SPRINGER BRIEFS IN BIOLOGY O k u d a · W a t a n a b e · F u k u m Noboru Okuda · Katsutoshi Watanabe o r i Kayoko Fukumori · Shin-ichi Nakano Takefumi Nakazawa Biodiversity in Aquatic Systems and Environments Lake Biwa 123 SpringerBriefs in Biology For further volumes: http://www.springer.com/series/10121 Noboru Okuda (cid:129) Katsutoshi Watanabe Kayoko Fukumori (cid:129) Shin-ichi Nakano Takefumi Nakazawa Biodiversity in Aquatic Systems and Environments Lake Biwa Noboru Okuda Katsutoshi Watanabe Center for Ecological Research Department of Zoology Kyoto University Graduate School of Science Otsu, Japan Kyoto University Kyoto , Japan Kayoko Fukumori Section of Integrative Biology Shin-ichi Nakano The University of Texas at Austin Center for Ecological Research Austin , TX , USA Kyoto University Otsu, Japan Takefumi Nakazawa Department of Life Sciences The College of Biosciences and Biotechnology National Cheng Kung University Tainan , Taiwan ISSN 2192-2179 ISSN 2192-2187 (electronic) ISBN 978-4-431-54149-3 ISBN 978-4-431-54150-9 (eBook) DOI 10.1007/978-4-431-54150-9 Springer Tokyo Heidelberg New York Dordrecht London Library of Congress Control Number: 2013951142 © The Author(s) 2014 This work is subject to copyright. 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Printed on acid-free paper Springer is part of Springer Science+Business Media (www.springer.com) Foreword While the twentieth century was the century when researchers tried to discover “the general basic principles of organisms,” the twenty-fi rst century is expected to be the century when researchers try to understand “the evolution and diversity of organ- isms” on the basis of such general principles of organisms by integrating various disciplines such as morphology, physiology, and ecology. The chief diffi culty in studying “the evolution and diversity of organisms” lies in the fact that we have to consider factors at various levels ranging from the genome to the ecosystem. As taking various factors into account may cause a loss of focus, traditional studies have been restricted to analyzing only one individual level or fac- tor. However, unfortunately, the current research and education system based on such a compartmentalized approach is inadequate for incisively studying “the evo- lution and diversity of organisms.” In order to solve these problems, we should strongly emphasize the necessity for joint studies and integration of the education programs between micro-level biology (genomic science, evolutionary developmental biology, genetic science, cell biol- ogy, neurobiology, molecular physiology, and molecular evolutionary studies) and macro-level biology (primatology, anthropology, ethology, environmental biology, evolutionary taxonomy, and so on) to young biologists. We launched a new educa- tion program in Kyoto University, called “Global COE program for Evolution and Biodiversity Research” to promote such integrative studies at various levels, and have succeeded in initiating novel currents of study of biodiversity that led rather than followed those in the rest of the world. To this aim, we decided to publish six books in “SpringerBriefs in Biology” which we hope will stimulate interest in such novel approaches on the evolution and diversity of organisms in the world and among young biologists. This book covers a broad range of aquatic biology from molecular biology, through ecology, to paleobiology in Lake Biwa, a fascinating ancient lake that is also famed as a biodiversity hotspot. It will be a useful resource not only for researchers and technicians but also for graduate students who want to learn aquatic science. Naturalists and nature lovers can enjoy here a virtual tour of the world of biodiversity in this ancient lake. That biodiversity ranges over vast differences of v vi Foreword scale: We describe the latest molecular genetics techniques that have revealed a relationship between the lake’s microbial diversity and its ecosystem functioning. We also describe the evolutionary history of the lake’s biodiversity, especially fi sh diversity, as well as laboratory experiments that revealed that diversity of fi sh feed- ing morphology affects the body size of plankton communities and consequently the overall ecosystem properties. Unfortunately, Lake Biwa is also known as a tragic lake which has suffered from a variety of human disturbances, such as eutrophication, habitat destruction, exotic species introduction, and global warming, and that is now threatened by biodiver- sity loss and ecosystem deterioration. This book thus will appeal to conservationists and policy makers who are interested in biodiversity conservation and ecosystem management. As well, it will provide an opportunity for all readers to think deeply about the need to conserve the earth’s biodiversity. Kiyokazu Agata Professor, Department of Biophysics, Kyoto University Project Leader of Kyoto University Global COE program “Evolution and Biodiversity” Pref ace Two decades have passed since the Earth Summit, at which the Convention on Biological Diversity (CBD) came into force to encourage the conservation of bio- logical diversity on the earth and the fair and equitable sharing of benefi ts arising from the sustainable use of its components. At present, the loss of biological diver- sity has progressed at an accelerating rate and is particularly severe in freshwater ecosystems, in which environmental alterations have been extreme due to drastic changes in land-use patterns. For most of us, it is intuitively understandable why fi shery resources should be conserved, because they provide humankind with ben- efi ts such as food sources, i.e., a provisioning service from aquatic ecosystems. However, it is not so easy to answer the question of why fi sh diversity is necessary for human well-being. We also have little knowledge on how diversity of other aquatic biota, especially of microbes, affects ecosystem properties such as organic production, water purifi cation, and nutrient cycling. Or rather, we human beings have no inherent sense to discern the invisible nature of diversity in a microscopic world. For aquatic biologists, therefore, it is a great challenge to perceive the entity of biological diversity in aquatic ecosystems, trace its evolutionary history, and dis- cover the ecological consequences of its evolutionary diversifi cation, toward the integration of biodiversity sciences. Here we introduce the latest topics of ecological