The Ecology and Evolution of Ant-Plant Interactions

by Victor Rico-Gray and Paulo S. Oliveira

University of Chicago Press, 2007
Cloth: 978-0-226-71347-2 | Paper: 978-0-226-71348-9 | Electronic: 978-0-226-71354-0
DOI: 10.7208/chicago/9780226713540.001.0001

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ABOUT THIS BOOKAUTHOR BIOGRAPHYREVIEWSTABLE OF CONTENTS

ABOUT THIS BOOK

Ants are probably the most dominant insect group on Earth, representing ten to fifteen percent of animal biomass in terrestrial ecosystems. Flowering plants, meanwhile, owe their evolutionary success to an array of interspecific interactions—such as pollination, seed dispersal, and herbivory—that have helped to shape their great diversity. The Ecology and Evolution of Ant-Plant Interactions brings together findings from the scientific literature on the coevolution of ants and plants to provide a better understanding of the unparalleled success of these two remarkable groups, of interspecific interactions in general, and ultimately of terrestrial biological communities.

The Ecology and Evolution of Ant-Plant Interactions synthesizes the dynamics of ant-plant interactions, including the sources of variation in their outcomes. Victor Rico-Gray and Paulo S. Oliveira capture both the emerging appreciation of the importance of these interactions within ecosystems and the developing approaches that place studies of these interactions into a broader ecological and evolutionary context. The collaboration of two internationally renowned scientists, The Ecology and Evolution of Ant-Plant Interactions will become a standard reference for understanding the complex interactions between these two taxa.

AUTHOR BIOGRAPHY

Victor Rico-Gray is a research scientist of ecology and Chairman of the Applied Ecology Department at the Instituto de Ecologia, A. C. in Xalapa, Veracruz, Mexico. Paulo S. Oliveira is professor of ecology at the Universidade Estadual de Campinas, São Paulo, Brazil.

REVIEWS

“I have been waiting for somebody to write this book! It’s a remarkable synthesis of deep and wide-ranging conceptual issues, a feast of natural history, and an up-to-date summary of the field. Given that plants feed the world and ants eat it, churn it, and direct traffic, it is no wonder than ant-plant interactions are so pervasive. Rico-Gray and Oliveira have succeeded in producing a book that will drive the field for at least a decade, and one that will have far-reaching impacts on anybody interested in the nature of how species interact.”

— Anurag Agrawal, Cornell University

“Victor Rico-Gray and Paulo Oliveira, both foremost researchers exploring the enormously diverse ant-plant associations, have written an impressive, authoritative monograph on this subject. This is an important book; it provides a timely critical account of a fundamental body of work. The overarching theme is of great interest to ecologists in general and in particular to social insect biologists.”

— Bert Hoelldobler, Arizona State University

“A reader can sense the authors’ delight and fascination with the subject on every page of The Ecology and Evolution of Ant-Plant Interactions. The breadth and depth of Rico-Gray and Oliveira’s experience and understanding, and the enthusiasm with which these are transmitted to paper, is inspirational. Clearly and authoritatively written, rich with citations, and comprehensive, the book will remain an essential reference for decades.”

— Peter W. Price, Regents’ Professor Emeritus, Northern Arizona University

"The ecology and evolution of ant–plant interactions is an essential book for anyone who currently studies ant–plant interactions. It will also serve as required reading for graduate students who are beginning work on topics in this field. More generally, it should appeal to anyone with an interest in the ecology and evolution of mutualism."

— John Mull, Ecology

"[This book] will be appreciated not only by professional myrmecologists but also by other entomologists and ecologists in general, students, and all trying to understand the amazing natural processes related to this group of social insects."

— M. Suvak, Thaiszia Journal of Botany

"This book is a must-read for ant-plant researchers, and should be assigned reading for graduate students on plant-anmial interactions. It is the most current and thorough treatment of ant-plant interactions to come along in over a decade."

