Nathan Muchhala | University of Missouri - St. Louis (original) (raw)

Papers by Nathan Muchhala

PLOS ONE, 2015

Given their small size and high metabolism, nectar bats need to be able to quickly locate flowers... more 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.

Molecular phylogenetics and evolution, Jan 21, 2016

The field of molecular systematics has benefited greatly with the advent of high-throughput seque... more The field of molecular systematics has benefited greatly with the advent of high-throughput sequencing (HTS), making large genomic datasets commonplace. However, a large number of targeted Sanger sequences produced by many studies over the last two decades are publicly available and should not be overlooked. In this study, we elucidate the phylogenetic relationships of the plant genus Burmeistera (Campanulaceae: Lobelioideae), while investigating how to best combine targeted Sanger loci with HTS data. We sequence, annotate, and analyze complete to nearly complete plastomes for a subset of the genus. We then combine these data with a much larger taxonomic dataset for which only Sanger sequences are available, making this the most comprehensively sampled study in the genus to date. We show that using a phylogeny inferred from the species with plastome data as a topological constraint for the larger dataset increases the resolution of our data and produces a more robust evolutionary hy...

Examining dispersal is critical for understanding the diversity of Andean-centered plant lineages... more Examining dispersal is critical for understanding the diversity of Andean-centered plant lineages, like Burmeistera (Campanulaceae). One-third of its species present an unusual inflated berry. Unlike the bright colors of non-inflated fruits in the genus, these fruits are typically dull-green; however, the fact that the seeds are loosely held in the placenta and easily removed when touched seems to suggest adaptation to animal dispersal. We studied two inflated-baccate species, Burmeistera glabrata and B. borjensis, with the aim of testing the non-exclusive hypotheses that their seeds are dispersed by (1) small mammals, (2) slugs, or (3) adult flies that develop inside the fruits. In two sites in the Ecuadorian Andes, we performed observations at dusk and dawn to examine the fate of fruits and seeds; recording fruit fall, formation of holes in the fruits, and seed loss from the placenta. We documented fruit visitors with cameras, and surveyed unopened fruits for the presence of insect larvae and seed condition. Finally, we performed an experiment to examine the effect of holes and rain in germination, in order to evaluate if holes are required for seeds to leave the fruits and subsequently germinate. For both species, most fruits fell and decomposed beneath the mother plant. However, we found limited support for small mammal dispersal; videos and observations revealed that mice and squirrels are potential, but rare, seed dispersers. We found no evidence for slug or fly dispersal; fly larvae were common inside fruits, but acted exclusively as seed predators. Crickets often chewed holes in fruits on plants and on the ground. Holes did not have an effect on germination, which was induced only by rain. Hence, the majority of seeds end up under the mother plant, with rare but potentially important events of primary or secondary dispersal by small mammals. The combination of limited dispersal due to gravity and rare events of mammal dispersal may have played a critical role in the rapid diversification of Burmeistera.

Novon: A Journal for Botanical Nomenclature, 2015

Evolutionary Ecology, 2015

Darwin hypothesized that extremely long flowers and the long mouthparts of the animals that polli... more Darwin hypothesized that extremely long flowers and the long mouthparts of the animals that pollinate them evolved together in a coevolutionary race. While selective pressures for the animal side of such a race are relatively clear (longer tongues allow the animal to reach more ...

American journal of botany, 2014

Evolution, 2014

One classic explanation for the remarkable diversity of flower colors across angiosperms involves... more One classic explanation for the remarkable diversity of flower colors across angiosperms involves evolutionary shifts among different types of pollinators with different color preferences. However, the pollinator shift model fails to account for the many examples of color variation within clades that share the same pollination system. An alternate explanation is the competition model, which suggests that color divergence evolves in response to interspecific competition for pollinators, as a means to decrease interspecific pollinator movements. This model predicts color overdispersion within communities relative to null assemblages. Here, we combine morphometric analyses, field surveys, and models of pollinator vision with a species-level phylogeny to test the competition model in the primarily hummingbird-pollinated clade Iochrominae (Solanaceae). Results show that flower color as perceived by pollinators is significantly overdispersed within sites. This pattern is not simply due to phylogenetic history: phylogenetic community structure does not deviate from random expectations, and flower color lacks phylogenetic signal. Moreover, taxa that occur in sympatry occupy a significantly larger volume of color space than those in allopatry, supporting the hypothesis that competition in sympatry drove the evolution of novel colors. We suggest that competition among close relatives may commonly underlie floral divergence, especially in species-rich habitats where congeners frequently co-occur.

