The selective advantage of mast flowering in Veratrum album subsp. oxysepalum: Implications of the predator satiation hypothesis.

PREMISE: Synchronous, highly variable flower or seed production among years within a population (i.e., masting) has been reported in numerous perennial plants. Although masting provides ecological advantages such as enhancing pollination efficiency and/or escape from predator attack, little is known about the degree of these advantages and variations in masting behavior among populations of conspecific plants. METHODS: We determined flowering ramet density and reproductive success (fruit-set success and herbivorous damage) of a perennial herb, Veratrum album subsp. oxysepalum, across six lowland and six alpine populations in northern Japan during 2-3 years. We then analyzed the relationship between floral density and reproductive success to assess the ecological significance of mast flowering. Flowering intervals of individual plants were estimated by counting annual scars on rhizomes. RESULTS: Most populations had mast flowering, but the intervals between flowering for individual plants were shorter in the alpine populations than in the lowland populations. Floral damage by stem borers (dipteran larvae) and seed predation by lepidopteran larvae were intense in the lowland populations. Seed production of individual ramets increased with higher floral density owing to the effective avoidance of floral-stem damage and seed predation. Although stem borers were absent in the alpine habitat, seed predation decreased with higher floral density also in the alpine populations. Pollination success was independent of floral density in both of the alpine and lowland populations. CONCLUSIONS: These results strongly support the predator satiation hypothesis for mast flowering by this species.

Does masting scale with plant size? High reproductive variability and low synchrony in small and unproductive individuals.

BACKGROUND AND AIMS: In a range of plant species, the distribution of individual mean fecundity is skewed and dominated by a few highly fecund individuals. Larger plants produce greater seed crops, but the exact nature of the relationship between size and reproductive patterns is poorly understood. This is especially clear in plants that reproduce by exhibiting synchronized quasi-periodic variation in fruit production, a process called masting. METHODS: We investigated covariation of plant size and fecundity with individual-plant-level masting patterns and seed predation in 12 mast-seeding species: Pinus pinea, Astragalus scaphoides, Sorbus aucuparia, Quercus ilex, Q. humilis, Q. rubra, Q. alba, Q. montana, Chionochloa pallens, C. macra, Celmisia lyallii and Phormium tenax. KEY RESULTS: Fecundity was non-linearly related to masting patterns. Small and unproductive plants frequently failed to produce any seeds, which elevated their annual variation and decreased synchrony. Above a low fecundity threshold, plants had similar variability and synchrony, regardless of their size and productivity. CONCLUSIONS: Our study shows that within-species variation in masting patterns is correlated with variation in fecundity, which in turn is related to plant size. Low synchrony of low-fertility plants shows that the failure years were idiosyncratic to each small plant, which in turn implies that the small plants fail to reproduce because of plant-specific factors (e.g. internal resource limits). Thus, the behaviour of these sub-producers is apparently the result of trade-offs in resource allocation and environmental limits with which the small plants cannot cope. Plant size and especially fecundity and propensity for mast failure years play a major role in determining the variability and synchrony of reproduction in plants.

Bifurcations of cycles in nonlinear semelparous Leslie matrix models.

This paper develops a method for studying bifurcations that occur in a neighborhood of the extinction equilibrium in nonlinear semelparous Leslie matrix models. The method uses a Lotka-Volterra equation with cyclic symmetry to detect the existence and to evaluate the stability of bifurcating equilibria and cycles. An application of the method provides sharp stability conditions for both a single-class cycle and a positive equilibrium bifurcating from the extinction equilibrium. The stability condition for a bifurcating single-class cycle confirms that the periodicity observed in periodical insects occurs if competition is more severe between than within age-classes. The developed method is also used to investigate two examples of nonlinear semelparous Leslie matrix models incorporating predator satiation. The investigation shows that a single-class cycle, which is associated with the periodicity in periodical insects, is a unique stable cycle in a neighborhood of the extinction equilibrium if the density effects in survival probabilities are identical among age-classes.

Rapid aggregative and reproductive responses of weevils to masting of North American oaks counteract predator satiation.

