Messages from Islands: A Global Biodiversity Tour 9780226406589

Citation preview

Messages from Islands

Messages from

ISLANDS A Global Biodiversity Tour

Ilkka Hanski

The University of Chicago Press Chicago and London

The University of Chicago Press, Chicago 60637 The University of Chicago Press, Ltd., London © 2016 by The University of Chicago All rights reserved. Published 2016. Printed in the United States of America 25 24 23 22 21 20 19 18 17 16

1 2 3 4 5

ISBN-13: 978-0-226-40630-5 (cloth) ISBN-13: 978-0-226-40644-2 (paper) ISBN-13: 978-0-226-40658-9 (e-book) DOI: 10.7208/chicago/9780226406589.001.0001 Library of Congress Cataloging-in-Publication Data Names: Hanski, Ilkka, author. Title: Messages from islands: a global biodiversity tour / Ilkka Hanski. Description: Chicago: The University of Chicago Press, 2016. | Includes bibliographical references and index. Identifiers: LCCN 2016019373 | ISBN 9780226406305 (cloth : alk. paper) | ISBN 9780226406442 (pbk.) | ISBN 9780226406589 (e-book) Subjects: LCSH: Biodiversity. | Island ecology. Classification: LCC QH541.15.B56 H364 2016 | DDC 577.5/2—dc23 LC record available at https://lccn.loc.gov/2016019373 ♾ This paper meets the requirements of ANSI/NISO Z39.48-1992 (Permanence of Paper).

To Eeva and Natalie, a chronicle of what your life partner and grandfather has done

Contents

Preface  ix 1

Biodiversity: Species and Where They Live  1

2

How Is Biodiversity Generated?  42

3

Changing Biodiversity  76

4

Species on the Move  114

5

Habitat Loss and Fragmentation  146

6

Why Is Biodiversity Important?  186 Epilogue  221 References  225 Index  241

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Preface

Biodiversity, and life in general, is the defining feature of our planet. Small children are fascinated by biodiversity, but sadly that interest often wanes because we grown-ups and our educational systems fail to nurture it, and fail to build bridges between children’s instinctive attraction to animals and plants and sound understanding of the ecological and evolutionary processes that keep the world running. Not all children lose their early curiosity about biodiversity, however; their interest may mature and lead to a profession in ecology and evolutionary biology. That is what happened to me. I remember one early incident that played an especially big role. I spent all my school holidays in the country, at my grandmother’s place, which I value in hindsight as a huge privilege. At the age of eight, I took up collecting butterflies and moths, following the example of a few older boys. For the others this interest lasted a year or two, but mine never stopped. One reason that I stayed interested was a butterfly that I collected in 1964. The butterfly, a dusky meadow brown (Hyponephele lycaon), had gone extinct in Finland around 1936. My specimen must have been a vagrant from somewhere southeast of Finland. I was surprised and delighted to have captured such an unusual species; my father thought that I should let others know about it, and so I attended my first meeting of the local entomological club. The news about my butterfly was conveyed to Esko Suomalainen at the University of Helsinki, a population geneticist who is still remembered for his work on ix

x

Preface

chromosome evolution in Lepidoptera (butterflies and moths). Suomalainen published a paper in 1958 on the extinction of the dusky meadow brown from Finland, in which he discussed the role of inbreeding in the disappearance of the last small populations. His thinking was ahead of his time; research on the effect of inbreeding on extinction became a hot topic only in the 1970s. He sent me a reprint of his publication, which I could not read as it was written in German, but you can imagine the effect on an eleven-year-old boy of receiving his letter and a copy of his scientific paper. Collecting that butterfly and receiving that reprint made it practically certain that I would become a biologist. Research on biodiversity, and reading and finding out more about it, has a dark side that most other fields of research do not. Biodiversity is declining rapidly both locally and globally, because the human impact on the planet has reached such a level that many researchers describe our time as a new geological epoch, the Anthropocene. The world is changing so rapidly that an individual observer can record very substantial changes in his or her lifetime. I have been struck by dramatic changes in the composition of a bird community on a small island in the Gulf of Finland during forty-six years, changes in the elevational distribution of dung beetles on a mountain slope in Borneo during thirty-five years, and a sudden shift in the lemming dynamics in Greenland at the turn of the century, apparently due to climate warming. Changes can be represented by numbers in tables and graphs, but the human mind is such that only what we have seen with our own eyes, heard with our own ears, and touched with our own fingers seems real. A cool summer makes people doubt climate change. At the same time, the human perception of time is so inadequate that unless you make an effort, you can miss the change. You become used to the altered environment so quickly that you do not realize that the world is changing at all. Researchers who are concerned about the loss of biodiversity and speak out about it are occasionally accused of partisanship. (Oddly enough, medical doctors who are concerned about public health are unlikely to be accused of partisanship.) Many discoveries about biodiversity and the ecological and evolutionary processes shaping it have been made on islands. Isolation and distinctness of islands have influenced the populations and communities inhabiting them, and these features have also affected researchers. Island populations are well-delimited targets for research; the island environment is often different enough to impose new selection pressures; the size of island populations is related to island area; and the exchange of genes and individuals with

Preface

xi

The six islands featured in this book.

other populations is affected by island isolation— all features that facilitate research. It is probable that the short visit that Charles Darwin made to the Galápagos Islands in September 1835, toward the end of his five-year voyage around the world, and the birds that he collected there helped him take the mental leap to the idea of natural selection. The equilibrium theory of island biogeography composed by Robert MacArthur and Edward O. Wilson was not based on any particular island, but on islands in general, and the result was a paradigm change in biogeography and ecology. Closer to home, my predecessor in the chair of ecology in the University of Helsinki, Olli Järvinen, biogeographer and conservation biologist, thought that Finnish population biologists are especially fortunate because of the huge number of islands in the Baltic Sea and in the many large lakes in Finland. Each of the six chapters in this book is launched with a short narrative of my personal experiences and, in most cases, research done on six islands, from a tiny islet in the Gulf of Finland to Borneo, Madagascar, and Greenland. The purpose of this book is not to describe the global distribution of biodiversity. There is no shortage of wonderful field guides, especially on birds, but also on many other groups of animals and plants. Leafing through the maps of species’ geographical ranges helps one understand the big picture of biodiversity around the planet. Naturally, the best way to become familiar with biodiversity locally is to take your field guides to the field. Neither does this book catalogue changes in the state of biodiversity, which is well done in many books, reports, and websites. My purpose is to present an overview of what biodiversity is, how it has evolved in the course of evolution, and how it changes at present; how we humans shape biodiversity by unintentionally helping other species expand their distributions and by converting their

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Preface

habitats; and why biodiversity is important, why we must protect it. These are big topics on which there is a vast literature. My goal is not to summarize all that knowledge, but rather to present it from the perspective of one working scientist. I hope that short stories of how research has been done will convey a glimpse of the excitement of doing research on biodiversity. There are many friends and colleagues whom I wish to thank for providing illustrations, material, and advice and for comments on particular sections of the text: Robert Angus, Tony Barnosky, Paulo Borges, Stan Boutin, Jukka Corander, Maria Dornelas, Steve Ellner, Mikael Fortelius, Marcos Baez Fumero, Eeva Furman, Nanna Fyhrquist, Olivier Gilg, Peter Grant, Tari Haahtela, Jorma Keskitalo, Ilpo Kojola, Janne Kotiaho, Bill Laurance, Marko Mutanen, Otso Ovaskainen, Camille Parmesan, Stuart Pimm, Juha Pöyry, Tomas Roslin, Marjo Saastamoinen, Ilik Saccheri, Dan Simberloff, Benoît Sittler, Olli Tahvonen, Chris Thomas, David Tilman, Tuuli Toivonen, Heidi Viljanen, and Chris Wheat. Juha Markola drew the illustrations that appear at the beginning of each chapter. Sami Ojanen, Jenni Hämäläinen, and Joann Hoy helped in many ways during the preparation of the manuscript, and Christie Henry and Gina Wadas from the University of Chicago Press assisted me greatly in turning the manuscript into this volume. I thank them all. Words are not sufficient to thank my wife, Eeva, and my children, Katri, Matti, and Eveliina, for supporting me during this difficult time after an exceptionally lucky life.

1

Biodiversity Species and Where They Live

Island Area Maximum elevation Age Time since isolation Current isolation Inhabitants Breeding birds Endemic birds Butterflies Flowering plants

Borneo 743,330 square kilometers 4,095 meters Varies from one part of the island to another; youngest area 5 million years 12,000 to 18,000 years 550 kilometers 18,590,000 420 species 37 species About 1,000 species 15,000 species

Expedition to Borneo

T

he airplane landed at the Bandar Seri Begawan airport in Brunei, on the north coast of Borneo, on March 22, 1978. I could hardly believe it. I had never been in the tropics, and now in Borneo, of all places! For the young ecologist this was a dream come true. I could have run after the first butterfly crossing the runway, but instead I had to walk with my expedition companions through passport control and customs. The rules and regulations may have changed since 1978, but in that year any male traveler entering the state of Brunei was expected to possess a feature that I lacked— short hair. 1

2

Chapter One

To their credit, the authorities offered me two options, either to have an instant hair cut or an instant departure from the country. I could have agreed to the former, but there was no need for it— a driver was waiting to take us from the airport across the border to the town of Miri in Sarawak, Malaysia, where the length of my hair was my own problem. From Miri we continued in a big fast boat along the Baram River to Marudi, where we boarded, a day later, a narrow longboat and spent ten more hours traveling up Baram and its tributary Tutoh, toward the mountain range that gradually took shape in the distance. Our destination was Gunung Mulu, a region of virgin forests on steep mountain slopes, 100 kilometers from the coast. The area was inhabited by nomadic Penan people in 1978 (figure 1.1). Today, the remaining Penans are settled, or have been settled, in a few villages. Gunung Mulu is a national park and a UNESCO World Heritage Site, famous for its caves, bats, and karst formations in the limestone mountains surrounding Gunung Mulu itself, a peak of sandstone towering above sea level. One reason for the exceptional biological diversity in the Gunung Mulu National Park is exceptional geological and topographical diversity. Indeed, an important facet of biodiversity is diversity of habitats and ecosystems, which set the living conditions for all the creatures inhabiting them, from microbes to plants and animals. For animals, plants and their communities are a big part of the living conditions. Cause and effect also work the other way around, especially when we consider long spans of time, as animals, plants, fungi, and microbes influence the way habitats and ecosystems change. The current atmosphere, especially the high concentration of oxygen (21% by volume), is the result of photosynthesis, started by cyanobacteria more than 2 billion years ago. Similarly, though less spectacularly, habitats and ecosystems were “engineered” by the ancestors of the species that now occupy them, which themselves keep the processes going. Our own species is the supreme engineer of the physical conditions on the planet, often, alas, to the detriment of many other species, which lose their prime habitat while our species converts it to something else, for instance, tropical forests to oilpalm plantations. Ecologists routinely use the terms habitat and ecosystem, but what do we actually mean by them? Habitat is the physical and biological conditions that can support, in principle, viable populations of a species. The conditions include the right kind of soil, the range of tolerable temperature and precipitation, food resources, and natural enemies. Different species tend to differ in their resource requirements and other needs; hence species differ in their

Fig. 1.1 Penan people lived in small family groups, constantly moving from one place to another without any permanent dwellings.

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Chapter One

habitats, at least in the fine details. In Gunung Mulu, as I was to discover, the limestone mountain Gunung Api and the sandstone mountain Gunung Mulu, though only kilometers apart, have very different kinds of plants and animals, most likely because the rocks and the soils are different. The forested slopes on the limestone and sandstone mountains represent different ecosystems, entities that consist of the physical environment as well as the community of all the organisms living in the area, plus all the interactions that take place between the species and their environment— a very complex system. Today, the word ecosystem is used by mobile-phone and other companies, which argue about whose ecosystem is most advanced and complete. Hijacking the term ecosystem for such usage may reflect an appreciation for the workings of real ecosystems, but I would prefer CEOs to use more imagination and other vocabulary. Talking about ecosystems around companies may lead people to think that real ecosystems are there only for the benefit of humans, and to value some ecosystems above others. People may start thinking that we should make natural ecosystems work better, and that manipulation of real ecosystems is not only possible but also desirable, comparable to companies arranging deals with their contractors. In reality, natural ecosystems have not been designed for any purpose, and tinkering with their components to enhance their performance (from a human perspective) is apt to lead to unexpected consequences. I return to these issues in later chapters, but for now I’ll just say that the task of predicting the dynamics of complex ecosystems with thousands of interacting species that may even evolve new features in response to our manipulation is simply beyond the capacity of today’s ecologists, and probably also beyond the capacity of tomorrow’s ecologists. In 1978 I was a member of the Royal Geographical Society Expedition from London to Gunung Mulu. During 15 months, more than 100 researchers spent time in Gunung Mulu, studying the habitats and their animal and plant inhabitants, or the biodiversity of Gunung Mulu, as we would say today. I became aware of Gunung Mulu in a pub in Oxford, where I overheard someone chatting about the upcoming expedition. I had started my doctoral studies in the autumn of 1976, supported by a fellowship from the Queen’s College, which I had been awarded in the third year of my undergraduate studies in Helsinki. I joined the Animal Ecology Research Group (AERG) without knowing anybody there, and without knowing what I would end up doing. There were no e-mails and no websites in those days,

Biodiversity: Species and Where They Live

5

of course— not even personal computers. The only computer at the Department of Zoology was a big machine that filled one small room. In the morning, and whenever some unexpected error had occurred, one Richard Dawkins entered the room and fed a big reel of paper tape to the guts of the machine to make it behave. After my arrival at Oxford, I talked to John Phillipson, the director of AERG, about possible doctoral projects. Phillipson was a pioneer in the measurement of the energetic content of animal populations, part of the broader effort to characterize the flow of energy and matter through populations and ecosystems. AERG and John Phillipson had replaced the Bureau of Animal Population and Charles Elton in the late 1960s. Elton is widely and properly credited for establishing the field of population ecology, and he was one reason that this young Finnish student wanted to go to Oxford. Elton had long been retired when I arrived, but he came to the office every now and then, and I had a chance to talk to him on a few occasions. Phillipson proposed that I start working on some old samples of soil mites that he had accumulated in a project that was part of the International Biological Program, a global initiative to kick-start ecosystem ecology in the 1960s. I panicked, but luckily rescue was at hand, by Malcolm Coe, a lecturer who had moved from Kenya to Oxford in the 1960s. Malcolm had worked on dung beetles, organisms that were familiar to me from my undergraduate studies in Finland and much preferable to soil mites. The decision was made that I would start work on the community of dung beetles in Wytham Woods near Oxford. This pleasing decision made me feel that I was following in the steps of Charles Elton, who pioneered much of population and community ecology through his long-term studies in Wytham Woods. Going to Gunung Mulu for two months in the spring of 1978 would be a distraction, but Malcolm understood that he could do little to stop me. Besides, I explained, very little was known about the ecology of dung beetles in tropical forests, I could produce some interesting results, and in any case I would be back in late spring to start fieldwork in Wytham Woods. The first days in the expedition base camp, a longhouse by the Tutoh River, surrounded by floodplain forest, were memorable (figure 1.2). On the way from England to Sarawak, my more experienced companions had explained in some detail the conditions that we should expect, with a particular emphasis on parasites and diseases— and leeches, with which the forests were teeming. There was plenty of time to mull over these matters, especially as we missed our flight at the Royal Air Force Brize Norton sta-

6

Chapter One

Fig. 1.2 Researchers at the expedition base camp in Gunung Mulu, Sarawak, in the spring of 1978. (Photo courtesy of Nigel de N. Winser.)

tion, north of Oxford. The Royal Air Force had agreed to take expedition members to Hong Kong in their weekly flights operated for their personnel. We had checked our bags in time and had then gone to have a cup of tea with a buddy’s aunt, who happened to live near the airport. We were careful to return in time, but that was our time; we did not realize that the Royal Air Force operated on GMT, one hour ahead of everyone else’s time. It was embarrassing to go back to the department in Oxford for another week, having just recovered from the farewell party the night before, but all these mishaps only increased my enthusiasm. Parasites and diseases were soon forgotten when I finally reached the jungle. And the leeches, yes, they were abundant in places, but you get used to them, just like you get used to mosquitoes in Finland. The first days in the forest showed that the student of dung beetles has an enormous advantage. Tropical forests harbor incredible numbers of insects, but researchers have to do an enormous amount of work to find out exactly how many there are. Yves Basset and no less than 101 colleagues spent nearly 25,000 trap days sampling a mere 0.5 hectare of tropical forest in Panama, using the full assortment of traps and sampling methods. The result: 6,144 species of insects in a sample of 129,494 individuals (Basset et al. 2012). In contrast, I was working on my own, helped by two young local men, and I had less than two months for my sampling. Nonetheless, at the end of my

Biodiversity: Species and Where They Live

7

study in Gunung Mulu, I could be rather confident that I had sampled a large fraction of all the dung beetle species that could be found there. This is how it was done. Take a small plastic cup and dig it into the ground so that the top is level with the ground; pour a little water into the cup; add a drop of liquid detergent to remove surface tension; take a piece of fish, wrap it in mesh, and hang it from a stick above the trap; leave it in the forest for two days and nights; and return to collect all the beetles that were attracted to the bait and fell into the trap. A single trap is not enough, of course, but it took us only half a day to set up 100 traps. I repeated trapping in many places in Gunung Mulu. Trapping for more than a few days at a particular site would have increased the numbers of beetles caught in the cups, but after the first few days, the species were mostly the same that had already been caught, which shows that dung beetles are easily attracted to traps. So the trick is, instead of crawling through the forest in search of them, letting them come to you! Using fish as a bait was also convenient. Most tropical forest dung beetles are attracted to any kind of decomposing animal matter, probably because severe competition for resources would make a high degree of specialization a real handicap. (I will say more below about the coexistence of many species in spite of their competition for shared resources.) Dung beetles’ appetite for dung and carrion may seem— how should I put it?— a less exciting spectacle than the spring migration of birds or the mating behavior of bears. But nobody can deny the significance of these little creatures for ecosystems, for cycling of nutrients, improving soils through their tunneling activities, and controlling populations of dung-breeding pestiferous flies. The numbers speak for themselves. In South Africa, 700 to 1,500 beetles colonized fresh cattle-dung pats in twenty-four hours (Bernon 1981), and 7,000 beetles representing no less than 120 species were counted from a single pile of elephant dung (Scholtz et al. 2009). I am happy to report that the record goes to my PhD supervisor, Malcolm Coe, who documented the incredible number of 16,000 dung beetles attracted to 1.5 liters of elephant dung in two hours in East Africa ( J. M. Anderson and Coe 1974)— after which there was nothing more to observe about that pile of dung. And it is not only eccentric researchers who know the importance of dung beetles. Many Australians do as well. There are no elephants, buffalo, antelopes, or other favorites of dung beetles in Australia, where the vast majority of native dung beetles have evolved to use the pellets of marsupials, the native dung producers. Today, Australia has some 30 million cattle and 100 million sheep, which produce, as a rough estimate, more than 1 million

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Chapter One

tons of dung every day. And what happens to that dung? The native dung beetles are ill prepared to do much; they are small-bodied and mostly occur in forests. They just cannot cope with the millions and millions of cattledung pats, a resource that their ancestors never encountered during their evolutionary history over tens of millions of years. In this situation, researchers initiated in the 1960s an extensive program to introduce dung beetles to Australia, apparently to good effect (more about this in chapter 4). My own fascination for dung beetles does not stem from their role in removing dung pats from pastures or in cycling nutrients, nor for any other reason that dung beetles might be considered useful to humans. I find dung beetles attractive because of biodiversity. I do not know many other communities of sizable animals that can be so easily attracted to a single spot in large numbers: hundreds or even thousands of beetles of different sizes and shapes, often of brilliant metallic colors. Admittedly, an even greater diversity of insects can be seen at night, especially in the tropics, in places where bright light has lured moths, beetles, stick insects, and others to the wall of a building or, even better, to a white bed sheet that you have hung out for the purpose. Without exception, people who see for the first time this congregation of literally hundreds of different kinds of insects—small and large, bright and dark, slow and fast—are surprised and fascinated. A knowledgeable entomologist can identify many species to the family level, but otherwise the species remain anonymous; not much is known about their biology. They arrive from the dark jungle as messengers of its riches. The assemblage of insects that is attracted to light in one place is just a small sample of the vast numbers of species in the forest— one would need to spend years sampling to see even a fraction of all the species. Dung beetles are different: their biology is well known, and they can be effectively attracted by bait, so that intensive sampling during a single week yields practically all the species that are present at a study site. As a researcher, I find dung beetles attractive because it is possible to address many fundamental questions about the ecology of populations and communities, and of biodiversity, by studying them. The number of beetles is often so huge that the resource is depleted in a short time. In other words, many species compete for the resource. So why doesn’t one or a few species replace the others? How can so many species coexist in spite of severe competition? I knew from lectures, textbooks, and scientific papers where the answers might lie. Tropical forest dung beetles use decomposing animal matter as their food resource, both dung and carcasses, but there is none-

Biodiversity: Species and Where They Live

9

theless room for specialization. Perhaps different forest types would have different species, though if they do, that would raise new questions as to why. I was in Gunung Mulu because I wanted to find out which species occurred in the lowlands and which species at higher elevations, and at exactly which elevations. Which species were attracted to the fish bait, and which species came only to primate dung (guess which primate), or some other type of dung? Which species were active in the day, and which species flew only at night? In brief, I was interested in describing the biodiversity of dung beetles in Gunung Mulu and how the different species differ in their habitat use, in resource requirements, and in any other way that I might find. This would go some way toward explaining how they could coexist in Gunung Mulu, though I realized that such a description would not suffice to predict why there were just so many species, not fewer, not more. My fellow expedition members were working on similar questions with their own favored groups of plants and animals. I will recount below what I discovered about dung beetles, and what others have found about the numbers of beetles and other insects in tropical forests. Studies on tropical forest beetles are instructive about biodiversity on Earth, because beetles make up a disproportionate fraction, roughly a quarter, of all the scientifically described species of animals and plants, and because there are many more species in tropical forests than in any other ecosystem. J. B. S. Haldane, a leading evolutionary biologist of his time (he died in 1964), famously replied to a clergyman who asked what could be inferred about the mind of the Creator from the works of his creation: “An inordinate fondness for beetles.” How Many Million Species? My work in Gunung Mulu made a small contribution toward answering a very basic question about biodiversity: How many species of animals, plants, and fungi exist on our planet? It may surprise many readers that the answer is not well known; all we have are rough estimates. Before examining what researchers have found out, let us ask another seemingly simple question: What is a species? Here is another surprise: biologists have not been able to come up with a clear-cut definition of species. The reason is not incompetence or lack of effort— the species concept has been fiercely debated for a long time. The reason there is no simple answer is evolution: species evolve all the time, and they all descend from a common ancestor. Therefore, if we had complete knowledge of the life of every individual that has lived on the

10

Chapter One

planet, we could place it in a huge family tree extending back in time over millennia and millennia. Examining this tree, it would be impossible to tell where one species ends and a “new” one begins, even if individuals in the beginning of the long chain of parents and their offspring were quite dissimilar from the present individuals. There are some exceptions: in some groups of plants, for instance, speciation, the appearance of a new species, may happen instantaneously, when two existing species hybridize and the offspring exceptionally retain all the chromosomes of both parents, leading to an increase in the number of chromosomes and the sudden emergence of a new species. But in general, considering all existing species, we should not be surprised to observe variation in terms of how different species are from each other, or indeed whether a population of individuals in some region composes a species of its own or not. Thinking of how evolution proceeds, it should not be surprising that different species are at different stages of becoming truly distinct species. I will say more about how species evolve in chapter 2, but let us consider here more practical issues. Delimiting and naming species, notwithstanding the difficulties, is of fundamental importance to biology and all its applications, and indeed it is the subject matter of a discipline of its own, taxonomy. If we treated biodiversity as an amorphous mass of individuals, without classifying them into species, we would not be able to ask and answer most of the questions that we are interested in. Our everyday experience also recognizes distinct species, though this is not a critical argument. For instance, consider the mammals that you are familiar with. You can name them, you can tell them apart, and you know something about their biology, which influences how you think about the species. You can communicate with others about these species, because other people delimit the species in the same way, based on the appearance of individuals. Professional biologists also rely on the physical appearance of individuals, called the phenotype, which mostly correlates well with what really matters, namely, the genotype, the genes that individuals possess. The common criterion to delimit sexually reproducing species is whether individuals routinely breed with each other in nature; if they do and produce viable offspring, they belong to the same species, according to the biological species concept; if not, they represent different species. One complication is that species that are biologically clearly distinct may nonetheless interbreed occasionally and produce viable offspring, which leads to transfer of genetic material from one species to another, as happened in the case of the Neanderthal and our own species some 50,000 years ago. Such

Biodiversity: Species and Where They Live

11

events of hybridization typically occur when species are still “young” and have not accumulated many genetic differences since they diverged from the common ancestor. If hybridization is very common, for instance, after distribution changes that brought species together, the two species may actually merge into one. But if hybridization is infrequent, for instance, because ecological differences between the species make interspecific mating uncommon, the two species may remain distinct and become ever more distinct in the course of time. Low levels of hybridization may even speed up evolutionary change because it brings additional genetic variation, the raw material of natural selection (chapter 2). Identifying species by their appearance works well for mammals, birds, fishes, and other vertebrates, for beetles and many other insects, and for most plants; but generally the smaller the organism, the simpler the body plan and the fewer visible features that can be used for identification. Consider nematodes, also known as roundworms; they are present and hugely abundant in all ecosystems, in lakes and oceans and on land, in the Arctic and in the tropics, and as parasites of plants and animals. Most nematodes are microscopically small, with a limited number of characters that can be used to differentiate between species. More than 20,000 species have been described so far, but researchers believe that 1 million species might exist. It is doubtful whether the true diversity of nematodes could ever be sorted out if we had to rely on their appearance only, especially because we humans find it easy to deal with just one kind of appearance, the visual appearance, whereas for other organisms it may be the olfactory, the acoustic, or some other feature that matters. Fortunately, one feature that is common to all living organisms, from bacteria to primates, can be used to identify species very effectively, namely, the hugely long macromolecule called DNA (deoxyribonucleic acid), which encodes the genetic information that serves as the blueprint of individual development and functioning in all organisms. Researchers can read the millions and millions of letters (called nucleotides) that make up DNA, which means that there is no practical limit to distinguishing any number of entities (species) if they differ in some of the letters, even if there are only four different letters. And they do differ. When cells multiply and DNA becomes replicated, errors (mutations) occur, one letter is transformed to another, and the mutated letter is passed on to subsequent generations. Some mutations are very harmful and are weeded out by natural selection, but other mutations make no real difference to the wellbeing and reproduction of the individual. In the long course of time, dif-

12

Chapter One

ferent branches of the family tree accumulate different mutations; in other words, they become systematically different. Individuals that belong to the same biological species have much the same mixture of genetic variation because they interbreed— these individuals are not assigned to distinct groups based on their genetic composition. In contrast, individuals of different species do make up distinct groups, because they do not regularly interbreed and therefore they accumulate different sets of mutations. Some parts of DNA (genes) have become modified by natural selection while the species adapted to their particular environments, but other parts of DNA are more or less neutral. These latter parts change in the course of time, but new mutations accumulate by random processes, without the influence of natural selection. This is convenient: the rate of accumulation of such mutations is relatively constant, and so the less similar that two individuals are in terms of these neutral DNA sequences, the more time has elapsed since they shared a common ancestor— and the less likely it is that they belong to the same species. These considerations have spawned a new approach to species identification, called DNA barcoding (Hebert et al. 2003). The idea is simple: select a part of DNA that is comparable in all species due to common ancestry, that is known to vary little among individuals of the same species, and that varies a lot between individuals belonging to different known species. It turns out that a single useful DNA barcode does not exist for all species, but researchers have selected one barcode for animals, two for plants, one for fungi, and one for bacteria. The animal barcode is a segment of about 650 nucleotides (the letters of DNA) of the mitochondrial gene cytochrome c oxidase subunit 1 (COI; figure 1.3). Mitochondria are cell organelles that are present in all eukaryote species (animals, plants, and fungi). Mitochondria are thought to have bacterial origin, in the distant past of evolutionary history, and they supply chemical energy to the cell and thereby sustain the metabolism of the organism. Mitochondria are usually inherited from the mother only, which is helpful, because it means that recombination, mixing of genetic material inherited from the two parents, is exceptional. Maternal inheritance guarantees that any changes in the COI sequence are passed on to the line of descendants. Let me give a practical example from the research of my former student Maaria Kankare, who worked on the parasitoid wasps of the Glanville fritillary (Melitaea cinxia) and its relatives. The Glanville fritillary is my favorite butterfly, which I have studied for twenty-five years (chapter 5). The female

Biodiversity: Species and Where They Live

13

Fig. 1.3 DNA barcodes for three closely related species of dung beetles from Madagascar, Nanos hanskii, N. punctatus, and N. manomboensis (the sequences are 661 base pairs long). The black and white lines represent alternative nucleotides. Notice that there are systematic differences between the three species in several places along the sequence, whereas the two individuals of each species are practically identical. (Figure prepared by Andreia Miraldo.)

wasps inject their eggs inside the host caterpillar, where the wasp larvae feed and develop, eventually killing the host and producing the next generation of wasps. The wasp Cotesia melitaearum was frequently reared from the caterpillars of the Glanville fritillary and the closely related heath fritillary. We were surprised to find big sequence differences in COI and other genes, so big that we had to conclude that the two butterfly species are parasitized by two different wasp species (Kankare et al. 2005), even if Mark Shaw, the foremost authority on these insects, could not find any consistent differences in their appearance. But the wasps knew better: in the experiments that Maaria conducted, female wasps did not parasitize caterpillars of the “wrong” host species. Maaria went on to show that the number of species in this genus of wasps in Europe and Asia is at least twice as large as previously thought, and many species that had been concluded to parasitize several host species are in fact completely specialized to use just one host species. Others have reported similar results. Barcoding parasitoid flies attacking caterpillars in Costa Rica, Smith et al. (2007) showed that what were previously considered to be 16 generalist species, each parasitizing many host species, represented not less than 73 mitochondrial lineages that were so different from each other that they could all be different species. Conventional taxonomy has missed large numbers of very similar-looking (called cryptic) species in many groups of animals and plants. DNA barcoding has remained controversial among researchers, many

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of whom are irritated by the grandiose claims made by the enthusiasts. It is true that variation in a single gene cannot offer all the information that is needed to reliably delineate all the species. As we will see in chapter 2, in many cases natural and sexual selection have produced very specific adaptations that affect only a small part of the genome but nonetheless effectively prevent interbreeding. Good understanding of the evolutionary history and the current status of species cannot be based on just a single gene. But such criticism misses the point. DNA barcoding is valuable because it allows fast screening of large numbers of individuals. Barcoding may reveal cases where current taxonomy has lumped cryptic species under a single name; it can be used to explore species diversity in poorly known groups of species, such as most tropical forest insects, and to identify species from tiny amounts of DNA. For instance, Schnell et al. (2012) have shown that blood recovered from the stomach of leeches is sufficient to identify the mammalian species that the blood-suckers had recently been feeding on. This clever discovery opens up an interesting technique to census rare mammals in leech-infested jungles. Or consider barcoding samples of caviar to find out its origin, especially whether it comes from illegal harvesting of threatened species. The dream is to have a handheld apparatus to do barcoding on the spot, which may become reality. Other researchers are already experimenting with methods to barcode mixed samples of hundreds or even thousands of individuals, to find out which species are present and even how abundant the different species are in the sample. I could not have even dreamed of such possibilities in 1978, when I returned from Gunung Mulu to Oxford with thousands of beetles. My study in Gunung Mulu came to an end in early May 1978. I had spent nearly two months trapping beetles in all the main forest types. The greatest effort went to working along the 25- kilometer trail from the expedition base camp in the lowlands to the summit of Gunung Mulu at 2,371 meters above sea level. Trapping was done at fifty-seven sites, equally spaced at increasing elevations. We moved from one forest camp to another while working our way toward the summit. My collections from Gunung Mulu consisted of 5,897 beetles, though I did not know this when I packed up my samples, preserved in ethanol in plastic tubes in the forest, with everything else that had dropped into the traps, including countless ants and termites. Back in Oxford, I spent several months sorting out the samples, first separating dung beetles from the rest (and cursing ants and termites), then sorting beetles into groups that I presumed were different species. I was not an expert on

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Borneo dung beetles, and I did not have a collection of previously identified species to which I could have compared my specimens. I contacted the experts, doctors Jan Krikken and Hans Huijbregts in Leiden, who agreed to identify the species in my samples as far as possible. Nearly a year passed before I finally had the results. My samples included sixty-six species, of which Krikken and Huijbregts could not identify twenty-three species— they were most likely undescribed, new species. Sixty-six species is naturally an underestimate, because surely I did not manage to find every rare species, even if dung beetles are exceptionally easy to trap. Some very similar-looking species may have escaped correct identification— no molecular methods were available in 1978. In any case the true number is likely to be less than 100. Other researchers have trapped dung beetles elsewhere in Borneo over many years; based on these results, we know that at least 150 species occur in Borneo as a whole. Dung beetles have been well sampled in many parts of the world, and the number of known species is more than 5,000. Again, the true number must be greater, but we can be rather confident that the true number is less than 10,000 species. Incidentally, this is also the number of bird species on Earth, which are very well known, though a few new birds are discovered every year, often aided by molecular genetic studies. Many dung beetles are similar to birds in producing only a few offspring in their lifetime, and in taking good care of them, which is unusual for insects. The extreme example is Kheper nigroaeneus, a large dung beetle that inhabits savannas in southern Africa. In this species, females rear just a single offspring in an underground nest in each breeding season. Beetles move dung, often in the form of well-shaped balls, to underground tunnels, where the female remains to guard the well-being of her offspring. Taking dung into underground tunnels avoids intense resource competition on the ground. Resource competition is also the likely explanation of why there not more species of dung beetles in local communities and on Earth in general. I would love to have a theory predicting how many species are able to coexist in the same community, and how this depends on the type of resources the species use. Unfortunately, I do not have such a theory, nor does anyone else; developing this theory has been the challenge for community ecologists for more than fifty years. Dung beetles make up a tiny fraction, roughly 1%, of the 400,000 known species of beetles, which make up about 40% of all known insect species and a quarter of all species of animals, plants, and fungi. In terms of species number, beetles rule the world! These numbers are for species that have

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been scientifically described: the true numbers, including species yet to be discovered, are much debated. It is astonishing that we may have a more accurate estimate of the number of stars in the Milky Way— 100 to 400 billion— than of the number of species on this planet. Many estimates have been presented, based on different types of data and arguments. In 1982 American entomologist Terry Erwin published a study of the numbers of beetle species in tropical forests. He noted that the majority of beetles and other insects in tropical forests are not found on the forest floor but in the canopy, which remained, for understandable reasons, poorly sampled. There are even a few dung beetles in the canopy, searching for monkey droppings on leaves; the beetle detaches the dropping and jumps down with it to breed on the ground. Erwin developed a new method for sampling. Using pulleys, he hoisted fumigation equipment up to the canopy, and sprayed the canopy with pyrethrine, a potent insecticide that knocks down beetles and other insects, which are collected with large sheets spread below the trees. Pyrethrine breaks down quickly and is not toxic to other animals. Erwin sprayed nineteen Luehea seemannii trees in Panama, and he collected the amazing number of 682 species of beetles. He then estimated the number of species on Earth in the following manner. He observed that there are about 50,000 species of trees in the tropics, an incredible number to Finns, who live in boreal forests with only a couple of tree species. In Gunung Mulu, researchers identified 780 tree species within an area of ten hectares, and a one-hectare plot in Ecuador had 942 vascular plant species, mostly trees ( J. B. Wilson et al. 2012). Assuming that L. seemannii is a representative species, and assuming that 20% of the beetle species that Erwin collected are specialized to use only L. seemannii, the number of specialist beetle species can be calculated as 50,000 × 0.2 × 682 = 6.82 million species. Assuming further that 80% of all species are herbivores (plant eaters), that 40% of all insect species are beetles, and that species living in the canopy of tropical forests represent a third of all species on Earth, Erwin arrived at the figure of 31 million species of animals and plants. To this figure one needs to add fungi and microbes, which likely amount to many more millions of species. These are huge numbers, and if correct, a huge amount of work remains to be done to catalogue life on Earth. So far, scientists have described only 1.7 million species, though even this figure is not certain, as an unknown number of species have mistakenly been described twice or more. At present, 15,000 to 20,000 new species are described per year. With this rate, and assuming that Erwin’s estimate is correct, it would take more than 1,000

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years to describe all the species— assuming that all these species will be around for 1,000 years to be discovered, which will not happen (chapter 3). Erwins’s study attracted lots of attention. Studies based on other types of data and arguments have challenged Erwin’s calculations, and the current consensus is that Erwin’s estimates are far too high. Some of the assumptions that he made are likely to be erroneous; for instance, the fraction of strictly host-specialist herbivorous beetles is likely to be less than 20%. Erwin’s calculations imply that the vast majority of species sampled in the tropics are new to science, but this is not the case. In my sample of dung beetles, only one-third of the species appeared to be new, undescribed species. Mora et al. (2011) took another approach to predicting the number of species on Earth. They showed that the assignment of species to the higher taxonomic units— phyla, classes, orders, families, and genera— follows a consistent and predictable pattern, from which the total number of species can be estimated on the assumption that the same pattern extends to species. With this approach, they estimated that there are altogether 8.7 million species, of which 2.2 million are marine species. Costello et al. (2013) used other data and methods to arrive at an estimate of 5 million species. The confidence limits of these estimates are wide, however, highlighting the fact that we do not really know the answer to this very basic question— with how many other species do we share this planet? Our knowledge is really good only for mammals and birds, of which there are 5,500 and 10,000 species, respectively. When we turn to microbes— bacteria, archaea, viruses, and various small-sized unicellular eukaryotic organisms— our knowledge about species richness is rudimentary, but here at least there are good reasons for our ignorance. Some say that viruses are not living organisms at all, because they can reproduce only inside the living cells of other organisms. What a species is can be a tricky question in the case of animals and plants, and researchers agree even less about how bacterial species should be defined. One consideration is that it may be insufficient to examine just genetic diversity and differentiation; one should also examine the ecology of the candidate species (Fraser et al. 2009). The main reason for the difficulties is that bacteria have various mechanisms other than reproduction to transfer genetic material, and hence there is extensive mixing of genetic material among different lineages (“species”) of bacteria. Moreover, such horizontal gene transfer is not restricted to closely related species. In a study of more than 2,000 bacterial genomes, Smillie et al. (2011) found that transfer of genes was influenced more by ecology than by genetic relatedness, that is, common ancestry. In

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other words, bacteria that coexist in the same habitat—for instance, some part of the human body—are most likely to transfer genes among themselves. This makes sense, because bacteria living in the same habitat have the best chance to meet and interact, but the finding underscores the fact that genetic material becomes very widely mixed across bacteria. Horizontal gene transfer speeds up bacterial evolution, such as the evolution of antibiotic resistance: one bacterial lineage acquires resistance, which later transfers to other lineages. For instance, studies of Streptococcus pneumoniae, a serious human respiratory pathogen, indicate that rapid evolution of multidrug resistance is based on horizontal gene transfer rather than on independent mutations (Chewapreecha et al. 2014). Moreover, year-to-year changes in antibiotic consumption, which imposes strong selection on bacteria, are reflected in changes in bacterial recombination rate, which means that when selection pressure is strong, the spread of resistant elements becomes especially rapid. The standard way of identifying bacteria is genetic barcoding, using a gene sequence that encodes ribosomal RNA, most commonly a part of the gene called 16S rRNA. The principle is the same as using the gene COI to barcode animals. One advantage of 16S rRNA as the barcode for bacteria is that it is little affected by horizontal gene transfer; it can be assumed to reflect genuine evolutionary lineages. Species are defined by requiring that the sequence similarity of bacteria is greater than some specific (but arbitrary) value, most often 97%. The entities thus defined are often called operational taxonomic units, OTUs, rather than species or genera. This is a rough approach to classifying bacteria. In many well-studied cases, in which other information points to distinct bacterial lineages, or species, the similarity of the 16S rRNA sequence is greater than 97%; hence using this limit most likely leads to an underestimate of the true number of species. For the time being, however, barcoding the 16S rRNA gene is the most practical method to tackle bacterial diversity, not least because a huge reference database now exists for this gene, allowing researchers to find a name for many sequences that they recovered from their samples. Large samples taken from soil, ocean water, sewage, plant surface, human gut, and so forth typically include up to 10,000 bacterial species in one place. Comparing species richness in samples of the same size, including the same number of bacterial cells, shows differences between different environments, with soils typically having very high bacterial diversity. Extending estimates of local diversity to the global scale remains a challenge. One survey based on more than 500 samples from different parts of

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the world’s oceans revealed about 100,000 bacterial species (Zinger et al. 2011), and another large collection of samples included about 150,000 eukaryotic OTUs, from tiny protists to very small animals (de Vargas et al. 2015). What is probably more important than counting bacterial species, which is problematic, is the diversity of their genes and hence the diversity of metabolic functions. Data from 243 ocean samples amounting to 7.2 terabases of metagenomic data yielded more than 40 million gene sequences from viruses, bacteria, archaea, and tiny planktonic eukaryotic organisms (Sunagawa et al. 2015). Bacteria have been evolving for more than 3 billion years, roughly 10,000 times longer than our own species, so it should come as no surprise that they have accumulated incredible genetic diversity. The bacteria that live in our bodies make up a huge community with several thousand species and altogether 100 times more bacterial genes than our own genes. No wonder that our well-being is closely linked with the functioning of this microbiome (chapter 6). The total number of bacterial genes is not known, but metagenomic studies, which aim to sequence all bacterial genes from environmental samples, indicate practically unlimited diversity: the more samples you sequence, the more genes you find. Whether the number of bacterial genes approaches the number of stars in the Milky Way remains a question for the future. Ecosystems in the Past 500 Million Years What might ecosystems have looked like 100,000 years ago, before any human influence, or when the world was ruled by dinosaurs, or even earlier, when the first vertebrate animals crawled onto land, 375 million years ago (mya)? We can never have accurate answers to these questions, but with meticulous studies of the evidence that can be gathered from fossils, combined with increasingly sophisticated understanding of biology, geology, geochemistry, and atmospheric and other natural sciences, experts have arrived at surprisingly detailed descriptions of what the world looked like in the past (Behrensmeyer et al. 1992). Learning about dramatic changes that have occurred during the geological history of our planet may tempt some to belittle the present global environmental changes: our inadequate perception of time makes it hard to understand how fast the world around us is changing right now, and how long the past episodes of change actually took to unfold. We grasp changes that occur in a span of years, but it is very hard to appreciate the real difference between thousands of years and millions of

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years. Knowing about the distant past will not give us a recipe for solving the present environmental problems, but if nothing else it is thrilling to contemplate landscapes that no human has seen. Although there has been life on Earth for 3.7 billion years, for more than 3 billion years ecosystems were structurally simple, bacterial mats covering shallow seabeds. Early life is thought to have depended on hydrothermal vents for energy and chemical elements. The evolution of oxygen-producing photosynthesis around 2 billion years ago could be ranked as the most significant evolutionary innovation ever, leading to gradual accumulation of free oxygen in the atmosphere and thereby making the planet fit for complex life. At the beginning of the Cambrian (541 mya), burrowing animals started to break down the bacterial mats in the sea, facilitating the circulation of water and oxygen below the mats and thus making the upper layers of the seafloor habitable for more kinds of animals. Such “ecological engineering” of the seafloor ecosystems by burrowing animals may be one reason for the Cambrian explosion, the rapid diversification and evolution of new types of animals within a geologically short period of time, perhaps only 20 million years. The Cambrian could well be called the period of innovations: evolution was fast and produced nearly all modern animal phyla from a single common ancestor. A phylum is the highest level in the classification of different kingdoms, such as animals and plants, defined by the fundamental features of the body plan. Arthropods, mollusks, and chordates are examples of phyla; we mammals belong to vertebrates, which is a subphylum of chordates. Species richness accumulated rapidly during and after the Cambrian, and species richness of animals in the sea has remained relatively constant ever since, for the past 500 million years (figure 1.4A), especially in comparison with biodiversity on land (figure 1.4B). Though the overall number of genera and families of marine life has remained relatively constant, however, the numerically dominant groups have changed over time. Filterfeeding brachiopods, or lampshells, which look like bivalve mollusks but are entirely unrelated, were hugely common and diverse reef builders for 200 million years after the Cambrian. More than 10,000 fossil species have been described, which must be a considerable underestimate of the true number of species, whereas only 300 species exist today. When brachiopod diversity waned rapidly 250 mya, in the third mass extinction at the end of the Permian, other groups of animals took their place, including bivalve mollusks, sea slugs, and sea snails. Life evolved in the sea, and conquering dry land was a huge challenge.

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Fig. 1.4 A, diversity of marine animals in the past 500 million years, during the Phanerozoic eon. The results are based on fossil records that have been corrected for unequal sample sizes (data from Alroy 2010). B, diversity of insects in the past 500 million years. Insects are so diverse compared with other animals and plants that this graph also gives an approximation of overall diversity on land. (Data from Grimaldi and Engel 2005.)

The first steps were taken in the Ordovician, around 450 mya, in the early Paleozoic, meaning “ancient life.” At that time, the world looked very different from what we see today. The northern landmasses formed one continent, called Laurasia, separated by sea from the greater southern continent, Gondwana. While the Cambrian explosion was an explosion of biodiversity in sea, land ecosystems were composed of simple microbial soil crusts, and the more complex life-forms were represented by browsing mollusks. Landscapes were inhospitable, dry and rocky, with no deep soils and without any vegetation. In the late Silurian, around 430 to 420 mya, jawless and jawed fishes proliferated in the seas, along with many other marine creatures, while on land vascular plants made their first appearance, such as the strange-looking rhyniophytes, simple sticklike, rootless, and leafless plants (DiMichele and Hook 1992). The primitive plants were probably confined to floodplains by rivers (Edward and Fanning 1985). Nonetheless, minimal terrestrial ecosystems were in place, with primary producers, decomposers (fungi), secondary consumers (microarthropods), and predatory animals. Diversification of vascular plants accelerated in the early Devonian around 400 mya, and though plants were still mostly small and may have formed local single-species patches, some of them reached at least two meters in height. Plant species diversity was low, as far as can be judged from the limited fossil record, ten to fifteen genera with a small number of species accounting for most of the diversity (Niklas et al. 1985). By the late Devonian, real forests appeared, represented by the fern Rhacophyton in peat swamps and Archaeopteris species on better-drained soils. Some of these plants were

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large, with stem diameters up to one meter (DiMichele and Hook 1992). In the next 50 million years, by the early Carboniferous (350 mya), plant evolution produced forests that were structurally not so different from present forests. A noteworthy feature of evolution on land is that plant communities became similar to their modern counterparts much earlier than animal communities; the development of terrestrial ecosystems was driven by plant evolution. In the early Carboniferous, there were herbivorous insects, but generally decomposers continued to form the major animal component of ecosystems. Thus plant production was transferred directly to decomposers, and herbivorous animals and their predators played a minor role in ecosystem functioning. This is a big difference from modern ecosystems on land. In the late Carboniferous, the continents moved together and formed a single supercontinent, Pangaea. Diversity of plants and plant communities increased, as did the complexity and spatial heterogeneity of ecosystems and landscapes in general. In this geological epoch, peat formation peaked and produced the coal deposits that we humans are now exploiting. Food webs were still dominated by plants and detritivorous animals (species using decomposing plant and animal matter), which facilitated peat formation when conditions were unfavorable for decomposition. The great evolutionary innovation in animals of the time was the egg of amniotes (comprising reptiles, birds, and mammals), which allowed reproduction without desiccation on land. The amniote egg paved the way for the evolution of tetrapods, four-limbed vertebrates, on dry land. Vertebrates were initially represented by insectivorous and carnivorous species; this situation started to change only in the Permian (300–250 mya), with the appearance of truly herbivorous tetrapods. In the Permian, plants invaded well-drained and seasonally dry habitats and formed new communities outside wetlands. At the global level, differentiation of the vegetation on different parts of Pangaea reached a higher level than before. The “ancient life,” the Paleozoic era, came to an end 252 mya. The causes are debated, and there were possibly several causes, including massive volcanism. In any case, the result was a calamity, by far the greatest mass extinction ever, with an estimated 95% loss of species in shallow-water marine faunas and 70% loss of vertebrates on land (D. H. Erwin 2006). Global average temperature was 10 degrees Celsius higher than today, perhaps the result of a runaway greenhouse effect. Ocean surface temperatures may have reached 40 degrees Celsius, too much for most plants and animals, especially when combined with low oxygen levels.

