Effective population size mediates the impact of pollination services on pollen limitation.

Inadequate pollen receipt limits flowering plant reproduction worldwide. Ecological causes of pollen limitation (PL), like pollinator scarcity and low plant abundance, have been a primary research focus. The genetic diversity of plant populations could impact both quantity and quality components of PL in concert with ecological factors, yet empirical examples are lacking. We evaluated joint effects of ecological factors (flower abundance, pollinator visitation) and genetic effective population size (NE) on PL across 13 populations of the common herb Argentina anserina. We used a histological approach with 5504 styles from 1137 flowers to separate quantity and quality components of PL, and link these to reproductive output. NE and pollinator visitation interacted to shape PL, but NE had stronger direct effects. Effectively smaller populations experienced stronger quantity PL, and controlled crosses in a pollinator-free environment revealed that stigmatic pollen quantity was an intrinsic population-level attribute that increased with NE. Pollinator visitation enhanced pollen quality, but only in effectively larger populations. Quantity and quality PL negatively impacted fruit and seed set, respectively. Results highlight that PL is dictated by plant population genetic diversity in addition to commonly evaluated ecological factors. Efforts to support pollinators will more strongly enhance plant reproduction in genetically diverse populations.

Pollination efficiency and the pollen-ovule ratio.

Pollination presents a risky journey for pollen grains. Pollen loss is sometimes thought to favour greater pollen investment to compensate for the inefficiency of transport. Sex allocation theory, to the contrary, has consistently concluded that postdispersal loss should have no selective effect on investment in either sex function. But the intuitively appealing compensation idea continues to be raised despite the lack of theoretical endorsement. We address the theoretical issue with a model that directly represents pollen loss (and ovule loss through floral demise or loss of receptivity) as rate-dependent dynamical processes. These loss rates can be varied to examine the effect of pollination efficiency on optimal sex allocation. Pollen-ovule ratios follow from the sex allocation based on the resource costs of pollen and ovule production. This model confirms conventional findings that pollen loss should have essentially no effect on sexual resource allocation in large, panmictic populations. Pollen limitation of seed set does not alter this conclusion. These results force us to rethink the empirical association of pollination efficiency with low pollen-ovule ratios. This pattern could arise if efficient pollen transport commonly results in stigmatic deposition of cohorts of related pollen. Empirical evidence of correlated paternity supports this explanation.

Does pollination interact with the abiotic environment to affect plant reproduction?

BACKGROUND AND AIMS: Abiotic and biotic components of the environment both limit plant reproduction, but how they interact with one another in combination is less understood. Understanding these interactions is especially relevant because abiotic and biotic environmental components respond differently to various global change drivers. Here we aim to understand whether the effects of pollination (biotic component) on plant reproduction depend on soil moisture (abiotic component), two factors known to affect plant reproduction and that are changing with global change. METHODS: We conducted pollen supplementation experiments for two plant species, Delphinium nuttallianum and Hydrophyllum fendleri, in subalpine meadows in the Western USA across four years that varied in soil moisture. In a separate one-year field experiment, we factorially crossed water addition with pollen supplementation. We measured proportion fruit set, seeds per fruit, and seeds per plant, in addition to stomatal conductance, to determine whether plant physiology responded to watering. KEY RESULTS: In the four-year study, only H. fendleri reproduction was pollen limited, and this occurred independently of soil moisture. Experimental water addition significantly increased soil moisture and stomatal conductance for both species. The effect of pollen addition on reproduction depended on the watering treatment only for H. fendleri fruit production. Reproduction in D. nuttallianum was not significantly affected by pollen addition or water addition, but it did respond to interannual variation in soil moisture. CONCLUSIONS: Although we find some evidence for the effect of a biotic interaction depending on abiotic conditions, it was only for one aspect of reproduction in one species, and it was in an unexpected direction. Our work highlights interactions between the abiotic and biotic components of the environment as an area of further research for improving our understanding of how plant reproduction responds to global change.

Support for Baker's law: Facultative self-fertilization ability decreases pollen limitation in experimental colonization.