Functional Ecology, Jan 1, 2012

1. Although competition for pollination is often invoked as a driver of broad-scale evolutionary ... more 1. Although competition for pollination is often invoked as a driver of broad-scale evolutionary and ecological patterns, we still lack a clear understanding of the mechanics of such competition. When flower visitors alternate between two species of flower, heterospecific pollen transfer takes place. The impact of these mixed loads on the female reproductive success of a recipient has received considerable attention, but the concomitant loss of male reproductive success -because of pollens grains being lost to foreign stigmas -has received less. Furthermore, pollen losses are not limited to grains that land on stigmas, but can also include deposition on non-stigmatic surfaces of the intervening flowers, or loss from the animal's body through passive detachment or active grooming. We collectively term these losses because of competition 'pollen misplacement'. 2. Here, we quantify pollen transferred by nectar bats between focal flowers (Aphelandra acanthus) with and without intervening visits to one of two competitor species. One competitor (Centropogon nigricans) places its pollen in the same region of bats' heads as the focal species, while the other (Burmeistera sodiroana) places its pollen farther forward. 3. We found that (i) any intervening visit caused some reduction in the number of pollen grains transferred, (ii) competitor flowers with similar pollen-placement locations caused greater reductions in pollen transfer and (iii) of these competitors, those in male phase (dispensing pollen) caused greater pollen loss than those in female phase (without pollen). 4. This study provides rare empirical support for the detrimental effects of competition for pollination on male fitness via pollen misplacement and is the first to show an added cost imposed by male-phase competitors. Although this competition is especially strong when competitors overlap in pollen placement, diverging in pollen placement will not completely eliminate pollen loss during visits to foreign flowers, simply because pollen sheds or is groomed from pollinator's bodies at some background rate over time. This suggests that any angiosperms that share pollinators face pervasive selection through male fitness to diverge in floral traits, alleviating competition by attracting different pollinators, altering floral phenology or encouraging floral constancy.

Abstract: Specialization in pollination systems has been a central process in the evolution and d... more Abstract: 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 ...

The American Naturalist, Jan 1, 2010

One floral characteristic associated with bat pollination (chiropterophily) is copious pollen pro... more 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.

Biotropica, Jan 1, 2008

What causes flowers to diverge? While a plant's primary pollinator should strongly influence flor... more What causes flowers to diverge? While a plant's primary pollinator should strongly influence floral phenotype, selective pressures may also be exerted by other flower visitors or competition with other plants for pollination. Species of the primarily bat-pollinated genus Burmeistera (Campanulaceae) frequently cooccur, with up to four species in a given site, and broadly overlap in flowering phenology, typically flowering throughout the year. The genus displays extensive interspecific variation in floral morphology in the degree that the reproductive parts (anthers and stigma) are exserted outside of the corolla, and species can be roughly classified as either long or short-exserted. I tested two hypotheses regarding the functional significance of such variation: (1) exsertion lengths correspond to pollination by bat species of different sizes; and (2) variation serves to partition pollinator's bodies spatially and thus reduces interspecific pollen transfer. I captured bats in Ecuador to evaluate the identity and location of the Burmeistera pollen they were carrying. Results show that exsertion does not correspond to specialization on different pollinators; different bat species carried pollen of both flower types just as frequently. In support of the second hypothesis, pollen from flowers of different exsertion lengths was found to occur on different regions of bats' heads. This may serve to reduce competition for pollination among coexisting Burmeistera.

The American Naturalist, Jan 1, 2010

Specialization in pollination systems played a central role in angiosperm diversification, yet th... more 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.

Novon

Burmeistera auriculata is described from a cloud forest remnant in Pichincha, Ecuador. Although a... more Burmeistera auriculata is described from a cloud forest remnant in Pichincha, Ecuador. Although allied to B. borjensis, this new species is distinguished from all known congeners by its auriculate calyx.

Annals of Botany, Jan 1, 2009

A number of different types of flower-visiting animals coexist in any given habitat. What evoluti... more 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. † Methods 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. † Key Results 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. † Conclusions 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.

