Interspecific pollen loss by hummingbirds visiting flower mixtures: Effects of floral architecture

Tropical hummingbirds often forage in mixtures of several plant species. As a result, pollen is often transferred among heterospecific flowers. The ''Sexual Architecture Hypothesis,'' a paradigm of pollination ecology and angiosperm evolution, suggests that the severity of such interspecific pollen transfer should reflect the similarity in the architecture of sexual structures (specifically, placement of stigma and anthers) among the flowers involved. We evaluated the hypothesis with six species of Costa Rican cloud-forest plants varying greatly in sexual architecture but all pollinated by the same hummingbird, Lampornis calolaema. Captive Lampornis visited five long-styled, ''pollen-donor'' flowers of distylous, self-incompatible Palicourea lasiorrachis (Rubiaceae), then 20 short-styled recipient flowers of Palicourea, with or without five flowers of a second species intervening. We assessed intraspecific pollen transfer from Palicourea donors by counting pollen tubes in styles of the recipients. We examined interspecific pollen transfer between Palicourea and each of the five other species by counting heterospecific grains deposited on stigmas of Palicourea recipients, and Palicourea grains deposited on stigmas and anthers of the heterospecific flowers. In a separate experiment, we examined how mixed-species flower visits modified the pollen loads actually carried by birds. Results did not uphold the Sexual Architecture Hypothesis. A single visit to any heterospecific flower greatly affected the hummingbird's prior load of Palicourea pollen, regardless of where the second species placed its own pollen on the bird. Interspecific pollen transfer occurred consistently, but (1) heterospecific grains usurped little space on stigmas of Palicourea recipients and had no discernible effect on pollen-tube growth, whereas (2) few Palicourea grains landed specifically on anthers and stigmas of heterospecific flowers. Instead, numerous Palicourea grains apparently were scraped off on other floral structures such as the corolla. Consequently, every species of intervening flowers, regardless of its sexual architecture per se, strongly reduced pollen transfer from donor to recipient Palicourea flowers, on average by 76%. In fact, the most drastic reductions resulted from the two species whose sexual architectures least resembled that of Palicourea. Results imply that ''pollen scraping'' by floral structures other than anthers and stigmas may be important and widespread among some animal-pollinated flowers. Thus, except in cases where no other floral structures contact pollinators, the positions of anthers and stigmas alone may have little bearing on the severity of interspecific pollen transfer and competitive interactions among plants sharing pollinators.