceptional bisexual individuals in four dioecious plant species

Exceptional, very rare, bisexual (hermaphroditic or monoecious) individuals have been detected in strictly dioecious populations of Rhamnus alaternus, R. palaestinus, Bryonia syriaca and Populus euphratica (a single individual in each species). While ordinary male plants in each species exhibited fully normal pollen, and female individuals set a considerable amount of fruit, the exceptional bisexual plants showed a reduction in male or female fertility, or both. This inability of the rare bisexual individuals to fully invest in the two genders suggests that trade-offs between male and female functions possibly play a major role in the breeding systems of these dioecious species, and probably implicates resource allocation (among other factors) as a selective force in the evolution of dioecy. Received: 5 April 1999 / Revision accepted: 30 June 1999     

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.     

Nitrogen storage dynamics are affected by masting events in Fagus crenata

It is generally assumed that the production of a large crop of seeds depletes stores of resources and that these take more than 1 year to replenish; this is accepted, theoretically, as the proximate mechanism of mast seeding (resource budget model). However, direct evidence of resource depletion in masting trees is very rare. Here, we trace seasonal and inter-annual variations in nitrogen (N) concentration and estimate the N storage pool of individuals after full masting of Fagus crenata in two stands. In 2005, a full masting year, the amount of N in fruit litter represented half of the N present in mature leaves in an old stand (age 190–260 years), and was about equivalent to the amount of N in mature leaves in a younger stand (age 83–84 years). Due to this additional burden, both tissue N concentration and individual N storage decreased in 2006; this was followed by significant replenishment in 2007, although a substantial N store remained even after full masting. These results indicate that internal storage may be important and that N may be the limiting factor for fruiting. In the 4 years following full masting, the old stand experienced two moderate masting events separated by 2 years, whilst trees in the younger stand did not fruit. This different fruiting behavior may be related to different “costs of reproduction” in the full masting year 2005, thus providing more evidence that N may limit fruiting. Compared to the non-fruiting stand, individuals in the fruiting stand exhibited an additional increase in N concentrations in roots early in the 2007 growing season, suggesting additional N uptake from the soil to supply resource demand. The enhanced uptake may alleviate the N storage depletion observed in the full masting year. This study suggests that masting affects N cycle dynamics in mature Fagus crenata and N may be one factor limiting fruiting.     

Flammability and serotiny as strategies: correlated evolution in pines

Fire may act as a selective force on plants both through its direct effects by killing or wounding susceptible individuals and through its effect on the environment: the post-fire environment may select specific physiological traits or life histories. We used phylogenetic independent contrasts to test the hypothesis that fire has selected for correlated evolution among alternative suites of traits in pines: a survival/avoidance suite characterized by thick bark, height, and self-pruning of dead branches; and a fire-embracing strategy in which plants invest little into survival, exhibit traits which enhance flammability, and use fire as a means to cue seedling establishment to the post-fire environment through serotinous cones. We created a set of alternative 'supertree' phylogenies for the genus Pinus from published sources. Using these alternative phylogenies, published ecological data for 38 pine species, and newly collected morphological data, we demonstrate that much variation in trait evolution occurs along a fire-surviving/fire-embracing axis. Pines vary in their susceptibility to ignition since a tree that retains dead branches is more likely to carry a fire into the canopy than a tree that self-prunes. The evolution of increased flammability may have altered evolutionary trajectories prompting an evolutionary switch from a fire-surviving to a fire-embracing life history. Alternatively, the fire-embracing strategy may in fact select for increased flammability to ensure canopy ignition and the realization of serotinous seed-release.     

Mutual benefit can promote the evolution of preferential interactions and in this way can lead to the evolution of true altruism

We analyse the evolution of the assortment of encounters through active choice of companions among individuals that interact cooperatively in a situation of mutual benefit. Using a simple mathematical model, we show that mutual benefit can favour the evolution of a preference to interact with individuals that are similar to themselves with respect to an arbitrary tag even when both the preference and the tag depend on two independent and unlinked genes. Two necessary requisites to obtain this result are: (i) a small population or a large subdivided metapulation and (ii) an asymmetry between partners in such a way that one of them (donor) proposes the cooperation and elects the partner, whereas the other (receiver) never rejects the offer. We also show that mutual benefit can be the starting point for the evolution of altruistic behaviours as long as there are preferential interactions. This requires that the tag used in the election of partners is the altruistic or selfish behaviour itself.     

Population and individual level of masting in a fleshy-fruited tree

Masting is usually considered as a population phenomenon but it results from individuals?? reproductive patterns. Studies of individual patterns of seed production and their synchrony are essential to an understanding of the mechanisms of masting. The aim of this study was to find the relationship between population and individual levels of masting. We examined individuals?? contribution to masting, considering their endogenous cycles, interannual variability and associated weather cues, as well as inter-individual synchrony of fruit production. We studied masting of Sorbus aucuparia L., which in Europe is one of the most common trees bearing fleshy fruits and is strongly affected by a specialized seed predator. The data are 11-year measurements of fruit production of 250 individuals distributed on a 27-ha area of subalpine forest in the Western Carpathians (Poland). Population- and individual-level interannual variability of fruit production was moderate. Synchrony among individuals was relatively high for all years, but the trees were much less synchronized in heavy crop years than in years of low fruit production. Weak synchrony among trees for heavy production years suggests that the predator satiation hypothesis does not explain the observed masting behavior. Fruit production, both at individual and at population level, was highly correlated with weather conditions. However, the presence of masting cannot be fully explained by the resource-matching hypothesis either. We suggest that adverse weather conditions effectively limit fruit production, causing high inter-individual synchrony in low crop years, whereas the unsynchronized heavy crop years seem to have been affected by individually available resources.