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The end of the Permian was a veritable catastrophe for life on Earth, but even so a fraction of biodiversity survived, to start the “middle life,” the Mesozoic era, often called the age of reptiles. The recovery did not restore biodiversity as it was before the Permian devastation, but something completely new was created: evolution advanced in entirely new directions. For the first time, species richness and dominance of large herbivorous animals started to increase with the appearance of prosauropod dinosaurs, which were facultative bipedals, reaching up to four meters while standing on the hind feet to eat tall vegetation. The evolution of prosauropods had great ecological and evolutionary consequences, as plants were now exposed to vertebrate herbivory over more of their life cycle (Wing and Sues 1992). The forest vegetation included primitive conifers and Ginkgoales, of which Ginkgo biloba has survived in China. At the end of the Triassic, 201 mya, there was another mass extinction, though nothing like the one at the end of the Permian, marked by the extinction of many groups of large-bodied reptiles, amphibians, and dinosaurs, and clearing the stage for the Jurassic (200 to 150 mya), the period of the largest terrestrial herbivores of all times, sauropods, which could browse up to ten meters high and weighed more than fifty tons. The body mass of sauropod species continued to increase during their evolution and reached the maximum in the Cretaceous. There has been some debate as to how the Jurassic vegetation could have supported the supposedly high population density of dinosaur-dominated herbivore communities. My PhD supervisor Malcolm Coe and his colleagues (Coe et al. 1987) calculated that the standing herbivore biomass at a well-studied site in Montana was twenty times greater than the current large herbivore biomass in Amboseli National Park, Kenya. However, these calculations involve many unknowns and uncertainties (Wing and Sues 1992). Productivity of Jurassic vegetation is likely to have been low, as it comprised woody gymnosperms, including species in the present conifer families Araucariaceae, Pinaceae, Taxaceae, and Podocarpaceae. The true population density of dinosaurs will remain unknown forever, but their diversity is becoming better known with the constant accumulation of new fossils. It has been estimated that the total number of nonavian dinosaurs that ever lived is nearly 2,000 genera (Wang and Dodson 2006), which means that the number of species is probably on the order of 10,000. The supercontinent Pangaea started to break into what would become the continents as we know them, and this process continued through the

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Jurassic. Nonetheless, barriers to migration were still limited, and many taxa had a cosmopolitan distribution. The global climate was warm, as it was during the entire Mesozoic, and subtropical climates extended as far north as latitude 60° north, the latitude of my hometown, Helsinki. The Jurassic was followed by the Cretaceous (145–66 mya), the period when flowering plants (angiosperms) made their appearance and subsequently radiated explosively to become the dominant element of forest vegetation (figure 1.5) toward the end of the Cretaceous (chapter 2). Browsing by herbivorous dinosaurs may have favored fast-growing angiosperms, and it has been suggested that dinosaurs and angiosperms were engaged in diffuse coevolution (Bakker 1978), speeding up each other’s evolution. In chapter 2, we see that coevolution between angiosperms and pollinating insects, and between angiosperms and herbivorous insects, may have similarly promoted rapid evolution of angiosperms. The Cretaceous ended, and the “new life,” the Cenozoic era, was started by another devastating event 66 mya, which had drastic consequences for the biota across the American continent and beyond. In the fossil record, the event is seen as the K/Pg (Cretaceous-Paleogene) boundary (formerly called the K/T boundary, T for Tertiary). The current consensus strongly supports what was first a wild idea by Luis Alvarez and his colleagues (Alvarez et al. 1980), namely that the K/Pg boundary is the result of the impact of a massive meteorite or asteroid at the northern end of the Yucatán Peninsula. It has been calculated that the impact had the energy of approximately 100 trillion tons of TNT, about 2 million times greater than the most powerful thermonuclear bomb ever tested. In North America, a layer of several centimeters above the K/Pg boundary contains just a few kinds of fern spores, while angiosperm pollen is completely absent (Wing and Sues 1992). Angiosperms recovered to become even more dominant than at the end of the Cretaceous, but the dinosaurs did not. The sudden burst of mammalian evolution after the K/Pg boundary, following 150 million years during which mammals were insignificant members of communities and ecosystems, is almost certainly related to the ecological opportunities created by the disappearance of dinosaurs. For the second half of the Cenozoic era, representing the past 34 million years, the picture becomes much clearer. There is rich fossil material with good temporal and spatial resolution; the species have mostly modern equivalents, which helps interpretation; and the geography of the world has been broadly the same as today, though large-scale changes in sea level asso-

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Fig. 1.5 An artist’s view of Cretaceous forests. (From © 2015 Miles Kelly / fotoLibra.)

ciated with glacial periods in the past 2.5 million years have created and disrupted land connections, which has affected migrations of terrestrial plants and animals. For most of the late Cenozoic, forests dominated Earth’s ecosystems, but toward the present, open vegetation types— savanna, steppe, tundra, and desert— have expanded. For instance, in Africa open woodlands, savannas, and grasslands have become more common in the past 15 million years (Potts and Behrensmeyer 1992). Expansion of open vegetation has been attributed to declining mean annual temperatures at high latitudes,

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increasing mean temperatures at low latitudes, and decreasing summer rainfall at mid-latitudes (Wolfe 1985), ultimately due to the formation of massive mountain ranges: the higher Himalayas, the Tibetan plateau, and the mountain ranges in western North America have had a long-term cooling and drying effect at a continental scale over the past 10 million years (Ruddiman and Kutzbach 1989). The Pleistocene epoch, from 2.588 mya until the beginning of the Holocene epoch, 11,700 years ago, was characterized by great climatic variation and consequent large-scale shifts in the distribution of species (chapter 3). The plant communities have been in constant flux, with new combinations of species coming together to form novel but geologically short-lasting species communities (Huntley and Webb 1989). The biotic dynamics have been in a persistent transient state dominated by delays— delays in the migration of species in response to changing climate, delays in community assembly due to long-term successional changes and soil formation, and delays due to evolutionary responses of populations to changing environments. In the Holocene, one omnivorous species, Homo sapiens, has had a dramatic impact on Earth’s ecosystems. Croplands and pastures now cover a third of Earth’s land surface and have practically replaced all other ecosystems in many parts of the world where the land is productive. It is only because we are so familiar with the sight of vast expanses of cornfields and grasslands without any large herbivores that we are not struck by the sweeping transformation of ecosystems. Humans have caused the large-scale demise of large-bodied mammals in the late Pleistocene (chapter 3). The human-caused change in the structure of Earth’s ecosystems has been compared to the change in the Permian, when evolutionary radiations of herbivorous animals revolutionized the functioning of ecosystems, produced complex food webs, and replaced the ancient ecosystems based on plants and decomposers (Potts and Behrensmeyer 1992). What are the general trends in the terrestrial ecosystems over the past 500 million years? One trend is dramatic increase in ecosystem complexity from microbial soil crusts to forests, and a continuous increase in biodiversity, further accelerated in the past 200 million years by rapid evolution of flowering plants and insects. The numerically dominant groups of vertebrates have changed, from amphibians in the Paleozoic to dinosaurs in the Mesozoic and to mammals in the Cenozoic. In terms of the trophic position of animals, the first to evolve were decomposers and predators, while herbivores appeared much later. This means that though massive forests have

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existed for 350 million years, the animal communities in these forests were originally very different from the present ones. Global temperature has fluctuated between 5 degrees Celsius below the current average temperature during the glacial maxima, most recently 20,000 years ago, and 12–14 degrees Celsius above the current average temperature, most recently 50 mya. Since then, average temperature has declined until the very recent global warming. Depending on how much the average global temperature increases in this century, the world will return to the temperature regime that last prevailed 3 to 5 mya, if the increase is 2 degrees Celsius, or to the regime that last prevailed 20 to 30 mya, if the increase is 6 degrees Celsius. The speed of change is phenomenal, 100,000 times faster on average than the rate of cooling in the past 50 million years on average. This very high rate of change is the reason that we need to be concerned about climate warming. Endless Variety of Habitats Describing the current habitats and ecosystems on Earth poses the opposite problem to what we have when considering the past: overabundance of information. The big picture, however, is clear and well summarized by the main land-cover types. Out of the total land area of 149 million square kilometers on Earth, 13% is croplands, 31% is grasslands/herbaceous/sparse vegetation, 27% is forested land, 15% is bare soil, 9% is snow and ice, 2% is water bodies/mangroves, and 3% is urban areas (Latham et al. 2014). Most of the grasslands/herbaceous/sparse vegetation land is grazed, and hence the share of agricultural land, including croplands and pastures, amounts to more than one-third of the total land area. The amount of land that is not yet used for agriculture but would be suitable for it, excluding forested, protected, and densely populated areas, is only 3% of the ice-free land area— so close is humanity to the planetary carrying capacity in terms of the land area used for food production, assuming that we do not cut down the forests, which would have many detrimental consequences. The long-term human impact on ecosystems is illustrated by a comparison of the main ecosystems 10,000 years ago, at the time of the Neolithic revolution, and at present. The estimated forest cover 10,000 years ago was about 50% of the land area, whereas today forests cover roughly half of their original extent. Moreover, of the remaining forests, only about half again have been classified as “relatively undisturbed large, intact natural forest ecosystems” (World Resources Institute 2000), and of them, only half have

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been classified as not threatened. Therefore, large areas of natural forest ecosystems that are not threatened have been reduced from around 70 million square kilometers 10,000 years ago to less than 10 million square kilometers today. The vast majority of the remaining extensive forests are boreal forests in Russia and North America and tropical forests in South America. The great reduction in the area of forests in the past 10,000 years is balanced by an equally dramatic increase in the area of agricultural land, though it is not the case that only forests have been transformed to croplands and pastures. The area of grasslands and other open vegetation has not changed greatly in the past 10,000 years, but previous grasslands have been turned into croplands, while much of previous forest is now various types of grasslands. The freshwater ecosystems— rivers, lakes, and wetlands— occupy about 1% of Earth’s surface. The human impact has been great: 60% of the world’s largest 227 rivers are strongly or moderately fragmented by dams and canals (World Resources Institute 2000), and half of the wetlands were lost in the twentieth century (Myers 1997). The coastal areas are defined as extending from the intertidal and subtidal areas above the continental shelf to the adjacent land as far as 100 kilometers from the coast. The coastal areas are a mixture of many kinds of habitats, and they are greatly affected by humans, as nearly 40% of the global human population lives within 100 kilometers of the coastline (World Resources Institute 2000). Two important habitat types of coastal areas are mangroves and coral reefs. Mangroves cover about one-quarter of tropical coastlines. Losses have been great, and it is estimated that about half the world’s mangrove forests have already been destroyed (Kelleher et al. 1995). Coral reef degradation (bleaching) has become a serious problem that is related to elevated seawater temperatures due to global warming. Coral reefs are the marine equivalent of tropical rain forests in terms of biodiversity; a quarter of marine species are associated with coral reefs. For many purposes, not least for conservation of biodiversity and management of populations and habitats, the above classification of land-cover types is far too simple. As an example of more refined classifications, the Habitats Directive of the European Union (Interpretation Manual 1999) describes a hierarchical classification of 198 natural habitat types. The toplevel categories include coastal and halophytic habitats, coastal sand dunes and inland dunes, freshwater habitats, temperate heath and scrub, sclerophyllous scrub (matorral), natural and semi-natural grassland formations,

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raised bogs and mires and fens, rocky habitats and caves, and forests. Each main category is further divided into subtypes; for instance, forests include boreal forests, temperate forests, Mediterranean deciduous forests, Mediterranean sclerophyllous forests, temperate mountainous coniferous forests, and Mediterranean and Macaronesian mountainous coniferous forests. And to consider the boreal forests, they are further divided into eight categories. Such classifications are like the classifications of species into genera, families, and so forth, though the underlying processes that have created the types are entirely different. Both classifications have their problems, as it is often difficult to assign particular populations or pieces of land to a species and a habitat type, but nonetheless the classifications capture important features of the natural world and are absolutely needed for communication, for organizing our knowledge, and for using that knowledge in practice. Different habitats have their own characteristic species of fungi, plants, and animals, but if we want to understand exactly where, and why, particular species are present, and where they are absent, we need to dig into further details about the habitat requirements of these species; generic classifications of habitat types are not sufficient. Species differ greatly in terms of how specialized they are in their habitat selection. Some species are extreme habitat generalists, inhabiting many broad categories. Our own species is a good example; our success is enhanced by our capacity to adapt to almost any kind of environment with the help of technology. The brown rat (Rattus norvegicus) has been equally successful without any technology, thanks to its superb ability to take advantage of the opportunities that we provide in cities and other built environments. Many invasive species are habitat generalists, which goes a long way toward explaining why they are able to spread and flourish (chapter 4). In contrast, most animal and plant species are more or less specialized in their habitat selection, and many are extreme habitat specialists. Consider the beetle Pytho kolwensis, which lives in boreal forests across Eurasia, from Siberia to Europe, but not in just any kind of boreal forest. The habitat of this beetle is like the matryoshka, a Russian doll: a series of environmental delimitations narrow down in ever greater detail the actual habitat where the beetle lives and reproduces. In this case the series of refinements goes like this: boreal forest; spruce-dominated boreal forest; spruce mire forest with high temporal continuity of downed logs; a downed spruce log with the base above the ground; a particular stage in the decay succession of phloem under the detaching bark (the larvae feed on phloem).

30

Chapter One

While starting to ponder all the reasons that a particular species occurs in a particular habitat, we quickly realize that the reasons are practically as many as there are species. Variation in habitat quality can be very subtle to a human observer. A classic example relates to the disappearance in 1979 of the large blue butterfly (Maculinea arion) from the United Kingdom ( J. A. Thomas 1980), which vividly illustrates both the problem of finding out exactly what the habitat of a species is and the race against time for ecologists trying to learn more before it’s too late for managers to respond. Local populations of the large blue had been disappearing from seemingly suitable grasslands ever since the nineteenth century. In the last phase of the eventual decline to extinction in the United Kingdom, the large blue faded from some thirty local populations and an estimated 100,000 butterflies in the mid-1950s, to just one population with 250 adult butterflies in the early 1970s. The large blue plummeted to extinction in spite of substantial conservation effort, largely because for fifty years conservation projects were based on erroneous information about the habitat requirements and the biology of the species. By the time Jeremy Thomas (1980, 1995) had documented the causes of most extinctions, it was too late— a series of four years of exceptionally unfavorable weather finished off the last population. Thomas found that the caterpillars are obligatory predators of the larvae of just one species of ant (Myrmica sabuleti), a species that is largely restricted to grasslands on warm southfacing slopes with turf height less than three centimeters. Lack of grazing at these sites allowed the vegetation to grow higher, which essentially made the habitat unsuitable for the butterfly. Additionally, Thomas showed that in order for the caterpillars to enter ant nests during the latter stage of their development, flowering thyme plants, the host plant of young caterpillars, had to be located within two meters of ant nests. The bottom line is that it is often difficult to arrive at a truly mechanistic understanding of the habitat requirements of a species without conducting detailed and time- consuming empirical studies. Notice also that interactions with other species are critically important in determining the suitability of the habitat; plants essentially delineate the habitat for many animals. Fortunately, not every species is as picky as the large blue butterfly in its habitat selection, and for many species we already have sufficient knowledge for conservation and management, even if the knowledge is not complete. The butterfly example highlights the overwhelming importance of habitat as the most significant concept for the management and conserva-

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tion of populations and species; sufficient amount of appropriate habitat is the most fundamental necessary condition for their survival. Conversely, loss of habitat is the single most important reason why innumerable populations and species have become threatened and why many of them are already extinct. I will expand on this topic in chapter 5. Exactly how particular habitats are defined can be important in the conflict between conservation and other land uses. Simply “redefining” a particular habitat, such as old-growth forest, may lead to very different assessment of the conservation status of that habitat, with significant implications for management. One distinction that needs to be made is between macrohabitats and microhabitats. Macrohabitats cover substantial areas of space and have complex structure, such as forests, meadows, wetlands, and so forth. Large-bodied species adapt to and use different macrohabitats in the sense that we humans (large-bodied mammals) tend to define habitats. Microhabitats are what matters for many small-bodied species and are embedded in appropriate macrohabitats. Microhabitats are small units such as heaps of dung, corpses of dead animals, decaying tree trunks, and so forth, which provide both shelter and food resources for their inhabitants. Many small-bodied species are entirely dependent on particular microhabitats, such as the beetle Pytho kol­ wensis that I mentioned above. Microhabitats are very significant for the overall biodiversity in many macrohabitats. Coarse woody debris—consisting of snags, decaying logs, and substantial branches—is a very abundant microhabitat in natural forests, with dead-wood volume on the order of 100 cubic meters per hectare in boreal forests (Siitonen 2001) and from 100 to 200 cubic meters per hectare in some tropical forests (Keller et al. 2004). In boreal forests in Finland, about a quarter of the 20,000 forest-inhabiting species of fungi, plants, and animals (mostly insects) live in or depend on the dead-wood microhabitat. Without these species, forest ecosystems could hardly function as they do; circulation of nutrients would greatly slow down. That dead wood should be such a hot spot of biodiversity is not surprising in view of its enormous quantity in forests for more than 350 million years, since the early Carboniferous. William Hamilton (1978), distinguished British evolutionary biologist, suggested that the dead-wood microhabitat has played a special role in the evolution of insects. Many evolutionary novelties have appeared several times in dead-wood-associated (saproxylic) insects, including wing polymorphism, sex dimorphism, male haploidy, and social life (in termites and ants). Unlike carrion, dung, and mushrooms, which are consumed fast and

32

Chapter One

usually remain available only for one insect generation, large logs may support populations of small organisms for tens or even hundreds of generations. Eventually, however, even the largest logs decay away, and successful lineages have to disperse and locate another place to breed. But it is exactly this combination of periods of local reproduction and periods of migration and intermixing that presents opportunities for evolution to experiment and innovate. Some microhabitats, such as springs, are extremely stable and often harbor very persistent populations. One can even extend the concept of microhabitat to host individuals for parasites. Like dung and carrion, and large decaying logs, which provide shelter and resources for their inhabitants, host individuals present the same benefits to parasites and to the hugely diverse communities of microbes that inhabit all animals, human beings included. Three Patterns in the Distribution of Biodiversity on Earth Biodiversity is the defining feature of our planet. There is life everywhere, from bedrock several kilometers deep to the upper atmosphere, from thermal vents and hot springs to the reader’s stomach and eyeball. But ubiquitous as biodiversity is, it is not evenly distributed across the globe. Researchers have delimited biodiversity hot spots on Earth, areas where species richness is particularly high and where there is a disproportionate number of endemic species, species that do not occur anywhere else. In a pioneering study, British environmentalist Norman Myers and his colleagues (2000) identified twenty-five biodiversity hot spots, of which Sundaland, including Borneo, and Madagascar are among the eight “hottest hot spots.” The primary criterion for hot spots in their scheme is that the region contains at least 1,500 endemic vascular plant species (Sundaland has 15,000 such species, Madagascar nearly 10,000). The second criterion concerns the threat: the region has lost at least 70% of the primary habitat for the endemic species. (Sundaland and Madagascar have about 10% of their primary vegetation left.) Hot spots typically occur where ecosystem productivity is high and conditions are generally favorable for life. The remaining primary vegetation in Myers’s hot spots covers only 1.4% of the total land area on Earth, but 44% of all vascular plant species and 35% of all species of mammals, birds, reptiles, and amphibians occur in the hot spots. It might seem especially cost-effective to focus biodiversity conservation in these hot spots. The problem is that the areas that are biologically rich tend to be densely populated, as many of these areas have productive land for agriculture. It

Biodiversity: Species and Where They Live

33

should also be noted that the above figures pay no attention to whether particular species have viable populations in the hot spots or have just been recorded there; many of them might not persist for long if the populations in the surrounding areas were lost. My colleague Atte Moilanen and his collaborators have asked where new protected areas should be located to obtain the best result for the conservation of threatened species (Montesino Pouzols et al. 2014). Their analysis is based on the known geographical ranges of 24,757 terrestrial vertebrates assessed under the International Union for Conservation of Nature (IUCN) red list of threatened species. The precise question they asked is this: If the Aichi Biodiversity Target 11 adopted by the Convention on Biological Diversity in 2010 is implemented and thereby 17% of the land area on Earth will be protected by 2020, where should the new protected areas be located? They show that the spatial scale of conservation decisions makes a big difference. If the new protected areas are placed optimally for biodiversity conservation at the global scale, the level of protection of species ranges and world’s ecoregions would be tripled from what it is now. But if the expansion of protected areas is optimized separately for each country, the level of protection is only 70% of what could be achieved through international collaboration. Apart from collaboration, or lack of it, the obvious obstacle for optimizing land use for conservation is competition with other land uses. Considering the present network of approximately 200,000 protected areas on land, with a total area of 20.6 million square kilometers ( Juffe-Bignoli et al. 2014), the protected areas are located more in biodiversity “cold spots” than in biodiversity hot spots. Historically, protected areas have been established mostly in areas where there is little competition from other forms of land use. This means that a large fraction of the current protected areas is marginal land in marginal areas, at high latitudes, at high altitudes, and on unproductive land that is not fit for anything else. Protecting these areas, and the species living in them, is valuable, but only a small part of global or national biodiversity is thereby protected. The world’s largest national park is located in northeastern Greenland, and it covers nearly 1 million square kilometers— more than the size of France and the United Kingdom put together, or six times the area of California, or about half of the pooled area of Myers’s twenty-five biodiversity hot spots. This national park in Greenland accounts for 5% of the world’s protected areas on land (actually much more, if we consider only the strictly protected areas), but the fraction of animal and plant species in the world

34

Chapter One

that occur in the national park in Greenland is only 0.01% (650 species divided by 5 million species; Wirta et al. 2014). To take a less extreme example, 13% of all forested land in Finland is protected, but if we exclude forests with very low productivity, less than one cubic meter of new biomass per hectare per year, the figure is only 8.4% (Peltola 2014). Moreover, if we consider only forests that are strictly protected (no selective logging allowed), the percentage is reduced to 5.2%. But that’s not all. The real problem is that most of the protected forests, however defined, occur in northern Finland, in Lapland, including areas that are so barren that they have stunted mountain birch at best. Considering the southern part of the country, roughly below latitude 64° north, only 2.3% of the 11.5 million hectares of forested land is protected, and if we exclude the very low productivity forests, the percentage is 1.9%. Finland will probably reach the 17% target of protected land area by 2020, but we are fooling ourselves if we are satisfied with this 17%, located as it is mostly on unproductive lands in Lapland. However, there is also another problem. Even if there were the political will to protect more habitat on productive land, there are only limited opportunities, in many parts of the world, to protect large continuous areas of natural or natural-like habitats: there simply are no such areas left. I return to this issue in chapter 5, where I outline one approach that aims to make the most of the opportunities available for conservation. Most biodiversity hot spots are located in the tropics, which is not a coincidence but reflects the second general pattern in the distribution of biodiversity on Earth: species richness increases from high latitudes toward the tropics. The latitudinal diversity gradient has been shown to be valid for different groups of animals and plants, for different habitats, and for different spatial scales (Hillebrand 2004). Comparing my home country, Finland, in the boreal region with Kenya in East Africa, two countries of roughly similar size, there are approximately 450 species of birds, 60 of mammals, 120 of butterflies, and 1,200 of vascular plants in Finland and 1,130, 65, 870, and 7,000 species in Kenya. On average, there are five times more species in Kenya than in Finland, some groups of species showing a greater difference, others a more even distribution of species diversity. Increasing species richness toward the tropics is an important generalization about global biodiversity, but it is not like the laws of physics, which can be derived from first principles and which apply everywhere. In the case of ecological generalizations, patterns are seldom informative about their causes, because several mechanisms may produce the same pattern. In the case of the latitudinal di-

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35

versity gradient, ecologists and evolutionary biologists have proposed three types of explanations (Mittelbach et al. 2007). Some hypotheses are focused on ecological mechanisms that allow more or fewer species to coexist in the same community; perhaps conditions for coexistence are generally more favorable in the tropics than at higher latitudes. Second, several hypotheses are concerned with evolutionary history, especially the rate of appearance of new species in the course of evolution; perhaps speciation rate is especially high in the tropics. And third, historical hypotheses emphasize how long current or similar environmental conditions have prevailed at different latitudes; perhaps tropical environments are older than the others and thus have had more time to accumulate species. Tropical regions receive more solar energy than localities at high latitudes. Combined with abundance of water in many, though not all, tropical regions, plant production is high, which may facilitate adaptations to the environment and thereby help many species coexist. However, whether productivity really increases plant species richness remains a controversial issue, and the relationship is unlikely to be as simple as once thought. But whatever the cause of high plant species richness in the tropics, this will inevitably create opportunities for herbivores to specialize on different host plants, and hence increases opportunities for coexistence, which in turn have the same effect on their natural enemies. In this sense, diversity begets diversity. The cause and effect may also work the other way around, from high diversity of natural enemies to high diversity of host species. A good example of this is the Janzen-Connell hypothesis, proposed by two eminent American ecologists to explain why there are so many tree species in tropical forests (Connell 1970; Janzen 1970). Consider specialist natural enemies, such as pathogenic fungi and herbivorous insects, which reduce the survival of tree seedlings. When a tree species becomes more abundant, the populations of specialist natural enemies increase, and they inflict higher mortality, which may reverse the population increase. In contrast, seedling survival of rare species is expected to be higher, because the populations of their specialist natural enemies are scarce or even locally absent. This gives an advantage to species that are presently uncommon, which facilitates coexistence of many species. Thus diversity begets diversity not only from plants to herbivores and predators but also from natural enemies to plants. In the early Cenozoic, 50 to 60 mya, when average global temperature was more than 10 degrees Celsius higher than today, tropical vegetation extended as far north as south England in Europe and the Midwest in North

36

Chapter One

America. Tropical biota thus covered a huge area. Since then, global climate has been cooling and the tropical region has contracted, but even now the tropical zone is greater than the subtropical, temperate, or boreal zones, especially in the Southern Hemisphere. In brief, tropical environments are ancient, and they have covered most of the land; hence there has been more opportunity for evolution to produce species adapted to tropical conditions than to other climatic conditions. Analyses of evolutionary trees have shown that many groups of species originated in the tropics, while temperate species are offshoots from the evolutionary tree; every now and then a species in the mostly tropical group has moved and adapted to non-tropical conditions. Moreover, assuming that everything else is equal, larger areas have more chances for speciation, and for this reason alone one could expect that evolution has produced more species adapted to the tropics than to other biomes. Another factor that may enhance species richness in the tropics is interactions with other species, which I have alluded to above and will return to in chapter 2. Species are evolving in response to their environment, which includes all the other species, and this will lead to a shifting selective regime in which reciprocal evolutionary responses among interacting species (coevolution) drive further evolutionary change. This is often called the Red Queen hypothesis: species have to keep evolving just to retain their position and viability in the community. (The Red Queen in Lewis Carroll’s story told Alice, “Now, here, you see, it takes all the running you can do, to keep in the same place.”) Yet another consideration is that boreal and temperate regions have experienced major perturbations in the form of repeated glacial cycles in the Pleistocene, in the past 2.5 million years, during which the entire fauna and flora were repeatedly removed from the glaciated areas, which were recolonized after the glacier retreated. Many species may have been lost during these disruptions, reducing biodiversity, and in any case the continent-wide migrations of species help explain why boreal species tend to have large geographical ranges. In summary, a large number of factors help explain why there are so many tropical species. Biodiversity hot spots and the latitudinal diversity gradient are two patterns on the global scale, generated during millions of years and shaped by the evolutionary history of species. The third pattern in the distribution of biodiversity is evident on smaller scales, from local to regional. Consider two areas that have similar habitat but different sizes. The two areas may be discrete fragments of habitat, such as islands, or they may have been delim-

Biodiversity: Species and Where They Live

37

ited more arbitrarily from the rest of environment. The pattern is called the species-area relationship: the larger area has more species than the smaller one. More generally, the number of species is predicted to increase when the area of the habitat increases. This may appear an entirely unsurprising result; it would be weird if small areas regularly had more species than large ones. So why have ecologists spent so much time and effort in exploring the species-area relationship? There are two reasons. First, ecologists have attempted to quantify exactly how fast species richness increases with area, in the hope that this might reveal something about the processes that influence patterns of biodiversity. Second, the species-area relationship can be used in reverse, to make predictions about the numbers of species that are expected to go extinct when a certain fraction of habitat is lost. The first example of the species-area relationship was documented by British natural historian H. C. Watson in 1859, the same year that Charles Darwin published his book on natural selection (Rosenzweig 1995). Watson tabulated the numbers of plant species that had been recorded for all of Great Britain and in parts of it, and related the number of species to the respective area. The result in figure 1.6 shows that the logarithm of species number S increases very systematically with the logarithm of area A, and this relationship can be described by the equation of a straight line, log S = c + z log A.

The values of the parameters c and z are not constant but vary from one case to another, which gives the flexibility to “fit” the species-area relationship to different groups of species and to different environments. Researchers are interested in the value of z, which describes how fast species number increases with increasing area. The value of z is approximately 0.1 in figure 1.6. Knowing the value of z, we can calculate, for instance, that the number of species is predicted to increase by 25% when the area of habitat becomes ten times greater. (The equation reads S = cA z. The new species number is Snew = c(10A)0.1, and hence (Snew − Sold)/Sold = [c(10A)0.1 − cA0.1]/ cA0.1 ] ≈ 0.25.) There are two main reasons for the species-area relationship: population dynamics and habitat heterogeneity. To start with the latter, though comparisons of different-sized areas should be of areas that have broadly similar habitat composition, in practice larger areas tend to have more variation in habitat type and quality, which makes it possible for more species with somewhat different habitat requirements to have populations in larger

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Chapter One

Fig. 1.6 The species-area relationship for plants in Britain, based on data published by H. C. Watson in 1859. (Graph from Rosenzweig 1995.)

areas. The second mechanism is the dynamic occurrence of species within any area. Species that are present may go extinct, and the smaller the area the greater the probability of extinction for the reasons that are discussed in chapter 5. But species that are now absent may immigrate to the focal areas and establish new populations, which increases species number. The colonization rate is not very strongly affected by the area of the habitat, and therefore at steady state, when extinctions are compensated for by colonization, the species number increases with area. This explanation of the species-area relationship received much attention in the 1960s after the publication of the pathbreaking book by American biologists Robert MacArthur and Edward O. Wilson (1967), The Theory of Island Biogeography, to which I return in chapter 5. The species-area relationship and the island theory were two important building blocks for the new discipline of conservation biology that emerged in the 1970s (Hanski and Simberloff 1997). The species-area relationship allows a rough calculation of the number of species that are expected to be lost when part of the habitat is lost. According to the equation above, if habitat area is reduced to a fraction x of the original area, the number of species is reduced by a factor xz. For instance, if the area of habitat is reduced to one-third of the original area, x = 0.33, if the value of the slope is z = 0.25, and if there were originally 120 species, the number of species that is predicted to remain after two-thirds of the habitat

Biodiversity: Species and Where They Live

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is lost is 0.330.25 × 120 = 91 species. This simple calculation naturally ignores many factors, but it gives a valuable point of reference for what to expect when other things are equal. As with the use of all models in ecology, however, the calculations must be based on proper understanding of the biology of the species. A dispute about bird extinctions on Puerto Rico gives an example of what happens if the species-area relationship is applied with no regard to the biology of species. Puerto Rico is an island in the Caribbean Sea, with an area of 9,000 square kilometers. Christopher Columbus arrived at Puerto Rico on November 19, 1493, at which time the island was covered by rain forest, from the coast to the top of the mountain at 1,300 meters above sea level. Since then, the human population has increased to nearly 4 million, and the area of primary forest has shrunk to one reserve of 10,000 hectares, El Yunque National Forest, just 1% of the island area. In 1900, the total forest cover was around 20%, of which much was degraded forest, but since then the area of forest and scrubland has increased. If we assume that forest cover was reduced to 10% of the original cover before it started to increase, and assume that the slope of the species-area relationship is z = 0.25, a common value for islands, we predict that half of the species have gone extinct (0.10.25 = 0.56). This prediction was singled out by Bjørn Lomborg (2001) as an example that supposedly illustrates that the area-based predictions about species extinctions are entirely misleading. Lomborg is a Danish political scientist, whose book The Skeptical Environmentalist: Measuring the Real State of the World is loaded with dubious claims about various issues concerning the environment. Lomborg observed that only 7 species of birds have gone extinct in Puerto Rico, out of the total of nearly 100 species. Taking these figures at their face value, you do not need to be a statistician to conclude that the model prediction failed miserably. But there is a serious fault in Lomborg’s argument: he paid no attention to the ecology of the species. The nearly 100 species of birds in Puerto Rico represent a very mixed bag: some are transients, some are visitors, and a third were introduced by humans. It makes no biological sense to assume that the occurrence of all these species, many of which never enter any kind of forest, depends on the original and present area of forest in Puerto Rico. The set of species that we should consider are the native forest-inhabiting species, the species that evolved to live in forests. According to ecologist Stuart Pimm, there are 20 such species, of which 7 have gone extinct; another 4 species are nearly extinct, as they have declined to less than 200 individuals and have survived only because of in-

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Chapter One

tensive conservation measures. Hence, 11 of the 20 species are either extinct or threatened by imminent extinction, which is exactly what the species- area relationship predicted. Not too much should be made of the excellent match between the predicted and observed numbers, because the species-area relationship is a simple descriptive model that necessarily ignores many factors that can affect species number in particular situations. But Lomborg’s claim that the area-based predictions of biodiversity loss are misleading is in itself wrong and misleading, and we understand why he erred in the case of Puerto Rico. To summarize the requirements for the application of the species-area relationship, the species to consider live in the main habitat in the study areas, and the areas to be compared must have broadly similar habitat composition; it makes no sense to compare forests with open grasslands. At the global scale, history, geography, evolution, and environmental factors, such as productivity of soils and climate, have produced areas of especially high levels of endemicity and species richness— the biodiversity hot spots. Nothing is learned by applying the species-area relationship to such unique situations. At smaller spatial scales, other factors need to be taken into account. For instance, if a large amount of habitat was recently lost, not all species may have had enough time to respond to the change in the environment; the community may include slow-responding species that are on their way to extinction even if there were no further deterioration of the habitat. These species, which may properly be called the living dead, constitute the extinction debt of the community. Another complication arises due to habitat fragmentation: when the total amount of habitat is reduced, the remaining habitat becomes increasingly fragmented into more or less isolated patches, which is likely to influence the viability of species. I return to extinction debt and the consequences of habitat fragmentation in chapter 5. The three patterns in the distribution of biodiversity— biodiversity hot spots, the latitudinal diversity gradient, and the species-area relationship— are important generalizations with complex causes. Our planet has biodiversity everywhere, but some areas have more of it than others. Messages 1. More than half of all terrestrial species live in tropical rain forests, and a quarter of the marine life is associated with coral reefs; hence these ecosys-

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tems are especially significant for global biodiversity. Of animals, the vast majority, 80% to 90%, are insects, and of the currently known insect species, 40% are beetles. In terms of biodiversity, beetles rule the world. 2. Researchers estimate that there are 5 to 8 million species of animals, plants, and fungi, of which only around 20% are known to science, meaning that there is a scientific description of what they look like, what their biology is like, where on Earth they occur, and what their name is. Only birds and mammals are known so well that practically all existing species have been described. Modern studies include description of genetic differences among related species, which allows the assessment of their evolutionary relationships. Genetic diversity of microbes is vast and largely unknown. 3. Life arose in seas. In the Cambrian period 500 mya, there was a huge upsurge of marine biodiversity, the Cambrian explosion, after which diversity of animals in the seas has remained relatively constant, even if the numerically dominant groups of species have changed. More complex ecosystems on land first appeared 400 mya, and the number of species, most of which are insects and flowering plants, has steadily increased in the past 200 million years. 4. Differences in soils, temperature, precipitation, and other environmental factors produce a huge diversity of habitats, where the plant and animal species that have become adapted to those conditions have viable populations. In the past centuries, humans have largely converted the more productive parts of the total land area on Earth (149 million square kilometers) to croplands (covering 13% of the land area) and pastures (31%). The amount of land that is not yet cultivated but would be suitable for agriculture, excluding forested, protected, and densely populated areas, is only 3% of the ice-free land area— so close is humanity to the planetary carrying capacity. 5. Biodiversity is not evenly distributed across the planet. Researchers have identified biodiversity hot spots, including Borneo and Madagascar, which have disproportionate numbers of endemic species and have high species richness in general. Many ecological and evolutionary processes have contributed to a latitudinal gradient of increasing biodiversity toward the tropics. The number of species increases with increasing area of habitat. This species-area relationship can be used to make rough predictions about the number of species that are expected to go extinct when a certain proportion of the original habitat area is lost.

2

How Is Biodiversity Generated?

Island Area Maximum elevation Age Time since isolation Current isolation Inhabitants Breeding birds Endemic birds Butterflies Flowering plants

Madagascar 587,040 square kilometers 2,876 meters More than 550 million years 165 million years from Africa; 80 million years from the Indian plate 640 kilometers 22,600,000 285 species 105 species 297 species 11,000 species (90% endemic)

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Chapter Two

Madagascar, Biodiversity Hot Spot

I

n the summer of 2001, I was writing a grant proposal to the National Research Council. This is what researchers regularly do: try to convince the funding agencies that their work is worth public support, would advance science, and would ultimately be of benefit to society at large. In the case of my work, the benefits include better understanding of the processes that affect the viability of animal and plant populations in the wild. I had been appointed to a research professorship for another five-year period, and I now explained how much money would be needed to carry out the research I proposed to do. The application included a small project that was not central to my research but about which I was very enthusiastic: I wanted to return to Gunung Mulu in Sarawak in 2003, to repeat the sampling of dung beetles that I carried out in the spring of 1978 (chapter 1). The application said: “Gunung Mulu National Park has some of the biologically most diverse forests in SE Asia and a nearly aseasonal climate. The plan is to repeat exactly the same trapping program in the spring of 2003, 25 years after the first sampling. Comparison between the two sets of results will provide a unique opportunity to examine the stability of insect populations and their spatial population structures over a long period of time in an exceptionally stable tropical environment.” What I did not mention was that in 2003 I would be 50 years old myself. The trip was written in the stars, because the funding was awarded. Unfortunately, that was the end of the heavenly support. I made inquiries about practical matters, such as the various permits that would be needed— and I was advised to forget it. I was told that the chances of success would be very small. We would need to camp in the forest on our own and export large numbers of unspecified insect samples out of the country, which would be difficult to arrange. I presume that the authorities in Malaysia are concerned about biologists prospecting natural populations for the pharmaceutical industry and other commercial purposes without dividends being paid to the country where the samples were obtained. I can understand the concern. I happened to tell my worries to Jari Niemelä, a colleague in the department, and to my surprise he had an instant solution: why not go to Madagascar instead of Borneo? The University of Helsinki had been funding, with other institutions, the construction of a research station in southeast Madagascar, in Ranomafana National Park, where Jari had a couple of students. A slight worry was the politics; there had been a major crisis in early 2002,

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but things seemed to have calmed down by the summer. The procedures to apply and secure the research permits were in place. I had the money. Madagascar would not be the same as Borneo, of course, and I had not been working there in 1978. Moreover, I knew next to nothing about Malagasy dung beetles, but the temptation to return to tropical forests to study beetle ecology and evolution was too great to resist, and I decided to do a short trip by myself to find out about Ranomafana National Park and something about the beetles. The preferred itinerary was via Paris, which has direct flights to the capital, Antananarivo. I had a flight booked from Helsinki on the evening of November 26, 2002, springtime in Madagascar and very dark time in Helsinki. In the afternoon the day before, my secretary knocked on the door and said that there would be a one-day strike in Paris on November 26, so I could not fly there as planned. A one-day strike in Paris was not a big surprise, but why did it have to be on November 26! There were two options: I could fly in five hours’ time today, which was not possible because my wife was out of town and the children could not be left alone, or I could fly to Brussels tomorrow and try to get to the airport in Paris by the morning of November 27 to board the flight to Madagascar. I would be carrying a tent, a sleeping bag, and other camping gear, plus traps for beetles, but I thought, I’m not yet too old to do that. And I wasn’t: the trip was a success, even if it was drizzling every day that I spent in the forest. Madagascar and Borneo are large tropical islands, Borneo the third largest island in the world and Madagascar the fourth largest, both more than half a million square kilometers. (Greenland and New Guinea are the two largest islands.) Madagascar and Borneo are megadiverse; they are among the eight hottest global biodiversity hot spots delimited by Norman Myers and colleagues in 2000. But in terms of the evolutionary history of their plants and animals, they are very different. The oldest parts of Borneo were dry land in the Cretaceous, 145 to 66 mya, but most of Borneo was lifted above sea level much later, 15 mya, when the mountain range formed in the center of the island. In the Pleistocene, the past 2.5 million years, Borneo has been part of Sundaland, together with Java, Sumatra, many smaller islands, and the Malaysian Peninsula. Sea level has fluctuated depending on the glacial cycle, and the parts of Sundaland were either connected to each other and had a land connection to mainland Asia, or they were separated from each other by a shallow sea, as they are today. Borneo as we know it today is a recent island; the present shoreline dates to the latest melting of the continental glaciers and subsequent increase in sea level. Considering this

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history, it is not surprising that the plants and animals are largely the same as on the neighboring large islands. For instance, of the 420 bird species breeding in Borneo, only 37 species are endemic, and even these probably did not become separate species after Borneo became the present island; they may have gone extinct elsewhere. The contrast with Madagascar is as great as it could be. In the Jurassic, 200 to 140 mya, dinosaurs were the dominant large animals on land. Madagascar and India were part of the southern supercontinent Gondwana, together with Africa, South America, Antarctica, and Australia. Some 165 mya, plate tectonics separated Madagascar and India from Africa, and they started to drift eastward together; later the Indian plate separated and started its journey northward. The speed of movement was modest, 20 centimeters per year, but after enough time the Indian plate collided with the Eurasian plate along the boundary between what are now India and Nepal, giving rise to the Plateau of Tibet and the Himalayas. Madagascar, on its own plate, remained more or less where it is today. Thus the Mozambique Channel, presently less than 500 kilometers wide, has separated Madagascar and east Africa for tens of millions of years. The Mozambique Channel is wide enough to make crossing very unlikely by most organisms, but not so wide as to make it entirely impossible, given enough time. This situation has been favorable for the buildup of the unique fauna and flora in Madagascar. The rare colonizers that have arrived at some point during the past 100 million years have given rise to spectacular evolutionary radiations, groups of related species originating from the common ancestor that managed to colonize Madagascar. All these species are endemic to Madagascar. The overall level of endemism is higher than anywhere else: 89% in plants, 59% in freshwater fishes, 99% in amphibians, 96% in reptiles, 58% in birds, and 93% in mammals. It is hardly a coincidence that endemism is somewhat lower in birds than in other vertebrates, as birds can fly and are hence likely colonizers. My short visit to Ranomafana National Park in November 2002 was the beginning of a research project during which much knowledge about the ecology, biogeography, and evolution of Malagasy dung beetles has been accumulated. Nearly 300 species are known from Madagascar (figure 2.1), about twice the number in Borneo, and the level of endemism is very high, 96%. There are several clear differences in the communities between the two islands. Borneo has several large species, but Madagascar has none: all Malagasy dung beetles are less than 25 millimeters long. The overall abundance of

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beetles is higher in Borneo, as is the number of species coexisting at any one locality: 70–80 species in Borneo but only 20–40 species in Madagascar, in spite of the much smaller total species number in Borneo than in Madagascar. These differences are natural, given the much more diverse mammalian fauna in Borneo, which leads to greater diversity and total amount of resources for dung beetles. The mammalian fauna in Borneo includes five species of deer; wild ox; wild boar; rhinoceros (now close to extinction); elephant (now within a small area); ten species of primates; sun bear, leopard, and many other predatory mammals; many squirrels, flying squirrels, and small mammals; and a few very odd species, such as the otter civet and bearcat. In contrast, the Malagasy mammals consist of small and medium-sized lemurs (primates) and a few other native, mostly small mammals. The situation was somewhat different only 2,000 years ago, when humans colonized Madagascar. Curiously, the immigrants did not arrive from mainland Africa but probably from Borneo and in any case from Southeast Asia, which is reflected in some notable similarities in the languages. Similar words that I learned in the field include salt (sira in both languages), peninsula (tanjung in Malay, tanjona in Malagasy), spider (kala, hala), and to be back (lambosir, lamosina). The arrival of humans in Madagascar had the same consequence as the arrival of humans in Australia and North America— the extinction of the megafauna. That the megafaunal extinctions on different continents occurred at different times but always coincided with the arrival of our species strongly supports the hypothesis that humans were involved, in one way or another. In Madagascar, at least seventeen species of large-bodied lemurs went extinct, including the gorilla-sized sloth lemur. Amazingly, all the species that went extinct had larger bodies than the species that survived (see figure 3.2). There were possibly as many as three species of dwarf hippopotamuses, some of which survived until 1,000 years ago; giant land-living tortoises; and the elephant bird, the largest bird ever, three meters tall and up to 500 kilograms in body mass. The last elephant birds disappeared so recently that stories about them have survived, attesting, among other things, that one egg was enough for an omelet for 150 people. From the dung beetles’ point of view, only the giant lemurs were of significance; the droppings of the other megafaunal species were not that suitable for beetles. Thus the range of resources available for Malagasy dung beetles has been much more limited than that for Borneo beetles, even taking the extinct megafauna into account. There are no large-bodied dung beetles in Madagascar because these beetles typically use the dung of un-

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gulates for reproduction, and there are no native ungulates in Madagascar. The greater local diversity of beetles in Borneo than in Madagascar is almost certainly due to the greater diversity of resource types in Borneo, which has facilitated ecological diversification of species and thereby helped more species to coexist locally. But why is the total number of species much greater in Madagascar than in Borneo? Different localities in Madagascar have largely different species, whereas in Borneo most species are widely distributed on the island. Madagascar on its own tectonic plate has remained for a long time a large heterogeneous island, or a small continent, whereas Borneo belongs to one of the most geologically active regions on Earth. It is reasonable to assume that the more stable, long-term geological history of Madagascar has allowed more species with narrow geographical ranges to evolve and persist. We shall consider the dynamics of geographical ranges of species later in this chapter, but meanwhile let us consider how new species appear in the course of evolution. Origin of Species Charles Darwin arrived at the Galápagos Islands on board HMS Beagle, a Cherokee-class brig-sloop, in September 1835. The Galápagos were just one stop among many during his five-year voyage around the world, but many have thought that this was the most significant stop for Darwin. As usual, he collected everything that he could lay his hands on: birds, lizards, tortoises, fishes, insects, and plants. After returning to England, he sorted out his samples and sent specimens to experts for close examination and for scientific description of new species. In his travel memoirs, Journal of Researches (Darwin 1842), Darwin first describes the particular features of each group of species, then ponders a curious thing about the natural history of the Galápagos Islands: different islands appeared to be inhabited by slightly different-looking individuals of the same species. The giant tortoises were the prime example. The vice governor of the Galápagos colony told Darwin that he could tell from the appearance of a tortoise from which island it came. Back at home, Darwin regretted that he had not kept all specimens from different islands separate, though fortunately in most cases this information had been recorded. Darwin found it most remarkable that different islands would have different forms— or could they even be different species?— even if the islands shared much the same climate and natural con-

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Fig. 2.1 An assortment of endemic dung beetle species from Madagascar, out of about 300 endemic species.

ditions, and were within sight of each other, at distances of some tens of kilometers. Among Darwin’s collections of birds was a set of monotonically dark finches. These birds, altogether fourteen species, are now called Darwin’s finches, and they make up a textbook example of how new species arise— or at any rate how new species are commonly thought to arise. The Galápagos Islands are 1,000 kilometers from South America, west of Ecuador. The islands are of volcanic origin; the first ones emerged above sea level 5–10 mya. Today there are 18 main islands, 3 smaller islands, and 107 rocks and small islets. The current understanding is that a flock of the common ancestor of Darwin’s finches went astray from the South American coast and

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arrived at the Galápagos 1–2 mya. It is of course possible that more birds arrived over a longer period of time, but in any case the story of Darwin’s finches began when a permanent breeding population was established on some Galápagos island. A new species was not established at this point; the new population represented a common South American species that just happened to find itself in a strange place, an island in the middle of the ocean. The environment was novel in comparison with the mainland, probably also including the available food resources. Natural selection started to favor individuals that had heritable features best fitted to the new conditions. These features, including the appearance of the birds, started to change gradually, and after millennia the population consisted of birds clearly distinct from the birds on the continent, so different that, had a competent bird-watcher been on the island, he or she could have seen the difference. Let us digress for a moment to contemplate natural selection, Darwin’s big theory. Natural selection is one of those truly revolutionary ideas that are not difficult to understand for anybody who cares to spend a moment to think about it, yet the brightest minds in the early nineteenth century could not see it. Natural selection is a process that influences biological evolution; hence, to appreciate natural selection, one has to have an open mind about evolution. Two hundred years ago the belief that life, and the cosmos, was created by God was so much a part of people’s worldview that any alternative was entirely inconceivable for the vast majority of people, scientists included. Today the support for evolution is so strong and manifold, that nobody who is willing to become familiar with the evidence can doubt that evolution has occurred. For natural selection to lead to an evolutionary change, the first requirement is variation among individuals— if there is no variation, there is nothing to select from. In natural populations, variation among individuals is ubiquitous; we are all unique in many ways, except for organisms that reproduce clonally, in which case mothers produce identical copies of themselves. Additionally, for selection to affect the individual phenotype, by which we mean all the measurable morphological, physiological, behavioral, and other features, variation among individuals must to some extent be heritable from parents. If it were not, selection would not lead to a change from one generation to another. Because much of the phenotypic variation is due to genetic variation among individuals, and the genes are inherited from two parents, phenotypic variation is usually heritable to some extent. Finally, for evo-

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lutionary change to take place, the phenotypic traits must affect the lifetime reproductive success of individuals, their fitness, which is the mechanism whereby natural selection works. For instance, consider a population of seed-eating Darwin’s finches living on an island with mostly large hard seeds. There is variation in beak size and shape of individual birds, which is to some extent inherited by the offspring. Individuals with the heaviest beaks are better at using large seeds than individuals with slender beaks, and if this is reflected in the numbers of chicks successfully reared by pairs of finches, the average beak size in the population will change from one generation to the next. In other words, a small evolutionary change has taken place. Natural selection is comparable to the artificial selection imposed by plant and animal breeders, though in the latter case selection is much more systematic and so leads to a faster change in the desired direction. In natural selection, the agent that selects is the environmental conditions, which favor certain kinds of individuals. However, different aspects of the environment can favor different kinds of individuals, the environmental conditions often change from one year to another, and so forth, making the outcome over a few generations more variable than in artificial selection. To put this in mathematical terms, the response to selection depends on three factors in a multiplicative manner: Response to selection = i σp2 h2

I use here the symbols from the scientific literature for the three factors of importance. Parameter i denotes the intensity of selection, meaning how different the individuals that are favored (selected) by the prevailing environmental conditions are from the average individual in the population. The term σp2 stands for the amount of variation in the phenotypic trait, and the term h2 is heritability. To repeat, the response to selection is stronger when the differences are large between the selected individuals and the average individual in the population, when there is more variation in the population, and when the variable trait is more heritable. If any of these factors is zero, there is no response to selection and hence no evolution, regardless of the values of the other terms. Artificial selection by animal and plant breeders can be made very effective by selecting very extreme individuals with respect to the trait of interest (large i). Returning to Darwin’s finches, how did evolution produce the current fourteen species from the single ancestral species? The likely scenario goes

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like this. The ancestral population occurred initially on just a single island, but at some point the species colonized one or more other islands. The distances between the islands are not great for birds, some tens of kilometers, and migration between the islands has been recorded by direct observations in the past decades (Grant 1999). Different islands have broadly similar environments, as Darwin observed, but not quite the same, and natural selection favors somewhat different kinds of individuals on different islands, depending, for instance, on the type of food that is commonly available. Random factors may have played a role, too, and caused small populations on different islands to diverge from each other in the course of time. This is called genetic drift: the relative abundance of different genetic variants (alleles) vary by chance alone among offspring, and the smaller the population, the greater is the role of this kind of randomness. Some island populations may have gone extinct and new ones appeared due to migration and colonization. At some point birds colonized an island that already had a resident population, after which two things may have happened. The resident birds and the newcomers may not have had substantial genetic or ecological differences; they would interbreed and produce viable offspring, and the newcomers would merge with the resident population. If this happened, the resident population would not return to square one, however, as the immigrants brought new genetic material from the other population, and this additional genetic variation would facilitate further response to selection and hence advance adaptation to the environment (see the equation above). On the other hand, if the newcomers came from a population that had already diverged more from the resident population, some interbreeding may still have occurred, but the hybrid offspring may have had reduced fitness, which would select against further hybridization. The newcomers could also be ecologically different than the residents, which could reduce the likelihood of interbreeding in the first place. The residents and the newcomers would represent two incipient species. Once they coexisted on the same island, they would likely compete for the same resources, and natural selection on each species would favor individuals that are less similar to the competitor, thereby reducing the strength of interspecific competition. In the course of such selection, the two species would become increasingly dissimilar with respect to the relevant ecological traits. This is how researchers have explained the diversity of beak sizes and shapes in Darwin’s finches (figure 2.2). Most of the species feed primarily on seeds, and different species have

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Fig. 2.2 Charles Darwin (1845) wrote one of the best natural history travel books ever, about his five-year voyage (1831–36) around the world. One of the few figures in Darwin’s book illustrates small passerine birds, which are currently known as Darwin’s finches. The finches look rather similar, but they have evolved to use different food resources, including different types of seeds and insects, which is reflected in the size and shape of their beaks. The species in the figure (clockwise from upper left) are large ground finch (Geospiza magnirostris), medium ground finch (G. fortis), warbler finch (Certhidea olivacea), and small tree finch (Camarhynchus parvulus).

specialized to feed on the seeds of different plant species, whose seeds differ in size and hardness; yet other species feed on insects. An important auxiliary assumption here is that it does not pay for individuals to try to use many different food types, because that would require a compromise, for instance, having an intermediate beak, which would not be very good for any kind of food— a jack of all trades is master of none. Under many circumstances, such a generalist is expected to lose out in competition with two or more specialist species. However, it should be noted that there are other circumstances in which a generalist actually performs better, for instance, when the abundances of different food types fluctuate a lot, making it hard for specialists to survive on their preferred food type, which is not abundant all the time. Evolution of two distinct species from a single ancestor—in other words, speciation—is practically certain to happen when the distribution of the

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ancestral species permanently splits into two parts because of a barrier to dispersal— most dramatically when the distribution of a widespread species splits because of plate tectonics. Most likely, the environment is different in the two regions inhabited by the populations of the ancestral species, and given enough time, the populations evolve by natural selection to become different species. Even if the environments were the same, evolution that takes place independently in the two regions will not lead to the same outcome; there is always historical contingency, unpredictability, in evolutionary change. Whether due to natural selection or other reasons, populations that inhabit the two separate regions become genetically and ecologically differentiated, and after a sufficiently long time, they cannot produce viable offspring even if there were an opportunity to interbreed. Speciation that occurs in this manner is called allopatric speciation; this is the common mode of speciation. Speciation is sympatric if the ancestral species gives rise to two species without any physical isolation. Sympatric speciation at first seems very unlikely; if the two incipient species mix in the same area, shouldn’t there be continuous interbreeding that will prevent differentiation? Yes, indeed, and special circumstances are required for sympatric speciation to proceed. For instance, consider an insect species with two host plants. Variation in the population might lead some females to prefer one of the host species for oviposition and some to prefer the other host species. If mating occurs on or near the host plant, parallel evolution might make each insect better at using one host species and have a preference for mating location, which would effectively isolate the two parts of the original population. The possibility of sympatric speciation has attracted much attention from biologists, and there are some well-studied examples, but by and large, allopatric speciation is a much more likely mode of speciation. Innovations, Range Expansions, and Evolutionary Radiations A traveler to Madagascar can easily find Helictopleurus quadripunctatus, one of the most beautiful and interesting dung beetles on the island. To find it, you just flip over half-dry cattle-dung pats where you see a few zebus, and most likely you will see the beetle running for cover. A shiny black body and red forewings with four black dots make it very distinctive; it cannot be confused with any other dung beetle. You can hardly fail to spot the beetle, and we can assume that the same goes for birds and mammals foraging for insects. But why should the beetle advertise itself with conspicuous colors?

