Reproductive success of individuals with different fruit production patterns. What does it mean for the predator satiation hypothesis?

The predator satiation hypothesis states that synchronous periodic production of seeds is an adaptive strategy evolved to reduce the pressure of seed predators. The seed production pattern is crucial to the predator satiation hypothesis, but there are few studies documenting the success of individuals that are in synchrony and out of synchrony with the whole population. This study is based on long-term data on seed production of Sorbus aucuparia and specialised pre-dispersal seed predation by Argyresthia conjugella, in a subalpine spruce forest in the Western Carpathians (Poland). At the population level, we tested whether functional and numerical responses of predators to the variation of fruit production operate. At the individual level, we tested whether individuals with higher interannual variability in their own seed crops and higher synchrony with the population have higher percentages of uninfested fruits. The intensity of pre-dispersal seed predation was high (average 70 %; range 19–100 %). There were both functional and numerical responses of predators to the variation of fruit production at the population level. We found that individuals that were expected to be preferred under seed predator pressure had higher reproductive success. With increasing synchrony of fruit production between individual trees and the population, the percentage of infested fruits decreased. There was also a negative relationship between the interannual variation in individual fruit production and the percentage of infested fruits. These results confirm selection for individuals with a masting strategy. However, the population does not seem well adapted to strong seed predation pressure and we suggest that this may be a result of prolonged diapause of A. conjugella.     

Within-season synchrony of a masting conifer enhances seed escape

Predator satiation resulting from interannual reproductive synchrony has been widely documented in masting plants, but how reproductive synchrony within a year influences seed escape is poorly understood. We evaluated whether the intra-annual reproductive synchrony of individual white spruce trees (Picea glauca) increased seed escape from their primary predispersal seed predator, North American red squirrels (Tamiasciurus hudsonicus). Trees with cones that matured synchronously relative to those of other trees within red squirrel territories were significantly more likely to escape squirrel predation in years with both low and superabundant levels of cone production, generating a significantly positive linear selection differential for increasing intra-annual reproductive synchrony. Thus, this masting plant escapes seed predation in numbers through interannual synchrony in seed production and in time through intra-annual synchrony of seed availability.     

Does a heavy fruit crop reduce the tree ring increment? Results from a 12-year study in a subalpine zone

Life history theory posits that an increased investment in reproduction should result in decreased vegetative investment. Switching resources from growth to reproduction are also expected in species experiencing selection pressure for high variation of seed crops. In this study, we tested whether the reproductive effort of trees, measured as the number of fruits produced, is related to their radial growth increment. We examined a population of Sorbus aucuparia, a fleshy-fruited tree species with highly variable interannual individual fruit production growing in the subalpine zone and under strong selection pressure from pre-dispersal seed predators. We used 12-year data to test the relationship between fruit crop and radial growth increments in current, previous and subsequent years, and found no trade-off between growth and reproduction. For almost all trees, there was no correlation between fruit crop and radial growth increment in the same year or next year. Only a few trees showed a positive correlation between fruit crop and previous-year growth. In the statistics, we took advantage of the high variability of individual fruit crops in high production years. In four heavy crop years, we compared the radial growth increments of trees with heavy crops with those of trees with low fruit crops. Current and next-year radial growth did not differ between trees with low and high fruit crops. In all those years, however, trees having heavy fruit crops had higher previous-year growth increments. We suggest that the harsh subalpine weather conditions account for the lack of a trade-off between growth and reproduction in the studied population.     

Measuring mast seeding behavior: relationships among population variation,individual variation and synchrony

Mast seeding, or masting, is the variable production of flowers, seeds, or fruit across years more or less synchronously by individuals within a population. A critical issue is the extent to which temporal variation in seed production over a collection of individuals can be viewed as arising from a combination of individual variation and synchrony among individuals. Studies of masting typically quantify such variation in terms of the coefficient of variation (CV). In this paper we examine mathematically how the population CV relates to the mean individual CV and synchrony, concluding that the relationship is a complex one which cannot isolate an overall measure of synchrony, and involves additional factors, principally the number of plants sampled and the mean productivity per plant. Our development suggests some simple approximate relationships of population CV to individual variability, synchrony and the number of individuals. These were found to fit quite well when applied to data from 59 studies which included seed production at the individual level.     

