Land use and pollinator dependency drives global patterns of pollen limitation in the Anthropocene.

Land use change, by disrupting the co-evolved interactions between plants and their pollinators, could be causing plant reproduction to be limited by pollen supply. Using a phylogenetically controlled meta-analysis on over 2200 experimental studies and more than 1200 wild plants, we ask if land use intensification is causing plant reproduction to be pollen limited at global scales. Here we report that plants reliant on pollinators in urban settings are more pollen limited than similarly pollinator-reliant plants in other landscapes. Plants functionally specialized on bee pollinators are more pollen limited in natural than managed vegetation, but the reverse is true for plants pollinated exclusively by a non-bee functional group or those pollinated by multiple functional groups. Plants ecologically specialized on a single pollinator taxon were extremely pollen limited across land use types. These results suggest that while urbanization intensifies pollen limitation, ecologically and functionally specialized plants are at risk of pollen limitation across land use categories.

Plant traits moderate pollen limitation of introduced and native plants: a phylogenetic meta-analysis of global scale.

The role of pollination in the success of invasive plants needs to be understood because invasives have substantial effects on species interactions and ecosystem functions. Previous research has shown both that reproduction of invasive plants is often pollen limited and that invasive plants can have high seed production, motivating the questions: How do invasive populations maintain reproductive success in spite of pollen limitation? What species traits moderate pollen limitation for invaders? We conducted a phylogenetic meta-analysis with 68 invasive, 50 introduced noninvasive and 1931 native plant populations, across 1249 species. We found that invasive populations with generalist pollination or pollinator dependence were less pollen limited than natives, but invasives and introduced noninvasives did not differ. Invasive species produced 3× fewer ovules/flower and >250× more flowers per plant, compared with their native relatives. While these traits were negatively correlated, consistent with a tradeoff, this did not differ with invasion status. Invasive plants that produce many flowers and have floral generalisation are able to compensate for or avoid pollen limitation, potentially helping to explain the invaders' reproductive successes.

Resource Allocation and Seed Size Selection in Perennial Plants under Pollen Limitation.

Pollen limitation may affect resource allocation patterns in plants, but its role in the selection of seed size is not known. Using an evolutionarily stable strategy model of resource allocation in perennial iteroparous plants, we show that under density-independent population growth, pollen limitation (i.e., a reduction in ovule fertilization rate) should increase the optimal seed size. At any level of pollen limitation (including none), the optimal seed size maximizes the ratio of juvenile survival rate to the resource investment needed to produce one seed (including both ovule production and seed provisioning); that is, the optimum maximizes the fitness effect per unit cost. Seed investment may affect allocation to postbreeding adult survival. In our model, pollen limitation increases individual seed size but decreases overall reproductive allocation, so that pollen limitation should also increase the optimal allocation to postbreeding adult survival. Under density-dependent population growth, the optimal seed size is inversely proportional to ovule fertilization rate. However, pollen limitation does not affect the optimal allocation to postbreeding adult survival and ovule production. These results highlight the importance of allocation trade-offs in the effect pollen limitation has on the ecology and evolution of seed size and postbreeding adult survival in perennial plants.

Pollen Limitation Is Common--Should It Be?

Although several meta-analyses have indicated that pollen limitation of seed output is widespread and often severe in flowering plants, a theoretical model of Rosenheim et al. published in 2014 predicts otherwise. Their predictions of infrequent pollen limitation were based on estimated ratios between prefertilization and postfertilization costs that are likely to be unrealistically low and on an assumption about variance in ovule fertilization among plants that is likely to be unrealistically narrow. I show that the predictions of the model of Rosenheim et al. are sensitive to these assumptions. In particular, more realistic distributions of pollination variation yield predictions that are in better accord with empirical data. Pervasive pollen limitation therefore remains unsurprising, although the extent of lifetime pollen limitation remains an important frontier for research.

Are relationships between pollen-ovule ratio and pollen and seed size explained by sex allocation?

Positive correlations between pollen-ovule ratio and seed size, and negative correlations between pollen-ovule ratio and pollen grain size have been noted frequently in a wide variety of angiosperm taxa. These relationships are commonly explained as a consequence of sex allocation on the basis of a simple model proposed by Charnov. Indeed, the theoretical expectation from the model has been the basis for interest in the empirical pattern. However, the predicted relationship is a necessary consequence of the mathematics of the model, which therefore has little explanatory power, even though its predictions are consistent with empirical results. The evolution of pollen-ovule ratios is likely to depend on selective factors affecting mating system, pollen presentation and dispensing, patterns of pollen receipt, pollen tube competition, female mate choice through embryo abortion, as well as genetic covariances among pollen, ovule, and seed size and other reproductive traits. To the extent the empirical correlations involving pollen-ovule ratios are interesting, they will need explanation in terms of a suite of selective factors. They are not explained simply by sex allocation trade-offs.

A test of simultaneous resource and pollen limitation in Stylidium armeria.

This study tests the Haig-Westoby model, which predicts that seed output will be limited simultaneously by pollen and resources when plants optimally distribute their reproductive investment. The test was conducted over 2 yr using Stylidium armeria in a factorial design that fully crossed three pollination levels (small stigmatic loads, open pollination, and supplementation of natural loads) with three levels of resource availability (reduction through partial defoliation, unmanipulated resource conditions, and supplementation through nitrogen, phosphorus and potassium (NPK) addition). There was no evidence of pollen limitation from supplemental pollination; however, pollen reductions (to about half the normal mean stigmatic loads) sharply reduced seed output. There was no evidence of resource limitation, in that NPK addition did not, by itself, significantly elevate seed output in either year of the study, while resource reduction by defoliation lowered seed output in the second year. Simultaneous addition of both pollen and resources strongly and significantly increased seed production. These results match the direction of effects predicted by the Haig-Westoby model, and suggest that S. armeria plants at our site are at or near an equilibrium of joint limitation of seed production by pollen capture and resource availability.

Pollination decays in biodiversity hotspots.

As pollinators decline globally, competition for their services is expected to intensify, and this antagonism may be most severe where the number of plant species is the greatest. Using meta-analysis and comparative phylogenetic analysis, we provide a global-scale test of whether reproduction becomes more limited by pollen receipt (pollen limitation) as the number of coexisting plant species increases. As predicted, we find a significant positive relationship between pollen limitation and species richness. In addition, this pattern is particularly strong for species that are obligately outcrossing and for trees relative to herbs or shrubs. We suggest that plants occurring in species-rich communities may be more prone to pollen limitation because of interspecific competition for pollinators. As a consequence, plants in biodiversity hotspots may have a higher risk of extinction and/or experience increased selection pressure to specialize on certain pollinators or diversify into different phenological niches. The combination of higher pollen limitation and habitat destruction represents a dual risk to tropical plant species that has not been previously identified.