PREMISE: The ability to self-fertilize is predicted to provide an advantage in colonization because a single individual can reproduce and establish a next generation in a new location regardless of the density of mates. While there is theoretical and correlative support for this idea, the strength of mate limitation as a selective agent has not yet been delineated from other factors that can also select for self-fertilization in colonization of new habitats. We used known mating-system variation in the American bellflower (Campanula americana) to explore how plants' ability to self-fertilize can mitigate density-dependent reproduction and impact colonization success. METHODS: We created experimental populations of single individuals or a small number of plants to emulate isolated colonization events. These populations were composed of plants that differed in their ability to self-fertilize. We compared pollen limitation of the single individuals to that of small populations. RESULTS: Experimental populations of plants that readily self-fertilize produced consistent seed numbers regardless of population size, whereas plants with lower ability to self-fertilize had density-dependent reproduction with greater seed production in small populations than in populations composed of a single individual. CONCLUSIONS: We experimentally isolated the effect of mate limitation in colonization and found that it can select for increased self-fertilization. We show the benefit of self-fertilization in colonization, which helps to explain geographic patterns of self-fertilization and shows support for Baker's law, a long-held hypothesis in the field of mating-system evolution.

Population Rescue through an Increase in the Selfing Rate under Pollen Limitation: Plasticity versus Evolution.

AbstractIncreased rates of self-fertilization offer reproductive assurance when plant populations experience pollen limitation, but self-fertilization may reduce fitness by exposing deleterious mutations. If an environmental change responsible for pollen limitation also induces plastic mating system shifts toward self-pollination, the reproductive assurance benefit and inbreeding depression cost of increased self-fertilization occur immediately, while the benefit and cost happen more gradually when increased self-fertilization occur through evolution. I built eco-evolutionary models to explore the demographic and genetic conditions in which higher self-fertilization by plasticity and/or evolution rescues populations, following deficits due to a sudden onset of pollen limitation. Rescue is most likely under an intermediate level of selfing rate increase, either through plasticity or evolution, and this critical level of selfing rate increase is higher under stronger pollen limitation. Generally, rescue is more likely through plasticity than through evolution. Under weak pollen limitation, rescue by enhanced self-fertilization may mainly occur through purging of deleterious mutations rather than reproductive assurance. The selfing rate increase conferring the highest rescue probability is lower when the initial population size is smaller. This article shows the importance of plasticity during plant population rescue and offers insights for future studies of the evolution of mating system plasticity.

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.

Sustained mangrove reproduction despite major turnover in pollinator community composition at expanding range edge.

BACKGROUND AND AIMS: How well plants reproduce near their geographic range edge can determine whether distributions will shift in response to changing climate. Reproduction at the range edge can be limiting if pollinator scarcity leads to pollen limitation, or if abiotic stressors affect allocation to reproduction. For many animal-pollinated plants with expanding ranges, the mechanisms by which they have overcome these barriers are poorly understood. METHODS: In this study, we examined plant-pollinator interactions hypothesized to impact reproduction of the black mangrove, Avicennia germinans, which is expanding northward in coastal Florida, USA. We monitored insects visiting A. germinans populations varying in proximity to the geographic range edge, measured the pollen loads of the most common insect taxa and pollen receipt by A. germinans stigmas, and quantified flower and propagule production. KEY RESULTS: We found that despite an 84 % decline in median floral visits by insects at northernmost versus southernmost sites, range-edge pollen receipt remained high. Notably, local floral visitor assemblages exhibited substantial turnover along the study's latitudinal gradient, with large-bodied bees and hover flies increasingly common at northern sites. We also observed elevated flower production in northern populations and higher per capita reproductive output at the range edge. Furthermore, mean propagule mass in northern populations was 18 % larger than that from the southernmost populations. CONCLUSIONS: These findings reveal no erosion of fecundity in A. germinans populations at range limits, allowing rapid expansion of mangrove cover in the region. These results also illustrate that substantial turnover in the assemblage of flower-visiting insects can occur at an expanding range edge without altering pollen receipt.

Disentangling the components of pollen limitation in a widespread herb with gametophytic self-incompatibility.

