Mutualistic Networks (Monographs in Population Biology): 53 - Hardcover

Bascompte, Jordi; Jordano, Pedro

Hardcover

ISBN 10: 0691131260 ISBN 13: 9780691131269

Publisher: Princeton University Press, 2013

Synopsis

Mutualistic interactions among plants and animals have played a paramount role in shaping biodiversity. Yet the majority of studies on mutualistic interactions have involved only a few species, as opposed to broader mutual connections between communities of organisms. Mutualistic Networks is the first book to comprehensively explore this burgeoning field. Integrating different approaches, from the statistical description of network structures to the development of new analytical frameworks, Jordi Bascompte and Pedro Jordano describe the architecture of these mutualistic networks and show their importance for the robustness of biodiversity and the coevolutionary process. Making a case for why we should care about mutualisms and their complex networks, this book offers a new perspective on the study and synthesis of this growing area for ecologists and evolutionary biologists. It will serve as the standard reference for all future work on mutualistic interactions in biological communities.

About this title

About the Author

Jordi Bascompte is professor of ecology at the University of Zurich. He is the coauthor of Self-Organization in Complex Ecosystems (Princeton). Pedro Jordano is a professor at the Spanish Research Council and honorary professor at the University of Sevilla.

From the Back Cover

"Until recently, the study of mutualism was replete with lovely natural history details, but largely divorced from ecological theory. In this fine book, Bascompte and Jordano take an important step toward rectifying this situation, by applying a rich array of network tools and phylogenetically informed analyses to webs of mutualistic interactions. The authors deftly synthesize a wide range of empirical case studies and theoretical perspectives, draw a number of intriguing and unexpected conclusions, and provide useful, detailed methodological appendices which will facilitate future studies of mutualism in a community context."--Robert D. Holt, University of Florida

"This engaging book is required reading for anyone interested in how the web of life is organized. With impeccable scholarship, a broad and careful presentation, and nuanced interpretation, it probes deep questions about the structure of biodiversity, and weaves innovative approaches with insightful interpretations."--John Thompson, University of California, Santa Cruz

"This useful book examines the structure of mutualistic networks by delving into emerging structures from mutualistic network research, explaining what drives the structure, and investigating its implications on the robustness of ecological communities. Comprehensively reviewing this important field, this work will find a significant readership and promote further research."--Kevin McCann, University of Guelph

From the Inside Flap

"Until recently, the study of mutualism was replete with lovely natural history details, but largely divorced from ecological theory. In this fine book, Bascompte and Jordano take an important step toward rectifying this situation, by applying a rich array of network tools and phylogenetically informed analyses to webs of mutualistic interactions. The authors deftly synthesize a wide range of empirical case studies and theoretical perspectives, draw a number of intriguing and unexpected conclusions, and provide useful, detailed methodological appendices which will facilitate future studies of mutualism in a community context."--Robert D. Holt, University of Florida

"This engaging book is required reading for anyone interested in how the web of life is organized. With impeccable scholarship, a broad and careful presentation, and nuanced interpretation, it probes deep questions about the structure of biodiversity, and weaves innovative approaches with insightful interpretations."--John Thompson, University of California, Santa Cruz

"This useful book examines the structure of mutualistic networks by delving into emerging structures from mutualistic network research, explaining what drives the structure, and investigating its implications on the robustness of ecological communities. Comprehensively reviewing this important field, this work will find a significant readership and promote further research."--Kevin McCann, University of Guelph

Excerpt. © Reprinted by permission. All rights reserved.

Mutualistic Networks

By JORDI BASCOMPTE, PEDRO JORDANO

PRINCETON UNIVERSITY PRESS

Copyright © 2014 Princeton University Press
All rights reserved.

