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Plant-Animal Interactions Source of Biodiversity

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DOI: 10.1007/978-3-030-66877-8

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Plant-Animal Interactions
Kleber Del-Claro  •  Helena Maura Torezan-Silingardi
Editors

Plant-Animal
Interactions
Source of Biodiversity
Editors Helena Maura Torezan-Silingardi
Kleber Del-Claro Inst de Biologia, Campus Umuarama
Inst de Biologia, Campus Umuarama Universidade Federal de Uberlandia
Universidade Federal de Uberlandia Uberlandia, Brazil
Uberlandia, Brazil

ISBN 978-3-030-66876-1    ISBN 978-3-030-66877-8 (eBook)


https://doi.org/10.1007/978-3-030-66877-8

© Springer Nature Switzerland AG 2021


This work is subject to copyright. All rights are reserved by the Publisher, whether the whole or part of
the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recita-
tion, broadcasting, reproduction on microfilms or in any other physical way, and transmission or infor-
mation storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar
methodology now known or hereafter developed.
The use of general descriptive names, registered names, trademarks, service marks, etc. in this publica-
tion does not imply, even in the absence of a specific statement, that such names are exempt from the
relevant protective laws and regulations and therefore free for general use.
The publisher, the authors and the editors are safe to assume that the advice and information in this
book are believed to be true and accurate at the date of publication. Neither the publisher nor the
authors or the editors give a warranty, expressed or implied, with respect to the material contained
herein or for any errors or omissions that may have been made. The publisher remains neutral with
regard to jurisdictional claims in published maps and institutional affiliations.

This Springer imprint is published by the registered company Springer Nature Switzerland AG
The registered company address is: Gewerbestrasse 11, 6330 Cham, Switzerland
V

To Angela Helena Torezan Silingardi, our first mentor.


Preface

Biotic interactions are ubiquitous and have shaped the evolution of Earth’s amaz-
ing biodiversity. Undoubtedly, plant-animal interactions have structured the
majority of ecological networks and the biodiversity of interactions therein
through evolutionary time. From antagonisms to mutualisms, plant-animal inter-
actions are basic pieces of the evolutionary puzzle underpinning natural systems.
Comprehending these relationships in all of their multidisciplinary aspects is fun-
damental to the future of life on a planet where negative human interference in
natural systems is growing at an alarming pace.
Plant-Animal Interactions: Source of Biodiversity is a collaborative approach to
this huge challenge, offering researchers and students new views, without leaving
behind basic information. This book is an effort to pave the way for scientists inter-
ested in improving our knowledge of how plant-animal interactions shape biodi-
versity. Our book calls you to join us in studying and preserving plant-animal
interactions, because they are sources of biodiversity. The book covers the most
important theoretical aspects of this line of study, considering classical, basic, and
naturalistic knowledge, but also presents advanced and applied approaches. Thus,
in the opening chapter, we present a general view of plant-animal interactions. As
editors, we considered it important to provide the foundations of plant-animal
interactions from an evolutionary approach. A great deal of research in ecology
and evolution has examined chemical mediation of plant-animal interactions.
Thus, in 7 Chap. 2, Lee A.  Dyer and Chris S.  Jeffrey discuss classical studies

focused on plant compounds that reduce or deter insect damage (herbivory) and
directly or indirectly affect secondary consumers. Here, the authors present a new
view considering two focal theoretical frameworks that drive investigations of
chemically mediated interactions, with a focus on phytochemical mixtures: coevo-
lution and trophic interaction theory. This approach enables us to proceed to the
field of herbivory with Robert J. Marquis and Renan F. Moura, who, in 7 Chap. 3,

discuss traits that enable plants to escape from their herbivores but have not been
formerly considered part of plant resistance theory. They will brilliantly convince
you that escape from herbivores can be used to effectively reduce herbivore pres-
sure in agricultural systems, and that escape also contributes to biodiversity main-
tenance in preserved ecosystems. This chapter presents a full new perspective on
the antagonistic relationships between plants and animals. However, to understand
how plant defense against herbivory evolves, it is necessary to characterize the
genetic underpinnings of resistance traits, quantify genetic variation in defense
trait production, and characterize how natural selection is acting on these traits.
We thank Liza M.  Holeski for giving us 7 Chap. 4, an amazing review of the

genetic basis of plant-­herbivore interactions and the evolutionary and ecological


