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Barriers to Perception:
From a World of Interconnection to Fragmentation
Making Sense of the Cosmos
The great molecular biologist and Nobel laureate Francois Jacob has stated that the human brain has a built-in need for order. From earliest times, human beings looked out and recognized cycles, repetitive patterns in natureday following night, the seasons, tides, lunar cycles, plant succession, animal migrationthat conferred the ability to predict their recurrence, and thus people acquired a semblance of understanding of and control over the cosmic forces impinging on their lives. Gifted with an enormous brain, our distant ancestors were inquisitive, experimental, and inventive. Over time, they acquired profound insights into their immediate surroundings that had conferred survival value. No doubt they pondered many of the same cosmic questions that we ask today: How did we get here? Where are we going? What is the meaning of life? As the great French anthropologist Claude Lévi-Strauss wrote:
I see no reason why mankind should have waited until recent times to produce minds of the caliber of a Plato or an Einstein. Already over two or three hundred thousand years ago, there were probably men of similar capacity (Lévi-Strauss 1968).
From the dawn of human awareness, people accumulated insights and understanding and superstitions that were woven into their mythologies, into the fabric of their culture and identity. Anthropologists call this a “worldview”; in it, nothing exists in isolation from anything else. The rocks, the wind, the stars, the
rivers, the forests,and people are all inseparably intertwined. The past, the present, and the future form a seamless flowing continuum. In such a world, human beings often were saddled with enormous responsibility to keep it all going. They had to behave properly, say the right prayers, and follow the proper rituals and ceremonies, or the world could collapse. So the great bounty of the world of which humans partook was laden with responsibility.
From Interconnection to Fragmentation
When Francis Bacon recognized that knowledge (scientia) is power, he began a fundamental shift in how we perceive our surroundings. Science is a radically different way of seeing the world. Instead of trying to understand the whole universe, scientists focus on a part of nature, separate it from its surroundings, control everything impinging on it, measure everything within it, and thereby acquire profound insights into that isolated bit of nature. Ever since Newton described the universe as an immense clockwork mechanism, scientists have been motivated by the notion that by analyzing nature in fragments, we could eventually understand the whole by putting the pieces together as in a giant jigsaw puzzle. Reductionism is at the heart of modern science.
Physicists recognized in this century that reductionism does not work. The universe is not like a giant machine. Quantum mechanics revealed that at the most fundamental level of subatomic particles we could not know their precise location with certainty, only by statistical probability. Furthermore, as Nobel laureate Roger Sperry pointed out, properties emerge from the interactions of parts of nature that cannot be predicted on the basis of the individual properties of the parts (Sperry 1968). However, most of biology and medicine remains predicated on reductionism.
In this century, humankind has undergone massive changes with explosive speed. Harnessing the enormous power of technology, increasing in number exponentially, and accepting a global economy based on endless growth and productivity, we have become a superspecies capable as no other species has ever been of modifying the biophysical features of the planet on a geological scale. In a moment of evolutionary time, great rivers can be diverted or dammed, wetlands drained, ancient forests cleared, and air, water, and soil polluted. As technology and the economy have become the dominant elements of our lives, worldviews have been shattered, and we are no longer able to recognize the exquisite interconnections that mean that every human action has enormous repercussions throughout the biological world. As Thomas Berry says:
It's all a question of story. We are in trouble just now because we do not have a good story. We are in between stories. The old story, the account of how we fit into it, is no longer effective. Yet we have not learned the new story (Berry 1988).
The challenge we face is to rediscover those connections and recognize that we remain embedded in nature so our every action is laden with consequences
and ramifications. The difficulty is that we have barriers that blind us to those interconnections. If we are to pass through the barriers, we first have to recognize them.
Barriers to Interconnectedness
The Move to Cities.
If we look at humankind over the vast sweep of evolutionary time, one of the monumental transitions has been the change in this century in how we live. In 1900, only 16 cities had a million or more people. The largest was London, with 6.5 million. Tokyo was seventh, with 1.5 million. More than 95% of humanity lived in rural village communities. We were an agrarian species. Today, over 400 cities have a million or more people. The top 10 all have more than 11 million, and Tokyo is the largest with 26.5 million! Over half of all people now live in large urban settings, and the proportion is increasing all the time (World Almanac 1996).
Designed properly, cities could be ecologically far more benign in energy use, pollution, use of cars, and so on. But in cities, we live in a human-created habitat that is severely diminished in biological diversity. Our surroundings are dominated by one speciesusand the few plants and animals that we decide to share space with or cannot quite eliminate. In such an environment, it becomes easy to think that we are special, that our creativity has enabled us to escape the constraints of our biological nature. It is easy to forget that we remain absolutely dependent on air, water, soil, energy, and biodiversity for our survival and good health.
I have been shocked while making television programs by the number of urban children (and adults) who have little idea of the source of their food. Many do not know that vegetables grow in the “dirt” or that wieners, hamburgers, and drumsticks are the muscles of animals. They do not know where electricity, water, plastic, or glass comes from or where sewage and garbage go. Yet they are all services delivered not by the economy, but by Earth itself.
Science and Technology
As a student in the immediate post-Sputnik years, I was taught and believed that science enables us to push back the curtains of ignorance to unlock the deepest secrets of the universe and thereby to acquire the understanding that is vital to control and manage the world around us. Progress in science during this century has been spectacular; in my field of genetics, it takes my breath away to see techniques used in undergraduate laboratories that I never dreamed would be available in my lifetime. And the technological prowess that accompanies our insights is truly phenomenal. But in our understandable exuberance over our discoveries, we forget how science progresses, and we forget the extent of our ignorance.
When I graduated as a fully accredited geneticist in 1961, I thought I was pretty hot. I knew about DNA and operons and cistrons. But now when I tell
students about our 1961 ideas of chromosome structure, gene function, and regulation, they laugh in disbelief. Seen through the perspective of what we know in 1997, our hotshot ideas of 1961 are naive and far off the mark. But students are stunned when I remind them that when they have been professors for 20 years and tell their students what the hottest ideas of 1997 were, those students will also be highly amused. The very nature of science is that we know that most of our current ideas, models, and hypotheses are wrong, in need of major modification, or irrelevant. As we rush to patent and apply ideas and techniques in molecular biology, we remain ignorant about the makeup and extent of biological diversity on the planet. As E.O. Wilson has argued, the 1.6 million species identified may be less than 20% of all species on Earth (Wilson 1992). And identification of a species merely means that a biologist has classified and named a dead specimen; it does not mean that we know anything about how many individuals there are, the distribution of the species, how it interacts with other species, or anything about its basic biology. We are tearing at the intricate web of living things before we have any understanding of its components or how they interact to maintain the planet's productivity. Our basic descriptive research is imperative. Currently, the strength of scientists is description: because we know so little, we make discoveries wherever we look. But for the same reason, we cannot be prescriptive in recommending meaningful action for environmental problems that we encounter.
Rachel Carson's 1962 seminal book Silent Spring was a warning that technology, however beneficial, invariably has costs, and because our knowledge is still so limited, our capacity to anticipate or predict all consequences and costs is extremely restricted. When the insecticidal properties of some molecules were discovered, the benefits of killing insect pests were obvious. At that time, geneticists knew enough to predict that resistant mutants would quickly render an insecticide ineffective, and ecologists understood that the use of broad-spectrum insecticides made little ecological sense when fewer than one-thousandth of all insect species are pests to human beings. But no one could have anticipated the biomagnification of insecticides, because scientists discovered the phenomenon only when populations of some birds, such as eagles, decreased drastically. If we cannot anticipate the consequences of powerful new technologies and if our knowledge of the basic biological and physical makeup of Earth is minuscule, can we go on embracing new technologies with the hope that the inevitable problems that they create will be correctable by further technological innovation? I don't see how we can.
The Information Explosion
Today, as we prepare to leap into a new millennium, our leaders wax eloquent and ecstatic about the information superhighway that will take us there. But having worked as both a university professor and a host in television and radio since 1962, I can tell you that the challenge we face today is not a need for access to more information but a way of wading through information overload. The average person today is confronted with “info-glut,” and most of what passes as information is junk. On an anecdotal level, I encounter many
people who regale me with fantastic ideasBermuda triangles, extraterrestrial abductions, or scientific breakthroughsand when I ask the source of their stories, the answer is often “I read it” or “I saw it on TV.” But if people do not make a distinction between information obtained from the National Enquirer and information obtained from Scientific American or the New Scientist, or between Geraldo Rivera and The Nature of Things or Nova, then information is validated simply on the grounds that it exists.
And the nature of the electronic media is that they create a virtual reality that is better than the real thing. After all, you can now experience the kinkiest sex without fear of being caught or catching AIDS; you can lose a gunfight and live to fight again; you can have a horrendous crash in a car race and walk away. When I began my career in television, I had the great conceit to think that through this medium I would create films that would stand out like jewels, entertaining while educating the viewing public. My hope was that with good natural-history films people would grow to love and value the wonderful diversity of other species and complex ecosystems. But I have learned that our programs, too, are a form of virtual reality.
Years ago, I was on a talk show on national television, and the host asked me, “As a scientist, what do you think the world will be like in 100 years?” I responded that if human beings are still around in a century, I would hazard a guess that they would curse us for two thingsnuclear power and television. Ignoring the nuclear issue, the host did a double take and stammered, “Why television?” My response was “Bob, you asked me a very tough question. If I had responded ‘Gee, Bob, that's a hard one’ and then proceeded to think for 10 seconds, you would have cut to commercials within 3 seconds. Because television is not serious, it cannot tolerate dead air.” Now in reflecting on that exchange, I have recognized that when we assemble a nature film, we create an artifact: we send a photographer to the Arctic or the Amazon for months to get all kinds of shots-to-end-all-shots. Then in an editing room, we string them all together to produce an illusion that a tropical rain forest or the Arctic is a blur of activity. But the one ingredient that is indispensable to experience the real world is time. As telecommunication technology jams more and more information into less and less space, it delivers more jolts per second to an audience now hooked on and demanding more and more adrenaline-charged jolts. And the overriding message within the medium, even for a public-supported medium like the Canadian Broadcasting Corporation, is consume, consume, consume.
As Thomas Veltre of the New York Zoological Association has pointed out, the underlying message in television is diametrically opposed to that of environmentalism (Veltre 1990). Those of us concerned with sustainable futures look at the world on a geological time scale; we try to see the whole picture, and we urge conservation. Information conveyed by the electronic media is conveyed as a series of unrelated bullets conveying little sense of the context and history that give us an understanding of why they matter. We are assaulted by instant and fragmented factoids; and throughout, we are exhorted to buy, buy, buy.
Politics, Politicians, and Bureaucracy
Now that the ideological battle and insane arms race between the Soviet Union and the United States has ended, we revel in the apparent triumph of democracy and the efficiency of the global market. But there are enormous ecological problems that governments on any side of the political spectrum are ill equipped to handle.
To begin with, political action is predicated on the need to obtain tangible results in time for the next election, a timeframe that is too short to deal seriously with many of our most important challenges, such as species extinction and climate change. Thus, for example, in a study initiated by Prime Minister Brian Mulroney in 1988, it was found that Canada could readily achieve a 20% reduction in CO2 emission in 15 years for a net savings of $150 billion! That apparent good news has never been formally released, and nothing was ever done to implement it. That is because to achieve the CO2 reduction and save an enormous sum, an initial $74 billion has to be invested. It would be political suicide to announce such an up-front expenditure; besides, the political beneficiary of the savings would be someone else 15 years later.
A further problem that I have found in Canada is that elected politicians come primarily from two professions: business and law. In part, that reflects the fact that few people from labor, farming, homemaking, teaching, and so on can afford to run for office and lose. But this skewed representation distorts perceptions of government priorities. It is not an accident that in my country there is excessive concern with economic and jurisdictional issues. In the last session of Parliament, of more than 600 questions asked during Question Period, a mere seven were on the environment, but many concerned Quebec separation, gun control, and athletics. To compound the limited perspectives of government, when 50 members of Parliament were tested for their comprehension of scientific and technological terms and concepts, lawyers and businesspeople scored at the absolute rock bottom of the heap. Yet they will make decisions about the future of old-growth forests, climate change, ozone depletion, toxic pollution, genetic engineering, artificial intelligence, and many other issues requiring an understanding of science and technology. Clearly, the challenge is to make science and technology a fundamental part of every citizen's education.
Perhaps the greatest challenge is that political priorities are defined by a profound species chauvinism that blinds us to larger ecological principles. Once elected to office, politicians are beholden to financial backers, their party, and the electorate, apparently in descending order of importance. But children do not vote. For that matter, future generations do not vote. Yet they are the ones with the most at stake in the decisions now being made by governments. In addition, our governments' priorities are too restricted along species lines to enable them to assess ecological problems adequately. Thus, we create political boundaries that we then deploy every effort to protect. But human borders make little ecological sense to air, water, plants, and animals. Watersheds, mountaintops, ozone layer, valley bottoms, jet streams, wetlands, flyways, ocean currentsthese are the real ecological determinants of meaningful boundaries.
Nothing illustrates better the ludicrousness of our political attempts to manage nature than Pacific salmon, which currently inflame American and Canadian political rhetoric. Adults of the five species of salmon know very well where they “belong”: in the natal rivers and streams that they left 2–5 years before. But because fishing fleets intercept them at sea, we must establish an International Salmon Commission to set quotas for each nation. As the animals move from Alaska past British Columbia to Washington, Oregon, and California, fishers take them in the open sea as though the fish belong to them. Even when the fish reach their river homes in British Columbia, the federal government decrees that they fall under the Department of Indian Affairs for the aboriginal food fishery and the Department of Fisheries and Oceans for the commercial fishers, while the provincial government claims the highest revenue from sport fishing, which falls under the Department of Tourism. As the salmon move up the rivers, activities administered under the Departments of Urban Affairs, Mining, Agriculture, Forestry, and Science and Technology impinge on their fate. So human categories and priorities transform what is a single biological issue into a multiplicity of bureaucratic turf wars, thereby making it certain that the fish will never be dealt with in a way that will ensure their long-term survival and abundance.
When politicians attempt to bring “all the stakeholders” to the table to hash out a contentious issuesuch as clear-cutting old-growth forests, damming a river, or building a new nuclear facilitythe most important stakeholders are not present. Where are the children, the unborn generations, the fish, air, trees, water, or topsoil? Our minister of forests does not speak on behalf of the forest, nor the minister of agriculture on behalf of the soil, nor the minister of fisheries on behalf of the fish. Instead, we attempt to shoehorn nature into the demands of human economic, political, and social priorities, often rationalizing our actions by claiming that environmental assessments permit them. In Canada, environmental regulations are often suspended because of the need to stimulate the economy or create jobs.