Reproductive collapse in European beech results from declining pollination efficiency in large trees

Climate warming increases tree mortality which will require sufficient reproduction to ensure population viability. However, the response of tree reproduction to climate change remains poorly understood. Warming can reduce synchrony and interannual variability of seed production (“masting breakdown”) which can increase seed predation and decrease pollination efficiency in trees. Here, using 40 years of observations of individual seed production in European beech (Fagus sylvatica), we showed that masting breakdown results in declining viable seed production over time, in contrast to the positive trend apparent in raw seed count data. Furthermore, tree size modulates the consequences of masting breakdown on viable seed production. While seed predation increased over time mainly in small trees, pollination efficiency disproportionately decreased in larger individuals. Consequently, fecundity declined over time across all size classes, but the overall effect was greatest in large trees. Our study showed that a fundamental biological relationship—correlation between tree size and viable seed production—has been reversed as the climate has warmed. That reversal has diverse consequences for forest dynamics; including for stand- and biogeographical-level dynamics of forest regeneration. The tree size effects suggest management options to increase forest resilience under changing climates.     

Aridity drives spatiotemporal patterns of masting across the latitudinal range of a dryland conifer

Masting, or the synchronous and irregular production of seed crops, is controlled by environmental conditions and resource budgets. Increasing temperatures and shifting precipitation regimes may alter the frequency and magnitude of masting, especially in species that experience chronic resource stress. Yet the effects of a changing climate on seed production are unlikely to be uniform across populations, particularly those that span broad abiotic gradients. In this study, we assessed the spatiotemporal patterns of masting across the latitudinal distribution of a widely distributed dryland conifer species, piñon pine Pinus edulis. We quantified seed cone production from 2004 to 2017 using cone abscission scars in 187 trees from 28 sites along an 1100 km latitudinal gradient to investigate the spatiotemporal drivers of seed cone production and synchrony across populations. Populations from chronically hot and dry areas (greater climatic water deficits and less monsoonal precipitation) tended to have greater interannual variability in seed cone production and smaller crop sizes. Mast years generally followed years with low vapor pressure deficits and high precipitation during key periods of the reproductive process, but the strength of these relationships varied across the region. Populations that received greater monsoonal precipitation were less sensitive to late summer vapor pressure deficits during seed cone initiation yet more sensitive to spring vapor pressure deficits during pollination. Spatially correlated patterns of vapor pressure deficit better predicted synchrony in seed cone production than geographic distance, and these patterns were conserved at distances up to 500 km. These results demonstrate that aridity drives spatiotemporal variability in seed cone production. As a result, projected increases in aridity are likely to decrease the frequency and magnitude of masting in these dry forests and woodlands. Declines in seed production may compound climatic limitations to recruitment and impede tree regeneration, with cascading effects for numerous wildlife species.     

Masting in ponderosa pine: comparisons of pollen and seed over space and time

Many plant species exhibit variable and synchronized reproduction, or masting, but less is known of the spatial scale of synchrony, effects of climate, or differences between patterns of pollen and seed production. We monitored pollen and seed cone production for seven Pinus ponderosa populations (607 trees) separated by up to 28?km and 1,350?m in elevation in Boulder County, Colorado, USA for periods of 4?C31?years for a mean per site of 8.7?years for pollen and 12.1 for seed cone production. We also analyzed climate data and a published dataset on 21?years of seed production for an eighth population (Manitou) 100?km away. Individual trees showed high inter-annual variation in reproduction. Synchrony was high within populations, but quickly became asynchronous among populations with a combination of increasing distance and elevational difference. Inter-annual variation in temperature and precipitation had differing influences on seed production for Boulder County and Manitou. We speculate that geographically variable effects of climate on reproduction arise from environmental heterogeneity and population genetic differentiation, which in turn result in localized synchrony. Although individual pines produce pollen and seed, only one-third of the covariation within trees was shared. As compared to seed cones, pollen had lower inter-annual variation at the level of the individual tree and was more synchronous. However, pollen and seed production were similar with respect to inter-annual variation at the population level, spatial scales of synchrony and associations with climate. Our results show that strong masting can occur at a localized scale, and that reproductive patterns can differ between pollen and seed cone production in a hermaphroditic plant.     

