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 4–31 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

The Tri-Trophic Interactions Hypothesis: Interactive Effects of Host Plant Quality, Diet Breadth and Natural Enemies on Herbivores

Several influential hypotheses in plant-herbivore and herbivore-predator interactions consider the interactive effects of plant quality, herbivore diet breadth, and predation on herbivore performance. Yet individually and collectively, these hypotheses fail to address the simultaneous influence of all three factors. Here we review existing hypotheses, and propose the tri-trophic interactions (TTI) hypothesis to consolidate and integrate their predictions. The TTI hypothesis predicts that dietary specialist herbivores (as compared to generalists) should escape predators and be competitively dominant due to faster growth rates, and that such differences should be greater on low quality (as compared to high quality) host plants. To provide a preliminary test of these predictions, we conducted an empirical study comparing the effects of plant (Baccharis salicifolia) quality and predators between a specialist (Uroleucon macolai) and a generalist (Aphis gossypii) aphid herbivore. Consistent with predictions, these three factors interactively determine herbivore performance in ways not addressed by existing hypotheses. Compared to the specialist, the generalist was less fecund, competitively inferior, and more sensitive to low plant quality. Correspondingly, predator effects were contingent upon plant quality only for the generalist. Contrary to predictions, predator effects were weaker for the generalist and on low-quality plants, likely due to density-dependent benefits provided to the generalist by mutualist ants. Because the TTI hypothesis predicts the superior performance of specialists, mutualist ants may be critical to A. gossypii persistence under competition from U. macolai. In summary, the integrative nature of the TTI hypothesis offers novel insight into the determinants of plant-herbivore and herbivore-predator interactions and the coexistence of specialist and generalist herbivores

Variability in seed cone production and functional response of seed predators to seed cone availability: Support for the predator satiation hypothesis

Mast seeding is a reproductive strategy in some perennial plants defined as synchronous production of large seed crops at irregular intervals. One widely accepted theory to explain this behaviour is the predator satiation hypothesis, which states that the synchronous and variable production of seeds within a population will maximize the probability of seed survival through satiation of seed predators. Although some short-term studies have documented the influence of variable and synchronized production of seeds on herbivore attack rate during one or few mast years, long-term data including multiple mast seeding years and patterns of cone production and herbivore attack on individual trees are needed to assess (i) how cone production, variability and synchrony affect individual plant fitness and (ii) the functional responses of seed predators to mast seeding events. We tested these objectives, collecting long-term (29 years) data on female seed cone production and rates of seed predator attack from 217 individual contiguous trees within a Pinus ponderosa population. Our results support the predator satiation hypothesis. First, we found high interannual synchrony and variability in seed cone production and a type II functional response of seed predators to available cones. Secondly, years with high cone production (mast years) had markedly lower rates of seed predator attack than years of low production (i.e. a population-level satiation effect). Thirdly, within mast years, individuals with high cone production had markedly lower rates of attack than individuals with low cone production (i.e. an individual-level satiation effect). Finally, individual trees with greater synchrony and more variable cone production suffered lower rates of attack. Synthesis: Our long-term data on individual trees lend strong support to the hypothesis that mast seeding in Pinus ponderosa has evolved in response to natural selection from insect seed predators. Pinus ponderosa escapes its seed predators in time by reproducing at irregular intervals (masting). In years when many cones are available, trees suffer markedly lower rates of seed predator attack than years of low production: white dots = non-mast years, grey dots = intermediate years, black dots = mast years. These data provide evidence that mast seeding in this species evolved in response to natural selection from insect seed predators. © 2014 British Ecological Society.National Foundation ScienceMinistry of EducationThis research was supported by National Foundation Science grants BMS 75-14050, DEB78-16798, BSR 8918478, and BSR 912065. XM received financial support from Postdoctoral Fulbright/Ministry of Education grant program.Peer Reviewe

Masting promotes individual- and population-level reproduction by increasing pollination efficiency

Copyright by the Ecological Society of AmericaMasting is a reproductive strategy defined as the intermittent and synchronized production of large seed crops by a plant population. The pollination efficiency hypothesis proposes that masting increases pollination success in plants. Despite its general appeal, no previous studies have used long-term data together with population- and individual-level analyses to assess pollination efficiency between mast and non-mast events. Here we rigorously tested the pollination efficiency hypothesis in ponderosa pine (Pinus ponderosa), a long-lived monoecious, wind-pollinated species, using a data set on 217 trees monitored annually for 20 years. Relative investment in male and female function by individual trees did not vary between mast and non-mast years. At both the population and individual level, the rate of production of mature female cones relative to male strobili production was higher in mast than non-mast years, consistent with the predicted benefit of reproductive synchrony on reproductive success. In addition, at the individual level we found a higher conversion of unfertilized female conelets into mature female cones during a mast year compared to a non-mast year. Collectively, parallel results at the population and individual tree level provide robust evidence for the ecological, and potentially also evolutionary, benefits of masting through increased pollination efficiency.This research was supported by National Foundation Science grants BMS 75-14050, DEB 78-16798, BSR 8918478, and BSR 912065 to Y. B. Linhart and DEB 1120794 to K. A. Mooney. X. Moreira received financial support from Postdoctoral Fulbright/Spanish Ministry of Education grant program. L. Abdala-Roberts was funded by a GAANN fellowship and a UCMEXUS-CONACyT scholar- ship.Peer reviewe