In our position of dominance, we now assume that the planet is a massive resource that is ours to exploit as we wish. Thus, the 1987 UN Commission on the Environment and Development report Our Common Future suggested a goal of protecting 12% of the land in every country. Canada does not come close to that target either federally or provincially, and there has been vehement opposition to attempting to achieve it. It is assumed that human beingsone of perhaps 10–30 million specieshave the right to exploit 88% of the land!
The Global Economy
Finally, we are being sold on a kind of global economics that runs counter to what we have learned from biology in the second part of the century. In the early 1960s, geneticists began to apply the tools of molecular biology to look at the products of single genes within a species. To their amazement, they discovered that there was a tremendous amount of genetic polymorphism. Now we understand that genetic diversity is the key to a species's resilience and adaptability as the environment changes. It also appears that species diversity within ecosystems
and ecosystem diversity around the world are also critical elements in life's resilience. Humans have added another level of diversity that is important for our species's resilience: culture. Human cultures are profoundly local and have enabled groups of our species to survive and flourish in environments as different as the Arctic, grasslands, mountain ranges, steaming jungles and rain forests, and arid deserts. We even flourish in New York, Tokyo, and London, for Heaven's sake!
We have learned that when we attempt to raise large numbers of organisms of a single species or one genetic strain of animal or plant, that population becomes extremely vulnerable to pests, infection, or environmental change. Monoculture runs counter to the fundamental biological principle of maximal diversity as the key to adaptability, and we have learned that at great cost in agriculture, forestry, and fisheries. In spite of this insight, we continue to ignore the importance of maximizing diversity and thus sacrifice long-term resilience and sustainability for the sake of immediate human needs. And we are drastically reducing diversity, not just in the natural world but in human societies around the world. A single notion of economics and development has been spread throughout the globe as nations ignore the 1933 warning of the father of the International Monetary Fund and World Bank, John Maynard Keynes:
I sympathize with those who would minimize rather than maximize economic entanglement between nations. Ideas, knowledge, art, hospitality, travelthese are the things which should of their nature be international. But let goods be homespun whenever it is reasonable and conveniently possible; and above all, let finance be primarily national (Keynes 1933).
The economic monoculture that is pursued by every government in the world makes no ecological sense. Most economists externalize the very support systems of lifeair, ozone layer, topsoil, water, and biodiversity itself. Small wonder, then, that it is cheaper for a Toronto restaurant-owner to serve lamb imported from New Zealand than mutton purchased from a farm 40 km north.
Even though we live in a finite world, economics is predicated on the notion that it is not only possible but necessary to strive for steady, endless growth. It is suicidal for a single species that is increasing in numbers exponentially and that has already co-opted 40% of the net primary productivity (NPP) of the planet to demand further economic growth that will come from increasing its share of the NPP (Vitousek and others 1986).
The destructive consequences of this mindless fixation on economic growth as society's most important goal are exacerbated by the measurements of economic success. Any transaction of goods and services resulting in an exchange of money registers as an increase in GDP, whether it is the purchase of weapons to counter high crime rates, hospital and funeral costs of homicides and cigarette-smoking, or cleaning up after an oil or chemical spill. In the GDP, whether money is spent to correct social or ecological damage is irrelevant. As shown by the organization Redefining Progress, which uses an economic indicator that subtracts for such costs, the per capita GDP has more than doubled since 1950, but the Genuine Progress Indicator (GPI) rose slowly to a peak about 1970 and has been declining ever since (Cobb and others 1994).
The global economy that Keynes warned about is dominated by speculators and transnational corporations (TNCs) that are no longer tied to local populations or ecosystems. The current attempt by the OECD to gain passage of the Multilateral Agreement on Investments will open each country to the depredations of the TNCs while freeing them of responsibility to provide jobs or income for local communities or environmental protection of local ecosystems. Maximizing profit appears to be sufficient rationale for globalization of markets and economies.
Where once currency represented something tangible, increasingly it stands for itself. Today, we can buy money, sell money, and make more money without adding anything of value to society or the planet. The $1.3 trillion in daily currency speculation is bigger than most government treasuries, as we see when governments attempt without success to stop the fall in the franc and peso. This global currency flows electronically across all borders and grows far more quickly than real things. So now, as companies diversify, they can deplete one sector and then move to the remaining areas of income. The great temperate rain forests of British Columbia add “fiber” at the rate of 2–3% per year. Obviously, by cutting only 2% or 3% of the trees each year, forest companies could remove the equivalent of the entire forest in 35 or 23 years, respectively, and still have the entire forest left. But it makes no economic “sense” to take only 2% or 3% per year if a company can make 8% or 9% on its investment by clear-cutting an entire forest and putting the money in the bank. If the money is invested in forests in other countries, it might be possible to make far more; and when the forests are gone, the money can be put into fish; and when they are gone, the money can go into biotechnology or computers. So the economics drive a company to maximize profit without regard to long-term sustainability.
Reconnecting Ourselves by Setting the Bottom Line
Today, governments around the world pursue a “bottom line” that is driven by an economy that is disconnected from the real world and fundamentally destructive of local communities and local ecosystems. Global competitiveness, efficiency, debt, deficit, and profit are buzzwords defining bottom lines. But it is a bottom line that omits the fundamental basic needs of all human societies. To see what our real nonnegotiable needs are, we must first recognize and surmount the barriers to the interconnections between our activities and the rest of the world that nurtures us.
The first level of human need is defined by our biologyas animals, we have fundamental requirements, and failure to meet them adequately results in death or truncated lives. These needs are so important that our bodies have a multitude of safety devices to ensure that they are met. I am speaking, of course, of our need for clean air, clean water, clean soil, and clean energy, all of which are delivered by the planet's collective biodiversity. We need only hold our breath for 1 minute to recognize the life-giving nature of air. Deprived of air for 3 minutes, we are permanently brain-damaged; after 5 minutes, we die. From the moment of our birth to the instant of our death, we need air. We take each breath
of air deep into the most intimate moist, warm parts of our body, where we literally fuse with the air at the surfactant layer lining the alveoli of the lungs. And when we exhale, our breath rushes out and into the noses of our neighbors! We inhale atoms that once were parts of trees, birds, worms, and snakes. We inhale atoms that were once breathed in by Joan of Arc and Jesus Christ. Air is not empty space; it is a physical substance, a matrix in which we are embedded and linked to all terrestrial life on Earth.
We can make a similar case for water, which is at least 60% of our body weight. Water inflates us, enters into metabolic reactions, cools us, and delivers atoms and molecules that we need to survive. Through the hydrologic cycle, water cartwheels endlessly around the planet, purified by soil and plants, transpired back into the air by forests. Water is another glue that holds all of life together; we only have to go without a drink for a day to know how important it is.
Every bit of our nutrition that builds and renews our bodies was once alive. As botanist Martha Crouch says, our relationship with food is the most intimate relationship we have with other beings in that we take them into our bodies and incorporate them into our cells and tissues. And all of our food ultimately comes from the soil. It is remarkable then, when our absolute survival and quality of life depend on the quality of air, water, and soil, that we use them freely as dumping grounds for our toxic wastes.
As living beings, we need energy; and all the energy that we use ultimately comes from the sun. The capacity to capture that energy and send it to us in a usable form resides in Earth's great forests and ocean systems. Ultimately, it is the sum total of all of life's formsEarth's biodiversitythat somehow purifies and renews our real necessities.
We have another level of fundamental needs, for we are social animals. As the young field of ecopsychology emphasizes, we are deeply embedded in the natural world, and it is an illusion to suggest that we are truly independent beings. Whatever we do to our surroundings, we do to ourselves. Numerous studies show that as social animals, we need the early experience of love for the full development of our potential. Studies done in Romania after Ceaucescu's fall indicate that children raised in orphanages and provided with food, clothing, and shelter but never held or cuddled grow up physically and psychically damaged (Johnson and others 1992). The best way to ensure the love that humanizes us is to provide the opportunity for stable family relationships, and that is generally ensured by strong local communities. Employment is a fundamental need, and numerous scientific studies document the medical, physical, and psychological problems that arise from chronic unemployment or unexpected loss of a job (Lin and others 1995). We must be able to ensure justice and security to avoid the problems that can result from their absence. These are the fundamental social needs that must be met for long-term sustainable futures.
Finally, we are spiritual animals that need to be connected to the natural world. E.O. Wilson has called our need to be with other species biophilia, an innate requirement (Wilson 1984). As mortal beings, we are sustained by the knowledge that our kind will live on and that nature itself will continue to thrive after our individual deaths.
I suggest that by re-examining the fundamental needs on which a truly sustainable future can be built, we will also rediscover the incredible interconnections that once held people together in their surroundings.
Berry T. 1988. The dream of the Earth. San Francisco CA: Sierra Club Bk.
Carson R. 1962. Silent spring. Boston MA: Houghton Mifflin.
Cobb C, Halsted T. 1994. The genuine progress indicator: summary of data and methodology. San Francisco CA: Redefining Progress Inst.
Johnson DE, Miller LC, Iverson S, Thomas W, Franchino B, Dole K, Kiernan MT, Georgieff MK, Hostetter MK. 1992. The health of children adopted from Romania. J Amer Med Asso 268:3446–51.
Keynes JM. 1933. National self-sufficiency. In: Moggeridge D (ed). The collected writings of John Maynard Keynes Vol 21. London UK: Cambridge Univ Pr.
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Lin RL, Shah CP, Svoboda TJ. 1995. The impact of unemployment on health: a review of the evidence. Can Med Asso J 153:529–40.
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Wilson EO. 1984. Biophilia: the human bond with other species. Cambridge MA: Harvard Univ Pr.
Wilson EO. 1992. The diversity of life. New York NY: WW Norton.
The Creation of Biodiversity
The term biodiversity, short for biological diversity, was introduced by the National Research Council staff at the first National Forum on BioDiversity, held in Washington in September 1986; and it gained rapid global currency after the publication of the forum proceedings in 1988. Biodiversity means, in simplest terms, the variety of life found in the Creation; it is the entirety of life on the planet.
Biologists rescue this conception from vacuity by analyzing biodiversity at different levels of organization, from biosphere downward to gene, and integrating the information to address the fundamental questions of its breadth and origin. More recently, with growing alarm, they have widened their focus to include the causes of the accelerating decline of biodiversity in the human-saturated environment. The first process, creation, is the concern of evolutionary theory; the second is the subject of the new discipline of conservation biology. I will now address the first process.
Researchers have found it most useful to stress diversity at just three levels of biological organization, namely, ecosystem, species, and gene. An ecosystem is a local community of species organisms plus their physical environment. Familiar examples are a New England pond, an old-growth forest in Oregon, and a deepsea thermal vent off the Pacific coast. Although broad types of ecosystems, such as old-growth conifer forests and thermal vents, can be roughly defined by properties they have in common, no two particular ecosystems belonging to a given type are ever exactly alike, either in their species composition or in their physical environment. Throughout the world, individual ecosystems are highly endangered or have disappeared. When a forest is cut, others of the same ecosystem type can
persist nearby, but its unique properties have vanished forever. Moreover, many ecosystems contain endemic species, native to that place and environment and found nowhere else. A threatened individual ecosystem or aggregate of ecosystems with many endemic species is called a “hot spot.” The rain forest of Kauai is a hot spot; and because so many other kinds of ecosystems on Kauai and the surrounding islands contain threatened endemic species, all of Hawaii is justifiably called a hot spot.
Because ecosystems are difficult to classify and even in many cases to delimit geographically, they are seldom used in quantitative studies of biodiversity. The unit of choice is the species; species are relatively easy to describe and have been the focus of more than 2 centuries of research in classification and biogeography. The traditional definition of the species is the one given in the “biological species concept”: a population or series of populations of individuals capable of freely interbreeding with one another under natural conditionsin short, a closed gene pool. The occurrence of an occasional hybrid is not enough to combine two species into one under this definition; only free interbreeding can do that. Also, the ready production of hybrids in zoos and botanical gardensfor example, between lions and tigersdoes not suffice. Gene flow must occur under natural conditions, which apparently never occurred between lions and tigers where they coexisted in the past.
The biological species concept works very well for most kinds of animals and for some plants, such as the orchids, but it has serious problems. In a large percentage of cases, there is no way to know whether two populations that occupy different geographic ranges would interbreed if somehow they met under natural conditions. A population of birds on Oahu, for example, cannot be judged with certainty against a somewhat different population on Kauai. The usual taxonomic solution to the dilemma under the biological species concept is to classify the two populations as subspecies, or geographic races, of the same species.
Yet another problem with the biological species concept is its irrelevance to the vast assemblage of life forms that do not reproduce sexuallyor else do so rarely enough to reduce sexuality to marginal importance in the life cycle. Thus bacteria, which with the asexual Archaea are both the most primitive and the most numerous organisms on Earth, cannot be classified by the biological species concept. A bacterial species is instead defined as a lineage with 30% or more difference from other lineages in DNA base pairs or else subjectively different enough in traits of biochemistry and structure to justify such recognition. As a result, and with insufficient technology to impose even these loose criteria, no one knows to within a factor of less than 100 how many bacterial species exist on the planet.
Understandable dissatisfaction with the biological species concept has encouraged the devising of an alternative definition, that of the phylogenetic species. In this view, the most meaningful species is a distinctive population with a monophyletic lineagein other words, derived from a single ancestral species. It is of little concern in this view if the populations have indeterminate breeding potential with other populations. As long as the population comprises individuals of the same coherent lineage that are distinguishable to a subjectively agreed-on degree from that of other populations, it can be ranked as a species.
The advantage of the biological species concept is its recognition that closed gene pools are entities that have for the most part been irreversibly launched on an independent course of evolution by mutation and recombination. Given enough time, and without regression by hybridization, species that are at first barely distinguishable are destined to become very distinguishable. The advantage of the phylogenetic species concept is that it reflects rigorously the history of groups of related species without reference to their hypothesized future.
The two cross-cutting criteria, breeding and phylogenetic, can be joined to create a synthetic species concept as follows. A sexual species is a population that is both reproductively isolated and monophyletic. Suppose that a monophyletic sexual population is geographically isolated, so that its reproductive status vis-à-vis similar populations is indecipherable. It can be called a species if it is markedly distinct, or a subspecies if only slightly distinct.
