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Multiple ecological interactions between species in a model Eastern deciduous forest result in a trophic cascade in which the effects of acorn crop size ripple through the food web, setting off a chain of events that cause animal populations to change. Large amounts of energy (arrows) flow through the system during a mast year (right) when a large acorn crop is produced by an oak (center), causing populations of deer, mice and ticks to increase and raising the incidence of tick-borne Lyme disease (+). Populations of ground-nesting birds and gypsy moths decrease (–) owing to predation by mice. During a mast failure (left) effects of an acorn shortage on the food web are negative for acorn-eaters and their predators and positive for birds and moths, whose eggs and larvae are eaten by mice.
Source publication
his autumn, the vast hardwood forests of North America could be chock full of acorns, a pulse of resources that will cascade through the ecosystem, affecting mice, birds and other wildlife for years to come. Over far-flung areas virtually all the oaks of the same species, and perhaps more than one species, are already gearing up to produce the seed...
Similar publications
Pre-dispersal seed predation (PDSP) is commonly observed in woody plants, and recognized as a driver of seed production variability that is critical for successful regeneration. Earlier studies on PDSP and its determinants were mostly species specific, with community-level PDSP rarely estimated; and the interactions between the temporal variability...
Citations
... The cascading effects of resource pulses within ecosystems (Koenig & Knops, 2005;Ostfeld et al., 1996;Ostfeld & Keesing, 2000) can aggregate predators (Jensen et al., 2012;Schindler et al., 2013) and lead to irruptions of highly mobile species to areas outside of their 'normal' distributions (Newton, 2006;Therrien et al., 2014; e.g., snowy owl, Bubo scandiacus). When resource pulses occur, even species with limited dispersal abilities (i.e., small mammals) can temporarily expand their elevational range limits to capitalise on the ephemeral resources (Carpenter et al., 2022). ...
Aim
Spatiotemporal variation in resource availability is a strong driver of animal distributions. In the northern hardwood and boreal forests of the northeastern United States, tree mast events provide resource pulses that drive the population dynamics of small mammals, including the American red squirrel (Tamiasciurus hudsonicus), a primary songbird nest predator. This study sought to determine whether mast availability ameliorates their abiotic limits, enabling red squirrel elevational distributions to temporarily expand and negatively impact high‐elevation songbirds.
Location
Northeastern United States.
Methods
We used two independent datasets to evaluate our hypotheses. First, we fit a dynamic occupancy model using data from camera trap surveys to evaluate red squirrel distributional responses to pulses in the tree mast. We also assessed population responses using systematic auditory surveys analysed with an open‐population binomial mixture model. Further, we used modelled red squirrel abundance in nest‐survival models to evaluate whether their abundance is correlated with the daily nest survival of three songbird species.
Results
The tree mast provided a critical resource pulse that resulted in a two‐fold increase in the annual elevational distribution of red squirrels. The elevational distribution of red squirrels ranged from a minimum of ~450 m (range: 663–1145 m asl) following two consecutive years without a masting event to a maximum of over 1000 m (range: 443–1545 m asl) after a large mast event. The daily nest survival of three songbird species tended to decline with an increase in the abundance of red squirrels.
Main Conclusions
Tree mast is a central biological phenomenon in many temperate and boreal forests. This study reveals how this resource pulse results in range changes in a small mammal that is both a seed and bird predator, as well as prey for many carnivores. Thus, understanding this phenomenon can inform the conservation and management of northern forests, including breeding songbirds.
... Biennial bearing has accompanied fruit trees since their domestication. Natural forest species also regularly go through masting phases (years of high yields) that are accompanied by periods of low seed or fruit production (Koenig and Knops, 2005). Biennial bearing refers to the tendency of a tree to bear a light ("off") crop following a year when the crop load was high or "on", although it can last three to four years (Krasniqi et al., 2013) (Fig. 1). ...
Biennial bearing has long been a challenge for perennial tree fruit production. Some cultivars are more susceptible and can have excessive bloom and fruit set in one year followed by insufficient bloom and fruit set in the next year. Although crop load management can be used to reduce biennial bearing, optimum crop loads in one year can still sometimes be followed by high variability in return bloom the next. Moreover, the fundamental mechanisms that drive this behavior are poorly understood. The two primary hypotheses of biennial bearing consider hormonal control and resource competition for carbohydrates and nutrients. Through reviewing the current literature and gaining a better understanding of carbohydrate and hormone cycling/signaling within trees, a framework for biennial bearing control can be developed. With an understanding of the physiological responses contributing to biennial bearing patterns, manipulation of carbohydrate and nutrient cycling within trees through management practices may influence flowering and fruit bud formation. Improved management practices of biennial bearing can be evaluated and adjusted to suit different planting systems and species.