PREMISE: Seed production is frequently limited by the receipt of insufficient or low-quality pollen, collectively termed "pollen limitation" (PL). In taxa with gametophytic self-incompatibility (GSI), incompatible pollen can germinate on stigmas but pollen tubes are arrested in styles. This allows for estimates of pollen performance before, during, and after self-recognition, as well as insight into the factors underlying pollen quality limitation in GSI taxa. METHODS: We scored pollen performance following self and outcross pollinations in Argentina anserina to identify the location of self-recognition and establish the relationship between pollen tubes and seed production. We then estimated quantity and quality components of PL from >3300 field-collected styles. We combined our results with other studies to test the prediction that low pollen quality, but not quantity, drives higher PL in self-incompatible (SI) taxa than in self-compatible taxa (SC). RESULTS: Self and outcross pollen germinated readily on stigmas, but 96% of germinated self-pollen was arrested during early tube elongation. Reproduction in the field was more limited by pollen quality than by quantity, and pollen failure near the location of self-recognition was a stronger barrier to fertilization than pollen germination. Across 26 taxa, SI species experienced stronger pollen quality, but not quantity, limitation than SC species. CONCLUSIONS: Evaluating pollen performance at multiple points within pistils can elucidate potential causes of pollen quality limitation. The receipt of incompatible pollen inhibits fertilization success more than insufficient pollen receipt or poor pollen germination in A. anserina. Likewise, pollen quality limitation drives high overall PL in other SI taxa.

Differences in individual flowering time change pollen limitation and seed set in three montane wildflowers.

PREMISE: Changes to flowering time caused by climate change could affects plant fecundity, but studies that compare the individual-level responses of phenologically distinct, co-occurring species are lacking. We assessed how variation in floral phenology affects the fecundity of individuals from three montane species with different seasonal flowering times, including in snowmelt acceleration treatments to increase variability in phenology. METHODS: We collected floral phenology and seed set data for individuals of three montane plant species (Mertensia fusiformis, Delphinium nuttallianum, Potentilla pulcherrima). To examine the drivers of seed set, we measured conspecific floral density and conducted pollen limitation experiments to isolate pollination function. We advanced the phenology of plant communities in a controlled large-scale snowmelt acceleration experiment. RESULTS: Differences in individual phenology relative to the rest of the population affected fecundity in our focal species, but effects were species-specific. For our early-season species, individuals that bloomed later than the population peak bloom had increased fecundity, while for our midseason species, simply blooming before or after the population peak increased individual fecundity. For our late-season species, blooming earlier than the population peak increased fecundity. The early and midseason species were pollen-limited, and conspecific density affected seed set only for our early-season species. CONCLUSIONS: Our study shows that variation in individual phenology affects fecundity in three phenologically distinct montane species, and that pollen limitation may be more influential than conspecific density. Our results suggest that individual-level changes in phenology are important to consider for understanding plant reproductive success.

Do Silene species with exposed stigmas tolerate interference by heterospecific pollen?

PREMISE: Co-flowering species that have not evolved an avoidance mechanism may have tolerance to heterospecific pollen (HP) deposition as an adaptive strategy to minimize any deleterious effects of HP transfer, but empirical evidence for the tolerance hypothesis remains scarce. METHODS: To estimate the potential effects of heterospecific pollen deposition (HPD) on female reproductive success, we counted conspecific (CP) and HP pollen grains deposited on stigmas and assessed subsequent seed set of both open- and hand-pollinated flowers in three co-flowering Silene species with exposed stigmas that usually received numerous HP grains on the elongated receptive area. RESULTS: The percentage of HP grains per flower (HP%) varied from 16.6% to 43.0% among three species. Silene chungtienensis had lower HP%, and the CP-HP relationship was neutral; S. gracilicaulis and S. yunnanensis had a relatively higher HP% with a positive CP-HP relationship. The effects of CP and HP number on natural seed set were positive for all three species, but HP% had stronger negative effects in S. chungtienensis and S. gracilicaulis. In hand-pollinated flowers of the three Silene species, seed set did not decrease with HP whether CP was in excess or insufficient, indicating no negative effects of HPD on seed production. CONCLUSIONS: Consistent with the tolerance hypothesis, our results indicated that species with higher HP interference are likely to be tolerant to an increase in HP%. These species with generalist-pollinated flowers and exposed large stigmas may benefit from an increase of conspecific pollen deposition, despite the associated increase in heterospecific pollen deposition.

Reproductive biology of an endangered lithophytic shrub and implications for its conservation.