What the new emphasis on molecular markers and phylogenetic analysis comes down to is, I believe, the prospect of increasing the number of formally recognized species through ever finer analyses of the phylogeny of populations, especially such analyses based on DNA sequencing. More subspecies, once they have been found to have substantial differences that are concordant across their ranges, will be raised to species rank. And more sibling species, which are hard to detect with conventional anatomical characters, will be recognized and named. The new emphasis does not, however, in my opinion represent a fundamental shift away from the species concept already used by most practicing taxonomists. As a rule, they have embraced the concepts of both reproductive isolation and monophyly while recognizing as guesswork the assignment of reproductive relationships among closely related but geographically isolated populations.
The current trend of systematic theory is toward a higher degree of objectivity and consensus than existed in the past. A synthetic, truly biological species concept, providing considerable information about each genetically distinguishable population, seems attainable. This aim is of central importance in ecology and conservation biology. How species are delimited and classified determines the number recognized, as well as the number of genera and other higher categories into which they can be defensibly grouped, and hence the magnitude of both local and global biodiversity. It affects the evaluation of the status of individual populations in conservation planning, that is, whether the populations are ranked as species, subspecies, or neither. And finally, the refined species concept conforms more closely to the emerging picture of how biodiversity is created.
Biodiversity is the product of two complementary processes of evolution. The first is vertical evolution of individual populations by changes in chromosome composition and gene frequency. During the process, biodiversity at the level of this hereditary unit grows or declines. But the number of species, the next level up, does not necessarily change as a result. The second evolutionary process, then, is the multiplication of species, often called speciation. In the course of vertical evolution, some species split into two or more daughter species; others do not.
Virtually all biologists closely familiar with the details of vertical evolution give natural selection the dominant role in evolution. In simplest terms, it begins when
different forms of the same genes, or alleles, originate by mutations, which are random changes in the long sequences of DNA that compose the genes. In addition to such point-by-point scrambling of the DNA, new mixes of alleles are created by the recombining processes of sexual reproduction. Other forms of mutation occur when entire chromosomes, the carriers of the genes, are duplicated, deleted, broken, fused, or otherwise reconfigured. The mutations, genic and chromosomal, that enhance survival and reproduction of the carrier organisms spread through the population.
The ones that do not enhance fitness fall to very low frequencies or disappear altogether. Chance mutations are the raw material of evolution. Environmental challenge, deciding which mutants and their combinations will survive and reproduce, molds the population from this protean genetic clay.
Although natural selection has the commanding creative role, another force must be mentioned in any account of evolution. By chance alone, substitutions occur through long stretches of time in some of the genes. The continuity of random change is often smooth enough to measure the age of different evolving lines of organisms. But this genetic drift, as it is called, while altering the diversity of genes, adds little to evolution at the level of cells, organisms, and populations. The reason is that the mutants involved in drift must be neutral, or nearly so, in the crucible of natural selection; in other words, they can have little or no effect on the details of higher biological organization on which organisms depend for survival and reproduction.
Driven by natural selection, some species break into daughter species. By the criterion of reproductive isolation, species multiply when populations acquire genetic differences that interfere with mating or the healthy growth of hybrid offspring. These differences are called intrinsic isolating mechanisms. They affect various parts of the life cycle concerned with sexual reproduction, such as differences between populations in times or places of mating, in courtship and mating procedures, and in the developmental physiology of offspring. They can occur singly or in any combination, depending on the biological nature of the species and vagaries of natural selection affecting its evolution.
The classic model of species formation is geographic speciation. Its principal steps, which have been richly documented, are the following. A single population of interbreeding individuals is split into two or more populations by a geographic barrier. Because the barrier is not part of the genomes of the populations, it can consist of almost any feature of the physical environment. It can be the drying of a mesa when the climate enters an arid phase, causing the forest that once covered it to break into fragments sheltered by scattered canyons. It can be the straits that separate two islands of an archipelago. A bird species might only rarely cross this permanent water barrier, but when the event does occur, individuals from one island are able to invade the other island, where the colonists form a population almost entirely isolated from the source population.
As the two populations separated by geographic barriers of whatever nature diverge, they progress from being genetically identical or nearly so to slightly or moderately different, at which point they can be called subspeciesor, meaning the same thing in this context, geographic races. At this stage, the systematist
who emphasizes interbreeding capacity says, “The differences are worthy of recognition but not strong enough or involved enough with reproductive traits to call the populations species. If the diagnostic traits were stronger and especially of this nature, I'd call them species.” Another systematist, concerned more with phylogenetic criteria, might respond, “All right, but I'll call them species if there are multiple and well-marked diagnostic characters throughout the population, and if the species with which they are compared share an immediate common ancestor and possess their own well-marked and consistent traits. I am not so interested in trying to predict their future.”
Even with such clarification, however, the distinctions between subspecies and species are filled with residual ambiguities difficult to explain to impatient students or members of Congress. Here are several:
• A subspecies, or geographic race, can contain genes and traits that are even more distinctive than those of otherwise similar reproductively isolated species, yet not be reproductively isolated or coherent enough to meet the criteria of a phylogenetic species.
• Two species can be separated by numerous genetic differences that nevertheless produce no outward traits easily discerned by investigators. Examples include odors used in communication and internally hidden physiological processes. These “sibling species,” even though important elements of biodiversity, are nevertheless consistently undercounted.
• Some species, especially on continents or large islands, are broken into numerous local populations that vary genetically from one another. The temptation exists to recognize many subspecies among the populations, but two outstanding difficulties are often encountered in such cases. First, the geographic limits of each population are often difficult, if not impossible, to define. Second, the traits typically vary discordantly. To take an imaginary but realistic example of discordance, size might decrease from north to south, color from east to west, food preference from northwest to southeast, and so on, indefinitely. The number of geographic character lines that can be drawn and hence the number of subspecies recognized in such discordantly varied species depend on which traits are chosen to follow them. Still, in spite of this difficulty, a large percentage of species comprise local populations that can be easily delimited and whose diagnostic traits are concordant enough to justify subspecific or, by stress on the phylogenetic criterion, specific status.
• To add to the many complications inherent in geographic differentiation, species can also multiply in the absence of geographic barriers. Almost half of living plant species and a smaller number of animal species have arisen by polyploidy, the multiplication of entire chromosome sets. The idea of polyploidy can be quickly grasped as follows. If the number of chromosomes in the egg or sperm of a nonpolyploid organism is N (haploid), then the number in the fertilized egg and ensuing organism is 2N (diploid). In a polyploid, the number in the fertilized egg and ensuing polyploid organism is 3N (triploid), or 4N (tetraploid), and so on. A polyploid with 4N chromosomes can in some cases breed with its 2N ancestor, but the hybrid offspring, which carries 3N chromosomes in each cell, is ordinarily
unable to complete the steps of meiosis and hence to produce viable sex cells of its own. As a result, the 2N ancestor and its 4N derivative are distinct species. The splitting of one species into two species in this case occurred across only two generationsa near instant in evolutionary time. A variation of the process can occur when two species create a hybrid that is also a polyploid. With two of each kind of chromosome thus provisioned in each cell of the organism, the chromosomes can pair off with exact equivalents in the first meiotic division, permitting the production of normal sex cells. The polyploid hybrids can as a result breed successfully with one another, but not with their diploid parents; so they are established as a new, reproductively isolated species.
Another form of sympatric speciation, or species multiplication in the absence of geographic barriers, is through host races. The process is hard to detect and harder to prove, but it might be far more important in nature than previously appreciated. It unfolds when a species of say, an insect is specialized to feed on the leaves or fruit of one species of tree, a common situation in nature. It also mates exclusively on this same host plant. A few individuals, either because they are mutants in food preference or because they make an error in plant selection (and then become imprinted on the wrong tree species), move to an alternative host, where they proceed to feed and mate in isolation. As a result, two populations coexist in the same locality. At first, when the differences among them are slight, they are legitimately called host races, or ecological subspecies. But as they diverge genetically, and especially if the host preferences have a hereditary basis, they are classifiable as distinct species.
No one at this time can confidently evaluate the prevalence of sympatric speciation by host races or other highly local splitting of populations. But given that insect species alone number in the millions, many of them specialized as herbivores on plants or as inhabitants of microhabitats, the process might in time prove to be one of the most important in the origin of biodiversity.
As new species originatesometimes across only two generations, sometimes during a period of hundreds or thousands of generationsother species die. Over large geographic areas and spans of time, the balance of birth and death maintains a roughly equilibrial number of species in major groups, such as birds, ants, conifers, and mosses. The number appears to be a complex correlate of factors summarized by the acronym ESA, not for the Endangered Species Act or the Ecological Society of America, but for Energy, Stability, and Area. In general, the greater the amount of energy available to the ecosystems, the larger the number of species; thus, high levels exist in the energy-rich coral reefs worldwide and the great tropical moist forests of South America, Africa, and Asia. The more environmental stability, as in the tropical forests and bottoms of the oceans, the greater the number. And, finally, the larger the area, the more species that can be sustained within it.
The role of area in particular can be described by the following broad rule: the number of species occurring in physically well-demarcated habitatssuch as islands of an archipelago, patches of woodland in a fragmented forest, or clusters of lakesvaries from the sixth to the third root of the area of the habitats. The
exact value varies with the kinds of habitat and organisms studied and the part of the world in which they occur. A common central value is the fourth root, which translates to an easily recalled rule of thumb: a 10-fold increase in area results in a doubling of the number of species.
Where the ESA factors combine, an astonishing number of species have typically accumulated. The greatest biodiversity overall in the world appears to occur in the upper Amazon Basin, which is notably high in all the ESA factors. For example, the largest number of butterfly species in the world observed at a single locality is 1,300, recorded within 3,925 hectares of mostly lowland rain forest at Pakitza, Parque Nacional del Manu, Peru, by Robbins and co-workers (1996). By comparison, only 380 species are known from all of western Europe (Higgins and Riley 1970). Similarly, the world record for ants is 365 species, collected within only 8 hectares of lowland rain forest at Cuzco Amazónico, also in Amazonian Peru, by Stefan Cover and John Tobin (personal communication). That diversity can be instructively compared with the 555 species found in all of North America (Bolton 1995).
The assembly of biodiversity at the level of ecosystems encompasses two complementary principles of organic evolution. The first is adaptive radiation, the expansion of multiplying species from individual stocks into niches available to them. The second is convergent evolution, the increasing similarity in anatomy, physiology, or behavior, singly or in combination (but not in the underlying genetic codes), of radiating groups found in different parts of the world.
The Hawaiian archipelago, the most isolated islands on Earth, are appropriately cited as a natural laboratory that displays the two complementary principles with exceptional clarity. Its roughly 8,000 known endemic land and freshwater species (Eldredge and Miller 1995) have been derived from only a few hundred ancestral species that managed to cross the immense barrier of the Pacific Ocean from continents and islands on both sides. Many of the colonists, arriving over a period of several million years, found an array of major niches open that were closed by competitors in other parts of the world. Among the insects that converged dramatically to adaptive types in other places are geometrid moths whose caterpillars abandoned herbivory to become ambush predators of other insects and a dragonfly whose nymphs have left freshwater streams to forage on land. One lineage of ducks, the moa-nalos, now extinct, evolved into large flightless forms with tortoise-like bills. The fullest and best-known radiation among animals is in the Hawaiian honeycreepers of the family Drepanidinae, whose 23 species (living and recently extinct) were derived from a single ancestral fringillid bird species. In anatomy and behavior, they have variously filled the niches of warblers, woodpeckers, finches, nectar-feeding sunbirds, and parrots. The most striking example among plants is in the tarweeds of the sunflower family Asteraceae, whose numerous species vary from low, herbaceous mats to shrubs and trees, to the spectacular silversword of Maui's Haleakala Crater.
It is by countless such radiations and exchanges of species among their own evolutionary headquarters that the ecosystems have assembled. On a grand scale, much of the history of life can be viewed as a succession of adaptive radiations during which major groups displaced previous assemblages or were able to spread
into wholly new adaptive zones made possible by the increasing complexity of preexisting ecosystems. Life has always expanded to fill the space and use the energy offered to it. The glory of this creative process is the biosphere, billions of years old, over which humanity has lately taken command. The tragedy is that we are thoughtlessly tearing it down before we fully understand its origin, how it is sustained, and the essential role that it plays in human welfare.
Because this essay is a primer of a broad array of topics, it is appropriate to recommend three general texts, of the many available, for a more detailed introduction:
Raven PH, Evert RF, Eichhorn SE. 1999. Biology of plants, 6th ed., New York NY: Worth Publ. Futuyma DJ. 1997. Evolutionary biology, 3rd ed., Sunderland MA: Sinauer Assoc. Wilson EO. 1992. The diversity of life. Cambridge MA: Harvard Univ. Pr.
Several specialized citations not covered in these general works are given below.
Bolton B. 1995. A taxonomic and zoogeographical census of the extant ant taxa (Hymenoptera: Formiddae). J Nat Hist 29:1037–56.
Eldredge LG, Miller SE. 1995. How many species are there in Hawaii? Bishop Mus Occas Pap 41:1–18.
Higgins LG, Riley ND. 1970. A field guide to the butterflies of Britain and Europe. Boston MA: Houghton Mifflin.
Robbins RK, Lamas G, Mielke OHH, Harvey DJ, Casagrande M. 1996. Taxonomic composition and ecological structure of the species-rich butterfly community at Pakitza, Parque Nacional del Manu, Perú. In: Wilson DE, Sandoval A (eds). Manu: the biodiversity of Southeastern Peru. Washington DC: Smithsonian Inst Pr. p 217–52.
The Dimensions of Life on Earth
This paper aims to give estimates of the numbers of living and distinct species of eukaryotes that have been named and recorded. As will be seen, the factual numbers are accurate only to within 10% or more, mainly because we lack a well-documented and synoptic catalog of all named species. Next, I survey estimates of the total numbers of eukaryotic species on Earth today. Here, our ignorance is such that defensible estimates have a range of a factor of over 100from a few million to 100 million or more. I conclude by asking what fraction of species that have ever lived on Earth are with us today and outlining an approach to an answer that avoids the huge uncertainties in absolute species numbers.
On the one hand, this paper builds on Wilson's (this volume) scene-setting account of the evolutionary and ecological causes and consequences of biological diversity, seeking to quantify the resulting abundance of life forms. On the other hand, the concluding part of the paper prepares the ground for Pimm and Brooks's (this volume) assessment of likely future rates and patterns of extinction.
