Macroevolution of the plant–hummingbird pollination system

ABSTRACTPlant–hummingbird interactions are considered a classic example of coevolution, a process in which mutually dependent species influence each other's evolution. Plants depend on hummingbirds for pollination, whereas hummingbirds rely on nectar for food. As a step towards understanding coevolution, this review focuses on the macroevolutionary consequences of plant–hummingbird interactions, a relatively underexplored area in the current literature. We synthesize prior studies, illustrating the origins and dynamics of hummingbird pollination across different angiosperm clades previously pollinated by insects (mostly bees), bats, and passerine birds. In some cases, the crown age of hummingbirds pre‐dates the plants they pollinate. In other cases, plant groups transitioned to hummingbird pollination early in the establishment of this bird group in the Americas, with the build‐up of both diversities coinciding temporally, and hence suggesting co‐diversification. Determining what triggers shifts to and away from hummingbird pollination remains a major open challenge. The impact of hummingbirds on plant diversification is complex, with many tropical plant lineages experiencing increased diversification after acquiring flowers that attract hummingbirds, and others experiencing no change or even a decrease in diversification rates. This mixed evidence suggests that other extrinsic or intrinsic factors, such as local climate and isolation, are important covariables driving the diversification of plants adapted to hummingbird pollination. To guide future studies, we discuss the mechanisms and contexts under which hummingbirds, as a clade and as individual species (e.g. traits, foraging behaviour, degree of specialization), could influence plant evolution. We conclude by commenting on how macroevolutionary signals of the mutualism could relate to coevolution, highlighting the unbalanced focus on the plant side of the interaction, and advocating for the use of species‐level interaction data in macroevolutionary studies

Bats, birds, and Burmeistera: The evolution of specialized pollination in the neotropics

Specialization in pollination systems has been a central process in the evolution and diversification of angiosperms. However, we still lack an understanding of why plants specialize or switch pollination modes. I studied various aspects of the pollination and floral evolution of the neotropical subshrub, Burmeistera (Campanulaceae). Videotaping flowers and quantifying pollen transfer demonstrated that most species are pollinated by bats, with hummingbirds occasionally serving as secondary pollinators. One species (Burmeistera rubrosepala) was exclusively pollinated by hummingbirds. Floral traits matched the traditional bat and hummingbird pollination syndromes. The degree of exsertion of the floral reproductive parts varied extensively across the genus. To explore the adaptive significance of this trait, I analyzed pollen deposition on Burmeistera flowers, and captured bats to examine pollen loads on their fur. Results show that variation in exsertion length does not correspond to specialization on different pollinators; hummingbirds are not more effective pollinators of short-exserted flowers, and different bat species are just as effective pollinators of all flower types. However, pollen from differently-exserted flowers was found on different regions of bats\u27 heads, suggesting that variation in exsertion may serve to reduce competition for pollination by spatially partitioning bats\u27 bodies. Flight cage experiments with bats and pairs of Burmeistera provide further support for this hypothesis: the greater the difference in exsertion length, the less pollen transferred interspecifically. Additionally, null model analyses of 18 sites (each with 2-4 Burmeistera species) demonstrated that exsertion lengths of coexisting species were significantly overdispersed relative to what would be expected by chance. Thus results provide strong evidence of floral character displacement: coexisting Burmeistera evolved different exsertion lengths to reduce competition for pollination. For the final part of this project, I wanted to know why Burmeistera specialize on pollination by either bats or hummingbirds rather than using both. Flight cage experiments with artificial flowers demonstrated that flower-pollinator fit is critical; wide corollas guided bat snouts better, while narrow corollas guided hummingbird bills better. Poor fit resulted in variable entry angles and decreased pollen transfer. This adaptive tradeoff was strong enough to favor specialization rather than generalization on both bats and hummingbirds

Fur versus Feathers: Pollen Delivery by Bats and Hummingbirds, and Consequences for Pollen Production