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Toxic prey often do this, to the benefit of both themselves and their predators, but dung beetles are unlikely to be toxic. More probably, H. quadripunc­ tatus imitates the warning colors of some other species that have effective defenses, for instance, some wasps. This is called Batesian mimicry, and it works as long as the species that the beetle mimics is common enough to “train” predators. However, the reason that H. quadripunctatus is especially interesting is different: it is the fact that it feeds on cattle dung. In mainland Africa, this is the norm: ungulate dung, cattle dung included, is the preferred food for hundreds of species, which often engage in fierce competition for the limiting resource (chapter 1). In general, dung beetle evolution in the past tens of millions of years has been greatly accelerated by the expansion of grasslands with a high density of ungulates and other large herbivorous mammals in Africa (Hanski and Cambefort 1991). But Madagascar has no native ungulates and never has, and the vast majority of Malagasy beetles have adapted to use lemur droppings, or they have become generalists and use both dung and carrion. Primate and cattle dung have very different textures, fiber content, and chemical composition, so different that switching from one to the other is far from trivial. Many forest localities in Madagascar have feral zebus, but their dung is not used by the many common forestinhabiting beetles, which proves that changing diet is difficult. Only about 10 endemic species have evolved to use cattle dung, out of nearly 300, and these species, including H. quadripunctatus, occur in open and semi-open habitats. Additionally, the cattle pats have 10 to 15 mostly uncommon introduced species (Rahagalala et al. 2009). It is not known which traits of the native beetles have changed to make the new diet possible, but whatever the innovation, it has made a huge amount of new resource, produced by 10 million zebus across Madagascar, available to beetles. Malagasy dung beetles have typically small geographical ranges, but the few cattledung specialists are exceptional; they occur literally everywhere there are cattle. Thus the evolutionary innovation has allowed the species to greatly expand their ranges. That the species expanded their distributions after the shift to the new resource is known from molecular studies. In other dung beetles in Madagascar, and in most animals and plants anywhere, if you pick up two individuals from the same or nearby local populations, they have greater genetic similarity than if you select two individuals from distant localities. The reason is that individuals that are located near each other are on average more related to each other than individuals located far from each other. The cattle-dung-inhabiting beetles in Madagascar do not show this

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relationship; all individuals are genetically very similar to each other regardless of which part of Madagascar they come from (Hanski et al. 2008). The natural explanation of this exceptional situation is that the species have recently expanded their distributions from one region, the one in which the innovation arose. Hence all individuals across Madagascar are closely related; they share a common ancestor less than 1,000 years ago, since cattle were introduced to Madagascar. Having successfully made the switch to using cattle dung, is H. quadri­ punctatus a new species? It is probable that the now-abundant form that feeds on cattle dung has replaced the original form, which was probably a generalist in terms of its diet and occurred somewhere in western Madagascar; hence no direct comparison is possible. Nonetheless, so little time has passed since the introduction of cattle to Madagascar that relatively few new mutations have had time to accumulate, so that most genes, including the “barcode” gene discussed in chapter 1, would not show any significant differentiation. However, natural selection has most likely led to significant changes in some genes—namely, the ones that affect resource use—and have made it possible for the beetle to successfully use cattle dung. From this perspective, we have a new species. Fortunately, we do not need a definition of species that would encompass all possible situations; it is more important that we understand the process of evolution, which in the course of time and via different genetic and ecological mechanisms leads to new forms that we call species. Another question that we cannot answer but can ponder is what happens next. Helictopleurus quadripunctatus now occurs everywhere in Madagascar and lives in many kinds of environmental conditions. This beetle is not more dispersive than the others, so one could expect that over time, beetles in different regions will become genetically differentiated. Ultimately, the single widespread species may split into several species with non-overlapping distributions, which is a common pattern in many Malagasy species, not only dung beetles, and which explains why the overall diversity in Madagascar is so high. To find out about genes that influence ecologically important traits, researchers have started to sequence the entire genomes of many individuals representing different species. In a nutshell, the idea is to find genetic variants that best discriminate among species (or populations) with dissimilar ecological traits. Such variants are good candidates for genes that may influence these traits and may be mechanistically involved in the evo-

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lution of the species. In the well-studied Darwin’s finches, the key feature is beak size and shape, which influence the kinds of seeds that a bird can efficiently use. A recent study found several genes that show systematic differences between species with pointed versus blunt beaks; these genes may underpin the evolution of beak size and shape (Lamichhaney et al. 2015). In this work, the authors sequenced the full genomes of all known species and several populations of many species. In addition to finding candidate genes affecting beak development, they also found evidence for widespread hybridization during the evolution of the finches, which may have speeded up evolutionary change by introducing new genetic variation. It is well known that exchange of genetic material among lineages is widespread and greatly influences evolution in bacteria, but gene flow between species may be common also in vertebrates during the early stages of species differentiation, before there are major genetic obstacles to hybridization. The pattern of genetic variation across the genomes also revealed that some of the recognized species consist of genetically well-differentiated populations on different islands; thus the researchers now think that there may be more species of Darwin’s finches than previously thought, perhaps up to eighteen species. The Malagasy fauna features an even more striking radiation of birds with greatly modified beaks, the vangas, which colonized Madagascar about 20 mya (Reddy et al. 2012). As is typical for many old radiations, in vangas the rate of speciation was rapid at first but slowed down, apparently when most of the “empty niches” suitable for these birds had been occupied. As Madagascar lacks many groups of birds that are prevalent elsewhere, there has been an opportunity for extreme specialization. Two striking examples of species that occupy the “woodpecker niche” in the absence of woodpeckers in Madagascar are the sickle-billed vanga (Falculea palliata) and, even more so, the aye-aye (Daubentonia madagascariensis), a highly specialized lemur, which uses its thin and greatly elongated middle finger for the same purpose that woodpeckers use their tongue and beak (figure 2.3). Speciation and evolution may produce a large number of species that share a common ancestor and that adapt through natural selection to use different niches in the environment, which is reflected in differences in their ecology, behavior, and other features. This process is called adaptive radiation. Evolution of beak sizes and shapes in Darwin’s finches and in Malagasy vangas are two examples of adaptive radiation. The common ancestor of lemurs arrived at Madagascar just after the fifth mass extinction that terminated the Mesozoic era, 66 mya, possibly as passengers on floating vegeta-

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Fig. 2.3 The sickle-billed vanga (Falculea palliata) and the aye-aye (Daubentonia madagascariensis), a highly specialized lemur, have evolved to occupy the “woodpecker niche” in Madagascar, where there are no woodpeckers. The aye-aye has an unusual foraging method to find grubs living in dead wood: it gnaws small holes in wood with its forward-slanting incisors and pulls the grub out with its narrow middle finger. (Drawings by Juha Markula.)

tion carried by sea currents from mainland Africa. From this single ancestor, Malagasy lemurs have radiated to about 100 extant species, which constitutes nearly 20% of all living primates in the world. The radiation of lemurs is so old that a succession of species have gone extinct and new ones evolved. Most recently, the seventeen largest species went extinct in the megafaunal extinction starting 2,000 years ago. In the case of Malagasy dung beetles, the first colonization may have occurred before the end of Mesozoic era, when there were dinosaurs and primitive mammals in Madagascar, which all went extinct. Molecular studies show that not all of the approximately 300 extant dung beetle species share the same common ancestor, but instead the present species originate from eight independent colonizations, most probably from mainland Africa (Miraldo et al. 2011). There were probably even more colonizations, but if so the additional ones failed to leave any descendants that survive today. Accurate timing of the eight colonizations is not possible in the absence of beetle fossils, but the molecular results give a rough idea when they took place, from 79 to 15 mya (Miraldo et al. 2011). The oldest radiation (Arachnodes) is also

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the largest one, with more than 100 extant species. These species exhibit a greater range of ecological differentiation than species in the younger radiations. This is what one might expect: the beetles in the Arachnodes radiation initially had no competitors, and they had an opportunity to expand into previously unoccupied niches, into a virgin land as far as dung beetles are concerned. The Arachnodes radiation includes very small species (3 millimeters) to species that are large by Malagasy standards (15 millimeters). Some species use only lemur (primate) dung, and some use both dung and carrion (generalists). A few species have shifted to use cattle dung in open areas, like Helictopleurus quadripunctatus. Six species have shifted to forage for lemur dung in forest canopy, thereby avoiding resource competition on the ground. These beetles locate a lemur dropping on a leaf, detach it, and jump with it to the ground to breed. Several species have lost their wings or have greatly reduced wings, which indicates some highly specialized foraging behavior, perhaps feeding on small mammal droppings in their tunnels. There is no predefined design; evolution by natural selection finds its way opportunistically. The situation was fundamentally different when the ancestor of the second oldest radiation, making up the genus Helictopleurus, landed in Madagascar; native dung beetles were already present. The voyage from mainland Africa across the Mozambique Channel may have used floating mats of vegetation, like those carried by ocean currents after the 2004 Indian Ocean tsunami. This radiation has sixty-five extant species, which are mostly dung feeders or generalists like the species in the first radiation, but there is one striking difference in their biology: Helictopleurus are diurnal, whereas Arachnodes are nocturnal or crepuscular. Elsewhere in the tropics, the relatives of both Helictopleurus and Arachnodes include both diurnal and nocturnal species; hence the situation in Madagascar is unusual. The species in the two oldest radiations appear to have divided the twenty-four hours among them. The time of day and night that the beetles are active influences who gets to new pieces of resource first. The medium-sized lemurs are mostly day active, which may have been a factor shaping the evolution of Helicto­ pleurus species. The major radiation of lemurs occurred 44 to 22 mya, which coincides exactly with the admittedly rough timing of the initial radiation of Helictopleurus, 44 to 23 mya (Wirta et al. 2010). During this same period, other groups of mammals—including tenrecs, rodents, and carnivores— arrived at Madagascar, and radiations of lemurs and other mammals generated further opportunities for more dung beetles to fit into the community.

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The two youngest radiations with many surviving species took place 25 to 15 mya, including the genera Epactoides and Nanos, which are mostly small and medium-sized species that feed on carrion or are generalists. The many small Epactoides species in particular have evolved into marginal ecological niches, such as forest at high elevation. The vast majority of species in the four successful dung beetle radiations occur in wet forests. For much of its history, Madagascar has probably been heavily forested, and most of the mammals, including nearly all lemurs, are forest species. The four remaining dung beetle radiations out of the total of eight are restricted to dry areas in western Madagascar, and they all have only one or a few species each: these radiations have largely been failures. The open habitats in western Madagascar have never had native ungulates or other mammals that would have produced dung suitable for beetles. It is especially noteworthy that three of the four “unsuccessful” radiations belong to the tribe Onthophagini, which has been extremely successful worldwide and has hundreds of species inhabiting wet forests elsewhere in the tropics. In my trapping of dung beetles in Gunung Mulu National Park in Sarawak, Onthophagus was by far the most speciose genus. The fact that there is not a single Onthophagus or related species in wet forests in Madagascar, though there are a few species in open areas in western Madagascar, testifies to the difficulty of new species entering a community that already has a full set of species exploiting the full range of available resources. The composition of the dung beetle communities in rain forests in Madagascar speaks for the importance of long-term history in the buildup of communities and ecosystems, and warns against trying to explain every pattern in modern communities by present-day ecological factors alone. At the same time, the interpretation of what happened during tens of millions of years is naturally a hypothesis, which remains impossible to test conclusively. The best we can do is to construct interpretations that are consistent with as much empirical data as possible and consistent with our understanding of the relevant processes. This is what makes all historical studies both challenging and appealing. Butterflies and Plants, Bees and Flowers Many evolutionary radiations started when the common ancestor migrated to a new region, which offered new opportunities for speciation and ecological differentiation in the form of unused resources. The Darwin’s finches

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and Malagasy dung beetles are examples of young and old radiations, respectively. The rate of speciation is typically high early on in the radiation, when new species fit easily into the environment, but gradually the niches become occupied and the rate of speciation slows down. This pattern is occasionally disrupted when a species in an existing radiation evolves some completely new feature, a key innovation, which makes it possible for all the descending species to carry the new innovation and to use resources that would otherwise remain unexploited. Evolution of key innovations also highlights the fact that species do not just adapt to preexisting niches in the environment; the “niche,” an ecological opportunity to establish a viable population, is as much the result of the biology of a species as it is a feature of the environment. The key innovation may lead to a secondary burst in speciation rate, such as the radiation of Nanos dung beetles mentioned above. There was an overall decline in species accumulation through time since the colonization of Madagascar 24 to 13 mya, but one part (clade) of the radiation, stemming from one species that appeared 6 mya, shows a significant increase in speciation rate, which is associated with a significant increase in body size (figure 2.4). Large body size often confers a competitive advantage in dung beetles, and hence large body size may represent a key innovation in this radiation. The clade with large body size now includes twenty-four species, after 6 million years of evolution, and the species have strikingly allopatric (nonoverlapping) distributions, which helps explain how so many similar species manage to coexist in Madagascar as a whole, though only one or a few species occur at any one locality. The above scenarios make a distinction between constant environment and the evolving species that constitute the radiation. What happens if an important part of the environment actually consists of other species that can also evolve? An example would be a new kind of predator that colonizes an area with a variety of prey species, where the prey evolve in response to the predator, and the radiation stemming from the common ancestor of the predators reflects in part the evolutionary changes in the prey species. Or consider, as Paul Ehrlich and Peter Raven did in a classic paper (1964), butterflies that feed on a range of plant species. Ehrlich and Raven summarized a large body of knowledge about the host plants of butterflies— who is feeding on whom— and they proposed the term coevolution to describe the evolution of one set of species, such as butterflies, interacting and evolving with another set of species, such as the plants that caterpillars eat. Plants produce, collectively, a vast number of secondary metabolites, plant biochem-

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Fig. 2.4 A tree showing the evolutionary relationships among the species in the radiation of Nanos dung beetles. The original colonization occurred 24 to 13 mya (the figure shows the average estimate), after which many species evolved, but gradually, new species were appearing more slowly. Between 8 and 6 mya, a species appeared that gave rise to the group (clade) of 16 species at the bottom of the tree, with a significantly higher rate of speciation than in the rest of the species in the past 6 million years. The line thickness indicates the body size of the species: the largest species are shown by the thickest line. Thus the new clade consists of large, fast-speciating species. Large body size may be related to some key innovation that has facilitated speciation. (Data from Miraldo and Hanski 2014.)

ical substances that are not necessary for plants’ growth and reproduction. Secondary metabolites may originally have been by-products of essential metabolic processes, but they often acquire the function of plant chemical defense: these metabolites are toxic to insects. Examples include alkaloids, terpenoids, and glycosides. The butterfly family Pieridae, which includes the white and sulfur butterflies, has been studied in great detail in this context (Wheat et al. 2007; Edger et al. 2015). Originally, the caterpillars of

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these butterflies fed on legumes, which has been discovered by mapping the host plants of the existing species on the evolutionary tree constructed for the butterflies. Around 90 mya, the order Brassicales of flowering plants, including cabbages and papaya, first appeared. All Brassicales possess a biochemical glucosinolate-myrosinase system, a very effective chemical defense against insects. Evolution of the glucosinolate-myrosinase system was a key innovation, which allowed Brassicales to escape herbivory and thereby accelerated their radiation. But a challenge is also an opportunity in evolution. Following the key innovation in plants, the ancestor of the butterfly subfamily Pierinae evolved an effective detoxification mechanism for the glucosinolate-myrosinase system— another key innovation, but this time in butterflies, which now speciated faster than their close relatives, taking advantage of the new range of host plants in Brassicales, which were likely abundant and little used by other insects because of their chemical defense. A detailed genomic study of the plants and the butterflies has demonstrated the evolution of increasing biochemical complexity after the initial key innovations, with three major steps in plants, involving duplication of important genes that allowed them to produce increasingly effective chemical defenses (Edger et al. 2015). At each step, butterflies responded to plant innovations by counter-adaptations, leading to an escalating evolutionary arms race. Importantly, the new adaptations in both plants and butterflies increased speciation rate. This is the type of coevolution that Ehrlich and Raven envisioned: escape from a previous constraint by evolving a key innovation, then radiating into a large number of new species. In principle, there is no limit to the amount of biodiversity that can be generated in this manner, essentially because the environment is not constant but changes all the time. Butterflies have currently 17,000 species worldwide, and the angiosperms have 300,000 to 400,000 species. Apart from butterflies, there is a huge number of other herbivorous insects. Another group of insects that are closely associated with flowering plants is insect pollinators. Herbivorous insects harm the host plant, but for pollinators the relationship is different, as both the plants and the insects benefit from their interaction. Some insects, notably butterflies, play a part in both interactions, as the nectar-feeding adults help pollinate the plant, while their caterpillars feed on plants, though usually not on the same plant species, and thereby cause some harm. Engaging insects and, less commonly, other animals in their reproduction was a truly marvelous key innovation in plants. Compared with pollination via wind, which is the mechanism used by

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grasses, sedges, and coniferous trees, animal pollination leads to less waste of pollen and reduces the likelihood of inbreeding. Animal pollination may facilitate speciation, when different plant species evolve different kinds of flowers to attract particular pollinators. Flowers often have tubular structures that hold nectar and allow the plant to discriminate between different flower visitors, favoring pollinators with appropriately sized mouthparts and preventing non-pollinating animals from stealing the nectar. Orchids are an extreme example, with flowers of some species mimicking the female of a particular wasp, with which the male wasp attempts to mate— thereby pollinating the flower (figure 2.5). It may not be a coincidence that orchids are megadiverse, with around 25,000 species worldwide. Another benefit of animal pollination is that it helps rare plant species to persist, as the pollinators are good in finding even highly scattered plant individuals that they prefer. This benefit may be especially important in tropical forests, where there are commonly hundreds of species per hectare, most of which are necessarily uncommon. A recent study estimated that there are 3.9 × 1011 tree individuals in lowland Amazonia, representing around 16,000 tree species (ter Steege et al. 2013). Of these species, 227 species account for half of all tree individuals in Amazonia, while the rarest 11,000 species account for only 0.12% of the trees. Insect pollinators are probably the reason that many very rare cross-pollinated species can persist at all. Animals are also involved in the distribution of seeds. Long-range seed dispersal is an important element in the Janzen-Connell hypothesis about the maintenance of high diversity of tree species in tropical forests (chapter 1). According to this hypothesis, seedlings that germinate close to the parent tree have a higher likelihood of being attacked and killed by host- specific predators and pathogens than seedlings located far from trees of the same species. Such a mechanism would tend to maintain sparse distribution of species, which requires both efficient pollinators and efficient seed dispersers. Turning to evolutionary history, the earliest evidence of angiosperms is fossil pollen 140 to 130 mya, though estimates based on molecular divergence put their origin at 180 to 160 mya or even earlier (Grimaldi and Engel 2005). The greatest diversification occurred approximately 115 to 90 mya in the late Cretaceous. The early angiosperms were weedy herbs and shrubs, but by the end of the Cretaceous, woody species were common and started to replace conifers as dominant tree species. The symbiotic relationship between angiosperms and insect pollinators may have started as early as 140 to 130 mya, and the origin of the most significant groups of pollina-

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Fig. 2.5 The flower of the bee orchid (Ophrys apifera) has a bee-shaped lip. The flowers are either self-pollinated or pollinated by bees in the genus Eucera, which are attracted by a scent that mimics the scent of the female bee. Moreover, the lip of the flower is a decoy that the male bee confuses with a female. (Modified from © 2015 Miles Kelly / fotoLibra.)

tors has been estimated to be 120 mya (Grimaldi and Engel 2005). Without doubt, radiations of pollinators and many groups of angiosperms represent coevolution. In many cases, including some orchids, coevolution can be very specific, concerning just a single species of plant and a single species (or genus) of pollinators, especially bees, which are the archetypal insect pollinators. In contrast, coevolution between plants and herbivorous insects is more diffuse, involving large numbers of species. Among the bees, of which there are approximately 20,000 living species, the honeybee is of special importance to humans. The honeybee originated from Southeast Asia, where there are six other species apart from the domesticated Apis mellifera. The value of the “service” that the honeybee provides to humankind is billions of dollars per year, and indeed pollination both by the honeybee and wild pollinators is one of the best-characterized and understood ecosystem ser-

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vices (chapter 6). Apart from bees, many wasps, flies, butterflies, moths, and beetles pollinate particular groups of plants. Considering global biodiversity, radiation of angiosperms and the associated insect species has been the major theme in the development of biodiversity on land in the past 100 million years. For comparison, biodiversity in seas has remained relatively constant since the Cambrian, for 550 million years, notwithstanding the five episodes of mass extinction and the subsequent periods of recovery. In contrast, there was little biodiversity on land before the Permian, 299 to 252 mya, after which the diversity of insects and plants has kept increasing (figure 1.4). Evolution Now “Beautiful hypotheses and ugly facts.” This is the subtitle of a book published by Dennis Chitty, a Canadian ecologist who moved to Oxford in 1937 to join Charles Elton’s Bureau of Animal Population. Elton is the forerunner of population ecology, the study of how and why populations of plants and animals vary in time and space in the way they do. One striking ecological wonder is the regular population cycle of boreal voles and arctic lemmings (figure 6.2). Toward the peak of each cycle, lemmings often participate in mass migrations before they suddenly disappear, which made people think that desperate animals commit mass suicide, iconized in the images of lemmings jumping off cliffs. Natural historians in the sixteenth century explained the sudden appearance of thousands of lemmings in the early phase of the cycle by lemmings falling out of the sky during stormy weather. Elton was the first to systematically collect data on small-mammal population cycles. He published a pioneering paper on the subject in 1924 and an influential book in 1942, but the explanation for cyclic dynamics was not convincing. There is still no agreement, though ecologists now agree that there is no single cause that would apply to all species in all environments. Regular cyclic dynamics may be generated by many mechanisms that share one critical feature, namely that the regulation of population size involves a temporal delay, without which population size would remain more stable. Over the years, a large number of processes that involve delayed effects have been proposed, such as physiological and hormonal regulation of reproduction, maternal effects, territorial behavior, interaction with food plants and disease agents, and predator-prey dynamics. In Oxford, Chitty became interested in cyclic populations, and he developed an entirely new

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idea of the causes of cyclicity, based on individual variation in behavior and reproduction. This was a radical departure from the prevailing theories of population dynamics, which were focused on changes in the numbers of individuals due to births, deaths, and movements, but which ignored variation among individuals other than that due to sex and age. This is now history, and ecologists have become increasingly aware that just counting numbers of individuals is often not enough: individuals are different, and these differences may have important consequences. Ecologists have realized that better understanding of population dynamics can be achieved by taking into account individual variation that exists in practically all life-history traits. From here it is a small step to the idea that genetic variation among individuals, which underlies much of the variation in life-history traits and in phenotypes in general, might influence ecological population dynamics. This is a radical idea, because it assumes that ecological and evolutionary dynamics can interact. Rate of reproduction and the risk of death among individuals vary partly for genetic reasons; hence the genetic makeup of populations should indeed influence their demography, while demographic changes influenced by variation among individuals will lead to changes in the genetic composition of populations. In the past two decades, researchers have become increasingly interested in merging ecological and evolutionary dynamics under the rubric of eco-evolutionary dynamics (Pelletier et al. 2009). It is of course true that major evolutionary changes typically take a long time, as shown by the fossil record, but this perspective misses the point that large changes over long periods of time must be the result of small changes over short periods of time. Dennis Chitty had this “beautiful hypothesis” in mind earlier than others did, but unluckily he used it to explain population cycles of small mammals, for which it did not work (hence the “ugly facts”). But this was not apparent in the beginning; the Chitty hypothesis could have worked along the lines that he reasoned about vole cycles. Assume that individuals differ in how aggressive they are, which is a fact. Assume that these differences are caused by genetic differences, which is likely to be true at least to some extent. Assume also that the more aggressive individuals are favored by natural selection when population density is high and competition for space and food resources is fierce. The aggressive individuals do well in individual-toindividual competition, but they bear the cost of low rate of reproduction; hence, when the frequency of aggressive individuals in the population becomes high, the population size declines. When density has dropped to a

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low level, selection starts to favor nonaggressive individuals with a high rate of reproduction, and the next cycle is ready to start. The delay in generating cyclic dynamics is due to the fact that frequencies of aggressive and docile individuals cannot change suddenly. The Chitty hypothesis remained controversial for many reasons, but the final blow came when empirical studies showed that the heritability of the relevant behavioral traits is not high enough to lead to the observed fast changes in the relative abundances of different types of individuals (recall that when heritability is low, the response to selection is weak). It also did not help the Chitty hypothesis that empirical evidence had accumulated that explained small-mammal population cycles by other factors, especially by interaction between small mammals and their predators (chapter 6). The failure of the Chitty hypothesis may have discouraged population ecologists from entertaining eco-evolutionary dynamics until recently. Nevertheless, none of this detracts from the value of Chitty’s pathbreaking work, which highlighted how ecological and evolutionary dynamics could play together to explain interesting population dynamics. Fashion is an important feature of any collective human enterprise, and science is no exception. When a seemingly important new observation has been made, or an exciting new idea or theory has been put forward, researchers flock together like moths congregate at bright light during night, to contemplate whether and how their own data and results could be used to inform the new advance. This is understandable from the viewpoint of individual researchers, and beneficial for science in general, because this is an efficient way of testing whether there is anything of real importance in the new observation or idea. Often there is not, and researchers start looking for something else. In the past decade, more researchers have become interested in eco-evolutionary dynamics, and more examples of fast evolutionary changes and of coupling between ecological and evolutionary dynamics have been documented for wild populations. Returning to Darwin’s finches, the long-term study conducted by Peter and Rosemary Grant since the 1970s has produced an iconic example of rapid evolution and a good understanding of exactly why an episode of rapid evolution occurred (Grant and Grant 2008). In 1977, the Grants documented severe drought on one of the islands in the Galápagos, Daphne Major. The drought was so severe that 85% of one of the finch species, the medium ground finch (Geospiza fortis), died. Before the drought, the finches fed on small and soft seeds that were plentiful. The drought, however, hit

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hard the annual plants that produced small seeds. The finches depleted the standing stock of small seeds on the ground, and they had to turn to large and hard seeds, which were now relatively more abundant. It became evident that variation among individuals really matters. Larger individuals of G. fortis with larger and stronger beaks could crack large and hard seeds with relative ease, whereas small individuals could not, or they had to spend much time to succeed. This had consequences for the survival of the birds; small birds died at a higher rate than large ones, and for that reason the average beak and body size in the population increased over the next year. Beak size has high heritability, and hence there was a measurable evolutionary change in the population in the next generation: the population now consisted of larger birds with stronger beaks on average. This situation prevailed for several years, until 1983, which had an exceptional El Niño, when rains continued for eight months. The species composition in the plant community changed again, and now plants that produced small and soft seeds became common. Under these conditions, smaller birds with smaller and more pointed beaks performed better, and the direction of natural selection changed: average body size decreased, close to the size of birds before the drought in 1977. The shape of the beak, however, did not return to exactly what it had been before 1977. The birds had more pointed beaks after 1983 than before. This appears to represent another adaptive shift: birds with fine tweezer-like bill tips had an advantage in being able to pick up small soft seeds from the soil and rock crevices (Grant and Grant 2014). The main message is that when environmental conditions change, the strength and even the direction of natural selection may change, and so over the short run, evolution rambles around in the abstract space delimited by the traits of the species. The finch population on Daphne Major also exemplifies the reciprocal effects between demographic and evolutionary dynamics: the ecological conditions set the stage for selection, but reproductive performance and demographic dynamics were greatly influenced by the kinds of birds that were present in the population, which was the result of past ecological and evolutionary dynamics. Peter and Rosemary Grant’s results have greatly influenced how biologists think about natural selection, speciation, and radiation, but these results have also attracted the attention of creationists and those who advocate an “intelligent design” as the blueprint of evolution. Creationists claim that the Grants’ results highlight problems in the interpretation of evolution. Evolution does not proceed slowly and majestically in one direction— so how can it produce new species?— and Darwin’s finches are not proper

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species after all, because, according to the Grants’ results, they can hybridize with each other; they are just races of the same species. These views are based on simplistic concepts of species and evolution, and unwillingness to think about how short-term microevolutionary changes are related to longterm macroevolutionary changes as documented in the fossil record. It is unfortunate, and sad, that some people refuse to even think about the exciting history of life on Earth, although we ourselves are part of it, as is compellingly revealed by the rich fossil record and the makeup of the genetic code that we share with all other living organisms. People who consider evolution a mere theory rather than a fact have been badly failed by their education. Fast evolutionary changes can be expected to take place when there are fast changes in the environment, which alters the strength and often the direction of natural selection. At present, many environments change rapidly because of what we humans do, and it is not surprising that many examples of fast evolutionary change originate from such situations. For instance, consider eutrophication of lakes and water bodies, a global environmental problem. Eutrophication changes the composition of algal communities, which are consumed by many small animals; hence the situation is comparable to Darwin’s finches encountering different kinds of seeds, depending on the environmental circumstances. In Lake Constance near the Alps, the water flea Daphnia galeata evolved in response to a period of eutrophication in the 1960s and 1970s, which increased the abundance of cyanobacteria, poorquality food for Daphnia (Hairston et al. 2001). In their work, researchers took advantage of a special feature of Daphnia, namely that they have dormant eggs that remain viable for a long time in lake sediments. Researchers could thus do experiments using Daphnia genotypes that occurred before the period of eutrophication and genotypes that were present after it. Juvenile growth rate of both kinds of Daphnia was reduced by low-quality food, but the reduction was smaller in the case of Daphnia sampled after the eutrophication. The logical conclusion is that these water fleas had evolved to perform better while consuming cyanobacteria, which they had encountered for many generations. Just like Darwin’s finches, the water fleas showed a fast evolutionary response to environmental change (Ellner et al. 2011). All species in natural ecosystems interact with many others in the sense of ecological dynamics, but these interactions may also involve fast evolutionary changes. For instance, herbivores often reduce the growth rate and reproductive success of their host plants, because plants have responded to herbivory by allocating resources away from growth and toward many kinds

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of defenses, such as changes in the structure of leaves and stems and in secondary chemical substances. An experimental study of the common evening primrose (Oenothera biennis) showed just how fast plants could change when they were experimentally protected from insect herbivores (Agrawal et al. 2012). In study plots from which insects were excluded, the plants showed reduced resistance to insect herbivores, owing to changes in flowering times and lowered concentration of defensive secondary compounds, but they showed increased competitive ability against other plant species. Apparently, maintaining defenses is costly to the primrose, and the plants quickly evolved to avoid this cost when the need for defenses was reduced, while the resources thus saved were used to improve the ability to compete against other plants. Temporal variation in the environment often alters natural selection; the spatial structure of the habitat combined with movements of individuals may have comparable consequences. The Glanville fritillary butterfly (Melitaea cinxia) lives in a large network of about 4,000 small dry meadows in the Åland Islands in Finland. In chapter 5, I describe a long-term research project on this species and what has been learned about the conditions that allow species to persist in highly fragmented landscapes. A local population inhabiting one small meadow is small and has a high risk of local extinction; hence a necessary condition for long-term persistence in the patch network is that dispersing butterflies establish new populations on currently unoccupied patches sufficiently often to compensate for local extinctions. We have surveyed the entire patch network for butterfly populations for more than twenty years, and we have sampled butterflies from old local populations and from newly established populations. For practical reasons it is not possible to sample the colonizers themselves, but we can sample their offspring. The main finding is that butterflies from new populations and those from old populations differ systematically from each other in many respects. The new-population butterflies have higher flight metabolic rate, which enhances their movement capacity, and indeed in experiments conducted in the field (figure 2.6), butterflies from new populations flew longer distances on average than butterflies from old populations (Ovaskainen et al. 2008). Flight metabolic rate has high heritability; hence we may conclude that the reason for greater flight capacity of the new-population butterflies is that they inherited it from their mothers, the butterflies that dispersed from their natal population to another meadow to establish a new population. The finding itself is not surprising— if there is variation among butterflies

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Fig. 2.6 The flight paths of free-flying butterflies can be tracked with high accuracy using harmonic radar. The radar signal reflects from the light antenna that has been attached to the abdomen of the butterfly. This figure shows the flight paths of six Glanville fritillary females during two hours. The paths of three females originating from newly established populations are shown in black; the flight paths of three females from old local populations are shown in gray. Females from new populations are generally much more mobile than females from old populations, for reasons explained in the text. (Data from Ovaskainen et al. 2008.)

in dispersal capacity, surely the better dispersers are more likely to establish new populations than an average butterfly— but it is an important one, because it shows that natural selection is likely to enhance dispersal capacity in species that inhabit a highly fragmented landscape with frequent local extinctions and recolonizations. And not only dispersal capacity, but other traits, including traits related to reproduction, are associated with dispersal rate. Natural selection cannot produce better and better dispersers forever, however, because there are physiological constraints on how fast and how far butterflies can fly, and because being very dispersive has costs, such as

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less resources and time available for reproduction. So the level of dispersal in a particular environment represents a compromise, which depends on the costs and benefits of dispersal under particular environmental conditions. We can predict that butterflies in highly fragmented landscapes are, on average, more dispersive than butterflies living in more continuous landscapes, and this is what has been observed (Duplouy et al. 2013). Here is another example of feedback between ecological and evolutionary dynamics: the ecological processes of dispersal and recolonization select for certain kinds of butterflies, and these butterflies are better at establishing new populations, a key feature of large-scale ecological dynamics (often called metapopulation dynamics; chapter 5). The opposite situation occurs in very isolated populations, such as populations on islands that are far from any other population. Here dispersers are at a definite disadvantage, because all those who leave the population necessarily perish, and no immigrants arrive from elsewhere; natural selection is expected to reduce dispersal rate. This explains the reduced flight capacity of many insects and birds on oceanic islands, where some species have entirely lost flight ability. Being flightless is not an option for butterflies, however, because they need to fly to find mates, to forage on flowers, and to search for larval host plants, not only to disperse to other populations and habitat patches. Often there are multiple solutions to the same problem, however, as we discovered while studying a unique population of the Glanville fritillary on a very isolated small island in the Gulf of Finland in the Baltic Sea (more about this population in chapter 5). The population has been on the island at least since the 1930s, and it is known to suffer from reduced fitness due to high frequency of deleterious genetic variants, which have become common through long-term inbreeding (Mattila et al. 2012). The butterflies can fly, but my assistant who reared them in captivity commented that they were unusually tame: when she persuaded a butterfly to climb on her finger to move it into another cage, the butterfly tended to stay on the finger, even if the assistant attempted to shake it off. Butterflies from other populations flew away quickly. Could the butterflies from the isolated island have evolved behavior that would allow them to attach themselves firmly on the substrate, to avoid being blown off the island in a windy day? Anne Duplouy, a former postdoc of mine, did an experiment by measuring how strong a wind the butterflies could resist while standing on a surface (Duplouy and Hanski 2013). The wind was generated with a hair dryer, which was placed at different distances from the butterfly— not all experiments require fancy

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equipment! And indeed, butterflies from the small island were able to resist two and a half times more force than butterflies from a mainland population. On close examination, the island butterflies have evolved a better grip by having significantly more-curved tarsal claws on their legs than butterflies from mainland populations. Note that this difference had evolved in spite of small population size and hence limited genetic variation. The lesson is that if natural selection is very strong, it may lead to an adaptive change even in a small population. If populations respond to environmental changes by evolving fast, is it possible that such evolution could rescue a population from extinction? This apparently happened in the Geospiza fortis population on Daphne Major in the Galápagos after the exceptional drought year in 1977, when 85% of the individuals died and the survivors were on average larger birds with stronger beaks. If the population had not responded with an evolutionary change, it probably would have perished in a few years’ time while forced to use large and hard seeds, difficult for small birds to handle. In the case of the water flea Daphnia galeata in Lake Constance, eutrophication had a negative effect on adult body mass, because eutrophication increased the abundance of cyanobacteria, poor-quality food for Daphnia, which reduced growth rate. This was compensated by juveniles having evolved a higher growth rate under eutrophic conditions. In a quantitative analysis, the evolutionary response was one-third the magnitude of the ecological response, and thus the evolutionary response offset a third of the effect of deteriorating food quality on adult body mass (Ellner et al. 2011). In this case the evolutionary change was not strong enough to entirely compensate for the deterioration in the quality of the environment. The same is true about species living in fragmented landscapes. Habitat loss and fragmentation may select for increased dispersal capacity, but this comes with a cost, and ultimately a limit is reached where no evolutionary change is enough to compensate for the direct negative effect of habitat loss and fragmentation. An evolutionary rescue is possible under some circumstances, but we cannot rely on evolution to solve the biodiversity crisis caused by environmental deterioration. Messages 1. Madagascar is an example of how a unique fauna and flora evolves in a very large island (half a million square kilometers) when it remains almost completely isolated from the rest of the world for 100 million years. The few

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successful colonists have given rise to remarkable evolutionary radiations, groups of species that have a common ancestor but that have diverged in their ecologies. Primates are an example, with approximately 100 species of lemurs that have all descended from one colonist 65 mya. Lemurs now constitute 20% of all primate species in the world. 2. New species commonly arise when the geographical distribution of a widely distributed species is split into two or more isolated parts by some barrier to dispersal. Populations in the separate parts of the original distribution of a single species evolve independently, adapting to their respective environments and accumulating genetic differences, which will ultimately prevent interbreeding if populations become connected in the future. This is how new species arise. 3. Evolution occasionally produces a radically new feature in the biology of species, a key innovation that opens up new opportunities to adapt to the environment. The key innovation, which is inherited by the new species, may allow species to expand their geographical ranges. It also often increases the rate of speciation and thereby accelerates the speed of evolution. 4. Biodiversity on land started to increase rapidly approximately 100 mya when reciprocal evolution, called coevolution, between angiosperms and pollinating and herbivorous insects increased speciation rate. In coevolution, species respond to evolutionary changes in each other, leading to a neverending race to persist in a changing world. 5. Evolutionary dynamics are commonly thought to occur on a much longer time scale than ecological dynamics, but new research has shown that often the two kinds of dynamics are coupled with each other (ecoevolutionary dynamics). Evolutionary adjustments in a rapidly changing world can increase the viability of populations and prevent extinction (evolutionary rescue), though more commonly the evolutionary changes compensate only partly for the reduced fitness of populations due to adverse environmental changes. Therefore, we cannot outsource the solution of the biodiversity crisis to evolution.

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Changing Biodiversity

Island Area Maximum elevation Age Time since isolation Current isolation Inhabitants Breeding birds Endemic birds Butterflies Flowering plants

Haminanluoto* 2 hectares 4 meters 1,600 years No mainland connection ever 200 meters None 14–17 species None 4–7 species 72 species

*Top of photo.

My First Island

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he first island that I ever visited is called Haminanluoto, in the eastern part of the Gulf of Finland in the Baltic Sea. I cannot recall the first visit in the summer of 1953; I was five months old (figure 3.1). The crossing from the shore was ten minutes in a small rowboat, in the company of my father and my mother. Haminanluoto is an islet just outside the small village where my father was born. The village was established in the early seventeenth century by Erik Hannunpoika (meaning the son of Hannu), a maritime pilot appointed by the king of Sweden and of Finland, which was then part of 77

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Fig. 3.1 Getting ready for my first island trip with my father in the summer of 1953. Notice the tall vegetation in the yard, which was the norm in those days. I remember my grandmother picking flowers from the yard; I do not think that she would have preferred a lawn. Even a small patch of meadow vegetation supports hundreds of species of plants and insects, while a lawn would have very few. People’s aesthetic preferences influence greatly the survival of thousands of species in built environments.

Sweden. Erik’s father and his grandfather practiced the same profession on the island of Pitkäpaasi, on the Russian side of the current national border. Life was unsettled, with frequent skirmishes with Russians. In the summer of 1571, the entire village on Pitkäpaasi was conquered and burned down. Erik Hannunpoika’s grandfather is believed to have been killed, but his father escaped and settled in a village a few kilometers inland from the coast. He prospered, and so did his son Erik, who is recorded to have owned, in 1620, 1 horse, 2 oxen, 12 cows, 4 bull calves, 6 heifers, 10 sheep, 10 lambs, 2 pigs, and 2 piglets; and he had rye, barley, and oats in his fields. In spite of all this wealth, Erik seemed to have yearned to move next to the sea, which he did in 1625. Erik Hannunpoika is my ancestor, thirteen generations back. I spent all the summers until I graduated from high school in the small village that he founded. The name of the village is Hanski, a name which I have inherited, and which was probably Hannu’s nickname. The name Haminanluoto must originate from the Swedish word hamn, harbor. Haminanluoto thus means the islet of the harbor, a fitting name, as Haminanluoto is located on the border of deep water and the shallow bay in front of the village; bigger

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ships had to be anchored at the edge of the deep water. The sheltered position was a big advantage for the village, as was easy access to the open sea. Fishing in the coastal waters occupied much of the villagers’ time, but many of them sailed farther, to the coast of Estonia, across the 100-kilometer-wide Gulf of Finland, to trade herring for grain and spirits. What is the origin of Haminanluoto, and how old is it? These are easy questions for islands along the coast of Finland, where land has gradually lifted above the sea because of release from the pressure of a glacier that was 2 kilometers thick. I have read that another 100 meters of land uplift will take place; what is surprising is how regular the uplift has been, 2.5 millimeters per year in this part of the Baltic, with no jolts and jerks that one could notice. Because the islet has emerged from the sea, it has never had a land connection, which influences the kinds of plants and animals that have been able to colonize it. In this case the obstacle to dispersal is not great— only 200 meters. Knowing the height of the islet, 4 meters, and the rate of uplift, 2.5 millimeters per year, we can calculate the age of Haminanluoto: 1,600 years. I visited Haminanluoto often when I was a child, first with my parents, then with other boys of my age and on my own. I was interested in birds and owned a pair of binoculars and a field guide. June 6, 1967, was a cool cloudy day, temperature was 15 degrees Celsius at noon, wind was from northwest. Israel had started the Six-Day War with its neighbors the day before, and fighting must have been fierce when I landed in Haminanluoto in the early morning. I had decided to count the numbers of breeding birds on the islet. My notebook does not tell exactly how I did the census, but I remember that I had studied the field methods from a book on birds that I had. The task of surveying the birds was not very demanding, as the islet is only 2 hectares in size and the single pine tree did not much obstruct the view. The result was 36 pairs of birds representing 15 species. Thirty-six years later, in June 2003, I visited Haminanluoto to count the birds with my son, Matti. The early morning was warm and sunny; we did the census as best we could. The number of species was 14, almost the same as in 1967, but the abundance of birds was now much greater, 152 pairs in comparison with only 36 in 1967. The biggest surprise was a greylag goose (Anser anser), which jumped into the air from its nest on the far corner of the islet. Matti was as startled as the goose, and I was delighted. When I was a boy in 1967, the greylag goose was a rare bird on the south coast of Finland; I do not remember having ever seen it. The third census took place

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in early June 2013, when I visited Haminanluoto with my student Reima Hyytiäinen. Reima has much experience in conducting bird censuses; he works part-time for a consulting company, which takes him from north to south in Finland, from forests and bogs to lakes. I stayed in the small boat off the islet while Reima systematically searched for nests and nestlings, with a shrieking cloud of terns following him wherever he went. I admired his determination and was impressed by his confident count of the birds. I could confirm that, yes, I saw a female shoveler taking off from her nest, and there was only one pair of Caspian terns. The number of bird species was about the same as before, 17 species, and the number of pairs of birds, 141, was similar to my count ten years earlier. I have reproduced the results of the three censuses in table 3.1. Haminanluoto has not been directly affected by people, which helps explain why species number has varied so little, from 14 to 17, over nearly half a century. Yet when you look at the results in the table, the composition of the bird community has changed dramatically; there is little support for the idea of balance of nature, not at least in the sense that species have stable populations. What is especially noteworthy is the increase in the numbers of large-bodied species: swans, geese, ducks, and gulls. In contrast, smallbodied species, waders and passerines, have declined. This change may be related to eutrophication of the entire Baltic Sea, which has increased the food resources for many large species of birds. Here is an important lesson that applies widely: though no environmental changes have taken place on the island itself, changes in the surrounding environment are reflected in the size of the island populations. Another factor that has been decisive over longer periods of time is the pressure from the human population. At the time when Erik Hannunpoika established the village nearly 400 years ago, the chances for swans, geese, and ducks to successfully breed in Haminanluoto and other small islets with easy access from the shore must have been close to nil— people would have collected the eggs and killed any bird they could. One cannot blame them; life was tough. Imagine the long, dark, cold winters in small houses without windows and chimneys. Starvation was not only a possibility but a reality in many years. In the years 1696–97, summers were miserable and the crops failed; nearly a third of the population in the county surrounding Hanski died. Imagine then the spring: days become long and warm, fishing in the sea becomes possible when the ice melts away. A manuscript written by Eljas Raussi, a local self-taught trader, in the 1840s describes the joy of people, young and old, when they could go to islands

Table 3.1. Numbers of breeding birds on Haminanluoto and the body mass of the species 1967

2003

2013

Weight (kg)

Mute swan (Cygnus olor)

—

Greylag goose (Anser anser)

—

—

1

11.0

1

—

3.5

Barnacle goose (Branta leucopsis)

—

—

15

1.9

—

6

28

1.5

Shoveler (Anas clypeata)

—

—

1

0.6

Tufted duck (Aythya fuligula)

6

5

4

0.7

Red-breasted merganser (Mergus serrator)

1

—

1

1.0

Great crested grebe (Podiceps cristatus)

1

—

2

1.6

Herring gull (Larus argentatus)

1

5

2

1.0

Common gull (Larus canus)

2

18

35

0.4

Black-headed gull (Larus ridibundus)

2

47

22

0.3

Swans and geese

Ducks and grebes Eider (Somateria mollissima)

Gulls and terns

Great black-backed gull (Larus marinus)

—

1

1

1.5

Arctic tern (Sterna paradisaea)

9

54

15

0.1

Common tern (Sterna hirundo)

6

10

5

0.12

Caspian tern (Hydroprogne caspia)

—

—

1

0.7

Waders Turnstone (Arenaria interpres)

2

1

—

0.11

Redshank (Tringa totanus)

1

1

1

0.11

Oystercatcher (Haematopus ostralegus)

1

1

2

0.4

Ringed plover (Charadrius hiaticula)

1

—

—

0.05

Common sandpiper (Actitis hypoleucos)

1

—

—

0.06

White wagtail (Motacilla alba)

1

1

2

0.02

Wheatear (Oenanthe oenanthe)

1

1

—

0.02

Passerines

 Species

15

14

17

 Number of bird pairs

36

152

141

 Total biomass (kg)

11.7

51.1

117.0

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in early summer, to fish and, I trust, just to enjoy life, having survived the winter (my translation): Long are the days at springtime Short and gay are the nights To watch fish spawning And waterbirds courting.

No chance for ducks and geese to rear their young. Much later, 100 years ago, with better boats and guns, the situation for waterbirds was not any better. The first scientific surveys at the end of the nineteenth century and in the beginning of the twentieth century documented a decline of duck populations on the south coast of Finland. I remember my grandmother telling how the villagers used to erect a big bonfire on Haminanluoto to celebrate midsummer— not much regard for the birds and their chicks. The bird community that I surveyed over a half a century showed no decrease in species number; if anything there was a slight increase. In contrast, the species composition has changed greatly, and less than half the species were recorded in each of the three censuses. Naturally, one should not rush to draw far-reaching conclusions from one bird community on a single small island. Fortunately, many researchers have examined the same questions in many other communities with proper studies. Maria Dornelas and her colleagues (2014) have analyzed data from 100 studies of animal and plant communities across the globe, each data set covering on average twenty years, though some were as long as forty years, the length of time covered by my bird censuses in Haminanluoto. The 100 communities included 35,613 species of mammals, birds, fishes, invertebrates, and plants, a huge sample of species. Some communities showed decreasing species richness over time, but others showed the opposite trend, and on average species richness had not changed significantly in one way or another. What had changed greatly, and more than expected, was the species composition in these communities, so much so that roughly 10% of the species in each community were replaced each decade, on average, by some other species. As it happens, this is roughly the same amount of change in the species composition that I recorded in the bird community in table 3.1. What should we think about these results? Do they show that concern about biodiversity loss is misguided? Not necessarily. Species richness in communities that have been little affected by humans may stay about the

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same, and such undisturbed communities are the ones that are likely to be studied by researchers for a long time. Haminanluoto is an example, with no human impact on the island itself. The communities analyzed by Dornelas et al. (2014) include both pristine and human-affected study sites, but apparently the environmental conditions stayed about the same during the course of the study. The result would most likely be different had long-term studies been initiated at localities where the habitat was later converted to something else. An example is the drainage of millions of hectares of peat bogs and fens in Finland, which has changed the environmental conditions to the extent that the populations of well-studied birds and butterflies have become halved in only thirty years, and many species have disappeared entirely from large parts of the country. Or consider the conversion of tropical forests to oil-palm plantations in Malaysia and elsewhere in Southeast Asia. Studies have shown that more than three-quarters of birds and butterflies are lost when forests are converted to plantations (Wilcove et al. 2013). Naturally, these are not surprising results; we can expect a large loss of biodiversity when the habitat is lost. I will return to these questions in chapter 5, on the biological consequences of habitat loss and fragmentation. It is good news that species richness has remained unchanged for decades in areas with limited human influence. But why has species composition in these communities changed so greatly? Dornelas and colleagues (2014) suggest that invasion of exotic species, enhanced by increased trade and transport and by climate change, supply extra species to communities that may have lost some of their former residents. This is indeed a big part of the answer (chapter 4), and it applies also to changes in the bird communities in Haminanluoto and other islands in the Baltic. The species that have turned up in the northern Baltic in the past fifty years include many large-bodied species: the mute swan, the Canada goose, the barnacle goose, and the cormorant. The barnacle goose is an especially interesting case. It used to be a bird of the Arctic region only; most individuals still migrate to the Arctic to breed. But since the 1970s, there has been a rapidly increasing breeding population in the Baltic, apparently taking advantage of change in people’s attitudes (no persecution) and conservation legislation (no hunting season). These observations, and the changes in the species composition of communities documented by Dornelas and colleagues, reflect one of the megatrends in changing biodiversity— globalization of nature, the increase in the populations of species that for various reasons can take advantage of the altered environments and expand their distributions, and the decline of

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large numbers of other species that typically are more specialized in their ecological requirements and have had narrow distributions (chapter 4). The causes of globalization in the natural world are similar to the causes of globalization in human societies, namely, increased connectivity facilitating the expansion of one set of species, languages, or cultures, and the vulnerability of local specialties facing increasing pressure from the expanding types. The Destiny of Large-Bodied Species Most animals are small. The smallest insects, some species of beetles and parasitic wasps, are so small that you can hardly see them, only 0.2 millimeters long. The largest animals are all vertebrates— mammals, birds, reptiles, amphibians, and fishes— but only a few hundred species are really large, comparable in size to our own species or larger. If large-bodied species make up only a tiny fraction of all biodiversity, why do we have such an interest in them? One reason is emotional: we feel sympathy for species that are comparable to ourselves in size and which evidently have substantial cognitive powers apart from just being charismatic in our eyes. The second reason is the role of large-bodied species in ecosystems as keystone species with a disproportionately large effect on other species and ecosystem processes. The third reason is that large- bodied species have had, and continue to have, a troubled time with us humans, and many are in danger of going extinct. Animal groups that now include some of the largest species have small ancestors, indicating that evolution has often favored an increase in body size. A comprehensive analysis of 17,208 genera of fossil marine animals since the Cambrian, 541 mya, demonstrated a systematic increase in average body mass across all groups of marine animals (Heim et al. 2015). In mammals, both the fossil record and statistical analyses of evolutionary trees clearly show a long-term bias toward increasing body size in the course of evolution (Baker et al. 2015). The first placental mammals were insectivores, including Juramaia sinensis, a shrew-sized species discovered in China as a 160-million-year-old fossil. At the other extreme, the largest mammal that has ever lived on Earth is still alive, the blue whale (Balaenoptera musculus), which may weigh almost 200 metric tons. The largest-ever land mammal was the hornless rhinoceros Paraceratherium, which weighed 10 to 15 tons, twice the mass of the African bush elephant, and which was widely distributed across Europe and Asia in the Oligocene, 34 to 24 mya. By these compari-

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sons, the maximum size of mammals has increased 20-million-fold during roughly 150 million years of evolution. If evolution had marched systematically toward larger body size during all that time, it would have had the rate of 0.13 darwins (one darwin denotes 2.7-fold change in 1 million years). In reality, the rate of evolution and even its direction are not constant but change with changing environmental conditions (chapter 2). Thus during a shorter period, 1.6 million years, the rate has been much higher, 2.9 darwins (Evans et al. 2012), but evolution of mammalian body size has not proceeded at this rate for much longer periods. In any case, the above figures illustrate the power of evolution— given enough time, there are no hard limits to what may evolve. A similar increase in maximum body size occurred in dinosaurs, from dog-sized saurischians that lived 230 mya to the largest beast to have ever roamed on land, the herbivorous sauropod Argentinosaurus, which weighed almost 100 tons and lived in South America 100 mya. The general increase in body size over evolutionary time is called Cope’s rule, named after American paleontologist Edward Drinker Cope. There are several scenarios under which natural selection can be expected to favor increase in body size. In the case of dinosaurs that fed on coniferous trees, increase in body size may have been favored as plants became taller. Coevolutionary arms races between predatory and herbivorous dinosaurs, and between predatory and herbivorous mammals, may have propelled an increase in body size, in the predators to overpower their prey, and in the prey to escape predation. Among the predators, competition is likely to be a factor of great importance, as larger individuals are typically superior to smaller individuals in interference competition. The ultimate limit to increase in body size is set by physiological constraints. For instance, very large individuals risk becoming overheated, as the ratio of mass (related to heat production) to surface area (related to cooling) becomes greater with increasing body size. One should note that Cope’s rule is a generalization that is often but not always valid; it does not mean that evolution toward smaller body size never occurs. We can expect it to occur whenever conditions favor smaller individuals. A well-documented example is species of megaherbivores evolving smaller body size on islands, such as dwarf elephants on many Mediterranean islands, which were colonized during periods of low sea level in the Pleistocene. Islands may have low productivity, and limited area means low carrying capacity for populations, which can give smaller individuals an

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advantage. It is tempting to speculate that the small, extinct Homo floresien­ sis, nicknamed the hobbit, on the island of Flores in Indonesia represents another example of insular dwarfism. Evidently, evolution of body size, like the evolution of any other trait of plants and animals, depends on the various advantages and disadvantages of being larger than the other individuals in the populations. The overall viability of large-bodied mammals changed dramatically when one of them—namely, our own species—emerged as the supreme predator and the supreme competitor some tens of thousands of years ago. In fact, a strong influence of hominins on other megafauna may reach much further back in time. Lars Werdelin from the Swedish Museum of Natural History in Stockholm has championed the view that competition between hominins and large predatory mammals (carnivores) goes back as far as 1–2 million years, to the time of our ancestor Homo erectus, which evolved in Africa but subsequently expanded its geographical distribution to Europe and Asia more than 1 mya. (The origin of Homo erectus is still debated; some researchers consider that it evolved in Eurasia.) Werdelin (2013) has documented a decline in species richness, and an especially striking decrease in functional diversity, of large-bodied carnivores in Africa from 1.5 to 2 mya. Hominins could not have competed in sheer strength with beasts such as saber-tooth cats, which went extinct in Africa, but our ancestors may have overpowered other species by cooperation and superior hunting skills, the benefits of evolving hominin cognitive capacity. This is an intriguing idea, which at first appears implausible in view of the low density of hominins, but perhaps the density was higher than we think. Unfortunately, it may be impossible to ever find out how large the populations of Homo erectus really were. What we know is that when our own species spread out from Africa, starting 80,000 to 100,000 years ago, a series of encounters took place with megafaunas that had had no previous contact with hominins. The consequences were lethal: a large fraction of megafaunal species disappeared, first in Australia beginning around 46,000 before present (BP), then in North America around 13,000 BP, a few thousand years later in South America, and lastly in Madagascar around 2,000 BP (figure 3.2). Significantly, the megafaunal extinctions on different continents occurred soon after the arrival of Homo sapiens, suggesting that our species was involved in one way or another. Globally, the number of megafaunal species, defined here as species with body mass greater than 44 kilograms, was around 350 species 50,000

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Fig. 3.2 Humans settled in Madagascar only 2,000 years ago, after which at least 17 species of lemurs went extinct. The species that went extinct are systematically larger than any of the surviving species. Only a selection of species is illustrated in this plate; there are altogether approximately 100 living species, most of which are small and highly endangered. (From Mittermeier et al. 2006.)

