Spatiotemporal Variations in Seed Set and Pollen Limitation in Populations of the Rare Generalist Species Polemonium caeruleum in Poland

A vast majority of angiosperms are pollinated by animals, and a decline in the number and diversity of insects often affects plant reproduction through pollen limitation. This phenomenon may be particularly severe in rare plant species, whose populations are shrinking. Here, we examined the variability in factors shaping reproductive success and pollen limitation in red-listed Polemonium caeruleum L. During a 5-year study in several populations of P. caeruleum (7–15, depending on year), we assessed the degree of pollen limitation based on differences in seed set between open-pollinated (control) and hand-pollinated flowers. We analysed the effects of flower visitors, population size, and meteorological data on plant reproductive success and pollen limitation. Our study showed that pollen limitation rarely affected P. caeruleum populations, and was present mainly in small populations. Pollen limitation index was negatively affected by the size of population, visitation frequency of all insects, and when considering the visitation frequency of individual groups, also by honeybee visits. Seed production in control treatment was positively influenced by the population size, average monthly precipitation in June and visits of hoverflies, while visits of honeybees, average monthly temperature in September, and average monthly precipitation in August influenced seed production negatively. As generalist plant P. caeruleum can be pollinated by diverse insect groups, however, in small populations their main visitors, the honeybees and bumblebees, may be less attracted, eventually leading to the disappearance of these populations. In pollination of P. caeruleum managed honeybees may play a dual role: while they are the most frequent and efficient flower visitors, their presence decreases seed set in open-pollinated flowers, which is most probably related to efficient pollen collection by these insects.

Bees increase seed set of wild plants while the proportion of arable land has a variable effect on pollination in European agricultural landscapes

Background and aims – Agricultural intensification and loss of farmland heterogeneity have contributed to population declines of wild bees and other pollinators, which may have caused subsequent declines in insect-pollinated wild plants. Material and methods – Using data from 37 studies on 22 pollinator-dependent wild plant species across Europe, we investigated whether flower visitation and seed set of insect-pollinated plants decline with an increasing proportion of arable land within 1 km. Key results – Seed set increased with increasing flower visitation by bees, most of which were wild bees, but not with increasing flower visitation by other insects. Increasing proportion of arable land had a strongly variable effect on seed set and flower visitation by bees across studies. Conclusion – Factors such as landscape configuration, local habitat quality, and temporally changing resource availability (e.g. due to mass-flowering crops or honey bee hives) could have modified the effect of arable land on pollination. While our results highlight that the persistence of wild bees is crucial to maintain plant diversity, we also show that pollen limitation due to declining bee populations in homogenized agricultural landscapes is not a universal driver causing parallel losses of bees and insect-pollinated plants.

By wind or wing: pollination syndromes and alternate bearing in horticultural systems

Cyclical fluctuations in reproductive output are widespread among perennial plants, from multi-year masting cycles in forest trees to alternate bearing in horticultural crops. In natural systems, ecological drivers such as climate and pollen limitation can result in synchrony among plants. Agricultural practices are generally assumed to outweigh ecological drivers that might synchronize alternate-bearing individuals, but this assumption has not been rigorously assessed and little is known about the role of pollen limitation as a driver of synchrony in alternate-bearing crops. We tested whether alternate-bearing perennial crops show signs of alternate bearing at a national scale and whether the magnitude of national-scale alternate bearing differs across pollination syndromes. We analysed the Food and Agriculture Organization of the United Nations time series (1961–2018) of national crop yields across the top-producing countries of 27 alternate-bearing taxa, 6 wind-pollinated and 21 insect-pollinated. Alternate bearing was common in these national data and more pronounced in wind-pollinated taxa, which exhibited a more negative lag-1 autocorrelation and a higher coefficient of variation (CV). We highlight the mutual benefits of integrating ecological theory and agricultural data for (i) advancing our understanding of perennial plant reproduction across time, space and taxa, and (ii) promoting stable farmer livelihoods and global food supply. This article is part of the theme issue ‘The ecology and evolution of synchronized seed production in plants’.