Throughout the paper, the focus is on species, and eukaryotic species at that.
Why species? As discussed elsewhere (Collar 1997; Groombridge 1992; Heywood 1995; May 1994a; Wilson 1992), biological diversity exists on many levels, from the genetic diversity in local populations of a species or between geographically distinct populations of a species, all the way up to communities or ecosystems. Any level can be predominant, depending on the questions being asked. At the most basic level, genetic diversity in a species is the raw stuff on which
evolutionary processes work their wonders. At the opposite extreme, “we do not have to embrace the wilder poetic flights of Gaians to acknowledge that ecosystems can usefully be regarded as supraorganisms for many discussions of the way biological and physical processes entwine to maintain the biosphere as a place where life can flourish” (May 1994a). A different kind of stratification is oriented toward taxonomy, from races and subspecies through genera and families to phyla and kingdoms.
Given the variety of ways of measuring the dimensions of life on Earth, I nevertheless believe that species are usually the best place to begin. For one thing, there is the practical reason that effective conservation action needs public support, and the public identifies more easily with tangible biological species than with abstractions such as gene pools or ecosystems. For another thing, although it is undoubtedly more important to preserve habitats and ecosystems than individual species, the choices that we will increasingly be forced to make are likely ultimately to be species-based (Claridge and others 1997; Wilcove 1994).
Why eukaryotic species? A molecular biologist could justifiably argue that plants, animals and fungi represent only a recently diversified tip of an evolutionary tree whose main flowering is among bacteria and archaea. But what is meant by species among bacteria and the like is vastly different from what is meant among plants and animals (see, for example, Bisby and Coddington 1995; Vane-Wright 1992). For instance, different strains of what is currently classified as a single bacterial species, Legionella pneumophila, have nucleotide-sequence homologies (as revealed by DNA hybridization) of less than 50%; this is as large as the characteristic genetic distance between mammals and fishes (Selander 1985). Relatively easy exchange of genetic material among different “species” of such microorganisms means, I think, that basic notions about what constitutes a species are necessarily different between animals and bacteria. That holds even more strongly for viral species, many of which are best regarded as “quasispecies swarms” (Eigen and Schuster 1977; Nowak 1992). Of course, even within well-studied groups of plants and animals, some workers recognize many more species than others, especially when the organisms in question can reproduce asexually; thus, some taxonomists recognize around 200 species of the parthenogenetic British blackberry, others see only around 20, and a “lumping” invertebrate taxonomist might concede only two or three.
Be this as it may, in what follows I restrict attention to numbers of distinct species of living eukaryotic organisms. In academic fashion, I begin by dwelling on a range of problems before turning to group-by-group assessments of known and suspected total numbers.
Numbers of Named Species
Patterns of Effort
From Linnaeus's time to our own, it has often been noted that some groups have received much more taxonomic attention than others (see, for example, Hawksworth 1997). One indication of this is the rates at which species are being
recorded. Over the span 1978–1987, an average of five new species of birds was described each year, representing an annual average growth rate in the bird species list of 0.05%. For insects, nematodes, and fungi, the corresponding annual averages for newly added species were 7,222, 364, and 1,700, respectively, representing species-list growth rates of 0.76%, 2.4%, and 2.4% (Hammond 1992, table 4.6). From an academic dean's view, the typical bird or mammal species gets about 1.0 scientific paper per year, other vertebrate species get about 0.5 paper per year, and the average invertebrate species is lucky to average 0.1 paper per year and more likely to get 0.01 (May 1988, table 3).
That pattern of attention among groups reflects the distribution of the taxonomic workforce, as summarized in table 1 (condensed from Gaston and May 1992). Taking a very conservative estimate of 3 million invertebrate species as the global total, table 1 shows that the ratio of taxonomists to species is an order of magnitude greater for vertebrates than for plants and two orders of magnitude greater for vertebrates than for invertebrates. This is no way to run a business. It reflects intellectual fashions and bears no relation to the relative importance of taxa either in the sweep of the evolutionary story or in the delivery of ecosystem services.
Reorganizing our priorities rapidly, to learn more about the little things that arguably run a lot of the natural world, will not be easy. Fascination with the furries and featheries goes deep: in the UK, the Royal Society for the Protection of Birds (RSPB) has almost 1 million members; the analogous society for plants (the Botanical Society of the British Isles) has around 10,000; and there is no corresponding society to express affection for nematodes.
Problems with Synonyms
Despite the gross incompleteness of, and biases in, the taxonomic record, a colleague in the physical sciences might reasonably expect that we could at least say how many living species have been named and recorded. It is a simple fact, ascertainable in principle. But the lack of synoptic databases for most groups means that such factual totals are not generally available. Hence the embarrassing situation that “the figures for described species given, even in high profile re-
ports and ostensibly authoritative works, vary considerably (for examples see Gaston 1991a,b; Hammond 1992, 1995b), and are almost always, and notably with respect to some of the larger invertebrate animal groups, out-of-date, due to delays in cataloguing” (Hammond 1995a).
This is one reason why I cannot provide a crisp and definitive table of recorded species numbers, group by group. There is, however, a more fundamental and nastier problem. The count of recorded species is inflated by synonyms: single species have been independently and differently named and recorded on two or more occasions. Given, for example, that some 40% of all named beetle species are known from only one geographic site, and that no intercollated database exists, the synonymy problem should not surprise us.
For the better-studied groupssuch as birds, mammals and many plant familiessynonyms have usually been fairly thoroughly resolved. In contrast, among the more poorly known groups, which tend to contain many more species than the better-known ones, synonymy rates can run high. Hammond (1995a) notes that in 1979 some 2,116 beetle species were newly described and 426 named beetle species were recognized as synonymous with others; thus the net gain in known beetle species in 1979 was roughly 80% of the number newly described. Gaston (1991a) surveyed known synonymy rates for the four major insect ordersColeoptera, Lepidoptera, Hymenoptera, and Dipterafor the period 1986–1989; he found that the rates varied, but averaged about one-third of the number of species newly described over the same period. Another study of particular groups, mainly insects, found typical synonymy rates of around 20% with some groups exceeding 50% (Gaston and Mound 1993). Bland Findlay (Natural Environmental Research Council, Lake Windermere, UK, pers. comm.) and collaborators have focused on six recent taxonomic revisions of six species-rich genera of ciliates and have found that 584 previously recognized species were reduced to 293 when synonyms were removed; this represents a synonymy rate of 50%. The recently published checklist of Nearctic insects (Poole and Gentili 1996) recognizes 95,694 distinct species but acknowledges 152,079 species names, for an overall rate of resolved synonymy of 37%; the rates in individual orders range from 49% for lepidoptera to around 20% for mecoptera, megaloptera, and trichoptera.
Moreover, any such assessment of synonymy rates must be a lower limit; other synonyms are yet to be uncovered or to accumulate in new work. Solow and others (1995) have made a start on estimating the true rate of synonymy. They used the records of thrip (Thysanoptera) species as published each year since 1901. Some 197 workers have named thrip species (and 28 of these have had all their names relegated to synonymy). Of the total of 6,112 thrip names, 1,326 are currently recognized as synonyms, for an observed synonymy rate of 22%. We also know what proportion of the names published each year are known to be synonyms. Not surprisingly, there is a much higher rate among the names assigned in earlier years; it takes time to uncover aliases. Using this information, Solow and others fitted a probability distribution to the time taken to uncover a synonym and then estimated how many more have yet to be revealed. They conclude that the true proportion of synonyms is around 39%, roughly double the observed rate. They also estimate that on the average it takes around 43 years to
identify a synonym. Although there can be some technical quibbles about the details of the calculation (May and Nee 1995), it is clearly indicative.
A more serious question concerns the extent to which the thrip data are representative of other groups. Altaba (1996) has noted the great variations in synonymy rates among mollusk taxa in Mediterranean regions: for melanopsids (relatively large freshwater snails), recent work suggests an observed synonymy rate of roughly 40%; for unionoids (freshwater mussels), he estimates a rate of around 93%; but for hydrobiids (minute snails, often living in springs and subterranean waters), he estimates a rate of 5% or less.
Even for mammals, things are not really as simple as suggested above. Using the database for Neotropical mammals that he is compiling, Patterson (1996) notes that three-fourths of the names for all species recognized since 1980 had earlier been regarded as synonyms. Over that period, the number of species resurrected from earlier relegation to synonymy (173) was three times the number newly banished as synonyms (62) or the number newly described (60). These reappraisals derive more from changing emphases in taxonomic research (in particular, the relatively recent shift toward phylogenetic concepts to replace earlier biological species concepts) than from the independent rediscoveries that account for many insect synonyms. But the complexities that they introduce into the listing of numbers of distinct species are nonetheless real.
In summary, even if we could pull together all the catalogs scattered among museums and other institutions around the world, an accurate assessment of the total number of distinct species currently named and recorded would elude us. The synonymy problem varies from group to group, and it tends to be worst for the most species-rich groups. In light of the work of Solow and others, it could be argued that an overall discount factor of something like 20% might be applied to existing species lists (Hammond 1992, 1995a). But other people are entitled to other guesses.
Numbers of Named and Distinct Eukaryotic Species
The list of numbers of described and extant species in table 2 is derived largely from the thorough work of Hammond (1992, 1995a), itself based on wide consultation. Hammond's estimates were around 1.7 million in 1992 and around 1.74 million in 1995; the largest components of the latter assessment are listed in table 2. Hammond (1995a) also estimated that a total of “13,000 or so” new species are described each year, and that this number had been strikingly constant over the preceding decades. Allowing for synonyms, I would place the true rate of addition of new and distinct species at around 10,000 per year (which roughly reconciles Hammond's 1992 and 1995 estimates).
The right-hand column in table 2 gives my own current assessment, modified in the light of discussion at, and immediately arising from, the meeting on which this volume is based. For some of the groups synonymy might not pose a problem, but it undoubtedly does for the species-rich groups that dominate the overall number (particularly insects, but also crustaceans, nematodes, arachnids, and fungi). My estimated total count of distinct living species is 1.5 million, and this number probably contains an uncertainty of about 10% or so.
The estimate of 1.5 million is essentially identical with Wilson's (1988) widely cited figure of 1.4 million (based mainly on expert opinions for various groups), if we update to allow for adding around 10,000 new and distinct species each year over the last decade.
Before commenting on some individual entries in the right-hand column of table 2, it is helpful to draw back and consider the more coarsely grained picture presented in table 3 of metazoan species in different phyla, subdivided by broad habitat (marine, freshwater, symbiotic, and terrestrial). Here we see order-of-magnitude assessments of species numbers, which highlight how any overall estimate of recorded species diversity is dominated by a few groups. Terrestrial arthropod species are roughly ten times more numerous than any other group, and benthic arthropods and annelids, with mollusks and platyhelminths, account for most of the remaining animal species. The table also underlines how diversity measured by species numbers is very different from diversity in terms of basic body plans (reflected at the phylum level). Although more than 85% of all recorded species are terrestrial (Barnes 1989; Briggs 1994), phyla are predominantly aquatic: 32 of 33 are found in the sea (21 are exclusively marine), whereas only 12 are found on land (only one exclusively).
Before presenting some telegraphic comments on table 2, I emphasize that (with a few exceptions for arithmetic clarity) I have given all numbers to only two significant figures. In some cases, the second digit is reasonably secure (for example, the number of distinct plant species currently described is probably 270,000 rather than 280,000 or 260,000), but in other casesespecially the overwhelmingly important insectseven the first digit is unsure. Systematists and conservation biologists have an unfortunate tendency to present estimates that convey a mislead-
ing sense of precision; for example, Wilson's actual estimate in 1988 was 1,392,485 named species rather than 1.4 million. This should be avoided.
Table 2 shows that my assessment of 1.5 million species differs from Hammond's (1995a) 1.74 million by virtue of my estimating 0.23 million fewer insect species, and 0.01 million fewer nematode species. Hammond's 950,000 insect species
comprise 400,000 beetle species, 150,000 lepidopteran species, 130,000 hymenopteran species, 120,000 dipteran species, and 150,000 other species. Although Hammond gives a good discussion of the problems of synonymy (referred to above), I believe that he does not adequately discount the totals. My suggested 720,000 insect species in table 2 are 300,000 beetles; 300,000 lepidopteran, hymenopteran, and dipteran species combined; and 120,000 other species. This accords roughly with Nielsen's (Australian National Insect Collection, CSIRO, Canberra, Australia, pers. comm.) estimate of around 750,000 insect species and brings the present estimate into accord with Wilson's (1988) earlier one. I have reduced the nematode species total from 25,000 to 15,000 on the basis of discussions and other published estimates.
My other numbers in table 2 agree with Hammond's (1995a) estimates. Most seem reasonably agreed on among the relevant experts. The roughly 80,000 species of Protoctista (protozoans and algae) are mainly in Bacillariophyta (12,000), Foraminifera (10,000), Gamophyta (10,000), Rhodophyta (5,000), Actinopoda (6,000), Ciliophora (8,000), and Sporozoa (5,000). The estimated 270,000 plant species (embryophytes) are mainly in Spermatophyta (240,000), Pteridophytes (10,000), and mosses and liverworts (16,000). The estimate of 70,000 distinct species of mollusks strikes me as having an uncertainty of about 10%. The same is true for the estimate of 75,000 species of arachnids; an estimate of 36,000 distinct spider species is fairly sure, but the very rough estimate of 40,000 distinct mite species might have an uncertainty of 10% or more.
Numbers of Species Extant Today
The true total of extant species, as distinct from those we have named and recorded, is hugely uncertain. Table 4 shows Hammond's (1995a) excellent summary of the range of estimates of the possible totals in the major groups of eukaryotes and his own “working figures”.
My current estimate is presented in the right-hand column of table 4. The most important discrepancies between my best guesses and Hammond's are in my lower numbers for fungi (1 million fewer species) and for insects (4 million fewer). There are other minor differences, but those two account for essentially all the difference between Hammond's estimate of roughly 12 million and mine of roughly 7 million species. Hammond's (1995a, table 3.1.2) estimated total was actually 13.6 million, but this included 1.4 million bacteria and viruses.
Before briefly discussing table 4, I emphasize the great uncertainty in many of its numbers. The overall range of estimates runs from 3 million to more than 100 million species, with a conservative estimate of the likely range being 5–15 million eukaryotic species. Hammond's 12.2 million best guess is remarkably close to Briggs's (1994) independent estimate of 12.3 million, although they differ considerably in detail (Briggs has 10 million insects, 1 million nematodes, but essentially no fungi).
