-
[show abstract]
[hide abstract]
ABSTRACT: It has been proposed frequently, from Darwin’s time onwards, that specialized pollination increases speciation rates and thus
the diversity of plant species (i.e. clade species richness). We suggest here that the correlation between clade species richness
and floral specialization is real, but that clade species richness is frequently the cause, not the result of floral specialization.
We urge a broader, variance-partitioning perspective for assessing the causes of this correlation by suggesting four models
of how the diversity-specialization correlation might come about: (1) floral specialization promotes initial reproductive
isolation (“Initial-RI” model), (2) floral specialization promotes reinforcement of reproductive isolation upon secondary
contact (“Reinforcement” model), (3) floral specialization reduces the extinction rate by promoting tighter species packing
(“Extinction” model), (4) floral specialization is the result of high clade species richness, which increases the number of
related species in communities, and thus selects for floral character displacement (“Character-Displacement” model). These
hypotheses are evaluated by comparing the relationships between species richness, speciation mechanisms, and pollination precision,
accuracy, and specialization in the broader literature and, more specifically, in four study systems: Dalechampia (Euphorbiaceae), Collinsia (Plantaginaceae), Burmeistera (Campanulaceae), and Stylidium (Stylidiaceae). These systems provide stronger support for the character-displacement hypothesis, wherein local species diversity
drives the evolution of specialized pollination. Although the two reproductive-isolation hypotheses may hold for plants like
orchids, with extremely precise pollination systems, the reproductive character-displacement hypothesis seems likely to be
more important for plant groups with less precise pollination systems.
Evolutionary Ecology 04/2012; 23(1):159-179. · 2.45 Impact Factor
-
[show abstract]
[hide abstract]
ABSTRACT: Specialization in pollination systems played a central role in angiosperm diversification, yet the evolution of specialization remains poorly understood. Competition through interspecific pollen transfer may select for specialization through costs to male fitness (pollen lost to heterospecific flowers) or female fitness (heterospecific pollen deposited on stigmas). Previous theoretical treatments of pollination focused solely on seed set, thus overlooking male fitness. Here we use individual-based models that explicitly track pollen fates to explore how competition affects the evolution of specialization. Results show that plants specialize on different pollinators when visit rates are high enough to remove most pollen from anthers; this increases male fitness by minimizing pollen loss to foreign flowers. At low visitation, plants generalize, which minimizes pollen left undispersed in anthers. A model variant in which plants can also evolve differences in sex allocation (pollen/ovule production) produces similar patterns of specialization. At low visitation, plants generalize and allocate more to female function. At high visitation, plants specialize and allocate equally to both sexes (in line with sex-allocation theory). This study demonstrates that floral specialization can be driven by selection through male function alone and more generally highlights the importance of community context in the ecology and evolution of pollination systems.
The American Naturalist 10/2010; 176(6):732-43. · 4.72 Impact Factor
-
[show abstract]
[hide abstract]
ABSTRACT: 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.
The American Naturalist 06/2010; 175(6):717-26. · 4.72 Impact Factor
-
[show abstract]
[hide abstract]
ABSTRACT: In a hypothesis that has remained controversial since its inception, Darwin suggested that long-tubed flowers and long-tongued pollinators evolved together in a coevolutionary race, with each selecting for increasing length in the other. Although the selective pressures that flowers impose on tongue length are relatively straightforward, in that longer tongues allow access to more nectar, selective pressures that pollinators impose on flower length are less clear. Here, we test for such selective pressures in the highly specialized mutualism between the nectar bat Anoura fistulata, which can extend its tongue twice as far as other nectar bats, and Centropogon nigricans, which has flowers of a similar length (8-9 cm). We used flight cage experiments to examine the effects of artificially manipulated flower lengths on (i) bat behaviour and (ii) pollen transfer. Increased length produced longer visits, but did not affect the force bats applied during visits. In the second experiment, flower length increased both the male and female components of flower function: long male flowers delivered more pollen grains and long female flowers received more pollen grains. However, pollen transfer was not correlated with visit duration, so the mechanism behind differences in pollen transfer remains unclear. By demonstrating that bats select for increasing flower length, these results are consistent with the hypothesis that A. fistulata evolved its remarkable tongue in a coevolutionary race with long-tubed flowers similar to that envisioned by Darwin.