— Megan E. Frederickson, Ecoscience

"An essential compendium of information for anyone in the field of ants, plants, and their interactions. Moreover, it places ant-plant interactions in the larger context of the geographic mosaic of coevolution, and broader ecological theory, and will be a useful text for ecologists generally. Rico-Gray and Oliveira have produced a thorough and well-timed synthesis of an incredibly diverse field."

— Kirsten L. Abbott, Integrative and Comparative Biology

"An authoritative and well-rounded book. It ranges widely over the subject and has a nice historical view, as well as being up-to-date, so that everyone can learn from it. . . . It is worth buying."

— Mark Young, Bulletin of the British Ecological Society

"The broad synthesis and overview that Rico-Gray and Oliveira have provided on this hugely diverse subject, coupled with the comprehensiveness of their literature review, place this book firmly in the 'must-have' category for anyone interested in ants and plants and of great interest for ecologists interested more generally in the ecology and evolution of interspecific interactions."

— Duncan Mackay, Austral Ecology

Preface

Ant-Plant Interactions - Victor Rico-Gray, Paulo S. Oliveira
DOI: 10.7208/chicago/9780226713540.003.0001
[ants, plants, ant–plant interactions, evolution, coevolution, phylogenetic associations, interspecific interactions]
Ants (Hymenoptera: Formicidae) are probably the most dominant insect group on earth, both ecologically and numerically. They are so abundant that approximately 8 million individuals live underground in one hectare of Amazonian rain forest, and ants are estimated to represent 10–15 percent of the entire animal biomass in many terrestrial ecosystems. On this basis alone, the study of the ecology and evolution of ants would be important for understanding the ecology of terrestrial biological communities. Angiosperms make up much of the visible world of modern plants, and the study of their evolution and ecology, like that of ants, is important to understanding the ecology of terrestrial biological communities. This chapter explores the origin and early evolution of ant–plant interactions, describes possible phylogenetic associations between the groups, presents some of the current evidence on the latter, and discusses some general ideas on coevolution and interspecific interactions, specifically related to ant–plant interactions. (pages 1 - 20)
This chapter is available at:
https://academic.oup.com/chica...

Antagonistic Interactions: Leaf-Cutting and Seed-Harvesting Ants - Victor Rico-Gray, Paulo S. Oliveira
DOI: 10.7208/chicago/9780226713540.003.0002
[leaf-cutting ants, grazing, seed-harvesting ants, antagonistic interactions, parasitism, predation, competition, plant communities, seed dispersal]
In antagonistic interactions, the fitness of individuals of one of the interacting species increases, while that of individuals of other interacting species decreases as a result of the interaction. Basically, antagonistic interactions occur between species because living organisms are concentrated packages of energy and nutrients (trophic interactions) and because resources are limited (competition). Antagonistic interactions can be divided into four basic types: parasitism, grazing, predation, and competition. Ants and plants are associated basically in two categories of antagonistic interaction: grazing (leaf-cutting ants) and predation (seed-harvesting ants). Due to the large numbers of seeds removed by ants and the often intense interspecific competition for seeds among ants, granivory and seed harvesting have been considered to be important interactions structuring plant communities. The relationship between antagonism (seed predation) and mutualism (seed dispersal) may be based on the availability of unspecialized seed-collecting ants that contribute to the prevalence of myrmecochory. This chapter reviews leaf-cutter and seed-harvesting ant systems, focusing on the interactions and their effects on the plant community. (pages 21 - 41)
This chapter is available at:
https://academic.oup.com/chica...