As discussed much more fully elsewhere (May 1988, 1990, 1994a; Hammond 1992, 1995a), there are many ways to estimate species totals. They include subjective expert opinion, extrapolation of trends, assessments of ratios of unknown
to known species in previously unstudied places, and other methods that combine evidence with various degrees of theoretical argument. The remainder of this section outlines some of the salient points of the various approaches, particularly in relation to my choice of lower estimates in table 4.
As reviewed by May (1994a) and Hammond (1995a), extrapolation of past trends and surveys of expert opinion tend to put insect species totals in the rough range of 5–10 million. Estimates based on detailed keying-out of the fraction of species new to science in previously unexplored regions tend to give lower numbersaround 3 million (for example, Hodgkinson and Casson 1993). Conversely, estimates reached by using a chain of theoretical arguments to scale from numbers of beetle species in the canopies of individual tropical tree species to tropical insect species totals about 30 million (Irwin 1984); reappraisal of such theoretical arguments has, however, suggested totals more like 3 million (May 1988, 1990; Stork 1988).
I have chosen a best guess of 4 million (rather than Hammond's 8 million, or the lower 2 million guess by Nielsen and Mound, this volume) largely on the basis of the new approach developed by Gaston and Hudson (1994). This original method first asks what fractions of the species in particular taxa are found in each
of nine biogeographic realms (these nine realms represent a slight extension of the conventional Wallace scheme); the reference taxa range from general categories (such as higher plants, amphibians, birds, and mammals) to very particular ones (such as dragonflies, tiger beetles, and swallowtails). Gaston and Hudson then take a range of estimated total numbers of insect species in the Nearctic and in Australia and scale them up to global totals on these biogeographic bases. For example, given that Nearctic higher plants represent 6.5% of the global total, an estimated total of 200,000 Nearctic insect species would imply around 3 million insect species in total. For their fairly wide range of estimators, Gaston and Hudson arrive at global insect totals in the range of 1–10 million. I favor an assessment of around 150,000–250,000 Nearctic insects (with Australian insect totals less sure), and use of the higher plants as the biogeographic template, which gives 2–4 million insects in total. This estimate tends to accord with those from empirical studies, such as those of Hodgkinson and Casson (1993); hence my choice of 4 million insect species in table 4. It also accords with Erwin's (Smithsonian Institution, Washington, DC, pers. comm.) recent estimate that preliminary keying-out of some of his tropical-canopy beetle collection suggests that around 80% of the species are new; this implies multiplying the insect total in table 2 by 5, which again gives around 4 million.
Observing that there are about six to seven fungal species for each indigenous plant species in the United Kingdom, Hawksworth (1991) suggested that the global total of around 270,000 plant species should be scaled up to yield around 1.5 million species of fungi. Given that only some 72,000 fungal species have yet been named, that would imply that 95% remain to be discovered. Put another way, we might expect that in collections from previously unstudied places, only 5% of fungal species would be known, which is very discordant with the facts (May 1991). Seemingly in support of the 1.5 million estimate (Hawksworth and Rossman 1997), Mibey and Hawksworth (1997) cite 43 species new of 61 species of Meliolaceae and 10 new of 14 Asterinaceae studied in Kenya: but if the 71% figure were representative, it would scale from the known 72,000 fungal species to only around 250,000.
I think the inconsistencies here are associated with problems in simply scaling from UK fungus-plant ratios to global totals. As discussed more carefully, and with other examples elsewhere, such scaling up assumes, among many other things, that fungal species and flowering-plant species characteristically have similar geographic ranges and latitudinal distributions (May 1990). I think it more likely that typical fungal species have wider geographic distributions than typical plant species. Witness the study by Rossman and Farr (1997) of four representative groups of fungi, of which the North American species represented 40–50%, 16%, 54%, and 68% of the world total. The corresponding figure for North American flowering-plant species is 6.5%: maybe the North American fungi are vastly better known than those of other parts of the world, but surely not to this extent. Also, the flowering-plant diversity of the United Kingdom is depauperate, still recovering from the last ice age.
Such considerations undercut many other scaling-up exercises. A count of Heliconius butterfly species to Passiflora species in typical Neotropical sites, scaled against the roughly 360 species of Passiflora in South America, would suggest around 500 species of Heliconius. There are in fact only 66. The same butterflies use different Passiflora species in different places. There are many other such cautionary tales (May 1990).
Some other “high” entries in table 4 also come from scaling-up of one kind or another. Grassle and Maciolek (1992) have suggested 10 million or more marine macrofaunal species (mostly mollusks, crustaceans, and polychaete worms) on the basis of a different kind of extrapolation. As pointed out on ecological (May 1992) and statistical (Solow 1995) grounds, such projections must be treated with considerable caution.
Apart from insects and fungi, my estimates in table 4 differ little from those discussed fully by Hammond (1995a). I have revised protozoa, algae, and mollusks down a bit and nematodes up a bit as a result of input from this forum. Influenced by Platnick (1997), I have revised arachnids down to around two-thirds of Hammond's estimate. These changes, however, have little effect on my best guess of about 7 million species, some 5 million lower than Hammond's (1995a).
Species Alive Today as a Fraction of the Historical Total
Given the great uncertainties in how many species are alive today, any estimate of the total numbers ever to have lived, or of likely future numbers of extinctions over the coming century, is even more imprecise.
There is, however, an alternative approach that asks about the fraction of species alive today, or about comparative rates of extinction (in terms of probabilities that species in particular groups became extinct recently, or under various assumptions about the future relative to average extinction probabilities over the sweep of the geological record). Such assessments involve dimensionless ratios and thereby factor out the gross uncertainties associated with absolute numbers of species, permitting quite accurate statements to be made.
For an assessment of f, the fraction of all species to have lived since the Cambrian dawn of hard-bodied fossils (some 600 million years ago) that are alive today, we first ask what is the average life span of a species in the fossil record, from origination to extinction. Such life spans vary greatly, both within and among groups. Raup (1978) brought together several studies and then analyzed some 8,500 cohorts of fossil genera to conclude that the average life span of invertebrate species is around 11 million years. A later, and particularly thoughtful, review by Sepkoski (1992) suggests that 5 million might be a better estimate. The top part of table 5 summarizes the studies surveyed by Sepkoski (1992) and some others, giving an overall impression that the average species has a life span of around 5–10 million years, but with much variability (May and others 1995).
Cocks (Natural History Museum, London, UK, pers. comm.) has recently compiled a somewhat wider range of estimated species life spans, arguing broadly for a shorter average figure than those above. Graptolites in the Lower Palaeozoic seem to evolve particularly quickly: a collection of more than 30 species from the Silurian of Kazakhstan has examples of three successive species within a single graptolite zone, the duration of which is probably 500,000 years; thus, individual species life spans could be as short as 150,000 years. Likewise, Cambrian trilobites in the Acado-Baltic realm show 25 species with an average life span of 500,000 years. Brachiopods also can be short lived, with particular examples (such as Eocoelia intermedia) having life spans less than 500,000 years. Turning to vertebrates, small mammals have evolved at such speeds that most rodent species have life spans of less than 1 million years, with even shorter durations (300,000–400,000 years) in times of rapid dispersal. Perrissodactyls also typically have life spans of less than 500,000 years. Insectivore species live longer, averaging maybe
3 million years. A sample of 175 species of tertiary to recent Corals has species life spans ranging from 200,000 years to 7 million years, with an average of about 4 million years. Moving on up to longer life spans, we find an analysis of 131 species of benthic Foraminifera with average life spans of 14–16 million years, although some have shorter spans, around 7 million years. Coccoliths have comparable longevity. Perhaps the longest-lived species that is well documented is a bryozoan that ranges from the early Cretaceous to the present, a span of around 85 million years (PBT Taylor, Natural History Museum, London, UK, pers. comm.). These estimates, and supporting references, are set out in the lower part of table 5.
In short, there is very great variabilityover a range of a factor of 100among species life spans in the documented fossil record. If one is to speak of an average, it might be better to offer a range like 1–10 million years. Forced to produce a more definite guess, Cocks and his colleagues in the Natural History Museum in London produce a figure of 4–5 million years.
If the sweep of the fossil record is around 600 million years and the average life span from origin to extinction of individual species averages around 4–5 million years, then we might conclude that the species living todayor at any other specific instantrepresent just under 1% of the total ever to have lived; that is, f is about 0.01.
Such an estimate, however, assumes total species numbers to have been roughly constant over the 600 million years. That, of course, is not so. As has been argued by Sepkoski (1992), and more recently by Rosenzweig (1997), on the grounds of apparent trends, and by others from more recondite analyses (some involving power laws and fractal measurements; for example, Solé and others (1997), in a very broad outline the history of the fossil record is one of roughly linear increase in species numbers. That implies that the number of species living today is roughly twice the average over the fossil record, which suggests that they make up more like 2% of those ever to have lived, or an f of around 0.02. Benton (1995, 1997) has gone further, marshaling evidence in support of an exponential increase in terrestrial species diversity since the end of the Precambrian; I read this work as arguing for an f of 0.03 or higher.
The latter estimate is subject both to the uncertainties in species life spans and to other complications. For instance, given that most living species are terrestrial insects, whose origins were more like 400 million years ago (and whose average life spans might be somewhat longer than the overall averagesee May and others 1995), f could be somewhat larger than 0.02.
Whatever the details, today's evolutionary heritage of living species is not a negligible fraction of those ever to have graced the planet. By the same token, only relatively few past species have exited in dramatic mass extinctions (by the above estimate, the “big five” mass extinctions, even if they had each wiped out virtually all extant species, account for only 5%, or at most 10%, of all endings). The sixth wave, on whose breaking tip we stand, is an uncommon evolutionary event, when judged against the geological record.
Pimm and Brooks (this volume) extend earlier work by May and others (1995) and themselves (Pimm and others 1995), applying similar arguments based on
comparative species life spans to estimate recent and likely future changes in extinction rates, as seen against the background average of the fossil record.
Emphasizing the uncertainties, I have estimated that the number of distinct eukaryotic species alive on Earth today lies in the 5–15 million range, with a best guess of around 7 million. Of these, roughly 1.5 million have been recognized. Allowing for the resolution of synonyms, new species are being recorded at around 10,000 each year. At that rate, it will take over 500 years to complete the catalog.
Such a 500-year estimate is, of course, misleading on several grounds. For one thing, recent and likely future extinction rates point toward qualitative reductions in the catalog. Even more important, I believe that advances in automating molecular sequencing, along with more systematic and computerized handling of phylogenetic information, will revolutionize the basic task of taxonomy in ways that we can yet barely imagine. I guess that within 50 years, and possibly much sooner, we will put a small DNA sample from a newly collected specimen into a machine and be told its exact location in a synoptic tree of living species.
The task of inventorying is sometimes mistaken for “stamp collecting” by thoughtless colleagues in the physical sciences. But such information is a prerequisite to the proper formulation of evolutionary and ecological questions, and essential for rational assignment of priorities in conservation biology (Nee and May 1997; Vane-Wright and others 1990). Lacking basic knowledge about the underlying taxonomic facts, we are impeded in our efforts to understand the structure and dynamics of food webs, patterns in the relative abundance of species, or, ultimately, the causes and consequences of biological diversity.
It is interesting to speculate whether the denizens of other inhabited planetsif there are anyshare the vagaries of our intellectual history: a fascination with the fate of the universe and the structure of the atom, lagging well behind interest in the living things with which we share our world. A different, but related, question lies in human institutions' difficulties in taking action to address longterm problems at the expense of short-term interests (witness climate change). Such questions do not come readily under Medawar's rubric of science as “the art of the soluble”, but they go to the heart of humanity's future, which unwittingly entrains the rest of life on Earth.
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The Sixth Extinction:
How Large, Where, and When?
The scientific consensus is that if current rates of species extinction continue, the fraction of species lost will be comparable to that of the five major extinction events in Earth's geological past (Leakey and Lewin 1996). Unlike the past episodethe famous one exterminated the dinosaursthis sixth extinction is driven by the dominance of one species, humans (Ehrlich and Ehrlich 1981). The powerful ethical (Norton 1988) and economic (Costanza and others 1996) reasons why we should prevent this scenario are well known (Myers 2000). Less clear are the details. How many species will we lose? Will these losses occur across the globe, or are some areas more vulnerable than others? How quickly will species disappear: do we have years, decades, or centuries to mitigate our current actions?
Those are the questions we will address here. They are circumscribed in one obvious way: we count species, in part, because it is easy to do so. How, then, might our answers apply to other levels of biodiversity? The utility of the term biodiversity stems from the recognition that there is variety in life between individuals in a given population, between populations of a given species, and between species (Wilson 1992, 2000).
Killing individuals does not necessarily kill a population, exterminating a population does not necessarily eliminate the species, the species its genus, and so on. What happens when we reverse this logic (Raup 1979)? When we exterminate, for example, 10% of all species, we will likely exterminate far more than 10% of all populations. Some species will survive our depredations but with severely pruned populations. As Hughes and others (1997, 2000) point out, many important justifications for protecting biodiversity emerge from populations, not species.
In what follows, whatever statistics we estimate for species must be substantial underestimates of the effects on populations.
Some species have many populations, others few. Similarly, some genera have many species, others few; and so on through the taxonomic hierarchy of families, orders, and classes. This hierarchy is the sometimes imperfect surrogates for evolutionary lineages of increasing depth. Random species kills often fall on genera with many species, so generic diversity will survive. A benevolent species killer might select some of the buntings (Emberiza), sandpipers (Calidris), and greenbuls (Phyllastrephus). This action might remove no genera, but only species (whose loss would be mourned only by us connoisseurs of subtle differences in their shades of brown and green). Humanity, however, can be malevolent. Elsewhere, we show that we have already lost more genera of birds and mammals than one expects to lose by chance on the basis of random species losses (Russell and others 1998). So, perversely, the impacts we estimate for species also underestimate the impacts we might expect on the diversity of higher taxonomic categories.
Species Losses Past and Present
The vast majority of the species that have ever lived are now extinct. So the question “How many species are going extinct?” has to be rephrased: “How much faster are species going extinct than one would expect?” The contrast is one of rate.