BP, after which it at first declined steadily, and then crashed from 15,000 to 11,000 BP, when the human population is thought to have increased (Barnosky 2008). The result was that the number of megafaunal species was halved between 50,000 and 10,000 BP, to less than 200 species, the vast majority of which survive today. What is truly striking are the corresponding changes in biomass. It has been estimated that the pooled biomass of all megafauna was 250 teragrams (1012 grams) 50,000 BP, of which the human biomass was an insignificant 0.01 teragram (Barnosky 2008). Today, the numbers are reversed: the pooled biomass of all wild megafauna is 50 teragrams, while human biomass is a whopping 500 teragrams, twice the mass of all large-bodied mammals before human influence. Moreover, the biomass of domestic mammals amounts to 1,000 teragrams; hence the modern

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megafaunal biomass is approximately 1,500 teragrams, six times greater than what it was 50,000 BP (250 teragrams), which reflects the natural carrying capacity of the planet. The sixfold increase has been possible because of technological innovations and energy obtained from fossil fuels. Whether it is a worthy goal of the human enterprise to maximize the mammalian biomass on the planet is another matter. Following the wave of megafaunal extinctions at the end of the Pleistocene, 15,000 to 11,000 BP, there are only a few documented extinctions of large-bodied mammals, including the extinctions in Madagascar (figure 3.2). This may reflect to a large extent selective extinctions in the past: those species that were most vulnerable to human influence, for one reason or another, went extinct, while the remaining species are more resistant. Unfortunately, this does not mean that the future is secure for the species that have survived until the present. Quite the opposite: the next 100 years will see another dramatic peak in megafaunal extinctions unless some really effective measures are agreed upon and properly implemented. Of the seventy-four largest terrestrial herbivorous mammals, weighing more than 100 kilograms (Ripple et al. 2015), and of the thirty-one largest carnivores weighing more than 15 kilograms, 60% are threatened by extinction (Ripple et al. 2014). Most of these species have a rapidly shrinking geographical distribution as well as declining overall population size. The main threats are hunting and poaching and changes in land use, deforestation and expanding agricultural ecosystems and plantations. In the case of large carnivores, an additional threat is people’s negative attitudes and unwillingness to share the same environment with these species. Large-bodied mammals are not safe even in protected areas, especially in developing countries, where hunting pressure is often great (chapter 5). Declining and ultimately disappearing populations of large-bodied mammals have many adverse consequences. It has been estimated that 1 billion people rely on wild meat for subsistence (Brashares et al. 2014). This means that populations of wild mammals that are collapsing due to excessive hunting undermine food security for a large fraction of human populations, and thereby increases pressure on remaining forests and land not under cultivation. There are consequences also for the general functioning of communities and ecosystems, as large-bodied herbivores and carnivores have well-documented cascading effects on other species. In Australia, the largest native predator, the dingo, has been suppressed because of the threat it poses to the sheep-farming industry. Reduced predation by dingoes has helped the

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introduced medium-sized predators, the feral cat and the red fox, to proliferate, which has been a major contributing factor in the extinction of thirty endemic mammals since the late eighteenth century (Lindenmayer 2015). Another example is the gray wolf, which has been hunted and persecuted to very low densities or even to extinction over much of its range in Europe and North America. In boreal regions, absence of wolves allows the moose population to increase to very high densities, which practically prevents the regeneration of the aspen tree, a keystone species for biodiversity in boreal forests. Some consequences of the absence of large carnivores affect people in unexpected ways. The debate about wolf conservation in Finland gives an amusing example. One argument against protecting the wolf is that this would prevent people from safely walking in forests and enjoying the ecosystem services (chapter 6), picking berries and mushrooms and relaxing in an environment with measurable health benefits. In reality, the chance of meeting a wolf in Finland without somebody’s help is smaller than winning $1 million in a lottery. On the other hand, the exceedingly high density of moose, in the near absence of wolves, has allowed the deer ked (Lipoptena cervi), a parasitic fly attacking the moose, to increase to such a high density that in many parts of the country, dozens of deer keds will land on a person walking in the forest for a few hours. After landing, the deer keds shed their wings and are ready to start feeding and reproducing. They do not parasitize humans, but they do bite. For many people this is a nuisance only, but others develop an allergic skin reaction, which can be so severe that it truly prevents people from safely walking in forests. Large-bodied mammals and large animals in general have not fared well over the past 50,000 years, especially over the past centuries. The main reason is hunting and persecution, our refusal to accept peaceful coexistence with other large animals. Large species are seldom highly specialized in their habitat selection; hence most large mammals and birds are not very sensitive to changes in land use or to climate change. On the contrary, they are flexible, and some of them are even moving to cities. If human attitudes changed, large-bodied mammals and birds could thrive more than they do now, even if their low rate of reproduction makes them vulnerable to any extra mortality and slows down recovery when conditions turn more favorable. An encouraging example is the improved populations of the four top carnivores— the brown bear, the Eurasian lynx, the gray wolf, and the wolverine— in many European countries, owing to improved conservation legislation, increasingly supportive public opinion, and a variety of practices

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facilitating coexistence between people and large carnivores (Chapron et al. 2014). Recovery and survival of large-bodied mammals and birds is definitely possible even in the human-dominated world. The choice is ours. Beetles and Butterflies Shifting Their Distributions I started my thesis project in Oxford in earnest in the spring of 1977. The thesis was about the ecology of dung beetles colonizing cattle-dung pats in the pastures near Wytham Woods, the locality that had been made world famous by Charles Elton, the forerunner of population ecology. That summer, I sampled more than 32,000 beetles across many pastures, comprising 22 species of Aphodius, the numerically dominant genus of dung beetles in north temperate regions. My aim was to investigate spatial and temporal variation in the numbers of species in this community, in which competition for the shared resource (cattle dung) is likely to be a key factor in shaping the structure of the beetle community. While doing my analyses, I came across a PhD thesis by M. A. Robinson, who had studied the insect remains recovered from Roman wells in the London area, dated to around AD 400. Pieces of beetles’ forewings, mostly made of chitin, were well preserved, so well that they could be assigned to species based on the details of their surface structure, easily observed under a microscope. Robinson identified 11 species in a sample of 208 beetles, of which 7 species were shared between his sample and my sample. Taking into account that Robinson’s sample (208 beetles) was much smaller than mine (32,000 beetles), it is not surprising that I found twice as many species as he did. When the effect of sample size was accounted for in a statistical analysis, I could conclude that species richness was nearly the same in the samples from Roman wells and from my pitfall traps. I was pleased to have demonstrated such long-term stability in species richness, which suggested that the community might be saturated with species; perhaps no more species could stably coexist in the same community because of severe resource competition. But I did not stop there. Pieces of beetles’ wings have been recovered from much older samples than those unintentionally collected by the Romans. British entomologist Russell Coope amassed unique data on insect fossils during his long career, including fossils from the warm interstadial preceding the last cold glacial period. I was thus able to compare my sample with a 43,000-year-old sample from Isle-

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worth in south England. At that time summer temperatures in England were comparable to those prevailing today, and large herbivores, such as reindeer and bison, were abundant. From the dung beetles’ point of view, the difference was not that great; cattle dung is similar to bison dung. I compared my sample from Wytham Woods with a sample of 64 specimens representing 10 species from Isleworth (Coope and Angus 1975). Six species occurred in both samples. Taking into account the effect of sample size on the number of species recorded, I again arrived at the conclusion that species richness was about the same 43,000 years ago as today. This is quite remarkable, especially when we recall that a glacial period happened between the two samples. There is no way that the same beetle community could have persisted in south England during all this time, even if south England was not covered by ice; the climate was very different during the peak of the glaciation, and so were the beetles, which we know from Coope’s studies. The most abundant species in south England during the peak of the glacial period was Aphodius holdereri, a large-bodied species that for long remained unidentified and was a good candidate for a species that had gone extinct following the glacial period (figure 3.3). But it did not go extinct; it was later discovered in the collections of the British Museum of Natural History. The museum specimens had been collected at high altitudes, between 3,000 and 5,000 meters above sea level, on the northern slopes of the Himalayas, during the 1924 British Everest Expedition (Coope 1973). Just as many species have “migrated” back to northern Europe from Asia following the retreat of the glacier, A. holdereri moved in the opposite direction. Naturally, the species may have occurred widely in Eurasia during the glacial period, not only in south England, but in any case A. holdereri makes a good point about large-scale distributional changes. Had it not been found as a fossil in England, we might now wrongly classify it as a high-altitude Tibetan endemic. Of the species in Isleworth 43,000 years ago, in the warm interstadial, two did not return with the others after the glacial period. Aphodius bou­ vouloiri occurs today only on the Iberian peninsula, and A. costalis is known from a region north of the Caspian Sea. In principle, these species could have returned to England along with many others, but they did not. Perhaps their ecology is somehow different, and they do best under some particular conditions, which made their return to northern Europe unlikely. Or perhaps their failure to come back is simply due to historical contingency. We do not know the explanation, but these examples illustrate how the distributions

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Fig. 3.3 Aphodius holdereri, a species of dung beetle that was first discovered as a 43,000year-old fossil in south England, and that was later found living on the northern slopes of the Himalayas. This specimen was collected during an expedition in 1924, but it was correctly identified much later. (Photo courtesy of Max Barclay.)

of species have changed dramatically, even across the globe, in the course of time. If individuals can move a few kilometers per generation, the species could turn up on the other side of a continent after a few thousand years. Average global temperature has changed greatly in the past 500 million years, from values 5 degrees Celsius lower than at present to values 14 degrees Celsius higher. Since 1880, the average global temperature has increased by 0.9 degrees Celsius, which can be largely attributed to the increasing concentration of greenhouse gases in the atmosphere, the result of us humans burning fossil fuels that accumulated over millions of years. Less than 1 degree Celsius may appear a modest increase, especially as there were periods of no increase at all in the early part of the last century, in the 1950s and 1960s, and in the beginning of this century. Insect populations fluctuate wildly, in response to annual changes in weather conditions. Could we nonetheless see a signal of warming climate in changing distributions of insect species in spite of the inevitable noise? That was my ques-

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tion when I received a request to review a short manuscript for Nature, the leading journal in science, in 1995. My task was to find any weaknesses in the study material and in the arguments that the author used to support the conclusions. Reviewing each other’s manuscripts in this manner is the well-established quality-control mechanism in science. Such peer review is often criticized for various reasons, and it has its weaknesses, but no better and fairer method has yet been invented. It is also cheap, as scientists usually do this service to the community for free. I remember that, in my opinion, Camille Parmesan’s material had some minor problems, but the question marks that I scribbled in the margins did not affect the main message of the manuscript, which was accepted and published. Today, Camille’s two-page paper is a classic in the field. So what had Camille done to deserve publication in the coveted pages of Nature? During five years, she traveled across the states of California, Oregon, and Washington on the west coast of the United States, crossing the border into Canada in the north and Mexico in the south, and she went from the Pacific coast to the mountains of Colorado (figure 3.4). The purpose of her travels: to visit as many localities as possible where the Edith’s checkerspot butterfly (Euphydryas editha) had been recorded, and to ascertain whether the population was still alive. Amateurs and researchers alike have accumulated records of populations for more than 100 years. Checkerspot butterflies often appear in well-defined populations at particular sites, which is the feature that attracted the attention of Paul Ehrlich, a renowned biologist from Stanford University who firmly established the concept and theory of local population through his pioneering field studies of Edith’s checkerspot in the 1960s. Many local populations are so isolated from one another that they become genetically differentiated, which is often apparent from the colors on their wings and had made these butterflies popular among butterfly collectors, when butterfly collecting was still a popular hobby. Camille was not interested in wing patterns, however; she had another question in mind: At which localities, among those where the butterfly had been recorded, could she still find them? She considered only localities that had good habitat during her survey; if the population had gone extinct, the cause was not loss or degradation of habitat. The results showed that the two kinds of historical populations, those that had survived and those that had gone extinct, did not occur randomly among all the localities. An especially large fraction of populations in the southern part of the species’ geographical range had gone extinct, and likewise many populations located at low

Fig. 3.4 Camille Parmesan in the field at Big White Mountain in Canada, at a study site where a local population of Edith’s checkerspot (Euphydryas editha) had been recorded in 1977 at 2,240 meters above sea level. This site has very good habitat for the butterfly; nevertheless, the population had gone extinct by the time Camille surveyed the site. (Photo courtesy of Camille Parmesan.)

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elevations could not be found anymore. In quantitative terms, a population in Mexico had four times greater probability of having gone extinct than a population in Canada. Camille’s hypothesis was that the climatic conditions in the south and at low elevations had become less favorable for the butterfly, whereas in the north and at high elevations they had become more favorable. Hence it had apparently “moved” north and toward higher elevations on mountains. It is important to note that this shift north and toward higher elevations is not so much due to migration of individual butterflies but to differential survival of local populations in different parts of the geographical range. At the limits of the past distribution in the north and at high elevation, entirely new populations may actually have been established beyond the old distribution limit, by individual butterflies flying from nearby populations, but this was not something that Camille was attempting to record. When Camille Parmesan’s results appeared twenty years ago, many researchers had their doubts— could the effects of climate warming really be demonstrated so easily by recording shifts in species’ geographical distributions toward localities with previously cooler climates? Today, there is no room for such doubts; the northward march of species has been thoroughly demonstrated for the past century, not only for butterflies but also for birds, plants, and many other taxa (Parmesan and Yohe 2003), even for marine species; the oceans also are warming up (Poloczanska et al. 2013). Much of this research has been conducted in Europe, where natural history and geographical ranges are better known than on the other continents. The changes have been so rapid that they are apparent in the records of individual researchers, myself included. I was an ardent collector of butterflies and moths during my teenage years. In 1972, my last summer before entering the university, I recorded fifty-eight species of butterflies within 10 kilometers of Hanski, a good fraction of the species that I could have encountered. Others have continued recording butterflies in the same region, and it is now known that eight species that used to occur in the 1970s have since disappeared, mostly because the area of their habitat, meadows and bogs, has been greatly reduced. Thus, roughly 15% of the species have disappeared, but like the birds listed in table 3.1, about an equal number of new species have turned up, including species that nobody would have expected to record in Finland in the 1970s. These species used to be denizens of countries with a warmer climate than Finland, and they still are: the butterflies have not changed— the climate has.

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Conditions are especially favorable for recording shifts in species’ latitudinal distributions in Finland, because the generally flat country with relatively homogeneous vegetation extends for more than 1,000 kilometers between latitude 60° north, where the capital, Helsinki, is located, to latitude 70° north, close to the Arctic Ocean. Two of my former students, Juha Pöyry and Mikko Kuussaari, have analyzed with their colleagues recent changes in forty-eight species of butterflies that reach their northern range limit in Finland (Pöyry et al. 2009). Between two five-year periods, 1992–96 and 2000–2004, the species’ northern range boundary has moved northward 7 kilometers per year on average; seven species have moved more than 20 kilometers per year. In general, large mobile species living in forest edges and using woody plants as their larval host plants have showed the greatest range shifts. These species have abundant habitat and are hence in the best position to expand when climatic conditions make that possible. At the European scale, birds and butterflies, the two best-studied groups of animals, moved 37 and 114 kilometers northward on average in 1990–2008, corresponding to 2 and 6 kilometers per year. On the other hand, based on the northward shift in the length of the growing season, birds and butterflies could have been expected to move 212 and 135 kilometers, respectively (Devictor et al. 2012). The lower-than-expected rate of expansion has been called the climatic debt— shifts in species’ ranges are lagging behind the changing climate. Climatic debt is conceptually comparable to extinction debt in the response of species to land-use changes (chapter 5). While the species that used to be more southerly are expanding their ranges northward, the species that occurred at high latitudes in the past do the same— except that, sooner or later, they encounter an insurmountable barrier, the Arctic Ocean. The same happens on mountains, where species are expected to move to ever higher elevations, until there is no more habitat for them to colonize. In the Sierra de Guadarrama in central Spain, butterfly species richness and composition have moved uphill 293 meters between 1967–73 and 2004–5, in good agreement with an upward shift of 225 meters in the mean annual isotherms in the same period (R. J. Wilson et al. 2007). Similar results have been reported for other temperate mountains, but tropical mountains have been less well studied. In March 2013, when I had just turned sixty, I decided to do something special— to repeat the sampling of dung beetles in the Gunung Mulu National Park in Sarawak, which I recounted in chapter 1. I traveled with nine of my students and postdoctoral

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researchers to the same place that I had visited as a young student in the spring of 1978. The travel was of course very different in 2013 than it had been in 1978, when the final leg from the town of Miri took a full day in a longboat. Miri was there, much bigger and prosperous than before, but this time we boarded a plane; less than an hour later, the plane landed at the small airport just outside the park. During my first trip I had witnessed a wall of tall forest by the river, interrupted by small villages and their cultivations. Not much tall forest could be seen from the plane in 2013; most of it had been replaced by oil-palm plantations, which often extended as far as one could see from the airplane window. In 1978, oil-palm plantations in Sarawak covered only 20,000 hectares; today the plantations cover 1 million hectares, and the goal is to double that area by 2020. This huge transformation of the environment left Gunung Mulu an isolated island. At the park headquarters, I inquired about Tapit, my local assistant during the 1978 expedition. To my delight, I was told that he lived just thirty minutes away by boat, in a small Penan village across the river from the park. I went to see him. His daughter was there and translated our discussion. He remembered me and our trapping of beetles. Tapit looked old and frail; I was told that he had high blood pressure. I asked whether he had medication for it: he did not, because it was too expensive. I was told that the villagers were saddened by the oil-palm plantation, soon to extend to the river, next to the park, and only a few hectares of land would be left for them. They had asked whether the company would sponsor schooling for their children, who could barely continue living in the village. No, this was not possible. It was clear to me that though palm oil has brought wealth to Sarawak, the new prosperity is unevenly distributed. Putting aside thoughts about how our planet is being transformed, it was thrilling to be back in the same forest and to walk along the same trails that I had walked as a student. The results are not yet fully analyzed as I write this; some groups of beetles are hard to identify, and there are more than 200 species, including many rove beetles in addition to dung beetles. But the bottom line about the distributions of species on Gunung Mulu is clear enough. The upper and lower elevational distribution limits of those species that have been assessed so far have moved up 110 meters on average in thirty-five years, from 1978 to 2013. Climate warming in northern Borneo has been 0.58 degrees Celsius during the same period (Chen et al. 2009). Models for tropical mountains predict that temperature drops by 0.55 degrees Celsius for a 100-meter increase in altitude (Gaffen et al. 2000). From

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these figures we can calculate the predicted upward shift in species’ elevational distributions, 105 meters in thirty-five years, which is almost exactly what we observed. To summarize, changes in the butterfly fauna in the part of Finland that I know best, in Finland as a whole, in Europe, and in North America show systematic extension of species’ geographical distributions northward, and similar changes have been documented for other animals and for plants. Similarly, species’ elevational distribution limits on mountains have moved upward. The rate of these changes corresponds roughly to the rate of change in the relevant climatic conditions. We do not need to wait for decades to see the consequences of climate warming; the consequences are already here. On the other hand, not all species show the same changes, as discussed below. Move, Adapt, or Go Extinct Human-caused climate change is a global megatrend, comparable in magnitude to the massive conversion of natural habitats across the globe (chapter 5). Both megatrends have monumental consequences for most species, the human species included. These changes are dramatic not because similar changes would not have occurred in the geological history of the planet. The contemporary changes are dramatic because they are so fast. In the past and at present, when environmental conditions turn unfavorable, species respond in one or more of three possible ways: populations may move elsewhere, where conditions are favorable; populations may remain where they are and adapt to the new conditions; or, these outcomes failing, populations just suffer, decline, and ultimately go extinct. By “moving elsewhere” I mean the kind of distributional changes discussed above, consisting of the disappearance of populations where their viability has become compromised, and flourishing of populations elsewhere, where they did not do so well in the past, as well as establishment of new populations beyond the past range boundary. The latter involves movement of individuals to new territory, and the speed of range expansion depends on the movement capacity of individuals. Adapt has several meanings. Classic evolutionary adaptation involves natural selection and changes in the genetic composition of populations— certain genetic variants increase in abundance at the expense of others, because individuals possessing these variants have higher lifetime reproductive success, fitness, than the others, and are hence favored by natural selection

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(chapter 2). But individuals may adapt also by simply adjusting their behavior or physiology in response to changing environmental conditions, which is called plasticity. Moving elsewhere, adapting, and going extinct are all common responses to rapidly changing environments. Expansion of species’ geographical ranges requires that individuals can locate favorable habitat that is beyond the past range boundary but within the spatial range of individual movements. Range expansion is becoming increasingly difficult in human-dominated landscapes, which are often highly fragmented. In a study of Finnish butterflies, there was a striking difference between threatened and non-threatened species (Pöyry et al. 2009): the threatened species showed no range expansion at all, whereas the nonthreatened species moved on average 85 kilometers northward in a decade (figure 3.5). The threatened species are typically habitat specialists, whose habitat has become so scarce that movements from one habitat patch to another are difficult, effectively preventing large-scale movements across landscapes. Most non-threatened species are habitat generalists and do not have such limitations. Similar results have been obtained for butterflies in the United Kingdom: half the species that are mobile habitat generalists have expanded their distributions, whereas the distributions of nearly all habitat specialists have declined, in spite of climate warming, because of habitat loss (Warren et al. 2001). In brief, many common species are habitat generalists and respond to climate warming by shifting their geographical ranges, while habitat specialists have isolated remnant populations with limited chances of movement. The result is homogenization of communities across large areas, globalization of the natural world (chapter 4): common species become ever more common and widely distributed; rare species decline further. If species cannot respond to a changing environment by moving elsewhere, what are the chances of their adapting, on the spot, to the altered environment? Before considering local adaptation, let us note that evolutionary adaptation can occur also in species that respond by shifting their ranges, in which case evolutionary changes may speed up or otherwise facilitate movements. In Europe, the speed of climate change has outpaced the capacity of birds and butterflies to move northward, creating “climate debt,” as I explained above. In this situation, one could expect that natural selection would favor the more dispersive individuals in populations near the range margin, because these individuals can establish new populations faster and farther away, thus leading to faster tracking of the changing environment. In England, the long-winged cone-head (Conocephalus discolor), a species of

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Fig. 3.5 Two examples of changes in the geographical distributions of Finnish butterflies. The poplar admiral (Limenitis populi) on the left is a large butterfly with good dispersal capacity and much habitat in current landscapes (host plant: Populus tremula). The poplar admiral has greatly expanded its range in the past two decades. In contrast, the green-underside blue (Glaucopsyche alexis) on the right is a small species with limited dispersal capacity and more narrow habitat selection (host plant: Vicia cracca). This species has not expanded its geographical range in the past decades; on the contrary, the latest records indicate range contraction. (Reprinted with permission from Pöyry et al. 2009.)

cricket, has two kinds of individuals, those with long wings and those with extra-long wings; the latter are especially good fliers. In Roesel’s bush cricket (Metrioptera roeselii), the contrast is even greater, as short-winged individuals cannot fly at all. Both species have been spreading northward and have established new populations beyond the past range boundary (C. D. Thomas et al. 2001). Significantly, the frequency of the good fliers with longer wings is higher in new than in old populations, indicating that new populations are predominantly established by the more dispersive individuals, as one would expect. My former student Varpu Mitikka worked on the European map butterfly (Araschnia levana), which is one of the butterfly species that have expanded their ranges northward in northern Europe. Varpu examined

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variation in the gene phosphoglucose isomerase (Pgi), which is known to be associated with flight capacity in many butterfly species. Varpu compared populations at the expanding range margin with those in the more central parts of the species’ range. The frequency of the genetic variant associated with superior flight capacity was higher in the marginal populations (Mitikka and Hanski 2010), pointing to the same conclusion that was drawn from the bush cricket studies in England: natural selection has increased the dispersal capacity of individuals in the populations at the range margin, where new populations have been established by the good dispersers. These examples indicate that natural selection may enhance the dispersal capacity of individuals at expanding range margins, but this result also highlights an interesting question that has remained a puzzle in evolutionary biology for a long time. Most species have limited geographical distributions, presumably because they are not adapted to live under the climatic and other environmental conditions beyond their current distributions. The puzzle is this: why do not individuals that occasionally disperse beyond the range boundary establish new populations that would gradually become adapted to the slightly different conditions and would thereby expand the species’ geographical range? One hypothesis is that such adaptation is prevented by gene flow from the old populations within the existing range, which may swamp any new adaptations beyond the range boundary, especially because the new populations are initially small. Small population size also means that randomness in passing different genetic variants to the next generation in reproduction, called genetic drift, is likely to override the strength of natural selection and may thus prevent adaptation in marginal populations. Another contributing factor is the amount of genetic variation, which is often limited in marginal populations, especially in species that have expanded their distributions in the near past. In the Northern Hemisphere, this is a common situation in species that have returned to deglaciated areas following the glacial period. The expansion may have involved a limited number of individuals that carried only a limited amount of genetic variation, while much variation that existed in the glacial refuge populations was lost during the migration. A good example is the beetle Pytho kolwensis, which moved to northern Europe from glacial refuges in Siberia and China. There is much genetic variation in populations in China, but very limited variation in northern Europe (Painter et al. 2007), where the beetle is highly threatened because intensive forestry has eliminated all but a few percent of old- growth spruce forests (the beetle’s habitat selection was described in chapter 1).

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Limited genetic variation may be a contributing factor to the demise of the beetle, reducing the capacity of populations to adapt to changing environmental conditions. Species’ geographical distributions are shifting in response to climate change, just as they have done throughout the history of life. Another common response to warming climate is change in the seasonal timing of growth and reproduction, called phenology, which may be achieved simply by species’ responding to climate cues in the same way as before— if the timing of the cues changes, so will the phenology of the species. Comprehensive data for birds, amphibians, fishes, butterflies, trees, shrubs, and herbs have shown a systematic shift toward earlier seasonal onset of growth and reproduction in Europe and North America, by 2.3 days per decade on average (Parmesan and Yohe 2003). The greatest changes have been observed in amphibians and butterflies. However, one difficulty in interpreting these results is that studies have been conducted in different localities at different times. To overcome this complication, Otso Ovaskainen and his colleagues have analyzed a forty-year time series from a Russian national park north of St. Petersburg, including data for 97 plant, 78 bird, 10 amphibian, 19 insect, and 9 fungal species as well as for 77 climatic variables (Ovaskainen et al. 2013). They showed that different species have shifted their phenologies at different rates, partly because different species respond to different climatic factors, which themselves have shifted at different rates. Phenological events in birds and insects were mainly affected by short-term climate cues, such as variation in temperature and snow and ice cover, but many plants, amphibians, and fungi responded to long-term climatic averages. In this community, species that showed synchronous year-to-year dynamics tended to shift their phenology in congruence. This is not always the case, however, and climate change may disrupt phenological synchrony among interacting species, with adverse consequences to their population dynamics (McKinney et al. 2012). Plastic changes in behavior have allowed many birds and mammals to adapt to changes in land use; for instance, they have established populations in towns and cities. A few years ago, a pair of eagle owls raised a clutch of chicks on the roof of a building in downtown Helsinki, observed by people sitting in a sky bar across the street. Phenological changes may be fast plastic responses, which occur in each generation without any new or special adaptations; it is enough to react to the environment as before. However, phenological changes may also involve adaptive evolutionary changes, that is, changes in the genetic composition

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of populations. Very few studies have succeeded so far in distinguishing between plasticity and adaptive evolution in phenological changes in response to warming climate, largely because conclusive results require a combination of long-term field study and experiments. In a 38-year field study on the forb Boechera stricta, native to the Rocky Mountains in the United States, the first flowering advanced 0.34 days per year, or 12.9 days during the 38-year period ( J. T. Anderson et al. 2012). Experiments demonstrated the operation of directional selection in the current population; in other words, individuals with earlier-than-average flowering time were favored by natural selection. Under current conditions, the flowering time advanced 0.2 to 0.5 days per generation due to selection. Assuming that the strength of selection has remained constant during the entire study period, and that the generation length is 3 years, the predicted genetic response to selection is 2.6 to 6.3 days in 38 years. This means that 20% to 50% of the observed change in flowering time can be attributed to an evolutionary change; the rest is due to plasticity. These results may represent what happens in many other species of plants and animals: phenotypic plasticity and adaptive evolution both contribute to phenological shifts in response to climate warming. Plasticity allows individuals to respond quickly to altered conditions, but without adaptive evolutionary changes, populations could become increasingly poorly adapted, and their extinction risk could increase. In summary, species may track changing environmental conditions by shifting their geographical ranges or by adapting to new conditions. If, for one reason or another, such responses do not take place, and the environmental changes are strong enough to reduce the reproductive performance of the populations, the outcome is bleak; populations lose viability and eventually go extinct. How Fast Is Biodiversity Disappearing? British ecologist Chris Thomas published a paper in Nature in 2004, together with eighteen other researchers, in which they predicted what kind of changes we could expect to take place in the distributions of 1,103 wellstudied species of plants and animals by the year 2050 (C. D. Thomas et al. 2004). To make these predictions, they assembled data on species’ current distributions, which were linked, with statistical models, to the climatic conditions within the geographical areas occupied by each species. In other words, they constructed models to find out the climatic factors that predict

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where each species does occur, and where it does not occur. Naturally, climate is not the only factor that sets the limits of species’ distributions, but often it is the main factor. When the model was successfully constructed for a particular species, it could be applied to different climatic conditions than those prevailing at present, for instance, to the climate predicted to occur in 2050. The ultimate purpose is to predict the species’ new distribution, assuming that climate affects species’ distributions in the same way in 2050 as it does today. Furthermore, these predictions assume no evolutionary changes in the species; the assumption is that the distributions just shift in response to changing climatic conditions. The results for the 1,103 species showed mostly shrinking geographical ranges, especially in species that occurred on mountains, and Thomas and his colleagues concluded that 15% to 37% of all the species that they had analyzed would become threatened by 2050. For some species, no area with suitable climate would remain at all, in which case the species was predicted to go extinct. The article in Nature received huge attention, perhaps more than any other single paper in the history of ecology; it was reported by more than 1,000 TV and radio stations and newspapers around the world. The reason for all the attention was partly due to a misunderstanding, as the article was interpreted as predicting that a third of all species would go extinct, rather than become threatened, by 2050. Still, a large fraction of species that are threatened in 2050 would go extinct by 2100, assuming that environmental conditions do not change for the better. So the message was not distorted very badly after all. Other researchers have pointed out that the predictions rely on many assumptions and hence involve much uncertainty. For instance, species may adapt to some extent to the altered environmental conditions, or they may persist in some corner of their past geographical range in which the climate is favorable, a detail that cannot be taken into account in a model that deals with continent-wide climate. On the other hand, complications can also work in the opposite direction, making the model predictions too optimistic. In particular, many species cannot shift their geographical distributions with warming climate because their habitat is highly fragmented, and hence the change in their distribution lags behind the change in the climate. On balance, the climate-based models of changing distributions give a credible point of reference— what should we expect to happen, other things being equal, with warming climate? Climate change is expected to become a severe threat to biodiversity in the near future, and to some extent it already is. Until now, by far the most

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important threat to species is changing land use— conversion of natural habitats to agricultural ecosystems, plantations, urban and other built areas, and so forth. Habitat conversion will continue in the future, though the absolute size of the areas affected will decrease because most of the more productive land has already been converted (chapter 1). What are the consequences of further habitat conversion? My colleague Atte Moilanen and his coworkers (Montesino Pouzols 2014) have analyzed the known geographical distributions of the 24,757 terrestrial vertebrate species whose threat status has been assessed for the International Union for Conservation of Nature (IUCN) red list. They combined this information with global landuse changes that are predicted to take place by 2040. Under the projected land-use changes, more than 1,000 threatened species are predicted to lose more than 30% of their current range size, 440 species more than 50%, and 110 species more than 70%. These figures are of similar magnitude to those presented by Chris Thomas and his colleagues (2004) about the consequences of climate change. Notice, however, that these two sets of predictions do not take each other into account. In reality, climate change and land-use changes occur simultaneously, and the consequence is more rapidly diminishing distributions of species than predicted by either climate change or land-use changes alone. Moreover, as species cannot move across highly fragmented landscapes in response to climate change, there is an important interaction between the two types of changes, making the prospects for biodiversity even worse. The Living Planet Index (LPI) of the World Wildlife Fund is a global indicator of biodiversity. LPI summarizes population sizes in thousands of well-studied species of mammals, birds, fishes, and amphibians across all the major ecosystems around the world. The figures for 2014 show that populations are on average 50% smaller than in 1970. The decline has been greater in the tropics, 56%, based on data for 3,811 populations of 1,638 species, than in temperate regions, 36%, based on 6,569 populations of 1,606 species (figure 3.6). Some readers may find the strongly declining trend in LPI surprising in view of the results of Maria Dornelas and her coworkers (2014), which I described at the beginning of this chapter. Dornelas and her coworkers analyzed long-term changes in the population sizes of 35,613 species of mammals, birds, fishes, invertebrates, and plants in 100 communities. They found marked changes in the species composition but no overall decline in species richness. How can this result be reconciled with the declining trend shown by the LPI? Species richness is not the same thing

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Fig. 3.6 The Living Planet Index for tropical and temperate populations since 1970. (Data from Living Planet Report 2014.)

as average population sizes in a community, but one might nonetheless expect reduced diversity if many populations became small and hence more vulnerable to extinction. One reason for the apparent discrepancy may be the quality of the data used to construct LPI, which are somewhat fragmentary, based on what studies have been available. On the other hand, it is probable that the 100 long- term community studies in the analysis of Dornelas and others were conducted at sites where the environmental conditions remained relatively stable for the duration of the study. For instance, it is hard to imagine that an ecologist studying forest birds would continue his or her study if the study forest was cut down— not much to study. To obtain a truly representative picture of changes in biodiversity across large areas, one should start with randomly selected study sites and retain these sites in the calculation, no matter what happens to them. If populations on two-thirds of the sites remained stable, but populations on one-third of the original sites were lost because of habitat conversion, we should not base our assessment of global trends in biodiversity on only those sites that were not converted. The above difficulties are avoided and a more objective assessment of the state of and changes in biodiversity can be achieved if the assessment is based on all the existing knowledge on species, assuming of course that the knowledge is sufficiently comprehensive. Since the 1970s, the IUCN

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together with other organizations and with the help of a large number of experts on particular groups of animals and plants have compiled the global red data book. Many countries have followed suit and prepared national red data books, many of which are more complete than the global one. Listing species in the red data books is based on the criteria that were adopted in 1994 (Living Planet Report 2014). The threatened species are classified into three categories: critically endangered (CR), endangered (EN), and vulnerable (VU). For example, a species is classified as endangered if at least one of the following conditions is satisfied: population size has declined by at least 70% during the past ten years or three generations (whichever is longer); the geographical range is less than 5,000 square kilometers; the population has fewer than 2,500 individuals and has declined by at least 20% during the past five years or two generations (whichever is longer); the population has fewer than 250 individuals; a quantitative population viability analysis predicts that the probability of extinction is at least 20% during the next twenty years or five generations (whichever is longer). As is apparent from this account, which has been simplified from the actual criteria, the assessment is based on quantitative data, not just the opinion of people responsible for the assessment. If there is insufficient information, the species is not evaluated at all and is placed in the category “data deficient.” Table 3.2 summarizes results for vertebrates, insects, and angiosperms, giving the numbers of species that have gone globally extinct in historical times, since their description, most often in the nineteenth century, as well as the percentage of threatened species among those that could be assessed. Mammals and birds are known so well that all the species in the world have been evaluated for their conservation status. The figures to remember are these: 1.5% of the species have gone extinct, and 15% to 20% of the species are currently threatened, with a somewhat higher percentage for mammals than for birds. In reptiles, amphibians, and fishes, a large fraction of the scientifically described species are too poorly known to allow their evaluation, but of the species that have been evaluated, less than 1% have gone extinct, and 20% to 30% are threatened. Knowledge on insects is so limited that less than 1% of the species have been evaluated, and the situation is not much better in angiosperms, for which the threat level is nevertheless very high; more than half the species that have been evaluated are threatened. In a recent analysis of 200 randomly selected species of land snails, chosen as an example of poorly known invertebrates, the conclusion was that 7% of the species have gone extinct in historical times (Régnier et al. 2015). Therefore,

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Table 3.2. Percentages of globally extinct and threatened species in vertebrates, insects, and flowering plants in 2014 Number of

Percentage

Percentage

Percentage

described

of species

of extinct

of threatened

species

evaluated

speciesa

speciesa

5,513

100

1.4

21.7

Birds

10,425

100

1.5

13.2

Reptiles

10,038

44

0.5

21.0

7,302

88

0.5

30.5

32,900

38

0.6

17.8

Species group Mammals

Amphibians Fishes Insects Angiosperms

ca. 1,000,000

0.5

1.1

18.7

268,000

6.3

0.6

54.4

Source: http://www.iucnredlist.org (May 2015). Note: For more detailed analyses of birds, mammals, and amphibians, see Pimm et al. 2014. a These values have been calculated for species that have been evaluated.

the well-studied mammals and birds may actually underestimate the proportion of all species that have gone extinct since the year 1600. Let us pause for a moment to reflect on insects. Roughly 1 million species are known to science, but all experts agree that the true number is several million species (chapter 1). There is no way that biologists could ever accumulate detailed knowledge on all the species of insects, comparable to the knowledge that is available for mammals and birds. For smaller areas it is possible to do better, especially in northern Europe, where there is a long tradition of natural history studies. In Finland, with a beetle fauna of 3,640 species, 12.1% of the species are classified as nationally extinct (1.6%) or threatened (10.5%), compared with 15% in birds, 17% in mammals, and 15% in vascular plants (Rassi et al. 2001). These figures are similar to the global figures for mammals and birds (table 3.2), suggesting no fundamental difference in the threat level for vertebrates and invertebrates, though the causes of threat are somewhat different. Because most insect species occur in tropical forests (chapter 1), what matters most for their long-term survival is the fate of the forests. If tropical deforestation continues at the present rate, around 0.5% per year, it is obvious that the result is a mass extinction of tropical forest species, including insects, by the end of this century. Most likely, large numbers have al-

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ready gone extinct in those regions where forest loss has been the greatest. In Madagascar, forest cover has declined by 40% in the past fifty years, and what remains is a highly fragmented landscape (Harper et al. 2007). Most Malagasy insects are poorly known, but there are some exceptions: for instance, the endemic dung beetles in the genus Helictopleurus are relatively large, brightly colored, and well collected by entomologists since 1875. There are altogether fifty-four species, of which fifty species are strictly confined to wet forests. In our intensive trapping of dung beetles across Madagascar for nearly ten years, we collected thirty-three of the fifty species, but not a single individual of the remaining seventeen species (Hanski et al. 2009), which nobody has seen in the wild for the past fifty years or more. The seventeen missing species have been historically uncommon; they are, on average, larger than the rest of the species; and most importantly, the degree of deforestation has been greater within their historical geographical ranges than within the ranges of the other species. It is impossible to conclusively prove that these species have gone extinct, but minimally they should be classified as critically endangered species. Thus Helictopleurus, as an example of wetforest insects, are even more threatened than the well-studied vertebrates in table 3.2. In a similar in-depth analysis of fifty-five endemic beetle species in the Azores, seven species were judged to have gone extinct (Terzopoulou et al. 2015). Just as with dung beetles in Madagascar, species with small historical ranges and large body size have been most prone to go extinct. The figures in table 3.2 show that in the best-known taxa, mammals and birds, 1.5% of the species have gone extinct in roughly the past 200 years, corresponding to 0.8% in 100 years. The extinction rate is often expressed as the number of extinctions per species per 1 million years, but it is easier to grasp the meaning of the unit that I use: what percentage of currently existing species will go extinct in 100 years? For mammals, birds, and amphibians, the documented extinction rate has accelerated, so that it has been 2.5 times higher since 1900 than from 1600 to 1900 (Pimm et al. 2014). Therefore, in birds and mammals the current rate is likely to be roughly 2% of the existing species going extinct in 100 years. Based on the fossil record, the current rate for birds and mammals has been estimated as approximately 1,000 times higher than the background rate, the rate of extinctions before any human influence (Pimm et al. 2014). However, this may be an underestimate for all the species, because the figures cited above on the proportion of extinct species in Malagasy forest dung beetles (34%), in endemic beetles in the Azores (13%), and in a random selection of land snails (7%), indi-

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cate that the percentage of species going extinct in 100 years is substantially higher than 2%, perhaps closer to 5%. Considering the near future, and taking into account that the various estimates of the percentage of threatened species range from 15% to 50% in different taxa, a conservative estimate of the rate of extinctions in the coming decades is 10% of the existing species going extinct in 100 years. What percentage of the species will actually go extinct and by what year critically depends on the magnitude of climate change and land-use changes in this century, and especially on the rate of deforestation in the tropics. One can only hope that societies will realize soon, rather than when it is too late, that the current trend will inevitably lead to a catastrophe. Many ecologists and evolutionary biologists have concluded that we are living in the midst of the sixth mass extinction of species since the beginning of the Cambrian, 500 mya (chapter 1). Most readers have heard about the fifth mass extinction, which terminated the Mesozoic era 66 mya, and was caused by a 10-kilometer asteroid or comet hitting Earth. The amount of energy released in that collision corresponds to the simultaneous detonation of 10 billion Hiroshima-sized atomic bombs. The amount of energy that humanity has released and will release by burning fossil fuels is not many orders of magnitude different; I calculated some years ago that the energy released from fossil fuels would correspond to 300 million Hiroshima-sized bombs. There may be no deeper significance to these figures, but they give us a perspective on the forces involved in the fifth and sixth mass extinctions. To be sure, some paleontologists have argued that the present wave of extinctions is not comparable to the past mass extinctions, in which entire groups of common and widespread species went extinct, whereas the present extinctions concern mostly rare species with restricted distributions. Perhaps so, but if the current trends continue, we need to wait for less than a blink of an eye on the geological time scale for the sixth mass extinction, by any criteria. Besides, taking into account that humans have almost certainly played a decisive role in the extinction of mammalian megafauna in the past 50,000 years, most recently in Madagascar, it is not true that only uncommon species have gone extinct; about half of all large-bodied mammalian species have gone extinct in the past 50,000 years, and many of them used to be dominant species in their ecosystems. I have met people who take some comfort in the thought that, whatever the human impact on species and ecosystems in the coming decades and

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centuries, we will not eradicate all life on Earth. There are indeed many species of animals, plants, and fungi that are even more resilient than our own species, to say nothing about microbes, which occupy the full range of environments from bedrock and deep ocean bottoms to the upper atmosphere, covering environments that are already so inhospitable to life that we can hardly make them worse. Humans have supposedly eradicated smallpox, but this is an exception, a viral disease that emerged in the human population at the time of the agricultural revolution around 10,000 years ago. Microbial life has been present on Earth for more than 3 billion years, and microbes continue to make up the core of life— microbes run the world. If they were gone, we would not be here, whereas the reverse is not true. In the words of Stephen Jay Gould, an American evolutionary biologist, we live in the “age of bacteria” rather than the age of mammals— and the planet has always been in the age of bacteria, ever since the beginning of life. Microbial life may appear so infinitely diverse and adaptable that one might assume it to be entirely immune to human influence. Indeed, we cannot have a big impact on microbes collectively, but the ecosystem transformations that we are causing may have a big effect on the species composition, the kinds of microbes that predominate in the ecosystems, and the kinds of microbes with which we are likely to interact. I return to this topic and possible consequences for our health and well-being in chapter 6. Messages 1. The mixture of species in local communities of plants and animals is so dynamic that up to 10% of species per decade are often replaced by others, even if the total number of species remains about the same. Changes in biodiversity occur for natural causes, but there is one megatrend that is caused by humans via climate change and land-use changes: uncommon specialist species decline and go locally extinct, while common generalist species become ever more common and widespread. 2. In the course of mammalian evolution, body size tends to increase, indicating that large body size confers some general benefit. In the past 50,000 years, with increasing human effect on communities and ecosystems, most large-bodied mammals have declined, and more than half have gone extinct. On the other hand, most large-bodied species are flexible in their behavior and requirements, and they adapt to live in human-dominated landscapes if

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they are not persecuted and killed. The future of large mammals depends on whether humans learn to coexist with them. 3. The geographical distributions of many species are presently shifting northward and toward higher elevations on mountains in response to warming climate. 4. Not all species manage to track the changing environmental conditions by shifting their geographical distributions or by adapting genetically to altered environments. These species are prone to go extinct. Specialist species that occur in uncommon natural habitats are in the greatest trouble, and many of them have survived so far as isolated remnant populations, which have a high risk of local and ultimately global extinction. 5. The current rate of species extinctions is roughly 1,000 times higher than the background rate, the rate of extinctions before any human influence. At the current rate, 1% to 5% of the species that now exist will be extinct in 100 years, but this rate is increasing to the level where 10% to 30% of species will go extinct by 2100. If the extinction rate does not abate soon, the future poses great risks for humans.

4

Species on the Move

Island Area Maximum elevation Age Time since isolation Current isolation Inhabitants Breeding birds Endemic birds Butterflies Flowering plants

La Gomera 378 square kilometers 1,487 meters 5–12 million years No mainland connection ever 370 kilometers (30 kilometers from Tenerife) 21,800 40 species (excluding seabirds) 6 species (present also on other islands in the Canaries) 22 species About 2,000 species (Canary Islands)

Irresistible Temptation

I

arrived at San Sebastian de la Gomera in the afternoon, December 28, 1976. The ferry from Tenerife to La Gomera had taken two hours, and my plan was to reach the village of Agulo on the other side of the island before the evening, a distance of approximately twenty kilometers according to the map. I think there were no buses, and I think I first tried to hitchhike. What I do remember for sure is that I soon started to walk along the road uphill, 115

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ascending toward the center of La Gomera, where the road would continue to the opposite side of the island. I was in La Gomera because of irresistible temptation. With Christmas approaching, I did not wish to go back to Finland, which I left in September to start my PhD studies in Oxford. I had struggled for some time to conceive the topic of my thesis project— the ecology of dung beetle communities— and when this had been settled, I longed to go where I could at least see a dung beetle or two. The dream had been to go to East Africa, where my supervisor, Malcolm Coe, and his other student, Tim Kingston, had been working. I still recall the feeling when I saw the mouse-sized beetles in Tim’s boxes. A trip to African savannas was out of question, of course; I did not have the money or the other requirements. The Canary Islands was a possibility. I landed at Santa Cruz de Tenerife on December 17. The travel itself was an experience, my second time ever in an airplane. I brought some equipment for sampling insects. I spent the first few days looking for cattle and dung beetles, and I realized that with no prior knowledge of what to expect where, and with limited public transport to go from one unknown place to another, I could not accomplish much. Fortunately, metallic green blowflies were everywhere in great abundance, not least in the fish market. I was familiar with blowflies, because I had done my master’s project on larval competition among blowfly species. I went to the entomology department at the University of San Fernando de la Laguna, established in 1701, and I found Marcos Baez Fumero, who could tell me about the blowflies in the Canary Islands. The community was apparently in transition due to ongoing invasion of tropical species. I asked what might be happening to the native species. The answer was not known— and then I knew what I might try to do. I also learned that an endemic species, Calliphora splendens, was found in the montane laurel forests on La Gomera (figure 4.1). I knew other species of Calliphora, but I wanted to see splendens, and that is why I was climbing the road toward the laurisilva in the early evening of December 28. I had reached 1,000 meters elevation, and it became clear that I could not reach the village of Agulo before night. But no worries— I had a sleeping bag with me. I did not have a tent, but what would one need a tent for in the Canary Islands? I took a small trail off the road and started to look for a suitable spot for the night. The trail followed the mountain slope, which was quite steep, and I could not find a flat area. It became dark, it was cloudy, and it started to rain. It was not a storm, but a steady rain, and it became ever darker. I hurried forward but could not find even a few square

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Fig. 4.1 Laurel forest on La Gomera. (Photo courtesy of Hannu Aarnio.)

meters of level ground; the narrow trail just continued and continued. I had no light of any kind, and I drew the inevitable conclusion: I had to stop and spend the night where I was, making sure that there was no real danger of rolling down the slope or sitting in an expanding puddle. I guess it was silly to crawl into the sleeping bag, but that is what I did for part of the night. It was still pitch-dark when I was sitting again on the trail and waiting for the sun to rise. In the morning, I collected two males and eleven females of Cal­ liphora splendens, which looked just as magnificent as their name had promised. A splendid morning! There are two other species of Calliphora in the Canary Islands, apart from splendens, namely C. vomitoria and C. vicina, which are common species across Europe. I sampled the flies in different habitats and at different elevations. It turned out that C. vicina was everywhere, from the seashore to the top of the mountains, but it was especially common in open habitats. Calliphora splendens was the dominant species in the laurisilva, and C. vom­ itoria was uncommon, found here and there. How had these species arrived at the Canary Islands? La Gomera emerged as an island after volcanic eruptions 10 mya, but the environment was inhospitable to plants and animals for a long time, and perhaps only in the past 1–2 million years were many species able to move to La Gomera. Calliphora splendens is found only in the

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Canary Islands, on Tenerife, La Gomera, and La Palma. These islands have remnants of laurisilva, an ancient type of subtropical forest growing in areas with stable and mild temperatures and high humidity. Most likely, the ancestor that colonized the Canary Islands gradually evolved into a new species, adapting to the conditions in the new environment. Later on, perhaps much later on, the two other species, C. vomitoria and C. vicina, also managed to colonize, and these species have not yet greatly differentiated from the populations in Europe. All three species have a common ancestor in the past, and perhaps the lineage that gave rise to C. splendens in the Canary Islands gave rise to C. vomitoria or C. vicina elsewhere. By the time the others arrived in the Canary Islands, however, C. splendens had already become genetically and ecologically different from the others, and it did not hybridize with them. It is noteworthy that C. splendens, the endemic species, is the most highly specialized of the three species, being confined to the special forest habitat, while the latecomers are generalists. The American biologist Edward O. Wilson has contributed many influential concepts and theories in ecology and evolutionary biology, more than anyone else over the past fifty years. Wilson is well known for the equilibrium theory of island biogeography, which revolutionized biogeography and established new aims for spatial ecology in the 1970s (chapter 5), and of sociobiology, but his first major contribution that has survived the test of time is less well known: the taxon cycle (E. O. Wilson 1961). Wilson worked on the ants in the Melanesian islands, especially on how their habitat selection and degree of ecological specialization evolved after the colonization of an island. Researchers continue to debate what exactly constitutes the taxon cycle, and whether it is a distinct phenomenon at all, or rather varies in dependence on the ecology of the species and their environments. One interpretation is as follows. Species that occur in disturbed habitats often make good colonizers, because such species have evolved a great capacity for dispersal to track the changing environment and are often found in habitats near the coast (chapter 2). After dispersal to an island, the species first occur in habitats similar to those on the mainland, but in the course of time, the species and their descendants evolve to occupy other habitats, such as forests. I presume that the ancestor of Calliphora splendens first occurred at sea level, but subsequently evolved to inhabit laurisilva at higher elevations. The shift in habitat selection may have been at least partly the result of interspecific competition with later-arriving species. Apart from blowflies, the Canary Islands have

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likely examples of taxon cycle among its birds. The blue chaffinch (Fringilla teydea), similar to the common European chaffinch but with blue males, is a specialist in the pine forests in the highlands of Tenerife and Grand Canary, while the common chaffinch occurs in other habitats. Among the pigeons, there are two endemic species in the laurisilva, Columba trocaz and C. junoniae. The large dung beetle fauna of Madagascar that was described in chapter 2 has evolved in a similar manner. The ancestral species occurred in open habitats close to the coast, but 60 to 70 million years of evolution has produced the current fauna of about 300 species, most of which live in forests and many at high altitudes. In a nutshell, species that are good colonizers are often ecological generalists that occur in disturbed habitats, but after colonization of a new area, they become more specialized, partly perhaps because of the “push” of later-arriving species. On islands with limited area, the more specialized species have an increased risk of extinction, and while new generalist species arrive, some of the old species go extinct, keeping the taxon cycle moving. I sampled blowflies everywhere I could find them. There are not many species, but they are all interesting. Lucilia sericata, the common green bottle fly, which has a metallic sheen, is a cosmopolitan species that most readers have seen, though perhaps not paid much attention to—unless you are a sheep farmer. Lucilia sericata is also known as the sheep blowfly, because females often lay eggs in the wool of sheep, and after hatching, the maggots (larvae) move down the wool to feed on the skin surface, which may lead to lesions, bacterial infections, much discomfort to the sheep, and great economic cost. Lucilia caesar is a bigger relative that I had reared on rotting fish for my master’s thesis in Finland. It was recorded from the Canary Islands in the nineteenth century but not afterward, and I could not find it. Unfortunately, the old specimens cannot be located in museum collections to confirm their identification— thus important information has been lost forever. This is not a great tragedy in this particular case, but one can imagine situations where it would be critically important to know for sure which species were in which places in the past, and perhaps to obtain DNA from the museum specimens. It would be interesting to know the past composition of blowfly species in the Canary Islands because several new invading species may have had an adverse effect on the old residents. In recent decades, the Canary Islands, like many other tropical and subtropical areas around the world, have been colonized by species in the blowfly genus Chrysomya. One species, C. albiceps, has been known from the Canary Islands for a long time.