ISBN: 978-0-691-13126-9

Contents

Preface....................................................................
xi
Chapter 1. Biodiversity and Plant-Animal Coevolution.......................
1
Chapter 2. An Introduction to Complex Networks.............................
15
Chapter 3. The Structure of Plant-Animal Mutualistic Networks..............
42
Chapter 4. Ecological and Evolutionary Mechanisms..........................
64
Chapter 5. Mutualistic Networks in Time and Space..........................
87
Chapter 6. Consequences of Network Structure...............................
107
Chapter 7. Epilogue........................................................
136
Appendix A. Indices Used in Mutualistic Network Analyses...................
139
Appendix B. Fitting Degree Distributions...................................
143
Appendix C. Measures of Nestedness.........................................
147
Appendix D. Measures of Modularity.........................................
150
Appendix E. Phylogenetic Methods and Network Analysis......................
154
Appendix F. Null Models for Assessing Network Structure....................
160
Appendix G. An Analytical Theory of Mutualistic Networks...................
167
Appendix H. Software for the Analysis of Complex Networks..................
175
Bibliography...............................................................
179
Index......................................................................
201

CHAPTER 1

Biodiversity and Plant-Animal Coevolution

HISTORICAL OVERVIEW

The almost-perfect matching between the morphology of some orchids andthat of their insect pollinators fascinated Charles Darwin, who foresaw thatthe reproduction of these plants was intimately linked to their interaction withthe insects (Darwin, 1862). Darwin even predicted that the extinction of oneof the species would lead to the extinction of its partner:

If such great moths were to become extinct in Madagascar, assuredly theAngraecum would become extinct (Darwin, 1862, p. 202).

Later on, Alfred Russell Wallace would take the examples of plant-animalinteractions to illustrate the force and potential of natural selection to shapephenotypic traits. He already noted that the selective pressures derive directlyfrom the interaction itself (Wallace, 1889).

The fascinating experimental work by Darwin on plant sexuality was veryinfluenced by the earlier work of Sprengel (1793) demonstrating the role ofinsects in plant fertilization (Fig. 1.1a). Similarly, his work on hybridizationshows the strong influence by Köllreuter (1761; seeWaser 2006, for a historicaloverview). Köllreuter already documented the diversified pollination servicethat multiple insect species provide to plants. However, the major advancesat that time in documenting the specificity of pollination patterns are dueto the monumental work of Müller, Thompson, et al. (1883), providing thelist of pollinator species for 400 plant species, and Knuth (1898), reportingrecords for more than 6000 species. Early researchers on plant-seed disperserinteractions (Hill, 1883; Beal, 1898; Sernander, 1906) also emphasized thediversity and subtleties of mutual dependencies among the partners andprovided well-grounded evidence for mutual coadaptations between them(Fig. 1.1b). Beal provides an analogy with pollination systems, quoting

Darwin's orchid book (Darwin, 1862):

The more we study in detail the methods of plant dispersion, the morewe shall come to agree with a statement made by Darwin concerning thedevices for securing cross-fertilization of flowers, that they "transcend,"in an incomparable degree, the contrivances and adaptations which themost fertile imagination of the most imaginative man could suggest withunlimited time at his disposal (Beal, 1898, p. 88).

The complexity that such interactions could take was already recognized byDarwin in the final paragraphs for the first edition of on the Origin:

It is interesting to contemplate an entangled bank, clothed with many plantsof many kinds, with birds singing on the bushes, with various insects flittingabout, and with worms crawling through the damp earth, and to reflectthat these elaborately constructed forms, so different from each other, anddependent on each other in so complex a manner, have all been producedby laws acting around us (Darwin, 1859, p. 498).

Similarly, in Chapter III, Struggle for Existence, we can read:

I am tempted to give one more instance showing how plants and animals,most remote in the scale of nature, are bound together by a web of complexrelations (Darwin, 1859, p. 73).

Darwin also envisioned the mutually reciprocal effects involved in thepollination of red clover by "humble-bees" and the potential effects of declinesin pollinator abundance. He foresaw the complexity of mutualistic networks, acomplexity that precluded a community-wide approach.