Thirteen studies of the fossil record show that species persist for one to a few million years (May and others 1995). We know the names of about 1.55 million species (May, this volume), so each year we would expect one or at most a few species to expire. Within small subsets of species, we would expect to wait longer to see just one extinctionabout a century for the 10,000 species of birds, for example. Calculating extinction rates as ‘extinctions per species per year’ provides a convenient frame of reference for calculating human impact (Pimm and others 1995). We know the names of only a small fraction of the planet's species (May 2000), and so by design, this measure does not depend on our knowing them all.
The fossil-record estimate of roughly a million-year life span for a species is suspect in two obvious ways. First, most kinds of species are absent from the record while invertebrates with hard shells (mollusks and brachiopods) dominate. Second, rare species are likely to be missed entirely (McKinney and others 1996). So how typical is this estimate of the rare vertebrates that form the core of our subsequent discussion? An important clue comes from the constraint that natural extinction rates cannot greatly exceed natural speciation rates (Pimm and others 1995). If it were otherwise, there would be no species in the group in question for us to observe.
The common model of speciation assumes an interbreeding population, and then a barrier that splits it allowing the daughter populations to diverge evolutionarily. Taxonomists pass judgment on whether this divergence is sufficient to have formed species. Alternatively, the barrier might later dissolve and the two populations, by not interbreeding, unequivocally demonstrate their distinctiveness. The distinctiveness of two populations in the latter alternative (sympatry) informs
the taxonomic judgments about the former (allopatry). In this model, barriers make species and geological knowledge allows us to date the barriers (Rosenzweig 1995). On the average, species-making barriers should form half a species's lifetime in the past, for some species are near their births, and others are near their deaths.
In North America, the presence of many pairs of similar bird species in forests on either side of the central prairies suggests the Late Pleistocene glaciation only 10,000 years ago as the species-making barrier. This high speciation rate might have been a fortuitous baby boom in species, with current high extinction rates a natural pruning of evolutionary exuberance. In fact, the suggestion itself is wrong. Klicka and Zink (1997) use molecular data to show that for 35 such species pairs the average divergence time is 2.45 million years. Increasing numbers of similar studies will likely flesh out many other details, but overall they support the million-year life span as a conservative estimate for species in general.
Humanity's Impact on Species' Lifetimes
The expectation that one should wait a century to observe an extinction among a sample of 10,000 species is rudely rejected by birds. In recent history (the last 2,000 years), the 10,000 bird species have suffered an average of one or a few extinctions each year (Steadman 1997). Humanity has decreased the average species lifetime and consequently increased the extinction rate by a factor of several hundred (Pimm and others 1995). We know birds well, and the details are informative.
Most of the bird extinctions have been in islands in the Pacific (Steadman 1995). The extinctions represented by stuffed skins in museums, collected within the last century or so, are a small fraction of the total. We know of many more species only as bones from archaeological samples. These species persist up to, but not through, the layers indicating the island's human colonization. The archaeological samples are inevitably incomplete. On the basis of what fraction of today's species the samples include, we estimate that they have found only half the extinct species (Pimm and others 1994). In addition, few of the 700 Pacific islands large enough and isolated enough to host unique species have been explored by archaeologists. Once again, we must correct the body count to reflect the incompleteness of the sampling. Statistical corrections from known species and surveyed islands suggest that the Polynesian colonization of the Pacific exterminated at least 1,000 species of birds. Locally, as in Hawai'i, the Polynesians exterminated over 90% of bird faunas (Pimm and others 1994).
Conclusion 1. Over the last few thousand years, humans have eliminated over 10% of the world's bird species and locally over 90% of them. Double-digit extinction percentages are part of our history, not merely a prediction about our future.
The obvious question is whether birds are exceptionally wimpy. They are well-known and so provide unusual details, but are they just extinction-prone? The answer is an emphatic no. Those who argue, like Simon (1986), that the only current extinctions among the 1.55 million named species are a few species of birds and mammals each year are simply ignorant of the facts. The data prove that extinctions are much more comprehensive. The examples are extraordinarily diverse, including animals and plants, invertebrate and vertebrate animals, species on islands and those on continents, desert species and rain-forest species, and aquatic and terrestrial species (Pimm and others 1995).
Statisticians know that their craft depends on samples and the inferences made from them. Reliable inferences require that samples be representative. Reading the list of examples in the previous paragraph, it is hard to imagine a more representative selection of samples. (Those who deny the generality of high extinction rates frequently use economic statistics based on samplessometimes very small samplesof the numbers in question. The uncritical faith in statistics in one field and the denial of their existence in others is incongruous.) The high rates of extinction in so many different groups lead to our second conclusion.
Conclusion 2. Surveys of many groups of plants and animals uncover global rates of extinction at least several hundred times the rate expected on the basis of the geological record. These groups are diverse in their natural histories and evolutionary origins. With high statistical confidence, they are typical of the many groups of plants and animals about which we know too little to document their extinction.
That is an ecologically surprising conclusion. Would it not be more reasonable for some kinds of species, such as birds versus beetles, or some kinds of places, such as forests versus deserts, to display concentrations of extinctions? Certainly, islands are home to many of the groups of species that are endangered. Yet extinction centers are found on continents, too, so there is nothing unique about islands. There are some differences between taxa. In North America, The Nature Conservancy has surveyed 18 groups of animals and plants to calculate the fraction that are on the verge of extinction (TNC 1996). Only butterflies are less vulnerable than birds. Proportionally, freshwater fishes, amphibians, crayfish, and freshwater mussels have 3–7 times more species at risk.
Despite these differences in places and taxa, we find high extinction rates in almost every group of species and in almost every kind of place. This “ecologically surprising conclusion” suggests that general ecological principles that work across all groups lead to substantial fractions of their constituent species becoming vulnerable to extinction. We suggest that there are three such principles:
• Many species have very small range sizes, relative to the average range size. (In other words, the statistical distribution of range size is highly right-skewed). Among birds, 30% of all terrestrial species have ranges smaller than 50,000 km2 (Stattersfield and others 1998)an area half the size of Tennesseewhereas the average size is some 40 times larger.
• Species that have small ranges are typically less abundant within those ranges than are species that have large ranges (Gaston 1994).
• Species with small ranges are often geographically concentrated (ICBP 1992). We call these areas of concentration hot spots of endemism (Myers 1988; Reid 1998).
Low numbers make a species vulnerable to disasters. So, too, do small geographic ranges; human impacts destroy habitats locally (Manne and others 1999). Nature has put her eggsspecies with small geographic ranges that typically have relatively low densitiesinto a few baskets, the hot spots. The pattern is general because the ecological principles that generate it are ubiquitous. These features, in turn, might be derived from deeper ecological causes, and indeed, ecologists seek such explanations. Whatever the underlying causes of the patterns, their consequences are obvious.
Conclusion 3. Many species are rare and local and so at particular risk from humanity's impact. Such species are not spread evenly; extinctions will be geographically clumped, like broken eggs in a dropped basket.
The aggregation of range-restricted species is the feature common to all the examples of high extinction rates listed earlier. Fish in East African lakes, freshwater mussels in the Mississippi drainage, mammals in Australia, flowering plants in the Cape Province of South Africa, and just about everything on oceanic islandsare all examples of aggregations of range-restricted species and very high extinction rates. Where there are not aggregations of range-restricted species, extinction rates will be low. There have been few bird extinctions in eastern North Americaan example to which we will return.
There could be two classes of exceptions to the common pattern: aggregations of range-restricted species that do not suffer high extinction rates, and extinctions of widely distributed species. Salamanders constitute an example of the first. Some 20% of the world's salamanders are found in the mountains of the eastern United States, but few are threatened. The reason could be simply that the nature of the terrain protected it from logging or that salamanders can survive well in the moist, deciduous second growth typical of the region. Some species aggregations are just lucky. Other amphibians illustrate the second class: species appear to be in decline worldwide (Berger and others 1998).
Such exceptions apart, the concentration of extinctions in hot spots for species with small ranges has two consequences for policies to prevent extinction:
Policy consequence 1. The history of areas that do not have concentrations of range-restricted species (cold spots) does not inform us in any simple way about the likely fate of concentrations (hot spots).
Eastern North America is an illustration. After European settlement in the 1600s, most of the forest was cleared, although not simultaneously. There were few extinctionsonly four species of birds, for example. That does not mean that
clearing other comparable areas elsewhere will have correspondingly small impacts. For birds, eastern North America is a cold spot: of its 160 forest species, only 25 are found only there (Pimm and Askins 1995). Clearing a roughly equal area of forest in insular Southeast Asia would exterminate nearly 600 species of birds (Brooks and others 1997).
Policy consequence 2. The fraction of species that will go extinct will depend critically on whether we lose or protect aggregations of range-restricted species.
The good news is that vulnerable species are concentrated, so saving them requires relatively little area. The bad news is that many of these areas have rapidly growing human populations and are in less-developed countries that have sparse resources to protect them (Balmford and Long 1995). Combining those statements leads to
Conclusion 4. How large the sixth extinction will be is still a matter of human choice, not of predestination.
Where are the Hot Spots of Endemism?
Myers informally identified 18 hot spots (Myers 1988, 1990). More recently, there have been many efforts worldwide to identify these key areas formally. There are now sophisticated algorithms for picking the smallest subset of locations that encompass all or some specified fraction of the species that one must protect (Pressey and others 1993). Some of these provide important exercises in method development (Csuti and others 1997). Others, such as the work of Lombard (1995) in the Cape Province of South Africa, inform practical decisions about where to establish nature reserves in this extraordinarily rich (and threatened) plant hot spot (Pimm and Lawton 1998).
There are several limitations. The most severe is that only a small fraction of the planet's species are named (May 2000), and we have range distributions for only a tiny fraction of them. Stork (1997) found that the great majority of insects are known from only one specimen each, and so only one location. Worse, there are complications even for the species we do know well.
Areas rich in species are typically not those rich in range-restricted species (Prendegast and others 1993; Curnutt and others 1993). Equivalently, areas that have similar numbers of species can differ greatly in their numbers of range-restricted species. The Hawaiian Islands, eastern North America, and Great Britain have broadly similar numbers of forest-living bird species (about 150); the percentages of species restricted to those areas are 100%, 17%, and less than 1% respectively. Nor are areas rich in range-restricted species in one group always rich in another: eastern North America is a hot spot for salamanders but not for birds. Recent work in Uganda suggests that this lack of correspondence might not matter, because key areas for each species group still represent other groups
remarkably well (Howard and others 1998). Nevertheless, we have much to learn about the geography of hot spots (Pimm and Lawton 1998).
Policy consequence 3. We cannot protect hot spots if we do not know where they are.
When comprehensive data are available, the algorithms to select areas for protection typically choose samples widely scattered across the study region. The size of the samples is set by the resolution of the range maps and is usually arbitrary. (An exception is Lombard's work [above] where the areas are set by the mosaic of different land uses and ownership.) Obviously, we can apply such methods to an ever-diminishing spatial scale. Two individuals of every species require remarkably little space. Thus, even with comprehensive data on species ranges, we must ask the ecological question: How much space must be set aside to protect species?
The question has a political answer: worldwide, about 5% of the land has been set aside for protection. The allocation of this to small and large areas also has a political answer. In the Americas, from Florida (US) southward through Mexico, Central America, and South America, only 21 national parks are larger than 10,000 km2roughly a square of 1 degree of latitude and longitude on each side (Mayer and Pimm 1998).
Policy consequence 4. Even if we know where to protect species, we must determine how much area is necessary.
How Much Area for How Many Species?
Global extinction is driven by the fate of the hot spots (Myers 1988). As the area of these hot spots shrinks because of habitat loss and fragmentation, how many species do we lose? One way to approach the question is simply to count the numbers of threatened and endangered species. That is the approach taken by the “Red Data Books” (Baillie and Groombridge 1996). But only for a few well-known groups of species is such information available (Pimm and others 1995). Fortunately, we can estimate losses of species by considering the amount of habitat that is being destroyed.
Exhaustive surveys of species in progressively larger areas of continuous habitat show that the larger the area surveyed is, the more species there will be. These surveys make it possible to deduce a mathematical relationship between species and area. Surveys of archipelagoes show the same relationship but with fewer species for an area of given size than in areas of continuous habitat. The derivation of a power function from first principles by Preston (1962) has led to the nearly universal acceptance of a form S = cAz for this relationship, where S is species number, A is area, and c and z are constants (Rosenzweig 1995). Typical values of z for increasingly large subsets of continuous habitat are about 0.15; values for areas between islands within an archipelago are about 0.25 (Rosenzweig 1995).
We can use this relationship to derive mathematically the species loss after fragmentation of a once-continuous habitat area, Atotal, initially holding Stotal species that are found only in this habitat (figure 1A). When we destroy the habitat,
leaving only an archipelago of fragments, the z value necessary to estimate the number of species that survive, Sfragment,, in a fragment of area Afragment is the “archipelago value” of 0.25 (figure 1C). In graphical terms, our number of species extinctions is represented by the drop from Stotal (figure 1A) to Sfragment (figure 1C).
We have calibrated this approach for three areas. For eastern North America, a region that has long been deforested and is a cold spot for bird diversity, we find that this recipe exactly predicts the number of bird extinctions (four) that have occurred (Pimm and Askins 1995). For two recently deforested hot spots, insular Southeast Asia (Brooks and others 1997) and the Atlantic forests of South America (Brooks and Balmford 1996), the recipe accurately predicts the numbers of bird species threatened with extinction in the medium term. The recipe is silent, however, about how long the still-surviving but probably doomed species will last. That leads us to our last question.
How Long Does it Take to Lose Species?
There are many ways to answer the question. Extensive modern experience shows that populations numbering in the thousands have risks of extinction observable within human lifetimes. Populations numbering in the tens and hundreds frequently become extinct. Computer and mathematical models provide the theoretical underpinnings of such observations and inform the management of particular species (Pimm 1991).
An entirely different tack comes from looking at the large national parks that are the flagships of their nations' conservation policies. Our experience in advising management about the endangered species in one of these, Everglades National Park in Florida, is that even at this scale, protecting such species requires constant vigilance (Mayer and Pimm 1998). Similar results across similarly large areas have been found elsewhere (Brash 1987; Daniels and others 1990; Diamond 1972; Newmark 1996; Soulé and others 1979; Terborgh 1975).
Between the management of particular endangered species and that of large parks are studies of fragmented habitats. It is on these that we shall concentrate. We can estimate the time that it takes for small patches of natural habitat to lose their species in at least two ways.
