Plant-Pollinator Interactions: From Specialization to Generalization


Just as flowering plants depend on their pollinators, many birds, insects, and bats rely on plants for energy and nutrients. This plant-pollinator relationship is essential to the survival of natural and agricultural ecosystems. Plant-Pollinator Interactions portrays the intimate relationships of pollination over time and space and reveals patterns of interactions from individual to community levels, showing how these patterns change at different spatial and temporal scales.


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Just as flowering plants depend on their pollinators, many birds, insects, and bats rely on plants for energy and nutrients. This plant-pollinator relationship is essential to the survival of natural and agricultural ecosystems. Plant-Pollinator Interactions portrays the intimate relationships of pollination over time and space and reveals patterns of interactions from individual to community levels, showing how these patterns change at different spatial and temporal scales.

Nickolas M. Waser and Jeff Ollerton bring together experts from around the world to offer a comprehensive analysis of pollination, including the history of thinking about specialization and generalization and a comparison of pollination to other mutualisms. An overview of current thinking and of future research priorities, Plant-Pollinator Interactions covers an important theme in evolutionary ecology with far-reaching applications in conservation and agriculture. This book will find an eager audience in specialists studying pollination and other mutualisms, as well as with biologists who are interested in ecological, evolutionary, and behavioral aspects of the specialization and generalization of species.

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Editorial Reviews

Judith Bronstein

PlantPollinator Interactions is a multifaceted exploration of the specialization–generalization continuum in pollination; however, it goes well beyond pollination to draw novel connections with other interspecific interactions. Conceptually framed, highly synthetic, and up-to-date, this impressive edited volume should appeal to a broad cross-section of ecologists and evolutionary biologists.”—Judith Bronstein, University of Arizona
Jacqui Shykoff

“This is an excellent book that masterfully covers the field of pollination biology at different scales, from populations through communities to landscapes, and from both basic and applied viewpoints. It represents a balanced mix of largely conceptual and empirical chapters. Empirical work employs the three mainstays of ecological research— careful observation, planned experimentation, and comparative analysis with phylogenetic control. This book would be an ideal starting point for students interested in studying plant–pollinator interactions but also, more broadly, for anyone interested in interspecific interactions and coevolution.”—Jacqui Shykoff, Laboratoire d'Ecologie, Systématique et Evolution, CNRS-Université Paris-Sud
Trends in Ecology and Evolution - Shuang-Quan Huang

"In Plant–Pollinator Interactions, Waser and Ollerton bring together experts from different regions of the world to address how patterns of specialization and generalization in pollination systems vary across spatial and temporal scales. . . . An important contribution to our understanding of plant–pollinator interactions. . . . By reading this book . . . one will conclude that pollination biology is undergoing a renaissance that will ultimately provide us with a deeper understanding of the evolutionary and ecological processes involved in this fascinating interaction."
Ecology & Evolution - Ethology

"Plant-Pollinator Interactions covers an important theme in evolutionary ecology with far-reaching applications in conservation and agriculture. This book will find an eager audience in specialists studying pollination and other mutualisms, as well as with biologists who are interested in ecological, evolutionary, and behavioral aspects of the specialization and generalization of species."
BioScience - Henry F. Howe

"A masterful overview of a rich field in a stage of dynamic ferment....Plant-Pollinator Interactions will define much of the debate on the central issue of specialization and generalization in pollination biology. I recommend it to all students of pollination, as well as to those interested in broader issues of plant and animal interactions."
Annals of Botany - Peter Klinkhamer

"The book will not only prove to be a handy reference but it will also prove to stimulate new research by showing how recently developed tools . . . have enabled researchers to address questions that for a long time have been inaccessible."
Basic and Applied Ecology - Markus Fischer

"Pollination biology at its best!...This book is a must-read for pollination biologists, and for those interested in evolutionary ecology, biological interactions, and co-evolution."

Ecoscience - Rebecca E. Irwin

"A timely piece, providing a comprehensive view of our current understanding of multispecies plant-pollinator interactions. The chapters are well referenced and well written, making for an informative text for graduate students as well as researchers."
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Product Details

  • ISBN-13: 9780226874005
  • Publisher: University of Chicago Press
  • Publication date: 1/15/2006
  • Pages: 488
  • Product dimensions: 6.00 (w) x 9.00 (h) x 1.10 (d)

Meet the Author

Nickolas M. Waser is professor emeritus of biology at the University of California, Riverside, and adjunct professor at the School of Natural Resources at the University of Arizona. Jeff Ollerton is senior lecturer in ecology at the School of Applied Sciences at University College Northampton.
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Plant-Pollinator Interactions
From Specialization to Generalization
The University of Chicago Press
Copyright © 2006
The University of Chicago
All right reserved.