Data from: Effects of climate on reproductive investment in a masting species: assessment of climatic predictors and underlying mechanisms

1. Mechanisms by which climatic factors drive reproductive investment and phenology in masting species are not completely understood. Climatic conditions may act as a proximate cue, stimulating the onset of reproduction and indirectly increasing fitness through benefits associated with synchronous reproduction among individuals. Alternatively, climatic conditions may directly influence individual level allocation to reproduction and reproductive success through effects occurring independently of synchronous reproduction. We previously showed that masting in a ponderosa pine (Pinus ponderosa) population was strongly influenced by spring mean temperature two years before seed cone maturation (Ti-2). However, recent work shows that the difference in temperature between previous growing seasons (ΔT) is more predictive of reproductive investment in long-lived tree species. 2. Here we compared four candidate models that predict seed cone production in P. ponderosa based upon different climatic factors (including Ti-2 and ΔT models). After determining the best climatic predictor, we tested for a potential mechanism by which climate might directly influence seed cone production independent of benefits via synchrony, namely effects of temperature on trade-offs between current and past reproduction (determined by underlying resource availability). 3. We found that Ti-2 (rather than ΔT) was the best predictor of seed cone production. We further show that this same climatic factor exerts a direct fitness benefit to individuals by reducing the strength of trade-offs between current and past reproductive efforts. 4. Synthesis: We demonstrate that a single climatic factor provides fitness benefits to individuals directly, by weakening reproductive trade-offs, and indirectly through the benefits associated with synchrony and masting. This suggests a mechanism for the origin and maintenance of masting: individuals initially respond to climatic cues that directly enhance reproduction (e.g. lower reproductive costs through weakened trade-offs) and this dynamic, expressed across multiple individuals, reinforces these benefits through the economies of scale associated with synchrony and masting

Appendix A. Classification of mast and non-mast years by using the number of standardized deviations of the annual cone production from the long-term mean seed production.

Classification of mast and non-mast years by using the number of standardized deviations of the annual cone production from the long-term mean seed production

Climatic predictors of masting

Climatic predictors of mastin

Weather cues associated with masting behavior dampen the negative autocorrelation between past and current reproduction in oaks

10 páginas.-- 3 figuras.-- 2 tablas.-- 45 referencias.-- Additional Supporting Information may be found online in the Supporting Information section at the end of the articleResearch Article: Free Access in the publisher https://doi.org/10.1002/ajb2.1210Premise of the Study: The influence of weather conditions on masting and the ecological advantages of this reproductive behavior have been the subject of much interest. Weather conditions act as cues influencing reproduction of individual plants, and similar responses expressed across many individuals lead to population-level synchrony in reproductive output. In turn, synchrony leads to benefits from economies of scale such as enhanced pollination success and seed predator satiation. However, there may also be individual-level benefits from reproductive responses to weather cues, which may explain the origin of masting in the absence of economies of scale. In a previous study, we found support for a mechanism whereby individual responses to weather cues attenuate the negative autocorrelation between past and current annual seed production—a pattern typically attributed to resource limitation and reproductive tradeoffs among years. Methods: Here we provide a follow-up and more robust evaluation of this hypothesis in 12 species of oaks (Quercus spp.), testing for a negative autocorrelation (tradeoff) between past and current reproduction and whether responses to weather cues associated with masting reduce the strength of this negative autocorrelation. Key Results: Our results showed a strong negative autocorrelation for 11 of the species, and that species-specific reproductive responses to weather cues dampened this negative autocorrelation in 10 of them. Conclusions: This dampening effect presumably reflects a reduction in resource limitation or increased resource use associated with weather conditions, and suggests that responses to weather cues conferring these advantages should be selected for based on individual benefitsThis study was supported by a National Science Foundation grant DEB‐1256394 to WDK, by the Ramon y Cajal Research Programme (RYC‐2013‐13230) to XM, by a Spanish National Research Grant (AGL2015‐70748‐R) to XM, by the Spanish MEC projects Heteromed (REN2002‐4041‐C02‐02), Dinamed (CGL2005‐5830‐C03‐01) and Interbos (CGL2008‐04503‐C03‐01) to IMPR, and by the Andalusian Anasinque‐PE2010‐RNM‐5782 project to IMPR.Peer reviewe