... Recent research, however, suggests that masting species may practice different adaptive strategies of either "fruit maturation" or "flower masting", with the prevalence of one strategy over the other dependent on the environmental conditions of the site (Fleurot et al. 2023). Masting is hypothesized to have evolved as a predator satiation strategy and may be mechanistically controlled by resource dynamics (Isagi et al. 1997;Koenig and Knops 2005). The significance of fruit production in mature communities for tree demography and the maintenance of food webs makes it important to determine the effects of elevated CO 2 on seed production in masting species empirically. ...
Acorn production in oak (Quercus spp.) shows considerable inter-annual variation, known as masting, which provides a natural defence against seed predators but a highly-variable supply of acorns for uses such as in commercial tree planting each year. Anthropogenic emissions of greenhouse gases have been very widely reported to influence plant growth and seed or fruit size and quantity via the ‘fertilisation effect’ that leads to enhanced photosynthesis. To examine if acorn production in mature woodland communities will be affected by further increase in CO2, the contents of litter traps from a Free Air Carbon Enrichment (FACE) experiment in deciduous woodland in central England were analysed for numbers of flowers and acorns of pedunculate oak (Quercus robur L.) at different stages of development and their predation levels under ambient and elevated CO2 concentrations. Inter-annual variation in acorn numbers was considerable and cyclical between 2015 and 2021, with the greatest numbers of mature acorns in 2015, 2017 and 2020 but almost none in 2018. The numbers of flowers, enlarged cups, immature acorns, empty acorn cups, and galls in the litter traps also varied amongst years; comparatively high numbers of enlarged cups were recorded in 2018, suggesting Q. robur at this site is a fruit maturation masting species (i.e., the extent of abortion of pollinated flowers during acorn development affects mature acorn numbers greatly). Raising the atmospheric CO2 concentration by 150 μL L−1, from early 2017, increased the numbers of immature acorns, and all acorn evidence (empty cups + immature acorns + mature acorns) detected in the litter traps compared to ambient controls by 2021, but did not consistently affect the numbers of flowers, enlarged cups, empty cups, or mature acorns. The number of flowers in the elevated CO2 plots’ litter traps was greater in 2018 than 2017, one year after CO2 enrichment began, whereas numbers declined in ambient plots. Enrichment with CO2 also increased the number of oak knopper galls (Andricus quercuscalicis Burgsdorf). We conclude that elevated CO2 increased the occurrence of acorns developing from flowers, but the putative benefit to mature acorn numbers may have been hidden by excessive pre- and/or post-dispersal predation. There was no evidence that elevated CO2 altered masting behaviour.
... The depletion of carbohydrates in the previous year's crop has a direct impact on the subsequent year's crop, creating a cyclical pattern in production [14]. The cyclic nature of alternate bearing allows perennial plants can lead to various types of dynamic behavior [23][24][25][26]. The interconnections of two coupled plants resulted in a remarkable display of out-of-phase synchronization, which remained prominent despite the presence of indirect interactions [21]. ...
... The indirect coupling has been well studied in diverse systems [30,31] and has also been shown to affect populations of trees in many ways. For example, pollen interactions with wind and insects increase the production of seed and/or fruit in plants [26,32,33]. ...
... But a large part of this observed IV is actually structured in time and associated with temporal changes in the environment. For instance, the temporal storage effect (Chesson & Warner, 1981), a well-known coexistence mechanism, structures species performance because species are able to "store" growth during favorable timespans to overcome lean times; mast-seeding or masting, which describes periodic and synchronized massive seed production of conspecific individuals, would also result in a temporally structured IV (Koenig & Knops, 2005). Temporal variation in individual response within a species can typically be structured with temporal random effects (Clark et al., 2007). ...
Intraspecific variability (IV) has been proposed as a new track to explain species coexistence. Previous studies generally assumed that IV results from intrinsic differences between conspecifics that widen species’ fundamental niches and blur differences among species, thus impeding stable coexistence, but also slowing down the rate of competitive exclusion. Based on a body of evidence, we here argue that IV does not necessarily imply differences among conspecifics, nor species niches overlap: conspecifics differ in their measured attributes mainly due to differences in the micro-environment they thrive in. Consequently, they respond more similarly to environmental variation than heterospecifics, thereby concentrating competition within species – a necessary condition for species coexistence. We call for new studies exploring observed IV as an outcome of species-specific responses to high-dimensional environmental variations that can lead to inversions of species hierarchy in space and time promoting stable coexistence.