Mutualism and symbiosis became quickly incorporated into the researchagenda after de Bary (1879) coined the term symbiosis to account for interactionsamong two or more dissimilar entities living in or on one anotherin intimate contact. These developments of the study of mutualisms werewell grounded on the empirical evidence obtained by botanists documentingevery detail of the morphological structures of flowers, fruits and seeds(Fig. 1.1) as well as the intricacies of the interactions with animals. Sincethen, a myriad of scientific papers have described the mutually beneficial(mutualistic) interactions between plants and their animal pollinators or seeddispersers. But the interest of ecologists and evolutionary biologists in mutualisticinteractions has been quite variable in emphasis and prevalence duringthis period of time.

Work on mutualism, like the analysis by Pound (1893), remained marginalto dominant views in ecology. Antagonistic interactions were at the core ofClements and Tansley's views of plant ecology, which dominated the field inthe United States and United Kingdom during the early 20th century. This wasparadoxical given the rapid discovery of new major symbiotic interactions likemycorrhizae in the 1880s and 1890s (Schneider, 1897). In fact, a few yearsafter the Lotka-Volterra models were developed for antagonistic interactions,Gause and Witt (1935) proposed dynamic models of mutualism based onvery similar formulations. However, mutualistic interactions were ignored inthe extensive treatment that Volterra and D'Ancona (1935) dedicated to thedynamics of "biological associations" among multiple species. Up to the early1970s, mutualism was not at the center of ecological thinking (L. E. Gilbertand Raven, 1975), which was more focused on the dynamics of antagonisticinteractions such as predation and competition as the major forces drivingcommunity dynamics.

Most recent textbooks on ecology and evolution just treat mutualismsas iconic representations of amazing interactions among species, lacking aformal conceptual treatment at a similar depth to predation or competition(Sapp, 1994). Boucher (1985a) provides a lucid analysis for the reasons whymutualism had a marginal importance in ecological studies up to the late 1970sand early 1980s, when dynamic and genetic models of mutualistic interactionsstarted to be revisited (May, 1982). Among these reasons, there are thetechnical difficulties to find stable solutions for dynamic models of mutualism(May, 1973) and the lack of appropriate empirical and theoretical tools todevelop a synthesis of the enormous diversity of mutualistic interactions (May,1976). Also, the association of the idea of mutualism with anarchist thinkingrelated to the 1902 book Mutual Aid by Peter Kropotkin most likely hadan influential effect on the demise of mutualism in the early 1900s and itsmarginal consideration (Boucher, 1985a).

Ehrlich and Raven, in their classic paper, emphasized the pivotal role ofplant-animal interactions in the generation of biodiversity on Earth (Ehrlichand Raven, 1964). Interestingly enough, insects and flowering plants areamong the most diverse groups of living beings, and it is assumed that theappearance of flowering plants opened new niches for insect diversification,which in turn further spurred plant speciation (Farrell, 1998; McKenna,Sequeira, et al., 2009). This scheme has some alternative explanations, such asthat one group may have been tracking the previous diversification of the otherone without affecting it (Ehrlich and Raven, 1964; Pellmyr, 1992; Ramírez,Eltz, et al., 2011). However, the relevant point is that animal-pollinatedangiosperm families are more diverse than their abiotically pollinated sister-clades(Dodd, Silvertown, et al., 1999).

Since the seminal paper by Ehrlich and Raven (1964), there has been aflourishing of studies on plant-animal interactions in general and on mutualismsamong free-living species in particular. A significant amount of thiswork stems from recent advances in the study of coevolutionary processes(Thompson, 1994, 1999a) and the recognition of their importance in generatingbiodiversity on Earth.

Fortunately, there is ample fossil evidence of the origin of mutualistic interactions.Thus, the first preliminary adaptations to pollination can already betracked around the mid-Mesozoic, almost 200 million years ago, and becamewidely observed from the mid-Cretaceous, more than 100 million years ago(Labandeira, 2002). In relation to seed dispersal, the early evolution of animal-dispersedfruits in the upper Carboniferous, together with the diversification ofsmall mammals and birds in the Tertiary, allowed the diversification of plantfruit structures and dispersal devices (Tiffney, 2004). Therefore, multi-specificinteractions among free-living animals and plants have been an importantfactor in the generation of biodiversity patterns for a very long time.