genetics of plant resistance against herbivory. Different aspects of defense against
herbivory were considered in the previous chapters, and 7 Chap. 5 continues this

by presenting the role of biotic defenses in plant-animal interactions. Biotic


VII
Preface

defenses are relationships in which one organism (usually a plant or trophobiont


herbivore) attracts predators of its own enemies. In 7 Chap. 5, a team of young

biologists—Renan F. Moura, Eva Colberg, Estevão Alves-Silva, Isamara Mendes-


Silva, Roberth Fagundes, and Vanessa Stefani, joined by me (the old guy!)—deeply
discuss all types of biotic defense systems and their mechanisms. Full of examples
and exploring a very useful tool, experimental manipulation, this chapter illus-
trates how conditional the outcomes of biotic interactions may be, and how we still
are in the infancy of these studies.
Starting with a holistic view of plant-animal interactions and their impact on
biodiversity, the first five chapters of this book present the chemical and genetic
aspects of plant-animal interactions and explore the most antagonistic relation-
ships among these organisms, herbivory, and defenses against herbivores. However,
recent reviews in plant-animal interactions suggest that mutualistic relationships
(positive results to interacting organisms) are probably the strongest forces gener-
ating biodiversity. We will return to this issue later, after we present and compe-
tently exemplify the two main mutualistic relationships between plants and animals:
pollination and seed dispersal. The following two chapters are very similar in struc-
ture, starting by covering the natural history and basic aspects of the main animal
groups involved in these interactions, and then presenting new pathways for those
interested in these lines of research. In 7 Chap. 6, Helena Maura Torezan-­

Silingardi, Ilse Silberbauer-Gottesberger, and Gerhard Gottesberger draw on their


backgrounds in pollination, and in 7 Chap. 7, Richard T. Corlett covers seed dis-

persal and frugivory; these colleagues fulfilled the difficult mission of synthesizing
in each of these chapters issues worthy of a whole book. In both chapters the
authors go beyond characterizing and illustrating (with marvelous images) the
most important mutualistic plant-animal interactions, also alerting us to the dras-
tic problems caused by human impacts in natural systems. The reductions in popu-
lations and diversity of pollinators and seed dispersers are contributing to an
enormous loss of ecological services, putting human food security at risk.
Plant belowground interactions with soil microbes alter plant fitness and physi-
ology, affecting the performance of plant-associated aboveground organisms.
Although this issue is clear to all biologists, especially field researchers, these
aspects have only been superficially explored in previous books related to the evo-
lutionary ecology of plant-animal interactions. So, we thank Frédérique Rever-
chon and Alfonso Méndez-Bravo in 7 Chap. 8 for giving us a better understanding

of the ecological interactions occurring within the phytobiome and their impacts
on plant-animal interactions and associated biodiversity. This chapter opens up
discussion into the main examples of facilitation in plant-animal interactions, that
is, how these interactions can modify the environment by enlarging the niche for
opportunistic organisms. In 7 Chap. 9, an emerging group of very competent

young ecologists, headed by Eduardo S.  Calixto, and Danilo F.  B. dos Santos,
Diego V. Anjos, and Eva Colberg, discuss the concept of ecosystem engineering.
This chapter addresses the concepts, applications, biodiversity implications, and
future perspectives for the study of ecosystem engineers, especially regarding plant-
arthropod interactions.
VIII Preface

With these nine initial chapters, we are sure that the book provides all the
basic, updated, and useful knowledge, including new approaches, for anyone
interested in getting started in studying plant-animal interactions or settling pre-
vious fundamental questions. In the final part we have four chapters that place
this book even further than the previous ones. In 7 Chap. 10, Pedro Luna and

Wesley Dáttilo start by explaining how interactive communities and populations


generate organized networks and how these ecological networks vary over space
and time. They close the chapter by calling attention to the importance of plant-
animal networks in understanding the mechanisms and processes driving the
geographic mosaic of coevolution, as proposed by John N.  Thompson. This
chapter complements the initial chapter in considering the geographic mosaic of
coevolution theory as a key approach for understanding of origins and mainte-
nance of biodiversity of interactions. Next, Judith L. Bronstein in 7 Chap. 11

presents a new and very intriguing question in plant-animal interactions. She


starts by considering that mutualisms are not only present, but are common and
prominent interactions in every habitat on Earth. Thus, in a chapter full of won-
derful examples from pollination, biotic defenses, and other mutualisms, she pro-
poses an underlying rationale for why biological diversity tends to accumulate
around mutualisms. And is mutualism a source of evolutionary innovation?
7 Chap. 12, written by Rodrigo A. S. Pereira and Finn Kjellberg, explores this

