skip to main content
US FlagAn official website of the United States government
dot gov icon
Official websites use .gov
A .gov website belongs to an official government organization in the United States.
https lock icon
Secure .gov websites use HTTPS
A lock ( lock ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites.


Title: Mast seeding promotes evolution of scatter-hoarding
Many plant species worldwide are dispersed by scatter-hoarding granivores: animals that hide seeds in numerous, small caches for future consumption. Yet, the evolution of scatter-hoarding is difficult to explain because undefended caches are at high risk of pilferage. Previous models have attempted to solve this problem by giving cache owners large advantages in cache recovery, by kin selection, or by introducing reciprocal pilferage of ‘shared’ seed resources. However, the role of environmental variability has been so far overlooked in this context. One important form of such variability is masting, which is displayed by many plant species dispersed by scatterhoarders. We use a mathematical model to investigate the influence of masting on the evolution of scatter-hoarding. The model accounts for periodically varying annual seed fall, caching and pilfering behaviour, and the demography of scatterhoarders. The parameter values are based mostly on research on European beech ( Fagus sylvatica ) and yellow-necked mice ( Apodemus flavicollis ). Starvation of scatterhoarders between mast years decreases the population density that enters masting events, which leads to reduced seed pilferage. Satiation of scatterhoarders during mast events lowers the reproductive cost of caching (i.e. the cost of caching for the future rather than using seeds for current reproduction). These reductions promote the evolution of scatter-hoarding behaviour especially when interannual variation in seed fall and the period between masting events are large. This article is part of the theme issue ‘The ecology and evolution of synchronized seed production in plants’.  more » « less
Award ID(s):
1716803
PAR ID:
10326989
Author(s) / Creator(s):
; ; ;
Date Published:
Journal Name:
Philosophical Transactions of the Royal Society B: Biological Sciences
Volume:
376
Issue:
1839
ISSN:
0962-8436
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. null (Ed.)
    Abstract Background and Aims In a range of plant species, the distribution of individual mean fecundity is skewed and dominated by a few highly fecund individuals. Larger plants produce greater seed crops, but the exact nature of the relationship between size and reproductive patterns is poorly understood. This is especially clear in plants that reproduce by exhibiting synchronized quasi-periodic variation in fruit production, a process called masting. Methods We investigated covariation of plant size and fecundity with individual-plant-level masting patterns and seed predation in 12 mast-seeding species: Pinus pinea, Astragalus scaphoides, Sorbus aucuparia, Quercus ilex, Q. humilis, Q. rubra, Q. alba, Q. montana, Chionochloa pallens, C. macra, Celmisia lyallii and Phormium tenax. Key Results Fecundity was non-linearly related to masting patterns. Small and unproductive plants frequently failed to produce any seeds, which elevated their annual variation and decreased synchrony. Above a low fecundity threshold, plants had similar variability and synchrony, regardless of their size and productivity. Conclusions Our study shows that within-species variation in masting patterns is correlated with variation in fecundity, which in turn is related to plant size. Low synchrony of low-fertility plants shows that the failure years were idiosyncratic to each small plant, which in turn implies that the small plants fail to reproduce because of plant-specific factors (e.g. internal resource limits). Thus, the behaviour of these sub-producers is apparently the result of trade-offs in resource allocation and environmental limits with which the small plants cannot cope. Plant size and especially fecundity and propensity for mast failure years play a major role in determining the variability and synchrony of reproduction in plants. 
    more » « less
  2. Abstract Small mammals such as mice and voles play a fundamental role in the ecosystem service of seed dispersal by caching seeds in small hoards that germinate under beneficial conditions. Pilferage is a critical step in this process in which animals steal seeds from other individuals' caches. Pilferers often recache stolen seeds, which are often pilfered by new individuals, who may recache again, and so on, potentially leading to compounded increased dispersal distance. However, little research has investigated intraspecific differences in pilfering frequency, despite its importance in better understanding the role of behavioural diversity in the valuable ecosystem service of seed dispersal.We conducted a field experiment in Maine (USA) investigating how intraspecific variation, including personality, influences pilferage effectiveness.Within the context of a long‐term capture‐mark‐recapture study, we measured the unique personality of 3311 individual small mammals of 10 species over a 7‐year period. For this experiment, we created artificial caches using eastern white pine (Pinus strobus) seeds monitored with trail cameras and buried antennas for individual identification.Of the 436 caches created, 83.5% were pilfered by 10 species, including deer mice ((Peromyscus maniculatus) and southern red‐backed voles (Myodes gapperi). We show how individuals differ in their ability to pilfer seeds and that these differences are driven by personality, body condition and sex. More exploratory deer mice and those with lower body condition were more likely to locate a cache, and female southern red‐backed voles were more likely than males to locate caches. Also, caches were more likely to be pilfered in areas of higher small mammal abundance.Because the risk of pilferage drives decisions concerning where an animal chooses to store seeds, pilferage pressure is thought to drive the evolution of food‐hoarding behaviour. Our study shows that pilferage ability varies between individuals, meaning that some individuals have a disproportionately strong influence on others' caching decisions and disproportionately contribute to compounded longer‐distance seed dispersal facilitated by pilferage. Our results add to a growing body of knowledge showing that the unique personalities of individual small mammals play a critical role in forest regeneration by impacting seed dispersal. 
