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-Examples of density-independent (left) and density-dependent (right) mechanisms with adaptive benefits linked to models of climate variability. In North-West America (left) the onset of El Niño time spruce reproduction to anticipate favourable conditions for offspring early-life fitness due to fire disturbance. In SouthEast Asia (right) the transition from La Niña to El Niño synchronizes community-wide reproduction in Dipterocarp forest setting a "regional" escape from mobile animal predators such as Sus barbatus and Pongo pygmaeus.
Source publication
There is evidence that variable and synchronous reproduction in seed plants (masting) correlates to modes of climate variability, e.g. El Niño Southern Oscillation and North Atlantic Oscillation. In this perspective, we explore the breadth of knowledge on how climate modes control reproduction in major masting species throughout Earth's biomes. We...
Contexts in source publication
Context 1
... Chechina and Hamann (2019) suggest a cumulative-trigger model to predict flowering in Dipterocarps that incorporates temporal accumulation of resources. Interestingly, these regional masting events occur preferentially during the transition from La Niña (negative ENSO phase) to the onset of El Niño (positive ENSO phase) ( Figure S4) indicating a potential dynamic role of ENSO in aligning cumulative and synergic cues. A wet period during La Niña stimulates resource priming [38,57] (Table S1), while the onset of El Niño reduces cloud cover [57], leading to increased daytime radiation, lower night-time temperatures ( Figure S5a), and dry conditions ( Figure S5b) over peninsular Malaysia, the Northern Sumatra and western Borneo, approximately 12 months before the El Niño peak (usually from December to February). ...
Context 2
... caused by the transition from La Niña to El Niño also appear relevant for Picea glauca reproduction in Western [7] and Eastern North America ( Figure S4). Masting of P. glauca in Eastern regions of North America is associated with temperature differences from the two prior summers [60], a cue known as ΔT [17]. ...
Context 3
... in South-East Asia the complexity created by the Malaysian Peninsula and Bornean and Sumatran coastlines and mountain ridges interacts with the response of atmospheric circulation to ENSO and generates regional weather and masting patterns. In SouthWestern peninsular Malaysia and Western Borneo, flowering and fruiting of Dipterocarp often occurs during the transition from La Niña to El Niño ( Figure S4). However, flowering starts in March in Peninsular Malaysia and in July in South-Western Borneo, which mirrors the North-West to South-East shift of dry-cool air that precedes the onset of El Niño ( Figure S5a, c, g, i). ...
Context 4
... brought by El Niño can cause the formation of canopy gaps [73] and fire disturbance, which peaks six months before the El Niño in Eastern Borneo, and during El Niño in Western Borneo [75], prior to seed dispersal. Similarly, in boreal forests of Northern America the onset of El Niño leads to regional drought and heat pulses responsible for both fire disturbance and floral bud initiation in P. glauca (Figure 4 -left), resulting in masting the ensuing year [7]. This alignment benefits spruce recruitment because seeds dispersed shortly after fire germinate more easily due to partial litter consumption, and seedlings can establish in canopy openings [76]. ...
Context 5
... examples are the interaction between Araucaria araucana and the Austral parakeet, which is highly mobile [104] and effectively satiated by seeding synchrony over distances of 10-100 km [105]. A similar interaction occurs between Dipterocarps and large bodied, highly mobile generalist predators (Pongo pygmaeus, Sus barbatus) in Borneo [1,106] (Figure 4). Over 800,000 pigs were observed migrating out of Northeast Kalimantan after the 1983 Dipterocarp mast event and severe El Niño-associated drought [107]. ...
Citations
... Moreover, in some species tree and leaf growth is reduced in years of high seed production, creating large-scale fluctuations in carbon sequestration [14][15][16] . The spatial scale of synchrony is a key aspect that amplifies the ecological importance of year-to-year variation in seed production [17][18][19] . However, several key questions on how plants synchronize masting over such extensive spatial scales remain unanswered. ...
... The synchronized, substantial year-to-year variation in seed production effectively starves seed consumers in low-seeding years, making it easier to satiate these consumer populations in mast years 56 . High regional synchrony of masting appears to have a selective advantage, as it allows trees to satiate mobile seed consumers (such as highly mobile vertebrates 9,18 ) that can prevent regeneration if mast years are localized 57 . Large-scale synchrony also increases the likelihood of seed release into disturbed areas 18 . ...