Masting and trophic cascades: interplay between rowan trees, apple fruit moth, and their parasitoid in southern Norway

We analyzed berry production in rowan, Sorbus aucuparia L., in southern Norway and examined the ramifying effects of rowan masting on the dynamics of the dominant seed predator and its parasitoid. The apple fruit moth, Argyresthia conjugella Zeller, is a pre-dispersal seed predator of rowan. The larva of the apple fruit moth rely on rowan berries, which in turn is attacked by the parasitoid wasp, Microgaster politus Marsh. We found classic masting in rowan: berry production varied across years (the mean coefficient of variation=1.02) and was spatially synchronized at large scale (the averaged correlation coefficient=0.67). Berry production represented a two-year cycle in western but a three-year cycle in eastern Norway. The abundance of the moth and the parasitoid also varied across years and were spatially synchronized. The degree of spatial synchrony decreased and cyclicity became obscure with increasing trophic level. We attempted to assess two different components to the predator satiation, functional and numerical satiations, based on a simple population dynamics model. The observed pattern of seed predation testified that both of functional and numerical satiations were at work in this system. In a comparison at different locations, rowan trees with more variable berry production were more effective in reducing losses to the seed predator. The parasitoids also seemed to experience satiation through the fluctuation in their host abundance. These results show that rowan masting has an adaptive foundation, which impacts the dynamics of higher trophic levels.     

The coexistence of acorns with different maturation patterns explains acorn production variability in cork oak

In dry areas such as Mediterranean ecosystems, fluctuations in seed production are typically explained by resource (water) availability. However, acorn production in cork oak (Quercus suber) populations shows a very low relationship to weather. Because cork oak trees produce acorns with different maturation patterns (annual and biennial), we hypothesized that acorn production in coexisting individuals with a different dominant acorn maturation type should respond differently to climatic factors and that disaggregating the trees according to their acorn-maturation pattern should provide a more proximal relation to weather factors. We assessed acorn production variability in fragmented cork oak populations of the eastern Iberian Peninsula by counting the total number of acorns in 155 trees during an 8-year period. An initial assessment of acorn production variability in relation to weather parameters yielded very low explained variance (7%). However, after the trees were grouped according to their dominant acorn maturation pattern, weather parameters were found to account for 44% of the variability in acorn crops, with trees with annual acorns exhibiting mast fruiting in years with reduced spring frost and shorter summer droughts and trees with biennial acorns showing the opposite pattern. Thus, conditions that negatively affect annual production could be beneficial for biennial production (and vice versa). The results highlight the importance of the resource-matching hypothesis for explaining acorn production in Quercus suber and suggest that different seed maturation types within a population may allow the species to deal with highly variable weather conditions. They also emphasize the importance of understanding acorn maturation patterns for interpreting masting cycles.     

Masting in Buxus balearica: assessing fruiting patterns and processes at a large spatial scale

Masting consists of the synchronous highly variable seed production among years by a plant population. We studied spatiotemporal variation in fruit production in ten populations of Buxus balearica (six in the Balearic Islands and four in the Iberian Peninsula) from 2001 to 2004 in the light of masting. In some of them we assessed, by means of both observational and experimental data, the relationship between fruit production and some abiotic variables, the role of previous reproduction, the "pollination efficiency" and the "predator satiation" hypotheses, as well as the consequences for seedling density and survival. Fruit production in B. balearica showed substantial between-year variation, especially in island compared to mainland populations. Correlative evidence indicated that this variation and its geographic pattern were related to differences between regions in rainfall variability, cost of reproduction and the degree of ambophily. We found no indication of predator satiation. However, experimental tests failed to support many of our results, namely a negative effect of previous reproduction on future flowering in island populations and lower pollen limitation with increasing flower production. We therefore warn against exclusive reliance on correlations when testing hypotheses related to masting. In addition, seedling recruitment increased after some episodes of high fruit production but probably additional factors had a role in recruitment, suggesting that mast events not always translate into increased reproductive success. Although a limited time series only allows considering B. balearica as showing 'putative' masting, weather and pollination-related processes are good candidates for further exploration of fruiting patterns and processes at a large spatial scale.     

