Ann. N.Y. Acad. Sci. ISSN 0077-8923

A N N A L S O F T H E N E W Y O R K A C A D E M Y O F SC I E N C E S Issue: The Year in Ecology and Conservation Biology

Resource depletion, pollen coupling, and the ecology of mast seeding Elizabeth E. Crone and Joshua M. Rapp Department of Biology, Tufts University, Medford, Massachusetts Address for correspondence: Elizabeth E. Crone, Department of Biology, Tufts University, 163 Packard Ave., Medford, Massachusetts 02155. [email protected]

Masting, the highly variable and synchronous production of seeds across a population of perennial plants, is an ecologically important, but still poorly understood, phenomenon. While much is known about the fitness benefits of masting and its effects on seed consumers and trophic interactions, less is understood about the proximate mechanisms of masting. The resource budget model (RBM) posits that masting requires more resources than plants can gain in a single year. Individual plants store resources until a threshold is reached and then produce seeds, which depletes resources so that plants cannot reproduce again for 2 or more years. Individuals are synchronized by pollen coupling or environmental forcing. We review the assumptions of these models and assess the extent to which they are consistent with general patterns in plant populations. We discuss the implications of the RBM for how plants respond to changes in the external environment. Overall, the RBM is a likely cause of synchrony in many, but not all, masting species. This mechanistic hypothesis also leads to specific, but not always intuitive, expectations about how plant resources affect mast seeding. Keywords: mast seeding; alternate bearing; resource budget model; pollen coupling; nonstructural carbohydrates

Introduction Synchronous, highly variable reproduction of perennial plants, often known as mast seeding, has long been of interest to plant ecologists.1,2 Past reviews3–5 suggest that noticeably synchronous flowering and/or seed set are common in plant populations.6–14 Synchronous alternate bearing (i.e., 2-year reproductive cycle) is also widely reported in fruit and nut crops (e.g., citrus,15 apple,16 pistachio,17 pecan,18,19 avocado,20 and olive21 ).22,23 Similarly, across a broad group of woody plants, reproductive output is bimodally distributed in time.3,24,25 In other words, many plant populations fluctuate between high and low years of flowering, with fewer average years. In the 20th century, most ecological research on mast seeding addressed one of three distinct aspects of mast seeding. First, a large body of research has evaluated ways in which mast seeding increases plant fitness. Mechanisms of increased seed output or survival when many seeds are produced are

often called economies of scale.1,2,4,5 Numerous possible economies of scale have been proposed, three of which have been widely tested and supported: predator satiation, meaning the proportion of seeds consumed by seed predators is inversely correlated with the number of seeds produced; pollination efficiency, meaning plants are pollen limited in low- but not high-flowering years; and enhanced seed dispersal. Kelly and Sork5 review numerous examples of reduced seed predation in mast years and increased pollination efficiency for wind-pollinated species in high-flowering years.10,26 Enhanced seed dispersal is less well supported, with improved dispersal by scatter-hoarding animals in mast years largely being the result of animals failing to retrieve cached seeds (i.e., postdispersal predator satiation).27 However, an increased probability of seed dispersal in mast years has been confirmed in some species, mainly pines.28–30 Second, mast seeding causes a diverse array of phenomena at higher trophic levels, including outbreaks of rodents and rodent-borne diseases,31,32