... High regional synchrony of masting appears to have a selective advantage, as it allows trees to satiate mobile seed consumers (such as highly mobile vertebrates 9,18 ) that can prevent regeneration if mast years are localized 57 . Large-scale synchrony also increases the likelihood of seed release into disturbed areas 18 . Variation in day length provides a reliable signal of seasonal shifts and is unaffected by climatic changes in space and time 58 . ...
High interannual variation in seed production in perennial plants can be synchronized at subcontinental scales with wide consequences for ecosystem functioning, but how such synchrony is generated is unclear1–3. We investigated the factors contributing to masting synchrony in European beech (Fagus sylvatica), which extends to a geographic range of 2,000 km. Maximizing masting synchrony via spatial weather coordination, known as the Moran effect, requires a simultaneous response to weather conditions across distant populations. A celestial cue that occurs simultaneously across the entire hemisphere is the longest day (the summer solstice). We show that European beech abruptly opens its temperature-sensing window on the solstice, and hence widely separated populations all start responding to weather signals in the same week. This celestial ‘starting gun’ generates ecological events with high spatial synchrony across the continent.
... Other authors confirmed this pattern, concluding that A. araucana has a high variability in annual cone production (Sanguinetti andKitzberger 2008, 2009;Sanguinetti 2014). We explained this pattern with the hypothesis of the economy of scale, where by concentrating reproductive efforts in a few events is more efficient (Silvertown 1980;Bogdziewicz et al. 2020;Ascoli et al. 2021;Zhang et al. 2022). We know that the costs of reproduction are defined in terms of losses in potential future reproductive success that current investments in reproduction causes (Seget et al. 2022). ...
Background
Araucaria araucana is a mast species that presents a high variability in annual cone production. Researchers have recorded synchronization events in cone production in different populations, which allows the seed production to be concentrated, reducing the percentage of seeds consumed by different animal species.
Methods
We sampled three populations located in the Andes Mountains, Araucanía Region, Chile. In 2004 we began the collection of data on cone production, for which we installed permanent plots (1200 m ² each) at each location. We identified and labeled each female tree in each plot to monitor its cone production. In 2012 we selected a total of 30 trees near the plots to evaluate the number of seeds per cone. In each February from 2012 to 2014 we selected two mature cones and covered them with a porous mesh for subsequent collection and storage in March. At the beginning of June, we counted and weighed the seeds, determining the average weight, the number of seeds per cone, the germination capacity (GC), and the germination speed (GS).
Results
Cone production was synchronous across the three locations. We observed significant differences among the locations and years evaluated. The cones had fewer seeds in 2013 (high production) compared to those in 2012 (low production), but their weights were similar. In 2014 the cones produced smaller seeds in fewer quantities. The difference between the years 2013 and 2014 resulted from the high-energy expenditure in 2013. Regarding GC and GS, there were significant differences among the three locations (GC: F = 45.41, p < 0.01; GS: F = 96.08, p < 0.01), where the highest values were observed in 2013.
Conclusions
Both GC and GS are related to seed weight but not to the number of cones produced in a given year. These annual fluctuations in seed production are determining factors in the population dynamics of forest species. Our results allow a better understanding of the reproductive phenology of A. araucana and could help define sustainable use and conservation actions for this species.
... 118subsequently, termed cue alignment(Pesendorfer et al., 2016;Ascoli et al., 2021). In European119 beech (Fagus sylvatica), for example, once ŕowers are initiated, spring weather conditions can 120 either enhance (in dry conditions) or impede (in wet conditions) pollination (Ascoli et al., 2017; 121 Journé et al., 2023). ...
Spatial synchrony is the tendency of spatially separated populations to display similar temporal fluctuations. Spatial synchrony may be tail-dependent, meaning it is stronger for peaks rather than troughs, or vice versa. High interannual variation in seed production in perennial plants, called masting, can be synchronized at subcontinental scales. Resulting resource pulses and periods of seed scarcity have important but distinct ecosystem consequences that are amplified by their scale of synchrony. In this study, we used data from 99 populations of European beech (Fagus sylvatica) sampled across the species range to examine whether masting synchrony differs between mast peaks and years of seed scarcity. The association between masting and the weather cue driving regional synchrony was stronger in the upper tails (corresponding to large values of the driver), translating into synchrony of mast peaks reaching 1000 km. However, the synchrony of seed scarcity was even higher, exceeding 1800 km. Consistently low seed production across a large range of low cue values homogenizes seed production across extensive spatial scales. Extensive synchrony in the masting lower tail means that famines caused by beech seed scarcity are amplified by their extensive spatial synchrony, with diverse consequences for food web functioning and climate change biology.