The predator satiation hypothesis posits that masting helps plants escape seed predation through starvation of predators in lean years, followed by satiation of predators in mast years. Importantly, successful satiation requires sufficiently delayed bottom-up effects of seed availability on seed consumers. However, some seed consumers may be capable of quick aggregative and reproductive responses to masting, which may jeopardize positive density dependence of seed survival. We used a 17-yr data set on seed production and insect (Curculio weevils) infestation of three North American oaks species (northern red Quercus rubra, white Q. alba, and chestnut oak Q. montana) to test predictions of the predation satiation hypothesis. Furthermore, we tested for the unlagged numerical response of Curculio to acorn production. We found that masting results in a bottom-up effect on the insect population; both through increased reproductive output and aggregation at seed-rich trees. Consequently, mast seeding in two out of three studied oaks (white and chestnut oak) did not help to escape insect seed predation, whereas, in the red oak, the escape depended on the synchronization of mast crops within the population. Bottom-up effects of masting on seed consumer populations are assumed to be delayed, and therefore to have negligible effects on seed survival in mast years. Our research suggests that insect populations may be able to mount rapid reproductive and aggregative responses when seed availability increases, possibly hindering satiation effects of masting. Many insect species are able to quickly benefit from pulsed resources, making mechanisms described here potentially relevant in many other systems.

Inter-annual variation in seed production has increased over time (1900-2014).

Mast seeding, or masting, is the highly variable and spatially synchronous production of seeds by a population of plants. The production of variable seed crops is typically correlated with weather, so it is of considerable interest whether global climate change has altered the variability of masting or the size of masting events. We compiled 1086 datasets of plant seed production spanning 1900-2014 and from around the world, and then analysed whether the coefficient of variation (CV) in seed set, a measure of masting, increased over time. Over this 115-year period, seed set became more variable for plants as a whole and for the particularly well-studied taxa of conifers and oaks. The increase in CV corresponded with a decrease in the long-term mean of seed set of plant species. Seed set CV increased to a greater degree in plant taxa with a tendency towards masting. Seed set is becoming more variable among years, especially for plant taxa whose masting events are known to affect animal populations. Such subtle change in reproduction can have wide-ranging effects on ecosystems because seed crops provide critical resources for a wide range of taxa and have cascading effects throughout food webs.

Seed production and predation in a changing climate: new roles for resource and seed predator feedback?

Climate change may cause changes in the dynamics of populations beyond comparatively simple directional effects. To better understand complex effects on dynamics requires long-term studies of populations that experience changes in climatic conditions. We study the dynamics of a seed-production-seed-predation system, consisting of a perennial herb and its two seed predatory insects, over a 40-yr period during which climate change has caused the annual growing season to increase by 20 d. During this period, plant patches have increased almost threefold in size and seed production has slipped into a pattern of alternate high and low years with a higher variance than in the beginning of the period. We find that seed production is associated with precipitation of the present summer and a non-linear feedback from seed production of the previous year. When previous year's seed production is low, weather forcing and unexplained noise determine the extent of seed production. When previous seed production is high, depleted resources limit seed production. Resource depletion happened frequently in the latter parts of the study but rarely in the beginning. The changing patterns of seed production in turn affect the dynamics of seed predation, which is dominated by one of the seed predators. Its dynamics are strongly linked to seed density fluctuations, but its population growth rate is satiated when resource fluctuations become too large. In the latter part of the study period, when seed fluctuations were alternating between years of high and low density, satiation was common and there was a large increase in surviving seeds in good years. Our study illustrates that a changing climate can fundamentally influence patterns of long-term dynamics at multiple trophic levels.

Seed-predator satiation and Janzen-Connell effects vary with spatial scales for seed-feeding insects.