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I collected C. chloropyga for the first time in 1977, and yet another species, C. megacephala, was collected in the late 1970s (Baez Fumero et al. 1981). The blowflies inhabit very competitive communities; hence it is probable that invading species influence the residents. The three species of Chrysomya that have colonized the Canary Islands are native to Southeast Asia and Africa. They all colonized Brazil around 1975; since then they have been rapidly spreading across South America, with an apparent negative effect on native species. Thus at a study site in Peru, the native species Cochliomyia macellaria declined from a relative abundance of 89% to a mere 0.2% in only eighteen months, after the invasion by two Chrysomya species (Baumgartner 1988). The European explorers colonized La Gomera and the rest of the Canary Islands in the fourteenth century. San Sebastian de la Gomera is famous as the port where Christopher Columbus sailed to cross the Atlantic in 1492. Much earlier, the Canary Islands had been visited by the Phoenicians, the Greeks, and the Carthaginians. Moreover, when the first modern sailors landed 700 years ago, they found that the Canary Islands were inhabited; there were Neolithic indigenous populations, known as Guanches and thought to have a common ancestry with North African Berbers. In La Gomera, Guanches had developed a unique whistled language, silbo, to communicate across the deep ravines that dissect the cone-shaped mountain in all directions. Surprisingly, silbo was learned by the Spanish colonizers, and it survives today and is officially protected as an example of intangible cultural heritage. Thinking of the indigenous people in La Gomera, it is difficult for me not to think about the Calliphora blowflies, which colonized the Canary Islands in several phases. Calliphora splendens, tracing its ancestry to the original colonizer, has survived in the laurisilva, and I presume that Guanches similarly retreated to the mountains when the Spanish conquerors arrived. There are also important differences. Guanches were not a different species, and they probably interbred with the Spanish before going extinct as a people. Nonetheless, in La Gomera as well as in many other oceanic islands, native people and cultures have succumbed when new colonizers have arrived. There is no need here to elaborate on the moral issues related to the historical expansion of our own species, but if there were impartial observers, they would probably nominate Homo sapiens as the world’s worst colonizer in terms of the impact on other species and ecosystems. Besides, we are responsible, in one way or another, for the havoc done by the world’s other worst invading species.

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The Green Tsunami In the late spring of 2000, I attended a European Union biodiversity forum organized by Portugal in the Azores, with the title “Islands and Archipelagos: European Biodiversity Issues Seen from the Atlantic.” The Azores are in the middle of the northern Atlantic, a series of volcanic islands above a junction of three large tectonic plates. The islands have arisen through volcanic and seismic activity in the past 10 million years; the youngest island, Pico, is only 250,000 years old. According to the booklet that I leafed through during the flight, São Miguel is known as the Green Island, with wonderful flowerbeds by narrow roads, a perfect place for walks and hikes. The environment is indeed perfect for plant growth. The volcanic soils have high fertility and good water-holding capacity, and the climate is temperate throughout the year, with an average temperature of 17 degrees Celsius. The conditions are favorable for plants, but the Azores are very isolated and geologically relatively young; most island terrain is less than 1 million years old. For these reasons, the number of native angiosperm species is low, approximately 200 species (Carine and Schaefer 2010). There is a substantial number of endemic species, but they have not given rise to large radiations, contrary to what has been observed in many other groups of oceanic islands (chapter 2). In addition to the native species, there are more than 600 introduced species, which define the vegetation in the Azores today. The Azores have been known since the fourteenth century. Two islands, Santa Maria and São Miguel, were settled around 1430, by people and by sheep; the latter were set loose to compensate for the lack of any large animals on the islands. At present, the main industries are agriculture, dairy farming, livestock ranching, fishing, and tourism. For tourism, the greenness of the islands is an asset, and it does not seem to matter that much of the greenness is due to extensive pastures dissected by small roads bordered by exotic flowers. Mild climate with enough but not too much rainfall helps maintain lush pastures. The original vegetation consisted of laurisilva as in the Canary Islands, but only a few percent of them are left. The native forests have been cleared for agriculture and for plantations of Cryptomeria japon­ ica, the Japanese cedar, which is grown for timber. One of Europe’s rarest bird species, the Azores bullfinch (Pyrrhula murina), persists in a remaining patch of laurisilva on São Miguel, an area of only some hundreds of hectares. In addition to the forests, all the other plant communities have been altered by introduced and invasive plants from all over the world. Abandoned agri-

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cultural lands are becoming reforested by Pittosporum undulatum, a weedy small tree, and by the Australian blackwood (Acacia melanoxylon), both from Australia, preventing regrowth of the original laurisilva. Cliffs and other coastal areas harbor the American aloe (Agave americana) and prickly pears (Opuntia species) from America, and the sour fig (Carpobrotus edulis) from South Africa. Roadsides are populated by Chilean rhubarb (Gunnera tincto­ ria) from Chile, bearberry honeysuckle (Lonicera involucrata) from China, and angel lips (Lantana camara) from Mexico. The most ominous of all may be ginger lily (Hedychium gardnerianum) from the Himalayas, which has also invaded the remaining fragments of laurisilva. The lush vegetation in the Azores is an incredible assortment of plant species from all over the world. The Azores may be one of the more extreme examples, but oceanic islands in general have been especially vulnerable to invasion by alien plant species (Lonsdale 1999). One hypothesis is the relatively small number of native species on isolated islands. When the number of resident species is small, there are likely to be opportunities, vacant niches as it were, for additional species to establish themselves. In support of this idea, studies of grassland plant communities have shown that experimental reduction of species number makes an area more vulnerable to invasion by other plant species (Knops et  al. 1999). However, it is questionable whether results from small study plots can be extended to large heterogeneous islands, and, indeed, there is no direct support for this hypothesis in island communities (Lonsdale 1999). Another hypothesis, which applies to both islands and mainland areas, states that invasive plant species often reallocate resources, from defense mechanisms against specialist herbivores, into growth and development (Blossey and Nötzold 1995). Defense against specialist herbivores is superfluous in a new area that harbors no such specialists. Note that this hypothesis assumes that the competitive advantage of the invading species evolves over some length of time; the alien species are not immediately superior competitors. One of the examples of fast evolutionary change mentioned in chapter 2 is the common evening primrose (Oenothera biennis). When plants were experimentally protected from their insect herbivores, they quickly evolved reduced resistance to herbivores and increased competitive ability against other plants (Agrawal et al. 2012). In addition to such evolutionary adjustments after colonization, native species on isolated oceanic islands, which have coexisted with a small number of other species during all their evolutionary history, might be less competitive with plant species that have been exposed to a wide range of

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different types of competitors and other interacting species during their evolution. In the case of animals, the iconic example is the dodo, an extinct flightless bird that occurred only on Mauritius. The dodo was a huge bird, up to 20 kilograms, related to pigeons. In the absence of any native predators, the dodo was completely unafraid of humans and hence easy to catch and kill. It is probable that many other species, both plants and animals, that are inhabitants of isolated islands are similarly handicapped with respect to traits that are important in interspecific interactions, and this may explain at least partly why so many species on oceanic islands have succumbed in the presence of alien species. For instance, sailors and settlers have often released pigs, goats, and sheep on islands to have a supply of meat in the future. Alien plants include species that have evolved in the presence of grazing mammals, but the island endemics have not, which gives a competitive edge to the former. Many endemic bird species on oceanic islands nested on the ground and were devastated by rats, cats, and the small Indian mongoose (Herpestes auropunctatus) on many islands. The native vegetation of the Azores has been overrun by hundreds of invasive plant species originating from different corners of the world. Other and even more striking examples of “green tsunamis” include particular invasive species that can increase to astronomical numbers. Tropical ponds, lakes, reservoirs, and other water bodies are often invaded so effectively by single plant species that everything else is practically eliminated. An example of the worst kind is the water hyacinth (Eichhornia crassipes) from South America, which presently occurs throughout the tropics. Its rate of biomass production under favorable conditions is phenomenal. It was recorded for the first time in Lake Victoria, the largest lake in Africa, in 1988. After only six years, it covered 80% of the shoreline as a mat that was in places 15 to 50 meters wide and 4 meters thick. Measurements have shown that water hyacinth can grow several meters in length in just a single day. The masses of decomposing plants consume the oxygen in the water and thereby kill fish and most other organisms. Water bodies infested with water hyacinth are prime habitat for mosquitos and may exacerbate problems with malaria and other diseases. Mark Lonsdale (1999) has compiled data for 184 sites around the world on the numbers of native and alien plant species, including islands, protected areas, and various kinds of mainland areas. Overall, across all the sites, the average percentage of alien species was 16%; hence you could expect that every sixth plant species that you encounter in the wild is an alien species at

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the site. However, there is much variation. The percentage of alien species is highest on oceanic islands, 43%, and lowest in wet tropics and deserts, both 6%. The Azores is an outlier among the oceanic islands with its extremely high fraction of exotic species, 75%. Africa and Asia have lower percentages of alien species, both 7%, while North America has a high value, 19%. Europe in general is intermediate, but Britain is an exception with 31%, perhaps reflecting its long history as a colonial power and the strong tradition of gardening. Among different biomes, temperate agricultural and urban areas have a high percentage of alien species, 31%. Here are some examples from European cities (Niemelä et al. 2011): Dublin 50% (total number of species 315), London 57% (1,171), Frankfurt 46% (845), and Warsaw 31% (1,109). The reasons that urban areas have such large numbers of alien species are probably different from the reasons for oceanic islands. Generally, the numbers of alien species in a given area increase with propagule pressure and the rate of survival following introduction. Propagule pressure has two components, the number of individuals introduced into a new area during one event (called propagule size) and the number of such introduction or release events (called propagule number). Wherever there are many people, sites for travel and trade, the propagule pressure is high and is probably the primary factor increasing the number of alien species. Successful immigration is a necessary condition for an alien species to invade a new area; the other conditions are survival following arrival and establishment of a viable population. The latter may be affected by the traits of the species, for instance, the rate of reproduction, as well as how vulnerable the community in the new area is. But propagule pressure itself has a big influence on the success of establishing a new population: how many individuals arrived, did they arrive all at once or over an extended period, from how many source populations did they originate, and so forth (Simberloff 2009). Increasing propagule pressure ameliorates the effects of random variation in environmental conditions (environmental stochasticity) and random variation among individuals in reproduction and survival (demographic stochasticity), which make colonization more difficult. Additionally, increasing propagule pressure reduces genetic drift and inbreeding depression, which are discussed below, and thereby increases the viability of the new population. If the propagule consists of individuals from several source populations, the amount of genetic variation for a given propagule size increases, and this has beneficial effects for the viability of the new population. These benefits are illustrated by an experimental study in which mated females of the water

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strider Aquarius najas were introduced into ninety streams, but with variation in both the propagule size, from two to sixteen mated females, and the number of source populations, either one or two (Ahlroth et al. 2003). The results showed that the probability of successful colonization increased with increasing propagule size, and it was significantly higher when the number of source populations was two rather than one. One Hundred of the Worst Invasive Species in the World The Invasive Species Specialist Group of the IUCN maintains a list of 100 of the worst invasive species in the world— worst in the sense of how much harm the species cause to other species and to humans, in one way or another. There are of course no objective criteria that could be applied to rank the “badness” of species, but the list is informative in illustrating the range of issues related to invasive species as well as the diversity of species involved. Only one species per genus has been selected for this list, though often there are several congeneric species that are equally harmful. Several invasive trees and shrubs in the Azores, such as the Australian blackwood, ginger lily, angel lips, and prickly pear, have made it to the list of 100 of the worst invasive species. The water hyacinth is there, as is the giant salvinia (Salvinia molesta), a floating aquatic fern, which can completely cover small lakes and water bodies. The giant salvinia was recently added to the list after the successful global eradication of rinderpest (cattle plague), a viral disease of cattle and some wild ungulate species, and an earlier member of the 100 (Luque et al. 2014). One-third of the species on the list are trees, shrubs, herbs, and other plants, but there are also many mammals (14 species), insects (14), fish (8), and mollusks (6). The native ranges of the worst invasive species are varied, including both temperate and tropical regions. About half the species originate from Asia and South and Central America, while Africa has contributed only a handful of species. It would be interesting to know whether there is a real difference in this respect between tropical Asia, South America, and Africa, but to find out would require a study of its own. More than half the species can be described as occurring very widely at present, on many continents, which is one of the reasons that these species have been included in the list. Around fifteen species are widely distributed on oceanic islands in particular, which reflects the high percentage of invasive species in island communities. Below, I elaborate on a few species and lessons that can be drawn from their biology.

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Fig. 4.2 Prickly pears covered 25 million hectares of land in Australia in 1925. (Photo from the archives of the Prickly Pear Destruction Commission.)

The common prickly pear cactus (Opuntia stricta) and a few related species were imported to Australia in the eighteenth century to be used as natural fences in agricultural areas and as a resource for the dye industry (the red carminic acid dye, which is not obtained from O. stricta itself but from a scale insect that infects the cactus; “Prickly Pear Story” 2011). The prickly pears were not satisfied to be just fences, however; they spread across the fields and beyond, and covered 25 million hectares by 1925. A very large portion of this area, up to 10 million hectares, was so thickly covered that the land could be used for nothing else; one could not even walk through the O. stricta thickets (figure 4.2). A committee was established in 1920 to find a solution. As is customary in these cases, the committee screened the natural enemies of the prickly pear within its native range, in Central and South America. Altogether fifty insect species were transported to Australia for intensive studies. Among these species was a small moth, Cactoblastis cactorum, which was mass-reared, and millions of eggs were moved from the laboratory to the field. Finally, this small moth did what everything else had failed to do: in only five years, the moth population increased to such huge numbers that the larvae caused nearly complete destruction of O. stricta. And not only that: when O. stricta density had declined to a small fraction of its previous level, the moth did not go extinct. It survived by eating some

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other plants, and now both O. stricta and C. cactorum are uncommon curiosities in Australia. This is the ideal outcome of any “biological control” program. The interaction between C. cactorum and O. stricta is not robust, however, in the sense that the outcome would be the same everywhere. In North America, C. cactorum attacks not only prickly pears but also the many related native species, such as the endangered Opuntia corallicola, and C. cac­ torum is a potential threat to the large ornamental cactus industry. Therefore, the moth itself has been classified as a serious invasive species, and attempts have been made to control it by its own natural enemies, which presumably regulate the moth populations in South America. We should not be overly surprised by such complications, because population dynamics among many interacting species are indeed very complex and may be sensitive to particular factors that are difficult to identify (chapter 6). The prickly pear exemplifies the complex issues related to many invasive species, because apart from smothering the native vegetation and in the worst case preventing any other land use, the species can also be a valuable resource in some areas and for some communities. Southwestern Madagascar is a case in point (Larsson 2004). Several species of Opuntia were introduced to Madagascar in the late eighteenth century, and they are by now so much a part of the local economy and culture that there are more than thirty local names for the species and their varieties. As in Australia, Opun­ tia species have been used as an effective living fence around gardens and agricultural fields, it is an important fodder for livestock, and people eat the fruits. The economic importance was demonstrated by successful biological control of O. stricta by Dactylopius scale insects in southern Madagascar in the 1920s (the same insect that produces the carminic acid dye). Just as with Cactoblastis cactorum in Australia, it took only a few years for the scale insect to practically eliminate O. stricta—as well as the pastoralists dependent on the cactus, with tens of thousands of cows dying and even more people dying or migrating away from the worst districts (Larsson 2004). In subsequent years, resistant Opuntia species were introduced, and the previous situation was restored, including the economic benefits but also the problems. Opuntia stricta in particular is a severe weed and tends to overtake agricultural fields, from which it is practically impossible to eradicate using feasible chemical and physical control methods. Opuntia stricta invades villages and roads and makes travel and people’s movements difficult. The cacti also invade and ultimately kill the semi-open spiny forests. This is a tragedy for biodiversity and its conservation, because the spiny forest in Madagascar is a unique eco-

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Fig. 4.3 Spiny forest in Ifaty, southwestern Madagascar. (Photo courtesy of Ricardo Rocha.)

region with large numbers of endemic species, not to mention its spectacular appearance (figure 4.3). Characteristic plants include the endemic family Didiereaceae, woody plants that show extreme adaptations to drought and look like cacti though they are not closely related to them. Nearly 5 million hectares of southwestern Madagascar was once covered by the spiny forests, but only a few percent of this area has been protected. The total area of the spiny forest is dwindling rapidly because of excessive cutting of trees for firewood and charcoal production and because of the impact of Opuntia. The domestic cat (Felis catus) is one of the mammals on the list of the worst invaders in the world. The domestic cat has two features that make it especially harmful. As a pet, cats go wherever people go, including some of the most vulnerable communities on earth. And because many people allow their well-fed pet cats to roam out of doors, because “this is their nature,” people have created a very special kind of predator. The dynamics of wild predators that specialize on particular prey species are coupled with the dynamics of their prey populations, and predator populations decline when their prey becomes scarce. Cat populations are different, however, because people feed them, so the cat numbers become decoupled from the numbers of their wild prey. Hence cats inflict an especially high rate of predation on uncommon prey. It has been estimated that domestic cats kill 1.4 to 3.7 bil-

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lion birds and 6.9 to 20.7 billion mammals annually in the United States (Loss et al. 2013). Though much of this mortality is caused by feral cats, they all descend from pet cats, which should not be allowed to run free in the first place. The most famous cat in conservation biology is Tibbles, owned by a lighthouse keeper on Stephens Island in New Zealand (Galbreath and Brown 2004). Tibbles killed some of the last individuals of the Stephens Island wren, a small flightless passerine bird that occurred more widely in New Zealand in prehistoric times but was finally confined to the island, 1.5 square kilometers in size. The Stephens Island population was brought to extinction in 1895 by Tibbles and a few feral cats. The species’ extinction from mainland New Zealand was probably caused by the Polynesian rat, introduced to New Zealand by Maori. In Australia, feral cats and the introduced red fox (Vulpes vulpes) have caused massive damage to populations of small and medium-sized native mammals. The introduction of the red fox from Europe in the 1840s is a case where trouble should have been anticipated, but mind-sets were different in those days. The red fox was taken to Australia for traditional English fox hunting, presumably to bring civilization to the new territory. I do not know how much traditional fox hunting is going on in Australia today; the main methods of killing foxes are less glamorous, poisoned baits and shooting along roads at night. There are currently 6 million foxes across the continent. The problem is that the red fox is the top predator in Australia, with a great impact on ground-dwelling mammals. Red fox predation has been a big factor contributing to the extinction of thirty mammalian species in Australia (chapter 3). Many other species have disappeared from large areas, and some species survive as tiny remnant populations on fox-free islands. Some researchers have suggested that reintroducing the dingo into areas where it has been eliminated would help control the red fox and feral cat populations and thereby reduce the pressure on prey species, but the evidence for the role of the dingo remains mixed and controversial (Claridge 2013). In principle, this solution can be well justified ecologically: large-bodied predators generally suppress the populations of medium-sized predators, which benefits the prey populations of the latter. For instance, though the density of wolves in temperate and boreal regions in North America and Europe is low, their effects cascade down the food chains and are amplified into major effects at the base of the food web (chapter 3). The introduction of the cane toad (Rhinella marina) to Australia in 1935 is an example of intentional translocations whose pros and cons were

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presumably deliberated, yet the outcome turned out to be a surprise and a disaster (Shine 2010). The cane toad is a very large toad native to Central and South America. It is omnivorous, it can live more than ten years, and its populations have a very high growth rate when conditions are favorable. Like other toads, the cane toad has glands that excrete fluid (bufotoxin) that functions as a chemical defense against predators. Within its native range in America, the cane toad has effective predators, which have evolved ways of dealing with the poison, but such predators do not occur in Australia, giving the cane toad a definite advantage in Australian communities. The cane toad was introduced to Australia to prey upon and control the larvae of the cane beetle that infested sugarcane plantations, but like Opuntia, the toads did not fit the role assigned to them. They moved beyond the plantations and started to feed on small mammals, birds, reptiles, amphibians, invertebrates, and even household refuse. The cane toad also expanded its geographical range, which now covers a third of Australia. The range boundary advanced initially by some 10 kilometers per year, but the speed has accelerated to approximately 50 kilometers per year. Australian ecologist Richard Shine and his colleagues have demonstrated that the increased speed of range expansion is due to rapid evolutionary changes in the cane toad populations (Phillips et al. 2006). The researchers have found that the legs of the toad are 10% longer in regions to which the toad had spread only recently, compared with regions that the toads have inhabited for a long time. These results suggest that toads with long legs move faster than toads with shorter legs; hence the proportion of fast-moving toads with long legs increases by natural selection in the range margin. Other examples of fast evolutionary change of dispersal rate were presented in chapter 2. These examples demonstrate that significant evolutionary changes can occur in just a few generations when natural selection is strong. When the problems caused by the cane toad became apparent, it was too late— it was no longer possible to catch and kill all of them. This is a familiar story that has been repeated many times. The Frenchman Étienne Leopold Trouvelot was a portrait painter interested in moths whose caterpillars spin silk, though not quite as fine silk as the silk moth. Returning to the United States from a trip to France in the 1860s, he brought with him some egg clutches of the gypsy moth (Lymantria dispar). The gypsy moth is native to Europe and Asia, but it did not occur in North America. Trouvelot reared caterpillars outdoors, in trees in his backyard. After a while, some caterpillars escaped. Trouvelot understood that the escapees might become a

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problem, and so he informed the entomologists in the Boston region. Apparently nothing was done for a decade, until the gypsy moth started to move beyond Trouvelot’s street and to defoliate trees. Egg clutches were collected by hand; woodlots with the gypsy moth were burned down and sprayed with whatever insecticide existed at the time. But it was too late; the gypsy moth continued its expansion— and so it has done ever since, for more than 100 years. The gypsy moth is now considered one of the worst forest insect pests in North America. Dozens of its natural enemies have been imported from Europe and Asia, but without much success so far. Small mammals appear to control gypsy moth populations at low density, but every now and then the moth population escapes this control, grows enormously, and continues to expand. Why the gypsy moth is not a similar pest in Europe and Asia is a good question, with no clear-cut answer yet. The challenge is the very large network of species with which the gypsy moth interacts. Ecologists have developed solid theory for interactions between two species, and some results are available for three species, but when there are dozens of species in the food web, it becomes practically impossible to develop predictive knowledge about the dynamics. The list of 100 of the worst invasive species includes five species of ants. In terms of the numbers of individuals and impact on ecosystems, the role of ants is much greater than one might expect from their share of all species, approximately 0.2% (12,000 divided by 5 million). Nobody knows the exact figure, but it is estimated that ants compose 15% to 25% of the terrestrial animal biomass. The success of ants has been attributed to their capacity to modify habitats, to exploit many kinds of resources, and to defend themselves effectively, based on their numbers and the social organization of ant colonies (E. O. Wilson and Hölldobler 1990). In this respect, ants are better compared with our own species than with butterflies or most other insects. Two of the invasive ant species are the yellow crazy ant (Anoplolepis gracilipes), originally a West African species, and the Argentine ant (Linepi­ thema humile), native to Argentine, Uruguay, Paraguay, and southern Brazil. Both species have been unintentionally spread by humans to new areas, including oceanic islands and different continents. Following initial translocations, some ant species are good at expanding their ranges on their own, if the general environmental requirements are met. In their native ranges, different species of ants compete with each other, as do different colonies of the same species, and this competition constrains their population dynamics. Such brakes on population growth seem to be lacking in the case of

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the invading species. Amazingly, researchers have found that the Argentine ant comprises only a few megacolonies within its current worldwide distribution in America, Europe, and Asia (Sunamura et al. 2009). Ants belonging to the same megacolony show little or no genetic differentiation, and they do not behave aggressively toward each other, which goes a long way toward explaining their success. Argentine ants often eliminate most if not all of the native ant species, which has significant consequences for ecosystems. Argentine ants invade buildings and can become unsettling household pests. The yellow crazy ant similarly forms megacolonies with little aggression toward colony members and severe aggression against other ant species. The yellow crazy ant has a mutualistic relationship with scale insects, which are serious plant pests, and this mutualism exacerbates, from the human perspective, the ecosystem-wide damage that the ants cause. Assisted Migration People have translocated plants and animals since the Neolithic (agricultural) revolution 10,000 years ago, when they started to cultivate the first cereal grasses, emmer (Triticum turgidum, several subspecies), einkorn (T. bae­ oticum), and barley (Hordeum vulgare). In the past 500 years, a few plant species, such as maize (Zea mays; from Central America), wheat (Triticum species; Near East), rice (Oryza sativa; China), potatoes (Solanum tubero­ sum; the Andes), and cassava (Manihot esculenta; South America), have been spread around the world and have become the pillars of civilization. At the same time, large numbers of other plant and animal species have been deliberately moved to new areas or accidentally translocated in the course of trade and travel. Many of the species that we now consider harmful invaders, including those on the list of 100 of the worst invading species, are species that people moved to new areas for a particular purpose, but which unexpectedly interacted with native species and grew quickly in the new territory. With species translocations, unexpected outcomes are commonplace, which should make people think twice before they take action. Unfortunately, here as in many other spheres of human enterprise, caution has often been overridden by other considerations. Not all translocations are the result of reckless exploits. Many translocations have been well justified, at least in theory, and they have been carefully contemplated and cautiously implemented. This applies to many species that

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have been moved for biological control of pest species, and to species moved to improve ecosystem functioning. One example of the latter is the translocation of dung beetles to Australia in the 1960s and onward (chapter 1). The problem was the accumulation of large quantities of cattle dung on pastures, and the huge numbers of dung-breeding bush flies and buffalo flies that developed in dung pats and pestered both humans and domestic animals. The problem arose when the settlers introduced cattle, which do not have any equivalent (native ungulates) in the Australian mammal fauna. Cattle-dung pats quickly disintegrate and decompose in ecosystems where decomposers, including dung beetles, have evolved with large ungulates. The mostly smallbodied native dung beetles in Australia have evolved with marsupials that produce very different dung, and they cannot do much to cattle-dung pats. After careful consideration and research, nearly fifty species of dung beetles were successfully introduced in 1960–80 to Australia from South Africa and other areas with Mediterranean-type climate; more than half of the species have become well established. By moving much of the dung below ground quickly, the beetles hasten decomposition and thereby reduce the chances that pestilent flies will breed in dung pats. Because they are so specialized in their ecology, introduced dung beetles posed less risk than many other translocated species, although something could still have gone wrong; for instance, beetles could have carried microbes or parasites that interacted unexpectedly with native species. Another Australian success story is the introduction of the moth Cactoblastis cactorum to control the massive prickly pear outbreak in the early twentieth century. In that case, success was not as predictable as in the case of dung beetles. For instance, C. cactorum could have started using other plant species, as they have done in North America, to become a pest itself, as the cane toad did in Australia. Declining biodiversity has become another reason for contemplating species translocations, often called assisted migration. Assisted migration might be beneficial in two situations. Often there is suitable unoccupied habitat for the species within a large area, but located so far from existing populations that the species is unlikely to reach it through natural migration; hence assisted migration might be considered. The other scenario where assisted migration can be helpful in conservation is for preserving genetic variation. Small and isolated populations of threatened species lose genetic variation and become increasingly inbred over time, which leads to reduced individual fitness, called inbreeding depression. This can be severe enough

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to increase the risk of population extinction. To reduce the level of inbreeding, one could translocate unrelated individuals from other populations to the small population in question. The theory of population genetics allows quantitative predictions about the loss of genetic variation from isolated populations. Two important reasons that genetic diversity is lost is the inevitable genetic drift, which is especially potent in small populations, and inbreeding. To understand the mechanism of inbreeding depression, let us consider the basics of genetic inheritance of traits that influence fitness. Recall that genes are located on chromosomes, which are long chains of the DNA molecule and occur as pairs in many species, including humans— one chromosome inherited from the mother and the other from the father. For the genotype of an individual with respect to a particular gene that is polymorphic (variable) in the population, there are three possible variants, AA, AB, and BB, where A and B are two different forms of the gene. The two chromosomes in a pair may have the same variant, A or B, in which case the genotype is AA or BB, and the individual is homozygous with respect to this gene. Or the two chromosomes may have different variants, in which case the genotype is AB and the individual is heterozygous. One common cause of inbreeding depression is genetic variants that are deleterious, but the deleterious effect is expressed only in the homozygous form, while the heterozygotes are as fit as the homozygotes for the healthy genetic form. In this case, the deleterious form is said to be recessive. Consider now that B is such a recessive deleterious variant. Individuals with the genotype AB are healthy, but BB individuals have reduced fitness. Many genetically determined rare human disorders behave in this manner. In a large population, B remains uncommon, because selection disfavors BB individuals and hence reduces the frequency of B. When genetic diversity is lost in small populations, however, A may be lost by chance, so only BB individuals remain. The effect of BB on individual fitness may be small, but the genome may have hundreds of such genes, and their combined effect can be large enough to reduce individual fitness substantially. Now, the idea of assisted migration is to introduce into the population individuals that mostly do not have the deleterious variant and have the AA genotype. When these individuals breed with the residents, they produce AB offspring which have higher fitness than BBs. Hence the healthy variant A increases in the population and may rescue the population from inbreeding depression and looming extinction.

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Inbreeding is inevitable in a small population, where all individuals become related to each other in the course of time. The wolf population on Isle Royale in Lake Superior in the United States has been studied for more than half a century. On Isle Royale, wolves prey on moose, and a long-term study has highlighted the cascading effects of wolf predation down to the plants that moose eat, and ultimately to the functioning of the entire forest ecosystem (Post et al. 1999). On Isle Royale, the wolf population has fluctuated between a few individuals and 50, the moose population between 500 and 2,500 individuals. It has been evident for some time that the small wolf population suffers from inbreeding. It has probably survived for so long because during the coldest winters the lake freezes over, and a few wolves have occasionally arrived from the mainland and have added much-needed genetic variation to the population. In the spring of 2015, the fate of the population appeared to be dismal, with only three individuals left, a pair and a pup that suffers from spinal defects, most likely the result of close inbreeding. Over the years, the argument has been advanced that a genetic rescue should be attempted by introducing a few unrelated individuals to the Isle Royale population, but the National Park Service has chosen not to interfere. A comparable, well-studied, isolated wolf population occurs in southern Sweden (Räikkönen et al. 2013), established in the early 1980s by a pair of immigrants from Finland. The population remained small, and there was only one pack until 1991, when new genetic variation suddenly appeared and the population started to increase rapidly. Molecular analyses implied that a single new male had arrived, bred successfully, and essentially rescued the population (Vilà et al. 2003). In spite of continued poaching, the population increased to more than 200 individuals by 2010. A population of 200 individuals would be large enough to maintain genetic variation for a long time if it had sufficient variation in the first place. In this case, however, because of its history of rapid increase from a very small size, the population has limited genetic variation and a high level of inbreeding. Among 171 wolf individuals studied over the years, the incidence of morphological anomalies attributable to inbreeding has increased from 13% in the beginning of the study to 40% presently. Even if the population is not very small right now, its fate is as bleak in the long term as that of the Isle Royale population, unless new genetic variation is introduced via natural or assisted migration. An example in which assisted migration has rescued a threatened population is the Florida panther (Puma concolor coryi). In the early 1990s, only

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twenty to twenty-five adult individuals remained, all within a restricted area in southern Florida ( Johnson et al. 2010). The population had low genetic variation and high prevalence of various defects, almost certainly due to severe inbreeding. In 1995, eight female pumas from Texas were translocated to the Florida population, with good effects: panther numbers increased threefold, genetic heterozygosity doubled, survival and fitness measures improved, and correlates of inbreeding declined significantly ( Johnson et al. 2010). What remains are the other threats, including continued habitat loss. Small isolated populations of large predators are feasible targets for assisted migration, but unfortunately genetic deterioration is only one of the problems they face. Another well-documented example of genetic rescue due to assisted migration is a completely isolated adder (Vipera berus) population in southern Sweden (Madsen et al. 2004). The long-term study started to show a systematic decline in population size in the late 1980s, at which point the researchers decided to do an experiment. They introduced twenty unrelated adult males to the population in 1992. Male adders mature at the age of four years, so the introduction was expected to increase the numbers of adult males in 1996. Indeed, that happened, and the population then continued to increase (figure 4.4). As a scientific experiment, this study would have been more convincing if there had been several study populations, some of which received translocated individuals, and some of which did not. Unfortunately, although researchers would love to do such experiments in the wild, there are seldom enough isolated and comparable populations to do so. Assisted migration can be used to help species spread in fragmented landscapes, where natural migration is unlikely because of long distances between habitat fragments. With a warming climate, favorable habitat appears beyond the boundary of species’ current distribution. Many species manage to expand their ranges naturally toward the north and toward higher elevations on mountains, as described in chapter 3, but in many other instances, natural range expansion is unlikely because of long distances between the current populations and new unoccupied habitat. In the case of large-bodied mammals in human-dominated landscapes, there are various reasons, apart from climate change, that natural migration is slow or does not occur at all, and where assisted migration could be helpful. As an example, the wild forest reindeer (Rangifer tarandus fennicus) was hunted to extinction in Finland at the end of the nineteenth century (Kojola 1993). It returned from Russia in the 1940s, but the subsequent range expansion was limited,

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Fig. 4.4 Number of male adders (Vipera berus) recorded at a study site in Sweden. The isolated population showed a steady decline in the late 1980s, which was considered to be due to inbreeding. An experiment in 1992 introduced twenty unrelated males from other populations (these males are not included in the numbers shown in the figure). After the introduced males matured, four years later, the population started to increase, and the increase continued for many years, apparently due to a reduced level of inbreeding and hence increased fitness of adders in this population. (After Madsen et al. 2004.)

partly because the highly managed forests are not of high quality for the reindeer. A new population was established in western Finland by releasing the offspring of translocated reindeers that were kept in a large enclosure in the new area. The population started to increase rapidly after fifteen years and now has more than 1,000 individuals over an area of 25,000 square kilometers (figure 4.5). Two carnivores have been translocated in Finland with good effects. The wolverine (Gulo gulo) has a precarious existence in Lapland, where it preys on domesticated reindeer. Some twenty individuals have been translocated over the years to central Finland, where they have established an apparently healthy breeding population. The brown bear (Ursus arctos) was hunted to near-extinction by the early twentieth century, but it has been recovering since the 1970s. Genetic diversity has been low at the front of the expanding distribution, a result of a small number of founder events (Hagen et al. 2015). In this situation, translocating a few adult female bears, which are generally sedentary, has speeded up the recovery of genetic variation, though translocations were not needed for boosting the numbers of individuals. Finally, translocation of the gray wolf (Canis lupus) to increase its distribution in Finland has been contemplated, but not done, because of active opposition by some members of the public. The message is

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Fig. 4.5 A translocated population of the forest reindeer (Rangifer tarandus fennicus) has allowed the species to greatly expand its range in Finland. (Photo courtesy of Ilpo Kojola.)

that assisted migration is an effective technique to help large-bodied mammals expand their ranges in human-altered landscapes, but assisted migration needs to be applied in concert with other conservation measures. Assisted migration has its own problems. For one, it can be applied only to a relatively small number of species. In exceptional situations, however, many species could be translocated at the same time. For instance, large numbers of species living in dead wood are threatened by intensive forestry. In Finland, the amount of coarse woody debris in managed forests is only 5% to 10%, or even less, of the amount in natural forests, and hundreds of invertebrate and fungal species, as well as other animals and plants, have become nationally threatened (Rassi et al. 2001). In landscapes where forests with old-growth characteristics are being restored, the number of species associated with dead wood is presently very low because of forest history (Penttilä et al. 2006). It would be straightforward to load trucks with large decomposing tree trunks with many of their fungal and insect inhabitants from a region that has good populations and move them to regions where habitat is being restored. A conceptually similar case of assisted migration has been effective at a very different spatial scale and very close to all of us— in our gut. Experiments and clinical practice show that fecal transplantation

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is effective for the treatment of severe infections caused by the bacterium Clostridium difficile. The idea is to assist the migration of a healthy community of commensal bacteria into a gut dominated by this very unhealthy bacterium— and it works. A second worry about assisted migration is that removing individuals can affect the viability of the source populations. Clearly, one should consider removing individuals only from populations whose viability is not thereby threatened. Third, it is often not feasible to transfer individuals directly from one population to another. By rearing individuals in captivity, one can increase the number available to be released, which ameliorates the problem of harming the source populations. It introduces the possibility of fast microevolutionary changes in the individuals reared in captivity, however, and these changes may make them less fit in the wild. There is much evidence for such microevolution from fish hatcheries that supply juveniles to supplement exploited fish stocks. Fourth, there is little point in translocating individuals to areas where there is so little habitat, or the habitat is of such low quality, that the new populations are unlikely to persist in the long run. Hundreds of such translocations have nevertheless been carried out, for example with butterflies (Oates and Warren 1990). Fifth, translocations between different kinds of environments could limit success: translocating individuals to an environment in which they are not well adapted may lead to poor results. Finally, the translocated population could become invasive, a real possibility when translocation occurs beyond the established range of the species (Ricciardi and Simberloff 2009). Globalization of Nature Ecologists often distinguish between two main components of biodiversity, alpha diversity and beta diversity, or α and β diversity. These terms were coined by American plant ecologist Robert Whittaker in 1960, while he was studying the vegetation in the Siskiyou Mountains along the border of California and Oregon. The concepts can be applied to all kinds of communities, and they are so fundamentally useful that it is hard to imagine ecology without them. Alpha (α) diversity denotes local diversity, biodiversity in a local community. The simplest measure of diversity is just the number of different species, but there are many other measures as well. For instance, it often makes sense to take into account the relative abundances of the species, not just

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their presence or absence in the community; in this case, a community with more or less equally abundant species is more diverse than a community with the same number of species of which one or a few are very common while the others are rare. One may also consider the diversity of ecological traits possessed by species in the community. A community consisting of trees, shrubs, and grasses would then be more diverse than a community that has only grasses. One may even consider the evolutionary relationships among the species: diversity is high when the species are only distantly related to each other, while diversity is low when species are more closely related to each other. Thus a community of birds, mammals, and insects would be more diverse than a community of insects only, other things being equal. Whichever definition of diversity we want to use, the concept of α diversity is an essential building block for all theories about biodiversity. Now consider a large region, so large that it includes many local communities; local communities together make up what is often called the metacommunity (chapter 5). How diverse is the metacommunity? One could ignore the spatial structure; consider all the individuals and species in the metacommunity as a single, very large community; and characterize biodiversity using α diversity. Doing so would waste much information, however, about the local communities and how they differ from each other. This is where β diversity comes into the picture: β diversity describes how similar two or more local communities are in terms of their species. If all the local communities have the same species with the same relative abundances, β diversity is zero; if the species in the local communities are all different, each local community having unique species, β diversity attains its maximal value. Hundreds of papers argue the merits of different ways of defining and measuring β diversity, but for us it is sufficient to focus on the essence of the concept as I have just explained it. Finally, there is a third component, gamma diversity (γ diversity), by which ecologists mean diversity in the region (metacommunity) as a whole. The three diversities are related to each other, but we are free to assume how they relate. Assuming a multiplicative definition, we have γ = αβ. Assuming an additive definition, we have γ = α + β. Different studies may report different trends of changing biodiversity because they consider different components of it. This can be confusing. Consider the hypothetical political leader Amanda Smith, who is preparing her agenda on the environment and struggling to place the loss of biodiversity in its proper place among the many environmental issues. She finds out about the global and national red lists, which have species placed at different levels

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of threat using a set of well-defined criteria (chapter 3). She finds reports that convincingly demonstrate a rapid decline in biodiversity; for instance, the populations of the best-studied mammals and other vertebrates in the world have been halved in forty years (figure 3.6). Amanda Smith also learns about success stories in conservation, some species of birds and mammals that have been brought back from the brink of extinction by intensive conservation efforts, and she finds reports showing that in many well-studied localities biodiversity has remained steady or has even increased. She reads a report from Finland, where approximately 10% of all species are threatened according to the national red book, primarily because of industrial forestry and agricultural intensification, yet long-term studies have shown that species richness of butterflies and moths, of which there are 2,600 species in Finland, has increased by 15% to 20% at well-studied localities in only twenty years, and in the country as a whole, species number has increased by almost 10%. Amanda Smith finds it difficult to understand why and how biodiversity can decline rapidly at the global scale, while it has increased quite dramatically in well-studied localities. Are the global estimates based on wrong assumptions? Are the conclusions biased by researchers having selected certain types of species and communities to fit their preconceptions? These are valid questions. The solution to the apparent paradox lies in the different components of biodiversity, α, β, and γ diversity, which may respond differently to the drivers of biodiversity change. Loss and fragmentation of natural habitats typically reduce diversity at all spatial scales at which habitat conversion takes place, hence both local (α) and global (γ) diversity will decline. Land-use change will benefit some species, especially those that do well under disturbed conditions, but as natural and semi-natural habitats have more diverse communities than human-altered habitats, total diversity (γ) is likely to decline. Naturally, α diversity declines at the sites where habitat is being converted. Increasing numbers of invasive species due to unintentional translocations and climate change will generally increase α diversity but decrease β diversity. Here is the main reason for the seemingly conflicting reports that confused Amanda Smith. The global diversity and often the national diversity decline when rare species with narrow geographical distributions go extinct, while the local diversity may well increase due to expanding distributions of many species, which at the same time reduce β diversity. The result is increasing homogeneity of species composition across large areas, globalization of nature. Often the species that are expanding

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their ranges are recognized invasive species, but this is not always so. In the Atlantic forest region in Brazil, forest fragmentation has favored a subset of tree species, short-lived pioneer species that are ecological generalists. These species have expanded their distribution, and the species composition among nearby forest regions is presently 20% to 40% more similar than it was earlier in the twentieth century (Lobo et al. 2011). In this case, the species that have expanded are native species that have benefited from the early successional conditions created by forest fragmentation. The dynamics of invasive species and their interactions with native species are similar to those of the taxon cycle on islands, discussed above. Most successful invasive species flourish in environments that have been altered by humans; these species are typically ecological generalists (“weeds”), not dependent on particular resources or habitat types. Because the species occur in association with humans, they are the ones most likely to be accidentally translocated to new areas. In contrast, specialist species have adapted, during their evolution, to particular and often uncommon habitats, and they decline when the area of their habitat diminishes. Most invading species have weak interactions with native species, but every now and then an invasive species happens to have characteristics that give it an extra edge in the new environment. Its populations may grow to enormous size in the absence of the competitors, natural enemies, and diseases that keep it under control in the old geographical distribution. In this case, the newcomer may have strong adverse effects on one or more of the native species. The invasive plant species in the Azores is a community-wide example, while the expansion of the American gray squirrel (Sciurus carolinensis) in the United Kingdom and elsewhere in Europe illustrates the biological and even political processes influencing invasions. The gray squirrel was introduced to the United Kingdom in the 1870s, and it has by now largely replaced the native red squirrel (Sciurus vulgaris), partly because the gray squirrel is a stronger competitor, but also because it carries a virus, the squirrel box, that is lethal to the red squirrel. A few gray squirrels were introduced in northern Italy in 1948, 1966, and 1994 (Bertolino and Genovesi 2003). When the populations started to expand and the consequences for the red squirrel were observed, an eradication program was tested and found to be feasible. Unfortunately, this program had to be suspended for several years by a court order, asked for by an animal rights group concerned about the well-being of individual gray squirrels. The lengthy judicial process came to an end in 2000, but by then it was too

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late: the gray squirrel had increased its range to such an extent that eradication was no longer practical. Researchers predict that the gray squirrel will continue to expand through much of central Europe, will replace the native red squirrel, and will harm the forest ecosystem and forestry by its habit of debarking trees, especially sycamore (Acer pseudoplatanus) and beech (Fagus sylvatica), two important tree species in central Europe (Bertolino and Genovesi 2003). The court case on the eradication program is a perfect example of how well-meaning but naive concern about the welfare of individuals can lead to disastrous consequences for populations and ecosystems. The same opposition has emerged in the case of the American mink (Neovison vison), which was introduced to Europe in the 1920s for fur farming. Mink have escaped from the farms, partly with the help of animal rights activists, and established large populations in many European countries. While the American mink has increased in abundance, its European counterpart, the European mink (Musteola lutreola), has declined and gone extinct in large parts of its former range. Significantly, the European mink is more specialized than the American mink in its habitat selection, which makes it vulnerable to habitat loss in general and handicaps it in competition with the American mink. The American mink has turned out to be an effective predator of ground- nesting waterbirds, whose populations have plummeted where the American mink is abundant. Humans have translocated, accidentally and on purpose, thousands of species around the world. With all the transport and travel going on now and likely to continue, it is hard to stop the movement of species, especially those species predisposed to take advantage of changes in land use and climate change. There is another class of populations and species that I cannot avoid thinking about in this context, though other biologists might not agree. I am thinking of the genetically modified (GM) organisms and entirely novel species created by synthetic biology (figure 4.6). The reason many biologists do not share my concern is that biotechnology can potentially help solve some of the world’s “wicked problems,” such as problems created by the massive use of pesticides and herbicides, waste treatment, and food security. Some also consider that the environmental and health risks of GM plants are exaggerated. I do not deny the opportunities, and I agree that the current GM varieties do not pose significant risks, but I question this path that society is choosing over many other paths. I am not a molecular biologist, so I do not have a good understanding of the potential

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Fig. 4.6 Mycoplasma laboratorium is the first human-made (synthetic) bacterium.

of biotechnology and synthetic biology. If I did, I fear that I would be even more worried than I am now. In the future, let us say by 2050 or by the end of this century, scientists will be able to construct microbes, fungi, plants, and animals that have such radically new, designed features that they can be considered new species. Whether they will hybridize with existing species is to a large extent a matter of design, but we should not overestimate the control that can be imposed on these new organisms. When they have been released in the environment, they are exposed to natural selection just like existing species. The new species are products of “intelligent design,” but natural selection and evolution do not sign any contract with us; there is no guarantee what will happen. Is there going to be a battle between the 3.5-billion-year-old “old life” with the 100- year-old “new life”? Humans will create the new life, but when the battle starts, we become spectators. The arbiter may be artificial intelligence, which humans designed and launched and which has quickly penetrated all the human-created and robot-created physical world. In the future, the arbiter may “decide” not to remain impartial, but to join forces with the new life.

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Messages 1. Species that colonize islands are often ecological generalists that flourish in early successional, disturbed habitats. In the course of time, these species adapt to the prevailing environmental conditions and become more specialized, which may ultimately increase their risk of extinction from islands, while new generalists arrive to compensate for extinctions. Such dynamics are called the taxon cycle. 2. The percentage of invasive plant species is as high as 30% to 50% of all species on oceanic islands and in cities and other urban areas in temperate regions. The number of invading species at a particular locality increases with propagule pressure, which has two components, the number of individuals introduced into a new area during one event (propagule size) and the number of such introduction or release events (propagule number). High propagule pressure increases the probability of successful establishment of the invading species. 3. Many alien species have a limited influence on native species, but some aliens are truly destructive and have caused the extinction of numerous resident species. The list of 100 of the world’s worst invading species includes plants, mammals, fishes, insects, and other groups. These 100 species highlight the often subtle reasons why an invading species becomes especially harmful. 4. Conservation biologists have advocated translocating species, called assisted migration, in two kinds of situations. Small, isolated populations suffer from reduced genetic variation and inbreeding depression, which can be ameliorated by introducing even a small number of unrelated individuals from other populations. Many species cannot spread through fragmented landscapes to colonize isolated areas of unoccupied habitat; hence these species are not able to track changing environmental conditions due to climate warming. In such situations, assisted migration can be used to help species expand their distributions and thereby improve long-term viability. 5. Land-use change and climate warming allow many species to expand their distributions, which often increases local species richness (called α diversity) and reduces differences in the species composition between communities (β diversity). The result is increasing homogeneity of the fauna and flora across large areas. Widespread generalist species become even more widely distributed, while many specialist species with narrow geographical distributions decline and go extinct.