But mutualisms have been important not only in the past. They remainimportant in the present. Mutualisms among free-living species are one ofthe main wireframes of ecosystems, simply because extant ecosystems wouldcollapse in absence of animal-mediated pollination or seed dispersal of thehigher plants. Effective pollen transfer among individual plants is required bymany higher plants for successful fructification, and active seed dispersal byanimal vectors is a key demographic stage for maintaining forest regenerationand dynamics. Both processes depend on the provision by plants of some typeof food resource that animals can obtain while foraging. These plant resources(nectar, pollen, fleshy pulp, seeds, or oil) are fundamental in different typesof ecosystems for the maintenance of animal diversity through their keystoneinfluence on life histories and annual cycles.

From a conservation point of view, hunting and habitat loss are drivingseveral species of large seed dispersers toward extinction, and these effectscascade towards a general reduction of biodiversity through reductions in seeddispersal (Dirzo and Miranda, 1990; Kearns, Inouye, et al., 1998; S. J. Wright,2003). Looking back through time, evidence for these effects comes from thefossil record. Episodes of insect diversity decline, such as the ones during theMiddle to Late Pennsylvanian extinction, during the Permian event, and atthe Cretaceous/Tertiary boundary, have been followed by major extinctions offlowering plants (Labandeira, 2002; Labandeira, Johnson, et al., 2002). All thisevidence already suggests that in conservation we cannot treat these speciesisolated from each other or consider only pairs of interacting species. Rather,we need to have a network perspective.

The first studies on mutualism focused on highly specialized one-to-oneinteractions between one plant and one animal (Johnson and Steiner, 1997;Nilsson, 1988). Examples of these highly specific pairwise interactions areDarwin's moth and its orchid (Darwin, 1862; Nilsson, Jonsson, et al., 1987),long-tongued flies and monocot plants (Johnson and Steiner, 1997), fig waspsand figs (Galil, 1977; Wiebes, 1979; J. M. Cook and Rasplus, 2003), andyucca moths and yuccas (Pellmyr, 2003). However, their strong emphasisin evolutionary studies probably reflects more the aesthetics of such almostperfect matching than their frequency in nature (Schemske, 1983; Waser,Chittka, et al., 1996). Motivated by this fact, several authors already advocateda community context to address mutualistic interactions (Heithaus, 1974;Feinsinger, 1978; Janzen, 1980; Herrera, 1982; Jordano, 1987; Fox, 1988;Petanidou and Ellis, 1993; Bronstein, 1995; Waser, Chittka, et al., 1996; Iwaoand Rausher, 1997; Inouye and Stinchcombe, 2001).

Waser, Chittka, et al. (1996) made the point that generalism is widespreadin nature and advanced conceptual reasons based on fitness maximization inhighly fluctuating interaction environments. More recently, and as a consequenceof this interest in expanding the pairwise paradigm, there has beensignificant progress in our understanding of how pairwise interactions areshaped within small groups of species across time and space (Thompson andPellmyr, 1992; Thompson, 1994; Parchman and Benkman, 2002).

A BIT OF NATURAL HISTORY

Mutualisms are assumed to be among the most omnipresent type of interactionin terrestrial communities (Janzen, 1985). Beyond the mutualistic interactionsamong conspecific individuals (i.e., the subject of kin-selection and parent-offspringinteractions), most of these interactions are allospecific interactions,involving species, or sets of species, completely unrelated. Multispecificinteractions involving mutual benefits among partner species are extremelywidespread and involve all the terrestrial vertebrates, plants, and arthropods.Many of these mutualisms involve sets of animal species interacting with plantspecies.