BACKGROUND AND AIMS: The Janzen-Connell model predicts that common species suffer high seed predation from specialized natural enemies as a function of distance from parent trees, and consequently as a function of conspecific density, whereas the predator satiation hypothesis predicts that seed attack is reduced due to predator satiation at high seed densities. Pre-dispersal predation by insects was studied while seeds are still on parent trees, which represents a frequently overlooked stage in which seed predation occurs. METHODS: Reproductive tree density and seed production were investigated from ten Quercus serrata populations located in south-west China, quantifying density-dependent pre-dispersal seed predation over two years by three insect groups. KEY RESULTS: Acorn infestation was nearly twice as high in the low-seed year as that in the high-seed year, with considerable spatio-temporal variation in the direction and magnitude of density-dependent pre-dispersal seed predation evident. Across whole populations of trees, a high density of reproductive trees caused predator satiation and reduced insect attack in the high-seed year. Within individual trees, and consistent with the Janzen-Connell model, overall insect seed predation was positively correlated with seed production in the low-seed year. In addition, there was variation among insect taxa, with positive density-dependent seed predation by Curculio weevils in the high-seed year and moths in the low-seed year, but apparent density independence by Cyllorhynchites weevils in both years. CONCLUSIONS: The overall trend of negative density-dependent, pre-dispersal seed predation suggests that predator satiation limited the occurrence of Janzen-Connell effects across Q. serrata populations. Such effects may have large impacts on plant population dynamics and tree diversity, depending on the extent to which they are reduced by counteracting positive density-dependent predation for seeds on individual trees and other factors affecting successful recruitment.

Fire after a mast year triggers mass recruitment of slender mulga (Acacia aptaneura), a desert shrub with heat-stimulated germination.

PREMISE OF THE STUDY: Fire typically triggers extensive regeneration of plants with heat-stimulated germination by causing short periods of intense soil heating. If plants with heat-stimulated germination are also subject to seed predation and display mast-seeding cycles, postfire recruitment may be contingent on the seedfall density of prefire masts, and on whether granivores are satiated at the time of fire. METHODS: We conducted a longitudinal seedbank study and a mensurative field experiment in central Australia to examine whether fire and the variation in seedfall density across sites in a mast year interact to influence recruitment of slender mulga (Acacia aptaneura), an iteroparous masting shrub with heat-stimulated germination. KEY RESULT: The seedbank study showed seedbank pulsing after masting, with mean seed counts in the upper 4-cm soil layer being 132.8 seeds/m2 12-mo after a dense seedfall, but only 3.8 seeds/m2 following a year with no seed production. Consistent with this, recruitment increased postfire at sites where denser seedfall had occurred during the preburn mast year. Conversely, little recruitment occurred at unburnt populations, irrespective of prefire seedfall density. CONCLUSIONS: We attribute our findings to: (1) elevated soil temperatures during fires stimulating germination of heat-cued seeds; and (2) granivore satiation following masting facilitating assimilation of seeds into the soil seedbank. These results highlight the importance of rare seed-input events for regeneration in fire-prone systems dominated by masting plants, and provide the first example from an arid biome of fire interacting with masting to influence recruitment.

Evolutionary drivers of mast-seeding in a long-lived desert shrub.

PREMISE OF THE STUDY: The evolutionary drivers and proximal regulators of mast-seeding are well understood for species of mesic environments, but how these regulators interact with high spatial and interannual variability in growing-season precipitation for a masting species in a desert environment has never been examined. METHOD: We followed flowering and seed production in 16 populations of the North American desert shrub blackbrush (Coleogyne ramosissima) from contrasting environments across its range over an 11-year period to determine patterns of interannual reproductive output variation. KEY RESULT: Patterns of reproductive output in blackbrush did not track current growing season precipitation, but instead were regulated by prior-year weather cues. The strength of the response to the masting cue depended on habitat quality, with higher mean reproductive output, shorter intervals between years of high seed production, and lower CVp at more favorable sites. Wind pollination efficiency was demonstrated to be an important evolutionary driver of masting in blackbrush, and satiation of heteromyid seed predator-dispersers was supported as an evolutionary driver based on earlier studies. CONCLUSIONS: Both the evolutionary drivers and proximal regulators of masting in blackbrush are similar to those demonstrated for masting species of mesic environments. Relatively low synchrony across populations in response to regional masting cues occurs at least partly because prior-year environmental cues can trigger masting efforts in years with resource limitation due to suboptimal precipitation, especially in more xeric low-elevation habitats.