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Islands Area Maximum elevation Age Time since isolation Current isolation Inhabitants Breeding birds Endemic birds Butterflies Flowering plants

Åland 1,527 square kilometers 129 meters 10,000 years No mainland connection ever 50 kilometers 29,000 150–160 species None 75 species About 1,000 species

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heoretical physicists talk about the theory of everything, but it is difficult to imagine a theory that could predict everything of importance in biology or most other fields of science, and even less so in the humanities. There is always the opportunity to find out something radically new about the world surrounding us, something that could not have been anticipated from what is already known. That being said, it has to be admitted that most research results are not a huge advance in general knowledge; most studies 147

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add small pieces of empirical information that are not expected to change the world. Someone might ask how valuable it is to find out more details about a particular species in a particular ecosystem, when there are millions of species, and thousands of species have already been scrutinized. The answer is that we do not know for sure— without doing the research. Most research is incremental, but it occasionally leads to a big leap into the unknown. Thomas Kuhn, in his celebrated and controversial Structure of Scien­ tific Revolutions (1962), contrasted “normal science” with revolutionary discoveries, which lead to a paradigm shift in a field of science. Paradigm refers to the basic assumptions that scientists make, to the theoretical framework within which they work. For a population biologist, it is very easy to come up with an example of revolutionary research leading to a paradigm shift: Charles Darwin’s work, which culminated— though did not end— in the publication of On the Or­ igin of Species by Means of Natural Selection; or, The Preservation of Favoured Races in the Struggle of Life (1859). This is a paradigmatic example of a paradigm shift; when Darwin’s work had been fully assimilated by his fellow scientists, nothing in biology made sense anymore except in the light of Darwinian evolution. The paradigm shift that Darwin pushed into motion was so profound that it took several generations of researchers to work out the full implications, and the societal impact of this research has been enormous: it has changed people’s worldview. The scientific transformation was still going on when I started my studies at the University of Helsinki in 1972. Exciting new lines of research, such as behavioral ecology and sociobiology, were built upon the foundations of the evolutionary theory established by Darwin, themselves representing more circumscribed paradigm shifts in particular fields of population biology. These advances were much discussed among students and young researchers in the Department of Zoology. It seemed to us that the faculty in our department lived in the past, but this suited us fine: we were thereby free to absorb the rapidly progressing science directly from scientific papers and books. In hindsight, we were fortunate. What is best for students is to have active and knowledgeable professors; the worst is to have professors strong enough to dominate students’ thinking but weak in guiding them to new topical questions. Big paradigm shifts may require, in practice, that a new generation of researchers take over the field. Advances in evolutionary biology were exciting, but our group of young ecologists was more attracted by new developments in population and community ecology. The book that we discussed most was The Theory of Island

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Biogeography by American biologists Robert MacArthur and Edward O. Wilson, published in 1967. This book, and the “island theory” it described, has had an enormous and lasting influence in ecology, biogeography, and conservation biology all over the world. Other researchers have cited MacArthur and Wilson’s book in more than 15,000 publications, which is a clear indication of its great impact on the work of others. The reasons for the exceptional success of the island theory were the completely new perspective it offered and the simplicity of the key idea. Many must have thought, Of course, this is how it must be—why didn’t I come up with it myself? In the following years and decades, the island theory stimulated many new lines of research beyond the original aims, which is another sign of its exceptional quality. Past research on island biogeography emphasized the importance of particular features of particular islands in governing the biology of species found there. This perspective is relevant when we consider islands in very different parts of the world, for instance, the temperate islands in the Baltic Sea in northern Europe versus the Seychelles and other tropical islands in the Indian Ocean. But MacArthur and Wilson were not interested in specific islands; they were concerned with sets of islands with similar climatic and other environmental conditions but with differences in how far they were from the mainland and how large they were. Why do large islands have more species than small ones, and why does species number typically decline with increasing distance of the island from the mainland? The radical new idea was that the species assembly on each island is not stable, following some process of gradual accumulation in the distant past, but instead results from ongoing change: populations of species on particular islands have a substantial risk of going extinct, while species currently absent from the island may disperse from the mainland and establish new populations. The relationships between species number and island area, and species number and isolation from the mainland emerge from simple but realistic assumptions: extinction risk decreases with increasing island area because smaller islands tend to have smaller populations, and the rate of recolonization declines with increasing isolation because it is easier to disperse a short distance than a long one. The essence of the island model is simple, but it set in motion a dynamic view of the occurrence of species on islands—and not only on islands. MacArthur and Wilson suggested that similar considerations would affect the distribution of species in fragments of habitat on land, surrounded not by water but by some other unwelcom-

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ing habitat type, such as cultivated fields surrounding patches of forest. The island theory was soon applied to protected areas, and it was used as a tool to argue about the relative benefits of one large protected area versus several small ones with the same pooled area (more about this below). In hindsight, the great enthusiasm for the island theory led to simplistic applications, but this was inevitable. How widely new ideas apply has to be tested, and delineating the domain for their proper application requires some initial missteps. In the process, the island theory made an unexpected contribution to the birth of the new field of conservation biology in the 1970s (Hanski and Simberloff 1997). I became obsessed by the idea that the occurrence of species in fragmented landscapes is dynamic, and that local extinctions and recolonizations are commonplace. I started to think about what happens to species when some habitat patches are lost, for instance, in conversions to cultivated fields or housing developments. Is the rate of recolonization always sufficient to compensate for extinctions? Is it not possible that a particular species with poor dispersal capacity might disappear completely from a landscape following habitat loss? In the island model this does not happen, because the mainland is assumed to have permanent populations of each species; hence recolonization will always happen after extinction, sooner or later. Fortunately, I became aware of another simple model during my undergraduate studies, a model published by Richard Levins, an ingenious evolutionary biologist from Harvard University. The Levins model makes much the same assumptions as the island model, but with the key difference that there is no mainland, just a network of habitat patches. In this model, recolonization of currently unoccupied patches happens due to dispersal from the existing populations in the habitat patch network. Extinction from the entire network is not only possible but indeed a certainty if the structure of the network is such that extinctions always exceed recolonizations. Levins coined the term metapopulation to describe the set of local populations inhabiting the network of habitat patches. I became an ardent follower of Levins, whom I sadly never met, and a keen protagonist of metapopulation ecology (figure 5.1). I studied the Levins model and developed other models in the late 1970s and the 1980s by modifying the assumptions of the original model. I also collaborated with the mathematician Mats Gyllenberg to analyze more complex models. This was not enough for me, however; as an ecologist, I started to contemplate a field study that would test model assumptions and predictions. But a field

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Fig. 5.1 I gave a seminar at the University of Uppsala in May 2011. My presentation included a slide showing Robert MacArthur (left) and Richard Levins (right) during a visit with Edward O. Wilson in Dry Tortugas, Florida, in 1968. I was glad to be documented in this manner with the two researchers who had greatly influenced my thinking in the 1970s and 1980s. (Slide courtesy of Edward O. Wilson.)

study on which species, and where? In the spring of 1991, my wife, Eeva, gave me a birthday present, a new award-winning volume on Finnish butterflies (Marttila et al. 1990). I had told her about my aspiration to start a new project, possibly on butterflies, and her inscription on the first page wished me luck on my journey back to butterflies, which I had ignored since 1972 when I entered the University of Helsinki. I had been thinking of other taxa as well, including shrews, whose island populations I had studied, but I suppose my teenage enthusiasm for butterflies and moths started to creep back— and of course it would help that I knew butterflies well; I had spent ten years chasing them. There was also another factor. Paul Ehrlich, one of the foremost population biologists, visited Helsinki in the fall of 1990, and I had an opportunity to talk about his studies of the Edith’s checkerspot butterfly (Euphydryas editha) at Jasper Ridge near Stanford. I knew about his work (Ehrlich 1965, 1979), but it makes a difference to meet the person and to hear a firsthand

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Fig. 5.2 The Glanville fritillary (Melitaea cinxia). (Photo courtesy of Thomas Delahaye.)

account of the research. When I leafed through the volume on Finnish butterflies in the early spring of 1991 to select a species for the new project, discussions with Paul must have been in the back of my mind. I went through the entire fauna of 114 butterfly species (now 121 species, largely due to climate change), and thought about the pros and cons of every species. In the end, the choice was clear, the Glanville fritillary (Melitaea cinxia; figure 5.2), a close relative of the Edith’s checkerspot. I had never seen the Glanville fritillary alive, but I made up my mind based on what I had read about its biology and occurrence in Finland. Little did I know that I and others would study the Glanville fritillary for decades; it continues to be studied today. The Glanville fritillary, like the Edith’s checkerspot and many other temperate butterflies, is a host-plant specialist. The host plants for the Glanville fritillary are ribwort plantain (Plantago lanceolata) and spiked speedwell (Veronica spicata), both of which are uncommon species in Finland except in the Åland Islands in the northern Baltic, between southwest mainland Finland and Sweden. In this part of northern Europe, the bedrock is volcanic, formed more than 1,700 mya. Since its uplift after the last glacial period, the landscape has been a small-scale mosaic of granite outcrops and intervening areas with sedimentary deposits supporting forests and, presently, small cultivated fields. Roughly 1% of the land area is covered by small dry

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meadows, often on rocky outcrops, where the two host plants of the butterfly thrive. The Åland landscape is a perfect example of a highly fragmented landscape, with about 4,000 small meadows within the total area of more than 1,500 square kilometers. Most of the meadows occur on the main Åland Island, not on the innumerable surrounding small islands; hence the setting is not an archipelago of true islands but a huge network of habitat islands. The meadows are typically much smaller than 1 hectare (the median is 0.17 hectare), and none is greater than 10 hectares (Ojanen et al. 2013). In the beginning, I did not know about the 4,000 meadows; I had only a vague idea of many meadows, where the butterfly had previously been collected, though not very commonly. But I was soon to find out much more. In the spring of 1991, I sent two undergraduate students, Mikko Kuussaari and Marko Nieminen, who later became my first postgraduate students, to search for caterpillars that had broken from winter diapause (arrested development) in April. I asked Mikko and Marko to go to one particular area, where two lepidopterists had seen caterpillars in the late 1980s. And indeed, Mikko and Marko found a large population with thousands of caterpillars. That was good news, and we moved on to the next stage in our plans. In June 1991 we conducted a mark-recapture study within a network of fifty meadows, including the meadow where large numbers of caterpillars had been recorded in late April. Marking butterflies is simple: you just write a running number with a felt pen underneath the hind wing. After marking, the butterfly is released to continue its normal business, and if you subsequently recapture it, you gain new information: where it was caught first, how long ago, and how far from its present location. From the results one can calculate the rate of mortality and the rate of movement between habitat patches. We found that there were nearly 10,000 adult butterflies in this network of fifty meadows in June 1991. We recorded frequent movements among populations in different patches, and discovered local extinctions and colonizations by comparing the occurrence of caterpillars in the spring and in the next generation in the autumn. These and other results matched well the assumptions of the models— we had found a real metapopulation. From this first piece of fieldwork in 1991, the Glanville fritillary project has evolved into a large research enterprise and a well-recognized model system for metapopulation biology. Starting in 1993, we have mapped and surveyed the entire 4,000-meadow network, the largest patch network for any species that has been studied in similar detail. In any one year, 400 to 800 of the meadows have had a breeding population of the butterfly, based

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Fig. 5.3 One of the meadows in the Åland Islands in Finland with host plants for the Glanville fritillary. The drawing shows a group of post-diapause caterpillars basking in the sun in April, on top of a web that they have spun. Females prefer to oviposit on host plants in relatively open places, such as that in the photo, which have a warm microclimate in the spring. (Photo courtesy of Mikko Kuussaari; drawing by Zdravko Kolev.)

on the presence of caterpillars in late summer (Hanski 2011). With fifty to sixty undergraduate field assistants, the survey takes two weeks, during which every meadow is visited and the relatively conspicuous webs that the caterpillars spin around the small host plants are counted (figure 5.3). The web is a critical feature of the butterfly’s natural history for us researchers: were the caterpillars solitary, the large-scale survey would be entirely impractical; it would be impossible to find and count hundreds of thousands of cryptic larvae over a landscape of 50 by 70 kilometers. The function of the web remains uncertain. It does not seem to provide efficient protection against the parasitoid wasps that attack the caterpillars, but it may help keep the full-sib (brothers and sisters) caterpillars together, which may enhance their feeding efficiency. The compact web that the caterpillars spin at the end of the summer and that shelters them during diapause may be important in preventing dehydration during the long winter. In the spring, the caterpillar is black with a red head, warning generalist predators of its bad taste, which it acquires by sequestering particular chemical compounds, iridoid glycosides,

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from the host plants. The black color is also helpful when the caterpillars bask in the sun in small groups to raise their body temperature far above the ambient air temperature, without which they could not grow and develop during the cool days in April. Out of the 400 to 800 local populations that exist in any one year, a large fraction, around 100 populations, mostly the smallest ones, are extinct by next year, the exact number varying from one year to another, depending especially on the prevailing weather conditions. During dry summers, the host plants tend to wither in July, and many caterpillars starve. For this reason, though adult butterflies would benefit from sunny weather, substantial rainfall in early summer is important for the survival of their offspring. Climate warming has increased the frequency of dry, warm Julys in northern Europe, which has led to synchronous declines across the entire metapopulation. Fortunately for long-term persistence, the Glanville fritillary has very high fecundity; a female may lay more than 1,000 eggs in her lifetime, which lasts a couple of weeks. Hence the metapopulation has been able to bounce back in the following year, as long as two or more very bad years do not occur in a row. Other causes of local extinction apart from starvation include parasitism by specialist parasitoid wasps. When this happens, the local parasitoid population also goes extinct, as the parasitoid can use only the Glanville fritillary. Some host and parasitoid individuals may have dispersed to nearby meadows, and so the interaction persists, at the network level, in spite of local extinctions, in true metapopulation fashion (Lei and Hanski 1997). Other causes of local extinction include inbreeding depression: small local populations often consist of closely related individuals, and inbreeding reduces the fitness of the offspring so much that the risk of local extinction increases (Saccheri et al. 1998). In the habitat patch network in the Åland Islands, the level of inbreeding is kept in check because unrelated individuals often immigrate from other populations in the network. The situation is different for populations that have become completely isolated because of, for instance, extensive land conversion around them. Such remnant populations are common and are becoming more so where human population density is high and where the need for agricultural land, housing, roads, and other infrastructure reduces the natural habitat. A completely isolated small population of the Glanville fritillary on a small island, called PT, in the middle of the Gulf of Finland has presented a rare opportunity to study the biological consequences of isolation and small population size.

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The butterfly was first collected on the island in 1936. The island has never been inhabited, but it was regularly visited by fishermen and others, often traveling from the Estonian coast, and people most likely accidentally brought caterpillars to the island during their visits (Mattila et al. 2012). After the Second World War, the island remained behind the new border, in Russia. In 1993, a joint Russian-Finnish biological expedition to the islands in the Gulf of Finland was organized, and the Glanville fritillary was still present on PT. I was very excited to hear about this. PT has just a single shoreline meadow, about 10 hectares, and the island is very isolated, 30 kilometers from the Estonian coast, too far for the butterfly to travel on its own. This island is an ideal contrast with the large 4,000-meadow network in the Åland Islands. The only problem was access. The island is in the border zone, and hard as I tried, I could not find a way to get a permit for a visit. Finally, I made contact with a Russian botanist working on the islands in the Gulf of Finland, and we arranged for her to check whether the butterfly still occurred on the island and, if so, to collect a sample of caterpillars. The butterfly was there, and over the next three years, we conducted a series of studies to find out whether it had become locally adapted during roughly 100 years of complete isolation, which might have contributed to its longterm persistence. The results showed just the opposite: the population had greatly reduced genetic variation, as expected, and greatly reduced fitness in comparison with butterflies from the Åland Islands (Mattila et al. 2012). The fact that the population was still alive had more to do with good luck than good genes, but clearly the long-term prospects for its survival are not good at all. I fear that this unique population is an example of what happens to innumerable other populations that are left in complete isolation by habitat conversion in the surrounding landscape. The power of natural selection to improve the chances of their survival is limited by small population size, which means that there is little from which to select locally fit individuals. Nonetheless, if selection is strong enough, populations can still adapt locally (see chapter 2 for a description of the behavior of butterflies on this small island). In recent years, many researchers have started to integrate molecular and genomic tools with long-term ecological research. The purpose is to find out about the genetic and molecular mechanisms that underpin population processes and that may influence natural selection, local adaptation, and even population dynamics. We have sequenced the full genome of the

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Glanville fritillary (Ahola et al. 2014); two other butterfly genomes were already sequenced, the South American Heliconius melpomene (Dasmahapatra et al. 2012) and the monarch butterfly (Zhan et al. 2011). We now have knowledge of thousands of genes and of variation in these genes, which can be related to variation in life-history traits, measures of individual performance, and the dynamics of local populations. We have started to develop a molecular-level understanding of flight (Niitepõld et al. 2009; Wheat et al. 2011), which is critical for almost everything that butterflies do. We have shown that butterflies with high flight metabolic rate disperse longer distances in the field than butterflies with low flight metabolic rate, and we have documented changes in the expression of hundreds of genes associated with flight. At the landscape level, butterflies living in highly fragmented habitat such as the Åland Islands have a different gene-expression profile than butterflies living in more continuous habitat, which suggests that landscape structure has selected particular kinds of butterflies at the molecular level. Extinction Thresholds and the Living Dead The common flu spreads in a human population from infected individuals releasing viruses that infect susceptible (non-immune) individuals. Our parents and grandparents knew, and feared, many other infectious diseases, such as measles, syphilis, smallpox, and hepatitis B. The disease-causing organism, usually a virus or a bacterium, must be able to reproduce to survive in the long run, and it can do so only in host individuals. Reproduction is limited by two factors. The ultimate limit is set by the death of the host, but before that happens, the host immune system may learn to deal with the pathogen and stop its reproduction: the host becomes immune. Before the host develops immunity, however, the pathogen may have colonized another host, or several other individuals, in which reproduction is possible. Pathogen movement from one host individual to another, called transmission, gets easier when the density of susceptible hosts increases and when they have more contact with infected individuals. It is not difficult to imagine that the pathogen could fail to persist in a small host population, where the number of contacts among individuals is limited and therefore one infected individual causes, on average, the infection of less than one other individual. The number of secondary infections caused by one infected individual in a population consisting of susceptible individuals is called the basic reproduction number, R0. The pathogen does not persist if R0 < 1.

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The reason that vaccination works is that it pushes R0 below one by increasing the number of immune individuals, thereby reducing the number of susceptible individuals, and reducing the opportunity for the pathogen to spread. The critical host density of susceptible individuals below which the pathogen cannot spread because R0 < 1 is called the eradication threshold. Seen from the viewpoint of the pathogen, the vaccinated individuals have been removed from the population, and the remaining susceptible host individuals make up a sparse host network, possibly too sparse for the pathogen to invade and cause an epidemic. Many human infectious diseases could not have persisted in hunter-gatherer populations in the past, because these populations consisted of small groups of people and had low overall population density. It is thought that it was only after the Neolithic (agricultural) revolution 10,000 years ago that many disease-causing microbes could move to and evolve in the rapidly expanding human population. It may not be obvious, at first, what relevance infectious diseases have to the dynamics of butterflies and other animals and plants in fragmented landscapes. The correspondence is nonetheless fundamental. Replace a host individual with a meadow, a virus with a butterfly, and the eradication threshold with the concept of extinction threshold, and you have similar questions about long-term persistence of organisms, regardless of whether we consider the dynamics of a virus in a host population or the dynamics of a butterfly metapopulation in a network of habitat patches. The best way of thinking about the extinction threshold is to ask whether a species that is introduced into one habitat patch can spread to the rest of the network. If yes, the landscape is above the extinction threshold, and it can support a viable metapopulation; one local population will send out enough migrants during its lifetime to colonize more than one unoccupied habitat patch. If not, the landscape is below the extinction threshold, and it cannot support a viable metapopulation. Mathematical models have been developed to scrutinize the properties of the extinction threshold in detail, but the idea itself is simple and has been understood for a long time. In an insightful paper written more than half a century ago, American botanist John Curtis (1956, 729) observed: “Within the remnant forest stands, a number of changes of possible importance may take place. . . . Various accidental happenings in any given stand over a period of years may eliminate one or more species from the community. Such a local catastrophe under natural conditions would be quickly healed by migration of new individuals from adjacent unaffected areas. . . . In the isolated stands, however, opportunities for inward migration are small or nonexistent. As a

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result, the stands gradually lose some of their species, and those remaining achieve unusual positions of relative abundance.” There are some differences between the dynamics of infectious diseases and the dynamics of animals and plants living in fragmented landscapes. Meadows and other habitat patches do not become “immune,” though they may become unsuitable because of successional changes in the vegetation, for example, or because of overexploitation by the species that have colonized them. Note, however, that some infectious diseases, such as gonorrhea caused by the bacterium Neisseria gonorrhoeae, do not lead to immunity. Another difference is variation in patch sizes. Host individuals, habitat patches for pathogens, are roughly of the same size, but habitat patches for plants and animals typically vary greatly in size. For instance, the meadows in the Åland Islands where the Glanville fritillary thrives vary from a few dozen square meters to ten hectares. Other things being equal, large habitat patches have larger populations than small patches, and because larger populations typically have a longer lifetime than small populations, large habitat patches play an especially important role as sources of colonists to other patches in the network. This is comparable to some individuals in a host population being “super-spreaders,” particularly potent transmitters of the infectious disease to other individuals, for instance, because they have exceptionally large numbers of close contacts with other individuals. To predict the dynamics of a pathogen or a butterfly in a patch network, one needs to know the structure of the network, whether there are super-spreaders and particular habitat patches that support long-living local populations, and where in the network they are located. All these factors influence the extinction threshold. Finally, random environmental variation affects metapopulation persistence. For instance, unfavorable weather conditions can cause the extinction of a small metapopulation even if R0 > 1. The metapopulation is expected to survive, but it may nonetheless go extinct because of random environmental variation. The extinction threshold is a feature of a habitat patch network at the landscape level. At the level of individual habitat patches and populations, the concept of extinction threshold can be applied in terms of the balance between individual births and deaths. Clearly, any population will go extinct if deaths exceed births when the population is small. This may happen when habitat quality has deteriorated and has either increased the death rate or decreased the birth rate. The extinction threshold then depends on habitat quality. A related concept that ecologists, evolutionary biologists,

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and conservation biologists have debated for a long time is the minimum viable population size, which concerns the expected lifetime of populations. The 50/500 rule recommends that a population needs more than 50 breeding individuals to have a fair chance of surviving for at least tens of generations, and more than 500 breeding individuals to survive for a long time and to have the ability to adapt to changing environmental conditions (Franklin 1980). More recent studies suggest that somewhat higher numbers, around 100 and 1,000 individuals, are needed (Frankham et al. 2014), though strictly speaking there is no reason to assume that there would be any magical numbers that could separate populations that will survive from those that will not. The isolated Glanville fritillary population on PT has had approximately 100 breeding individuals over 100 years, yet it has accumulated a large genetic load of deleterious mutations because of inbreeding. Nonetheless, the above figures point in the right direction: conservation of wild populations should aim at maintaining or restoring populations with at least several hundred individuals to ensure their survival in the short run. The concept and theory of the extinction threshold at the landscape level are well formulated, but what about evidence from real metapopulations? The Glanville fritillary study has provided some of the best examples. The butterfly occupies a huge network of meadows across a large area, and there is much variation in the density of meadows from one part of the study area to another. Because butterflies disperse only a few kilometers in their lifetime, different butterflies living in different parts of the Åland Islands experience very different levels of habitat fragmentation. We divided the 4,000-meadow network into dozens of subnetworks, which are isolated from each other because of the butterflies’ restricted movement distances, and which can therefore be considered largely independent landscapes with different amounts of habitat distributed among a smaller or larger number of meadows. But how should we characterize the subnetworks, given all the variation in the number of meadows and in their size and distance from one another, which influence the expected lifetimes of local populations and the opportunities for colonization? Just counting how many meadows each subnetwork has would not be sufficient. My colleague Otso Ovaskainen and I (2000) have derived from mathematical theory a measure called metapopulation capacity, which takes into account the number, size, and isolation of individual habitat patches in a network. It turned out that the larger the metapopulation capacity of the subnetwork, the more habitat in the subnetwork was occupied by the butterfly (figure 5.4A). Moreover, there is clear

Fig. 5.4 A, the proportion of habitat patches (meadows) occupied by the Glanville fritillary in 25 networks in relation to the metapopulation capacity (λM) of the network. The 25 networks are part of the entire 4,000-patch network in the Åland Islands. Metapopulation capacity is a measure of the suitability of the network for the butterfly (see the text). The empirical data (dots) have been fitted to a spatially realistic metapopulation model (continuous line). These results are a good example of extinction threshold. (From Hanski and Ovaskainen 2000.) B, the proportion of forest fragments occupied by forest-specialist, nonflying small-mammal species in fragmented landscapes in the Atlantic forest region in Brazil. Data are from four landscapes of 100 square kilometers and with 10%, 30%, 50%, or 100% forest cover. Notice that most species have an extinction threshold between 10% and 30% forest cover in these data. Broken lines indicate the uncertainty about the precise extinction threshold. (Data from table S2 in Pardini et al. 2010.)

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evidence for an extinction threshold: when the value of the metapopulation capacity was smaller than a critical value, the butterfly was completely absent from the subnetwork, though meadow habitat was still available— but too little, and too fragmented, to support a viable metapopulation. The metapopulation capacity can be used to rank different landscapes in terms of how well they support metapopulations. This can be useful for practical conservation, because one can also compare hypothetical landscapes that could be created by appropriate restoration. We have developed models that can be used to ask about the value of adding habitat at particular spatial locations in the network (Ovaskainen and Hanski 2003). The second example of the extinction threshold concerns forest loss and fragmentation in the Atlantic forest region in Brazil, which is a global biodiversity hot spot and a region that has been very well studied— a natural laboratory for fragmentation studies. Brazilian ecologist Renata Pardini and her colleagues (2010) have investigated the occurrence of nonflying small mammals in large forested landscapes of 100 square kilometers. Some landscapes have essentially 100% forest cover; in other words, they are still in a more or less virgin state, while three other landscapes retain 10%, 30%, or 50% of the original forest cover. Pardini and her students trapped small mammals at approximately fifteen study sites across each landscape, to find out which species were present and which were absent in each landscape, and how common they were if present. Naturally, such trapping may miss some species; it would be impractical to trap every single forest fragment across a large landscape. However, as trapping was done where each landscape offered the best environmental conditions for the small mammals, it is reasonable to assume that the results allow a fair comparison between the landscapes. Pardini’s results are plotted in figure 5.4B: the horizontal axis gives forest cover in the landscape; the vertical axis shows the proportion of trapping sites in each landscape where a particular species was recorded. Note the large differences in overall commonness of species, which is typical for all animal and plant communities. A few species occurred at practically every trapping site in the landscape with continuous forest cover, but other species were uncommon, recorded from only a few sites. These differences likely reflect differences in species’ ecological requirements. For instance, some species may require particular microhabitats that have a patchy distribution in forest landscapes. In landscapes with less than 100% forest cover, many species tended to retain their overall commonness: species that were common in the landscape with 100% forest cover were common also in

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landscapes with 50% forest cover and even with 30% forest cover. But the striking result is the change between the landscapes with 30% and 10% forest cover: only a single species was recorded from the landscape with 10% forest cover. It is apparent that most species in this community have an extinction threshold between 10% and 30% forest cover. Similar results have been reported in other studies of the occurrence of birds and small mammals in fragmented forest landscapes (more about this below). Some may question whether the apparent extinction threshold in the small-mammal example really demonstrates the effect of fragmentation. Perhaps this result simply reflects the total amount of forest habitat in the landscape? It would be helpful to describe the forest structure using the measure of metapopulation capacity, as in the butterfly example, which would reflect the spatial configuration of the total amount of habitat within the landscape. In the absence of such data, a thought experiment can address the question about the role of fragmentation as opposed to loss of habitat area. Consider a landscape that has 10% forest cover across the area of 300 square kilometers. Based on Pardini et al.’s (2010) results, we can expect that just a single species would occur in this landscape, which is below the extinction threshold of the other species as shown in figure 5.4B. Note that it does not matter whether the total landscape area is 100 square kilometers or 300 square kilometers. Now, let us create a hypothetical landscape of 300 square kilometers by moving all the habitat in the original 300-square-kilometer landscape into one-third of its area, where there would now be 30% forest cover distributed in the same way as in the real landscape with 30% forest cover. Again based on Pardini’s results, we can assume that this hypothetical landscape of 300 square kilometers has many species, namely, those that are above their extinction threshold in the 30% landscape (figure 5.4B). Note that we have not changed the total area of the landscape (300 square kilometers) nor the total amount of forest (0.1 × 300 = 30 square kilometers): we have changed just the spatial configuration of the forest within the landscape, that is, the degree of fragmentation. This example highlights the significance of fragmentation for the occurrence of species. The results in figure 5.4 assume that metapopulations are at equilibrium between extinctions and colonizations. This is a reasonable assumption if habitat loss and fragmentation occurred mostly so long ago that the populations have had time to adjust to the new environment. This is known to be so in the examples in figure 5.4, but often habitat loss and fragmentation are recent, or even ongoing, and metapopulations are unlikely to be at equilib-

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rium. In these cases, it is not obvious whether a species that is not extinct is below its extinction threshold: perhaps it just has not had time to go extinct. It would be important to know how fast species generally decline to extinction. Finally, if the species is below its extinction threshold but has not yet gone extinct, can anything be done to stop it from going extinct? These are important questions about the future of biodiversity, especially because habitat loss and fragmentation are the main causes of threat and extinction in most ecosystems. If we are not aware that many rare species are actually below their extinction thresholds and hence doomed to extinction, we will underestimate the threat to biodiversity. We may mistakenly conclude that all the species that are still around will survive if there is no further damage to their environment. But this is not so: many of the rare and threatened species could be below their extinction threshold, on their way to extinction, “living dead.” The fraction of species in a community that are below their extinction threshold constitute the extinction debt of the community. Like any debt, extinction debt has to be paid, or one goes bankrupt. The extinction debt can be paid by improving the landscape so that species are again above their extinction threshold. This can be done by restoring habitat or by improving habitat quality. “Going bankrupt” means allowing species to go extinct and thereby losing forever the natural capital that they represent to humans (chapter 6). Can we determine the magnitude of the extinction debt in a particular community? In principle this is simple— just count the fraction of species that are systematically declining toward extinction— but in reality the calculation is nearly impossible. The size of natural populations fluctuates for all kinds of reasons, and even if there is no long-term declining trend, roughly half of the time populations show a temporary decline, before they start to increase again. Without very long records, which are usually not available, it is impossible to distinguish long-term decline from short-term population fluctuations. Moreover, even if there were a clear long-term trend in population size, the species is not necessarily below the extinction threshold; it could be just above it and on its way to becoming a permanently rare species. To assess the magnitude of the extinction debt, one needs to know the ecology of the species very well, have high-quality information about past changes in the amount and spatial configuration of the habitat, and have some additional information to make the calculation possible. Estonian botanist Aveliina Helm and her colleagues have attempted to estimate the size of the extinction debt in a study of vascular plant species in

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calcareous grasslands on the Estonian islands of Saaremaa and Muhu (Helm 2003). In the 1930s, there were 377 grassland patches with the total area of 260 square kilometers. By 2000, the total area had declined to 78 square kilometers, distributed among 413 patches (habitat loss had been accompanied by increased fragmentation). The current areas and connectivities of the grassland patches did not explain the current number of plant species in individual meadows, whereas the areas and connectivities of the meadows seventy years ago explained one-quarter of the variation in species number in 2000 (Helm et al. 2005). This finding indicates that the current distributions of species are not at equilibrium with the current environment, but reflect the structure of the environment in the past— the species have not had time to adjust to the new environment. The extra information that Helm and colleagues used was a set of fourteen meadows in which the species number had remained about the same for seventy years. They assumed that the plant communities in these meadows were at equilibrium, and constructed a species-area relationship (chapter 1) for these meadows to predict the equilibrium number of species for fragments that were evidently not at equilibrium. This analysis suggested that extinction debt was roughly 40%; that is, 40% of the current species in the habitat patches were predicted to go extinct because of the past habitat loss, even if the environment did not deteriorate any further. Extinction debt is common, though its magnitude is poorly known: a meta-analysis (meaning an analysis of the results of many previously published studies) of forty-two separate studies reported indications of extinction debt in thirty-eight studies (Kuussaari et al. 2009). Extinction debt can be assumed to be large, and the decline of the “living dead” species to extinction can be assumed to be slow, in species with slow population dynamics. For instance, perennial plants may persist as individuals for decades or even centuries in landscapes that do not allow enough reproduction and colonization of unoccupied habitat to compensate for deaths and extinctions. Many plant species in the study of Helm and her colleagues were perennials, which explains part of the large extinction debt they found (Helm et al. 2005). Rigueira and colleagues (2013) have reported on Myrtaceae, woody plants, in the Brazilian Atlantic forest. They compared species richness in nine large landscapes with 5% to 55% forest cover. Overall they recorded 174 species, but landscapes with less than 20% forest cover had just a few species, apparently because most species were below their extinction threshold there. The number of species represented by saplings and young trees showed clearly reduced species richness in landscapes where

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forest cover was below 40%, whereas species richness of adult trees started to decline only in landscapes with forest cover less than 30%. This makes sense: the adult trees were older than the age of deforestation, which was forty to sixty years; they were established when there was more forest than at present, and the presence of adult trees reflects the great longevity of individual trees, not the quality of the landscape. The occurrence of saplings, in contrast, reflects the processes that are taking place in the current landscape. Another factor that influences the speed of decline after habitat loss is counterintuitive: one might expect that approaching the new equilibrium, which could be extinction, is fast in species that are close to their extinction threshold after habitat loss, but in fact the opposite is true; these species have especially slow dynamics (Hanski and Ovaskainen 2002). This means that a large fraction of the currently rare species, including species that are classified as threatened species, are species that are responding very slowly to past habitat loss and fragmentation. Many of them are doomed to extinction unless the quantity and quality of their environment are improved. Debates about Habitat Fragmentation To outsiders, scientists may appear to work together like ants to advance their common plans. It is indeed true that scientists have occasionally joined forces to accomplish surprising undertakings, such as sequencing the human genome and discovering the Higgs boson. Some politicians seem to think that the best they can do is to direct this ant army toward tasks that would benefit the national economy. But this vision of science and scientists misses an essential element. Most scientists spend much of their time in doubting the results of other scientists and in thinking ways of showing that the others are just plain wrong. This does not imply that especially egocentric and spiteful individuals end up as scientists; rather this doubt indicates the very spirit of science. Science is a wonderful self- correcting enterprise, where wrong results are unlikely to survive for long, especially if they are of any real importance. It is a huge misunderstanding that scientists could conspire over some subject, such as climate change, to present misleading results and thereby obtain more money and other benefits for themselves and their work. They cannot, because the door is always open to anyone to demonstrate what is wrong, and the system rewards such demonstrations, as long as the evidence is there.

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Given the nature of science and scientists, there is no lack of those who look for faults in existing models, data, and analyses. Occasionally it turns out to be difficult to show that this or that theory is more or less correct than others, and disputes can continue for decades. One example related to metapopulations is group selection, which challenges the standard view that natural selection operates among individuals. It has been suggested that even human evolution has been shaped by group selection, on the assumption that our ancestors lived in small groups of hunter-gatherers, and the success of these groups depended on their collective attributes, not only the attributes of individual group members. The present view is that group- level selection may indeed occur under certain conditions, but the appropriate conditions are quite restrictive. Good examples are groups of parasites living in host individuals: selection for more competitive parasite individuals, which would be more harmful to the host, may be tempered by group-level selection, because a very aggressive group of parasites would quickly kill its host and the parasite would have limited opportunities to infect other hosts. Another controversy that has lasted for more than forty years concerns the consequences of habitat loss and fragmentation on population viability and biodiversity. Everybody agrees that the main cause of declining biodiversity in the past and at present is overall loss and degradation of habitat, which reduce the amount of living space and resources for populations. What is more contentious is the significance of habitat fragmentation, which almost always accompanies habitat loss: with decreasing total amount of habitat, the remaining habitat occurs in smaller patches that are more distant from each other. The reason it has been difficult to disentangle the possible independent effects of the reduction in the total area of habitat and increasing fragmentation is that they go hand in hand, making it difficult to distinguish correlation from causality. Nonetheless, questions about the ecological, genetic, and evolutionary consequences of fragmentation are important, and the degree of fragmentation is generally increasing with increasing pressure on natural and semi-natural habitats. We cannot afford misleading conclusions about the consequences of habitat fragmentation, which could lead to poor management decisions. Questions about the spatial configuration of habitat at the landscape level— how is habitat distributed in space?— came to the forefront in the mid-1970s, when several researchers proposed rules of design for protected areas, which were based, or were thought to be based, on the island theory

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Fig. 5.5 The “island biogeography” rules for the design of protected areas. For each rule, the design on the left is seen as superior to the alternative on the right. (After E. O. Wilson and Willis 1975; IUCN 1980.)

of MacArthur and Wilson. Figure 5.5 illustrates pairs of alternatives; the one on the left in each pair was considered to be superior to the alternative on the right. In the first pair (A), there is no dispute: Other things being equal, it is always better to have a larger protected area, which on average has more species with more viable populations than a small area. The next pair illustrates what is called the SLOSS question: Is it better to have a single large reserve or several small ones with the same total area? The other rules emphasize the role of spatial proximity (connectivity) of the reserves, which influences dispersal and gene flow among local populations and increases the probability of recolonization if one local population goes extinct. However, the degree of connectivity is related to other processes as well, to which I return below, and hence these contrasts do not have as much generality as once thought. The rules depicted in figure 5.5 were quickly adopted by conservation organizations as well as by conservation biologists, which is surprising in hindsight, because the island theory leads only to the first prediction (A), concerning the area effect. The framework probably became popular

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because it opened up a new way of thinking about habitat conservation, just as the island theory signified a paradigm shift in biogeography and spatial ecology in general. The message for conservation was that fragmentation is bad and that small protected areas are not that valuable, because the small populations inhabiting small habitat patches are likely to go extinct anyway. The first message continues to be valid, with various qualifications, but the second message is potentially misleading because it ignores the possibility of metapopulation-level persistence in fragmented landscapes, though again there are important caveats related to the extinction threshold. The SLOSS question (figure 5.5B) has been the focus of debates about habitat fragmentation: What difference does fragmentation make to population viability and species richness in addition to the effect of lost pooled area of habitat? It is now realized that several factors determine which option is preferable; there is no universal answer to the SLOSS question. For instance, it makes a difference how fast population viability (expected lifetime) increases with increasing area, whether the dynamics in several small fragments are correlated due to environmental factors (such as weather conditions), and indeed how isolated the fragments are from each other in relation to the dispersal capacity of the species. Other factors are not part of the question, strictly speaking, but nonetheless influence the outcome in practice. The edge effect, the influence of the environmental conditions outside the landscape fragments, has greater impact on small fragments than on large ones, because small fragments have more edge in relation to their area. Perhaps out of frustration with different answers to the same question, some researchers, especially Canadian landscape ecologist Lenore Fahrig (2013), have concluded that what really matters is just the total amount of habitat across the landscape, while the spatial configuration, that is habitat fragmentation, makes no or only limited difference. There was so much emphasis on spatial configuration of habitat in the 1970s and 1980s that the primary role of the total amount of habitat in setting the viability of species may have been obscured, and Fahrig’s work has helped correct the balance. The message is that we cannot solve problems of population viability caused by massive habitat loss by careful placement of the remaining small fragments. However, as is often the case when the relative contributions of two factors are being weighed, the balance can swing to the other extreme position. Habitat fragmentation does matter and is a very important issue for biodiversity conservation in landscapes where there is little natural or semi-natural habitat left.

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I have already explained that it is hard to separate how much the total amount of habitat and the degree of fragmentation affect biodiversity, because the two are typically strongly correlated. In this situation, one way forward is to use models to disentangle the effects of the two factors, as we can generate and study any kind of landscapes in terms of the spatial arrangement of the habitat. This is only a partial solution, because models are not reality, and we have to be cautious in interpreting modeling results. Nonetheless, carefully constructed models are as valuable in ecology as they are in other fields of science. Figure 5.6 shows the results of a model that I constructed with my colleague Joel Rybicki (Rybicki and Hanski 2013). We simulated the dynamics of a large number of species in a large landscape, modeled as a grid of 512 by 512 cells, thus altogether 0.25 million spatial locations. We made the model realistic by including various factors, such as spatially correlated, heterogeneous habitat and variation in species’ ecological requirements. In the model, habitat fragments are simply contiguous groups of cells of appropriate habitat for a particular species with its specific habitat preference, separated from other fragments by some entirely different habitat, just as in real landscapes. In figure 5.6, the total amount of habitat varies from 1% to 30% of the total landscape area, and the habitat is split into a smaller or larger number of randomly located, equally large fragments, as shown in the key. As expected, species richness is strongly affected by the total amount of habitat in the landscape and by the degree of fragmentation when the total amount of habitat is small. This is an important point: fragmentation matters when the total amount of habitat in the landscape is small. In figure 5.6, species richness is high when 5% of the landscape area consists of habitat that occurs in one or a few relatively large fragments, but no species persist when the same amount of habitat is split into a large number of small fragments. Note also that a moderate amount of fragmentation actually increases the number of species surviving in the landscape, because the fragments are spread out and have somewhat dissimilar habitat composition (an assumption of the model); hence these fragments support more species than a single large fragment that has less diversity in habitat type. Even in this case, however, a high level of fragmentation causes a reduction in species number. The explanation for these results is extinction threshold: when the total amount of habitat is small and fragmentation is high, many species are below their extinction threshold and thus go extinct, as in figure 5.4B, showing small mammals in the Atlantic forest region in Brazil.

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Fig. 5.6 Simulated results showing how many species are predicted to persist in landscapes that have habitat that is 1% to 30% of the total landscape area, and that have different degrees of habitat fragmentation. The lines show into how many equally large and randomly located fragments the given amount of habitat (horizontal axis) has been split. Notice that species number decreases with decreasing total amount of habitat and with increasing fragmentation. (From Rybicki and Hanski 2013.)

The most highly fragmented situation in figure 5.6 may seem extreme, but unfortunately it is not an unrealistic example. Highly fragmented landscapes are becoming ever more common with continuing habitat conversion. To take an example from practical conservation, in Finland more than 100,000 “woodland key habitats” (WKH) have been delimited in managed forests and are left untouched, in order to protect forest biodiversity, while the rest of the forest is clear-cut (Hanski 2008). There is thus a huge number of WKHs, but they are all very small, with an average area of 0.7 hectares, and they are widely scattered across 20 million hectares of forested land. A meta-analysis found no difference in the numbers of threatened species in WKHs and in equal-sized control plots in the surrounding managed forests— both had almost none (Timonen et al. 2011). The WKHs

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may represent an extreme example, but they are also an example of how managers claim to protect biodiversity, in spite of excessive fragmentation of the habitat. We should not endorse such practices, because we know that a very high level of habitat fragmentation undermines population viability. To take another example, vast areas of tropical forest are being converted to oil-palm plantations in Southeast Asia, where recommendations have been made to reduce species loss by retaining fragments of natural forest within plantations (Lucey et al. 2014). How large these fragments should be, and what their density should be across large areas to protect even a fraction of the original biodiversity are hugely important questions for conservation. The most important conclusion about habitat fragmentation in the case of land-covering habitats such as forests is this: Fragmentation makes little or no difference if the total amount of habitat is large, more than 20% to 30% of the landscape area. In that case, all habitat is relatively well connected and hence the spatial configuration does not matter. Conversely, when the total amount of habitat is less, the degree of fragmentation makes a difference, and the more so the less habitat there is. This conclusion is supported by many empirical studies (Lande 1987; Andrén 1994; Hanski 2005), one of which is shown in figure 5.4B, as well as by theoretical studies, exemplified by the results in figure 5.6. This threshold is often called the 20% rule, though the value depends on the ecology of the species. A highly dispersive species, or a species with high local population density, may have an extinction threshold that is substantially smaller than 20%. Note also that the threshold below which fragmentation makes some difference to the distribution and abundance of species is not the same as the extinction threshold, which gives the limit below which the species goes extinct. The 20% rule applies to landcovering habitats, which originally covered most of the landscape. In contrast, many habitat types are naturally sparse and patchy, and the species inhabiting these habitats have become adapted, in one way or another, to extreme fragmentation, in which case much less habitat out of the total landscape area is sufficient for viable populations. The Glanville fritillary in the Åland Islands is an example: the butterfly persists in the network of 4,000 meadows even if the meadows cover only 1% of the total landscape area. Nonetheless, even species adapted to living in highly patchy habitats lose their viability when the density of habitat patches becomes very low, that is, when the species drop below their extinction threshold, as shown by figure 5.4A for the Glanville fritillary.

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The Shrinking World of Forest-Inhabiting Species Forests represent the most complex ecosystem on land in terms of physical structure, which is produced by large trees and other plants, and in terms of the number of species. Nobody knows the true figure, but a conservative guess is that at least half of all the species on land occur in forests, and most of them occur in tropical forests. Forests provide vital renewable resources, without which civilization might not have emerged at all and which critically support many societies today. Another very different reason for focusing on forests in this section is that much of the research on habitat loss and fragmentation is concerned with forests, which often present a clear contrast to the surrounding non-forest habitat. In contrast to the constant physical size of our planet, the amount of forest has changed greatly at many time scales. To place the present in perspective, recall from chapter 1 that during the 300 million years of the Paleozoic era, from 541 to 252 mya, plants moved onto land and gradually grew into complex communities, including forests that were structurally similar to the present ones, though they lacked angiosperms and most herbivorous animals; the forest ecosystems consisted of primary producers and decomposers. In the 180 million years of the Mesozoic era, angiosperms came to dominate the vegetation, and the evolution of herbivorous vertebrates culminated in massive sauropods, which browsed trees up to the height of ten meters. After the fifth mass extinction 66 mya, mammals radiated into their present position in forest and non-forest ecosystems, and herbivorous insects radiated together with angiosperms (chapter 2) to make up the bulk of all biodiversity. Global climate has been cooling over the past tens of millions of years, which has reduced the area of forests and increased the area of open vegetation types— savanna, steppe, tundra, and desert. Before the Neolithic revolution, the beginning of human dominance on Earth, forests covered approximately half the land area; this is known from general ecological understanding of how soil properties, elevation, and climate influence potential vegetation. Since then, roughly half the forests have been converted to something else (Bryant et al. 1997), and forest loss continues today. A comprehensive analysis of high-resolution (thirty meters) satellite images covering the entire planet discovered that 2.3 million square kilometers of forests were lost in the period 2000–2012, while 0.8 million square kilometers of new forests appeared, either through natural succession or planting

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by humans (Hansen et al. 2013). Based on these figures, and the total forest area of 23.5 million square kilometers reported by Hansen and colleagues (2013), the annual rate of forest loss is approximately 0.5% per year. Here forest is defined as land with tree cover exceeding 76%, which corresponds to dense closed-canopy forests. There is much discrepancy in the figures concerning forest cover because different authors and organizations use different criteria. For instance, areas with more than 10% tree cover are defined as forest by the Food and Agriculture Organization of the United Nations (2010). In brief, the current amount of forests on Earth is approximately 40 million square kilometers, based on a compromise definition of forest, with tree cover exceeding 25% (Hansen et al. 2013), or 27% of land area— roughly half of what it was 10,000 years ago. This figure does not take into account three factors that reduce the viability of many forest-inhabiting species and reduce the overall biodiversity in forests: fragmentation, which may take a forested landscape below the extinction threshold of many species, and in any case increases edge effects; great simplification of forest structure and loss of microhabitats in intensively managed forests and in plantations; and defaunation, loss of large-bodied species due to excessive hunting and poaching, with cascading effects on the functioning of the forest ecosystem. Increasing fragmentation means that the amount of boundary between forest and non-forest habitats increases in relation to the pooled area of forests. The increased edge effects include physical, biological, and anthropogenic processes that extend from the forest edge toward the interior. This means that the quality of forest close to the edge is altered, and this reduces the fitness and abundance of forest specialist species, while it improves conditions for generalist species that flourish in heterogeneous landscapes, mixtures of different habitat types. Overall biodiversity may not be reduced much if at all by forest fragmentation, but the species composition is much affected, with a shift toward habitat generalists. From the viewpoint of conservation, this change is detrimental, because forest-specialist species typically include threatened species, whereas the generalists are mostly common, widely distributed species. A detailed analysis of global tree-cover data revealed that 20% of the world’s remaining forests are located within 100 meters of forest edge, and more than 70% are located within one kilometer of the edge (Haddad et al. 2015). These figures indicate massive edge effect. The largest non-fragmented expanses of forest are in the Amazon and Congo

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river basins, in parts of Southeast Asia, in New Guinea, and in the boreal region of North America and Eurasia. Decreasing the total amount of forests and increasing their fragmentation means that an increasing number of forest-specialist species approach their extinction threshold at the landscape level. With further loss and fragmentation of forests, many species risk crossing the threshold, especially endemic species with small geographical ranges. It would be interesting to know how much of the forested land has forest-specialist species that are below or close to the extinction threshold. Considering the thirty-five biodiversity hot spots defined by Mittermeier and colleagues (2004), the percentage of remaining natural vegetation varies from 3.5% to around 34.8% (Sloan et al. 2014). The original definition of hot spots required the percentage of remaining natural vegetation to be less than 30% (chapter 1), but reassessment of the vegetation types over the years has somewhat changed the values for the thirty-five hot spots. The natural vegetation includes forests and other habitat types in many hot spots. Three hot spots with a very low percentage of original forest vegetation include the Atlantic forest in Brazil (3.5%), coastal forest of eastern Africa (3.8%), and Madagascar (4.4%). Three to four percent of the original vegetation is very little indeed, and if the remaining forest were relatively evenly distributed across the entire hotspot area, most forest-specialist vertebrates and many other species as well would fall below their extinction threshold (see the example in figure 5.4B and the model prediction in figure 5.6). This means that the hot spots would have enormous extinction debt; their biodiversity, including the large numbers of endemic species that occur in hot spots, would be in a very steep decline. Fortunately, it helps that in practice, subregions within hot spots have a higher-than-average proportion of natural vegetation remaining. The spatial configuration of forests is especially well described for the Atlantic forest region in Brazil, a vast area that originally covered approximately 150 million hectares (Ribeiro et  al. 2009). The remaining forest, including secondary forests from intermediate to advanced successional stages, occurs in 245,000 fragments, of which nearly half are less than 50 hectares. Altogether, the remaining forest covers 11% of the original area, which is more than the 3.5% referred to above, because the analysis includes secondary forests as well as primary forests (Ribeiro et al. 2009). In any case, the degree of fragmentation is very high, and a very large proportion of the land has forest cover of less than 20%, the value below which many species

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lose viability, and biodiversity in general declines. On the positive side, a few very large forest fragments remain, mostly at high elevations on mountains, where the pressure to use land for other purposes has been lower than in the lowlands. The areas with higher-than-average density of forest fragments make up networks that potentially support viable metapopulations. Nobody has done a comprehensive global analysis of forest fragmentation to assess the proportion of forested land that is below particular values of forest cover, but the proportion that is below 20% forest cover is likely to be a substantial percentage of the global forest area of 40 million square kilometers. This means that, from the point of view of many forest-living species, the size of their world is much less than the total amount of forests, and the size of this world is shrinking. Estimates of the global area of forests include various kinds of managed forests and plantations as well as natural forests. It is important to have separate figures for the two main categories of forests, but apparently the distinction is difficult to make with remote-sensed information at the global scale. The main difference between plantations and intensively managed forests, on the one hand, and natural forests, on the other, is great simplification of forest structure. To maximize the production of biomass, plantations and intensively managed forest stands have just one tree species, the trees are of the same age and size, and the amount and diversity of microhabitats that characterize natural forests are minimized. The difference in tree species diversity between natural forests and plantations is the greatest in the tropics, where almost all herbivorous insects cannot find a host-plant species in plantations, so they are automatically excluded. Of the microhabitats, the amount of dead wood, or more technically coarse woody debris, including dead and decaying logs, stumps, and snags, is especially important in all kinds of forests, as this is the habitat for thousands of species of insects and other invertebrates and fungi, which participate in the decomposition of plant material and thereby maintain nutrient cycling in forest ecosystems. The difference in the amount of coarse woody debris between natural and intensively managed forests is up to two orders of magnitude, from 60 to 200 cubic meters per hectare in natural forests, and from 2 to 10 cubic meters or less per hectare in managed forests. In Finland, with approximately 20,000 forest-inhabiting species, 4,000 to 5,000 species live in the dead-wood microhabitat. The low amount of coarse woody debris is the most important cause of threat among the nearly 2,000 red-listed species whose primary habitat is forest (Rassi et al. 2010).

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Plantations and intensively managed forests deliver renewable resources, especially wood fiber and energy but also raw material for various products, and plantations and managed forests capture and store atmospheric carbon dioxide. Plantations and managed forests thereby make very positive contributions toward a more sustainable economy and development, but the big problem that should not be ignored is the very negative impact on biodiversity. Unfortunately, at present the future of biodiversity is only a secondary concern all over the world. In Sundaland in Southeast Asia, a biodiversity hot spot, oil-palm plantations as well as pulpwood and rubber plantations are replacing natural forests with frightening speed, often via forests that are first selectively logged. The result is the same. During my first visit to Gunung Mulu in 1978, Sarawak had 23,000 hectares of oil-palm plantations; today the area is more than 1 million hectares, and the aim is to increase it to 2 million hectares by 2020, which would mean replacing the vast majority of lowland forests in the entire state of Sarawak with plantations. If this happens, massive loss of biodiversity cannot be avoided. The oil palm is a wonderful plant, combining very high yield with modest nutrient requirements, but turning a biodiversity hot spot into a plantation is not wise policy. Apart from annihilating biodiversity, vast plantations of one or a few plant clones pose serious social, economic, and biological risks, including the almost inevitable emergence in the future of some disease that cannot be controlled. In the boreal region in my home country, the disappearance of forest biodiversity is an equally serious concern. The intensively managed forests are practically plantations that cover vast areas. The 140,000 kilometers of forest roads means that all of the 20 million hectares of forested land is within the reach of the heavy machinery of industrial forestry. One would hope that in a rich developed country such as Finland, biodiversity would be taken seriously in forest management, but this is not so. The measures that are supposed to protect biodiversity in managed forests are cosmetic (Hanski 2008). The third reason that global figures about the extent of forests give a misleading picture of the shrinkage of the world’s forests is defaunation, the decline and loss of large and medium-sized animals from the ecosystem. Turning forest into an intensively managed stand or plantation intensifies defaunation. It can also occur, due to excessive hunting and poaching, even if the forest trees remain intact. In a well-studied large region in the Brazilian Atlantic forest, researchers assessed the survival of 18 species of mediumsized and large-bodied mammals in 196 forest fragments (Canale et  al.

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2012). There were historical records of 3,528 populations of the 18 species in the 196 fragments, of which only 767 populations had survived. Each forest fragment had only 3.9 species, on average, out of the total of 18. In this region, forests are highly fragmented, and the fragments are highly accessible to hunters (Canale et al. 2012). Defaunation occurs even in protected areas, as I observed during my two visits to the Gunung Mulu National Park in Sarawak in 1978 and in 2013. The park is 500 square kilometers and generally well-managed, but the problem is hunting and poaching, which appear to stem from a failure to engage people in the surrounding villages in running the park. When the park was established, hunting rights were granted to people whose families used to be nomads in the park or lived in the surrounding villages; these rights have become inflated over the years, and there is no proper control. The caves in the park have huge colonies of edible-nest swiftlets, whose nests continue to be collected, legally or illegally, and people collecting the nests kill any larger mammals for food while in the park. When I was in Mulu in 1978, I saw abundant wild boars, mouse deer, macaque monkeys, and gibbons— none of which were visible in 2013. They are not yet extinct, but much scarcer than before. Gunung Mulu is not an exception; colossal defaunation is taking place across the tropics, including a large fraction of protected areas. In those regions with much forest left but rapidly increasing human population, such as parts of the Congo river basin in Africa, demand for bush meat is high among the urban population. Hence what used be sustainable hunting by people living in forests has turned to unsustainable trade (Wilkie and Carpenter 1999). The consequences of defaunation extend beyond the extirpation of the animals that are directly concerned. Defaunation has immediate consequences for tree dispersal, plant recruitment and understory plant diversity, and animal behavior, and ultimately for plant population and community dynamics and ecosystem functioning (Galetti and Dirzo 2013). The earth had forests without large vertebrates in the Paleozoic, before any large vertebrates had evolved, and again in the early Cenozoic, after the meteorite impact 66 mya that wiped out dinosaurs and before the evolution of large-bodied mammals. Are we now entering another period of empty forests?