ISBN: 978-0-226-87400-5

Chapter One Specialization and Generalization in Plant-Pollinator Interactions: A Historical Perspective

Nickolas M. Waser

und bey den Pflanzen, bey denen ihre allzu nahe Nachbarschaft, der Wind und Insekten zu einer widernatürlichen Vermischung täglich Gelegenheit geben.

(and with the plants, whose all too close proximity gives daily opportunity to wind and insects for an unnatural mixing.) -Kölreuter (1761)

[Ein System] müste auch die Beziehung zu den Bestäubern berücksichtigen, wenn es den Kern der Blütenbiologie überhaupt treffen soll.

([A system] also ought to consider the relationship to the pollinators, if it is at all to get at the essence of floral biology.) -Vogel (1954)

The angiosperms, or flowering plants, comprise about one-sixth of all described species, and the insects almost two-thirds (Wilson 1992). These speciose groups thereby dominate the flora and fauna of Earth's land surface, and interactions between them are dominant elements of terrestrial ecosystems. The most obvious of these interactions is that between flowering plants and insect herbivores, an elaborate evolutionary arms race which fosters remarkable adaptations in both adversaries (Labandeira et al. 1994; Schultz 2002). Almost as obvious is the interaction between flowering plants and the insects that visit and pollinate their flowers.

Not all insects are pollinators, nor pollinators insects. Most pollinators are drawn from the insect orders Hymenoptera, Diptera, Lepidoptera, and Coleoptera, and these animals are joined by some species from other insect orders and from the vertebrates, in particular some birds and bats (Proctor et al. 1996). The majority of angiosperms (by some estimates the great majority; Nabhan and Buchmann 1997; Renner 1998) rely in whole or part on such animals for pollination, rather than on abiotic agents such as wind or water. Hence, biotic pollination links some quarter-million angiosperm species with a similar number of insect and other animal species. From this emerges another quantitative conclusion: that pollination by animals constitutes a dominant, largely (but not entirely; Renner, chap. 6 in this volume) mutualistic ecological interaction of terrestrial habitats, perhaps, joining the mycorrhizal mutualism between plants and fungi in its ubiquity.

Those pollination interactions that truly are mutualistic are beneficial to plants and animals, but this does not imply cooperation (Waser and Price 1983; Howe 1984; Westerkamp 1997). The mutualism also directly benefits humanity through crop productivity, and indirectly, through ecosystem health. Hence, pollination is an important (and gratis) ecosystem "service" (Costanza et al. 1997). As is true for other ecosystem services, pollination by animals is not replaceable to any appreciable degree by technology. Thus, it is of concern that the mutualism is under threat from habitat alteration, invasive species, climate change, and other factors (e.g., Nabhan and Buchmann 1997; Kearns et al. 1998; Kremen et al. 2002; Steffan-Dewenter et al. 2001, chap. 17 in this volume). Although uncertainty surrounds the final effect of these anthropogenic changes on pollination (e.g., Cane and Tepedino 2001), there is enough cause for alarm that conservation biologists-not only "pure" ecologists-seek a deeper understanding of plant-pollinator interactions.

A fundamental aspect of any ecological interaction, including any pollination mutualism, is the degree to which it is specialized or generalized. Specialization and generalization suggest a dichotomy, but this is incorrect and only reflects the limits of language (Waser et al. 1996). In fact, obligate specialization and extreme generalization represent two ends of a continuum in resource use or niche breadth. For plants, the resource is pollination services from one or more species of animals that visit flowers; for animals, it is food or other benefit gained from such visits to one or more species of flowers. For simplicity, this summary leaves aside cases of "cheating" (which in themselves demonstrate that the interaction is not cooperative and sometimes not even mutualistic), as exhibited, for example, by flowers that promise food or sex but provide none (Renner, chap. 6 in this volume) or by visitors that extract nectar from flowers without pollinating (Irwin et al. 2001). In short, a deeper understanding of pollination requires a clearer picture of the range of specialization and generalization of plants and pollinating animals, of temporal and spatial variation in these niche relationships, and of their deeper explanation in terms of factors that constrain and promote the evolution of niche breadth (Waser et al. 1996). This is a large endeavor!