Density-dependent selection closes an eco-evolutionary feedback loop in the stick insect Timema cristinae.

Empirical demonstrations of feedbacks between ecology and evolution are rare. Here, we used a field experiment to test the hypothesis that avian predators impose density-dependent selection (DDS) on Timema cristinae stick insects. We transplanted wild-caught T. cristinae to wild bushes at 50 : 50 cryptic : conspicuous morph ratio and manipulated density by transplanting either 24 or 48 individuals. The frequency of the conspicuous morph was reduced by 73% in the low-density treatment, but only by 50% in the high-density treatment, supporting a hypothesis of negative DDS. Coupled with previous studies on T. cristinae, which demonstrate that maladaptive gene flow reduces population density, we support an eco-evolutionary feedback loop in this system. Furthermore, our results support the hypothesis that predator satiation is the mechanism driving DDS. We found no effects of T. cristinae density on the abundance or species richness of other arthropods. Eco-evolutionary feedbacks, driven by processes like DDS, can have implications for adaptive divergence and speciation.

Spatial and Temporal Variation in the Antagonistic and Mutualistic Interactions among Seed Predator Arthropods, Seed-Dispersing Birds, and the Spanish Juniper.

Plants interact with both antagonistic and mutualistic animals during reproduction, with the outcomes of these interactions significantly influencing plant reproductive success, population dynamics, and the evolution of plant traits. Here, we investigated the spatial and temporal variations in the interactions between Juniperus thurifera, its seed-dispersing birds, and three specific arthropod species that attack the fleshy cones during the predispersal period. We assessed how plant traits affect levels of cone damage by arthropods and seed dispersal by birds, the occurrence of competition among arthropod species, and the impact of seed predators on the activity of frugivores. Plant traits, cone damage by arthropods, and seed dispersal by birds showed spatiotemporal variability. Fluctuation in cone abundance was the leading factor determining damage by arthropods and bird dispersal with a secondary role of cone traits. Large crops satiated predispersal seed predators, although the amount of frugivory did not increase significantly, suggesting a potential satiation of bird dispersers. Crop size and cone traits at individual trees determined preferences by seed predator species and the foraging activity of bird dispersers. Competition among arthropods increased during years of low cone production, and seed predators sometimes negatively affected bird frugivory. High supra-annual variations in cone production appear to be a key evolutionary mechanism enhancing J. thurifera reproductive success. This strategy reduces the impact of specialized seed predators during years of high seed production, despite the potential drawback of satiating seed dispersers.

Masting, fire-stimulated flowering, and the evolutionary ecology of synchronized reproduction.

Synchronized episodic reproduction among long-lived plants shapes ecological interactions, ecosystem dynamics, and evolutionary processes worldwide. Two active scientific fields investigate the causes and consequences of such synchronized reproduction: the fields of masting and fire-stimulated flowering. While parallels between masting and fire-stimulated flowering have been previously noted, there has been little dialogue between these historically independent fields. We predict that the synthesis of these fields will facilitate new insight into the causes and consequences of synchronized reproduction. Here we briefly review parallels between masting and fire-stimulated flowering, using two case studies and a database of 1870 plant species to facilitate methodological, conceptual, geographical, taxonomic, and phylogenetic comparisons. We identify avenues for future research and describe three key opportunities associated with synthesis. First, the taxonomic and geographic complementarity of empirical studies from these historically independent fields highlights the potential to derive more general inferences about global patterns and consequences of synchronized reproduction in perennial plants. Second, masting's well developed conceptual framework for evaluating adaptive hypotheses can help guide empirical studies of fire-stimulated species and enable stronger inferences about the evolutionary ecology of fire-stimulated flowering. Third, experimental manipulation of reproductive variation in fire-stimulated species presents unique opportunities to empirically investigate foundational questions about ecological and evolutionary processes underlying synchronized reproduction. Synthesis of these fields and their complementary insights offers a unique opportunity to advance our understanding of the evolutionary ecology of synchronized reproduction in perennial plants.