... In arid lands, for example, ENSO produces periodic rains that prompt eruptive plant growth (Yang et al. 2010). Similarly, North Atlantic Oscillation weather patterns influence tree masting (Ascoli et al. 2017(Ascoli et al. , 2021 as well as coastal phytoplankton productivity (Tiselius et al. 2016), and some regions of the Southern Ocean experience unusually strong diatom blooms in response to periodic shifts in wind and ice related to the SAM (Saba et al. 2014;Soppa et al. 2016). Such episodic resource availability can lead to a variety of ecological impacts, including skewed population age structures, local extinctions, and species coexistence that would not otherwise be sustained (Ostfeld and Keesing 2000;Drinkwater et al. 2003;Tam et al. 2008;Yang et al. 2010;Edwards et al. 2010Edwards et al. , 2013. ...
Between 1992 and 2018, the breeding population of Adélie penguins around Anvers Island, Antarctica declined by 98%. In this region, natural climate variability drives five‐year cycling in marine phytoplankton productivity, leading to phase‐offset five‐year cycling in the size of the krill population. We demonstrate that the rate of change of the Adélie breeding population also shows five‐year cycling. We link this population response to cyclical krill scarcity, a phenomenon which appears to have arisen from the interaction between climate variability and climate change trends. Modeling suggests that, since at least 1980, natural climate variability has driven cycling in this marine system. However, anthropogenic climate change has shifted conditions so that fewer years in each cycle now prompt strong krill recruitment, triggering intervals of krill scarcity that result in drastic declines in Adélie penguins. Our results imply that climate change can amplify the impacts of natural climate oscillations across trophic levels, driving cycling across species and disrupting food webs. The findings indicate that climate variability plays an integral role in driving ecosystem dynamics under climate change.
... It has lost much of its distribution since the arrival of the Europeans due to habitat transformation that has destroyed and fragmented many populations, and seedling recruitment is limited within the remnant populations (Tyler et al. 2006). Thus, understanding the role of the local biophysical environment on flowering and fruiting will give insight about the vulnerability of this foundation species to climate change (Ascoli et al. 2021). ...
Biologists have long debated why some plant species produce many seeds synchronously during some years and few during others. One hypothesis is that selection on phenological synchrony of flowering improves pollination efficiency and leads to increased fecundity. In an 11-year study of valley oak ( Quercus lobata ), we found that, indeed, trees that produced flowers during mid-season tended to produce more acorns. But, is synchrony the key factor? Here, we test the phenological synchrony hypothesis versus the alternative hypothesis that the environment principally shapes flowering phenology and acorn production. At our site, we find that a tree’s microenvironment is associated with both timing of phenology and acorn production. Timing of flowering depends on air temperature and crop size is not related to synchrony but is best predicted by relative elevation – likely a proxy for substrate quality and access to water. We conclude that microenvironment - not phenological synchrony - shapes acorn production.
... Mass flowering (masting) has attracted the interest of ecologists with the aim of gaining a mechanistic understanding of this mysterious phenomenon (Koenig andKnops 2005, 2021;Pesendorfer et al. 2021). Studies have focused on unravelling the adaptive consequences of masting by developing several hypotheses (Kelly 1994;Ascoli et al. 2021;Pesendorfer et al. 2021). Predator satiation -decreasing the predator population by starving them during years of low plant reproduction and reducing the rate of seed predation in masting years -is a leading hypothesis to explain the evolutionary origin of masting (Janzen 1971(Janzen , 1974. ...