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wildlife–human interactions,33–35 and fluctuations in animal populations.36–42 Mast seeding is now recognized as a prominent example of a resource pulse, with cascading effects at higher tropic levels.43–45 The third body of research involves resource, climate, or weather cues that trigger flowering or fruiting in plants.1,4,5 In some cases, these resource cues directly relate to a plant’s ability to gain resources or produce reproductive structures.46–51 In other species, particular patterns of temperature and drought appear to cue reproduction.52–57 We find this body of literature less satisfying than the first two because resource environmental cues vary somewhat arbitrarily among studies, even for related species. For example, in dipterocarps, Ashton et al.58 report mast seeding in Malaysia after the temperature dropped 2 ºC in 3 days, while Sakai et al.57 reported that El Ni˜no–related drought cues masting in Borneo, but Hamann59 did not find a correlation between El Ni˜no/La Ni˜na events and flowering in the Philippines. In one striking example of a lack of environmental cues, Crawley and Long60 correlated 276 weather variables with acorn production in oaks and found two significant correlates, noticeably less than would be expected by random chance, if seed production were normally distributed over time. Furthermore, we know of only three cases61–63 where researchers have used manipulative experiments to test cues for masting that were derived from statistical correlations. In two of the cases,61,62 the manipulations failed to cause the predicted increased flowering in the subsequent year, and in the third,63 a temperature threshold prevented flowering as expected from statistical correlations. One hypothesis for these aberrant patterns is that correlative studies tend to explore a large number of environmental variables, relative to the length of the time series, and are likely to lead to spurious conclusions. This does not mean that weather cues cannot trigger flowering or that different cues cannot trigger flowering in different species. Indeed, if masting is selectively favored by an economy of scale, any weather cue that allowed reproductive synchrony would suffice.5,64,65 However, a more mechanistic understanding of the physiology of mast seeding could help to resolve this discrepancy. Beginning in 1997, theoretical ecologists introduced a new way of thinking about the proximate mechanisms that cause plants to reproduce synchronously. Rather than direct climate cues, mast 22

seeding could reflect temporal patterns of individual resource allocation and costs of reproduction. In a series of related resource budget models (RBMs), Isagi et al.,66 Satake and Iwasa,67,68 and Satake and Bjørnstad69 assumed that an individual plant requires more resources to flower and set seed than it gains in a year and therefore flowers only above some threshold amount of stored resources. These rules cause plants to have alternate-year or chaotic patterns of reproduction over time, if seed production depletes stored resources.66 Given alternateyear reproduction by individuals, small amounts of correlated environmental variation can potentially synchronize individuals within plant populations (Fig. 1).70,71 Furthermore, if plants are pollen limited in low-flowering years, synchronous mast seeding could occur in the absence of any environmental variation.67 In this review, rather than revisiting past reviews of evolutionary causes and ecological consequences of mast seeding, we focus on the resource budget hypothesis. Seventeen years after its introduction, to what extent is the idea supported by empirical evidence? This evidence comes from two sources: a limited body of research designed to evaluate the resource budget hypothesis per se for particular species and a more extensive body of general studies in plant ecology that test its assumptions. To put this review in context, we describe each assumption of the RBM in detail before describing the evidence. We also discuss the implications of this hypothesis for both understanding mast seeding and predicting changes in seed production in variable environments. Resource budget models Reproduction depletes stored resources Theoretical background. The core assumption of the resource budget hypothesis is a model of resource allocation to reproduction by individual plants. In any given year, plants acquire some amount of resources, a fraction of which are allocated to reproduction, and a fraction of which are allocated to other functions. For simplicity, the amount of resources is not explicitly modeled; instead the annual resource acquisition refers to the amount of resources acquired and allocated to reproduction in each year. Resources allocated to reproduction accumulate in a pool of stored resources. Once this pool is above a minimum

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Mechanisms of mast seeding

Figure 1. Hypothesized proximate mechanisms of synchronous mast seeding. Of the three possible ways in which resource dynamics can be synchronized, variation in resource acquisition is not widely supported by theoretical models, but factors that prevent reproduction (pollen coupling and environmental constraints) are.

threshold needed for reproduction, plants produce flowers (or similar reproductive structures, for example, cones in pines). In the simplest version of the model, plants then produce fruits and seeds in proportion to how much they flowered. If the cost of seed production is low relative to annual resource gain, plants produce seeds every year. If the cost of seed production is high relative to annual resource acquisition, plants reproduce at super-annual intervals. As costs of seed production increase, seed production by individuals is biennial, then has more erratic cycles, then is chaotic.66 Empirical patterns. Experimental tests have tended to confirm the assumption that masting depletes resources, preventing flowering in the next year. In one of the few experimental tests of the RBM, Crone et al.72 removed flowers from plants to prevent seed set, leading to larger nonstructural carbohydrate (NSC) stores and flowering again in the following year. Plants that were allowed to set seed had diminished NSC stores and did not flower in the following year. In another experimental test of resource depletion, production of male flowers in Cryptomeria japonica was positively related to sunshine in the previous year, and experimental shading reduced NSC stores and flowering.73 Experimental watering and fertilizing prompted a mast flowering

