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

Abstract

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.

Precision Pollination Strategies for Advancing Horticultural Tomato Crop Production

“…Poricidal anthers (those that open by a terminal pore, as in tomato) do not expel pollen from incidental contact, which would be wasteful, but require the 'buzz' of correct sonication for pollen release [12]. In essence, this morphology filters the taxa able to extract pollen through vibrations, as a means of ensuring its pollinators are effective at transmitting its gametes to the appropriate destinations [59]. When visits decrease, the pollen released per extraction is increased, as a compensatory mechanism [12].…”

“…Pollen reward is largest upon the first visit, but multiple or extended visits are necessary for complete extraction. Because of this, bees spend more time on newly opened flowers [59].…”

“…The amount of pollen released can increase with higher vibration velocities when artificially simulated [59]. In terms of the poricidal anther dispensing mechanisms, the vibration frequencies used by bees are likely to expel less pollen compared to higher optimal mechanical frequencies that are unattainable by a bee.…”

How and why do bees buzz? Implications for buzz pollination

“…Producing vibrations at maximum frequency regardless of bee size might be beneficial to increase the rate of pollen removed using vibrations ( Corbet and Huang, 2014 ; Switzer et al , 2019 ). For a given maximum displacement of the thorax, higher frequency vibrations should result in larger velocity and acceleration amplitudes, which in turn are associated with more pollen released from buzz-pollinated flowers ( Buchmann and Hurley, 1978 ; Harder and Barclay, 1994 ; King and Buchmann, 1996 ; De Luca et al , 2013 ; Corbet and Huang, 2014 ; Vallejo-Marín, 2019 ; Rosi-Denadai et al , 2020 ; Kemp and Vallejo-Marin, 2021 ).…”

Stamen dimorphism in bird‐pollinated flowers: Investigating alternative hypotheses on the evolution of heteranthery

“…Pollen can only be removed in small doses from these poricidal anthers when bees apply specific vibrations (buzzes) to the flowers (Dellinger et al. 2019a; Harder and Wilson 1994; Kemp and Vallejo‐Marín 2020). Thus, poricidal anthers and buzz‐pollination are generally interpreted as strategies to alleviate the “pollen dilemma” through pollen dosing.…”