BACKGROUND: Plants in cliff habitats may evolve specific reproductive strategies to cope with harsh environments, and unraveling these reproductive characteristics can improve our understanding of survival strategies and lithophyte evolution. This understanding is especially important for efforts to protect rare and endemic plants. Here, we investigated the reproductive biology of Lonicera oblata, an endangered lithophytic shrub that is scattered in highly fragmented and isolated cliff habitats of the Taihang and Yan mountains in North China. RESULTS: Flowers of L. oblata are herkogamous and protandrous, characteristics that can prevent autogamy at the single-flower level, and insects are necessary for pollination. The outcrossing index, pollen/ovule ratio, and the results of hand pollination were measured and all revealed a mixed mating system for L. oblata, that combines cross-fertilization and partial self-fertilization. The floral traits of L. oblata of zygomorphic and brightly yellowish corolla, heavy fragrance, and rich nectar, suggest an entomophilous pollination system. Sweat bees were observed as the most effective pollinators but their visiting frequencies were not high. Pollen limitation may limit the reproductive success of L. oblata. CONCLUSIONS: We determined the reproductive characteristics of L. oblata, a critically endangered species endemic to cliffs in North China, providing insight into its endangerment and suggesting conservation strategies. L. oblata has highly pollinator-dependent self-fertilization as part of a mixed mating system. Floral features such as low-flowering synchrony, asynchronous anthers dehiscence, and high duration of stigma receptivity, improve pollination efficiency in the case of low pollinator service. Our work provides reference information to understand the survival strategies and conservation of L. oblata and other lithophytes.

Effect of grazing disturbance on floral display, pollen limitation and plant pollination efficiency in the desert steppe.

BACKGROUND: Grazing disturbance usually affects floral display and pollination efficiency in the desert steppe, which may cause pollen limitation in insect-pollinated plants. Effective pollination is essential for the reproductive success of insect-pollinated plants and insufficient pollen transfer may result in pollen limitation. Caragana microphylla Lam is an arid region shrub with ecological importance. Few studies have been conducted on how grazing disturbance influences pollen limitation and pollination efficiency of C. microphylla. Here, we quantify the effect of different grazing intensities on floral display, pollinator visitation frequency and seed production in the Urat desert steppe. RESULTS: In C. microphylla, supplemental hand pollination increased the seed set, and pollen limitation was the predominant limiting factor. As the heavy grazing significantly reduced the seed set in plants that underwent open-pollination, but there was no significant difference in the seed set between plants in the control plots and plants in the moderate grazing plots. Furthermore, there was a higher pollinator visitation frequency in plants in the control plots than in plants in the heavy grazing plots. CONCLUSIONS: We found that pollinator visitation frequency was significantly associated with the number of open flowers. Our findings also demonstrated that seed production is associated with pollinator visitation frequency, as indicated by increased seed production in flowers with higher pollinator visitation frequency. Therefore, this study provides insight into the effect of different grazing intensities on floral display that are important for influencing pollinator visitation frequency and pollination efficiency in desert steppes.

Global analysis of floral longevity reveals latitudinal gradients and biotic and abiotic correlates.

The length of time a flower remains open and functional - floral longevity - governs important reproductive processes influencing pollination and mating and varies considerably among angiosperm species. However, little is known about large-scale biogeographic patterns and the correlates of floral longevity. Using published data on floral longevity from 818 angiosperm species in 134 families and 472 locations world-wide, we present the first global quantification of the latitudinal pattern of floral longevity and the relationships between floral longevity and a range of biotic and abiotic factors. Floral longevity exhibited a significant phylogenetic signal and was longer at higher latitudes in both northern and southern hemispheres, even after accounting for elevation. This latitudinal variation was associated with several biotic and abiotic variables. The mean temperature of the flowering season had the highest predictive power for floral longevity, followed by pollen number per flower. Surprisingly, compatibility status, flower size, pollination mode, and growth form had no significant effects on flower longevity. Our results suggest that physiological processes associated with floral maintenance play a key role in explaining latitudinal variation in floral longevity across global ecosystems, with potential implications for floral longevity under global climate change and species distributions.

Pollen limitation and xenia effects in a cultivated mass-flowering tree, Macadamia integrifolia (Proteaceae).