event in Juniperus thurifera, but not all flowering events resulted in mast seeding in natural populations, likely because of drought-induced resource limitation.74 Observational studies have been more equivocal, but some studies have found evidence for NSC depletion after reproduction. Among individual oak trees, reproductive biomass tracked productivity, with more productive trees allocating more to female reproductive function and producing more acorns.75 Also, flowering depleted NSC in an understory palm in Costa Rica, even though experimental defoliation did not; however, defoliation depressed subsequent flowering, suggesting that plants allocated resources to storage before allocating them to reproduction.76 Carbon dioxide (CO2 ) fertilization also led to Pinus taeda trees reaching reproductive maturity faster and producing more seeds.77 In contrast, Hoch et al.78 interpreted relatively minor changes of NSC in leaves, branches, and stems across the growing season in ten temperate tree species from Europe, as evidence that trees in general are not carbon limited. In particular, while NSC declined in mid-summer during a mast year in Fagus sylvatica, levels rebounded by the end of the season, suggesting that NSC levels were not strongly depleted by masting. Hoch et al.79 also used 13 C labeling to investigate whether stored or current

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photosynthate was used for flowering and fruiting in three temperate forest species, including F. sylvatica. Stored carbon was used for leaf expansion and flowering in all three species, but not for maturing fruits. In Japan, 14 C dating of seeds from 10 masting tree species showed that the carbon used in producing the seeds was less than 1.4 years old for all species, and carbon age was not related to masting behavior, suggesting that carbon stores did not drive masting dynamics.80 In a remarkable study in which whole-tree NSC was calculated by excavating and chipping whole trees, starch stored in a low seed production year could only account for 8% of fruit production in a mast year in a pistachio orchard.81 However, growth was lower during the mast year, suggesting a shift in allocation of current photosynthate from growth to reproduction. Defoliating and girdling experiments at the shoot level in Dryobalanops also suggested that current photosynthate, and not stored NSC, was used in fruit maturation,82 consistent with other species (e.g., peach83 and alder84 ).85 Although the RBM is framed with respect to carbon gain, similar dynamics could occur for any resource that limits reproduction. For example, seeds are strong nitrogen sinks, and several studies have found evidence for nitrogen dynamics in relation to masting. Immature cone removal experiments in Pinus albicaulis showed that seed production depleted nitrogen and phosphorous, but not NSC,86 a result that is broadly consistent with the idea the seed production depletes limiting resources, but not with the specific assumption that NSC limits seed production. In Fagus crenata, N content was also lower in leaves and xylem during a mast year.87 The same species had fewer leaves during a mast year, and dry mass and N content of leaf buds was lower in winter buds following a mast year.88 In two Mediterranean oak species, reproductive shoots were larger and produced more leaves than vegetative shoots; however, the nitrogen content of these leaves was lower than that of vegetative shoots.89 Two Chionochloa species flowered more prolifically on patch edges where nitrogen was more available.90 Lower nitrogen content of leaves is correlated with lower photosynthetic capacity.91 This may explain why, in Ocotea tenera, photosynthetic capacity was negatively correlated with fruit production.92 Finally, decreases in whole-tree nutrient content after heavy repro24