Proceedings of the Royal Society B: Biological Sciences 04/2009; 276(1665):2147-52. · 5.41 Impact Factor
-
[show abstract]
[hide abstract]
ABSTRACT: A number of different types of flower-visiting animals coexist in any given habitat. What evolutionary and ecological factors influence the subset of these that a given plant relies on for its pollination? Addressing this question requires a mechanistic understanding of the importance of different potential pollinators in terms of visitation rate (pollinator 'quantity') and effectiveness at transferring pollen (pollinator 'quality') is required. While bat-pollinated plants typically are highly specialized to bats, there are some instances of bat-pollinated plants that use other pollinators as well. These generalized exceptions tend to occur in habitats where bat 'quantity' is poor due to low or fluctuating bat densities.
Aphelandra acanthus occurs in tropical cloud forests with relatively high densities of bat visitors, yet displays a mix of floral syndrome characteristics, suggesting adaptation to multiple types of pollinators. To understand its pollination system better, aspects of its floral phenology and the 'quantity' and 'quality' components of pollination by its floral visitors are studied here.
Flowers were found to open and senesce throughout the day and night, although anther dehiscence was restricted to the late afternoon and night. Videotaping reveals that flowers are visited nocturnally by bats and moths, and diurnally by hummingbirds. Analysis of pollen deposition shows that bats regularly transfer large amounts of conspecific pollen, while hummingbirds occasionally transfer some pollen, and moths rarely do so.
Hummingbirds and bats were comparable in terms of pollination 'quantity', while bats were the most effective in terms of 'quality'. Considering these components together, bats are responsible for approx. 70 % of A. acanthus pollination. However, bats also transferred remarkably large amounts of foreign pollen along with the conspecific grains (three of four grains were foreign). It is suggested that the negative effects of interspecific pollen transfer may decrease bat 'quality' for A. acanthus, and thus select for generalization on multiple pollinators instead of specialization on bats.
Annals of Botany 02/2009; 103(9):1481-7. · 4.03 Impact Factor
-
[show abstract]
[hide abstract]
ABSTRACT: Coexisting plants that share pollinators can compete through interspecific pollen transfer. A long-standing idea holds that divergence in floral morphology may reduce this competition by placing pollen on different regions of the pollinator's bodies. However, surprisingly little empirical support for this idea exists. Burmeistera is a diverse neotropical genus that exhibits wide interspecific variation in the degree to which the reproductive parts are exserted outside the corolla. Coexisting Burmeistera share bats as their primary pollinators, and the degree of exsertion determines the site of pollen deposition on the bats' heads. Here we study the mechanism, process and pattern of floral character displacement for assemblages of coexisting Burmeistera. Flight cage experiments with bats and pairs of Burmeistera species demonstrate that the greater the divergence in exsertion length, the less pollen transferred interspecifically. Null model analyses of exsertion lengths for 19 species of Burmeistera across 18 sites (each containing two to four species) demonstrate that observed assemblage structure is significantly overdispersed relative to what would be expected by chance. Local evolution, rather than ecological sorting, appears to be the primary process driving this pattern of overdispersion because local adaptation of the nine widespread species accounts for a large portion of the observed pattern. Taken together, results of this study provide strong support for the idea that competition through interspecific pollen transfer can drive character displacement in plants.
Proceedings of the Royal Society B: Biological Sciences 12/2007; 274(1626):2731-7. · 5.41 Impact Factor
-
Nathan Muchhala
[show abstract]
[hide abstract]
ABSTRACT: Evolution toward increased specificity in pollination systems is thought to have played a central role in the diversification of angiosperms. Theory predicts that the presence of trade-offs in adapting to different pollinator types will favor specialization, yet few studies have attempted to characterize such interactions in nature. I conducted flight cage experiments with bats, hummingbirds, and artificial flowers to examine effects of corolla width on pollination. I videotaped visits to analyze pollinator behavior and counted pollen grains transferred to stigmas. Results demonstrated that flower-pollinator fit is critical to effective pollination; wide corollas guided bat snouts better, and narrow corollas guided hummingbird bills better. Poor fit resulted in variable entry angles and decreased pollen transfer. A model using these results predicts that wide corollas will be selected for when bats make more than 44% of the visits and narrow corollas when they make fewer. Intermediate corollas are never favored (i.e., generalization is always suboptimal). This is the first study to clearly document a pollinator-mediated fitness trade-off in floral morphology.