The simple way is to find a freshly isolated fragment and then to watch and wait. That is the approach being taken by the exemplary Biological Dynamics of Forest Fragments project in the Brazilian Amazon (Bierregaard and others 1992) and studies of islands isolated by rising waters after the damming of the Lago Gurí, Venezuela (Terborgh and others 1997). The only problem with the approach is that we might not have time to watch and wait. We would like the answers now, not in the future when it is too late to use them.
An alternative approach is to study old fragments of various ages. This approach relies on serendipity; but given the near ubiquity of habitat fragmentation, some fragments, somewhere, will surely provide something close to an ideal experiment. It is also less direct.
Historical collections can provide lists of the total species pool, Stotal, in the prefragmentation area, Atotal (figure 1A). Such records rarely distinguish the particular subset that now remains as a fragment, from the once-continuous habitat that surrounded it. We can estimate the number of species in such prefragmentation subsets, Soriginal, using the species-area relationship for the “continuous habitat value” of z = 0.15 (figure 1B). Similarly, we can estimate the number that will eventually remain after fragmentation, Sfragment, using the ‘archipelago value’ of z= 0.25 (figure 1C). Here, we are interested in the species loss from a particular subset, Afragment, (“local extinctions” or extirpations), rather than from the entire original area, Atotal (“global extinctions”). Graphically, the eventual species loss is represented by the drop from Soriginal (figure 1A) to Sfragment (figure 1C).
Addressing the issue of “how long” requires more information. We can determine through survey work the number of species surviving now, Snow, at any time t after fragmentation. This value should be somewhere between Soriginal and the final number, Sfragment. From those numbers, we can derive a ‘relaxation index’ (I), a ratio of the proportion of extinctions yet to occur after time t to the proportion that will eventually occur:
Immediately after fragmentation, I will equal 1.0, and it should eventually decline to zero. The final step is to assume a particular form for how I declines with time. As a first approximation, we assume that the decline in species is exponential (Diamond 1972) and therefore that we can characterize it by a fixed time to lose half its species (figure 2). (If the fragment loses 50% of its species in x years, it will lose half of what remains25% of the totalin another x years, half of what remains (12.5%) of the total in the next x years, and so on.) Thus,
where k is a decay constant and t is the time since the fragment was isolated. When I = 0.5, the fragment has lost half the species that it stands to lose, so t equals the half-life.
Elsewhere, we present data on birds in five rainforest fragments near Kakamega, western Kenya, that we collected over 1996 (Brooks and others 1999). Those data are the results of 8 months of bird surveys through mist-netting, spot counts, and extensive observation; a thorough literature review; an assessment of large quantities of forest-cover data in the form of aerial photographs dating back to 1948, satellite imagery, and anecdotal reports; and a survey of the historical bird specimens in most major museums. For each of the five fragments, we know Atotal, Afragment, Stotal, Snow, and t. From these we can estimate Soriginal and Sfragment and then use equation 1 to estimate I.
In figure 3 we plot the proportion of species still expected to be lost, I, against their times since isolation, t. If the declines in species numbers are all exponential with exactly the same half-lives, these points would fall along the same curve.
To a rough approximation, they do so, and their calculated half-times are all broadly similar at between 25 and 75 yearsaround 50 years.
The long technical details have a short conclusion. Of the species that fragments are going to lose, they lose half in about 50 years. In a century, they will lose 75% of those species.
Conclusion 5. Isolated habitat fragments (certainly fragments of tropical rain forest) will have suffered most of their extinctions by 100 years after isolation.
How do these results compare with other studies? Historical data on forest fragments are rare (Laurance and others 1997; Turner 1996), but a few studies do provide dated information on bird communities in fragmented tropical forests (Aleixo and Vielliard 1995; Christiansen and Pitter 1997; Corlett and Turner 1997; Diamond and others 1987; Kattan and others 1994; Robinson 1999; Renjifo 1998). Table 1 summarizes the data from those studies, giving the time between the historical and contemporary surveys (t) and the historical (Shistorical) and contemporary (Snow) numbers of bird species. Assuming a half-life of 50 years, we predict the future equilibrium numbers of species (Sfragment). Future resurveys of the sites could provide a third point in time along the relaxation curve (figure 2) and therefore test the predictions. Their value now is in suggesting how many more species the sites stand to lose.
How do our results extend globally? We know that over 10% of the world's roughly 10,000 bird species are threatened with extinction, with habitat loss and fragmentation as the main causes (Collar and others 1994). We therefore predict that about 500 of these bird species will go extinct in the next 50 years, producing an extinction rate of 1,000 extinctions per million species per year. The
rates for other groups of species will likely be higher in that they have much greater rates of current endangerment (TNC 1996).
There are sources of uncertainty in these estimates. For example, they assume that habitat destruction will freeze at current levels. Tropical deforestation, in particular, is continuing and accelerating. The worst-case scenario is that we retain only the 5% of the world's tropical forests in protected areasan event that will happen within 50 years at current rates (Myers 1992). Species-to-area relationships would predict that some 50% of the world's roughly 5,000 forest birds (and millions of other forest animals and plants) would go extinct eventually. Our results above suggest that half the 50% (1,250 species) will be lost before the end of the 21st century, giving an extinction rate of 1,250 extinctions per million species per year.
How do those results compare with other estimates of the magnitude and speed of the extinction? In table 2, we summarize estimates of current global extinction rates produced by seven methods, along with the background rate. The similarity of current rates and their difference by 3–4 orders of magnitude from background rates is striking.
There is a consequence:
Policy Consequence 5. To prevent species extinctions in fragmented habitats we must act immediately, for after a narrow window of only a century, it will be too late.
Finally, we can peer into the dim, more distant future for biodiversity. Prospective extinction rates vary greatly from group to group: 11% of bird species are currently threatened with extinction on the basis of our actions to date (Baillie and Groombridge 1996). Birds appear relatively resistant to extinction. Perhaps one-fourth of all mammal species and even higher proportions of some other groups are now on their way to extinction (Baillie and Groombridge 1996).
If the destruction of natural communities that is now underway throughout the world continues at expected rates, many more species might be similarly doomed to extinction by the end of the next century. The rich tropical forests might contain as many as two-thirds of all the planet's species (Raven 1988). The loss of these forests is rapid and accelerating. We might lose all their species. Suppose that we save 5% of the forests in parksthe average global value for all protected areasand effectively guard them from destructive incursions for the future. Our species-to-area calculations predict that we would eventually lose half the forest speciesone-third of all the planet's species. Experience with tropical forests suggests that saving 5% of them will require considerable effort.
We can now give answers to the questions that we posed at the outset. How soon will extinctions occur? Very soon: we can expect to see widespread extinctions in fragmented habitats within 50 years, with the extinction rate about 1,000–10,000 times greater than background rates. Where will extinctions strike hardest? In the hot spots of biodiversity in the tropics. How many species will be lost if current trends continue? Somewhere between one-third and two-thirds of all specieseasily making this event as large as the planet's previous five mass extinctions.
This study was funded by National Geographic Society Research Award 5542–95, a Pew Fellowship in Conservation to SLP, and an American Museum of Natural History Collection Study Grant to TMB. J. Akiwumi, J. Baraza, R. Fox, R. Honea, M. Ibrahim, L. Isavwa, M. Mwangi, K. Orvis, R. Peplies, and J. Robinson helped with forest cover data. In Kakamega, J. Barnes, R. Barnes, L. Bennun, D. Gitau, T. Imboma and his family, C. Jackson, J. Kageche Kihuria, M. Kahindi, S. Karimi, L. Lens, D. Muthui, J. Odanga, D. Onsembe, N. Sagita, J. Tobias, E. Waiyaki, C. Wilder, and the rest of the staff of the Ornithology Department, NMK, and the Kenya Wildlife Service and Forest Department staff were crucial to fieldwork. T., D., and G. Cheeseman, the late G.R. Cunningham-van Someren, M. Flieg, M. Lynch. D. Turner, and D.A. Zimmerman provided further data, as did many museum staff, in particular our hosts P. Sweet, D. Willard, R. Paynter, and P. Angle; and S. Conyne. Thanks to R. May, P. Raven, D. Vázquez, C. Wilder, and an anonymous reviewer for comments on the manuscript.
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The Meaning of Biodiversity Loss.
By the time we convene for the third National Forum on Biodiversity in 2007, we may have lost 1 million of Earth's putative 10 million species, counting all extinctions since the start of the biotic crisis a half-century ago. As with many other natural resources and their environmental services, we shall probably not understand the full consequences of biodiversity's decline until we, or rather our descendants, are obliged to learn by strictly empirical means. The loss could turn out to be greater than today's best theoretical models are likely to suggest. Meantime, we must peer into a clouded future and discern as best we can the “meaning” of this loss.
The world is increasingly subject to the dictates of the marketplace. Whether one likes this or not, it is a fact of biodiversity's life. So this paper deals largely with commercial and economic values of biodiversity as expressed through the marketplace or shadow prices. Many other values are at stake and are unamenable to even the most ingenious proxy pricing. It is surely the case, too, that there are many other values that we are simply not yet aware of. This paper's findings should be viewed strictly as a minimalist assessment.
The Role of Populations
Biodiversity is generally taken to comprise not only species but also units of species plus ecological processes. Those units, or populations, are more im-
portant than is sometimes supposed. Earth's 10 million species feature a rough total of 2.2 billion populations, and we are losing these populations at a rate of 43,000 per dayproportionately far faster than we are losing species (Ehrlich and Daily 1993; Hughes and others 1997). That is important because it is populations rather than species that supply us with the myriad environmental services (known ecosystem services) that support our lifestyles, if not our very survival.
Key question: suppose that in the foreseeable future we lose 50% of all species and the surviving species lose 90% of their populations. Which will carry the greater consequences for the environmental stability of the biosphere? Which will be the most adverse for ecosystem services and environmental stability, whether at local, regional, or global levels?
Some evolutionary biologists believe that speciation and other forms of origination (plus novelty, innovation, and the like) often stem from core populations; other scientists think that they derive primarily from peripheral populations. In support of the second viewpoint is the notion that populations in border zones of a species's distribution often contain a greater amount of genetic variability and are therefore best able to respond to the environmental pressures that might well arise in greatest measure at the limit of the species's distribution. Is it not in this border zone, then, that speciation processes are most likely to arise and develop? Or are the populations that are most “productive” in an evolutionary sense more likely to lie in the heartland of a species's distribution? Is there any substantive evidence from the palaeontological past to indicate which has been the most frequent and productive response? Or is it a case of both together? Or conceivably neither? Could it be that the richest resources for natural selection occur in the heartland zone but that natural selection pressures are greatest in the peripheries?
However we view these uncertainties, it is certain that many species have already lost many of their populations. Consider the case of wheat. In 1996, the crop flourished across an expanse of more than 240 million hectares, with a rough average of 2 million stalks per hectare. Wheat plants totaled almost 500 trillion individualsprobably a record. (In comparison, consider that 1 trillion seconds equals about 32,000 years.) As a species, then, wheat is the opposite of endangered. But because of a protracted breeding trend toward genetic uniformity, the crop has lost the great bulk of its populations and most of its genetic variability. In extensive sectors of wheat's original range where wild strains have all but disappeared, there is virtual “wipeout” of endemic genetic diversity. Of Greece's native wheats, 95% have become extinct; and in Turkey and extensive sectors of the Middle East, wild progenitors find sanctuary from grazing animals only in graveyards and castle ruins. As for wheat germplasm collections, they were described more than a dozen years ago as “completely inadequate”and that was without considering such future threats as macropollution in the form of acid rain and enhanced UV-B radiation.
In the rest of this paper, we consider species, these being the most recognizable components of biodiversity.
Utilitarian Benefits of Species
Conservation biologists increasingly face the question, What is biodiversity good for? Naive as it might sound to some, it is a valid question. There is no longer enough room for a complete stock of biodiversity on an overcrowded planet with almost 6 billion humans and their multifarious activities, let alone a projected two-thirds increase in human numbers and a several-times increase in human activities within the next half-century. So biodiversity must stake its claims for living space in competition with other causes. Generally speaking, biodiversity must urge the merits of its cause through what it contributes to human welfare, preferably in the way that most appeals to political leaders and the general public, namely, in economic terms. This is a strictly anthropocentric approach, and limited as it might seem, it reflects how the world (although not the planet) works.
There are two categories of economic contributions: material goods and environmental services. The first has been frequently and widely (Baskin 1997; Daily 1997; Ehrlich 1992; Myers 1982) documented, principally in the form of new and improved foods, medicines, and raw materials for industry and sources of bioenergy. The second has been far less documented even though it was identified as unusually important 2 decades ago (Westman 1977) and even though its total value is far greater than that of the first (Bishop 1993; Ehrlich 1992; Risser 1995). The main reason for this lacuna is that scientists find it much harder to demonstrate the precise nature of the services, and it is still harder to quantify them economically. Whereas the benefits of material goods tend to accrue to individuals, often producers or consumers in the marketplace, the values of environmental services generally pertain to society; hence, they mostly remain unmarketed (Brown and others 1993).
From morning coffee to evening nightcap, we benefit in our daily lives from our fellow species. Without recognizing it, we use hundreds of products each day that owe their origin to wild plants and animals. Conservationists can well proclaim that by saving the lives of wild species, we might be saving our own. Yet we enjoy the manifold benefits of biodiversity's genetic library after scientists have intensively investigated only one in 100 of Earth's 250,000 plant species and a far smaller proportion of the millions of animal species.
Regrettably, there is not space here to do more than cite a few economic evaluations to demonstrate the utilitarian clout at issue. Consider crop-plant germplasm. Wheat andgermplasm collected in developing countries by the International Maize and Wheat Improvement Center near Mexico City benefits industrialized countries to the tune of $2.7 billion per year. In Italy, wheat germ pasta contributes $300 million per year to the pasta industry. In Australia, grain varieties have boosted annual harvests by as much as $2.2 billion between 1974 and 1990. One-fifth of the value of the billion-dollar US rice crop is attributed to genetic infusions (Evanson 1991). As for new foods, North American stores now feature all manner of exotic vegetables and fruits; from 1970 to 1985, the number of items available doubled to more than 130, and in some instances to as
many as 250. By the middle-1980s, specialty produce, mostly from Asia and Latin America, had become a $200-million-a-year business in the United States alone (Vietmeyer 1986).