question by presenting examples of mutualisms that allowed insects and/or


plants to expand their ecological niches. From a naturalistic up to a theoretical
view, this book illustrates how plant-animal interactions are sources of biodiver-
sity. However, in 7 Chap. 13, Kleber Del-Claro and Rodolfo Dirzo close the

book with a very disturbing topic. They discuss how in the Anthropocene, due to
defaunation and deforestation, human interference in the structure of ecological
networks may be forcing mass, global disruptions of ecological interactions,
potentially leading to the end of the biodiversity of interactions.
All books have a singular history. Plant-Animal Interactions: Source of Biodiver-
sity has a history mediated by a worldwide crisis, the SARS-CoV-2 or COVID-­19
or simply the coronavirus pandemic. In normal times it is not easy to edit or to
write a book or a book chapter. In a year of restrictions, suffering, loss of loved
ones, a time when life was turned upside down, working was even harder. We thank
each one of our authors for all of your dedication, resilience, and love of science.
We know how difficult it was. Some of us have been closed in at home during all
this time. Some of us lost loved ones and friends. One has a new baby (a piece of
good news!). One retired and had to move to a new city during the pandemic crisis.
One was forced to quarantine in a hotel room for 2 weeks. One housed the entire
family of a colleague during the fires in California. We are sincerely thankful to you
all.
We, in name of the whole group, thank our financial agencies, universities and
employers. We sincerely thank our editor João Pildervasser and the marvelous
Springer Nature team of collaborators.
Our very special acknowledgement goes to Ms. Eva Colberg for kindly revising
the English of 7 Chaps. 1, 5, 6, 9, and 10. There are no words to thank her col-

laboration.
IX
Preface

We also thank our families for their support and patience. We thank each mutu-
alistic organism living inside our bodies and cells for our lives, and plants and
animals for their interactions that become this still wonderful world.

Kleber Del-Claro
Helena Maura Torezan-Silingardi
Uberlândia, MG, Brazil
XI

Contents

1 An Evolutionary Perspective on Plant-Animal Interactions���������������������������������������1


Kleber Del-Claro and Helena Maura Torezan-­Silingardi

2 Chemically Mediated Multi-­trophic Interactions���������������������������������������������������������� 17


Lee A. Dyer and Christopher S. Jeffrey

3 Escape as a Mechanism of Plant Resistance Against Herbivores ������������������������ 39


Robert J. Marquis and Renan F. Moura

4 The Genetic Basis of Plant-Herbivore Interactions ������������������������������������������������������ 59


Liza M. Holeski

5 Biotic Defenses Against Herbivory���������������������������������������������������������������������������������������� 93


Renan F. Moura, Eva Colberg, Estevão Alves-Silva, Isamara Mendes-Silva,
Roberth Fagundes, Vanessa Stefani, and Kleber Del-Claro

6 Pollination Ecology: Natural History, Perspectives


and Future Directions������������������������������������������������������������������������������������������������������������������119
Helena Maura Torezan-Silingardi, Ilse Silberbauer-­Gottsberger,
and Gerhard Gottsberger

7 Frugivory and Seed Dispersal ������������������������������������������������������������������������������������������������175


Richard T. Corlett

8 Plant-Mediated Above- Belowground Interactions:


A Phytobiome Story����������������������������������������������������������������������������������������������������������������������205
Frédérique Reverchon and Alfonso Méndez-­Bravo

9 How Plant-­Arthropod Interactions Modify the Environment:


Concepts and Perspectives ������������������������������������������������������������������������������������������������������233
Eduardo Soares Calixto, Danilo Ferreira Borges dos Santos, Diego V. Anjos,
and Eva Colberg

10 Disentangling Plant-Animal Interactions into Complex Networks:


A Multi-view Approach and Perspectives������������������������������������������������������������������������261
Pedro Luna and Wesley Dáttilo
XII Contents

11 The Gift That Keeps on Giving: Why Does


Biological Diversity Accumulate Around Mutualisms?��������������������������������������������283
Judith L. Bronstein

12  utualism as a Source of Evolutionary Innovation:


M
Insights from Insect-Plant Interactions ����������������������������������������������������������������������������307
Rodrigo Augusto Santinelo Pereira and Finn Kjellberg