duction have been reported in several alternatebearing crop species, including pistachio,93 citrus,94 and prune.95 Overall, masting effects on resource pools are common but not ubiquitous. In a general review of the costs of reproduction in plants, Obeso96 found that reproduction reduced somatic resource pools in 85% (11/13) of studies. However, resource depletion after seed production is not sufficient to cause periodic reproduction; resource depletion must also be linked to lower probability of future flowering. Many studies that do not measure resources directly corroborate this expected demographic pattern. Manipulations that increase seed production (e.g., by supplemental pollination)97,98 in 1 year tend to decrease the probability that a plant flowers in the following year. Manipulations that decrease seed production (e.g., by pollinator exclusion or flower removal)99 in 1 year tend to increase the probability that a plant flowers in the next. As of Obeso’s 2002 review,96 70% (28/40) of studies that tested for demographic costs of seed production with respect to future flowering have shown such costs. Pollen coupling can synchronize reproduction Theoretical background. Resource depletion after reproduction causes individual plants to produce seeds at supra-annual intervals. In order for masting to occur, there must be something that causes all plants to produce their seeds in the same years. One mechanism of synchronous seed production is density-dependent pollen limitation, which is often referred to as pollen coupling in this context. The idea, first introduced by Isagi et al.66 and formalized by Satake and Iwasa,67 is that plants are pollen limited in low- but not in high-flowering years. If a plant produces flowers in a low-flowering year, few of its ovules are fertilized, and so it makes few seeds. If flowers require few resources relative to seeds, the plant does not deplete stored resources and is able to produce flowers in the next year. The plant continues to flower again until there is a high-flowering year. In the high-flowering year, the plant is pollinated, produces seeds, depletes stored resources, and becomes synchronized with the rest of the population. Satake and Iwasa define density-dependent pollen limitation as the strength of the relationship between the density of flowering plants and the proportion of flowers that are pollinated on a focal (flowering) plant. If resource depletion parameters

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cause plants to flower in alternate years, any amount of density-dependent pollen limitation will cause plants to flower synchronously. As resource depletion becomes more severe, and reproduction by individuals becomes mathematically chaotic, stronger levels of density-dependent pollen limitation are needed to synchronize individual plants within a population. Empirical patterns. Pollen limitation in general has been widely reviewed by plant biologists.100–103 However, the specific assumption of pollen coupling is that plants experience density-dependent pollen limitation, where density is the density of flower production in a given year, and plants experience higher pollen limitation in low- than in high-flowering years. For monoecious and dioecious species, density-dependent pollen limitation also includes the implicit assumption that the years in which plants produce few female flowers are also the years in which pollen production is relatively low. Constant pollen limitation (in all environmental conditions) would not lead to the feedbacks that synchronize reproduction. Similarly, weather conditions that prevent pollen production or transfer act like environmental constraints to reproduction (as discussed in a subsequent section) and do not produce the density-dependent feedbacks that are found in pollen coupling models. Relatively few studies have tested for pollen coupling, in the form of density-dependent pollen limitation among years. Forsyth104 used a combination of observation and supplemental pollination experiments to show that populations of the endangered Haleakala silversword (Argyroxiphium sandwicense subsp. macrocephalum) had lower seed set and were more pollen limited in low-flowering years. Crone and Lesica61 used similar methods and found similar results for Astragalus scaphoides, an iteroparous perennial (20-year life span)105 bee-pollinated forb that flowers in alternate years. Rapp et al.106 used a monitoring study to show that, for whitebark pine (P. albicaluis), a mast-seeding tree, initiation of male and female cones was highly correlated in time, and female cones were more likely to mature in highpollen years. Other monitoring studies have shown synchronous flowering of male and female trees in J. thurifera74 and a positive correlation between seed production and seed maturation or viability in the dioecious tree Dacrydium cupressinum65 and in