One floral characteristic associated with bat pollination (chiropterophily) is copious pollen production, a pattern we confirmed in a local comparison of hummingbird- and bat-adapted flowers from a cloud forest site in Ecuador. Previous authors have suggested that wasteful pollen transfer by bats accounted for the pattern. Here we propose and test a new hypothesis: bats select for increased pollen production because they can efficiently transfer larger amounts of pollen, which leads to a more linear male fitness gain curve for bat-pollinated plants. Flight cage experiments with artificial flowers and flowers of Aphelandra acanthus provide support for this hypothesis; in both instances, the amount of pollen delivered to stigmas by birds is not related to the amount of pollen removed from anthers on the previous visit, while the same function for bats increases linearly. Thus, increased pollen production will be linearly related to increased male reproductive success for bat flowers, while for bird flowers, increased pollen production leads to rapidly diminishing fitness returns. We speculate that fur takes up and holds more pollen than feathers, which seem to readily shed excess grains. Our gain-curve hypothesis may also explain why evolutionary shifts from bird to bat pollination seem more common than shifts in the opposite direction

Data from: The complexity of background clutter affects nectar bat use of flower odor and shape cues

Given their small size and high metabolism, nectar bats need to be able to quickly locate flowers during foraging bouts. Chiropterophilous plants depend on these bats for their reproduction, thus they also benefit if their flowers can be easily located, and we would expect that floral traits such as odor and shape have evolved to maximize detection by bats. However, relatively little is known about the importance of different floral cues during foraging bouts. In the present study, we undertook a set of flight cage experiments with two species of nectar bats (Anoura caudifer and A. geoffroyi) and artificial flowers to compare the importance of shape and scent cues in locating flowers. In a training phase, a bat was presented an artificial flower with a given shape and scent, whose position was constantly shifted to prevent reliance on spatial memory. In the experimental phase, two flowers were presented, one with the training-flower scent and one with the training-flower shape. For each experimental repetition, we recorded which flower was located first, and then shifted flower positions. Additionally, experiments were repeated in a simple environment, without background clutter, or a complex environment, with a background of leaves and branches. Results demonstrate that bats visit either flower indiscriminately with simple backgrounds, with no significant difference in terms of whether they visit the training-flower odor or training-flower shape first. However, in a complex background olfaction was the most important cue; scented flowers were consistently located first. This suggests that for well-exposed flowers, without obstruction from clutter, vision and/or echolocation are sufficient in locating them. In more complex backgrounds, nectar bats depend more heavily on olfaction during foraging bouts

Dryad_diani_stats

Summarizes data from flight cage experiments for each individual bat (A-L) of the two species (Anoura caudifer or Anoura geoffroyi) for the two background types (Simple vs. Complex) and two scent types (Banana vs. Sulfur). "Trial1" and "Trial2" columns give the number of visits to the scented flower (out of the twenty total visits recorded; that is, 20 less this number is the number of visits to the unscented flower with the 'training-flower' shape)

A Gradient of Pollination Specialization in Three Species of Bolivian Centropogon

PremiseClosely related plant species with overlapping ranges often experience competition for pollination services. Such competition can select for divergence in floral traits that attract pollinators or determine pollen placement. While most species in Centropogon(Campanulaceae: Lobelioideae) have flowers that suggest adaptation to bat or hummingbird pollination, actual pollinators are rarely documented, and a few species have a mix of traits from both pollination syndromes. We studied the pollination biology of a “mixed‐syndrome” species and its co‐occurring congeners to examine the relationship between floral traits and visitation patterns for Centropogon.Methods Fieldwork at two sites in Bolivian cloud forests involved filming floral visitors, quantifying pollen transfer, and measuring floral traits. Stamen exsertion, which determines pollen placement, was measured from herbarium specimens across the geographic range of these species to test for character displacement.Results Results show a generalization gradient, from primarily bat pollination in white‐flowered Centropogon incanus, to bat pollination with secondary hummingbird pollination in the cream‐flowered C. brittonianus, to equal reliance on both pollinators in the red‐flowered, mixed‐syndrome C. mandonis. Pollen transfer between these species is further reduced by differences in stamen exsertion that are accentuated in zones of sympatry, a pattern consistent with character displacement.Conclusions Our results demonstrate that key differences in floral color and shape mediate a gradient of specialization in Bolivian Centropogon. Interspecific pollen transfer is further reduced by potential character displacement of a key trait. Broadly, our results have implications for understanding the hyper‐diversity of Andean cloud forests, in which multiple species of the same genus frequently co‐occur.PUBLISHER’S VERSION: https://bsapubs.onlinelibrary.wiley.com/doi/full/10.1002/ajb2.127