A lever action hypothesis for pendulous hummingbird flowers: experimental evidence from a columbine

Abstract

Background and Aims Pendulous flowers (due to a flexible pedicel) are a common, convergent trait of hummingbird-pollinated flowers. However, the role of flexible pedicels remains uncertain despite several functional hypotheses. Here we present and test the ‘lever action hypothesis’: flexible pedicels allow pendulous flowers to move upwards from all sides, pushing the stigma and anthers against the underside of the feeding hummingbird regardless of which nectary is being visited. Methods To test whether this lever action increased pollination success, we wired emasculated flowers of serpentine columbine, Aquilegia eximia, to prevent levering and compared pollination success of immobilized flowers with emasculated unwired and wire controls. Key Results Seed set was significantly lower in wire-immobilized flowers than unwired control and wire control flowers. Video analysis of visits to wire-immobilized and unwired flowers demonstrated that birds contacted the stigmas and anthers of immobilized flowers less often than those of flowers with flexible pedicels. Conclusions We conclude that flexible pedicels permit the levering of reproductive structures onto a hovering bird. Hummingbirds, as uniquely large, hovering pollinators, differ from flies or bees which are too small to cause levering of flowers while hovering. Thus, flexible pedicels may be an adaptation to hummingbird pollination, in particular due to hummingbird size. We further speculate that this mechanism is effective only in radially symmetric flowers; in contrast, zygomorphic hummingbird-pollinated flowers are usually more or less horizontally oriented rather than having pendulous flowers and flexible pedicels.

Review of "Birds & Flowers: An Intimate 50 Million Year Relationship"

“…In comparison with a recent review of bird pollination (Pauw 2019), less emphasis is given to natural selection by plants on bird traits, and also to how shape or other aspects of morphology of bird-pollinated flowers affect aspects of plant fitness, especially those that might differ from flower visitation. Floral morphology is certainly discussed, but not the rich complexity of how traits such as width or length of a tube, positioning of anthers, flexible pedicels, or spur curvature affects the amount of pollen removed, where it goes on a bird, or how much pollen is dispersed (Campbell et al 1996;Fulton & Hodges 1999;Kay 2006;LoPresti et al 2019). Such aspects of microevolution can provide a link between the ecology and macroevolution.…”

Como a assimetria de seleção e de especialização afetam a dinâmica coevolutiva em mutualismos?

“…Combining our results on indirect effects contribution to trait evolution and a stronger selection imposed on plant traits, it might contribute to the understanding on why: i) floral traits tend to rapidly evolve and; ii) flowers and fruits often show evidence of trait convergence, leading pollination and seed dispersal syndromes, whereas similar trait patterns are less common in animals (Howe and Smallwood 1982. In this context, indirect effects would be concentrated among plant species in plantanimal mutualisms, giving rise to trait convergence only in this set of species (Papiorek et al 2016, LoPresti et al 2020. For instance, in plant-hummingbird interactions in the tropics, convergent evolution is known to play a major role in shaping floral traits (Martín González et al 2015.…”