Coevolution of mast seeding in trees and extended diapause of seed predators.

Many trees in forests show synchronized and intermittent reproduction, which is called "masting" or mast seeding. According to recent theoretical studies, the evolution of masting is promoted both by recruitment through the seedling bank and by seed predators. An important class of specialist seed predators (e.g., weevils and some moths) are parasitoids that oviposit on or in fruits from which the next generation emerges over the following several years. This staggered emergence is called "extended diapause". In this paper, we study the simultaneous evolution of tree masting and extended diapause of seed predators. If a fixed fraction of diapausing larvae matures every year, the evolution of trees results in masting (intermittent reproduction with a large fluctuation in reproductive activity) or non-masting (trees reproduce every year). The transition occurs discontinuously, showing evolutionary jumping. The range of seedling survivorship for which masting evolves is broader when the ovipositing efficiency and larval survivorship of the seed predators are large. Interestingly, the conditions for the evolution of masting are broadest for an intermediate fraction of extended diapause of seed predators. When both tree masting and the extended diapause of seed predators evolve simultaneously, the evolutionary end point of the fraction of extended diapause is clearly greater than the value that most favors masting evolution. The stochasticity caused by the finiteness of the number of trees tends to promote masting evolution.

Tropical-temperate comparisons in insect seed predation vary between study levels and years.

The biotic interaction hypothesis, which states the species interaction becomes stronger in the tropics, is deeply rooted in classic ecological literature and widely accepted to contribute to the latitudinal gradients of biodiversity. Tests in latitudinal insect-plant interaction have emphasized leaf-eating insects on a single or a few plant species rather than within an entire community and mixed accumulating evidence, leaving the biotic interaction hypothesis disputed. We aimed to test the hypothesis by quantifying insect seed predation in a pair of tropical and temperate forest communities with similar elevations. We applied a consistent study design to sample predispersal seeds with systematically set seed traps in 2019-2020 and examined internally feeding insects. The intensity of seed predation was measured and further applied to tropical versus temperate comparison at two levels (cross-species and community-wide). Our results showed every latitudinal pattern associated with different study levels and years, that is, negative (greater granivory in the tropics in community-wide comparison in 2020), positive (less granivory in the tropics in community-wide and cross-species comparison in 2019), and missing (similar level of granivory in the tropics in cross-species comparisons in 2020). The cross-species level analyses ignore differences among species in seed production and weaken or even lose the latitudinal trend detected by community-wide comparisons. The between-year discrepancy in tropical-temperate comparisons relates to the highly variable annual seed composition in the temperate forest due to mast seeding of dominant species. Our study highlights that long-term community-level researches across biomes are essential to assess the latitudinal biotic interaction hypothesis.

Effects of masting on seedling establishment of a rodent-dispersed tree species in a warm-temperate region, northern China.

Masting is an evolutionary strategy used by plants to promote seed survival and/or seed dispersal under animal predation, but its effects on seedling establishment in field condition are rarely tested by long-term experiments incorporating combined effects of seed and animal abundance. Here, we tracked seed production, rodent-mediated seed dispersal, and seedling establishment in Armeniaca sibirica from 2005 to 2014 in a warm-temperate forest in northern China, and examined the effects of seed abundance and per capita seed availability on seed fate and seedling recruitment rate. Our results showed that seed abundance or per capita seed availability generally benefited the seedling recruitment of A. sibirica through increasing dispersal intensity, supporting predator dispersal hypothesis. However, seedling recruitment showed satiated or even dome-shaped association with per capita seed availability, suggesting the benefit to trees would be decreased when seed abundance were too high as compared to rodent abundance (a satiated effect). Our results suggest that the predator dispersal and satiation effects of masting on seedling recruitment can operate together in one system and conditionally change with seed and animal abundance.

How seed defense and seed abundance predict dispersal and survival patterns in Camellia.