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The Third-of-Third Rule The mass of the Earth is approximately 6,000 yottagrams, or 6,000 million million million million grams. The surface area is just over 500 million square kilometers, of which 30% is land; the rest is water. From the human perspective, the size of the earth is constant, not increasing or decreasing; the finite and constant size of the planet sets the carrying capacity for biodiversity as well as for humanity. If humankind were really smart, we would pretend that the planet is smaller than it is, for instance, only 70% of its true size, and we would set aside the remaining 30%, a part of the planet without any people at all, as a form of insurance for the future of our own species and that of the others. Naturally, this 30% should represent all the biomes and ecosystem types, not only ice and rock. After all, Earth’s area was not designed to be what it is; it just happens to be 500 million square kilometers. If only 70% were available to us, we would adjust to that size as well, or as poorly, as we have adjusted to the true size of the planet. But we are not so smart; our species discovered and conquered the entire planet a long time ago, and it is not conceivable that we would give up 30% of it. Other approaches to the conservation of environment and biodiversity are needed. Here, I sketch one approach. On the evening of January 19, 2011, I hosted a guest and a group of students and researchers in a restaurant in downtown Helsinki. I had forgotten to tell my wife where we were dining, and I had forgotten to take my mobile phone with me. She managed to locate me anyway, and she let me know via a student’s phone that I should be home in less than an hour to receive an important telephone call. That’s when I learned that I had been awarded the Crafoord Prize in biosciences by the Royal Swedish Academy of Sciences, a great honor. The ceremonies in Stockholm and Lund lasted four memorable days— the Swedes really know how to run these events. The editor of the journal Ambio, Bo Söderström, asked me whether I would like to write a short piece for the journal about something related to my research. Ambio specializes in articles on environmental sciences, and I decided to write about habitat conservation. I came up with a rule of thumb that I call the third-of-third rule. Consider a political decision to protect 10% of forests or other landcovering habitat type in a country or some other large region. This is not unrealistic— in the United Nations biodiversity summit in Nagoya in 2010,

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delegates from more than 190 countries agreed to increase the percentage of protected areas to 17% on land and to 10% in coastal and marine areas by 2020. The 17% target includes all protected areas, old and new, with different levels of protection, and of any habitat type. In any case, this target is ambitious and welcome, and if properly implemented, it would be a huge step toward advancing the protection of biodiversity. The problem, which is seldom if ever mentioned in political speeches, is that a very large fraction of the old and most likely of the new protected areas is located at high latitudes, at high altitudes on mountains, and generally in marginal, low-productivity areas, which have limited value for humans and biodiversity alike. This conflicts with the letter of the Nagoya agreement, to protect “especially areas of particular importance for biodiversity and ecosystem services, . . . ecologically representative and well-connected systems of protected areas . . . integrated into the wider landscapes” (Convention on Biological Diversity 2010). For the purpose of my argument, I stick here to the round number of 10% protected areas, and I assume that the habitat is forest. Importantly, I also assume that the 10% represents all forests, across the entire planning area, including productive forest lands. The same argument applies to other land-covering habitat types that are common across large areas. The 10% target is not a magical number; a larger value would be better for biodiversity conservation, but 10% would be very good if implemented in the way that I describe below. The question is how we achieve the target of 10% protected habitat. One option is to rely on national parks and other protected areas to save 10% in large pieces of land, which is how nature protection is organized in many countries today. The current network of protected areas could be expanded to 10%. The advantage is that problems of habitat fragmentation are minimized, and management and administration are straightforward to organize. But the drawback is that the protected areas are mostly located in regions with unproductive soils and severe climate. In these areas human population density and competition with other forms of land use are low, but there is little biodiversity to protect. For instance, in Finland, with the largest remaining percentage forest cover in Europe (72%), 13% of all forested land is protected at least to some extent, but 90% of the protected areas are located north of latitude 66° north, and a large fraction of the northern “forests” are not really forests at all. In southern Finland, only 2.3% of the forests are protected, and considering only productive forest land, where the annual increment of biomass is more than one cubic meter per hectare, the figure is even

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smaller, 1.9% (Peltola 2014). The problem is that there are no large areas of unused land with high productivity and biodiversity. In such regions, only fragments of natural and semi-natural habitat are left, typically in pieces of less than 100 hectares. The second approach to implementing the conservation target is to manage the entire country or management area uniformly, and to protect 10% of the land area in small fragments that are available. What would be the result? Look again at the example in figure 5.4B from the Atlantic forest region in Brazil, which shows the occurrence of forest species of small mammals in large landscapes with dissimilar amounts of remnant forest. The results suggest that most species have an extinction threshold somewhere between 10% and 30% forest cover. In other words, many species occur in landscapes with 30% or more forest out of the total area, but just a single species was present in the landscape with only 10% of forests left. Similar results have been reported in other studies. Assuming that these results are representative, conserving forests so that 10% of the land is protected throughout the landscape would lead to a dismal result— only a small number of species would persist; most species would go extinct. The third approach to implementing the conservation target is a simple way of avoiding such an unfortunate outcome without committing more land to conservation— the third-of-third rule. First, let us assign one-third of the entire country (or large management area) to regions called conservation landscapes. Conservation landscapes are distributed relatively evenly across the entire planning area, including the more productive lands. Second, let us protect 30% of the land in each conservation landscape. Because all protected areas are in the conservation landscapes, within one-third of the total area, overall the level of protection is within the limits set by the political decision: 2/3 × 0% + 1/3 × 30% equals 10% as an average for the entire country. The important point is that many species have their extinction thresholds below 30%; hence they can be expected to persist in conservation landscapes with 30% forest cover. Concentrating protected habitat within conservation landscapes reduces fragmentation and helps many species survive. For this to happen, an essential requirement is individual conservation landscapes large enough to support large populations that are not threatened by random environmental variation or by inbreeding. In practice, considering forest-inhabiting birds and mammals, conservation landscapes should be of the order of 100 square kilometers or larger, and the number of habitat fragments within each landscape should be around 100 or fewer.

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Assuming these figures, the average size of individual fragments would be approximately 30 hectares. In practice there is always variation in fragment areas. In the case of forest mammals and birds, I would set the minimum area for individual fragments at 10 hectares, while many fragments would be greater than 100 hectares. In any case, all fragments within conservation landscapes are likely to be well connected to each other. Finally, it is important to understand that the application of the third-of-third rule, or any other approach to habitat conservation, should not be applied blindly. Large regions always have particular places with exceptional value for biodiversity conservation that should be protected in any case, regardless of whether they are located within conservation landscapes (one-third of the entire region) or outside them. There are several advantages to the third-of-third rule for habitat conservation. First, this approach is cost effective, presenting a large benefit for the effort and cost. The second advantage is practical: there are opportunities to establish conservation landscapes in regions and countries where there would be no opportunity to establish conventional national parks or other large protected areas that would exclude humans. As the aim is to establish conservation landscapes that are spaced relatively evenly across the country, most conservation landscapes are inhabited by people. Often not enough high-quality habitat is present. But one has to start working with what is available, and have a long planning horizon; often it would be possible to restore degraded habitats. The third advantage addresses the longterm challenge that changing environmental conditions present for conventional national parks and other large protected areas. Researchers have repeatedly called for increased large-scale connectivity of protected areas to allow species to move across landscapes (Heller and Zavaleta 2009). If a third of the land area were covered by conservation landscapes, they would compose a large-scale network with neighboring conservation landscapes sufficiently well connected to provide opportunities for large-scale movements. A disadvantage of conventional national parks and large protected areas is that they largely separate biodiversity and people. A fourth benefit of conservation landscapes is that biodiversity and people coexist, and the distance to the nearest conservation landscape is not great for people who live outside a conservation landscape. Ecosystem services provided by biodiversity and natural habitats, including climate mitigation especially in the tropics (DeFries and Rosenzweig 2010) and various health benefits everywhere (chapter 6), bring direct gains to local communities and to society at

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large (Ostrom 1990). People living in conservation landscapes would have new livelihoods that do not degrade the habitat; for instance, natural products could be collected in a non-industrial manner and outdoor sports and nature tourism would provide jobs. Well-managed low-level selective logging in otherwise protected forests would provide high-quality timber for the furniture industry and other products with high added value. The third-of-third rule represents a compromise in the ongoing debate about the way biodiversity should be protected (Fischer et  al. 2014). At the landscape level, there is variation in the intensity of agriculture, forestry, housing development, and so forth. The more intensive the land use for these purposes, the less opportunity there is for preserving biodiversity in the same area. But intensive land use takes less land to produce a given amount of commodity than less intensive land use; hence the more intensive land use would make more land potentially available for other uses, such as protecting biodiversity. Based on such reasoning, one may ask which one is better for biodiversity conservation, land sharing or land sparing— in other words, extensive land use that accommodates both the production of the required commodity and biodiversity in the same area, or the separation of commodity production and biodiversity conservation in separate areas (Fischer et al. 2014). The latter is the current model in developed countries with industrial farming and national parks; the former is closer to reality in many developing countries with small family farms. The third-of-third rule is a compromise: it represents land sharing at the level of conservation landscapes and larger spatial scales, and land sparing in the sense that 30% of conservation landscapes comprise protected habitat fragments. The third-of-third rule is a theoretically sound way of conserving habitat in fragmented landscapes in a cost-effective manner. Admittedly, there are challenges in implementing such an approach. The greatest challenge is simply cultural inertia among politicians, which hinders substantial change. However, societies may be changing in this respect; one great example is the development of the energy sector in Germany. To implement the third-ofthird approach, the exact proportions are not critical; it is not essential that the conservation landscapes cover exactly one-third of the total area, nor that within conservation landscapes, exactly 30% of the habitat is protected; it is essential that the total area of protected habitat reaches the target, which I have here assumed to be 10% of the total land area. What is also essential is substantial concentration of the protected habitat, to make sure that many species can occur above their extinction thresholds. Real landscapes always

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have limitations concerning land use, and any ideal spatial configuration of the protected habitat cannot be attained. Another potential problem is that conservation landscapes are more difficult to govern and manage than conventional unbroken protected areas, which are separated from human activity and are often far from where most people live. Conservation landscapes are potentially more vulnerable to habitat degradation, poaching, and other disruptions, including roadkill of vertebrates. The solution is gradual evolution of management practices and administration that favor biodiversity rather than degrade it, which requires institutions that support alertness, adaptation, and control (Primmer and Karppinen 2010). Local communities are more likely to have an interest in conserving nature when it supports their livelihoods (Ostrom 1990), which is the key consideration for people living in conservation landscapes. The bottom line is that, however habitat is protected, we cannot afford to manage protected areas the way they have been managed in the past. At the global scale, the root causes of most problems are poverty and corruption combined with human overpopulation. Without solving poverty, corruption, and overpopulation, there is little hope for anything else. Large-scale habitat conservation cannot be designed or implemented in isolation from other forms of land use. Messages 1. The Glanville fritillary in the Åland Islands is a biological model system for population studies of the ecological, genetic, and evolutionary consequences of habitat fragmentation. The large body of information that has been accumulated for this study system allows researchers to address questions that otherwise would be difficult to tackle. The Glanville fritillary highlights the value of biological model systems beyond molecular biology. 2. Networks of local populations are called metapopulations. They persist in fragmented landscapes in a balance between local extinctions and establishment of new populations by females dispersing into currently unoccupied habitat patches. Increasing habitat fragmentation consists of decreasing fragment area and increasing isolation, which increases extinction rate and decreases colonization rate. Extinction threshold defines the limit below which extinctions always exceed colonizations and the metapopulation goes extinct. Extinction debt is the number of species in a community that are below their extinction thresholds and hence doomed to extinction,

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but they persist temporarily because it takes time for populations to adjust to the altered environment. 3. Habitat loss is typically accompanied by increasing fragmentation; hence it is not easy to tease apart the independent effects of the loss of pooled habitat area and fragmentation. Empirical and theoretical studies show that fragmentation matters when the total amount of habitat across the landscape is small. The 20% rule suggests that fragmentation matters when less than 20% of forests or other land-covering habitat is left. 4. The current amount of forest on Earth is approximately 40 million square kilometers, which amounts to around 25% of the land area on Earth, and is roughly half of what it used to be 10,000 years ago. At present, forests are lost globally at the rate of 0.5% per year, but there is much variation in different parts of the world. The effective area of forests for many forestinhabiting species is reduced by three factors: fragmentation, which may take a forested landscape below the extinction threshold of many species; great simplification of forest structure and loss of microhabitats in intensively managed forests and in plantations; and defaunation, loss of largebodied species due to excessive hunting and poaching. 5. If the amount of habitat that can be protected across a large area is so low that most species would be below their extinction thresholds if the protected habitat is distributed rather evenly, it would be wise to concentrate the protected habitat within about one-third of the total area. Within this one-third of the total area, one-third of the area would be protected, which is enough to maintain most species above their extinction thresholds. This is the third-of-third rule.

6

Why Is Biodiversity Important?

Island Area Maximum elevation Age Time since isolation Current isolation Inhabitants Breeding birds Endemic birds Butterflies Flowering plants

Greenland 2,166,086 square kilometers 3,693 meters More than 3.5 billion years 54–55 million years from Europe 1,000 kilometers from Europe; narrow strait to Ellesmere Island (North America) 56,900 60 species None 5 species 500 species

In the Steps of Charles Elton

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he small airplane approached the shore of King Oscar Fjord on Traill Island in east Greenland. Flat tundra behind the seawall was the runway; the airport facilities consisted of a red stick where the plane should stop, if not before. Among the people waving at us, I recognized Benoît Sittler. The landing was surprisingly smooth, and I was soon greeting Benoît and his companions (figure 6.1). The travel time from Iceland had been four hours. The sun was shining; the temperature was around 10 degrees Celsius on July 13, 1996. The plane took off with those who were leaving; we stayed be187

Fig. 6.1 On Traill Island in east Greenland in July 1996. (Photos courtesy of Oliver Gilg and Groupe de Recherches en Ecologie Arctique.)

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hind, 250 kilometers from the nearest village, Ittoqqortoormiit, with a few hundred inhabitants. Not many people live in east Greenland. The village of Tasiilak, with some thousands of people, is 850 kilometers from Ittoqqortoormiit, and there are a few small stations for the border patrol, meteorologists, and researchers. Benoît’s station consisted of a tiny wooden hut that had been used by trappers decades ago, and a set of tents for us to sleep in. Some years ago the tents had been surrounded by a rope on fence posts, connected to an alarm system that was supposed to warn researchers about approaching polar bears. Benoît said that this practice was discontinued when people who ventured out for a pee at night heard guns being loaded inside the other tents. We were located at latitude 72.5° north, at the edge of the world’s largest national park. The Northeast Greenland National Park was established in 1974, and it currently protects nearly 1 million square kilometers of ice, along with a narrow belt of tundra on the coast. It has been cheap to protect this land in the past; let us hope that protection continues when climate change inevitably changes the environment. The Northeast Greenland National Park accounts for a substantial fraction of all strictly protected land areas in the world. I noticed insects flying close to the ground. They have no need to fly high up above the Arctic tundra, because no vegetation blocks their route; the tallest willow bushes grow to the height of a few centimeters. Moreover, it pays to stay in the warm layer of air close to the ground, because insects flying higher up would quickly cool and be forced to land to warm up their flight muscles. My old habit of searching for butterflies was rewarded by four species in the first hour: the northern clouded yellow (Colias hecla), two fritillaries (Clossiana polaris and C. chariclea), and the arctic blue (Agriades glandon). After returning home, I found that I had missed just one other species, the small copper (Lycaena phlaeas), which is familiar to me from my boyhood and a species that can hardly be called an Arctic butterfly; it is widely distributed in Asia, Europe, North Africa, and North America. The first four are true Arctic species, though none is endemic to Greenland. Thinking of variation in biodiversity across the globe, it is unbelievable that one can find four out of the five species of butterflies that occur in Greenland in just one hour, in one small place. In comparison, Borneo has nearly 1,000 species of butterflies, and experience shows that it would take years and massive effort to see even half these species in the wild, so many of them are rare and confined to small parts of Borneo. This comparison reflects the general trend of increasing biodiversity from the Arctic to the

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Fig. 6.2 The dynamics of the collared lemming (Dicrostonyx groenlandicus) on Traill Island in east Greenland from 1988 to 2015. (Unpublished data from Benoît Sittler and Olivier Gilg.)

tropics (chapter 1). Another north-south trend that is often mentioned but that is not well understood is low stability of Arctic and temperate populations in comparison with tropical populations. I had been thinking of population stability during the flight from Iceland to Greenland, particularly the stability of mammalian populations, which my colleague Benoît Sittler and our student Olivier Gilg were studying on Traill Island. Benoît had started in 1988, and the study is still going on. The long-term record for the collared lemming (Dicrostonyx groenlandi­ cus) shows a most amazing pattern (figure 6.2). I was in Greenland to witness unstable Arctic populations, and I saw this in the lemming populations, which were in the low phase in 1996. This was expected, based on the results for the previous years, but nobody could have guessed in 1996 that the regular four-year population cycle that had been observed for the past ten years would completely and abruptly disappear after 2000 (though perhaps the minor peak in 2011–13 in figure 6.2 indicates yet another change in the dynamics). The regular cyclic dynamics of lemming populations were first described scientifically in 1924 by Charles Elton, a young zoologist from Oxford, who established the field of population ecology by his 1927 book Animal Ecology. On Traill Island, I was following in the steps of

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Charles Elton. What is particularly surprising about the drastic change in lemming dynamics is where it occurred— in the world’s largest national park, in Greenland. There is no way that any direct human influence could be responsible for this change. (I do not remember if I was thinking, in 1996, whether climate change could affect lemming population cycles.) When ecologists talk about the stability of populations and communities, they usually mean numerical stability: how much population size fluctuates over time. The collared lemming population was very unstable before the year 2000, though in a specific way, displaying high-amplitude, regular fluctuations. In contrast, the population was quite stable, though with low abundance, after 2000 (figure 6.2). High stability of populations typically means that their risk of extinction is low. A related concept is resilience, which applies not only to animal and plant populations but also to human-created systems. High resilience means capacity to resist change after disturbance, and capacity to return to the original state if a disturbance caused a change in the state of the system. How biodiversity relates to stability and resilience is one of the classic and arguably most important questions in ecology. For the past 100 years, the common opinion has been that more diverse communities and ecosystems are more stable than less diverse communities, though we now know that it is not necessarily biodiversity as such, but also the kind of biodiversity, that promotes stability. I return to this subject below. One can also ask whether the reverse causality might hold. Perhaps butterfly populations in Greenland are generally unstable because of environmental vagaries, for instance, because every now and then the summer is so disastrous that reproduction fails. On the time scale of millennia, species may have a substantial risk of going extinct from the entire country. If the rate of colonization of Greenland by new species from outside is very low, the depauperate fauna of Greenland could reflect the great instability of populations, rather than low stability reflecting low biodiversity. My observations on butterflies support this idea: four out of the five butterfly species occur very widely, which reduces their risk of extinction from Greenland as a whole; only the most widely distributed and potentially most abundant species are likely to survive in the long run. I was visiting Greenland to become familiar with the lemming project in the field and thereby become a better supervisor of Olivier’s thesis work. Because of the timing of my visit, I saw just a single lemming in two weeks. Had I been there in 1990, 1994, or 1998, I would have seen dozens of lemmings. If you do not count zero, Greenland has the smallest possible diversity of

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small mammals, just the collared lemming, a single species. There are four predator species, but even this community of predators is so simple that it is hard to find a simpler community of predatory vertebrates anywhere in the world. The predators are the snowy owl (Bubo scandiacus), the long-tailed skua (Stercorarius longicaudus), the arctic fox (Vulpes lagopus), and the stoat (Mustela erminea), which all devour lemmings when they are abundant. When lemming populations are in the low phase, the different predators do different things. The snowy owl is a true lemming specialist and a nomad. If the density of lemmings in the spring is less than two lemmings per hectare, the snowy owls apparently decide that the situation is hopeless; they do not settle down to breed but instead fly elsewhere, even thousands of kilometers away. In the right place at the right time, the density of breeding pairs can be high, and females lay large clutches, and why not? When lemmings reach their peak density, there is overabundant food for everybody. A pair of arctic foxes may also raise a large litter, more than ten kits, but when lemmings are scarce, the foxes cannot fly away. They just wander around looking for whatever might keep them alive, such as carcasses left behind by polar bears, or the remains of a musk ox that died for some other reason. I saw a few arctic foxes, one from very close quarters when it came to our camp and took a piece of cheese from my hand. I saw more of the long-tailed skuas, though they did not breed either. The long-tailed skuas have an amazing life history: if there are no lemmings and they cannot start breeding, they become vegetarians, feeding on berries in the summer, until they return to the South Atlantic to winter in the open ocean. The snowy owl, the arctic fox, and the long-tailed skua thus have very different ways of coping with years of low lemming density, and their impact on the lemming populations become apparent only at high prey density. Olivier’s results suggested that with increasing lemming density, mortality inflicted by these predators can be so high that they will stop the growth of the lemming population, before lemmings can exhaust their food resources (Gilg et al. 2006). But what about the stoat, the smallest and most difficult of the four predators to observe? I knew the stoat from my own research: it is a smallrodent specialist all over the circumpolar region, in Asia, North America, and Europe. It has an elongated body, an obvious advantage that allows it to hunt small mammals in their tunnels. Benoît has estimated the relative abundances of stoats and lemmings in each year within a large study area of 15 square kilometers, in the valley where the camp is located (figure 6.1).

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The study is based on counting, with his assistants, the lemming winter nests after snow melt in early summer. This is a huge undertaking, but Benoît explained that with a smaller study area, the sample size would be too small in years of low lemming abundance. Besides, as I soon realized, lemming winter nests are not difficult to spot. Lemmings reproduce throughout the winter, feeding on grasses, sedges, and twigs of willow, and construct their nests made of hay and other vegetation in snowbanks. When the snow melts, all the nests descend to the ground, where they are much taller than the vegetation and hence easy to see from some distance. The stoat hunts in the network of lemming tunnels in snow and takes over a fraction of lemming nests for its own use. These nests are easy to tell apart from the others, because the stoat uses the skin and the underfur of its prey to line the nest chamber. In Greenland, there is little alternative prey for the stoat, and because the stoat cannot travel long distances, it has to continue hunting lemmings however low their density. This is the key to the cyclic dynamics: stoats depress the lemming density to an exceedingly low level, and continue to do so until their own numbers have dwindled to almost nothing. Benoît’s results showed that stoat density lagged behind the lemming density by one year. Theory says that such delayed density-dependent predation has a destabilizing effect and may lead to cyclic population dynamics. When the stoat numbers have finally dropped to a sufficiently low level, the window opens up for the lemmings to increase rapidly— until there are so many lemmings that the other predators start breeding and stop the lemming population increase. Olivier Gilg worked out in great detail the responses of the predators to changing lemming numbers, and these results allowed us to construct a model that to our delight reproduced well the observed dynamics (Gilg et al. 2003). The model was helpful in clarifying the possible causes of the dramatic change that occurred in the dynamics in 2000, four years after my visit (figure 6.2). The most important conclusion was that though the change in dynamics is indeed dramatic, it does not mean that a dramatic change in the environment, or in one of the species in the community, had occurred. The system of five species— the collared lemming and the four predators— is actually complex enough to yield highly complex dynamics that depend on both direct and indirect interactions among the species. Modeling studies have shown that such systems can have alternative states, and a slight change in some model parameter—for instance, in the prey growth rate—can push the system into very different dynamics, where it may stay for a shorter or

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longer period. What could have triggered such a change? The obvious candidate is climate warming, which has progressed quickly in the Arctic area, including Benoît’s study area. The onset of the snow-free period has advanced, from around July 5 in the 1980s to the beginning of June in recent years; and while the snow-free period varied between 50 and 100 days from the 1960s to 1980, it has been much longer, 150 to 200 days, since 2000. Unfortunately, it is hard to pinpoint exactly which effect of climate warming on the species makes the biggest difference. Is it the earlier breeding season in summer, or the increasing frequency of frost-melt events, which may hit lemmings hard? With models, one can explore different possibilities, and we found that a likely consequence of climate warming is what has happened in reality, reduction in lemming peak density and increase in cycle length, or the disappearance of cycles altogether (Gilg et al. 2009). The repercussions for the predators are very significant. In the absence of years with high lemming abundance, the snowy owl has practically disappeared from the area, and the stoat has declined to a low level. After my trip to Greenland, my former student Tomas Roslin started an ambitious project to describe the entire community of insects in east Greenland. Later Helena Wirta, another former student, joined Tomas, and they now have a good idea of how many species there are in their study area: 163 species of plants and approximately 500 species of animals, mostly insects (Wirta et al. 2014). Tomas and Helena have been especially interested in working out which species interact with each other, and they have singled out the 20 species of butterflies and moths and the 30 species of wasps parasitizing them for a special study. It is possible to rear caterpillars to find out which parasitic wasps use which species of butterflies and moths as their hosts. The drawback of this method is that it takes a huge amount of time and work. They have hence complemented the rearing studies with another approach based on DNA barcoding (this method was discussed in chapter 1). They sequence a short string of DNA that is known to vary among species but not much among individuals of the same species. They extract DNA from the gut contents of the adult wasps. While the individual has undergone a full metamorphosis, its bowels are still intact, and a tiny amount of host DNA may remain in them. Using the DNA barcode, the researcher can then find out which host species the wasp actually fed on as a larva. In a similar manner, a parasitized moth larva contains DNA of its attacker. Using the known DNA barcodes for the different parasitoid species, one can find out who is devouring the larva from inside— without rearing the parasit-

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oid to adulthood. This may sound like science fiction, but it works often enough to provide useful data. The results revealed three times more links between pairs of species than had been established by traditional methods (Wirta et  al. 2014). Finding the links is a prerequisite for many further analyses. Charles Elton, in his Animal Ecology (1927), sketched many new concepts, principles, and research tasks for ecologists, one of which is the concept of a food chain. In 100 years, ecologists have made much progress, but the web of interactions among the hundreds or even thousands of species that occur in a single community remains a huge challenge. And identifying the interactions is just the beginning. To understand the dynamics of communities, one needs to learn much more about the interactions apart from just whether they exist or not, something along the lines that Benoît and his colleagues have done for the collared lemming and its predators. But there are hundreds of species, many cryptic and very small, which makes it hard to do any fieldwork or experiments. Ecologists can never have sufficient knowledge about all the species to construct predictive models that include species-specific information. The hope is that research on well-studied species and communities will lead to generalizations and theories that help resolve questions about biodiversity. One such question is whether the number of species in a community influences the stability of the community. Biodiversity Increases Ecosystem Stability—or Does It? Why should communities and ecosystems with many species be more stable than communities and ecosystems with only a few species? Traditionally, ecologists thought that if herbivorous animals have many alternative host plant species, or if predators have a choice among many prey species, their populations are buffered against changes in any particular host or prey species— if the availability of one prey species declines, there are others that can be used instead. Conversely, if there are no alternative prey species, the predator population necessarily fluctuates in response to changes in population size of the prey species. The collared lemming and its predators in Greenland are an example; all four predator species suffer during the low phase of the lemming cycle. Charles Elton (figure 6.3) was the first to emphasize the linkage between diversity and stability when he suggested that “simple communities were more easily upset than . . . richer ones; that is, more subject to destructive oscillations in populations, and more vulnerable

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Fig. 6.3 Charles Elton (1900–1991; middle) and Robert MacArthur (1930–72; right) were the leading ecologists of their times. They proposed that diverse communities are generally more stable than less diverse communities, which became the prevailing opinion until the 1970s. Theoretical ecologist Robert May (1936–; left) showed with mathematical models that diversity as such is not expected to increase stability. See the text for a discussion about diversity and stability. (Drawing by Jose Luis Ordoñez, in J. Piñol and J. Martinez-Vilalta, Ecología con números [Bellaterra, Spain: Lynx Edicions]; reprinted with permission.)

to invasions.” (Elton 1958, 145). The question whether simple communities are also more vulnerable than diverse communities to invasion by new species has been much debated, for instance, when contemplating why there are so many invasive plant species on species-poor oceanic islands (chapter 4). Over the years, many have thought that this is self-evident— just consider pest problems in agricultural fields and other monocultures— but the evidence is actually not so clear-cut. We now know that the numerical stability of populations is affected by many features of species’ interactions, not just whether there is an interaction. For instance, time delays generally have a destabilizing effect, and how fast per capita predation rate increases with increasing prey population size makes a big difference. The theory that diversity begets stability was the reigning paradigm in ecology until the 1970s. The challenge came from Robert May, a physicist who moved from Australia to Princeton University in the United States, and switched from physics to theoretical ecology (figure 6.3). May inherited the chair of Robert MacArthur, the researcher who formulated the equilibrium

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theory of island biogeography with Edward O. Wilson (chapter 5) and launched many new lines of investigation on questions that had previously lacked theoretical foundation. MacArthur died of cancer at the age of fortytwo, in 1972. In the following year, May published a book that established his leadership in theoretical ecology, Stability and Complexity in Model Eco­ systems (1973). The message was loud and clear: diversity as such does not increase stability; more likely it has just the opposite effect. This was surprising news to ecologists, and it took a long time to digest the importance of this work, even perhaps for May himself. In hindsight, the disagreement between May’s theory and previous thinking was not as great as it first appeared, but because there was no previous theory, it was not immediately evident what was at stake. May developed his argument in very general terms, as a general theory should be constructed. He defined stability as follows: Assume that there are initially m species in the community, before the species have influenced each other’s dynamics and abundance. Then “turn on” the interactions among the species, as specified below. If all species persist and settle down to a positive equilibrium abundance, the community is considered to be stable; if one or more species goes extinct, the community is unstable. Given that there are initially m species, there are (m × m)/2 − m pairs of species, and May assumed that the two species in each pair would interact with each other with probability C. Interaction means that one species either increases or decreases the growth rate of the other species. Finally, the average strength of interaction, if there is interaction, is given by parameter s, while the actual strength with which one species affects the other one is drawn from a normal distribution with zero mean and variance s2. May showed mathematically that the community is almost certainly unstable if s√m ⎯‾ C > 1.

It is always pleasing, and beautiful, to have a simple result for a complex problem, and the above result certainly is a good example. In words, the community is more likely to be unstable if it has many species, if many species interact with one another, and if the average strength of interaction is large. It seemed impossible to square such a clear-cut result with the old conjecture that diversity (species richness, m) increases stability. However, an important feature of May’s model did not get enough attention in the beginning: May analyzed random communities, random in the sense that

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those species that influence each other are randomly selected. This assumption was made to facilitate the mathematical analysis. In reality, however, randomness is not a feature of natural communities; on the contrary, there are systematic differences between the species, starting from the fact that prey and predator species interact differently with each other. Real communities have a long and complex history of assembly behind them, which is another reason for a nonrandom pattern of interactions among the species. It is not obvious that this difference between the model and real communities will change May’s conclusion, but neither can one be sure that it will not. When researchers have used more realistic assumptions about food web structure, and have assumed realistically that the distribution of interaction strengths is skewed with overabundance of weak interactions, the resulting communities tend to be more stable than random communities. However, the problem with nonrandom communities is that there is not just one such community: there are many different kinds of nonrandom communities. This variety makes it difficult to arrive at general conclusions comparable to May’s classic result for random communities. The lasting value of May’s work is that his results forced ecologists to think more deeply and more systematically about diversity and stability. In the past twenty years, hundreds of ecologists have conducted experiments, mostly on plant communities, to investigate the relationships between biodiversity, productivity, and stability. In a typical experiment, researchers manipulate biodiversity by seeding study plots with different numbers of species selected randomly from a large pool of species. Thus, by design, the study plots differ from each other only in terms of how many species they have. Moreover, there are several replicate plots with the same number of species, but with different mixtures of species, which allows the researcher to tease apart the effects of particular plant species from the effect of species richness as such. The general conclusion that has emerged from these studies is that high-diversity experimental plots have approximately twice as much biomass production as single-species plots (Tilman et  al. 2014). Higher productivity of high-diversity communities has many causes, including complementarity between the species (different species use resources in somewhat different ways), reduced levels of herbivory and disease (particular herbivores and disease agents do not attack all plant species), and feedback that increases nutrient storage and supply over longer periods of time, especially in species-rich communities. Indeed, long-term experiments show that the effects of diversity on biomass production increase with

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time, most likely because diversity-dependent ecosystem feedbacks and the effects of interspecific complementarity accumulate over time (Reich et al. 2012). This is an important finding: loss of species leads to gradual deterioration of ecosystem processes, and short-term experiments do not reveal the full consequences of biodiversity loss on the functioning of complex ecosystems. This result is similar to extinction debt, which was explained in chapter 5: habitat loss leaves many species with nonviable populations in the altered environment, but it takes time before all these species go extinct. They decline gradually to extinction, unless the quality of their habitat improves. These results indicate that not just the loss of some key species, but loss of biodiversity as such has detrimental consequences. It is not obvious that this should be so, because species have clear ecological differences that influence ecosystem processes. So is it really true that most species nonetheless have measurable consequences for ecosystem functioning? Isbell and colleagues (2011) have examined this question with the results of seventeen different experiments involving altogether 147 grassland plant species. They found that only a few species influenced ecosystem functions—for instance, biomass production and nutrient uptake—in short-term experiments. However, considering the results of all seventeen experiments, run under different environmental conditions, most species showed a significant effect at least once. In brief, at any one time and in any one place, the effects of a few species dominate, but most species have measurable effects in some years and in some places, under some environmental conditions. Here is another important message: We should not rush to conclude that some species are “insignificant” based on limited observations, especially not in a world where conditions are rapidly changing with climate warming and other human-caused environmental changes. This conclusion brings back a fond memory. When I started my PhD studies in Oxford in 1976, I had the honor of having Charles Elton attend my seminar in the first year. I talked about the species-rich community of dung beetles, and about my results and thoughts about the processes that influence the structure of this community. After I had finished my presentation, Elton asked an unexpected question: Could I name which species in the community have the greatest significance? I could not name the most, or the least, significant species. Elton appeared to be pleased by this response. Species richness increases productivity of plant communities, and probably of many other communities that are less well studied. But what about stability? Does stability decrease with increasing species richness, as the

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theory developed by May suggested? To start with, we have to make a distinction between the numerical stability and extinction proneness of individual species, which May’s theory is about, and the stability of productivity and other ecosystem functions, which most experiments have addressed. This distinction is important, because it is quite possible that communities that are stable in terms of productivity of all the species put together could nonetheless consist of species populations that fluctuate greatly, but not in synchrony, in which case the community as a whole could remain relatively stable. Comprehensive long-term experiments on plant communities conducted over the past twenty years at Cedar Creek Ecosystem Science Reserve in Minnesota support this conclusion: stability of productivity increases with species richness, but stability of population sizes of individual species is lower when diversity is high (Tilman et al. 2014). Importantly, the Cedar Creek data and data from other experiments have demonstrated that manipulations of the various factors that affect plant productivity—such as soil nitrogen, carbon dioxide, fire, herbivory, and water availability—influence community stability to the extent that the manipulations affect biodiversity, and these effects are comparable to the effects discovered in experiments in which biodiversity itself was manipulated (Hautier et al. 2015). The lesson is that the level of biodiversity really matters— more diverse communities show greater ecosystem stability. This conclusion is essentially the original proposition of Charles Elton and Robert MacArthur, though seemingly opposite to what Robert May found. Have researchers wasted their time and spent much effort on misguided ideas? No, because challenging what once appeared a self-evident truth forced researchers to perform carefully controlled experiments, and to explore the mechanistic causes of the diversity-stability relationship. Thereby it was discovered that stability at the community level can increase while stability at the species level decreases with increasing diversity. It is also evident that natural communities are not random assemblages of species; both ecological and evolutionary processes have influenced their composition— the populations and species that do not “fit” well into the community have a good chance of being weeded out. Ecosystem Services and Nature-Based Solutions The Neethlingshof Wine Estate in the heart of the Stellenbosch wine lands in Western Cape, South Africa, had a pest problem. Large numbers of small

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mammals gnawed the roots of grapevines and riddled the ground with tunnels. Poisons were used, but this inevitably polluted the wine. The way out was based on solid biology, though I do not know how the estate management arrived at the solution: erect tall posts for owls all over the vineyard, from which the birds like to swoop on their prey. This worked, and the numbers of small mammals decreased to a level where damage and economic losses were not an issue. Equally important for the estate, the solution initiated a loop of positive feedbacks. Neethlingshof Wine Estate linked the narrative of the return of the owls to wine marketing by naming a singlevineyard pinotage the Owl Post pinotage, apparently with good effects. The flagship Bordeaux blend of the estate, Laurentius, is now called the Caracal, after a beautiful local wild cat, Caracal caracal, which is making a comeback. Caracals used to be common until the middle of the last century, when their numbers crashed because of habitat loss. The estate is now protecting part of their land, and the caracal is benefiting from the restored wooded areas. In collaboration with World Wildlife Fund South Africa, Neethlingshof and other wine estates are involved in the Biodiversity and Wine Initiative, with the aim of contributing to the conservation of the unique Cape flora and fauna. Over 140,000 hectares of land have been conserved since the project started, which is more than the current total area of vineyards, and a commitment has been made to protect an additional hectare of natural vegetation for every new hectare under vineyards. These measures have encouraged tourism in the area; not only have the numbers of wine enthusiasts increased, there are also more bird-watchers and others interested in nature. Overall, the story appears too good to be true— everybody benefits, nature included. Nature was part of the initial problem (small-mammal pests) and its solution (owls), but what happened afterward shows close integration of economic development and the well-being of both humans and nature. British conservation biologist Georgina Mace (2014) has summarized changing views on nature and nature conservation in four main ways of framing conservation. Before the 1970s, the prevailing view was “nature for itself,” and the emphasis was on wilderness areas and intact nature, without people. The emphasis was on species. This perspective shifted in the late 1970s and the 1980s toward populations, and a more mechanistic understanding of their dynamics, reflecting the birth of modern conservation biology and advancing theories of sustainable harvesting. The new framing of conservation can be characterized as “nature despite people,” how populations and species survive in the human-dominated world. Conservation

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questions addressed minimum viable population size, and how much habitat should be protected and in what way (figure 5.5 dates to this period). The latter questions remain highly relevant today: habitat loss and fragmentation have been and still are the main causes of declining biodiversity, and whatever the framing of conservation, habitat protection is absolutely essential if we want to stop the decline of biodiversity (chapter 5). By the late 1990s, the emphasis in conservation moved from species and populations to ecosystems and ecosystem functions: nature provides societies crucial benefits that are irreplaceable. Ignoring nature and allowing ecosystem functions to deteriorate leads to economic losses and, ultimately, to something that can only be described as an ecocatastrophe. The parlance of ecosystem services and natural capital are part of this view about nature, and the perspective is “nature for people.” Finally, Mace’s fourth and most recent viewpoint about conservation can be labeled “nature and people.” The key ideas include socioecological systems, continuous environmental change, resilience, and adaptability. The term ecosystem services became widely used in media in 2006, following the Millennium Ecosystem Assessment (2005), a massive effort by more than a thousand researchers and other contributors to assess the effects of human activity on the environment. In the Millennium Ecosystem Assessment, ecosystem services were defined as the benefits people obtain from ecosystems. The idea itself is of course not new— people have always understood their dependence on natural resources— but what is less obvious is the many ways that our well-being depends on natural populations, communities, and ecosystems, and the long-term harm that environmental degradation does. Four kinds of services have been identified: supporting, provisioning, regulating, and cultural. Supporting services are necessary for the production of all other ecosystem services, including nutrient cycling, primary production, and soil formation. Provisioning services include all the products that can be obtained from ecosystems, including raw materials, food, and water (figure 6.4). Regulating services are benefits that are obtained by ecosystem processes such as purification of water and air, pest control, carbon sequestration, and waste decomposition. Finally, cultural services are nonmaterial benefits, including recreational experiences, spiritual and historical values, and the value of ecosystems for science and education. Provisioning services are easy to grasp— the use of natural resources, which have a monetary value— but the other categories are more challenging to apply and to take into account in economic decision making, with

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Fig. 6.4 Collecting natural products in forests and other ecosystems is an example of provisioning services. It represents an important cultural service to many people. My wife and I greatly enjoy picking blueberries in late summer.

some exceptions. The services that insects provide in pollinating crops are a good example. A comprehensive analysis of data from 200 countries found that fruit, vegetable, or seed production of 87 of the leading global food crops depends upon animal pollination, while the production of 28 crops does not (Klein et al. 2007). For crops that rely on wild pollinators, it is evident that agricultural intensification at large spatial scales is problematic, because less and less habitat remains for the pollinator populations to reproduce (figure 6.6, discussed in the next section). Pollination is an easy example of ecosystem services, because one can include food production and biodiversity in the same equation. Most other cases are not like that. If the focus is on provisioning services, use of natural resources, not much has been gained by using the new vocabulary; markets have known for centuries how to put a value on commodities. Though plenty of data demonstrate that biodiversity increases ecosystem productivity and stability, as I have described in this chapter, and though high productivity and stability are obviously desirable ecosystem properties, it is nonetheless hard to bring such arguments into short-term political and economic decisions. Even more difficult is dealing with many of the cultural services, including the intrinsic value of biodiversity. Many people see no intrinsic value of biodiversity, natural ecosystems, and nature, because their personal

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experience does not include any of them. The values of these citizens have been shaped by their life in urban environments. Thus the hope that many conservationists have for the concept of ecosystem services’ helping protect biodiversity may be ill founded; the entire concept could backfire, pushing us toward more intensive use of natural resources. Mace’s fourth view of nature and conservation is recent, the product of the 2010s. The other three views have not become obsolete, however; rather, the four perspectives coexist in different mixtures in different contexts. The slogan of the fourth view is nature-based solutions, and the framing of conservation is based on the notion of “people and nature” and on solving problems rather than valuing nature’s services. This viewpoint emphasizes how nature, including ecosystem processes, can be integrated into resolving practical problems. Improving wine production with biodiversity is one example. Another is addressing watershed management by including wetland conservation in waste water treatment and flood control. A really huge global problem for societies, even for humanity, is urbanization. More than half the world’s human population lives in cities, and the percentage is increasing globally. Urbanization is a major cause of biodiversity loss, for many reasons, but biodiversity is also a key component in many visions about the development of urbanization in the future. Urbanization is, of course, not only a problem but also an opportunity, a feature of civilization with problems that need to be solved. Biodiversity relates only to some aspects of urbanization, but many of these are fundamental, such as people’s health and well-being. The key term is green infrastructure: what kind of green space is needed, how much, and where. Physical variables and processes that can be affected and controlled by green infrastructure include air quality (improved by large trees) and storm-water control (unpaved areas absorb large quantities of water). Parks and other green areas are important for recreation, and they are irreplaceable as children’s playground, supporting their healthy development (Louv 2013). Unfortunately, increasingly busy schedules of families and the ever-increasing time in front of screens have reduced time spent playing outdoors. Another factor working in the same direction is parental fear, reflecting the general “culture of fear,” about the safety of children out of sight. In many cultures and societies, people use even very small areas of land that is available for food production, which increases food security in poor countries and wherever there is unrest. Bringing elements of the countryside into towns and cities is an important trend

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also in many wealthy countries, increasing the general well-being of the rapidly aging population. The examples from urban environments highlight a fundamentally important benefit that people obtain from nature, an ecosystem service par excellence: the effect of contacts with nature on our health and well-being. Living in a city greatly reduces the nature contacts of an average person; thus the benefits of even a modest increase in these contacts are the greatest in cities. The socioeconomic dimension is also important: wealthy families can spend time in natural environments during weekends and holidays, which poor urban families cannot afford. Apart from limited contacts with nature, people in cities spend more than 90% of their time inside buildings, with little physical activity. A sedentary lifestyle, both in children and adults, increases the risk of many chronic diseases, including high blood pressure, obesity, and heart disease. A Dutch study found that more green space in people’s living environment is associated with enhanced feelings of social safety (Maas et al. 2009). Another comprehensive Dutch study involving a population of 350,000 people examined whether physician-assessed morbidity was related to green space in people’s living environment. The results showed that the prevalence of fifteen out of twenty-four disease clusters was lower in living environments with more green space within a one-kilometer radius. The association was strongest for anxiety disorder and depression, and it was stronger for children and people with a lower socioeconomic status. These effects were attributed to less stress and more social cohesion for residents of greener areas, although they did not engage in more physical activity in this study (Groenewegen et al. 2012). Other studies have shown that exposure to natural environments enhances physical and mental health and cognitive functions (Bratman et al. 2012). Much research shows that visits to forests promote both physical and mental health by reducing stress (Karjalainen et al. 2010). One megatrend in developed countries and especially in urban environments over the past half a century is a rapid increase in the prevalence of non-communicable diseases, which typically have a basis in chronic inflammation and include allergic and autoimmune diseases, asthma, inflammatory bowel disease, and even certain cancers and depression. Figure 6.5B shows a striking trend in a large and representative sample, Finnish conscripts to compulsory army service. The common factor in these disorders is malfunctioning immune system. Rapidly advancing research has shown that

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Fig. 6.5 Two global megatrends in biodiversity and public health. A, three indices reflect declining biodiversity since the 1970s (LPI, Living Planet Index; WBI, World Bird Index; WPSI, Waterbird Population Status Index). The vertical axis gives the values of these indices (confidence intervals given with gray areas). B, two examples of increasing prevalence of inflammatory disorders, asthma and allergic rhinitis, among military conscripts in Finland from 1960 to 2003. The vertical axis gives the prevalence of the disorders. (After von Hertzen et al. 2011.)

normal development of the human immune function requires close crosstalk (signaling) between various human cells and the diverse microbial communities that inhabit our bodies. The worry is that urban living in built-up environments, combined with the use of processed water and food, may not provide the microbial stimulation necessary for the balanced development of the immune function. Increasingly sedentary lifestyle is another risk factor for chronic inflammatory disorders. I return to the relationship between biodiversity and non-communicable diseases below. Meanwhile, let us consider another global megatrend, the emergence of new types of ecosystems. Novel Ecosystems Agricultural systems and plantations are the ecosystems that have been most altered by humans. Does the management of these ecosystems benefit from what is known about more natural ecosystems? Ecological knowledge suggests that biodiversity helps buffer productivity and the stability of ecosystem functioning against environmental perturbations. High productivity and stability are desirable features from a human perspective, and high biodiversity provides these services for free. However, agriculture in developed countries and plantation forestry do not typically try to take advantage of

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these potential services; instead the prevailing paradigm has been to increase yields by moving in the opposite direction, to monocultures of single species. These ecosystems have no intrinsic stability at all: left on their own, they would rapidly turn into something different. High productivity and stability of modern agricultural ecosystems and plantations are achieved with great cost, by the use of fertilizers, herbicides, fungicides, irrigation, expensive machinery, and so forth. It is beyond the scope of this book to go into these matters, or to assess the feasibility and possible benefits of organic farming, for example. I understand the challenges of feeding the human population in the world, though I cannot see much sense in developing the agricultural sector to support even more people on the planet. It is also surprising that the management of agricultural ecosystems and plantations is not carefully optimized to maximize the net profit, the difference between output and input, until perhaps recently and in some regions. Often management seems to be based on the assumption that further intensification is always preferable, even if it is obvious without any calculations at all that intensification has proceeded too far. For instance, in a study comparing wind-pollinated and insect-pollinated crops in twentytwo regions in France (Deguines et al. 2014), researchers showed that agricultural intensification increased the yield of crops that do not depend on pollinators, but intensification did not increase the yield of pollinatordependent crops, apparently because the yields are limited by pollination in landscapes where intensive agriculture leaves too little habitat for the pollinator populations to reproduce (figure 6.6). In this case, it is clear that net profit for the farmer would be maximized by less intensive land use. Notice also that in the case of wind-pollinated crops, it is not obvious whether net profits are maximized; to find out, one needs to know how fast both the costs and benefits increase with intensification. Another example comes from Finnish forestry, which has become so intensive over large areas that the managed forest effectively represents boreal plantations. Over the years, forestry has become based on clear-cutting, after which a new single-species and even-aged stand is established by planting tree seedlings. Empirical studies have demonstrated that continuous-cover forestry would often be more profitable, largely because of the high cost of establishing a new cohort of trees after clear-cutting and the long time during which biomass production is minimal (Kuuluvainen et al. 2012). Nonetheless, foresters have been trained to favor the ever more intensive approach based on clear- cutting. This is unfortunate, because continuous-cover forestry achieves benefits

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of the high biomass production and stability conferred by high-diversity stands, and the adverse effect of forestry on forest biodiversity could be reduced. Agricultural ecosystems and plantations apart, alterations have taken place in most ecosystems, including those that have seemingly remained in their original state, such as well-protected national parks. Consider the Northeast Greenland National Park (figure 6.1). Climate warming has been greatest in the Arctic regions, including Greenland, where the dynamics of natural populations, otherwise completely unaffected by humans, have been disrupted (figure 6.2). Another example is ecosystem eutrophication due to nitrogen deposition, which is familiar in the case of freshwater ecosystems but occurs also in ecosystems on land. In communities and ecosystems that have developed under low-nutrient conditions, atmospheric nitrogen deposition may greatly affect community composition and interactions among species. For instance, of the more than forty forest habitat types in Finland, all the types that are growing on dry, infertile soils have been transformed because of high nitrogen deposition. Yet another common reason that ecosystems have changed is the establishment of invading species, which often greatly influence the dynamics of native species and may lead to changes in nutrient cycling and other ecosystem functions (chapter 4). At the tenth conference of parties to the Convention on Biological Diversity in Nagoya, Japan, in October 2010, the participating nations agreed that “by 2020, ecosystems that provide essential services, including services related to water, and contribute to health, livelihoods and well-being, are restored and safeguarded, taking into account the needs of women, indigenous and local communities, and the poor and vulnerable” (Target 14). This aim is ambitious though somewhat vague, but in any case it reflects the recognition that ecosystems have become extensively modified and that this is a threat to biodiversity and the benefits that humans may expect to obtain from ecosystems. The global causes of change, such as climate warming and eutrophication caused by atmospheric nitrogen deposition, cannot be reversed by local actions, but in many other cases interventions are possible and often highly effective. Examples include erosion control, reforestation and revegetation of disturbed areas, removal of non-native species and reintroduction of native species, and habitat improvement for targeted species. Some measures are both cheap and effective. For instance, in my home country Finland, millions of hectares of bogs and mires were drained in the 1960s and 1970s. In the case of wet mires, the original draining operation was not effective and

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Fig. 6.6 Effects of agricultural intensification on the mean yield and yield variability in two insect-pollinated (squashes and zucchini) and two wind-pollinated crops (spring barley and peas) in France. Notice that agricultural intensification increases the mean yield and decreases variability in wind-pollinated crops but not in insect-pollinated crops. (Based on data from Deguines et al. 2014.)

the ditches have started to accumulate peat. The recovery of such mires can easily be assisted by filling the main ditches. Restoring all altered ecosystems remains an unachievable goal, partly because the global drivers, climate warming and general eutrophication, continue to have an effect, partly because the cost of restoring all ecosystems that in principle could be restored would be very high. Some ecologists have argued that restoring ecosystems to their natural state is often impossible because ecosystems have passed a threshold, essentially becoming a permanently different ecosystem (Hobbs et al. 2014). These researchers also suggest that the concept of “natural state” of an ecosystem is ill defined, because there are no static states: ecosystems are constantly changing even without any human influence. Some go as far as to say that “natural ecosystems” are valued for sentimental reasons, and shouldn’t be; we should accept and value also the altered ecosystems, dubbed “novel ecosystems,” for the species they have and for the ecosystem services they provide. It is true that communities and ecosystems change over time, but as with other global environmental changes, such as climate change and invasive species, the difference between natural changes and human-caused changes is not the change itself, but its speed, which prevents species and communities from responding and adapting as they do when the rate of change is slow. There is no evidence that it is common for ecosystems to have passed a threshold (Murcia et al. 2014),

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though there are some well-documented examples resulting from eutrophication in lakes and other water bodies (Scheffer and Carpenter 2003). Even in these cases the ecosystem could, in principle at least, be “pushed” back across the threshold to its previous state. The different camps in the debate about novel ecosystems disagree about how desirable it is to minimize changes in ecosystems that involve much uncertainty and pose future risks. On this issue I agree with those who maintain that risks should be avoided. The term novel ecosystem may give the impression to non-ecologists of something new and valuable for its own sake, something that we should prefer; hence we should stop worrying about the human impact on ecosystems. But this is a slippery slope toward gradual acceptance of continuous and potentially dangerous environmental changes. The debate about novel ecosystems reminds me of the ongoing debate about the use of genetically modified organisms in agriculture and forestry. I do not see much environmental risk in the present GMOs, but I am worried about the possibility of ever more modified organisms in the future (chapter 4). Who is going to draw the line, and where and when? The Biodiversity Hypothesis I have known Tari Haahtela as a butterfly photographer since 1990, when he and his colleagues published an award-winning book on Finnish butterflies. This volume helped me select the Glanville fritillary for a long-term research project that has lasted to this day. In addition to being a professional butterfly photographer, Tari is professor emeritus of clinical allergology at the University of Helsinki. In early 2010, both of us attended a national meeting in Helsinki, where I talked about rapidly declining biodiversity and Tari talked about rapidly increasing prevalence of allergies, asthma, and other chronic inflammatory disorders (figure 6.5). After the talks, he came to see me and started to explain that these two global megatrends must surely be related. He had much to say about the molecular basis of allergy, which I struggled to understand. But I understood the main point, which was that we need microbes to train our immune system. And biodiversity includes microbes. Tari invited me to join the next meeting of his research group, which I did, and that meeting turned out to be the beginning of a new line of research for a highly interdisciplinary group of researchers. The excitement in the room was memorable. I thought about this afterward, and reckon that we became so easily committed to something new to most of us because the project grew

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out of our own ideas, truly bottom-up, and out of ideas that immediately resonated with the disciplinary knowledge and interests of each of us. I have participated in other interdisciplinary projects over the years, and most of them have been rather disappointing. These projects were started because funding was available, and researchers felt that it was an obligation rather than a privilege to participate. Researchers are more like cats than like dogs. Tari Haahtela’s research group is called KARA, the Karelian Allergy Project. Karelia is the region that extends across the border between Finland and Russia; the border is an abrupt boundary in terms of people’s standard of living. What Tari and his colleagues have documented is a dramatic difference in the prevalence of allergies and asthma in the two parts of Karelia, and a striking difference in temporal trends: the younger the study subjects, the higher the prevalence of disorders, but only in Finland, not in Russia (Haahtela et al. 2015). People in Russian Karelia have all kinds of health problems, many of them related to traffic accidents, heavy smoking, and alcohol abuse, and the expected lifetime is shorter than in Finland— but people in Russian Karelia suffer very little from asthma and allergies. The explanation in a nutshell, explained Tari, has to do with the impoverished microbial contacts of people in Finland and hence the reduced immunoregulatory service of microbes to people, especially in early childhood. The critical difference could be the abundance and composition of microbes at home. The Russian houses have a more diverse microbial flora in the dust, food is not industrially processed as in Finland, and the water people drink has a rich and mostly beneficial bacterial community. But what might also matter is people’s contacts with microbes in the surrounding outdoor environment. We started to talk about the biodiversity hypothesis, and I joined Leena von Hertzen and Tari Haahtela to write a short paper to describe it (von Hertzen et al. 2011). My task, as an ecologist, was to figure out what could be done to characterize environmental biodiversity. We realized quickly that extending the research to Russia was not an option at this time, so studies could be conducted only on the Finnish side. But that was perhaps an advantage, as the results would not be dominated by the striking contrast across the border. Tari’s group had studied a cohort of young schoolchildren in 2003, randomly selected across a heterogeneous region 100 by 100 kilometers, including a small town, villages of different sizes, and isolated farmhouses. Importantly, the vast majority of families had not moved; hence the children had been exposed, their entire life, to the same environment, but different

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individuals had been exposed to different environments. This group of study subjects would be ideal for examining possible associations between health and environmental biodiversity around the home. We recruited the same kids for another round of sampling. Blood samples were taken to measure immunoglobulin E antibodies, a marker of allergic sensitization, or atopy. The immunologists in our group planned to measure the expression of other molecules that would reflect pro-inflammatory and anti-inflammatory immune responses. But what about biodiversity? Which kind of biodiversity would matter, and which kind of data could be collected in practice? I came up with three answers. First, having the spatial coordinates of the children’s homes and high-resolution remote-sensed data, we could describe the land use around each home: for example, which proportion of land within a three-kilometer radius was forest, agricultural land, built areas, water, and wetlands? Second, I hired a group of my students to visit the yards of every home to census all vascular plants. We considered measuring microbial diversity in the environment, but decided that we did not know how to sample it in a meaningful manner with the resources available. But something we could do was to characterize the microbes on the bodies of the study subjects. We focused on bacteria on the skin, partly because they are easy to sample— a swab of the forearm— partly because many contacts with the environment presumably take place via environmental microbes colonizing the skin. I had entered a field of research far from my past work but with a plethora of previous studies, ideas, and hypotheses. David Strachan from the London School of Hygiene and Tropical Medicine published a short paper entitled “Hay Fever, Hygiene, and Household Size” in 1989. He analyzed the epidemiology of hay fever using data for 17,414 British children, and he concluded that his results could be explained “if allergic diseases were prevented by infection in early childhood, transmitted by unhygienic contact with older siblings.” Strachan’s short paper has become a citation classic, referred to when other researchers want to mention the “hygiene hypothesis,” though Strachan himself did not use this term. As a matter of fact, more recent research has shown that infectious diseases are not necessarily that beneficial, nor is hygiene critical in the sense envisioned by Strachan. On the contrary, many infectious diseases remain a huge health concern, as we all know. Strachan’s paper is nonetheless an important milestone: it inspired a new line of inquiry. Most familiar infections, including influenza, are caused by viruses. Our ancestors in the distant past did not have them, because the disease agent

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could not persist in sparse hunter-gatherer communities (chapter 5). Most infectious diseases began to spread in the human population following the Neolithic revolution, which gave rise to agriculture, bigger and more permanent settlements, and eventually to towns and cities. The infectious diseases that then emerged have not been around for long in the human population, only for some hundreds of generations. They may have influenced our biological evolution, but much less so than the parasites, such as helminths, which do persist in low-density host populations and have infected our ancestors forever. The same is true for the microbes that crowd the environment and our bodies. Microbial life evolved more than 3 billion years ago, and it is clear that our ancestors, however far back in time you want to consider, have been interacting with microbes; the microbes have fundamentally shaped our biology. All these microbes are not in our bodies just for our benefit, of course, but we know that many microbes interact with our cells and molecular processes, to the extent that we could hardly survive without them. It would be unethical to do experiments with humans to show that, but researchers have developed germ-free mice as a model to examine interactions between microbes and the immune system. The point is that our biology has evolved with a diverse assembly of microbes. Mitochondria are an extreme example: they supply cellular energy, without which we would be dead in seconds, yet originally they were independent bacteria that colonized the ancestors of eukaryotic organisms, which have cells with a nucleus enclosed within membranes. Eukaryotes developed approximately 2 billion years ago. The other extreme includes microbes, which could be called casual visitors and for which we provide temporary habitat, but which do not much affect us, as far as we know, and which may be present or absent. The other microbes are somewhere in between. These are the ones that Graham Rook likes to call our Old Friends (Rook 2009; Rook et al. 2014). These old companions of ours have been around during all our evolutionary history; these friends increase our well-being and play a critical role in immunoregulation. Graham Rook has likened our immune system to a computer that has genetically inherited mechanisms (programs) but lacks data. Our interactions with parasites and microbes, especially in infancy and early childhood, provide the database that is necessary for the immune system to react— but not to overreact! The immune system needs to develop a network of regulatory pathways and immunosuppressive cells that stop inappropriate immune attacks on self, harmless allergens, and gut contents (Rook et al. 2014). Hel-

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minths and other parasites represent one class of organisms that provide this training to our immune system. Infections by helminths are not necessarily harmless, but once the parasite is established, there is little that the immune system can do to get rid of it without causing even more damage to the host. Microbes that typically inhabit the human gut, airways, skin, and other body parts play a big role in training the immune system, and so may bacteria, archaea, fungi, protozoa, and viruses that enter our bodies with food, water, and air and via our various contacts with the environment. I like to consider the human body as a habitat patch for these microbes. We have our current, more or less permanent residents, which are transmitted between parents and their children and among other individuals; and there are billions of hopeful newcomers from the environment, colonizing us daily, which can establish temporary or more permanent populations in the habitat patch and interact with it like the old residents. In the course of evolution, today’s more permanent residents in and on our bodies, which make up the core human microbiota, were assembled from such colonists, and this process must continue today. Here I come to the question that we wanted to address in our research: what difference does the kind of environment, and therefore the kinds of microbes, we happen to interact with make to the functioning of our immune system and our general well-being? The biodiversity hypothesis is an extension of the Old Friends concept, with a focus on the influence of environmental biodiversity on our immune system. So does the environment around us influence the kinds of microbes we have in our bodies? There is clear evidence showing that the type of food we consume affects the composition of the gut microbiota (Wu et al. 2011), which is not surprising, as the microbes in the gut obtain their nourishment from what we swallow, and different microbes are somewhat specialized to use different resources. In our project, we sampled the skin microbiota. Comparing adolescents whose homes had more or less forest and agricultural land within a three-kilometer radius, we observed a clear pattern: the more forest and agricultural land around the home, the more Proteobacteria on the skin (figure 6.7). Proteobacteria comprise nearly half of all prokaryotic genera and include most gram-negative bacteria of medical, veterinary, industrial, and agricultural importance. Most Proteobacteria are free-living, and they are very common in soils. One study found that the relative abundance of Proteobacteria ranged between 20% and 60% in different soil types (Eilers et al. 2010), making it plausible that they would show much variation along the environmental gradient in our study (figure 6.7).

