Pollinator-mediated facilitation alleviates pollen limitation in a plant-hummingbird network.

Facilitation and competition among plants sharing pollinators have contrasting consequences for plant fitness. However, it is unclear whether pollinator-mediated facilitation and competition may affect pollen limitation (potential contribution of pollination to fitness) in pollination networks. Here, we investigated how pollinator sharing affects pollen limitation in a tropical hummingbird-pollinated community marked by facilitation. We employed indices describing how much a plant species potentially affects the pollination of other co-flowering species through shared pollinators (acting degree) and is affected by other co-flowering species (target degree) within the plant-hummingbird network. Since facilitation often increases pollination quantity but not necessarily quality, we expected both indices to be associated with reductions in pollen limitation estimates that depend on pollination quantity (fruit set and seed number) rather than estimates more strictly related to quality (seed weight and germination). We found that both indices were associated with reductions in pollen limitation only for seed weight and germination. Thus, facilitation occurred via qualitative estimates of pollen limitation. Our results suggest that facilitation may enhance plant fitness estimates even if quantitative components of plant fecundity are already saturated. Overall, we showed that pollinator-mediated indirect effects in a multispecies context are important drivers of plant fitness estimates with consequences for coexistence in diverse communities.

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.

Pollination outcomes reveal negative density-dependence coupled with interspecific facilitation among plants.

Pollination is thought to be under positive density-dependence, destabilising plant coexistence by conferring fitness disadvantages to rare species. Such disadvantage is exacerbated by interspecific competition but can be mitigated by facilitation and intraspecific competition. However, pollinator scarcity should enhance intraspecific plant competition and impose disadvantage on common over rare species (negative density-dependence, NDD). We assessed pollination proxies (visitation rate, pollen receipt, pollen tubes) in a generalised plant community and related them to conspecific and heterospecific density, expecting NDD and interspecific facilitation due to the natural pollinator scarcity. Contrary to usual expectations, all proxies indicated strong intraspecific competition for common plants. Moreover interspecific facilitation prevailed and was stronger for rare than for common plants. Both NDD and interspecific facilitation were modulated by specialisation, floral display and pollinator group. The combination of intraspecific competition and interspecific facilitation fosters plant coexistence, suggesting that pollination can be a niche axis maintaining plant diversity.

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.

Meta-analysis of pollen limitation reveals the relevance of pollination generalization in the Atlantic forest of Brazil.

Despite the extensive knowledge of pollen limitation in angiosperms, its assessment within tropical forests is still limited. Especially lacking are large scale comparisons of species within this biome - one that is highly diverse but also becoming increasingly threatened. In fact, many tropical plant species depend upon pollinators for reproduction but evaluation of the impact of this dependence via different levels of pollination specialization has yet to be made at the biome scale. We assessed the occurrence and magnitude of pollen limitation for species in the Brazilian Atlantic forest and tested the association of pollination specialization, breeding system, and life habit with pollination efficiency. We compiled data from studies published between 1985 and 2012. We calculated species' effect size (d) from data on fruit set after hand cross-pollination and natural pollination and conducted standard and phylogenetically independent meta-analysis. Overall pollen limitation was moderate, with magnitude of 0.50, and 95% confidence interval [0.37, 0.62] for 126 species. Pollen limitation was observed in 39% of species. Pollination specialization was the factor that best explained the occurrence of pollen limitation. Specifically, phenotypic and ecological specialists (plants with zygomorphic flowers and pollinated by one species of pollinator, respectively) had higher pollen limitation than generalist plants (actinomorphic flowers and pollination by two or more species). Functional generalists (plants pollinated by three or more functional groups) were not pollen limited. On the other hand, breeding system and life habit were not associated to pollen limitation. Pollen limitation was observed in the Atlantic forest and its magnitude was comparable to that for angiosperms as a whole. The finding that pollination specialization was the strongest predictor of pollen limitation suggests that specialist plants in this biome may be most prone to the reproductive failure as a result of pollinator loss.

Community-wide assessment of pollen limitation in hummingbird-pollinated plants of a tropical montane rain forest.

BACKGROUND AND AIMS: Although pollen limitation of reproduction (PL) has been widely studied, our understanding of its occurrence in tropical communities, especially for bird-pollinated plants, is underdeveloped. In addition, inclusion of both quantity and quality aspects in studies of PL are generally lacking. Within hummingbird-pollinated plants, a prediction was made for higher PL for the quality than quantity aspects and a minor effect of temporal variation because hummingbirds are constant and efficient pollen vectors but they may transfer low quality pollen. METHODS: Field hand and open pollination experiments were conducted on 21 species in a tropical montane rain forest over 2 years. The quantity (fruit set and seeds per fruit) and quality (seed weight and germination) aspects of reproduction were assessed as the response to open pollination relative to outcross hand pollination. The relationships between the effect size of quantity and quality aspects of reproduction and predictive plant features (self-incompatibility, autogamy, density and pollinator specialization level) were assessed with phylogenetic generalized linear models. KEY RESULTS: Just over half of all the species expressed PL for one or more response variables. On average, the severity of PL was strong for one quality variable (seed germination; 0·83), but insignificant for another (seed weight; -0·03), and low to moderate for quantity variables (0·31 for seeds per fruit and 0·39 for fruit set). There was only a minor contribution of temporal variation to PL within the studied species. Common predictors of PL, i.e. phylogenetic relatedness, self-incompatibility, autogamy, plant density and pollinator specialization level, did not adequately explain variation in PL within this community. CONCLUSIONS: Despite the measurable degree of PL within these hummingbird-pollinated plants, the causes of pollen quality and quantity insufficiency are not clear. Variables other than those tested may contribute to PL or causes of PL may vary among species and cannot adequately be accounted for when assessed from the within-community perspective.