Mutualism from Antagonism: Ants as Primary Seed-Dispersers - Victor Rico-Gray, Paulo S. Oliveira
DOI: 10.7208/chicago/9780226713540.003.0003
[elaiosomes, seed dispersal, ants, myrmecochory, mutualism, antagonism, plants]
Interspecific interactions are based on an entirely selfish cost–benefit system, which depends on the relative gain as compared to loss in fitness produced by the interaction. Antagonistic and mutualistic interactions are related in many ways. Over evolutionary time, certain antagonistic interactions can exhibit a shift in outcome so that the interacting species benefit from the interaction. A change in outcome from antagonism to mutualism is most likely in interactions that are inevitable within the lifetimes of individuals and may have their evolutionary origin in the defense reactions of species. Ants and plants are involved in seed and fruit dispersal as well as pollination. This chapter describes the general characteristics of the reward offered by the plants to the ants (elaiosomes). It offers some general concepts on the selective advantage to plants of seed dispersal by ants that have been associated with a variety of major benefits or hypotheses, followed by examples provided by research done in different regions of the world. The chapter also examines the distribution and significance of myrmecochory worldwide. (pages 42 - 67)
This chapter is available at:
https://academic.oup.com/chica...

Mutualism from Opportunism: Ants as Secondary Seed-Dispersers - Victor Rico-Gray, Paulo S. Oliveira
DOI: 10.7208/chicago/9780226713540.003.0004
[diaspores, ants, plants, seed dispersal, myrmecochory]
Studies on seed dispersal of tropical species have traditionally focused on fruit consumption and seed deposition patterns created by primary seed dispersers. More recently, however, the relevance of postdispersal events for seed fate and demography of plant species has been repeatedly emphasized for a number of dispersal systems. Indeed, recent studies have demonstrated that postdispersal events, some of them involving ants as seed vectors, can markedly affect seed fate in numerous plant species from different regions. Although myrmecochory can be an important dispersal strategy for some plant taxa in neotropical forests, typical myrmecochores are especially common in arid Australia and South Africa, and in Mediterranean and temperate areas. This chapter summarizes recent findings showing that the use of fallen fleshy diaspores by opportunistic ground-dwelling ants can have relevant effects on seed and seedling biology of primarily vertebrate-dispersed plant species. It characterizes the plant and ant species involved in these interactions, addresses the particular attributes of ants and diaspores that mediate the interaction, and discusses the possible consequences of the interaction for the plants. (pages 68 - 84)
This chapter is available at:
https://academic.oup.com/chica...

Mutualism from Antagonism: Ants and Flowers - Victor Rico-Gray, Paulo S. Oliveira
DOI: 10.7208/chicago/9780226713540.003.0005
[ants, pollination, floral visits, plants, flowers, angiosperms, antagonism, mutualism]
The evolution of interactions between plants and their pollinators provides some of the clearest examples of change in the outcome of interactions from antagonistic to mutualistic. Early insect pollinators of angiosperms fed on pollen, ovules, seeds, and flower parts. The vast majority of these interactions were detrimental to the plants, and the closed carpels of angiosperms were probably a defense against these flower visitors. However, these antagonistic interactions provided a basis on which selection could act, because some flower visitors were less detrimental to flower parts than others, while some plants possessed floral traits that caused the interaction to be less detrimental to the plant and, at some point in time, beneficial. This chapter explores antagonism and mutualism between ants and flowers, focusing on pollination by ants and how ants discourage floral visits. (pages 85 - 98)
This chapter is available at:
https://academic.oup.com/chica...

Antagonism and Mutualism: Direct Interactions - Victor Rico-Gray, Paulo S. Oliveira
DOI: 10.7208/chicago/9780226713540.003.0006
[Pseudomyrmex, Acacia, ants, plants, food bodies, antagonism, mutualism, conditionality, domatia, ant–plant interactions]
Although the origin of some mutualisms (for example, pollination and seed dispersal) mostly involves a change in the outcome of the interaction (from antagonism to mutualism), other mutualisms are built on interactions involving at least an antagonistic pair of species and a mutualistic pair of species. Most studies, however, consider directly the interaction between two species, even though the evolutionary unit of many mutualisms involves at least three species in a way that emphasizes the evolutionary relationships between antagonism and mutualism. This chapter first describes the classic case of the association between Pseudomyrmex and Acacia, in which plants offer inquiline ants a whole array of resources (food bodies, extrafloral nectar, and domatia) in exchange for defense against herbivores and competitors. It then reviews and discusses other cases of ant–plant interactions in which plants offer both food bodies and domatia, or only domatia, and also looks at interactions in which plants offer mainly extrafloral nectar (a few also provide domatia). Finally, the chapter focuses on plant defensive strategies, induced responses, and the nature of conditionality. (pages 99 - 141)
This chapter is available at:
https://academic.oup.com/chica...