    more » « less
  3. Abstract Plants display a range of temporal patterns of inter‐annual reproduction, from relatively constant seed production to “mast seeding,” the synchronized and highly variable interannual seed production of plants within a population. Previous efforts have compiled global records of seed production in long‐lived plants to gain insight into seed production, forest and animal population dynamics, and the effects of global change on masting. Existing datasets focus on seed production dynamics at the population scale but are limited in their ability to examine community‐level mast seeding dynamics across different plant species at the continental scale. We harmonized decades of plant reproduction data for 141 woody plant species across nine Long‐Term Ecological Research (LTER) or long‐term ecological monitoring sites from a wide range of habitats across the United States. Plant reproduction data are reported annually between 1957 and 2021 and based on either seed traps or seed and/or cone counts on individual trees. A wide range of woody plant species including trees, shrubs, and lianas are represented within sites allowing for direct community‐level comparisons among species. We share code for filtering of data that enables the comparison of plot and individual tree data across sites. For each species, we compiled relevant life history attributes (e.g., seed mass, dispersal syndrome, seed longevity, sexual system) that may serve as important predictors of mast seeding in future analyses. To aid in phylogenetically informed analyses, we also share a phylogeny and phylogenetic distance matrix for all species in the dataset. These data can be used to investigate continent‐scale ecological properties of seed production, including individual and population variability, synchrony within and across species, and how these properties of seed production vary in relation to plant species traits and environmental conditions. In addition, these data can be used to assess how annual variability in seed production is associated with climate conditions and how that varies across populations, species, and regions. The dataset is released under a CC0 1.0 Universal public domain license. 
    more » « less
  4. Abstract Synchronous pulses of seed masting and natural disturbance have positive feedbacks on the reproduction of masting species in disturbance‐prone ecosystems. We test the hypotheses that disturbances and proximate causes of masting are correlated, and that their large‐scale synchrony is driven by similar climate teleconnection patterns at both inter‐annual and decadal time scales.Hypotheses were tested on white spruce (Picea glauca), a masting species which surprisingly persists in fire‐prone boreal forests while lacking clear fire adaptations. We built masting, drought and fire indices at regional (Alaska, Yukon, Alberta, Quebec) and sub‐continental scales (western North America) spanning the second half of the 20th century. Superposed Epoch Analysis tested the temporal associations between masting events, drought and burnt area at the regional scale. At the sub‐continental scale, Superposed Epoch Analysis tested whether El Niño‐Southern Oscillation (ENSO) and its coupled effects with the Atlantic Multidecadal Oscillation (AMO) in the positive phase (AMO+/ENSO+) synchronize drought, burnt area and masting. We additionally tested the consistency of our synchronization hypotheses on a decadal temporal scale to verify whether long‐term oscillations in AMO+/ENSO+ are coherent to decadal variation in drought, burnt area and masting.Analyses demonstrated synchronicity between drought, fire and masting. In all regions the year before a mast event was drier and more fire‐prone than usual. During AMO+/ENSO+ events sub‐continental indices of drought and burnt area experienced significant departures from mean values. The same was observed for large‐scale masting in the subsequent year, confirming 1‐year lag between fire and masting. Sub‐continental indices of burnt area and masting showed in‐phase decadal fluctuations led by the AMO+/ENSO+. Results support the ‘Environmental prediction hypothesis’ for mast seeding.Synthesis. We provide evidence of large‐scale synchronicity between seed masting inPicea glaucaand fire regimes in boreal forests of western North America at both inter‐annual and decadal time scales. We conclude that seed production in white spruce predicts changes in disturbance regimes by sharing the same large‐scale climate drivers with drought and fire. This gives new insides in a mechanism providing a fire‐sensitive species with higher than expected adaptability to changes in climate. 
    more » « less
  5. Many perennial plants show mast seeding, characterized by synchronous and highly variable reproduction across years. We propose a general model of masting, integrating proximate factors (environmental variation, weather cues, and resource budgets) with ultimate drivers (predator satiation and pollination efficiency). This general model shows how the relationships between masting and weather shape the diverse responses of species to climate warming, ranging from no change to lower interannual variation or reproductive failure. The role of environmental prediction as a masting driver is being reassessed; future studies need to estimate prediction accuracy and the benefits acquired. Since reproduction is central to plant adaptation to climate change, understanding how masting adapts to shifting environmental conditions is now a central question. 
    more » « less