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several monoecious trees.107–113 In partial support of density-dependent pollen limitation, plants of Aciphylla squarrosa—an iteroparous, dioecious, moderately long-lived herb—were not pollen or resource limited (with respect to seed set) in a mast year, but reducing floral display caused lower seed set.114 As another line of partial support, supplemental pollination is widely used to increase seed yield in conifer seed orchards,115–117 and Smith et al.26 used qualitative observations of densitydependent pollen limitation to parameterize theoretical models of density-dependent pollen limitation in pines. A larger body of studies has shown densitydependent pollen limitation in space, largely in the context of Allee effects and conservation of small or isolated populations. These effects are common in animal-pollinated plants.118–131 Fewer studies have investigated density-dependent pollen limitation in wind-pollinated plants.132 However, for a wind-pollinated estuarine grass, pollen limitation was greater in lower-density patches,133 leading to faster population growth at higher density. Similarly, distance-related pollen limitation was observed in other wind-pollinated herbs.134–136 Pollination also increases with pollen production by neighboring trees in Taxus canadensis, a windpollinated tree,137 and in blue oak.138 In F. sylvatica, the proportion of empty seeds decreased with forest patch size.139 Nonetheless, as with resource depletion, density-dependent pollen limitation is not ubiquitous. Hesse and Pannell140 studied densitydependent pollen limitation in the wind-pollinated herb Mercurialis annua. Pollen limitation was greater in smaller populations of dioecious, but not of self-compatible monecious, plants. Higher plant densities can also lead to competition for pollinators or other resources, leading to lower seed set.141,142 Fluctuations in resource gain cannot synchronize reproduction Theoretical background. In principle, environmental conditions that influence resource availability can also help synchronize masting in the presence of underlying resource dynamics. Moran postulated that populations with similar internal dynamics would become synchronized by correlated environmental conditions,143 a phenomena that became known as the Moran effect.144,145 However, somewhat surprisingly, variation in resource-related

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parameters is not especially effective at synchronizing reproduction. Satake and Iwasa68,70 analyzed models that included correlated environmental variation in two of the resource budget parameters: the annual resource gain and the threshold for reproduction. In both cases, large among-year correlations in resource-related parameters did not lead to synchronized reproduction over most regions of parameter space. The problem is that, in the RBM, periodic mast seeding can be mathematically chaotic. In this model, periodic reproduction is also mathematically chaotic in many regions of parameter space (i.e., plants reproduce synchronously at approximately 2- to 3-year cycles, but the time series is mathematically chaotic, cf. Satake and Iwasa67 and Isagi et al.66 ). This means that both resource gain (or the threshold for reproduction) and initial resource levels must be identical across individual plants in order for them to remain synchronized. Only when resource depletion is small and reproduction is in approximately 2-year cycles can environmental noise synchronize individuals.70 Environmental variation in these variables can enhance synchrony driven by pollen coupling, but the pollen coupling is necessary to align plants in the first place. Empirical patterns. We know the most, and the least, about how variation in resource gain influences mast seeding. On one hand, a role for the Moran effect in synchronizing reproductive dynamics is indicated by a number of studies; on the other hand, variation in seed production that merely reflects available resources, which in turn are determined by environmental conditions, is known as resource matching, not mast seeding.4 Resource matching is the null expectation for reproduction in the absence of an evolved response to either increase the variability of reproduction (masting) or make reproduction more constant than the environment. Few empirical studies have explicitly linked variation in primary productivity to plant resource budgets (see review and discussion by Miyazaki146 ). Most studies supporting a role for the Moran effect do not also provide evidence for masting—changes in resource allocation into and out of reproduction or a negative autocorrelation in seed production among years.5 One expectation of the Moran effect is that the spatial synchrony of masting caused by environmental variability should be no greater than that 26

of the environmental variability,147 which generally declines with distance.148 Geographic patterns of masting in relation to environmental conditions are generally consistent with this mechanism of synchrony. Rosenstock et al.149 observed declining synchrony with distance in a pistachio orchard, while Koenig and Knops147 observed a similar pattern in oaks across California. Geburek et al.150 studied patterns of pollen production of 12 temperate tree genera in Austria, classifying five of the genera as masting pollen producers. In three of these genera (Fagus, Larix, and Picea), spatial synchrony was correlated with distance among sites, consistent with the Moran effect. While mast years were synchronous, the correlation of temporal patterns of seed production of Nothofagaus solandri var. cliffortioides decayed across an elevational gradient in New Zealand,151 consistent with an environmental influence on synchrony. Water availability, a limiting resource, was more strongly correlated with masting patterns than pollen availability in Mediterranean oaks,152 also supporting a role for resources in synchronizing reproduction. Stronger tests of the role of resource fluctuations in synchronizing reproduction come from RBMs parameterized to resource gain on the basis of weather conditions, but these are few. An RBM of birch pollen production, including weather conditions expected to affect resource conditions in the previous 2 years, explained 94.5% of variance in the current year’s pollen production.153 In Astragalus schaphoides, models including only heterogeneous resource acquisition and pollen limitation were necessary and sufficient to explain masting dynamics, but including precipitation improved model fit.154 Flowering was higher at upper patch edges where soil nitrate was elevated in Chionochloa, a masting tussock grass, with a larger effect at higher altitude where plants are expected to be more resource limited due to a shorter growing season.90 Environmental constraints can synchronize reproduction Theoretical background. Ecologists studying mast seeding have long distinguished variation in resource gain from environmental cues that determine whether or not plants reproduce in a given year.4,64 Environmental variables for which a particular environmental condition (or set of conditions) determines whether plants reproduce do seem to