... Contrary to what we expected, the proportion of hot points matching interannually among the same intervals was quite low. This can indicate the variable performance in crop production of the different trees and tree groups from year to year [36,70,71]. However, acorn density hot points were mostly identical intra-annually (between the acorn-fall and acorn-rich periods), which was also unexpected, thus we would assume that those will be the ones that would be depleted first by the seed predators. ...
The natural regeneration of the temperate oak forests is often insufficient. Acorns of the oak serve as the basis of the recruitment and key food resources in these ecosystems, thus the crop size, the germination success and seed predators have crucial roles in the process. Wild boar (Sus scrofa) is often considered as one of the main mitigating agents in oak regeneration. Therefore, in our study we analyzed and compared the spatial patterns of the acorn density and the patches rooted by wild boar within and among the different examined time intervals in a 28 ha Turkey-sessile oak (Quercus cerris, Q. petraea) forest stand. Data were collected between 2016 October and 2019 December. In the acorn density patterns, intra-annual similarities were recognized mainly, regardless of the crop size. Meanwhile, rooting patterns showed inter-and intra-annual similarities in mast years and intra-annual overlaps in non-mast years, indicating that masting is a fundamental driver of wild boar foraging behavior. However, a direct local connection between the rooting intensity and the acorn density could not be shown, as wild boars never fully depleted the acorns, even in intensively used patches. This study can help in predicting the intensively rooted forest patches, providing opportunities to manage wildlife conflicts.
... Data on oak (Quercus robur) bud burst (1988-2021) and on beech (Fagus sylvatica) crop (1977-2021) were only available for Hoge Veluwe but considered representative for all areas as trees across wide spatial ranges are highly correlated regarding leaving and crop production [32,33]. Temperature data was obtained from the KNMI (Royal Dutch Meteorological Institute) for the closest weather station that had homogenized data covering the whole study period, which was De Kooy for Vlieland and De Bilt for the remaining sites (data is highly correlated with data of weather stations closest to each site (R > 0.95)). ...
Climate change has led to changes in the strength of directional selection on seasonal timing. Understanding the causes and consequences of these changes is crucial to predict the impact of climate change. But are observed patterns in one population generalizable to others, and can spatial variation in selection be explained by environmental variation among populations? We used long-term data (1955–2022) on blue and great tits co-occurring in four locations across the Netherlands to assess inter-population variation in temporal patterns of selection on laying date. To analyse selection, we combine reproduction and adult survival into a joined fitness measure. We found distinct spatial variation in temporal patterns of selection which overall acted towards earlier laying, and which was due to selection through reproduction rather than through survival. The underlying relationships between temperature, bird and caterpillar phenology were however the same across populations, and the spatial variation in selection patterns is thus caused by spatial variation in the temperatures and other habitat characteristics to which birds and caterpillars respond. This underlines that climate change is not necessarily equally affecting populations, but that we can understand this spatial variation, which enables us to predict climate change effects on selection for other populations.
... From the plant perspective, masting-synchrony in seed production-leads to substantial variation across years with large consequences for animal populations and plant-herbivore interactions (Pearse et al. 2016). One well-studied example is the California blue oak (Quercus douglasii), which can produce from zero to more than 100,000 acorns per tree with production correlated at distances at least up to 800 km within years (Koenig & Knops 2005). Escaping herbivory through herbivore satiation is thought to be a key cause of masting (Crawley & Long 1995, Koenig & Knops 2005, Pearse et al. 2016). ...
... One well-studied example is the California blue oak (Quercus douglasii), which can produce from zero to more than 100,000 acorns per tree with production correlated at distances at least up to 800 km within years (Koenig & Knops 2005). Escaping herbivory through herbivore satiation is thought to be a key cause of masting (Crawley & Long 1995, Koenig & Knops 2005, Pearse et al. 2016). ...
Plants and herbivores are remarkably variable in space and time, and variability has been considered a defining feature of their interactions. Empirical research, however, has traditionally focused on understanding differences in means and overlooked the theoretically significant ecological and evolutionary roles of variability itself. We review the literature with the goal of showing how variability-explicit research expands our perspective on plant–herbivore ecology and evolution. We first clarify terminology for describing variation and then review patterns, causes, and consequences of variation in herbivory across scales of space, time, and biological organization. We consider how incorporating variability improves existing hypotheses and leads to new ones. We conclude by suggesting future work that reports full distributions, integrates effects of variation across scales, describes nonlinearities, and considers how stochastic and deterministic variation combine to determine herbivory distributions.
Expected final online publication date for the Annual Review of Ecology, Evolution, and Systematics, Volume 54 is November 2023. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.
