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

Ecology, March, 1996 by Carolina Murcia

Where has all the pollen gone? The "Pollen Scraping Hypothesis"

The Palicourea grains we found on anthers and stigmas of heterospecific flowers (Table 5) were many fewer than those that disappeared from bird bills [ILLUSTRATION FOR FIGURE 2 OMITTED], and were insufficient to explain the drastic declines in pollen tube numbers within recipient Palicourea styles (Table 3A). Where were the other grains? Designing our protocol in line with the Sexual Architecture Hypothesis, we did not look for Palicourea grains on other floral structures (corolla, column, and style). Still, the circumstantial evidence leaves little doubt: the missing grains must have been scraped off on those structures we did not examine, particularly the corolla. For example, while sliding into the constricted, relatively long corollas of Dicliptera and Hansteinia [ILLUSTRATION FOR FIGURE 1 OMITTED], birds' bills contacted the corolla roof just where a Palicourea load would be located [ILLUSTRATION FOR FIGURE 2 OMITTED]. The exserted sexual parts and distinctive pollen placement of these two Acanthaceae species were irrelevant to potential pollen scraping by the corolla, as Fig. 2 and Tables 3 and 5 demonstrate. Among the five intervening species examined, two (Satyria and Dicliptera) commonly have pendant flowers, further increasing the chances of contact between the dorsum of the bird's bill and the corolla roof. In trials with those two species especially, the proportion of grains lost from the dorsal part of Palicourea pollen loads greatly exceeded the proportion lost from the ventral part [ILLUSTRATION FOR FIGURE 2 OMITTED].

As an alternative to the Sexual Architecture Hypothesis, then, we propose the "Pollen Scraping Hypothesis:" any or all floral parts that scrape against a pollen-carrying animal may alter its pollen load and the pollen transfer that results. By this hypothesis, the extent and ecological impact of interspecific pollen loss increase with the increasing likelihood that the pollen load of Species 1 contacts any floral part whatsoever of Species 2, including, but certainly not limited to, the anthers and stigma. In hindsight, the Pollen Scraping Hypothesis seems intuitively obvious, yet, to our knowledge, no empirical test exists. The role of whole-flower morphology in pollination has been examined in detail within plant species (e.g., Murcia 1990, Campbell et al. 1991, 1994, Herrera 1993) but rarely between species (cf. Macior 1982). Given the bewildering variety of flower forms and floral structures even within a single pollination guild, deriving general, testable predictions from the hypothesis may be a daunting task. Nevertheless, the Pollen Scraping Hypothesis could stimulate novel ways to consider floral structures, their proximate consequences for interactions between species (interspecific pollen transfer), and their evolution under the selective pressure of minimizing interspecific pollen loss.

For example, the data of Tables 3 and 5 and Fig. 2 suggest that a competitive asymmetry may exist between short- and long-flowered species even if their pollen placement on the pollinators they share is entirely distinct. Corollas and other parts of long flowers are likely to scrape against the pollen loads deposited by shorter flowers, while the pollen loads deposited by the long flowers themselves might well be untouched by any part of short flowers. Among the five intervening species studies here, long-flowered Hansteinia and Dicliptera affected Palicourea pollen transfer the most (Table 3C), and, like other species, removed most of the grains from Palicourea pollen loads carried by birds [ILLUSTRATION FOR FIGURE 2 OMITTED]. However, few Palicourea grains contaminated the exserted sexual parts of Hansteinia in return (Table 5), and Palicourea pollen loads on birds scarcely affected the ability of Hansteinia to place pollen [ILLUSTRATION FOR FIGURE 2 OMITTED]. This reasoning might apply within polymorphic species as well: for example, pollen from long-stamened, short-styled individuals of distylous species may face fewer risks of scraping and may transfer more effectively to long-styled, short-stamened individuals than pollen travelling in the opposite direction (cf. Feinsinger and Busby 1987). In more general terms, the Pollen Scraping Hypothesis could provide new slants on theories about the evolution of flower form (e.g., Grant and Grant 1965, Leppik 1972, Levin 1978, Willemstein 1987, Nilsson 1988, Vogel 1990, Fenster 1991, Herrera 1993) or the evolution of pollen: ovule ratios (Cruden 1977).