Bamboos are known for flowering simultaneously over a wide geographic range at long intervals of more than several decades. Florivory by Dicraeus phyllostachyus and D. nartshukae causes severe damage to bamboo seed production. However, the nature of the life history of the two Dicraeus species, particularly how they sustain populations during non-masting years of bamboos such as their host plant range, is poorly explored. We hypothesised that the two Dicraeus species host on other plant species and/or on non-floral organs of bamboos and move to bamboo florets during masting years. We tested whether the two Dicraeus species oviposit and develop on florets of grasses excluding bamboos (other grasses), and on non-floral organs of bamboos, including branch buds and bamboo shoots, by conducting a natural population survey and laboratory experiments. We found that the two Dicraeus species utilise short, slender shoots of Phyllostachys nigra var. henonis and a few other grass florets in the natural populations. Laboratory experiments also showed that the two Dicraeus species oviposited and fed on non-floral organs of bamboos and several species of other grass florets, although the oviposition rate and number of eggs varied among organs and the survival rate was low on most other grass florets. The generalised feeding ability may have enabled the two Dicraeus species to utilise the bamboo florets during masting years and become the dominant florivorous insect of bamboos. Unravelling their life history strategies may contribute to understanding adaptation in florivorous insects of masting plants as well as their impact on the evolution of masting in plants.
... 435) remarked that this level of acceptance is "perhaps beyond what is warranted by the data." At the same time, the attention of researchers began to shift toward other (nonexclusive) explanations of masting, mostly the pollination efficiency hypothesis [stating that wind pollination is more effective when plants flower in synchrony (32)(33)(34)] but also others, such as environmental prediction [masting anticipates favorable conditions for recruitment (35)] or predator dispersal [masting attracts scatterhoarding seed dispersers (9)]. With plenty of other explanations, the venerable hypothesis of predator satiation was no longer the center of researchers' attention, but data on seed crops and levels of seed predation kept Significance Masting, or synchronous production of large seed crops, is widespread among plants. ...
Significance
Masting, or synchronous production of large seed crops, is widespread among plants. The predator satiation hypothesis states that masting evolved to overwhelm seed predators with an excess of food. Yet, this popular explanation faced few rigorous tests. We conducted a meta-analysis of studies that related the magnitude of seed production to the intensity of seed predation. Our results validate certain theoretical notions (e.g., that predator satiation is more effective at higher latitudes) but challenge others (e.g., that specialist and generalist consumers differ in the type of functional response to masting). We also found that masting is losing its ability to satiate consumers, probably because global warming affected masting patterns. This shift might considerably impair the reproduction of masting plants.
... The link between extreme humid-dry climatic events and wildfires and subsequent P. oocarpa regeneration in this study reflects the correlation between climate variability and synchronous reproduction in seed plants in most of the Earth's biomes (Ascoli et al. 2021). For instance, in boreal forests of North America, the onset of El Niño leads to regional drought and heat pulses that facilitate both wildfires and floral bud initiation in Picea glauca. ...
... For instance, in boreal forests of North America, the onset of El Niño leads to regional drought and heat pulses that facilitate both wildfires and floral bud initiation in Picea glauca. The masting in the following year, as well as the reduction in litter and creation of canopy openings caused by fire, favours P. glauca recruitment (Ascoli et al. 2021). ...
Historical information on wildfires and dendrochronological studies offer meaningful clues about fire and climate regimes, factors that affect forest structure and dynamics. This study aimed to determine the effect of fire history on vegetation dynamics and successional pathways of areas under different fire management policies in the Lagunas de Montebello National Park (LMNP), Chiapas, México. The selected study sites were El Parque area under fire exclusion policies since 1961; Tziscao-inhabited area under fire prohibition since 1984; and Antelá area with a traditional agricultural fire management history. A Pinus oocarpa ring-width chronology was used as a proxy for climate variability to which wildfire occurrence was mapped and to determine the establishment patterns of this dominant species. Current vegetation composition and structure and fuel loads were determined to characterise the study sites. Large wildfires, like those occurring in 1984 and 1998, were associated with periods of high humidity followed by intense droughts; they were linked to strong El Niño events and severely impacted the LMNP. Vegetation dynamics indicated simplification of mesophyll forest (climax) to pine-oaksweetgum forests, with Pinus dominating the overstorey in all sampling sites. Pine, oak and sweetgum species were the dominant juvenile trees in Antelá, El Parque and Tziscao, respectively. Late-successional seedlings (i.e., Prunus) were present in Antelá and El Parque, while were absent from Tziscao where several wildfires had occurred. Fuel accumulation in sites within protected areas subject to fire exclusion policies was very high (40-68 t ha⁻¹); in contrast, it was the lowest in rural Antelá (24 t ha⁻¹). Considering vegetation vulnerability to wildfires associated with extreme humid-dry climate events, increased fire hazard due to fuel accumulation, and the socio-ecological impacts of these events, we recommend revising the fire exclusion policies currently implemented in the LMNP and applying an integrated fire management approach that incorporates local socio-ecological conditions.