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synchronize reproduction by individual plants. Unlike environmental variation and pollen coupling, this possible mechanism of synchrony has received relatively little theoretical attention. Rees et al.71 analyzed a threshold model in which individual seed production fluctuated through time but required a threshold temperature in January (Austral midsummer) to initiate flowering. They did not present a global analysis of this model but did show that, for parameters tuned to Chionochloa pallens, a perennial bunch grass that flowers in approximately alternate years, observed frequencies of suitable years (0.42) led to alternate-year seed production in the presence of nonlinear resource dynamics (i.e., the resource budget hypothesis), but not in the presence of the environmental constraint alone. Lyles et al.155 demonstrate a similar phenomenon for alternate bearing in pistachio. They analyzed models in which the environment switches between three conditions: poor, average, and good. This form of discrete environmental variation led to synchronized mast seeding under a range of conditions. Although no one has done a comprehensive analysis of such models to date, it seems likely that environmental cues could increase the degree of synchrony in RBMs under a broad set of conditions. Our rationale for this assertion is that environmental cues and constraints are similar to pollen coupling in that a number of plants are not able to reproduce at all in some years, even if they have sufficient resource stores for reproduction. This forces multiple cohorts of plants onto the same periodic cycle. In years in which reproduction is not possible, plants would not deplete stored resources and should be able to flower during the next year. Under conditions that lead to 2-year cycles, this would synchronize reproduction, at least temporarily. Under conditions that lead to chaos, it might help synchronize enough plants to obtain masting at the population level. Environmental constraints do not have the immediate feedback mechanism of pollen coupling, in the sense that plants could remain out of phase for many years, depending on the number of years between the cues, relative to the time needed to recover resources after masting. Empirical patterns. In principle, environmental cues can result in masting without underlying resource dynamics. Most research in this area is focused on finding cues in the absence of resource

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dynamics. The common occurrence of negative autocorrelation of reproduction4,25 suggests that plants may respond to cues only when resource levels are sufficiently high. Thus, we briefly review cues and constraints to plant reproduction that seem to produce environmental thresholds for reproduction. Linking these mechanisms to resource dynamics of plants would be a valuable area for future research. One category of environmental cues is resource conditions that determine floral induction. Climate cues often associated with floral induction include drought52,54,56,57 and high temperatures.156–159 Drought as a cue is interesting because it would be expected to reduce resource acquisition by plants; high temperatures might increase or decrease resource acquisition, depending on the base climate. Kelly et al.55 showed a correlation between flowering and a difference in temperature between the previous two growing seasons for 15 plant species. Conditions during flowering can also be a cue if they lead to greater expression of previously induced floral buds.159 Satake160 differentiated between environmental effects on resources for fruit maturation versus environmental effects on floral induction (cues). Environmental constraints that prevent flower maturation are also common and likely to act as synchronizing mechanisms. For example, killing frosts prevent flowers from maturing.107,161,162 Weather during floral initiation can also negatively influence future seed production; drought during cone initiation is negatively correlated with cone production in P. taeda.163 Weather during pollination can also affect the onset of flowering and pollen release,152 and this can lead to biotic feedbacks that synchronize masting. For instance, weather-driven pollen limitation influences masting patterns in California oaks.147,164 Environmental conditions can also prevent reproduction via drought, causing fruit abortion.74 Drought negatively affected seed production of several shrub species in Canada.165 Implications of RBM How do resources limit mast seeding? The resource budget hypothesis emphasizes the importance of interpreting patterns of mast seeding in the context of overall plant resource budgets. This raises a number of unanswered questions in plant physiology. For example, the RBM is posed with