The purpose of this chapter is to provide a brief sketch of this endeavor to date. I have argued that scientists may make indifferent historians of science (Waser 1997); therefore, I approach this task with some trepidation and with the warning that many historical threads will remain unexplored. I will attempt to trace the development of some major ideas about specialization and generalization in pollination interactions based on historical summaries in the literature and my own reading and interpretation of some of the classic works.

The Past

Kölreuter and Sprengel

Joseph Gottlieb Kölreuter (1733-1806) is largely responsible for inaugurating the scientific-including experimental-study of pollination by animals. While at the University of Tübingen, Kölreuter was exposed to the ideas of J. G. Gmelin on the possibility of hybridization of species and to the earlier work of R. J. Camerarius showing that plants reproduce sexually (Mayr 1986). This exposure led to Kölreuter's own work on plant sexuality, the most important of which was described in a "preliminary" report (Vorläufige Nachricht) in 1761 and in sequels appearing in 1763, 1764, and 1766. These reports are written in a fashion quite different from modern scientific writing: they explore pollination (including self-pollination, wind pollination, and pollination by insects), sexual characteristics of flowers, and hybridization of species in an almost stream-of-consciousness manner, with few landmarks to guide the reader. The result is that important insights often must be extracted from a welter of details, and a given topic repeatedly disappears and later reappears. The analysis by Mayr (1986) of parts of Kölreuter's Voläufige Nachricht is a valuable aid in reconstructing its major themes.

For the present purpose, what interests us most is the recognition of animals as pollinators (fig. 1.1). Earlier workers had hinted at this interaction, but Kölreuter was the first to fully recognize it. He observed that many of the insects seen flying around flowers are carriers of pollen, which adheres to their bodies and is transferred to stigmas as a fortuitous by-product of the animals' activities in extracting sweet droplets of nectar for their own nourishment. To support the premise that these activities cause pollination, Kölreuter turned to experiments in which he added pollen to stigmas by hand, and characterized the relationship between number of pollen grains and production of fruits and seeds, as well as experiments in which he excluded insects from flowers, showing that this caused failure of fruit production. These studies involved common plants of a northern European garden-in particular, cucurbits, irises, and mallows, but also snapdragons, elderberries, and others-and common visitors such as bumblebees, wasps, flies, and thrips. Kölreuter (1761, 36) ventured to extend his results from this context to flowering plants in general, concluding that "[insects] probably provide this uncommonly great service, if not to most plants, then at least to a very large portion of them" (und wahrscheinlich leisten [Insekten], wo nicht den allermeisten Pflanzen, doch wenigstens einem sehr grosen Theil derselben, diesen ungemein grosen Dienst). This conclusion seems prophetic in light of recent estimates that 90% or more of angiosperm species benefit from animal pollination (e.g., Renner 1998).

Kölreuter's painstaking observations in nature, including entire days spent watching single plants, gave him a remarkable insight into the use of insects by flowers and flowers by insects. In most cases, he described multiple types of insects visiting a given plant species and, although this was not explicitly discussed, the impression is that some of the insects were observed visiting several plant species. As the quotation at the beginning of this chapter suggests, Kölreuter recognized that such generalized niche relationships set the stage for hybridization between related plant species, a possibility of interest (and which he described as "unnatural") given his assumption that species were fixed entities with absolute barriers between them. Kölreuter's subsequent experimental crosses demonstrated to his surprise that hybridization, indeed, could occur.

Kölreuter (1761, 23) described his discoveries of plant-pollinator interaction as "secrets of nature" (Geheimnisse der Natur), a term that reappears in the title of Christian Konrad Sprengel's 1793 book on the structure and fertilization of flowers. This classic work describes in detail features of flowers and their functions, which are taken as evidence for intentional design for pollination by insects or wind. In introducing the thesis of intricate and beautiful design for pollination, Sprengel summarizes numerous patterns and deductions which are foundational to subsequent studies of pollination, such as the structure and function of nectaries (nectar-secreting tissues), the function of flower colors (including "nectar guides"; areas of contrasting color assumed to guide visitors to rewards) and odors, the existence of deceit flowers and of insects that rob for nectar, and many other themes (Vogel 1996). Sprengel (1793, 17) mentions Kölreuter's earlier recognition of dichogamy (different timing of the maturation of anthers and stigma within hermaphroditic flowers) and, therefore, had read the work of his predecessor, although there has been some confusion on this point (Faegri and van der Pijl 1966, 2) and some incorrect assignment of precedence of certain contributions (see Vogel 1996).