13 I mpacts of Anthropocene Defaunation on


Plant-Animal Interactions����������������������������������������������������������������������������������������������������������333
Kleber Del-Claro and Rodolfo Dirzo

Supplementary Information
Index���������������������������������������������������������������������������������������������������������������������������������������������� 349
XIII

Contributors

Estevão Alves-Silva  Instituto Federal de Educação, Ciência e Tecnologia Goiano, campus


Urutaí, Urutaí Goiás, Brazil

Diego V. Anjos  Universidade de São Paulo, Ribeirão Preto, SP, Brazil


Universidade Federal de Uberlândia, Uberlândia, MG, Brazil

Judith  L.  Bronstein  Department of Ecology and Evolutionary Biology, University of


Arizona, Tucson, AZ, USA

Eduardo Soares Calixto  Universidade de São Paulo, Ribeirão Preto, SP, Brazil

Eva Colberg  University of Missouri-St. Louis, St. Louis, MO, USA


Harris World Ecology Center, St. Louis, MO, USA

Richard  T.  Corlett  Xishuangbanna Tropical Botanical Garden, Chinese Academy of


Sciences, Menglun, Yunnan, China

Wesley Dáttilo  Red de Ecoetología, Instituto de Ecología A.C., Xalapa, Mexico

Kleber  Del-Claro  Laboratório de Ecologia Comportamental e de Interações (LECI),


Instituto de Biologia, Universidade Federal de Uberlândia (UFU), Uberlândia, Minas
Gerais, Brazil

Rodolfo Dirzo  Department of Biology and Woods Institute for the Environment, Stanford
University, Stanford, CA, USA

Lee  A.  Dyer  Hitchcock Center for Chemical Ecology, University of Nevada, Reno,
Reno, NV, USA

Roberth  Fagundes  Instituto de Ciências Exatas e da Natureza, Universidade da


Integração Internacional da Lusofonia Afro-Brasileira, Redenção, Ceará, Brazil

Gerhard Gottsberger  Universität Ulm, Ulm, Germany

Liza  M.  Holeski  Department of Biological Sciences, Northern Arizona University,


Flagstaff, AZ, USA

Christopher  S.  Jeffrey  Hitchcock Center for Chemical Ecology, University of Nevada,
Reno, Reno, NV, USA

Finn Kjellberg  CEFE, CNRS, Université Montpellier, Université Paul Valéry, Montpellier,


EPHE, IRD, Montpellier Cédex, France
XIV Contributors

Pedro Luna  Red de Ecoetología, Instituto de Ecología A.C., Xalapa, Mexico

Robert  J.  Marquis  Department of Biology and the Whitney R.  Harris World Ecology
Center, St. Louis, MO, USA

Isamara  Mendes-Silva  Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto,


Universidade de São Paulo, Ribeirão Preto, São Paulo, Brazil

Alfonso  Méndez-Bravo  CONACYT  – Escuela Nacional de Estudios Superiores,


Laboratorio Nacional de Análisis y Síntesis Ecológica, Universidad Nacional Autónoma de
México, Morelia, Michoacán, Mexico

Renan  F.  Moura  Laboratório de Ecologia Comportamental e de Interações (LECI),


Instituto de Biologia, Universidade Federal de Uberlândia (UFU), Uberlândia, Minas
Gerais, Brazil

Rodrigo Augusto Santinelo Pereira  Depto de Biologia, Faculdade de Filosofia, Ciências


e Letras de Ribeirão Preto, Universidade de São Paulo, São Paulo, Brazil

Frédérique Reverchon  Red de Estudios Moleculares Avanzados, Instituto de Ecología,


A.C., Pátzcuaro, Michoacán, Mexico

Danilo Ferreira Borges dos Santos  Universidade de São Paulo, Ribeirão Preto, SP, Brazil

Ilse Silberbauer-Gottsberger  Universität Ulm, Ulm, Germany

Vanessa  Stefani  Laboratório de História Natural e Reprodutiva de Artrópodes


(LHINRA), Instituto de Biologia, Universidade Federal de Uberlândia (UFU), Uberlândia,
Minas Gerais, Brazil

Helena Maura Torezan-Silingardi  Universidade Federal de Uberlândia (UFU) – Instituto


de Biologia – Laboratório de Ecologia Comportamental e de Interações (LECI), Uberlândia,
MG, Brazil

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