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Fig. 6.7 Relative abundance of Proteobacteria on the skin of healthy individuals is associated with the relative abundance of forests and agricultural land around the home within a threekilometer radius (the land-use gradient; the relative abundance of forests and agricultural land varies from 0 to 1; the rest includes other forms of land use). (After Ruokolainen et al. 2015.)

Many Proteobacteria are pathogenic, which may cast doubt on their beneficial immunoregulatory role, but this need not be so. Pathogenicity is in most cases a contextual state; the capacity of a microbe to trigger disease depends on host status and genetics, where the microbe is located in the body, and which other microbes coexist with it. A puzzling feature in our results was that the relative abundance of Proteobacteria on the skin was related to the amount of forest and agricultural land around the home in healthy individuals only, whereas in atopic individuals, with elevated IgE antibodies in their blood, there was no such relationship. This may indicate that the cause and the effect are not one way; perhaps being atopic somehow influences the skin microbiota. Another interesting finding was that healthy individuals had significantly higher diversity of one class of Proteobacteria, called Gammaproteobacteria, on their skin than atopic individuals (Hanski et al. 2012). Other studies have shown that reduced diversity of intestinal microbiota is associated with increased risk of allergic diseases (Bisgaard et al. 2011), and that exposure to diverse environmental microbiota—for instance, on traditional farms—has a protective effect for asthma and atopy

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Fig. 6.8 The yard around this house may look messy to some people, but more than 100 species of native flowering plants and hundreds of insect species have been recorded here.

(Heederik and von Mutius 2012). We also found that healthy individuals were living in homes with more species of native flowering plants in the yard than found around the homes of atopic individuals. The mechanism remains unknown, but may be related to microbes on plant surfaces. Or perhaps high diversity of native flowering plants is just an indication that the family does not like to have a lawn or a paved yard around the home. A yard with a rich community of native flowering plants is likely to have a rich community of beneficial microbes. These yards contribute toward conserving biodiversity of plants and insects and, as our results hint, possibly also toward the health of children in the house (figure 6.8). The biggest surprise was yet to come. Immunologist Nanna Fyhrquist measured the expression of a range of genes in leukocytes in the blood samples we had obtained from the study subjects. I correlated these results with the relative abundance of different bacterial genera on the skin and found a striking relationship. If the subject had much bacteria belonging to the genus Acinetobacter on his or her skin, the measurements showed that the blood-derived leukocytes expressed much of a molecule called interleukin-10 (IL-10), which is a key anti-inflammatory molecule in our immune system. In other words, the more Acinetobacter you have on your skin, the more your immune system produces a molecule that increases your immune tolerance. Acinetobacter belongs to Gammaproteobacteria, connecting the

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immunological result to the environment- related pattern in figure 6.7. These are encouraging results, though one has to keep in mind that correlation does not prove causality. We cannot do experiments with Finnish school children to further test the hypothesis that Acinetobacter makes a difference, but Nanna did such experiments with mice. What she found was consistent with our hypothesis: in the mouse model, Acinetobacter induced strong TH1 (a type of T helper cells) and anti-inflammatory responses by immune and skin cells and protected against allergic sensitization and lung inflammation through the skin (Fyhrquist et al. 2014). Our studies have made a small contribution to rapidly expanding scientific knowledge about the role of microbes in human life and well-being. By now, it is clear that bacteria and other microbes are intimately connected to the proper functioning of our bodies. Every person is a hugely complex ecosystem, as complex as the ecosystems surrounding us. Many scientifically challenging and societally crucial questions remain to be studied, apart from the fundamental biological questions about how exactly the communication between microbes and our own cells takes place. Is the early childhood exposure to environmental microbes all that matters, or does our exposure as grown-ups enhance the immunoregulatory circuits? Both probably matter, but what happens in the first two or three years of life is especially important. We found that forests and agricultural land had similar beneficial effects, but most likely it makes a difference which kind of forest and which kind of agricultural land the home is surrounded by. Would city parks do, and which kinds of parks— a hugely significant question for city planning. Which particular components of biodiversity in the “macrobiota,” consisting of fungi, plants, and animals, are important for rich microbiota? Studies have shown that children growing up on traditional farms with many species of domestic mammals have less incidence of allergies and asthma in late childhood (von Mutius and Vercelli 2010). But what about wild animals? We share with them common agents of infection; surely we also share beneficial microbes. Does defaunation of tropical forests and the disappearance of large-bodied mammals from most ecosystems lead to diminishment of those microbial populations that are most beneficial to us? Some readers may ask whether it would be possible to culture the good bacteria and apply them to our skin. I take probiotics, including several species of Lactobacillus, Bifidobacterium, and others, and I believe that they may contribute to my healthy gut flora and well-being. Though what actually matters may be the diversity of beneficial microbes to which we are exposed

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rather than any particular microbial species or strains. Perhaps the same applies to other microbes and other parts of the body. Perhaps— or perhaps not. The microbiota inhabiting our bodies is a hugely diverse and complex community, and its interactions with the diverse environmental microbiota can hardly fail to be even more complex. A technological fix with a few bacteria might work in some cases, but probably not in many others. There is no other biodiversity with which we are equally connected than the biodiversity on our skin and in our gut, but this biodiversity may depend more on the environment and its biodiversity than we have thought, if we have thought about this question at all. We are the innermost doll in a Russian matryoshka, protected by two layers of biodiversity— we should not allow these shields to be broken. The microbial world with which we have lived during our entire evolutionary history represents a most intimate and tangible ecosystem service, which affects us all, all the time. We should take the rapidly increasing prevalence of allergies, asthma, and other chronic inflammatory disorders as a serious sign that our well-being is threatened by the breaking connections between us and nature. Messages 1. East Greenland has a very simple community of one species of small mammal, the collared lemming, which is preyed upon by four species. The lemming populations exhibited strikingly regular four-year cyclic fluctuations until the year 2000, after which peak lemming years have been missing, and the dynamics of the entire community have changed. The cause is climate warming, which is already affecting the dynamics and stability of the most remote populations. The simple community in Greenland is vulnerable to environmental perturbations. 2. Whether biodiversity increases the stability of populations, communities, and ecosystems has been debated for 100 years. Theoretical work done in the 1970s challenged the traditional view that diversity begets stability. This theory is now known to have limited applicability, but it stimulated a huge amount of new research, and demonstrated the value of theory and models in forcing researchers to formulate their ideas precisely and in a testable form. 3. Experimental studies conducted in the past twenty years demonstrate that diverse communities have higher productivity and greater stability than communities consisting of a small number of species, though at the same

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time more diverse communities may include species with highly fluctuating populations. In brief, biodiversity generally increases ecosystem productivity and stability. 4. Researchers debate what should be done with ecosystems that have been altered by humans, often called novel ecosystems. Some argue for valuing novel ecosystems for the ecosystem services they provide, but other researchers highlight the risks of ecosystem transformations. Generally, it is wise to minimize ecosystem-level alterations and to increase efforts to restore degraded ecosystems. 5. The prevalence of many non-communicable diseases is increasing rapidly worldwide, and they are replacing infectious diseases as major causes of death. Examples of non-communicable diseases include allergic and autoimmune diseases, asthma, inflammatory bowel disease, certain cancers, depression, and Parkinson’s disease. According to the biodiversity hypothesis, one reason for the rapid increase of non-communicable diseases is reduced contact of people with environmental biodiversity, which has adverse consequences for the composition of the microbial populations in and on our bodies. A healthy microbiota is needed for the normal development of the human immune system. The biodiversity hypothesis highlights one mechanism whereby biodiversity increases human health and well-being.

Epilogue

The first island in my life, Haminanluoto in the eastern corner of the Baltic Sea, is so small that regardless of which direction you look, the shoreline is only a few steps away. Everything can be observed from one spot without much effort. Even a child will understand that there are limits to Haminanluoto, limits that cannot be crossed. Most people have memories of islands, small and large, but one island often remains unnoticed. When you stand on it, you can see the skyline to the north and south, to the east and west, but it’s a curious skyline, because you can walk behind it. You can even circumnavigate the island by walking behind the horizon and ascending to your point of departure from the opposite direction. It took thousands of years before people realized that this island is a sphere. The island has no coastline, which makes it hard to understand that there are nonetheless limits to this island, just as there are limits to any other island. Another oddity is the isolation of this island. There are other islands in the surroundings, more than anybody could ever have time to count. It is possible, in principle, to land on those other islands, but in practice it is impossible; our island is completely isolated. If the reader were sent to my first island with the knowledge that there is no return, he or she would understandably be desperate. If the unfortunate individual had any energy to plan for the future, the first thought would not be to cut down the only tree on the island or to tear down the few bushes. 221

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Haminanluoto. (Photo courtesy of Eeva Furman.)

On the contrary, the solitary tree would seem like a companion, under which one could erect a shelter against wind and rain. The limited flora and fauna of Haminanluoto would quickly become familiar to the hungry inhabitant, who would wish that especially the larger and tastier animals would prosper. In the spring of 1978, I was camping in the forest in Gunung Mulu, Sarawak. On April 27, we had no work to do, and my assistant Tapit proposed that we visit a Penan family that he knew was camping in the neighborhood. After an hour’s walk we came to two small temporary shelters, erected on poles so that the floor was a meter above the ground. The shelters were temporary, because Penans were nomads; they erected a new hut every few days or weeks in a new spot, in their never-ending search for the sago palm and animals to hunt. I learned that the Penan language has forty words related to sago, but there is no word for good-bye or a word for thank you. All food is shared among the group members. A Penan elder has said, “The earth is sacred, it belongs to innumerable deceased people, those few who are presently alive, and all those who have not yet been born.” I don’t think that we are any cleverer or more stupid than the Penans, or that they had a higher morality than we do. A small family group used a limited piece of rain for-

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est from one generation to another. Food was not always plentiful, but the group survived as a group; sharing food was in the interest of both the individual and the group, and it was definitely in everybody’s interest to make sure that sago palms, fruiting trees, and wild boars and other animals survived. The group had to manage on its own within the small area that they and only they knew well. What happened elsewhere in the world did not have any influence on their life. When my own ancestors established the Hanski village on the Gulf of Finland in the beginning of the seventeenth century, they too were living an independent life. The outside world did make some difference, but what the king decided in Stockholm influenced the villagers after a long delay, and often not at all. Today, the world is very different. What one person does in one place on the planet can potentially affect the life of billions in a matter of hours, to say nothing of the collective actions of people that influence everybody, from the jungles of Borneo to the east coast of Greenland. When the interactions among individuals, companies, organizations, and societies extend over ever larger areas, encompassing ever more people, the feeling of being a member of a group changes to the feeling of being surrounded by competitors. If you were living in a small piece of rain forest in Borneo, or in a small village in southeastern Finland in the seventeenth century, you would know well what is there and what is available, and what are the likely consequences if you do this or you do that. When the entire planet is at your disposal, it is easy to forget that there are any limits at all. Nevertheless, limits exist, and humankind comes across these limits, sooner or later, when billions of us use sophisticated science and technology to extract resources with inevitable collateral damage to the environment. The world of the Penans was small, just a piece of forest on the slope of a single mountain, but they seemed to have an understanding of time: the dead, the living, and the unborn were all part of the Penan family. In our case the situation is just the opposite. We know the entire world; we know the height of every mountain, the width of every valley, and the length of every peninsula. But we have forgotten how to think about time; our perception of time has shrunk to the present and very immediate future. What should be done? There is no return to the past, not even for Penans, who have lost the nomadic life of their ancestors and have been forced to accept limited life in a small village with no true prospects for the future. The Penans have drifted to their present situation without their own planning. All of humanity appears to be drifting, without any real planning

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for the future. Most people, politicians and decision makers included, accept that there are problems, but their solutions— often based on religious beliefs about afterlife or the expectation that science and technology will always come to our rescue— are not realistic. We are trapped by ideology, the belief that there is no alternative to a global market economy. Those of us who live in wealthy countries have been misled by the recent history of steadily increasing standard of living, improving health, increasing longevity, and amazing opportunities to enjoy life in myriad ways. Most people are unable to see how quickly and how dramatically the world around us is changing, and we have been misled to believe that growth and increasing wealth will continue forever. In reality, there is little cause for optimism as long as the present economic and political orders prevail. We lack political leadership that would address the root problem, destructive competition among individuals, groups of individuals, companies, and organizations, and among nations. If our civilization is representative, one reason that there is no sign of intelligent life elsewhere in the universe may be that such life is ephemeral, likely to destroy its own material basis within a blink of geological time. It is difficult for societies and humankind to change their course, but it is also difficult to believe that attempts will not be made when it becomes sufficiently clear to most of us. The question is how much damage will be done by that time, and how permanent it will be. In the long run, microbial life will remain the hard core of the future biodiversity on Earth, just as it has been for the past 3 billion years. Let us hope that the yet unborn generations of our species are also part of the surviving biodiversity.

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Index

Note: Page numbers followed by f indicate a figure; those followed by t indicate a table. Acinetobacter, 216–17 adaptability, 202 adaptation, 98–103, 112; classical evolutionary form of, 98–100, 103; dispersal capacity in, 100–101; local forms of, 90–92; plasticity in, 99–103; timing of growth and reproduction and, 102–3 adaptive radiation, 57–60, 75 adder (Vipera berus), 136, 137t agriculture, 28, 41, 105, 206–9, 217; in biodiversity hot spots, 32; intensive cultivation in, 207–8, 209f; Neolithic revolution and, 27, 132, 158, 173, 213 Aichi Biodiversity Target 11, 33 Åland Islands: fragmented landscape of, 153–57, 159, 184; image of, 147f. See also Glanville fritillary butterfly alien species. See invasive species allergies and asthma, 205–6, 210–19 allopatric speciation, 54 alpha (α) diversity, 139–42, 145

Alvarez, Luis, 24 Amazon River basin, 174–75 American aloe (Agave americana), 122 American mink (Neovison vison), 143 amphibians, 107–9 angel lips (Lantana camara), 122, 125 angiosperms, 24, 107–8 Animal Ecology (Elton), 190, 195 Animal Ecology Research Group (AERG), 4–5 Anthropocene epoch, x ants, 131–32 Aphodius, 90–91 Aphodius bouvouloiri, 91 Aphodius costalis, 91 Aphodius holderieri, 91, 92f Arachnodes radiation, 58–59 Archaeopteris, 21–22 arctic blue butterfly (Agriades glandon), 189 arctic fox (Vulpes lagopus), 192 arctic lemmings. See collared lemmings

241

242

Index

Arctic regions: climate change and, 194, 208; increasing biodiversity in, 189– 90; low stability of mammalian populations in, 190–94; snow-free periods in, 194. See also Greenland Argentine ant (Linepithema humile), 131–32 Argentinosaurus, 85 assisted migration, 132–39, 145 atmospheric nitrogen deposition, 208 Australia: dingoes of, 88–89, 129; dung beetles in, 7–8, 133; invasive species in, 126–31, 133; losses of megafauna in, 86, 88–89, 129 Australian blackwood (Acacia malanoxy­ lon), 122, 125 average global temperature, 92 aye-aye lemur (Daubentonia madagascarien­ sis), 57, 58f Azores: endemic species of, 121–22; geological history of, 121; human settlement of, 121; invasive species in, 121–25 Azores bullfinch (Pyrrhula murina), 121 bacteria, 17–19 Baez Fumero, Marcos, 116 Baltic Sea, 11, 73; changing bird species of, 83; eutrophication of, 80; uplift of islets in, 79. See also Haminanluoto Island barley (Hordeum vulgare), 132 barnacle goose (Branta leucopsis), 81t, 83 Basset, Yves, 6 Batesian mimicry, 55 bearberry honeysuckle (Lonicera involu­ crata), 122 beech (Fagus sylvatica), 143 bee orchids (Ophrys apifera), 64, 65f bees, 64–66 beetles: biodiversity of, 41; genetic variation in populations of, 101–2; number of known species of, 15–17. See also dung beetles beta (β) diversity, 139–42, 145 biodiversity, ix–xii, 187–219; alpha (α) and beta (β) forms of, 139–42, 145;

changes in, 77–112; disappearance of, 103–12; ecosystem stability and, 195–200, 218–19; estimated numbers of species and, 9–10, 15–19, 41; evolutionary history of, 19–27; generation methods of, 44–75; global declines in, x, 133–38, 140–42; habitat and ecosystem variety in, 2, 27–32; immune system disorders and, 205–6, 210–19; Living Plant Index (LPI) of, 105–7; movement of species and, 115–45; north-south trends in, 189–90; patterns of distribution of, 32–41. See also species richness Biodiversity and Wine Initiative, 201 biodiversity hot spots, 32–34, 41, 175; Borneo, 45–46; Brazil’s Atlantic forest region, 161f, 162–64, 175–78, 181; definition of, 175; extinction debt in, 175; Madagascar, 44–48 biodiversity hypothesis, 210–19 biogeography, xi, 38, 118 birds, x; of the Azores, 121; of the Canary Islands, 119; cat predation on, 128– 29; climate debt and, 96, 99–100; on Haminanluoto Island, 79–82; IUCN red list of, 107–9; in Mauritius, 123; northward shifts in distributions of, 96; number of known species of, 15; reduced flight capacity in, 73; timing of growth and reproduction of, 102–3 blowflies, 116–18 blue chaffinch (Fringilla teydea), 119 blue whale (Balaenopter musculus), 84 boreal forests, 28, 29; assisted migration in, 137; deforestation of, 141; managed forestry of, 177, 207–8; microhabitats of, 31–32; non-fragmented expanses of, 175; threatened wolves of, 89, 129 boreal voles, 66–68 Borneo, xi, 32, 41, 44; butterfly species of, 189; climate change in, 97; dung beetle species of, 6–9, 14–17, 44, 46–48; endemic species of, 46; evolutionary

Index

history of, 45–46; geological activity on, 48; image of, 1f; mammalian fauna of, 47; shifting geographic distributions of dung beetles in, 96–98. See also Gunung Mulu Brazil: Amazon River basin of, 174–75; Atlantic forest region of, 161f, 162–66, 175–78, 181 British Everest Expedition of 1924, 91, 92f brown bear (Ursus arctos), 89–90, 137 brown rat (Rattus norvegicus), 29 butterflies: in Borneo, 189; climate debt and, 96, 99–100; coevolution of, 61– 63; genetic variations in flight capacity of, 101; genome sequences of, 156–57; in Greenland, 189–91; mark-recapture study of, 153; northward shift in distributions of, 93–96; parasitoid wasps and, 12–13, 155, 194–95; pollination role of, 63–64; range expansion of, 99– 101. See also Glanville fritillary butterfly Cactoblastis cactorum, 126–27, 133 Calliphora splendens, 116–20 Calliphora vicina, 117–18 Calliphora vomitoria, 117–18 Cambrian period, 66, 110; evolutionary innovations of, 20, 21f, 41; fossil marine animals of, 84 Canary Islands: bird species of, 119; blowfly species of, 116–20; whistled language (silbo) of, 120. See also La Gomera cane toad (Rhinella marina), 129–31 Caracal caracal, 201 Carboniferous period, 22, 31 cassava (Manihot esculenta), 132 Cedar Creek Ecosystem Science Reserve, 200 Cenozoic era, 24–27, 35–36, 178 changes in biodiversity, 77–112; adaptation and, 98–103; disappearance of biodiversity and, 103–12; globalization of nature and, 83–84, 139–45, 223– 24; global megatrends in, 97–98; on

243

Haminanluoto island, 79–83; in largebodied species, 80, 81t, 84–90; shifting geographical distributions and, 90–98, 112; in species richness and composition, 82–84, 90–92, 105–6, 111. See also climate change Chilean rhubarb (Gunnera tinctoria), 122 Chitty, Dennis, 66–67 Chitty hypothesis of population regulation, 67–68 chronic inflammatory disorders, 205–6, 210–19 Chrysomya albiceps, 119–20 Chrysomya chloropyga, 120 Chrysomya megacephala, 120 climate change, x, 98–99; adaptation and, 98–103; collared lemmings’ population cycles and, 194, 218; disappearance of biodiversity and, 103–12; Glanville fritillary butterflies and, 155; in Greenland, 189, 194, 208; habitat generalists vs. specialists and, 99; rapid rate of, 27, 95, 99–100; shifting geographical distributions and, 92–95, 97; timing of growth and reproduction and, 102–3 climate debt, 96, 99–100 Clostridium difficile, 138 coastal ecosystems, 28 Cochliomyia macellaria, 120 Coe, Malcolm, 5, 7, 23, 116 coevolution, 61–63, 65, 75; of dinosaurs and angiosperms, 24; of insects and angiosperms, 24; of large-bodied species, 85–86; of plants and herbivorous insects, 65 collared lemmings (Dicrostonyx groenlandi­ cus), x, 218; new population stability of, 193–94, 218; population cycles of, 66, 190–93, 195; predators of, 192–93 Columba junoniae, 119 Columba trocaz, 119 Columbus, Christopher, 39, 120 common evening primrose (Oenothera biennis), 71, 122

244

Index

common green bottle fly (Lucilia sericata), 119 common prickly pear cactus (Opuntia stricta), 126–28 community (alpha [α]) diversity, 139–42 competition for resources, 7; among dung beetles, 7–9, 15, 55, 90–91; specialization and, 9 complementarity, 198–99 Congo River basin, 174–75 conservation biology, 38, 150, 200–206, 219 conservation landscapes, 181–84 conserved land. See protected land continuous environmental change, 202 Convention on Biological Diversity of 2010, 33, 179–80, 208 Coope, Russell, 90–91 Cope, Edward Drinker, 85 Cope’s rule, 85–86 coral reefs, 28, 40–41 cormorants, 83 Costello, M. J., et al., 17 Crafoord Prize, 178 creationism, 69–70 Cretaceous period, 23–24, 25f; in Borneo, 45; insect pollination in, 64–65; in Madagascar, 46 crickets, 99–100 cryptic species, 13–14 Cryptomeria japonica, 121 cultural services, 202–4 Curtis, John, 158–59 cyclic populations, 66–68 Dactylopius scale insects, 126–27 Darwin, Charles, xi, 37, 48–54, 148. See also natural selection Darwin’s finches, 49–54, 57, 60–61, 68– 70, 74 Dawkins, Richard, 5 dead-wood microhabitat, 31–32, 176 decline of biodiversity, ix–x, 140–42; assisted migration and, 133, 145; habitat

fragmentation and loss in, 167; loss of genetic variation in, 133–38 deer ked (Lipoptena cervi), 89 defaunation, 177–78. See also extinction; threatened species Devonian period, 21–22 dingoes, 88–89, 129 dinosaurs, 23–24, 26; coevolution with angiosperms of, 24; evolution of large bodies of, 85; K/Pg (CretaceousPaleogene) boundary and, 24; mass extinction of, 24, 57–58, 110, 173, 178 disappearance of biodiversity, 103–12. See also extinction; threatened species distribution: climate-based models of shrinkage of, 103–11; habitat conversion and, 105–6; limitations on, 101; northward shifts in, 90–98, 112; range expansion and, 98–103 diversity. See biodiversity; species richness DNA barcoding, 11–14, 18 dodo bird, 123 domestic cat (Felis catus), 128–29 Dornelas, Maria, 82–84, 105–6 dung beetles, 5–17; adaptive radiations of, 57–60; in Australia, 7–8, 133; in Borneo, x, 6–9, 14–15, 44, 46–48, 96–98; competition for resources among, 7–9, 15, 55, 90–91; contribution to ecosystems by, 7–8; disappearances and extinctions of, 109–10; in Madagascar, 13f, 46–48, 49f, 54–61, 109, 119; number of known species of, 15, 17; rearing of offspring by, 15; sampling method for, 7; shifting geographical distributions of, 90–92, 96–98; in southeastern England, 90–92; specialization among, 9; speciation of, 54–61 dusky meadow brown butterfly (Hypo­ nephele lycaon), ix–x dwarf elephants, 85–86 eco-evolutionary dynamics, 67–68 ecosystems, 27; definition of, 2–4; of early

Index

life, 20; evolutionary change in, 19–27; human impact on, 27–28; stability of, 195–200, 218–19 ecosystem services, 201–6, 219 Edith’s checkerspot butterfly (Euphydryas editha), 93–95, 151–52 Ehrlich, Paul, 61–63, 93, 151–52 einkorn (Triticum baeoticum), 132 Elton, Charles, 5, 90, 196f, 199; on diversity and stability, 195–96, 200; on food chains, 195; on population cycles, 66, 190–91 emmer (Triticum turgidum), 132 endangered species. See threatened species Epactoides radiation, 60 equilibrium theory of island biogeography. See island theory eradication thresholds, 158 Erwin, Terry, 16–17 Eucera genus, 65f Eurasian lynx, 89–90 European map butterfly (Araschnia levana), 100–101 European mink (Musteola lutreola), 143 eutrophication of bodies of water, 70, 74, 80, 208–9 evolutionary history, xi–xii, 19–27, 41; of Borneo, 45–46; hybridization and, 10– 11; of increases in body size, 84–86; of Madagascar, 46; of mass extinctions, 24, 110–11; microevolutionary changes in, 70; natural selection and, 50–54; Neolithic revolution in, 27, 132, 158, 173, 213; trends in, 26–27 evolutionary radiation, 57–60, 75. See also generation of biodiversity evolutionary theory, 148. See also natural selection exotic species. See invasive species extinction, 24, 110, 145; changing land-use patterns and, 105; of dinosaurs, 24, 57–58, 110, 173, 178; failure to adapt or move and, 98–103; of Glanville fritillary butterflies, 155; increased

245

rates of, 110–11; invasive species and, 107–8, 145; living dead species and, 164–66; loss of genetic variation and, 133–38; mass extinctions, 24, 110–11; of megafaunal species, 47–48, 75, 86– 90, 110–11, 129, 177–78; northward shift in species’ distribution and, 93– 98; predictions of, 103–12; risks for humans of, 112 extinction debt, 96, 164–66, 175, 184–85 extinction thresholds, 157–64, 170, 172, 184; habitat quality and, 159; metapopulation capacity and, 160–62; minimum viable population size in, 160, 172 Fahrig, Lenore, 169 fast evolutionary changes, 68–75 fecal transplantation, 137–38 feral cats, 129 50/500 rule, 160 Finland, xi, 223; Åland Islands of, 147–57; butterfly species of, 99, 100f, 151–52; dead-wood microhabitat species of, 176; drained peat bogs and fens of, 83, 208–9; forest reindeer of, 136–38; Glanville fritillary butterfly of, 12–13, 71–74, 152–57, 159–62, 172; Haminanluoto Island in, 77–84, 221–22; high nitrogen deposition in, 208; managed forests in, 177, 207–8; northward shifts in distribution of butterflies in, 95–96, 100–101; protected land in, 34, 180–81; species diversity in, 34; threatened and extinct species in, 108, 141; translocated species in, 136–38; wolf conservation debates in, 89; woodland key habitats (WKH) in, 171–72 fishes, 107–8 Florida panther (Puma concolor coryi), 135–36 forest ecosystems, 27–28, 29, 217; defaunation in, 177–78; definition of, 174; evolutionary history of, 173–74;

246

Index

forest ecosystems (continued) fragmentation of, 174–78, 185; habitat loss in, 173–78; managed forests and plantations in, 176–77, 207–8; microhabitats in, 31–32, 176; total area of, 174, 185. See also boreal forests; tropical forests forest reindeer (Rangifer tarandus fennicus), 136–37 fragmented habitats, 147–73, 184–85; in the Åland Islands, 153–57, 159–62, 172; in Brazilian Atlantic forests, 161f, 162–66, 170, 175–78, 181; in Estonian island grasslands, 164–65; extinction debt in, 164–66, 184–85; extinction threshold in, 157–64, 170, 172, 184; of forest ecosystems, 174–78, 185; scientific debates on, 166–72; spatial configurations and SLOSS question of, 167–72; species richness in, 170; third-of-third rule of, 179–85; 20% rule of, 172. See also habitat conversion and loss freshwater ecosystems, 28, 70, 74, 208–9 fritillary butterfly (Clossiana chariclea), 189 fritillary butterfly (Clossiana polaris), 189 Fyhrquist, Nanna, 216–17 Galápagos Islands, xi; Darwin’s finches on, 49–54, 57, 60–61, 68–70, 74; Darwin’s visit to, 48–49; fast evolutionary changes on, 68–75 gamma (γ) diversity, 140 Gammaproteobacteria, 215–17 gene phosphoglucose isomerase (Pgi), 101 generalist species, 29, 99, 142, 145 generation of biodiversity: adaptive radiation in, 57–60, 75; among Darwin’s finches, 49–54, 57, 60–61, 68–70, 74; coevolution and key innovations in, 60–63, 65, 75; eco-evolutionary dynamics, 67–68; fast forms of, 68– 75; insect pollinators and, 63–66; of Malagasy dung beetles, 56–61. See also speciation

genetically modified (GM) organisms, 143–44, 210 genetic drift, 52 genetic rescue, 134–36 genetic variation: assisted migration and, 133–38, 145; in isolated populations, 155–57 genome sequences, 156–57 genotype, 10–14, 18 geographical distribution. See distribution giant salvinia (Salvinia molesta), 125 Gilg, Olivier, 190–93 ginger lily (Hedychium gardnerianum), 122, 125 Ginkgo biloba, 23 glacial periods, 25, 36; glacial maxima of, 27; migrations of populations during, 101–2 Glanville fritillary butterfly (Melitaea cinxia), 12–13, 71–74; caterpillar webs of, 154–55; dispersal capacity of, 72– 73; extinction threshold of, 160, 161f; fecundity of, 155; flight paths of, 72f; in fragmented habitats, 152–57, 159– 62, 172, 184; genome of, 156–57; grip strength and wind resistance of, 73– 74; host plants of, 152–53; inbreeding among, 155–57; local extinction among, 155; metapopulation capacity of, 160–62 globalization of nature, 83–84, 139–45, 223–24 global megatrends, 97 global warming. See climate change La Gomera (Canary Islands, Spain): blowfly species of, 116–20; human colonization of, 120; image of, 115f; laurel forests of, 117f, 118; whistled language (silbo) of, 120 Gondwana, 21, 46 gonorrhea (Neisseria gonorrhoeae), 159 Gould, Stephen Jay, 111 Grant, Peter, 68–70 Grant, Rosemary, 68–70

Index

grapevine pests, 200–201 grasslands, 27–28 gray squirrel (Sciurus carolinensis), 142–43 gray wolf (Canis lupus), 89–90, 137 Greenland, xi, 44, 187–95; butterfly species of, 189–91; climate change in, 189, 194, 208; collared lemming population of, x, 66, 190–94, 218; image of, 187f; insect species of, 194; low-flying insects of, 189; Northeast Greenland National Park in, 33–34, 189–91, 208; predator species of, 192–93, 195; rate of colonization by new species in, 191; species interactions in, 194–95 green tsunamis. See invasive species green-underside blue (Glaucopsyche alexis), 100f greylag goose (Anser anser), 79, 81t group selection, 167 Gulf of Finland. See Finland Gunung Mulu (Sarawak, Malaysia), 1–9, 222–24; dung beetle species of, 6–9, 14–15, 44; number of tree species in, 16; palm oil plantations in, 177; Penan people of, 2, 3f, 222–24; Royal Geographical Society Expedition to, 4–6; shifting geographic distributions of dung beetles in, 96–98; variety of habitats and ecosystems in, 4, 14 Gunung Mulu National Park, 2, 44, 178 Gyllenberg, Mats, 150 gypsy moth (Lymantria dispar), 130–31 Haahtela, Tari, 210–11 habitat conversion and loss, 31, 97, 105– 6, 185, 202; in the Azores, 121–25; extinction debt in, 96, 164–66, 175, 184–85; extinctions of megafauna and, 47–48, 86–90, 111–12, 129, 177–78; extinction threshold in, 157–64, 170, 172, 184; forest-inhabiting species and, 173–78; fragmented landscapes and, 150–51, 161f, 162–64; globalization of nature and, 141–45; inbreeding

247

depression and, 155–57; novel ecosystems and, 206–9, 219; third-of-third rule and, 179–85; threatened species and, 140–42; in tropical forests, 83, 97, 109–10, 175–78. See also fragmented habitats; protected land habitat generalists, 29, 99, 142, 145 habitats: definition of, 2–4; hierarchical classifications of, 28–29; land-cover types of, 27–28; species interactions and, 30; species’ requirements of, 29– 32; of threatened species, 31, 33, 88; variety of, 27–32 Habitats Directive of the European Union, 28–29 habitat specialization, 99 Hamilton, William, 31 Haminanluoto Island (Finland), 77–84, 221–22; body mass of birds on, 80, 81t; changes in bird community of, 79–82; changes in bird species composition on, 82–83; eutrophaction of the sea surrounding, 80; geological history of, 79; greylag goose on, 79; human pressures on, 80–82 Hannunpoka, Erik, 77–78, 80 Hansen, M. C., et al., 174 “Hay Fever, Hygiene, and Household Size” (Strachan), 212 heath fritillary, 13 Heliconius melpomene, 157 Helictopleurus genus, 59–60, 109 Helictopleurus quadripunctatus, 54–59 Helm, Aveliina, 164–65 Hertzen, Leena, 211–19 Holocene epoch, 26 Homo floresiensis, 86 Homo sapiens, 26; habitat requirements of, 29; increased biomass of, 87. See also human populations honeybees (Apis mellifera), 65–66 horizontal gene transfer, 17–18 hornless rhinoceros (Paraceratherium), 84 hot spots. See biodiversity hot spots

248

Index

Huijbregts, Hans, 15 human populations: extinctions of megafauna and, 47–48, 86–90, 111–12, 129; focus on nature-based solutions by, 201–2; immune system disorders in, 205–6, 210–19; infectious disease transmission among, 157–58, 212–13; movement of species and, 120–39; novel ecosystems of, 206–9, 219; pressure on fishing by, 80–82; risks of extinctions of species and, 112; urbanization challenges of, 204–6. See also habitat conversion and loss hunting and poaching, 174, 177–78 hybridization, 10–11 hygiene hypothesis, 212–13 Hyytiäinen, Reima, 80 immune system disorders, 205–6, 210–19 inbreeding depression, 133–38, 155–57, 160 Indian mongoose (Herpestes auropuncta­ tus), 123 infectious diseases, 157–58, 212–13 insect pollinators, 63–66 insects, 41; of the Cambrian epoch, 20, 21f; coevolution of, 61–63; dead-wood microhabitats of, 31–32, 176; in Greenland, 189; IUCN red list of, 107–10, 176; reduced flight capacity in, 73; sympatric speciation and, 54; timing of growth and reproduction of, 102–3. See also beetles interactions among species, 30, 36; as biological controls, 126–27; complementarity in, 198–99; of Greenland’s insects, 194–95; research challenges in study of, 195; stability of populations and, 196–200, 218–19 International Biological Program, 5 International Union for Conservation of Nature (IUCN), 33, 106–10; worst invasive species list of, 125, 132, 145, 176 intestinal microbiota, 215–16 invasive species, 29, 83, 125–32, 145;

assisted migration and, 132–33, 145; biological control of, 126–27; globalization of nature and, 141–44, 223–24; lack of competitors of, 122; lack of predators of, 129–31; percentages of, 123–24; political debates on, 142–43; propagule pressure and, 124–25; red lists of, 125, 132, 145; on species-poor islands, 121–25, 196; in urban areas, 124; value of, 127–28 Invasive Species Specialist Group of IUCN, 125 Isbell, F., et al., 199 island populations, x–xi; equilibrium theory of island biogeography and, xi, 38, 118, 147–57, 167–69; vulnerability to invasive species of, 121–25, 196 island theory, xi, 38, 118, 147–57, 167–69. See also fragmented habitats Isle Royale (U.S.) wolf population, 135 Islesworh (England), 90–91 IUCN. See International Union for Conservation of Nature Janzen-Connell hypothesis, 35, 64 Järvinen, Olli, xi Journal of Researches (Darwin), 48, 53f Juramaia sinensis, 84 Jurassic period, 23–24, 46 Kankare, Maaria, 12–13 Karelian Allergy Project (KARA), 210–11 key innovations, 60–63, 75 Kheper nigroaeneus, 15 Kingston, Tim, 116 K/Pg (Cretaceous-Paleogene) boundary, 24 Krikken, Jan, 15 Kuhn, Thomas, 148 Kuussaari, Mikko, 96, 153 land-cover types, 27–28 land-use changes. See habitat conversion and loss large blue butterfly (Maculinea arion), 30

Index

large-bodied species, 84–90; habitat loss and extinction of, 47–48, 75, 86–90, 110–11, 129, 177–78; hunting and poaching of, 174, 177–78; increased biomass of, 87–88; small ancestors of, 84–86 large ground finch (Geospiza magnirostris), 53f latitudinal diversity gradient, 34–36, 41 Laurasia, 21 laurisilva, 117f, 118, 121–22 lemmings. See collared lemmings lemurs, 47–48, 55, 57–60, 75, 87f Levins, Richard, 150, 151f living dead, 164–66. See also extinction debt Living Planet Index (LPI), 105–7 local (alpha [α]) diversity, 139–42, 145 Lomborg, Bjørn, 39–40 long-tailed skua (Stercorarius longicaudus), 192 long-winged cone-head (Conocephalus discolor), 99–100 Lonsdale, Mark, 123–24 loss of biodiversity. See habitat conversion and loss Lucilia caesar, 119 Lucilia sericata, 119 MacArthur, Robert, 151f, 196f; on diversity and ecosystem stability, 200; equilibrium theory of island biogeography of, xi, 38, 147, 168, 196–97 Mace, Georgina, 201–2 macrohabitats, 31 Madagascar, xi, 43–48, 74–75; adaptive radiation in, 57–60, 75; as biodiversity hot spot, 32, 41, 44–48; deforestation in, 109; disappeared species in, 109; dung beetle species of, 13f, 46–48, 49f, 54–61, 109, 119; endemic species of, 46; endemic spiny forests of, 126–27; evolutionary history of, 46; extinctions of megafauna of, 47–48, 75, 86–90,

249

110; geological activity on, 48; human settlement of, 86, 87f; image of, 43f; invasive prickly pears in, 127–28; lemurs of, 47–48, 55, 57–60, 75, 87f; mammalian fauna of, 47; Ranomafana National Park in, 44–46; woodpecker niche in, 57, 58f maize (Zea mays), 132 Malagasy vangas, 57, 58f mammals: cat predation on, 129; evolutionary history of, 24–27; IUCN red list of, 107–9; red fox predation on, 129 managed forests, 176–77, 207–8 mangroves, 28 maps, xi; of Åland Islands, 147f; of Borneo, 1f; of La Gomera, 115f; of Greenland, 187f; of Madagascar, 43f marine biodiversity, 20–21, 41, 66 mass extinctions, 24, 57–58, 110, 173, 178 May, Robert, 196–98, 200 medium ground finch (Geospiza fortis), 53f, 68–69, 74 megadiversity, 45. See also biodiversity hot spots megafauna. See large-bodied species Mesozoic era, 23–24, 25f; in Madagascar, 58–59; mass extinctions at end of, 24, 110 metacommunity (beta [β]) diversity, 139– 42, 145 metapopulation capacity, 160–62 metapopulation ecology, 150–57, 184; equilibrium in, 163–66; extinction thresholds in, 157–66, 170, 172, 184 microbial life, 111, 205–6, 210–19 microbiomes, 19 microevolutionary changes, 70, 139 microhabitats, 31–32, 176 migrations. See movement of species Millennium Ecosystem Assessment, 202 Mitikka, Varpu, 100–101 Mittermeier, R. A., et al., 175 Moilanen, Atte, 33, 105 monarch butterfly, 157

250

Index

Mora, C., et al., 17 movement of species, 115–45; assisted migration (translocation) and, 132–39, 145; to the Azores, 121–25; genetically modified (GM) organisms and, 143– 44; globalization of nature and, 83–84, 139–45, 223–24; of La Gomera’s blowflies, 117–18; taxon cycle and, 118–19, 145. See also invasive species mute swan (Cygnus olor), 81t, 83 Mycoplasma laboratorium, 144f Myers, Norman, et al., 32–33, 45 Myrmica sabuleti, 30 Nagoya agreement. See Convention on Biological Diversity of 2010 Nanos radiation, 60, 61, 62f national parks. See protected land natural capital, 202 natural selection, 50–54, 148; adaptive radiation in, 57–60, 75; fast evolutionary changes and, 68–75; genetic changes in, 56; group selection and, 167; range expansion and, 100–101. See also generation of biodiversity nature-based solutions, 200–206 Neethlingshof Wine Estate, 200–201 Neimelä, Jari, 44–45 nematodes (roundworms), 11 Neolithic revolution, 27, 132, 158, 173, 213 New Guinea, 44 new species. See speciation Nieminen, Marko, 153 nitrogen deposition, 208 non-communicable disease, 205–6, 210–19 nonrandom communities, 198 nonthreatened species, 99, 142, 145. See also invasive species North American megafauna, 86 Northeast Greenland National Park, 33–34, 189–91, 208 northern clouded yellow butterfly (Colias hecla), 189 novel ecosystems, 206–9, 219

Oligocene period, 84 On the Origin of Species (Darwin), 148 Onthophagus genus, 60 Opuntia corallicola, 127 Ordovician period, 20–21 organic agriculture, 207 Ovaskainen, Otso, 102, 160 Paleozoic era, 20–23, 26, 173, 178 Pangaea, 22–24 paradigm shifts, 147–49 parasites, 213–14 parasitoid wasps (Cotesia melitaearum), 12– 13, 155, 194–95 Pardini, Renata, 162–64 Parmesan, Camille, 93–95 patterns of biodiversity, 32–41; in biodiversity hot spots, 32–34, 41; latitudinal diversity gradient in, 34–36, 41; species-area relationship in, 36–41 Permian period, 22–23, 26, 66 Phacophyton, 21–22 phenological changes, 102–3 phenotype, 10 phenotypic variation, 50–52 Philipson, John, 5 photosynthesis, 20 Pimm, Stuart, 39–40 Pittosporum undulatum, 122 planetary carrying capacity, 41 plantations, 176–77 plasticity, 99–103 Pleistocene epoch, 26; in Borneo, 45; dwarf elephants of, 85–86; glacial cycles of, 36; megafaunal extinctions of, 86–88 pollination, 203 poplar admiral (Limenitis populi), 100f population ecology, 5, 66, 90, 148–49, 190–91; on diversity and stability, 195–200, 218–19; island theory on, xi, 38, 118, 147–57; on population cycles, 66–68, 190–94, 218; on population stability, 190–94, 196, 218; on resilience, 191

Index

potatoes (Solanum tuberosum), 132 Pöyry, Juha, 96 prickly pears (Opuntia), 122, 125–28 probiotics, 217–18 propagule pressure, 124–25 prosauropod dinosaurs, 23 protected land, 33–34, 167–69, 202; in Finland, 34, 180–81; Nagoya agreement on, 33, 179–80; third-of-third rule of, 179–85 Proteobacteria, 214–17 provisioning services, 202–4 Puerto Rico, 39–40 Pytho kolwensis, 29–31, 101–2 radiation, 57–60, 75 randomness, 197–98 range expansion, 98–99; assisted migration in, 136–37, 145; climate debt and, 96, 99–100; flight capacity and, 100–101; in human-dominated landscapes, 99; northward shifts in, 90–98 Ranomafana National Park, 44–46 rapid evolutionary changes, 68–75 Raussi, Eljas, 80–82 Raven, Peter, 61–63 red fox (Vulpes vulpes), 129 Red Queen hypothesis, 36 red squirrel (Sciurus vulgaris), 142–43 regional (gamma [γ]) diversity, 140–42 regulating services, 202 reptiles, 107–8 resilience, 191, 202 restoration of ecosystems, 208–9 ribwort plantain (Plantago lanceolata), 152–53 rice (Oryza sativa), 132 Rigueira, D. M. G., et al., 165–66 rinderpest (cattle plague), 125 Robinson, M. A. ., 90 Roesel’s bush cricket (Metrioptera roeselii), 100 Rook, Graham, 213 Roslin, Tomas, 194–95

251

Royal Swedish Academy of Sciences, 178 Rybicki, Joel, 170 Sarawak. See Gunung Mulu saurischians, 85 sauropods, 23 Schnell, I. B., et al., 14 Shaw, Mark, 13 Shine, Richard, 130 sickle-billed vanga (Falculea palliata), 57, 58f Silurian period, 21 Sittler, Benoît, 187–90, 192–95 16S rRNA barcoding, 18 sixth mass extinction, 110–11 Skeptical Environmentalist: Measuring the Real State of the World, The (Lomborg), 39–40 SLOSS question, 168–69 small copper butterfly (Lycaena phlaeas), 189 small tree finch (Camarhynchus parvulus), 53f Smillie, C. S., et al., 17–18 Smith, M. A., et al., 13 snowy owl (Bubo scadiacus), 192 socioecological systems, 202 Söderström, Bo, 178 sour fig (Carpobrotus edulis), 122 South American megafauna, 86 spatial ecology, 118 speciation, 10, 35–36; allopatric and sympatric forms of, 54; among Darwin’s finches, 49–54, 57, 60–61, 68–70, 74; of Malagasy dung beetles, 54–61 species: definition of, 9–10; estimates of numbers of, 9–10, 15–19, 41; habitat requirements of, 2–4, 29–32; identification and DNA barcoding of, 11–14; impact of individuals on ecosystem functioning, 199; movement of, 115– 45; naming and delimiting (taxonomy) of, 10–11, 29; stability at the level of, 200. See also threatened species

252

Index

species-area relationship, 36–41; biology of species and, 39–40; habitat heterogeneity in, 37–38; population dynamics in, 38 species richness, 17–18, 105–6; in biodiversity hot spots, 32, 41; changes over time in, 82–84, 90–92; complementarity in, 198–99; evolution of, 20, 23; extinction debt and, 165–66, 175; in fragmented habitats, 170–72; impact on ecosystem functioning of, 198–99; interaction with other species and, 36; latitudinal diversity gradient and, 34–36; stability of populations and, 197–200, 218–19. See also interactions among species; stability spiked speedwell (Veronica spicata), 152–53 stability: May’s model of, 196–98; of novel ecosystems, 206–9; of populations, 190–94, 196, 218; of productivity, 200; relationship of diversity to, 195–200, 218–19 Stability and Complexity in Model Ecosystems (May), 197 Stephens Island wren, 129 stoat (Mustela erminea), 192–93 Strachan, David, 212 Structure of Scientific Revolutions (Kuhn), 148 Sundaland, 32, 45–46, 177 Suomalainen, Esko, ix–x supporting services, 202 sycamore (Acer pseudoplatanus), 143 sympatric speciation, 54

Thomas, Jeremy, 30 threatened species, 14; classifications of, 107; extinction debt of, 96, 164–66, 175, 184–85; in Finland, 141; habitat specialization among, 99; from hunting and poaching, 174, 177–78; IUCN red list of, 33, 106–10; from loss of habitat, 31; of megafauna, 88–90, 110–11, 129, 177–78; protected areas for, 33 Traill Island (Greenland), 187–91. See also Greenland translocation, 132–39, 145 Triassic period, 23 tropical forests, 28, 40–41; in Brazil’s Atlantic region, 161f, 162–66, 175–78, 181; conversion to palm oil plantations of, 83, 97, 172, 177; insect pollination in, 64; Janzen-Connell hypothesis on tree diversity in, 35, 64; nonfragmented expanses of, 174–75; species richness in, 35–36, 165–66; threatened and extinct species in, 108–9 Tropical Living Planet Index, 106f Trouvelot, Étienne Leopold, 130–31

taxon cycle, 118–19, 145 taxonomy, 10–11, 29 Temperate Living Planet Index, 106f Theory of Island Biogeography, The (MacArthur and Wilson), 38, 148–49. See also island theory third-of-third rule, 179–85 Thomas, Chris, 103–5

warbler finch (Certhidea olivacea), 53f water flea (Daphnia galeata), 70, 74 water hyacinth (Eichhornia crassipes), 123, 125 water strider (Aquarius najas), 124–25 Watson, H. C., 37–38 wheat (Triticum), 132 Whittaker, Robert, 139

UN Food and Agriculture Organization, 174 United Kingdom, 90–92, 99–100 urbanization: human immune system disorders and, 205–6, 210–19; naturebased solutions for, 204–5 vaccination, 158 viruses, 17

Index

Wilson, Edward O., 151f; equilibrium theory of island biogeography of, xi, 38, 118, 147, 168, 196–98; on the taxon cycle, 118–19 Wirta, Helena, 194–95 wolverine (Gulo gulo), 89–90, 136–38

253

wolves, 89–90; conservation debates on, 129, 137; inbreeding depression of, 135 Wytham Woods (England), 90–91 yellow crazy ant (Anoplolepis gracilipes), 131–32