... The link between extreme humid-dry climatic events and wildfires and subsequent P. oocarpa regeneration in this study reflects the correlation between climate variability and synchronous reproduction in seed plants in most of the Earth's biomes (Ascoli et al. 2021). For instance, in boreal forests of North America, the onset of El Niño leads to regional drought and heat pulses that facilitate both wildfires and floral bud initiation in Picea glauca. ...
... For instance, in boreal forests of North America, the onset of El Niño leads to regional drought and heat pulses that facilitate both wildfires and floral bud initiation in Picea glauca. The masting in the following year, as well as the reduction in litter and creation of canopy openings caused by fire, favours P. glauca recruitment (Ascoli et al. 2021). ...
Historical information on wildfires and dendrochronological studies offer meaningful clues about fire and climate regimes, factors that affect forest structure and dynamics. This study aimed to determine the effect of fire history on vegetation dynamics and successional pathways of areas under different fire management policies in the Lagunas de Montebello National Park (LMNP), Chiapas, México. The selected study sites were El Parque area under fire exclusion policies since 1961; Tziscao-inhabited area under fire prohibition since 1984; and Antelá area with a traditional agricultural fire management history. A Pinus oocarpa ring-width chronology was used as a proxy for climate variability to which wildfire occurrence was mapped and to determine the establishment patterns of this dominant species. Current vegetation composition and structure and fuel loads were determined to characterise the study sites. Large wildfires, like those occurring in 1984 and 1998, were associated with periods of high humidity followed by intense droughts; they were linked to strong El Niño events and severely impacted the LMNP. Vegetation dynamics indicated simplification of mesophyll forest (climax) to pine-oak-sweetgum forests, with Pinus dominating the overstorey in all sampling sites. Pine, oak and sweetgum species were the dominant juvenile trees in Antelá, El Parque and Tziscao, respectively. Late-successional seedlings (i.e., Prunus) were present in Antelá and El Parque, while were absent from Tziscao where several wildfires had occurred. Fuel accumulation in sites within protected areas subject to fire exclusion policies was very high (40-68 t ha-1); in contrast, it was the lowest in rural Antelá (24 t ha-1). Considering vegetation vulnerability to wildfires associated with extreme humid-dry climate events, increased fire hazard due to fuel accumulation, and the socio-ecological impacts of these events, we recommend revising the fire exclusion policies currently implemented in the LMNP and applying an integrated fire management approach that incorporates local socio-ecological conditions.
... Long-term climatic cycles, such as El Niño Southern Oscillation (ENSO) events, could also play a role, particularly in rainfed systems that we may expect to exhibit stronger variability than their irrigated counterparts. ENSO phases have been shown to induce synchrony in masting systems [35,[65][66][67], but knowledge of ENSO effects on crop plants is largely limited to annual crops [68,69]. As a primary source of climate variation in Brazil and Iran, ENSO could be a cause of periodic yield in Brazilian tangerine and Iranian apricot (figure 4e,f; [70,71]). ...
Cyclical fluctuations in reproductive output are widespread among perennial plants, from multi-year masting cycles in forest trees to alternate bearing in horticultural crops. In natural systems, ecological drivers such as climate and pollen limitation can result in synchrony among plants. Agricultural practices are generally assumed to outweigh ecological drivers that might synchronize alternate-bearing individuals, but this assumption has not been rigorously assessed and little is known about the role of pollen limitation as a driver of synchrony in alternate-bearing crops. We tested whether alternate-bearing perennial crops show signs of alternate bearing at a national scale and whether the magnitude of national-scale alternate bearing differs across pollination syndromes. We analysed the Food and Agriculture Organization of the United Nations time series (1961–2018) of national crop yields across the top-producing countries of 27 alternate-bearing taxa, 6 wind-pollinated and 21 insect-pollinated. Alternate bearing was common in these national data and more pronounced in wind-pollinated taxa, which exhibited a more negative lag-1 autocorrelation and a higher coefficient of variation (CV). We highlight the mutual benefits of integrating ecological theory and agricultural data for (i) advancing our understanding of perennial plant reproduction across time, space and taxa, and (ii) promoting stable farmer livelihoods and global food supply.
This article is part of the theme issue ‘The ecology and evolution of synchronized seed production in plants’.