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respect to carbohydrate dynamics. NSCs are a natural resource to limit reproduction because sugar concentrations often signal developmental pathways for flowering.166–168 However, empirical studies show that seed production often depletes mineral nutrients but not carbohydrates, a pattern that may be especially common in trees.86 Changes in nutrients and carbohydrates are intimately linked. Higher nitrogen concentrations increase photosynthetic capacity.91 Plants also exchange carbon for nutrients via mycorrhizae.169 Another related question is, how large of a decline in resource stores after reproduction is needed to prevent flowering in the next year? One possible way to address this question is an empirical approach (i.e., measuring the probability of a plant flowering as a function of its resource stores, or comparing resource stores of flowering and nonflowering plants at the time of floral initiation).170 Another approach is to understand the mechanisms of floral induction with respect to candidate limiting resources (carbohydrates, nutrients, and possibly developmental constraints, e.g., meristems and hormone production), and how these are affected by reproduction. These processes have been studied by plant physiologists171 but have rarely been linked explicitly to resource dynamics in masting species (see Turnbull et al.159 for an example of hormone manipulation in a masting species). How does environmental variation affect mast seeding? In recent years, particularly in the context of climate change, ecologists have become interested in how variation in resource availability affects mast seeding. The answer to this question hinges on the mechanism of mast seeding. If masting depends only on an environmental cue (as opposed to an RBM), then knowing how that cue varies in space or time would predict changes in mast periodicity.55 If masting depends on nonlinear resource dynamics, then it is necessary to analyze model predictions under different resource conditions. In the RBM, changes in annual resource gain, such as increasing or decreasing primary productivity, change the magnitude of fluctuations in seed production but not the periodicity.69 More resources lead to higher seed production in mast years. Two experimental manipulations support this prediction. Changes in amplitude, but not periodicity, 28

of seed production occurred in response to fertilization to two masting trees: oaks (primarily Quercus rubra) in mixed hardwood forests in the northern United States172 and New Zealand mountain beech (Nothofagus solandri).173 However, observational studies suggest that mast years are more frequent in more productive environments (or less frequent and more variable in less productive environments; reviewed by Kelly and Sork).5 An observational study of New Zealand mountain beech correlated increasing temperature and carbon availability with more frequent intermediate seed years over decadal time periods.174 Rowan (Sorbus aucuparia) trees mast every 2 years in more productive climates in Norway and every 3 years in less productive climates.69 Shorter intervals between mast years observed in northern Europe in recent decades has also been attributed to reduced resource limitation due to some combination of warmer summertime temperatures, nitrogen deposition, or CO2 fertilization.87,158 In an interesting extension of RBMs, Satake and Bjornstad69 showed that, under a modified set of assumptions, systematic changes in annual resource gain or flowering thresholds could change the periodicity of flowering (e.g., populations shift from 3- to 2-year cycles with increasing annual resource gain). The specific assumption they modified was that plants cannot deplete resource stores indefinitely but reach a minimum resource level. Over some regions of parameter space, we expect increasing productivity to change seed production in mast years but not periodicity. As the annual productivity passes particular thresholds, the modified RBM predicts that periodicity will also change. If synchrony is driven by environmental cues or constraints, the response of masting depends on the change in the cue or constraint, as well as changing productivity. In their analysis of masting by Chionochloa, Rees et al.71 explored this possibility. They concluded that, if favorable conditions were to become more frequent, masting would fail because each plant would be able to reproduce as soon as it reached the resource threshold and would follow its own chaotic trajectory. We speculate that, similarly, if a cue were to become less frequent, or a constraint more frequent, mast seeding would become less frequent and more synchronized. In an extreme case, if reproduction is limited only by a cue that becomes so rare that all plants have sufficient