and evolutionary research on aquatic biological diversity from bacteria to fi shes, with special reference to the case of Lake Biwa. Lake Biwa, in western Japan, is an ancient lake with a geological history of four million years, making it the third oldest lake in the world. It is called a biodiversity hotspot, where 1,769 aquatic species including 61 endemics are recorded, providing a rare opportunity to study the evolutionary diversifi cation of aquatic biota and its ecological consequences. In this book, we fi rst narrate the evo- lutionary history of biological diversity, especially of fi sh diversity in this lake, focusing on its paleogeography and molecular phylogeny (Chap. 1 by Katsutoshi Watanabe). The reader will learn how physical features of the lake have promoted evolutionary diversifi cation of feeding functions in fi shes. vii viii Preface Functional diversifi cation of fi shes, which play important ecological roles as keystone predators of lake ecosystems, can sometimes be a major driver for altering an entire lake community through their top-down trophic cascading effects (Chap. 2 by Noboru Okuda and Kayoko Fukumori). We demonstrate that predator functional diversity has the potential for altering species composition, size structure, and tro- phic relations of an entire biological community, which in turn affects ecosystem functioning such as energy fl ows and nutrient cycling. In lakes, the leading actors in ecosystem functioning, such as production and mineralization of organic matter, are microbes, which are often regarded as ecosys- tem engineers altering aquatic environments because of their overwhelming domi- nance in number and mass. A few decades ago, the diversity of aquatic microbes in nature remained unexplored because a large portion of bacteria never grow under cultivation to be isolated for taxonomic identifi cation. However, the recent explo- sion of advances in molecular techniques has vigorously encouraged microbiolo- gists to characterize genetic and functional diversity of in situ microbial communities (Chap. 3 by Shin-ichi Nakano). While respecting the blessings of invaluable biological diversity in lake ecosys- tems, we have to warn that modern human activities have brought a crisis of biodi- versity loss in lakes worldwide, which will result in deterioration of ecosystem functioning and thus of ecosystem services. In the face of such human disturbances, ecosystem alterations are often catastrophic, a phenomenon known as ecological regime shift. To understand how human-mediated environmental changes can induce regime shifts in lake ecosystems and to evaluate how their biological diver- sity, especially intraspecifi c phenotypic diversity, affects ecosystem resilience, i.e., dampening the incidence and intensity of regime shifts, a promising approach is construction of theoretical models, which is considered a kind of thought experi- ment to test probable future scenarios (Chap. 4 by Takefumi Nakazawa). Again, we stress that Lake Biwa can be an ideal model system in which to prac- tice biodiversity conservation with the promotion of ecological and evolutionary understanding of biological diversity in lake ecosystems. This opportunity exists because Lake Biwa has experienced a variety of serious environmental problems that are shared by many other lakes worldwide, and also because the lake currently shows symptoms of recovery from the biodiversity loss and ecosystem deteriora- tion, recognized only by our persistent efforts in biodiversity research. Through this book, the reader will learn how the evolutionary diversifi cation of aquatic organ- isms interplays with the ecology of their populations and communities, and vice versa, and why we should conserve biological diversity at different levels of bio- logical organization from genes to ecosystems. Otsu , Japan N oboru Okuda Contents 1 Origin and Diversification of Freshwater Fishes in Lake Biwa .............. 1 1.1 Introduction: Lake Biwa and Its Fish Fauna ........................................ 1 1.2 A Brief Review on the Origins and Evolution of Freshwater Fishes ............................................................................ 8 1.3 Molecular Phylogenetic Approaches ................................................... 10 1.3.1 Origin of Endemic Lineages .................................................... 10 1.3.2 Population Establishment by Endemic and Non-endemic Species ........................................................ 14 1.4 Conclusions and Perspectives .............................................................. 15 References ..................................................................................................... 17 2 Predator Diversity Changes the World: From Gene to Ecosystem ........ 21 2.1 Why is Biodiversity Important? ........................................................... 21 2.2 Biodiversity at Three Levels ................................................................ 22 2.3 What is Phenotypic Polymorphism? .................................................... 22 2.4 Phenotypic Polymorphism in Aquatic Ecosystems ............................. 23 2.4.1 Trophic Polymorphism and Adaptive Divergence ................... 23 2.4.2 Ecological Speciation and Species Pair ................................... 25 2.4.3 The Ancient Lake Biwa as an Evolutionary Hot Spot ............. 26 2.4.4 Life History Polymorphism ..................................................... 27 2.4.5 Rapid Evolution of Trophic Polymorphism ............................. 28 2.4.6 Genetic Mechanisms of Trophic Polymorphism ..................... 30 2.5 Niche Construction .............................................................................. 31 2.6 Predator Diversity and Ecosystem Functioning ................................... 33 2.6.1 Mesocosm Experiments ........................................................... 35 2.6.2 Food Web Properties as a Universal Measure ......................... 37 2.7 Eco-Evolutionary Feedbacks ............................................................... 40 2.7.1 Feedback Loops ....................................................................... 41 2.7.2 Community Genomic Dynamics ............................................. 43 2.8 Why is Predator Diversity Important? ................................................. 44 References ..................................................................................................... 45 ix