A multivariate search for pollination syndromes among penstemons. -Oikos 104: 345-361.The seeming ubiquity of spatio-temporal variation in pollination regime suggests that flowers ought to be adapted to a wide range of pollinators, yet many comparative biologists perceive that in groups with complex flowers there is considerable specialization onto pollination syndromes. Statistical documentation of such syndromes has been presented for very few groups of flowers. Accordingly, we measured, for 49 species of Penstemon and close relatives, both the morphology of the flowers and visitation by pollinators. We describe the mechanics of pollination for representative species. Ordinations show a distinct difference between hummingbird-pollinated species and hymenopteran-pollinated species. Flower color is particularly good at separating hummingbird-from hymenopteran-flowers. Other characters are also correlated with this dichotomy. Within the hymenopteran-pollinated species, there are additional relationships between floral morphology and the size of the principal pollinators. Flowers frequented by large bees, such as Xylocopa, have large open vestibules and relatively short floral tubes. Flowers frequented by smaller bees, such as Osmia, have long narrow floral tubes. Unlike nectar-collecting bees, pollencollecting bees tend to be attracted to flowers of the hummingbird syndrome. The overarching pattern was that syndrome characterizations were successful at predicting pollination by hummingbirds versus Hymenoptera, two types of animals that are profoundly different, but less successful at predicting visitation by one kind of bee versus another.

Floral phenotypes may be as much the result of selection for avoidance of some animal visitors as selection for improving the interaction with better pollinators. When specializing on hummingbird‐pollination, Penstemon flowers may have evolved to improve the morphological fit between bird and flower, or to exclude less‐efficient bees, or both. We hypothesized how such selection might work on four floral characters that affect the mechanics of pollen transfer: anther/stigma exsertion, presence of a lower corolla lip, width of the corolla tube, and angle of flower inclination. We surgically modified bee‐pollinated P. strictus flowers changing one trait at a time to make them resemble hummingbird‐pollinated P. barbatus flowers, and measured pollen transfer by bumblebees and hummingbirds. Results suggest that, apart from ‘pro‐bird’ adaptations, specific ‘anti‐bee’ adaptations have been important in shaping hummingbird‐flowers. Moreover, some trait changes may have been selected for only if changing in concert with other traits.

We compared pollen removal and deposition by hummingbirds and bumblebees visiting bird-syndrome Penstemon barbatus and bee-syndrome P. strictus flowers. One model for evolutionary shifts from bee pollination to bird pollination has assumed that, mostly due to grooming, pollen on bee bodies quickly becomes unavailable for transfer to stigmas, whereas pollen on hummingbirds has greater carryover. Comparing bumblebees and hummingbirds seeking nectar in P. strictus, we confirmed that bees had a steeper pollen carryover curve than birds but, surprisingly, bees and birds removed similar amounts of pollen and had similar per-visit pollen transfer efficiencies. Comparing P. barbatus and P. strictus visited by hummingbirds, the bird-syndrome flowers had more pollen removed, more pollen deposited, and a higher transfer efficiency than the bee-syndrome flowers. In addition, P. barbatus flowers have evolved such that their anthers and stigmas would not easily come into contact with bumblebees if they were to forage on them. We discuss the role that differences in pollination efficiency between bees and hummingbirds may have played in the repeated evolution of hummingbird pollination in Penstemon.