What makes a good neighborhood? Interaction of spatial scale and fruit density in the predator satiation dynamics of a masting juniper tree

Spatio-temporal variability in fruit production (masting) has been regarded as a key mechanism to increase plant fitness by reducing seed predation. However, considerably more effort has been devoted into understanding the consequences of temporal rather than spatial variations in fruit crop for plant fitness. In order to simultaneously evaluate both components, we quantify fruit production and pre-dispersal damage by three arthropod species (mites, chalcid wasps and moths) in the Spanish juniper (Juniperus thurifera) during 3 years in a spatially explicit context. Our aims were to assess (1) the interaction between fruit production and pre-dispersal fruit damage by arthropods, (2) the potential interference or competition between arthropods, and (3) the form of the phenotypic selection exerted by arthropods on fruit traits considering the spatial context. Arthropods damaged a substantial fraction of fruits produced by Spanish juniper with levels of damage showing sharp inter-annual variations. Fruit damage by mites was negatively related to yearly fruit crop and positively correlated at individual trees fruiting in consecutive years. Increased interspecific interference was an additional consequence of reduced fruit availability during small crop years. During a masting year, fruit damage by less mobile species such as mites was negatively affected by tree crop size, and no spatial structure was observed for mite damage. The incidence of chalcid wasps was low, so the spatial pattern of seed predation was unclear, and no preferences for fruit or seed traits were detected. Conversely, moths selected larger fruits and their incidence on trees was spatially aggregated up to 20 m, with predation levels being negatively affected by fruit abundance at the patch level, suggesting a positive density-dependent effect of neighbors on fruit output. These results highlight the importance of including the spatial component to understand complex species interactions at local scales.     

Patterns and mechanisms of masting in the large‐seeded southern hemisphere conifer Araucaria araucana

Abstract Masting, the intermittent and synchronous production of large seed crops, may result from either of two major processes: resource matching and economy of scale. Components of cone production in Araucaria araucana were partitioned among populations and trees to ascertain the existence of masting and the processes involved. Cone production data from seven populations were obtained during a 9‐year period and seed gathering data were available for an 18‐year time series from six sites in an area of more than 7600 km². Araucaria araucana showed environmentally triggered, intermittent, moderately fluctuating, and highly regionally synchronous reproduction. The mean pairwise correlations of cones production among populations and seed gathering sites were 0.89 and 0.74, respectively, suggesting synchrony in reproduction. Among trees we observed a mean correlation of 0.74 with values ranging from 0.66 to 0.81 for the analysed populations. The existence of negative autocorrelation in seed production between year 0 and year ?2 at the individual tree level suggests the presence of ‘switching’ or internal resource allocation, thus discarding the Resource Matching hypothesis. Mean coefficient of variation (CV_p) among populations was moderate (0.95) and similar to the modal CV_p values reported in the published reports. Mean CV_i among individual trees was 1.16, suggesting a large number of equally and synchronously fluctuating trees, rather than a few largely fluctuating individuals. These results suggest that pollination efficiency and/or predator satiation hypotheses could be responsible for the masting cycles in this conifer. Ancillary data about limitation of airborne pollen dispersion and temporal variation in the amount of seeds per cone and about seed predator satiation, also support both proposed mechanisms.     

Mechanisms driving interspecific variation in regional synchrony of trees reproduction

Seed production in many plants is characterized by large interannual variation, which is synchronized at subcontinental scales in some species but local in others. The reproductive synchrony affects animal migrations, trophic responses to resource pulses and the planning of management and conservation. Spatial synchrony of reproduction is typically attributed to the Moran effect, but this alone is unable to explain interspecific differences in synchrony. We show that interspecific differences in the conservation of seed production-weather relationships combine with the Moran effect to explain variation in reproductive synchrony. Conservative timing of weather cues that trigger masting allows populations to be synchronized at distances >1000 km. Conversely, if populations respond to variable weather signals, synchrony cannot be achieved. Our study shows that species vary in the extent to which their weather cueing is spatiotemporally conserved, with important consequences, including an interspecific variation of masting vulnerability to climate change.     