Sprengel (1793, 19-20) concluded that "It is certain that many flowers are fertilized by multiple species of insects ... It also is certain that many flowers are fertilized solely by one species of insect, and this in a very distinct fashion" (Es ist gewis, dass viele Blumen von mehrern Arten von Insekten befruchtet werden ... Es ist aber auch gewis, das viele Blumen blos von einer Art von Insekten, und zwar auf eine sehr bestimmte Art, befruchtet werden ...) and furthermore (1793, 43) that "in the first case, the fertilization of the ovary and production of fruit must progress more easily" (so mus ... im ersten Fall die Befruchtung des Fruchtknotens und die Erzielung der Frucht leichter vor sich gehen) since there is less danger that pollination will utterly fail. As Vogel (1996) points out, such conclusions are based on comparative studies of several hundred plant species observed in natural or nearly natural conditions, which contrasts with Kölreuter's experimental studies of pollination of a much shorter list of native plant species. There appears to be a trade-off here, however, because Sprengel's individual descriptions of plant species focus far more on floral features than on insect visitors, and the latter (when mentioned at all) sometimes are inferred from the former, all suggesting that Sprengel was unable to spend substantial time observing pollination species by species.

Sprengel's influential work helped to inaugurate two different themes in the study of pollination, both of which have been pursued until the present time. The first is the steady accumulation of empirical information on pollination relationships of individual plant species (and to a lesser extent on floral affinities of individual pollinator species), which at its best combines the comparative scope of Sprengel with the lengthy observations pioneered by Kölreuter of each species. The second theme is the attempt to find order in the diversity of floral phenotypes, ultimately in relationship to the diversity of pollination relationships. Thus, Sprengel categorized the hundreds of flowers he studied into "classes," based on Linné's system of number and arrangement of stamens, combined with reward for pollinators (with or without nectar) and sex expression (hermaphroditic, monoecious, or dioecious). This scheme of classification did not survive, but it does presage later attempts which culminate ultimately in later ideas of the pollination syndromes.

Encyclopedic Observations of Pollination

Charles Darwin was influenced by Sprengel in his studies of plant sexuality, just as he was influenced by Kölreuter in his thoughts on hybridization. Where Sprengel saw intentional design in floral features, Darwin (1859) argued convincingly for adaptation by natural selection and elaborated on Kölreuter's much earlier recognition of the differing interests of plants and pollinators (sexual reproduction vs. food acquisition) that drive the mutualism and explain many of its observable dynamics (e.g., Waser 2000). Except that it is recast as the study of floral adaptation, Darwin's (1862) famous examination of orchid flowers follows in the tradition of Sprengel, even to the extent that description of the pollinators constitutes a minor theme. Although Darwin (1869) later contributed more detailed observations of orchid pollination, and discussion of pollination and pollinator behavior are found in some of his other writings (e.g., Darwin 1876), his main purpose (other than a general argument for adaptation) was to explore the thesis that selection favors cross-fertilization.

Darwin, therefore, placed the scientific study of pollination in its modern evolutionary framework. But, whereas he did contribute to the growing empirical description of who pollinates whom, the major contributions fell to botanist Hermann Müller, a champion of Darwinism in Germany and continental Europe, and to Müller's successor, Paul Knuth. Müller's compendium, published in German in 1873 as Die Befruchtung der Blumen durch Insekten and a decade later in slightly truncated translation as The fertilisation of flowers, brings together lists of pollinators and details of flower and pollinator characteristics for some 400 plant species, and more cursory descriptions for several thousand more, and also presents details of morphology and behavior related to pollination for the major pollinating insect orders. The justification given for this effort was the study of adaptations for cross-pollination, echoing Darwin's (1876) focus. A similar structure is found in Paul Knuth's Handbuch der Blütenbiologie, which provides records of flower visitation and pollination for 4028 European species and 2357 species in other parts of the world. This massive effort was published in German between 1898 and 1905 in three volumes, the last of which appeared after Knuth's death; the first two (but not the third!) were translated as Handbook of flower pollination between 1906 and 1909. (These were published as three volumes; nonetheless, they are missing some 1118 pages of Knuth's original.) Knuth (1898) introduced this work with a valuable historical overview of pollination research to the end of the 19th century, echoing the earlier historical summary of Müller (1883).