PLOS ONE, 2015

Given their small size and high metabolism, nectar bats need to be able to quickly locate flowers... more 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.

Molecular phylogenetics and evolution, Jan 21, 2016

The field of molecular systematics has benefited greatly with the advent of high-throughput seque... more The field of molecular systematics has benefited greatly with the advent of high-throughput sequencing (HTS), making large genomic datasets commonplace. However, a large number of targeted Sanger sequences produced by many studies over the last two decades are publicly available and should not be overlooked. In this study, we elucidate the phylogenetic relationships of the plant genus Burmeistera (Campanulaceae: Lobelioideae), while investigating how to best combine targeted Sanger loci with HTS data. We sequence, annotate, and analyze complete to nearly complete plastomes for a subset of the genus. We then combine these data with a much larger taxonomic dataset for which only Sanger sequences are available, making this the most comprehensively sampled study in the genus to date. We show that using a phylogeny inferred from the species with plastome data as a topological constraint for the larger dataset increases the resolution of our data and produces a more robust evolutionary hy...

Examining dispersal is critical for understanding the diversity of Andean-centered plant lineages... more Examining dispersal is critical for understanding the diversity of Andean-centered plant lineages, like Burmeistera (Campanulaceae). One-third of its species present an unusual inflated berry. Unlike the bright colors of non-inflated fruits in the genus, these fruits are typically dull-green; however, the fact that the seeds are loosely held in the placenta and easily removed when touched seems to suggest adaptation to animal dispersal. We studied two inflated-baccate species, Burmeistera glabrata and B. borjensis, with the aim of testing the non-exclusive hypotheses that their seeds are dispersed by (1) small mammals, (2) slugs, or (3) adult flies that develop inside the fruits. In two sites in the Ecuadorian Andes, we performed observations at dusk and dawn to examine the fate of fruits and seeds; recording fruit fall, formation of holes in the fruits, and seed loss from the placenta. We documented fruit visitors with cameras, and surveyed unopened fruits for the presence of insect larvae and seed condition. Finally, we performed an experiment to examine the effect of holes and rain in germination, in order to evaluate if holes are required for seeds to leave the fruits and subsequently germinate. For both species, most fruits fell and decomposed beneath the mother plant. However, we found limited support for small mammal dispersal; videos and observations revealed that mice and squirrels are potential, but rare, seed dispersers. We found no evidence for slug or fly dispersal; fly larvae were common inside fruits, but acted exclusively as seed predators. Crickets often chewed holes in fruits on plants and on the ground. Holes did not have an effect on germination, which was induced only by rain. Hence, the majority of seeds end up under the mother plant, with rare but potentially important events of primary or secondary dispersal by small mammals. The combination of limited dispersal due to gravity and rare events of mammal dispersal may have played a critical role in the rapid diversification of Burmeistera.

Novon: A Journal for Botanical Nomenclature, 2015

Evolutionary Ecology, 2015

Darwin hypothesized that extremely long flowers and the long mouthparts of the animals that polli... more Darwin hypothesized that extremely long flowers and the long mouthparts of the animals that pollinate them evolved together in a coevolutionary race. While selective pressures for the animal side of such a race are relatively clear (longer tongues allow the animal to reach more ...

American journal of botany, 2014

Evolution, 2014

One classic explanation for the remarkable diversity of flower colors across angiosperms involves... more One classic explanation for the remarkable diversity of flower colors across angiosperms involves evolutionary shifts among different types of pollinators with different color preferences. However, the pollinator shift model fails to account for the many examples of color variation within clades that share the same pollination system. An alternate explanation is the competition model, which suggests that color divergence evolves in response to interspecific competition for pollinators, as a means to decrease interspecific pollinator movements. This model predicts color overdispersion within communities relative to null assemblages. Here, we combine morphometric analyses, field surveys, and models of pollinator vision with a species-level phylogeny to test the competition model in the primarily hummingbird-pollinated clade Iochrominae (Solanaceae). Results show that flower color as perceived by pollinators is significantly overdispersed within sites. This pattern is not simply due to phylogenetic history: phylogenetic community structure does not deviate from random expectations, and flower color lacks phylogenetic signal. Moreover, taxa that occur in sympatry occupy a significantly larger volume of color space than those in allopatry, supporting the hypothesis that competition in sympatry drove the evolution of novel colors. We suggest that competition among close relatives may commonly underlie floral divergence, especially in species-rich habitats where congeners frequently co-occur.

