Reduced visitation to buzz-pollinated Cyanella hyacinthoides in the presence of other pollen sources in the hyperdiverse Cape Floristic Region.

Many plant species have floral morphologies that restrict access to floral resources, such as pollen or nectar, and only a subset of floral visitors can perform the handling behaviors required to extract restricted resources. Due to the time and energy required to extract resources from morphologically complex flowers, these plant species potentially compete for pollinators with co-flowering plants that have more easily accessible resources. A widespread floral mechanism restricting access to pollen is the presence of tubular anthers that open through small pores or slits (poricidal anthers). Some bees have evolved the capacity to remove pollen from poricidal anthers using vibrations, giving rise to the phenomenon of buzz-pollination. These bee vibrations that are produced for pollen extraction are presumably energetically costly, and to date, few studies have investigated whether buzz-pollinated flowers may be at a disadvantage when competing for pollinators' attention with plant species that present unrestricted pollen resources. Here, we studied Cyanella hyacinthoides (Tecophilaeaceae), a geophyte with poricidal anthers in the hyperdiverse Cape Floristic Region of South Africa, to assess how the composition and relative abundance of flowers with easily accessible pollen affect bee visitation to a buzz-pollinated plant. We found that the number of pollinator species of C. hyacinthoides was not influenced by community composition. However, visitation rates to C. hyacinthoides were reduced when the relative abundances of flowers with more accessible resources were high. Visitation rates were strongly associated with petal color, showing that flower color is important in mediating these interactions. We conclude that buzz-pollinated plants might be at a competitive disadvantage when many easily accessible pollen sources are available, particularly when competitor species share its floral signals.

Widespread vulnerability of flowering plant seed production to pollinator declines.

Despite evidence of pollinator declines from many regions across the globe, the threat this poses to plant populations is not clear because plants can often produce seeds without animal pollinators. Here, we quantify pollinator contribution to seed production by comparing fertility in the presence versus the absence of pollinators for a global dataset of 1174 plant species. We estimate that, without pollinators, a third of flowering plant species would produce no seeds and half would suffer an 80% or more reduction in fertility. Pollinator contribution to plant reproduction is higher in plants with tree growth form, multiple reproductive episodes, more specialized pollination systems, and tropical distributions, making these groups especially vulnerable to reduced service from pollinators. These results suggest that, without mitigating efforts, pollinator declines have the potential to reduce reproduction for most plant species, increasing the risk of population declines.

Pollen dispensing schedules in buzz-pollinated plants: experimental comparison of species with contrasting floral morphologies.

PREMISE: Plants can mitigate the fitness costs associated with pollen consumption by floral visitors by optimizing pollen release rates. In buzz-pollinated plants, bees apply vibrations to remove pollen from anthers with small pores. These poricidal anthers potentially function as mechanism staggering pollen release, but this has rarely been tested across plant species differing in anther morphology. METHODS: In Solanum Section Androceras, three pairs of buzz-pollinated species have undergone independent evolutionary shifts between large- and small-flowers, which are accompanied by replicate changes in anther morphology. We used these shifts in anther morphology to characterize the association between anther morphology and pollen dispensing schedules. We applied simulated bee-like vibrations to anthers to elicit pollen release, and compared pollen dispensing schedules across anther morphologies. We also investigated how vibration velocity affects pollen release. RESULTS: Replicate transitions in Solanum anther morphology are associated with consistent changes in pollen dispensing schedules. We found that small-flowered taxa release their pollen at higher rates than their large-flowered counterparts. Higher vibration velocities resulted in quicker pollen dispensing and more total pollen released. Finally, both the pollen dispensing rate and the amount of pollen released in the first vibration were negatively related to anther wall area, but we did not observe any association between pore size and pollen dispensing. CONCLUSIONS: Our results provide the first empirical demonstration that the pollen dispensing properties of poricidal anthers depend on both floral characteristics and bee vibration properties. Morphological modification of anthers could thus provide a mechanism to exploit different pollination environments.

Geographic Mosaics of Fly Pollinators With Divergent Color Preferences Drive Landscape-Scale Structuring of Flower Color in Daisy Communities.