Only five major groups of multispecific mutualisms exist in natural terrestrialecosystems: (1) pollination and (2) seed-dispersal mutualisms amonganimals and plants (Jordano, 1987); (3) protective mutualisms among ants(and sometimes other arthropods) that protect plants and homopterans (Rico-Grayand Oliveira, 2007); (4) harvest mutualisms, including the gut flora andfauna of all vertebrate species and many invertebrates, the root rhizosphereoccupants, lichens, decomposers, epiphyllae and some epiphytes, and ant-plants(ant-feeding plants; L. E. Gilbert and Raven 1975; Janzen 1985; Rico-Grayand Oliveira 2007). A fifth type of mutualism is the interaction betweenhumans and plants (agriculture) and animal husbandry (Boucher, 1985b),mediated by the domestication process. Facilitative interactions among plantscan also be considered as a type of mutualism with beneficial consequences forboth partners (Verdú and Valiente-Banuet, 2008), although in many cases thepositive effects occur only during specific stages (e.g., facilitation of seedlingestablishment).

In this book we focus on pollination and seed dispersal with brief excursionsinto protective and ant-plant mutualisms (Fig. 1.2). The reason for this choiceis because this is where the majority of research on mutualistic networks hasfocused and is where our expertise lies. Still, there is no evidence to suggestthat the same rules do not apply to other mutualistic networks.

Typically, we might expect the net outcomes of mutualistic interactionsamong individuals or among species to fall somewhere along a gradientbetween antagonism (e.g., parasitism or cheating) and legitimate mutualism(Thompson, 1982). For instance, Rico-Gray and Oliveira (2007) document thatant-plant interactions most likely originated from antagonistic interactions, butthe most frequent form of their ecological relationships is mutualistic. Andthis range can be observed in the interaction of two partner species (variationamong individual effects) or when multiple species are involved (variationamong species effects). For example, consider the diverse assemblage ofinsects visiting the flowers of a plant species. The whole range of interactionsin a given population of the plant would be the result of the combinedinteractions of individual plants with individuals of different flower-visitinginsects. Some individual plants will be visited by many insect species, whereasothers (e.g., plants growing in isolated patches within the population) would bevisited by a restricted set of flower-visitors, presumably with lower visitationfrequency. If insect species differ in the effectiveness of pollen transfer, wecould imagine that some individual plants receive most visits by legitimatepollinators, whereas other might be visited more frequently by noneffectivepollinators (e.g., nectar thieves). Individual fitness variation across individualplants would depend on the relative location of each plant along the gradientof effectiveness defined by its flower-visitor assemblage: plants with reducedfruit set most likely had visits by low-efficiency pollinators, and those withhigher seed set were most likely visited by legitimate pollinators. The overallinteraction pattern for the plant species would be a composite of the visitationpattern to the different individuals in the population.

The dynamics of mutualistic interactions are surprisingly robust to thepresence of cheaters or antagonists (Bronstein, Wilson, et al., 2003), yet theydetermine ample temporal and spatial variation in the outcomes. Multispecificmutualisms involving plant-animal interactions are harvest-based mutualisms,mostly through the feeding of one species on the other (Janzen, 1985; Holland,Ness et al., 2005). Plants offer a resource (nectar, pulp, pollen, volatilefragrances, resin material to build nests, corolla parts, or other ancillarystructures) that are collected by animals. The mutualistic service by animalsdirectly derives from their foraging and movement patterns, resulting indispersal of the plant propagules (seeds or pollen) or protection for the plantagainst herbivores or pathogens.

(Continues...)

Excerpted from Mutualistic Networks by JORDI BASCOMPTE, PEDRO JORDANO. Copyright © 2014 Princeton University Press. Excerpted by permission of PRINCETON UNIVERSITY PRESS.
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.

Edition details

• Publisher: Princeton University Press
• Publication date: 2013
• Language: English
• ISBN 10: 0691131260
• ISBN 13: 9780691131269
• Binding: Hardcover
• Number of pages: 224