BACKGROUND AND AIMS: Pollen limitation is most prevalent among bee-pollinated plants, self-incompatible plants and tropical plants. However, we have very little understanding of the extent to which pollen limitation affects fruit set in mass-flowering trees despite tree crops accounting for at least 600 million tons of the 9200 million tons of annual global food production. METHODS: We determined the extent of pollen limitation in a bee-pollinated, partially self-incompatible, subtropical tree by hand cross-pollinating the majority of flowers on mass-flowering macadamia (Macadamia integrifolia) trees that produce about 200 000-400 000 flowers. We measured tree yield and kernel quality and estimated final fruit set. We genotyped individual kernels by MassARRAY to determine levels of outcrossing in orchards and assess paternity effects on nut quality. KEY RESULTS: Macadamia trees were pollen-limited. Supplementary cross-pollination increased nut-in-shell yield, kernel yield and fruit set by as much as 97, 109 and 92 %, respectively. The extent of pollen limitation depended upon the proximity of experimental trees to trees of another cultivar because macadamia trees were highly outcrossing. Between 84 and 100 % of fruit arose from cross-pollination, even at 200 m (25 rows) from orchard blocks of another cultivar. Large variations in nut-in-shell mass, kernel mass, kernel recovery and kernel oil concentration were related to differences in fruit paternity, including between self-pollinated and cross-pollinated fruit, thus demonstrating pollen-parent effects on fruit quality (i.e. xenia). CONCLUSIONS: This study is the first to demonstrate pollen limitation in a mass-flowering tree. Improved pollination led to increased kernel yield of 0.31-0.59 tons ha-1, which equates currently to higher farm-gate income of approximately $US3720-$US7080 ha-1. The heavy reliance of macadamia flowers on cross-pollination and the strong xenia effects on kernel mass demonstrate the high value that pollination services can provide to food production.

Pollen limitation of native plant reproduction in an urban landscape.

PREMISE: Evidence suggests that bees may benefit from moderate levels of human development. However, the effects of human development on pollination and reproduction of bee-pollinated plants are less-well understood. Studies have measured natural variation in pollination and plant reproduction as a function of urbanization, but few have experimentally measured the magnitude of pollen limitation in urban vs. non-urban sites. Doing so is important to unambiguously link changes in pollination to plant reproduction. Previous work in the Southeastern United States found that urban sites supported twice the abundance of bees compared to non-urban sites. We tested the hypothesis that greater bee abundance in some of the same urban sites translates into reduced pollen limitation compared to non-urban sites. METHODS: We manipulated pollination to three native, wild-growing, bee-pollinated plants: Gelsemium sempervirens, Oenothera fruticosa, and Campsis radicans. Using supplemental pollinations, we tested for pollen limitation of three components of female reproduction in paired urban and non-urban sites. We also measured pollen receipt as a proxy for pollinator visitation. RESULTS: We found that all three plant species were pollen-limited for some measures of female reproduction. However, opposite to our original hypothesis, two of the three species were more pollen-limited in urban relative to non-urban sites. We found that open-pollinated flowers in urban sites received less conspecific and more heterospecific pollen on average than those in non-urban sites. CONCLUSIONS: These results suggest that even when urban sites have more abundant pollinators, this may not alleviate pollen limitation of native plant reproduction in urban landscapes.

The impact of habitat loss on pollination services for a threatened dune endemic plant.

Habitat loss is currently a major threat to biodiversity, affecting species interactions, such as plant-pollinator interactions. This is particularly important in self-incompatible plants relying on pollinators to reproduce and sustain their populations. Here, we evaluated how habitat loss affects the pollination system, plant individual-pollinator species interaction network, and plant reproductive fitness of the self-incompatible Jasione maritima var. sabularia, a threatened taxon from dune systems. This plant is a pollinator generalist, visited by 108 species from distinct taxonomic groups. Results suggest that increasing habitat loss led to a significant decline in pollinator richness, increased pollen limitation, and a decrease in reproductive fitness of J. maritima var. sabularia. Visitation rate per individual did not significantly change with available area, indicating that the quality of pollen differed across populations. The topology of the network between J. maritima var. sabularia individuals and its pollinator species did not change, which may be attributed to the stability in the core of pollinator species. This suggests that the lower fitness of plants with increasing habitat degradation may be explained not only by the lower richness of peripheral pollinators but also by the genetic structure of the plant populations, as there is a possible higher transference of less quality pollen by pollinators, ultimately compromising the persistence of plant populations. Our study highlights the need of future studies to integrate the fine details provided by individual-level networks, which will increase our understanding of the pattern of species interactions and its consequences for the fitness of threatened plant populations.

Plants and pollinators: Will natural selection cause an imbalance between nectar supply and demand?