The striking variation in flower color across and within Angiosperm species is often attributed to divergent selection resulting from geographic mosaics of pollinators with different color preferences. Despite the importance of pollinator mosaics in driving floral divergence, the distributions of pollinators and their color preferences are seldom quantified. The extensive mass-flowering displays of annual daisy species in Namaqualand, South Africa, are characterized by striking color convergence within communities, but also color turnover within species and genera across large geographic scales. We aimed to determine whether shifts between orange and white-flowered daisy communities are driven by the innate color preferences of different pollinators or by soil color, which can potentially affect the detectability of different colored flowers. Different bee-fly pollinators dominated in both community types so that largely non-overlapping pollinator distributions were strongly associated with different flower colors. Visual modeling demonstrated that orange and white-flowered species are distinguishable in fly vision, and choice experiments demonstrated strongly divergent color preferences. We found that the dominant pollinator in orange communities has a strong spontaneous preference for orange flowers, which was not altered by conditioning. Similarly, the dominant pollinator in white communities exhibited an innate preference for white flowers. Although detectability of white flowers varied across soil types, background contrast did not alter color preferences. These findings demonstrate that landscape-level flower color turnover across Namaqua daisy communities is likely shaped by a strong qualitative geographic mosaic of bee-fly pollinators with divergent color preferences. This is an unexpected result given the classically generalist pollination phenotype of daisies. However, because of the dominance of single fly pollinator species within communities, and the virtual absence of bees as pollinators, we suggest that Namaqua daisies function as pollination specialists despite their generalist phenotypes, thus facilitating differentiation of flower color by pollinator shifts across the fly pollinator mosaic.

Dominant pollinators drive non-random community assembly and shared flower colour patterns in daisy communities.

Background and Aims: As most plants rely on pollination for persistence in communities, pollination interactions should be important determinants of plant community assembly. Here, trait and phylogenetic null modelling approaches were combined with pollinator interaction networks to elucidate the processes structuring flower colour assembly patterns in Asteraceae communities in Namaqualand, South Africa. Methods: Plant species were assigned to flower colour pattern categories (CPCs) that incorporate the complexity of the bulls-eye colour pattern, using pollinator vision models. Null models were used to assess whether daisy communities exhibit clustering (driven by filtering, facilitation or convergence) or overdispersion (driven by competitive exclusion or character displacement) of CPCs. Next, flower visitor networks were constructed for communities with non-random CPC assembly to confirm the functional role of pollinators in determining floral trait assembly. Key Results: Plant species are unevenly distributed across CPCs, the majority of which are not phylogenetically conserved, suggesting that certain CPCs have a selective advantage. Clustering of CPCs in communities is more frequent than overdispersion, and this does not reflect non-random phylogenetic assembly. In most communities at least one CPC is overrepresented relative to null assemblages. Interaction networks show that each community has a single dominant pollinator that strongly interacts with the overrepresented CPC, suggesting a role for pollinator preferences in driving clustered assembly of CPCs within daisy communities. Conclusion: This novel approach, which demonstrates non-random assembly of complex flower colour patterns and corroborates their functional association with particular pollinators, provides strong evidence that pollinators influence plant community assembly. Results suggest that in some community contexts the benefits of pollinator sharing outweigh the costs of heterospecific pollen transfer, generating clustered assembly. They also challenge the perception of generalized pollination in daisies, suggesting instead that complex daisy colour patterns represent a pollination syndrome trait linked to specific fly pollinators.

Significant Local-Scale Plant-Insect Species Richness Relationship Independent of Abiotic Effects in the Temperate Cape Floristic Region Biodiversity Hotspot.

Globally plant species richness is a significant predictor of insect richness. Whether this is the result of insect diversity responding directly to plant diversity, or both groups responding in similar ways to extrinsic factors, has been much debated. Here we assess this relationship in the Cape Floristic Region (CFR), a biodiversity hotspot. The CFR has higher plant diversity than expected from latitude (i.e., abiotic conditions), but very little is known about the diversity of insects residing in this region. We first quantify diversity relationships at multiple spatial scales for one of the dominant plant families in the CFR, the Restionaceae, and its associated insect herbivore community. Plant and insect diversity are significantly positively correlated at the local scales (10-50 m; 0.1-3 km), but not at the regional scales (15-20 km; 50-70 km). The local scale relationship remains significantly positively correlated even when accounting for the influence of extrinsic variables and other vegetation attributes. This suggests that the diversity of local insect assemblages may be more strongly influenced by plant species richness than by abiotic variables. Further, vegetation age and plant structural complexity also influenced insect richness. The ratio of insect species per plant species in the CFR is comparable to other temperate regions around the world, suggesting that the insect diversity of the CFR is high relative to other areas of the globe with similar abiotic conditions, primarily as a result of the unusually high plant diversity in the region.