Functional Ecology, Jan 1, 2012

1. Although competition for pollination is often invoked as a driver of broad-scale evolutionary ... more 1. Although competition for pollination is often invoked as a driver of broad-scale evolutionary and ecological patterns, we still lack a clear understanding of the mechanics of such competition. When flower visitors alternate between two species of flower, heterospecific pollen transfer takes place. The impact of these mixed loads on the female reproductive success of a recipient has received considerable attention, but the concomitant loss of male reproductive success -because of pollens grains being lost to foreign stigmas -has received less. Furthermore, pollen losses are not limited to grains that land on stigmas, but can also include deposition on non-stigmatic surfaces of the intervening flowers, or loss from the animal's body through passive detachment or active grooming. We collectively term these losses because of competition 'pollen misplacement'. 2. Here, we quantify pollen transferred by nectar bats between focal flowers (Aphelandra acanthus) with and without intervening visits to one of two competitor species. One competitor (Centropogon nigricans) places its pollen in the same region of bats' heads as the focal species, while the other (Burmeistera sodiroana) places its pollen farther forward. 3. We found that (i) any intervening visit caused some reduction in the number of pollen grains transferred, (ii) competitor flowers with similar pollen-placement locations caused greater reductions in pollen transfer and (iii) of these competitors, those in male phase (dispensing pollen) caused greater pollen loss than those in female phase (without pollen). 4. This study provides rare empirical support for the detrimental effects of competition for pollination on male fitness via pollen misplacement and is the first to show an added cost imposed by male-phase competitors. Although this competition is especially strong when competitors overlap in pollen placement, diverging in pollen placement will not completely eliminate pollen loss during visits to foreign flowers, simply because pollen sheds or is groomed from pollinator's bodies at some background rate over time. This suggests that any angiosperms that share pollinators face pervasive selection through male fitness to diverge in floral traits, alleviating competition by attracting different pollinators, altering floral phenology or encouraging floral constancy.

Abstract: Specialization in pollination systems has been a central process in the evolution and d... more Abstract: 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 ...

The American Naturalist, Jan 1, 2010

One floral characteristic associated with bat pollination (chiropterophily) is copious pollen pro... more 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.

Biotropica, Jan 1, 2008

What causes flowers to diverge? While a plant's primary pollinator should strongly influence flor... more What causes flowers to diverge? While a plant's primary pollinator should strongly influence floral phenotype, selective pressures may also be exerted by other flower visitors or competition with other plants for pollination. Species of the primarily bat-pollinated genus Burmeistera (Campanulaceae) frequently cooccur, with up to four species in a given site, and broadly overlap in flowering phenology, typically flowering throughout the year. The genus displays extensive interspecific variation in floral morphology in the degree that the reproductive parts (anthers and stigma) are exserted outside of the corolla, and species can be roughly classified as either long or short-exserted. I tested two hypotheses regarding the functional significance of such variation: (1) exsertion lengths correspond to pollination by bat species of different sizes; and (2) variation serves to partition pollinator's bodies spatially and thus reduces interspecific pollen transfer. I captured bats in Ecuador to evaluate the identity and location of the Burmeistera pollen they were carrying. Results show that exsertion does not correspond to specialization on different pollinators; different bat species carried pollen of both flower types just as frequently. In support of the second hypothesis, pollen from flowers of different exsertion lengths was found to occur on different regions of bats' heads. This may serve to reduce competition for pollination among coexisting Burmeistera.

The American Naturalist, Jan 1, 2010

Specialization in pollination systems played a central role in angiosperm diversification, yet th... more 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.

Novon

Burmeistera auriculata is described from a cloud forest remnant in Pichincha, Ecuador. Although a... more Burmeistera auriculata is described from a cloud forest remnant in Pichincha, Ecuador. Although allied to B. borjensis, this new species is distinguished from all known congeners by its auriculate calyx.

Annals of Botany, Jan 1, 2009

A number of different types of flower-visiting animals coexist in any given habitat. What evoluti... more 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. † Methods 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. † Key Results 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. † Conclusions 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.