Pollination is an important ecological process. However, plant and pollinator needs are not always met. Commonly, pollen limitation reduces seed set or bees experience nectar dearth. Using a cost-benefit approach, we show that natural selection will lead to lower nectar production when pollinators are abundant, and vice-versa. At the community level, competition among plants for pollinators causes positive feedback that exacerbates pre-existing seasonal imbalances between nectar supply and demand. When pollinators are scarce, plants will be selected to produce more nectar to outcompete other plants in attracting pollinators, and when pollinators are abundant, plants will be selected to produce less nectar. We suggest ways to test this positive feedback hypothesis and note that evidence for seasonal variation in nectar availability provides preliminary empirical support. If correct, our hypothesis indicates that pollination faces a particular challenge in balancing nectar supply with pollinator demand and is a further example of the underappreciated role of positive feedback in ecology and evolution.

Can Conflicting Selection from Pollinators and Nectar-Robbing Antagonists Drive Adaptive Pollen Limitation? A Conceptual Model and Empirical Test.

AbstractPollen limitation is widespread, despite predictions that it should not be. We propose a novel mechanism generating pollen limitation: conflicting selection by pollinators and antagonists on pollinator attraction traits. We introduce a heuristic model demonstrating antagonist-induced adaptive pollen limitation and present a field study illustrating its occurrence in a wild population. For antagonist-induced adaptive pollen limitation to occur, four criteria must be met: (1) correlated attraction of pollinators and antagonists; (2) greater response by antagonists than pollinators to altered investment in attraction traits; (3) reduced investment in pollinator attraction, leading to pollen limitation; and (4) higher fitness for plants with reduced investment in pollinator attraction. We surveyed nectar robbery and reproductive output for 109 Odontonema cuspidatum (Acanthaceae) plants in a pollen-limited population over 2 years and used experimental floral arrays to evaluate how flower number affects pollination and nectar robbery. Both pollinators and nectar robbers preferred larger floral displays and nectar robbery reduced reproductive output, suggesting conflicting selection. Survey and experimental data agreed closely on the optimum flower number under antagonist-induced pollen limitation; this number was substantially overrepresented in the population. While criteria for antagonist-induced adaptive pollen limitation are restrictive, the necessary conditions may often be realized. Considering interactions beyond the plant-pollinator dyad illuminates previously overlooked mechanisms generating pollen limitation.

Comparative effects of pollen limitation, floral traits and pollinators on reproductive success of Hedysarum scoparium Fisch. et Mey. in different habitats.

BACKGROUND: Reproduction in most flowering plants may be limited because of the decreased visitation or activity of pollinators in fragmented habitats. Hedysarum scoparium Fisch. et Mey. is an arid region shrub with ecological importance. We explored the pollen limitation and seed set of Hedysarum scoparium in fragmented and restored environments, and examined whether pollen limitation is a significant limiting factor for seed set. We also compared floral traits and pollinator visitation between both habitats, and we determined the difference of floral traits and pollinators influenced reproductive success in Hedysarum scoparium. RESULTS: Our results indicated that supplementation with pollen significantly increased seed set per flower, which is pollen-limited in this species. Furthermore, there was greater seed set of the hand cross-pollination group in the restored habitat compared to the fragmented environment. More visits by Apis mellifera were recorded in the restored habitats, which may explain the difference in seed production between the fragmented and restored habitats. CONCLUSIONS: In this study, a positive association between pollinator visitation frequency and open flower number was observed. The findings of this study are important for experimentally quantifying the effects of floral traits and pollinators on plant reproductive success in different habitats.

Climate warming causes mast seeding to break down by reducing sensitivity to weather cues.

Climate change is altering patterns of seed production worldwide with consequences for population recruitment and migration potential. For the many species that regenerate through synchronized, quasiperiodic reproductive events termed masting, these changes include decreases in the synchrony and interannual variation in seed production. This breakdown in the occurrence of masting features harms reproduction by decreasing the efficiency of pollination and increasing seed predation. Changes in masting are often paralleled by warming temperatures, but the underlying proximate mechanisms are unknown. We used a unique 39-year study of 139 European beech (Fagus sylvatica) trees that experienced masting breakdown to track the seed developmental cycle and pinpoint phases where weather effects on seed production have changed over time. A cold followed by warm summer led to large coordinated flowering efforts among plants. However, trees failed to respond to the weather signal as summers warmed and the frequency of reproductive cues changed fivefold. Less synchronous flowering resulted in less efficient pollination that further decreased the synchrony of seed maturation. As global temperatures are expected to increase this century, perennial plants that fine-tune their reproductive schedules based on temperature cues may suffer regeneration failures.