Plant–Pollinator Interactions: From Specialization to Generalization. Nickolas M. Waser and Jeff Ollerton, eds. University of Chicago Press, Chicago, 2006. 445 pp. $45.00 (ISBN 0226874001 paper).
Ecologists no longer expect that field studies of mutualisms will commonly reveal obligate coevolved dependencies between particular plant and pollinator species. Figs and fig wasps still stand as the best suite of examples of one-to-one co-evolution of flowering plants and pollinators, but they are exceptions to the rule that few plant species depend entirely on a single pollinator species, and few species of pollinators depend entirely on a single plant species. The reality of specialization and generalization is vastly more complex. The reasons for real differences in pollinator and plant dependencies—and their consequences for understanding, conserving, managing, and using pollination systems in nature and in agriculture—are far too important to the ecology of populations and communities to relegate to tidy, oversimplified natural history lore.
Plant–Pollinator Interactions, edited by Nickolas Waser and Jeff Ollerton, is a masterful overview of a rich field in a stage of dynamic ferment. Thirty-eight contributing authors offer 18 chapters of experiences and perspectives ranging from those of new investigators to those of established scientists.
Waser's introduction (part 1) provides historical context. Although Sprengel (1793) expressed “certainty” that many plants are pollinated by single agents, Waser points out that specialization and generalization do not reflect dichotomies in nature, but instead a continuum of degrees to which particular taxa or functional groups of pollinators use and are used by particular taxa or functional groups of plants. Waser leaves it to his authors to define dependencies and asymmetries in different pollination systems and ecological communities. This historical overview frames, and promises to extend beyond the framework, the contemporary controversy about the degree to which pollination “syndromes”—defined by Stefan Vogel and others as suites of flower traits of color, shape, scent, nectar composition, and pollen rewards—reflect adaptation to and use by identifiable groups of pollinators. If specialization and generalization continue to be redefined by successive authors in this volume, this ambiguity reflects the field.
Part 2 (“Ecology and Evolution of Specialized and Generalized Pollination”) explores how use and selection by pollinators or plants influence the evolution of pollination mutualisms. José Gómez and Regino Zamora give a theoretical overview of ecological factors that promote
Do the trade-offs assumed by most discussions of specialization and generalization exist? Are some generalist pollinators or flowers disadvantaged by being jacks-of-all-trades and masters of none?
specialization and generalization in pollination. In the spirit of G. Ledyard Stebbins, they argue that pollinators that enhance plant fitness are selective agents, and that the more distinct different pollinators are in providing those fitness benefits for plants, the more likely it is that consistent use by those pollinators will promote specialization by plants. When different pollinators provide distinctive selective benefits for plants experiencing serious herbivory, the plants evolve complex life cycles that allow them to make generalized use of this array of pollinators. Gómez and Zamora distinguish this from adaptive generalization that occurs when effective pollinators vary in number or attention in space and time (e.g., the classic Calathea case; Horvitz and Schemske 1990). Nonadaptive generalization, in contrast, occurs when different taxa of pollinators do not differ in their fitness effects.
Other chapters consistent with the “Stebbins framework” explore selective and ecological effects of different pollinators on plants, or vice versa. Paul Wilson and colleagues discuss repeated shifts from insect to bird pollination among distantly related members of the genus Penstemon. By contrast, Robert Minckley and T'ai Roulston explore in the following chapter the distinction between evolved and incidental specialization of bee pollination of flowers. In rare cases, a single bee taxon has evolved to use a single plant taxon; more commonly, one or more bee taxa by chance use a given plant species at a particular place and time, with the plant adjusting, if at all, to multiple pollinators. Other bees remain unspecialized, using and pollinating a variety of plant taxa. This is a thoughtful exploration of the question posed by Janzen (1980): “When is it coevolution?” James Cane and Sedonia Sipes (chapter 5) are concerned with degrees of consistency in bee use of flower taxa, whether the interaction is evolved or not. Their revised lexicon of degrees of pollen specialization recognizes several levels of oligolecty but excludes nectar collection that occurs without pollen gathering.