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resources when it occurs, reproduction could shift from being driven by resource dynamics to being driven by the frequency of suitable conditions only. Similarly, we can speculate that, if masting is synchronized by pollen coupling, changes in pollinator abundance and behavior for animal-pollinated species, and conditions for pollen production and transfer for wind-pollinated species, will be as important as changes in productivity for determining mast years. As the Chionochloa case study demonstrates, an RBM parameterized for a particular species provides specific predictions for how changes in the environment affect mast seeding. The unfortunate message of RBM is that, for species in which masting is driven by resource dynamics, these changes depend on the specific regions of parameter space. We do not have simple predictions, such as increasing resources increases the frequency of mast years, because the answer depends on the region of parameter space, and the synchronizing mechanism of mast seeding. Given the interest in how forests will respond to climate change, linking experimental understanding of resource allocation and environmental cues with mechanistic RBMs would be a valuable area for future exploration. Is the RBM a general mechanism for mast seeding? It is tempting to close this review by asserting whether the RBM could be a general mechanism for mast seeding. The short answer is that we do not yet have enough data to know. The general empirical patterns discussed in this review indicate that the necessary mechanisms (resource depletion after seed production, combined with pollen coupling or environmental constraints) are common, but not ubiquitous, in plants. Both conditions have been demonstrated in only three of the species described above: A. scaphoides61,72 and P. albicaulis86,106 show resource (NSC and P and N, respectively) depletion after seed production and density-dependent pollen limitation. C. pallens show resource depletion after seed production and an environmental constraint to flowering.71 Other species show patterns that are consistent with RBM assumptions, although the assumptions have been less rigorously tested in those cases. For example, reproduction seems to deplete mineral nutrients in pistachio,93 and RBMs driven by environmental constraints reproduce observed

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masting patterns.155 Horticulturalists often limit alternate bearing in fruit trees by thinning immature fruits,22 a management strategy that fits exactly with the resource depletion assumptions of RBM. In part, few examples exist because there are very few species in which both the assumption of resource depletion after seed production and one or more mechanisms of synchrony have been explicitly tested. We expect that more examples will accumulate as the assumptions are tested in more systems. Tests of model predictions, such as desynchronization and resynchronization of reproduction, will always be more rare, but these tests would also be a valuable area for future research. With this said, the RBM cannot be the only mechanism of synchrony. Most notably, mast seeding is known to occur in monocarpic plants, such as bamboo1 and silverswords.104 These species flower only once in the year before they die. Monocarps are relatively rare among masting plants.5 Nonetheless, masting cannot be synchronized by the way in which resource stores fluctuate after seed production. It would also not surprise us if weather cues alone were the cause of masting in some species. In the context of support for RBM, we think that it is okay that this mechanism does not apply to all species. Given the many ways in which mast seeding increases fitness, it is not surprising that it would arise in different ways in different evolutionary lineages. Given the importance of mechanisms for how mast seeding changes in relation to environmental drivers, understanding other mechanisms of masting, especially in monocarpic species, remains an intriguing question in ecology. Conflicts of interest The authors declare no conflicts of interest. References 1. Janzen, D.H. 1976. Why bamboos wait so long to flower. Annu. Rev. Ecol. Syst. 7: 347–391. 2. Silvertown, J.W. 1980. The evolutionary ecology of mast seeding in trees. Biol. J. Linn. Soc. Lond. 14: 235–250. 3. Herrera, C.M., P. Jordano, J. Guitian, et al. 1998. Annual variability in seed production by woody plants and the masting concept: reassessment of principles and relationship to pollination and seed dispersal. Am. Nat. 152: 576– 594. 4. Kelly, D. 1994. The evolutionary ecology of mast seeding. Trends Ecol. Evol. 9: 465–470. 5. Kelly, D. & V.L. Sork. 2002. Mast seeding in perennial plants: why, how, where? Annu. Rev. Ecol. Syst. 33: 427–447.

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