Attempts at Floral Classification

Baker (1983) refers to Knuth's Handbook as the "old Testament" of pollination biology, marking the close of an era of enthusiastic accumulation of information on pollination relationships. This accumulation continues, thereafter, at a slower rate up to the present. Over the same period, ideas were also circulating about how one might bring order to the welter of detail on who pollinates whom, by finding some natural scheme for classifying flowers.

As noted earlier, the scheme used by Sprengel (1793) did not persist, presumably because classification of flowers based on number of pistils and nectar reward is not particularly natural or useful. The efforts of Italian botanist Federico Delpino (1868-1875) were much more influential. As had his contemporaries, Delpino contributed to detailed records of pollination, including pollination by birds. But his more lasting contribution was in proposing not one, but two general schemes for the classification of flowers, with the explicit purpose of finding natural groupings (Vogel 1954).


Excerpted from Plant-Pollinator Interactions Copyright © 2006 by The University of Chicago. Excerpted by permission.
All rights reserved. No part of this excerpt may be reproduced or reprinted without permission in writing from the publisher.
Excerpts are provided by Dial-A-Book Inc. solely for the personal use of visitors to this web site.
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Table of Contents

Preface Part I. Introduction and History
1          Specialization and Generalization in Plant–Pollinator Interactions: A Historical Perspective / Nickolas M. Waser
Part II. The Ecology and Evolution of Specialized and Generalized Pollination / Introductory comments by Jeff Ollerton, W. Scott Armbruster, and Diego P. Vázquez
2          The Evolution of Specialized Floral Phenotypes in a Fine-grained Pollination Environment / Paul A. Aigner
3          Shifts between Bee and Bird Pollination in Penstemons / Paul Wilson, Maria Clara Castellanos, Andrea D. Wolfe, and James D. Thomson
4          Incidental Mutualisms and Pollen Specialization among Bees / Robert L. Minckley and T'ai H. Roulston
5          Characterizing Floral Specialization by Bees: Analytical Methods and a Revised Lexicon for Oligolecty / James H. Cane and Sedonia Sipes
6          Rewardless Flowers in the Angiosperms and the Role of Insect Cognition in Their Evolution / Susanne S. Renner
7          Ecological Factors That Promote the Evolution of Generalization in Pollination Systems / José M. Gómez and Regino Zamora
Part III. Community and Biogeographic Perspectives / Introductory comments by Nickolas M. Waser and Jeff Ollerton
8          The Ecological Consequences of Complex Topology and Nested Structure in Pollination Webs / Pedro Jordano, Jordi Bascompte, and Jens M. Olesen
9          Community-wide Patterns of Specialization in Plant–Pollinator Interactions Revealed by Null Models / Diego P. Vázquez and Marcelo A. Aizen
10        Mutual Use of Resources in Mediterranean Plant–Pollinator Communities: How Specialized Are Pollination Webs? / Theodora Petanidou and Simon G. Potts
11        Measuring Generalization and Connectance in Temperate, Year-long Active Systems / Diego Medan, Alicia M. Basilio, Mariano Devoto, Norberto J. Bartoloni, Juan P. Torretta, and Theodora Petanidou
12        Evolutionary and Ecological Aspects of Specialized Pollination: Views from the Arctic to the Tropics / W. Scott Armbruster
13        Geographical Variation in Diversity and Specificity of Pollination Systems / Jeff Ollerton, Steven D. Johnson, and Andrew B. Hingston
Part IV. Applications in Agriculture and Conservation / Introductory comments by Nickolas M. Waser and Margaret M. Mayfield
14        A Typology of Pollination Systems: Implications for Crop Management and the Conservation of Wild Plants / Sarah A. Corbet
15        The Conservation of Specialized and Generalized Pollination Systems in Subtropical Ecosystems: A Case Study / Suzanne Koptur
16        Ecology of Plant Reproduction: Extinction Risks and Restoration Perspectives of Rare Plant Species / Manja M. Kwak and Renée M. Bekker
17        Bee Diversity and Plant–Pollinator Interactions in Fragmented Landscapes / Ingolf Steffan-Dewenter, Alexandra-Maria Klein, Volker Gaebele, Thomas Alfert, and Teja Tscharntke
Part V. Final Considerations: Pollination Compared to Other Interactions
18        "Biological Barter": Patterns of Specialization Compared across Different Mutualisms / Jeff Ollerton
List of Contributors


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