Do the trade-offs assumed by most discussions of specialization and generalization exist? Are some generalist pollinators or flowers disadvantaged by being jacks-of-all-trades and masters of none? Paul Aigner (chapter 2) models how specialization might evolve without tradeoffs in “fine-grained” environments in which mutualists depend on far fewer partners than they encounter. Trade-offs have not been addressed carefully in pollination biology; little evidence of reduced fitness from generalization seems to exist. In a clear departure from the Stebbins framework, Aigner suggests that trade-offs are not necessary for specialization. He hypothesizes that pollinators responsible for plant specialization need not be either the most numerous or the most effective ones for a plant if they supply marginal gains or deficits in fitness for the plant, and he offers a fascinating speculation about how to test the idea.
The studies discussed in part 3 leave us free to wonder what quantitative patterns of plant and pollinator association actually exist across communities, regions, and continents. Pedro Jordano and colleagues (chapter 8) probe nested structure in pollination in a wide array of systems, finding that all show a structure characterized by “nodes” of common plants, visited by common and rare pollinators, with the probability of pollinator interaction declining as the number of plants increases. In the same spirit but with different methods, Diego Vázquez and Marcelo Aizen (chapter 9) ask whether the probability of interaction is equal among plant and pollinator species within 18 communities. The answer is a clear no, with frequent asymmetric associations of plants and pollinators. Theodora Petanidou and Simon Potts (chapter 10) compare real and apparent specialization, judged by the number of plant species visited, in Greece, Israel, and Spain. They find that evolved specialization is rare, but that at any place and time, selectivity of insects for plants and vice versa may be quite high. Few extreme generalists are obvious. Using evidence from Greece and Argentina, Diego Medan and colleagues (chapter 11) argue that generalization must be understood through time, offering analyses of pollination systems that are active throughout the year.
Are tropical systems different? Ollerton and colleagues find, not surprisingly, more pollination systems in tropical than in temperate communities, with more diverse floras and faunas and therefore more opportunities for specialization. Within plant groups, it is not clear that greater specialization in pollinator systems exists in the tropics, although the open question of what defines specialization contributes to this continuing ambiguity.
Do pollinators consistently select for reward strategies of plants? Scott Armbruster compares arctic Saxifraga, which exhibits little specialization, with degrees of specialization in species of temperate Collinsia in California, Stylidium in Western Australia, and Dalechampia in the tropics. Repeated evolution of pollen or resin collection in the latter system of neo- and paleotropical vines presents a classic study of selection for specialization reverting in some lineages to generalization.
Part IV examines the relevance of specialization and generalization to agriculture and conservation. Sarah Corbet offers a typology of flower presentation and another of insect use, which together are more operationally useful for agricultural systems than are Vogel's syndromes. Suzanne Koptur has a similarly useful message concerning the endangered plants of vanishing pine rocklands in southern Florida; many endangered species appear to secure adequate pollination because their insect mutualists are maintained by residential gardens. Manja Kwak and Renee Bekker provide a unique contribution by calculating vulnerability indices for plant species used in European community restorations. Ingolf Steffan-Dewenter and colleagues address the effects of habitat fragmentation on bee pollination. These authors explore the consequences of fragmentation for common asymmetrical pollination systems that lie between rare one-to-one mutualisms and rare extreme generalization. Their chapter is especially interesting in pointing out that effects of fragmentation consist of much more than increased pollen limitation.
Ollerton (last chapter, part 5) closes with what may prove to be a seminal synthesis. Interactions between organisms are usually modeled as means of optimizing currencies of energy or nutrients. Ollerton promotes the idea of a “biological barter” economy, in which rewards may be exchanged for services that are sometimes reasonably modeled by energy optimization (nectar as food for bees), but in many cases not (resin for bee nest construction, flower fragrances for bee courtship). Ollerton is out of step with the parade here, but in my view the parade has been going in the wrong direction for some time. His chapter develops the idea that specialization occurs when exclusive mutualisms become “intimate through trophic, physiological, and/or physical integration.”
This collection of essays is stimulating, but will not suit all needs. The antagonistic roots of pollination mutualisms are apparent in Susanne Renner's comprehensive discussion of the pollination of flowers that offer no rewards—the ultimate plant “cheaters.” The collection would have profited from a theoretical discussion of the evolution of mutualism from antagonism (e.g., Bronstein 2001). Moreover, the phenomena examined are mostly temperate and might not be good models for tropical forests, where flower displays are often huge and high above the ground, and could conceivably attract thousands of pollinators—or very few.
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. My guess is that a volume of similar depth and reach with a tropical slant will change the debate again.