Climate-driven synchrony in seed production of masting deciduous and conifer tree species

Aims Understanding fluctuations in plant reproductive investment can constitute a key challenge in ecology, conservation and management. Masting events of trees (i.e. the intermittent and synchronous production of abundant seeding material) is an extreme example of such fluctuations. Our objective was to establish the degree of spatial and temporal synchrony in common four masting tree species in boreal Finland and account for potential causal drivers of these patterns.Methods We investigated the spatial intraspecific and temporal interspecific fluctuations in annual seed production of four tree species in Finland, silver birch Betula pendula Roth, downy birch Betula pubescens Ehrh., Norway spruce Picea abies (L.) H.Karst. and rowanberry Sorbus aucuparia L. We also tested to see whether variations in seed production were linked to annual weather conditions. Seeding abundance data were derived from tens of stands per species across large spatial scales within Finland during 1979 to 2014 (for rowanberries only 1986 to 2014).Important findings All species showed spatial synchrony in seed production at scales up to 1000 km. Annual estimates of seed production were strongly correlated between species. Spring and summer temperatures explained most variation in crop sizes of tree species with 0-to 2-year time lags, whereas rainfall had relatively little influence. Warm weather during flowering (May temperature) in the flowering year (Year t) and 2 years before (t ?2) were correlated with seed production. However, high May temperatures during the previous year (t^-1) adversely affected seed production. Summer temperatures in Year t^-1 was positively correlated with seed production, likely because this parameter enhances the development of flower primordials, but the effect was negative with a time lag of 2 years. The negative feedback in temperature coefficients is also likely due to patterns of resource allocation, as abundant flowering and seed production in these species is thought to reduce the subsequent initiation of potential new flower buds. Since the most important weather variables also showed spatial correlation up to 1000 km, weather parameters likely explain much of the spatial and temporal synchrony in seed production of these four studied tree species.     

The North Atlantic Oscillation synchronises fruit production in western European forests

Weather and its lagged effects have been associated with interannual variability and synchrony of fruit production for several tree species. Such relationships are used often in hypotheses relating interannual variability in fruit production with tree resources or favourable pollinating conditions and with synchrony in fruit production among sites through the Moran effect (the synchronisation of biological processes among populations driven by meteorological variability) or the local availability of pollen. Climatic teleconnections, such as the North Atlantic Oscillation (NAO), representing weather packages, however, have rarely been correlated with fruit production, despite often being better predictors of ecological processes than is local weather. The aim of this study was to test the utility of seasonal NAO indices for predicting interannual variability and synchrony in fruit production using data from 76 forests of Abies alba, Fagus sylvatica, Picea abies, Pseudotsuga menziesii, Quercus petraea, and Q. robur distributed across central Europe. Interannual variability in fruit production for all species was significantly correlated with seasonal NAO indices, which were more prominently important predictors than local meteorological variables. The relationships identified by these analyses indicated that proximal causes were mostly responsible for the interannual variability in fruit production, supporting the premise that local tree resources and favourable pollinating conditions are needed to produce large fruit crops. Synchrony in fruit production between forests was mainly associated with weather and geographical distance among sites. Also, fruit production for a given year was less variable among sites during warm and dry springs (negative spring NAO phases). Our results identify the Moran effect as the most likely mechanism for synchronisation of fruit production at large geographical scales and the possibility that pollen availability plays a role in synchronising fruit production at local scales. Our results highlight the influence of the NAO on the patterns of fruit production across western Europe.     

Patterns of Annual Seed Production by Northern Hemisphere Trees: A Global Perspective

We tested whether annual seed production (masting or mast fruiting) in Northern Hemisphere trees is an evolved strategy or a consequence of resource tracking by comparing masting patterns with those of annual rainfall and mean summer temperatures, two environmental variables likely to correlate with available resources. There were generally significant negative autocorrelations between the seed crop in year x and year x+1 (year x+2 in species of Quercus requiring 2 yr to mature acorns), as expected if resources are depleted in mast years in part by switching resources from growth to reproduction. Spatial autocorrelation in annual seed production generally declined with distance but was statistically significant over large geographic areas. Variability in annual seed production was relatively high and inversely correlated with latitude and generally not bimodally distributed. Patterns of spatial autocorrelation in annual rainfall and summer temperatures are generally similar to those exhibited by annual seed production, and relative variability in annual rainfall is also inversely correlated with latitude. However, these environmental variables exhibit distinctly different patterns of temporal autocorrelation, are much less variable, and are more normally distributed than annual seed production. Combined with the inverse relationship between growth and reproduction previously documented, these results support the hypothesis that variability in annual seed production is an evolved strategy and that annual seed production is more or less normally distributed rather than an all-or-none phenomenon.     