Antagonism and Mutualism: Indirect Interactions - Victor Rico-Gray, Paulo S. Oliveira
DOI: 10.7208/chicago/9780226713540.003.0007
[ants, plants, hemipterans, evolution, extrafloral nectaries, herbivores, fitness, ant–hemipteran interactions]
Some plants attract natural enemies of herbivores (for example, ants and predatory and parasitoid flies and wasps) by bearing honeydew-producing insects such as hemipterans, lepidopteran larvae, and gallmakers. Ant-tended Hemiptera (aphids, scales, coccids, whiteflies, leafhoppers, and treehoppers) are sap-sucking herbivores that excrete the excess liquid and sugars as energy-rich honeydew. Most Hemiptera are herbivores and their deleterious effect on plants is not only due to sap-sucking, which decreases plant fitness; they are also important vectors of plant pathogens). The presence of Hemiptera in low-diversity systems, including greenhouses, crop fields, and orchards, has been associated with high plant damage). However, it has been suggested that, under natural conditions, hemipterans do not reach high densities, and that their presence can therefore even be beneficial to some plants rather than harmful. This chapter examines the general characteristics of ant–hemipteran–plant interactions, including their conditional nature and possible outcomes, and their effects on the fitness of the various participants. Using fossil and current evidence, it also analyzes the ant–hemipteran interactions as they relate to the evolution of extrafloral nectaries. (pages 142 - 162)
This chapter is available at:
https://academic.oup.com/chica...

Nutrition of Plants by Ant Mutualists: Life History of Ant-Fed Plants and Ant-Garden Systems - Victor Rico-Gray, Paulo S. Oliveira
DOI: 10.7208/chicago/9780226713540.003.0008
[ant-fed plants, ant gardens, nutrition, mutualism, life history, ant–plant interactions, ants, myrmecophytes, geophytes]
Ants are probably the most common arboreal insects in tropical forests. Light gaps in forests induce a high richness of biotic interactions through intense competition among plants and through animal–plant interactions. Mutualism can be favored when organisms with a high probability of encounter and very low pre-mutualism growth rates live in environments that impose a high level of physical stress (for example, nutrient-poor habitats) but lack the richness of antagonistic interactions that is the basis for selection in many other mutualisms. Probably the clearest examples of how stressful environments can favor novel forms of interaction, including mutualism, involve the reversal of the usual trophic order of life. This chapter, which describes nutrition of plants by ant mutualists, focusing on the life history of ant-fed plants and ant-garden systems, first reviews the published literature and examples of ant-fed plants and then considers the ant–plant interactions commonly referred to as ant gardens. It also looks at the epiphytic myrmecophytes and then the geophytes or non-epiphytic myrmecophytes. (pages 163 - 176)
This chapter is available at:
https://academic.oup.com/chica...

Canopy-Dwelling Ants, Plant and Insect Exudates, and Ant Mosaics - Victor Rico-Gray, Paulo S. Oliveira
DOI: 10.7208/chicago/9780226713540.003.0009
[ant mosaics, competition, exudates, plants, ants, tropical forests, community structure, trophobionts, herbivores, forest canopies]
Interspecific competition has long been of interest to ecologists as a possible mechanism structuring natural communities and mediating phenomena such as resource partitioning within habitats. Ants are distributed over a wide variety of habitats and display a range of lifestyles; until recently they were regarded as fundamentally carnivorous. Although researchers recognized the role of some ant species as consumers of plant products, their function in food webs was considered to be primarily as predators and scavengers of animal matter. Because ants make up a major part of the arthropods living in the canopy of tropical forests, and because their biomass greatly surpasses that of their potential herbivore prey, this pattern poses a paradox and challenges our understanding of energy flow in forest canopies. This chapter, which focuses on canopy-dwelling ants, plant and insect exudates, and ant mosaics, also explores ant community structure, and investigates the effect of tending trophobionts on associated herbivores and on the host plant. (pages 177 - 192)
This chapter is available at:
https://academic.oup.com/chica...