The American Naturalist 04/2007; 169(4):494-504. · 4.72 Impact Factor
-
Nathan Muchhala
[show abstract]
[hide abstract]
ABSTRACT: Bats of the subfamily Glossophaginae (family Phyllostomidae) are arguably the most specialized of mammalian nectarivores, and hundreds of neotropical plants rely on them for pollination. But flowers pollinated by bats are not known to specialize for bat subgroups (unlike flowers that have adapted to the length and curvature of hummingbird bills, for example), possibly because the mouthparts of bats do not vary much compared with the bills of birds or the probosces of insects. Here I report a spectacular exception: a recently-described nectar bat that can extend its tongue twice as far as those of related bats and is the sole pollinator of a plant with corolla tubes of matching length.
Nature 01/2007; 444(7120):701-2. · 36.28 Impact Factor
-
Nathan Muchhala
[show abstract]
[hide abstract]
ABSTRACT: The floral traits of plants with specialized pollination systems both facilitate the primary pollinator and restrict other potential pollinators. To explore interactions between pollinators and floral traits of the genus Burmeistera, I filmed floral visitors and measured pollen deposition for 10 species in six cloud forest sites throughout northern Ecuador. Nine species were primarily bat-pollinated (84-100% of pollen transfer); another (B. rubrosepala) was exclusively hummingbird-pollinated. According to a principal components analysis of 11 floral measurements, flowers of B. rubrosepala were morphologically distinct. Floral traits of all species closely matched traditional ornithophilous and chiropterophilous pollination syndromes; flowers of B. rubrosepala were bright red, lacked odor, opened in the afternoon, and had narrow corolla apertures and flexible pedicels, which positioned them below the foliage. Flowers of the bat-pollinated species were dull-colored, emitted odor, opened in the evening, and had wide apertures and rigid pedicels, which positioned them beyond the foliage. Aperture width appeared most critical to restricting pollination; hummingbirds visited wide flowers without contacting the reproductive parts, and bats did not visit the narrow flowers of B. rubrosepala. Aperture width may impose an adaptive trade-off that favors the high degree of specialization in the genus. Other floral measurements were highly variable amongst bat-pollinated species, including stigma exsertion, calyx lobe morphology, and pedicel length. Because multiple species of Burmeistera often coexist, such morphological diversity may reduce pollen competition by encouraging pollinator fidelity and/or spatially partitioning pollinator's bodies.
American Journal of Botany 08/2006; 93(8):1081-9. · 2.66 Impact Factor
-
Nathan Muchhala
[show abstract]
[hide abstract]
ABSTRACT: In this study I documented the degree of specialization in the pollination systems of Burmeistera cyclostigmata and B. tenuiflora (Campanulaceae) to explore the potential role of floral isolation in the diversification of the genus. I asked which floral characteristics are important in specializing on either bat or hummingbird pollination, and whether overlap between these floral syndromes can exist. I examined nocturnal and diurnal pollen deposition, pollinator visitation rates, and single visit effectiveness and related them to intra- and interspecific variation in Burmeistera floral characteristics at Monteverde, Costa Rica. Bats and hummingbirds visited both Burmeistera species, and bats pollinated both species. Owing to differences in floral morphology, however, hummingbirds effectively pollinated only B. tenuiflora. The generalized pollination system of B. tenuiflora demonstrates that there can be overlap in the boundary between ornithophily and chiropterophily, and that nectar production and timing of anthesis do not serve as barriers between these syndromes. The high intraspecific variation in floral color from green to red or purple did not correlate with either nocturnal or diurnal pollen deposition. Degree of flower accessibility did affect pollination; nocturnal pollen deposition significantly decreased as flowers become more obstructed. In Burmeistera, floral morphology and accessibility appear to be the most important floral characteristics for specialization at the boundary between ornithophily and chiropterophily.
Oecologia 03/2003; 134(3):373-80. · 3.41 Impact Factor
