The biomechanics of pollen release: new perspectives on the evolution of wind pollination in angiosperms.

Evolutionary transitions from animal to wind pollination have occurred repeatedly during the history of the angiosperms, but the selective mechanisms remain elusive. Here, we propose that knowledge of pollen release biomechanics is critical for understanding the ecological and evolutionary processes underpinning this shift in pollination mode. Pollen release is the critical first stage of wind pollination (anemophily) and stamen properties are therefore likely to be under strong selection early in the transition. We describe current understanding of pollen release biomechanics to provide insights on the phenotypic and ecological drivers of wind pollination. Pollen release occurs when detachment forces dominate resistive forces retaining pollen within anthers. Detachment forces can be active or passive depending on whether they require energy input from the environment. Passive release is more widespread in anemophilous species and involves processes driven by steady or unsteady aerodynamic forces or turbulence-induced vibrations that shake pollen from anthers. We review empirical and theoretical studies suggesting that stamen vibration is likely to be a key mechanism of pollen release. The vibration response is governed by morphological and biomechanical properties of stamens, which may undergo divergent selection in the presence or absence of pollinators. Resistive forces have rarely been investigated for pollen within anthers, but are probably sensitive to environmental conditions and depend on flower age, varying systematically between animal- and wind-pollinated species. Animal and wind pollination are traditionally viewed as dichotomous alternatives because they are usually associated with strikingly different pollination syndromes. But this perspective has diverted attention from subtler, continuously varying traits which mediate the fluid dynamic process of pollen release. Reinterpreting the flower as a biomechanical entity that responds to fluctuating environmental forces may provide a promising way forward. We conclude by identifying several profitable areas for future research to obtain deeper insight into the evolution of wind pollination.

Influence of local density and sex ratio on pollination in an ambophilous flowering plant.

PREMISE: Variation in local density and sex ratio in dioecious plants can affect mating success through the actions of pollen vectors, principally generalist insects or wind. Increased density and male-biased sex ratios should promote pollen transfer and seed production, but their combined effects have not been investigated for ambophilous species, which exhibit both insect and wind pollination. METHODS: We manipulated density (low vs. high) and sex ratio (1:1 vs. 3:1 male-biased) in arrays of dioecious ambophilous Thalictrum pubescens. We quantified visitation rates and foraging times to examine whether pollinators exhibited sex-specific preferences and determined the seed set of arrays. RESULTS: Pollinators visited more plants per foraging bout at high than low density. Visitation rates and foraging times of visitors were greater for male than for female plants but did not depend on the density or sex ratio of arrays. However, whereas solitary bees displayed a strong preference for males, hover flies were indifferent to plant sex phenotype. Solitary bees also visited significantly more plants per foraging bout than hover flies. There was a significant interaction between density and sex ratio on seed set. At low density, seed set was greater for 3:1 than for 1:1 arrays, but at high density the opposite pattern occurred. CONCLUSIONS: The demographic factors we investigated had complex influences on pollinator foraging behavior and patterns of seed set. Several factors may explain our results, including the influence of density and sex ratio on pollen export from arrays, grooming by pollinators, and the contribution of wind pollination.

Comparative analysis of pollen release biomechanics in Thalictrum: implications for evolutionary transitions between animal and wind pollination.

Transitions from animal to wind pollination have occurred repeatedly in flowering plants, driven by structural and biomechanical modifications to flowers. But the initial changes promoting wind pollination are poorly understood, especially those required to release pollen into airflows - the critical first stage of wind pollination. Using a wind tunnel, we performed a comparative study of pollen release biomechanics in 36 species of animal- and wind-pollinated Thalictrum. We quantified pollination syndromes and stamen natural frequency (fn ), a key vibration parameter, to determine if floral traits reliably predicted pollen release probability. We then investigated if pollen release was caused by wind-induced resonance vibration of stamens. We detected wind-induced stamen resonance in 91% of species and a strong effect of stamen acceleration on pollen release, inversely driven by fn . However, unlike fn , pollination syndromes did not reliably predict the probability of pollen release among species. Our results directly link fn to the capacity of stamens to release pollen by wind and suggest that structural mechanisms reducing fn are likely to be important for initiating transitions from animal to wind pollination. Our inability to predict the probability of pollen release based on pollination syndromes suggests diverse phenotypic trajectories from animal to wind pollination.

Divergent selection on the biomechanical properties of stamens under wind and insect pollination.

Wind pollination has evolved from insect pollination in numerous angiosperm lineages and is associated with a characteristic syndrome of morphological traits. The traits initiating transitions to wind pollination and the ecological drivers involved are poorly understood. Here, we examine this problem in Thalictrum pubescens, an ambophilous (insect and wind pollination) species that probably represents a transitional state in the evolution of wind pollination. We investigated wind-induced pollen release by forced harmonic motion by measuring stamen natural frequency ( fn), a key vibration parameter, and its variability among nine populations. We assessed the repeatability of fn over consecutive growing seasons, the effect of this parameter on pollen release in a wind tunnel, and male reproductive success in the field using experimental manipulation of the presence or absence of pollinators. We found significant differences among populations and high repeatability within genotypes in fn. The wind tunnel assay revealed a strong negative correlation between fn and pollen release. Siring success was greatest for plants with lower fn when pollinators were absent, but this advantage diminished when pollinators were present. Our biomechanical analysis of the wind-flower interface has identified fn as a key trait for understanding early stages in the transition from insect to wind pollination.

Turbulence-induced resonance vibrations cause pollen release in wind-pollinated Plantago lanceolata L. (Plantaginaceae).

In wind pollination, the release of pollen from anthers into airflows determines the quantity and timing of pollen available for pollination. Despite the ecological and evolutionary importance of pollen release, wind-stamen interactions are poorly understood, as are the specific forces that deliver pollen grains into airflows. We present empirical evidence that atmospheric turbulence acts directly on stamens in the cosmopolitan, wind-pollinated weed, Plantago lanceolata, causing resonant vibrations that release episodic bursts of pollen grains. In laboratory experiments, we show that stamens have mechanical properties corresponding to theoretically predicted ranges for turbulence-driven resonant vibrations. The mechanical excitation of stamens at their characteristic resonance frequency caused them to resonate, shedding pollen vigorously. The characteristic natural frequency of the stamens increased over time with each shedding episode due to the reduction in anther mass, which increased the mechanical energy required to trigger subsequent episodes. Field observations of a natural population under turbulent wind conditions were consistent with these laboratory results and demonstrated that pollen is released from resonating stamens excited by small eddies whose turnover periods are similar to the characteristic resonance frequency measured in the laboratory. Turbulence-driven vibration of stamens at resonance may be a primary mechanism for pollen shedding in wind-pollinated angiosperms. The capacity to release pollen in wind can be viewed as a primary factor distinguishing animal- from wind-pollinated plants, and selection on traits such as the damping ratio and flexural rigidity may be of consequence in evolutionary transitions between pollination systems.