Variation in Ant-Plant Interactions - Victor Rico-Gray, Paulo S. Oliveira
DOI: 10.7208/chicago/9780226713540.003.0010
[temporal variation, spatial variation, ants, plants, ant–plant interactions, habitats, community structure, coevolution]
The distribution of species is far from even, creating a spatial mosaic of species richness. In general, the tropics contain more species than equivalent areas at higher latitudes, although exceptions are numerous when specific taxa are reviewed. Not only are species unevenly distributed, but their interactions also vary spatially and seasonally; variations occur in critical plant structures and/or food sources for interactions as well. Ant–plant interactions have been reported to change in number and in outcome among habitats, throughout the year and between years. However, most studies do not take into account temporal variation, or that ant colonies and their interactions with plants can change over time. The spatial variation in the richness and availability of energy-rich liquid food for ants can be associated with interhabitat differences in ant diversity and abundance, and thus generate variation in ant–plant interactions. This chapter looks at examples of temporal and geographic variation (latitudinal, altitudinal, and geographic variation) in ant–plant interactions, and associates variation with community structure and coevolution. (pages 193 - 214)
This chapter is available at:
https://academic.oup.com/chica...

Ant-Plant Interactions in Agriculture - Victor Rico-Gray, Paulo S. Oliveira
DOI: 10.7208/chicago/9780226713540.003.0011
[agricultural systems, herbivores, ants, biological control agents, ant–plant interactions, maize, coffee]
Data obtained from studies of various topics in ant–plant interactions could potentially be applied in insect pest management programs of agricultural systems. Ants possess many characteristics that are associated with the potential to act as biological control agents, especially in tropical agroecosystems, and an economically beneficial role has been associated with ants used for such purposes. Nevertheless, the positive effects of several ant attributes (for example, predation of herbivores, pollination, soil improvement, and nutrient cycling) must be weighed against possible disadvantages (such as leaf-cutter ants and seed predators). Some ants feed on or disturb plants, act as vectors of plant diseases, benefit damaging Hemiptera, and may attack humans, domestic animals, or other beneficial animals. In short, virtually all ant species that prey on pests also possess some potential disadvantages. This chapter reviews some general characteristics of agricultural systems, the herbivore–ant relationship, the role of ants as biological control agents (describing two case studies: maize and coffee), and the relationship between biological control and the study of interspecific interactions. (pages 215 - 230)
This chapter is available at:
https://academic.oup.com/chica...

Overview and Perspectives - Victor Rico-Gray, Paulo S. Oliveira
DOI: 10.7208/chicago/9780226713540.003.0012
[ants, plants, angiosperms, ant–plant interactions, ecology, evolution, temporal variation, herbivory, phylogeny, plant defense]
Ants are probably the most dominant insect family on earth, and flowering plants have been the dominant plant group on land for more than 100 million years. The evolutionary success of angiosperms cannot be ascribed solely to benefits conferred by possessing flowers; it is also the result of benefits conferred by an array of interspecific interactions (for example, pollination, herbivory, and seed dispersal) that have helped shape their great diversity. On those bases alone, the results of studies on the ecology and evolution of ant–plant interactions are crucial to an understanding of the ecology of terrestrial biological communities. This chapter discusses the importance of studies on ant–plant interactions for evolutionary ecology and presents an overview of what has been learned by studying such interactions. It examines spatial and temporal variation in ant–plant interactions, the role of induced responses to herbivory, the phylogeny of ant–plant interactions, and plant defense by ants. The chapter concludes by suggesting perspectives on what needs to be studied and how these studies should be approached, and by reporting on research that is currently in development. (pages 231 - 252)
This chapter is available at:
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Literature Cited

Index