Effects of climate change and pollen supplementation on the reproductive success of two grassland plant species

Climate change has the potential to alter plant reproductive success directly and indirectly through disruptions in animal pollination. Climate models project altered seasonal precipitation patterns and thus the effects of climate change on available resources and pollination services will depend on the season. Plants have evolved reproductive strategies to minimize pollen and resource limitations, and therefore we expect that the disruption of climate change might cause plants to be more pollen limited in seasons that become wetter than they were historically. In this study, we conducted a pollen supplementation experiment within the Global Change Experiment Facility (GCEF) in Central Germany. The GCEF experimentally manipulates future climate based on a realistic scenario of climate change for the region (drier summers and wetter springs and falls) in a native grassland ecosystem. We quantified seed production of two perennial species Dianthus carthusianorum and Scabiosa ochroleuca in response to pollination treatments (control, supplement), climate treatments (ambient and future) and season (summer and fall). Dianthus carthusianorum produced more seeds in future climate conditions independent of the season, but only when given supplemental pollen. Both species showed an increased reproduction in summer compared to the fall. We did not find any evidence for our expectation of higher pollen limitation in the future climate and fall season (i.e. no three-way interaction pollination x season x climate), which might be explained by the high drought tolerance and generalized pollination of our focal plant species. We conclude that plant reproductive success might be limited by the services of animal pollinators in future climates, and have many suggestions for future studies that are necessary to understand the context-dependence and underlying mechanisms of plant reproductive responses to climate.

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.

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 9,200 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 per hectare, which equates currently to higher farm-gate income of approximately US3,720–US7,080 per hectare. 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.

Does pollen limitation limit plant ranges? Evidence and implications

Range limits often involve declines in sexual reproduction, reducing fitness, dispersal, and adaptive potential at range edges. For plants, sexual reproduction is frequently limited by inadequate pollination. While case studies show that pollen limitation can limit plant distributions, the extent to which pollination commonly declines toward plant range edges is unknown. Here, we leverage global databases of pollen-supplementation experiments and plant occurrence data to test whether pollen limitation increases toward plant range edges, using a phylogenetically controlled meta-analysis. While there was significant pollen limitation across studies, we found little evidence that pollen limitation increases toward plant range edges. Pollen limitation was not stronger toward the tropics, nor at species' equatorward vs poleward range limits. Meta-analysis results are consistent with results from targeted experiments, in which pollen limitation increased significantly toward only 14% of 14 plant range edges, suggesting that pollination contributes to range limits less often than do other interactions. Together, these results suggest pollination is one of the rich variety of potential ecological factors that can contribute to range limits, rather than a generally important constraint on plant distributions.

Fruit Set in Avocado: Pollen Limitation, Pollen Load Size, and Selective Fruit Abortion

Avocado is a woody perennial fruit crop originating in Central America and Mexico domesticated and cultivated in the Americas since pre-Columbian times, currently cultivated in subtropical, tropical, and Mediterranean climates worldwide, with increasing importance in international trade. Avocado shows an exuberant flower production that, however, results in a very low fruit set reflected in a massive abscission of flowers and fruitlets. Several factors are involved in this behavior, and, in this work, we have focused on pollination limitation. The results obtained show that pollen deposition takes place at the female and male stages during the avocado flowering season and that the percentage of flowers with pollen on the stigma varies along the flowering season, probably due to changes in temperature that affect not only the floral behavior but also pollinator activity. However, no embryo or endosperm development took place when pollination occurred during the male flowering phase. Thus, the low number of pollen grains landing on the stigmas of female stage flowers observed under natural pollination conditions might not be enough to ensure a good yield. The production of an excess of flowers and subsequent flower drop of most of the flowers provides the opportunity of a selective fruitlet drop depending on the genotype of the embryo since fruits derived from outcrossing showed higher chances of reaching maturity. Moreover, an important competition for resources occurs among developing fruits and new vegetative growth, conferring importance to the time of flower fertilization for effective fruit set.