Effect of climate change on mast-seeding species: frequency of mass flowering and escape from specialist insect seed predators

Global surface temperatures are expected to increase by several degrees in the next century, with potentially large but poorly understood impacts on ecological interactions. Here we propose potential effects of increased temperatures on ecologically dominant New Zealand grasses (Chionochloa spp.) that mass flower and mast seed. Twenty-two years’ data from five masting Chionochloa species in New Zealand showed that the cue for heavy flowering was unusually high temperature in the summer of the year before flowering. Attack by predispersal insect seed predators was much reduced in mast years, apparently because predator populations were satiated. Increased temperatures would greatly decrease interannual variation in Chionochloa flowering, allowing seed predator populations to increase and potentially to devastate the seed crop annually. Similar responses are likely in masting species worldwide. This previously unrecognized effect of global warming could have widespread impacts on temperate ecosystems.     

Mast seeding in Abies balsamea, Acer saccharum and Betula alleghaniensis in an old growth, cold temperate forest of north-eastern North America

1 Several hypotheses have been put forward to explain the phenomenon of masting or mast seeding, i.e. the supra-annual, periodic production of a large number of seeds in long-lived plants. Some of these hypotheses deal with the proximate causes of masting (e.g. the climate hypothesis) but others are concerned mostly with ultimate, evolutionary explanations (e.g. the pollination efficiency hypothesis).
2 The seed production of three tree species, Abies balsamea , Acer saccharum and Betula alleghaniensis , was followed over a 7-year period in an old-growth, cold temperate forest of north-eastern North America. The main objectives were to determine the extent of interannual variations in seed production, to investigate the relationship between viable and potential seed crop and crop efficiency, and to explore the effects of climate on seed production.
3 Potential and viable seed production varied significantly among years for all three species. However, the timing of dispersal remained the same regardless of the level of seed production.
4 Seed rain was spatially less heterogeneous in years of high seed production, suggesting that most trees were reproducing in such years.
5 Over the 7-year period, there was a significant concordance among species in their viable seed crop and crop efficiency, but not in their potential seed crop. Crop efficiency was positively correlated to potential seed crop for Abies and Betula , but not for Acer .
6 High seed production was related to warm, dry conditions in the spring of the previous year (i.e. at reproductive bud initiation) but to a moist summer in the year of seed maturation.
7 Masting in these three species thus appears to be controlled by several factors, including climate and pollination efficiency.     

The evolutionary ecology of mast seeding

The past seven years have seen a revolution in understanding the causes of mast seeding In perennial plants. Before 1987, the two main theories were resource matching (i.e. plants vary their reproductive output to match variable resources) and predator satiation (i.e. losses to predators are reduced by varying the seed crop). Today, resource matching is restricted to a proximate role, and predator satiation is only one of many theories for the ultimate advantage of masting. Wind pollination, prediction of favourable years for seedling establishment, animal pollination, animal dispersal of fruits, high accessory costs of reproduction and large seed size have all been advanced as possible causes of masting. Of these, wind pollination, predator satiation and environmental prediction are important in a number of species, but the other theories have less support. In future, Important advances seem likely from quantifying synchrony within a population, and examining species with very constant reproduction between years.     

Long-term individual-level variation of reproductive features in Sorbus aucuparia,a fleshy-fruited tree

Key Message

Synchrony and fluctuation in reproductive output was not associated in individual trees.

Abstract

In a study conducted at the central Cantabrian Range, northern Iberia, we analyzed the fruiting pattern of 54 rowans (Sorbus aucuparia), a fleshy-fruited tree, over 16 consecutive years. Our objectives were: (a) to assess the covariation between several variables related to the reproductive performance of individual trees; (b) to measure the degree of synchrony shown by individuals; and (c) to address whether the reproductive behavior of individuals changed over the period of study. The fruiting performance of individuals was assessed in terms of the individual coefficient of variation in fruit output (CV _i ), synchrony (as the correlation between fruiting patterns), and the frequency of heavy crop years. Mean synchrony (0.52 ± 0.18) and CV _i values were large (1.92 ± 0.33) and correlated negatively. The average tree was synchronized with 60 ± 22 % of its conspecifics and about 36 ± 14 % of its fruiting years were heavy crop years. The study population included a distinct and small set of asynchronous trees and the synchrony between individual fruiting patterns was markedly reduced during the second half of the study period.