Little is known about how seed defense and seed abundance interact with behavioral responses of seed dispersers to predict dispersal and survival dynamics in animal-dispersed plants. By tracking the fate of individual seeds in Camellia stands with high and low seed abundance in Southwest China in 2007, we investigated the dispersal and survival of 2 high-saponin Camellia species (Camellia oleifera and Camellia sinensis and 1 non-saponin species (peanut Arachis hypogaea) as a control. Saponins in Camellia seeds are chemical compounds that act as seed defense. Our results were most consistent with the predictions based on the predator satiation hypothesis and the plant defense hypothesis. At the abundant Camellia stand (predators and dispersers were satiated), more Camellia seeds survived at the source but fewer were hoarded and survived at cache sites. At the sparse Camellia stand (predators and dispersers were not satiated), no Camellia seeds survived at the source, but more Camellia seeds were hoarded and survived at cache sites. Unlike Camellia seeds, no peanuts survived at the source at both stands, while more peanuts were hoarded and then survived at cache sites in the abundant Camellia stand compared to none at the sparse Camellia stand. In addition, the 2 Camellia species showed similar trends for seed fates across different dispersal stages. Our study indicates that the combined effects of seed abundance and seed defense, compared to their separate effects, provide a more accurate prediction for dispersal and survival patterns in animal-dispersed Camellia species.

Fluctuation in seed abundance has contrasting effects on the fate of seeds from two rapidly germinating tree species in an Asian tropical forest.

The seed predator satiation hypothesis states that high seed abundance can satiate seed predators or seed dispersers, thus promoting seed survival. However, for rapidly germinating seeds in tropical forests, high seed abundance may limit dispersal as the seeds usually remain under parent trees for long periods, which may lead to high mortality due to rodent predation or fungal infestations. By tracking 2 species of rapidly germinating seeds (Pittosporopsis kerrii, family Icacinaceae; Camellia kissi, family Theaceae), which depend on dispersal by scatter-hoarding rodents, we investigated the effects of seed abundance at the community level on predation and seed dispersal in the tropical forest of Xishuangbanna Prefecture, Southwest China. We found that high seed abundance at the community level was associated with delayed and reduced seed removal, decreased dispersal distance and increased pre-dispersal seed survival for both plant species. High seed abundance was also associated with reduced seed caching of C. kissi, but it showed little effect on seed caching of P. kerrii. However, post-dispersal seed survival for the 2 plant species followed the reverse pattern. High seed abundance in the community was associated with higher post-dispersal survival of P. kerrii seeds, but with lower post-dispersal survival of C. kissi seeds. Our results suggest that different plant species derive benefit from fluctuations in seed production in different ways.

Delayed Flowering in Bamboo: Evidence from Fargesia qinlingensis in the Qinling Mountains of China.

Gregarious flowering of bamboo species impacts ecosystem properties and conservation, but documentation of these periodic events is difficult. Here, we compare the characteristics of flowering sites and un-flowered patches of an arrow bamboo (Fargesia qinlingensis) in the Qinling Mountains, China, over a 5-year period (2003-2007) after a mast flowering event (2003). We examined flowering culm and seedling characteristics in relation to questions regarding the evolution of delayed flowering. Density of live culms decreased over the 5 years in both flowering sites and un-flowered patches. New shoots regenerated only in un-flowered patches. Chemical constituent allocation varied among culm parts (stems, branches, and leaves). Crude protein and extract ether in branches and leaves were less in flowering culms than in un-flowered culms. Seedling density was lower than expected based on floret counts, suggesting predation of seeds. Seedling density was significantly greater in flowering sites than in un-flowered patches and decreased over time. Seedlings performed better in flowering sites than in un-flowered patches based on their height, leaf number per seedling, and average leaf length, while fertilization on flowering sites had no significant effect on seedling growth, suggesting a saturation of resources. This study suggested that the characteristics of bamboos and bamboo stands were dramatically altered during this flowering event, enhancing seedling establishment and growth, and supporting mostly the habitat modification hypothesis of delayed reproduction.

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.