... But a large part of this observed IV is actually structured in time and associated with temporal changes in the environment. For instance, the temporal storage effect (Chesson & Warner, 1981), a well-known coexistence mechanism, structures species performance because species are able to "store" growth during favorable timespans to overcome lean times; mast-seeding or masting, which describes periodic and synchronized massive seed production of conspecific individuals, would also result in a temporally structured IV (Koenig & Knops, 2005). Temporal variation in individual response within a species can typically be structured with temporal random effects (Clark et al., 2007). ...
Intraspecific variability (IV) has been proposed to explain species coexistence in diverse communities. Assuming, sometimes implicitly, that conspecific individuals can perform differently in the same environment and that IV increases niche overlap, previous studies have found contrasting results regarding the effect of IV on species coexistence. We aim at showing that the large IV observed in data does not mean that conspecific individuals are necessarily different in their response to the environment
and that the role of high-dimensional environmental variation in determining IV has largely remained unexplored in forest plant communities. We first used a simulation
experiment where an individual attribute is derived from a high-dimensional model, representing “perfect knowledge” of individual response to the environment, to illustrate how large observed IV can result from “imperfect knowledge” of the environment. Second, using growth data from clonal Eucalyptus plantations in Brazil, we estimated a major contribution of the environment in determining individual growth.
Third, using tree growth data from long-term tropical forest inventories in French Guiana, Panama and India, we showed that tree growth in tropical forests is structured spatially and that despite a large observed IV at the population level, conspecific individuals perform more similarly locally than compared with heterospecific individuals. As the number of environmental dimensions that are well quantified at fine scale is generally lower than the actual number of dimensions influencing individual at-
tributes, a great part of observed IV might be represented as random variation across individuals when in fact it is environmentally driven. This mis-representation has important consequences for inference about community dynamics. We emphasize that observed IV does not necessarily impact species coexistence per se but can reveal species response to high-dimensional environment, which is consistent with niche theory and the observation of the many differences between species in nature.
... Many tree species undergo significant variations in seed production from year-to-year, a phenomenon known as masting (Kelly, 1994;Kelly and Sork, 2002;Pearse et al., 2016;Allen et al., 2017;Fernańdez-Martıńez et al., 2019;Fernańdez-Martıńez et al., 2020;Kelly, 2020). Inter-annual variations in seed production have been related to climatic conditions (Allen et al., 2014;Roland et al., 2014;Pearse et al., 2016;Fernańdez-Martıńez et al., 2019;LaMontagne et al., 2020), which affect annual growth (Yasumura et al., 2006;Smith and Samach, 2013;Nakahata et al., 2021), flowering (Law et al., 2000;Cook et al., 2012), pollen availability and pollination efficiency (Koenig and Knops, 2005;Koenig et Al., 2012;Peŕez-Ramos et al., 2015;Pearse et al., 2016;Venner et al., 2016). In addition to climatic conditions, nutrient cycling is essential in regulating masting behaviour and reproductive mechanisms (Kelly, 1994;Kelly and Sork, 2002;Sala et al., 2012;Pearse et al., 2016;Han et al., 2017;Fernańdez-Martıńez et al., 2019;Fernańdez-Martıńez et al., 2020;Kelly, 2020) because reproduction consumes a significant amount of carbohydrates and mineral nutrients. ...
Pinus koraiensis is famous for its high-quality timber production all the way and is much more famous for its high value health-care nut oil production potential since 1990’s, but the less understanding of its reproduction biology seriously hindered its nut productivity increase. Exploring the effects of reproduction on nutrient uptake, allocation and storage help to understand and modify reproduction patterns in masting species and high nut yield cultivar selection and breeding. Here, we compared seasonality in growth and in nitrogen ([N]) and phosphorus ([P]) concentrations in needles, branches and cones of reproductive (cone-bearing) and vegetative branches (having no cones) of P. koraiensis during a masting year. The growth of one- and two-year-old reproductive branches was significantly higher than that of vegetative branches. Needle, phloem and xylem [N] and [P] were lower in reproductive branches than in vegetative branches, although the extent and significance of the differences between branch types varied across dates. [N] and [P] in most tissues were high in spring, decreased during summer, and then recovered by the end of the growing season. Overall, [N] and [P] were highest in needles, lowest in the xylem and intermediate in the phloem. More than half of the N (73.5%) and P (51.6%) content in reproductive branches were allocated to cones. There was a positive correlation between cone number and N and P content in needles (R² = 0.64, R² = 0.73) and twigs (R² = 0.65, R² = 0.62) of two-year-old reproductive branches. High nutrient sink strength of cones and vegetative tissues of reproductive branches suggested that customized fertilization practices can help improve crop yield in Pinus koraiensis.