The cumulative commercial value of plant-based medicines in developed nations is estimated to amount to $500 billion1 during the 1990s (McNeely and others 1993; Principe 1997). Two anticancer drugs from the rosy periwinkle generate sales totaling more than $250 million per year in the United States alone, and all plant-derived anticancer drugs combined save around 30,000 lives in the United States each year (Principe 1997). According to the National Cancer Institute, tropical forests alone could well contain 20 plants with materials for several additional superstar anticancer drugs (Douros and Suffness 1980).
A number of analysts have attempted an economic assessment of tropical forest plants' overall potential worth, not just for anticancer purposes. Estimates range from $420 billion (Pearce and Puroshothaman 1993) to $900 billion (Gentry 1993; Mendelsohn and Balick 1995).
Suppose that until the year 2050 we will witness the extinction every 2 years of one plant species with medicinal potential. The cumulative retail-market loss from each such extinction will amount to $12 billion for the United States alone (Principe 1997).
Species supply us with entire suites of environmental services, which can be defined as functional attributes of natural ecosystems that are beneficial to humankind (Baskin 1997; Daily 1997). They include generating and maintaining soils, converting solar energy into plant tissue, sustaining hydrological cycles, storing and cycling essential nutrients (notably through nitrogen fixation), supplying clean air and water, absorbing and detoxifying pollutants, decomposing wastes, pollinating crops and other plants, controlling pests, running biogeochemical cycles (of such vital elements as carbon, nitrogen, phosphorus, and sulfur), controlling the gaseous mix of the atmosphere (which helps to determine climate), and regulating weather and climates (both macroclimates and microclimates). In addition, biodiversity provides sites for research, recreation, tourism, and inspiration.
However, it is far from true that all forms of biodiversity can contribute to all environmental services or that similar forms of biodiversity can perform similar tasks with similar efficiency. How far do environmental services depend on biodiversity itself? Recent research suggests that they are highly resilient in the face of some loss of species, and they can keep on supplying their services even in highly modified states. A sugar cane plantation might be more efficient at producing organic material than the natural vegetation that it replaced, and a tree farm might be more capable of fixing atmospheric carbon than a natural forest. At the same time, many natural ecosystems with low biodiversity, such as tropical freshwater swamps, have a high capacity to fix carbon.
1 On the basis on an average of $50 billion per year ($15 billion in the United States alone).
Similarly, the services supplied by one form of biodiversity in one locality might not necessarily be supplied by a similar form of biodiversity in another locality. Just because a wetland on the Louisiana coast performs a particular suite of functions, we cannot assume that a wetland on the Georgia coast will perform the same functionsstill less an inland wetland in Massachusetts or California and even less a montane wetland in Sweden or a forest wetland in Thailand. Services tend to be site-specific. That makes it much more difficult for conservation biologists to demonstrate the intrinsic value of wetlands or any other biotopes.
Biodiversity plays two critical roles. It provides the biospheric medium for energy and material flows, which in turn provide ecosystems with their functional properties; and it supports and fosters ecosystem resilience (Ehrlich and Roughgarden 1987; Schulze and Mooney 1994). The latter attribute could turn out to be the leading service supplied by biodiversity insofar as all other services appear to depend on it to a sizable degree (Perring and others 1995). As biodiversity is depleted, there is oftennot alwaysa decline in the integrity of ecosystem processes that supply environmental services.
Environmental services are so abundant and diverse that we cannot do more here than look at an illustrative selection. First, consider biotas as carbon sinks. The value of carbon storage in tropical forests as a counter to global warming is around $1,000–3,500/ha per year, depending on the type of forest (Brown and Pearce 1994). The value of the carbon-storage service supplied by Brazilian Amazonia is estimated to be some $46 billion (Guttierez and Pearce 1992). It has been further estimated that replacing the carbon-storage function of all tropical forests could well cost $3.7–25 trillion (Panayotou and Ashton 1992).
Next, note the role of biodiversity in protecting soil cover. Excessive runoff from denuded catchments causes soil erosion and siltation in valleyland water-courses. Siltation of only reservoirs costs the global economy some $6 billion per year in lost hydropower and irrigation water. In the last 200 years, the average topsoil depth in the United States has declined from 23 cm to 15 cm; this costs the average American consumer around $300 per year through loss of nutrients and water, with total annual costs (including degradation of watershed systems; pollution of soils, water, and air; and other off-farm problems) to the United States of $44 billion. Worldwide costs of soil erosion are around $400 billion per year (Pimentel and others 1995).
Consider, too, the important but little-recognized services performed by wetlands. These services include a supply of freshwater for household needs, sewage treatment, cleansing of industrial wastes, habitats for commercial and sport fisheries, recreation sites, and storm protection (Mitsch and Gosselink 1993). Their economic value can be sizable. Louisiana wetlands are estimated to be worth $6,000–16,000/ha with an 8% discount rate, or $22,500–42,500/ha with a 3% discount rate. At the lowest value, the current annual rate of loss of these wetlands is levying costs of about $600,000/km2 per year; at the largest value, $4.4 million/km2 (late 1980s values). Marshlands near Boston are valued at $72,000/ha per year solely on the basis of their role in reducing flood damage (Hair 1988).
About one-third of the human diet depends on insect-pollinated vegetables, legumes, and fruits. At least 40 crops in the U.S are completely dependent on in-
sect pollination with a marketplace value of $30 billion (Pimentel and others 1992).
Finally, note the vital part played by biodiversity in the fast-growing sector of ecotourism. Each year, people taking nature-related trips contribute to the national incomes of the countries concerned a sum estimated to be at least $500 billion, perhaps twice as much (Eagles and others 1993). Much of these ecotourists' enjoyment reflects the animal life that they encounter. In the late 1970s, each individual lion in Kenya's Amboseli Park produced $27,000 per year in tourist revenues, and an elephant herd produced $610,000 per year (Western and Henry 1979); today's figures would be much higher with many more tourists in the park. In 1994, whale-watching in 65 countries and dependent territories attracted 5.4 million viewers and generated tourism revenues of $504 million, with annual rates of increase of over 10% and almost 17%, respectively. A pod of 16 Bryde's whales at Ogata in Japan would, according to conservative estimates, produce at least $41 million from whale-watchers over the next 15 years (and be left alive), whereas if killed (as a one-shot affair) they would generate only $4.3 million (Hoyt 1995). In 1970, ecotourism in Costa Rica's Monteverde Cloud Forest Reservegenerated revenues of $4.5 million, or $1,250/ha, to be compared with $30–100/ha for land outside the reserve (Tobias and Mendelshn 1991). Florida's coral reefs are estimated to generate $1.6 billion per year in tourism revenues (Adams 1995).
A team of ecologists and economists has recently attempted a comprehensive evaluation of all the goods and services stemming from biodiversity. They offer a preliminary and exploratory total of $33 trillion per year (Constanza and others 1997), compared with a global GNP of $28 trillion. Thus, the world's gross natural product is in the same league as the world's gross national product and probably exceeds it.
Consider, too, Biosphere 2, the technosphere in the Arizona desert with its semisuccessful life-support systems for eight Biospherians over a period of 2 years. The cost was about $150 million, or $9 million per person per year. The same services are provided to the rest of us bynatural processes at no cost. But if we were charged at the rate levied by Biosphere 2, the total bill for all Earthospherians today would come to $3 quintillion (Avise 1994).
The biggest challenge of all is to determine a comprehensive answer to the question, What is biodiversity good for? At present lamentable rates of research and analysis, we might eventually find responses to that question only by discovering what has been lost after much biodiversity has been eliminated, with its goods and services.
Conservation biologists should feel more inclined to simply reject the question, What is biodiversity good for? We shall not have anywhere near a sufficient an-
swer within a timeframe to persuade political leaders, policy-makers, and the public (let alone the professional skeptics). Rather, we should invoke the uniqueness and irreversibility arguments and throw the burden of proof on the doubters, requiring them to demonstrate that biodiversity is generally worth so little that it can be dispensed with if human welfare demands as much, through, for example, agricultural encroachment on wildland habitats. True, there is vast uncertainty about what biodiversity contributes to the human cause. But because of the asymmetry of evaluation, the doubters are effectively saying that they are completely certain that we, and our descendants for millions of years (until evolution restores the loss), can manage well enough without large quantities of biodiversity.
This paper was written with financial support from a Pew fellowship in conservation and environment.
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The Loss of Population Diversity and Why it Matters.
Biodiversity encompasses variation at all levels of biological organization, including individuals, populations, species, and ecosystems (Wilson 1988), yet much of the current scientific and public concern over the extinction crisis is focused on the loss of species. The rate of species extinction, however, reflects only one aspect of the loss of biodiversity and its consequences. What if no further species became extinct, but every nonhuman species suddenly were reduced to a single, minimal population? Although global species diversity would remain unchanged, the planet would be largely devoid of life, and civilization as we know it would collapse. This is because many of the benefits that biodiversity confers on humanity are delivered locally, through populations of species. This extreme scenario highlights the idea that species, although important, are not the only dimension of biodiversity that we should be concerned about losing.
In this paper, we examine the consequences of the gradual extinction of populations that is occurring today. First, we discuss the importance of populations to humanity. Then, we present estimates of population diversity, that is, the number of populations on Earth. Finally, we make a preliminary attempt to evaluate the rate of populations extinction.
What is a Population?
Populations are geographical entities within a species, usually distinguished ecologically or genetically (Ehrlich and Daily 1993). The ecological entity is a demographic unita group of individuals whose population dynamics are not
influenced substantially by migration from nearby conspecific groups; that is, the fluctuations in the size of the population of one group are independent of those of other groups (Brown and Ehrlich 1980). The genetic entity is a Mendelian population (Sinnott and others 1950), defined here as a genetically distinguishable group of individuals that evolves independently of other groups. Demographic units may be Mendelian populations and vice versa, but the two are not necessarily congruent. As with species, both kinds of populations exist as parts of continua in space, rather than as clear, discrete units.
We adopted the Mendelian-population definition for our estimates of population diversity and its extinction rate for two reasons. First, the Mendelian definition directly includes the genetic variation between groups of individuals, and, as discussed below, this variation is of great importance to humanity. Second, we found that quantitative data on genetic-population structure was more comparable across species and investigations than were quantitative data on demographic-population structure.
The Importance of Populations
Why should one be concerned about the extinction of populations? Much has been written about the ethical and practical reasons for halting the species-extinction crisis that is driven by human activities (Ehrlich and Ehrlich 1981; Ehrlich and Wilson 1991; Myers 1979; Wilson 1992). Certainly, we agree with these reasons, yet simply arguing for saving species obscures an essential link between biodiversity and human welfare. Ultimately, most of the benefits that biodiversity confers on humanity are delivered through populations. These benefits include aesthetic enjoyment, discovery and improvement of pharmaceuticals and agricultural crops, species conservation, replenishment of stocks of economically valuable species, and, perhaps most important, delivery of ecosystem services.
Natural ecosystems are composed of populations of organisms, their physical environments, and the interactions between them. As such systems are disrupted or destroyed, people's enjoyment of their ambience and the aesthetic values of their component populations (for example, birds, butterflies, reef fishes, flowering plants, and shade trees) is diminished. In addition, the total aesthetic value of individual species declines as their populations disappear, although the aesthetic value of “rarity” may partially, and somewhat paradoxically, compensate for this loss. For instance, although wild populations of grizzly bears and remnants of old-growth redwood forest exist in the United States, the total aesthetic benefit conferred on Americans by watching a grizzly cub play or by hiking in a cathedral-like, old-growth redwood forest is relatively small because few people can experience them firsthand.
Much of the genetic diversity in species exists as genetic differences between populations. For an average animal species, 25–30% of its total ge-
netic variability is due to differences between populations. In an average outcrossing plant species, 10–20% of its genetic variability occurs among populations, whereas a selfing plant species exhibits about 50% of its genetic variability among populations (Hammond 1995). One result of this differentiation is that populations of the same species may produce different types or quantities of defensive chemicals (Dolinger and others 1973; Goméz-Pompa and others 1972; Hwang and Lindroth 1997), compounds that may have medicinal value.
An example of how genetic variation among populations is important to pharmaceuticals is the story behind the development of penicillin. The successful development of penicillin as a therapeutic drug did not occur until 15 years after Alexander Fleming's discovery of the compound in common bread mold. One reason for this delay was a worldwide search to find a strain (that is, a population) of the mold that produced greater quantities of penicillin than the original strain produced (Dowling 1977).
Population diversity among wild relatives of crops also supplies critical genetic material to agricultural strains. Genetically uniform strains of the world's three major crops (wheat, rice, and maize) are planted widely; as a result, large fractions of the harvest can be threatened at one time by a new disease or pest (Plucknett and others 1987). Thousands of strains, or populations, of wild relatives of crops may need to be tested until one is found that carries the desired genetic resistance that can be used to protect the crop. For example, when the grassy stunt virus emerged as a serious threat to the rice crop in Southeast Asia in the late 1960s and 1970s, an extensive search for resistant varieties of rice was conducted at the gene bank of the International Rice Research Institute. Five thousand accessions from populations all over the world and 1,000 breeding lines were screened. Only one accession of a wild rice collected in India was found to resist the virus (Plucknett and others 1987). Genetic variation in wild populations of crop species also will be crucial in providing genetic material to sustain yields with changing growing conditions, especially climate (Daily and Ehrlich 1990).
By definition, populations are essential to the conservation of species diversity, and the number and size of populations influence the probability of persistence of the entire species. Migrants between populations can prevent the local extinction of a species by contributing critical individuals when numbers are low (the rescue effect) (Brown and Kodric-Brown 1977) or by supplying the genetic variation needed to adapt to changing environmental conditions (Lande 1988). If local extinction does occur, individuals from other populations can recolonize the area. The threat of rapid global climatic change makes the safety net of population diversity for species even more important; a species that has many populations is more likely to include individuals that are genetically suited to new conditions than is a species that has only one or a few populations (Kareiva and others 1993).
Direct Economic Value
Destruction of populations of an economically valuable species not only increases the probability that the species will become extinct in the near future but also may decrease the species' harvest level. In the short term, as populations are exterminated, fewer will remain to be harvested; in the longer term, when a species is composed of a metapopulation, the stock levels of the remaining populations also may decline (Pulliam 1988). The reduction of these economically important species often has direct consequences for local peoples. For instance, overharvesting of oceanic fish stocks and the resulting decline in yields lead to loss of income to fishermen and loss of an important source of protein for much of the human population (Kaufman and Dayton 1997; Peterson and Lubchenco 1997; Safina 1995).
Perhaps the most important benefit that populations confer on humanity is ecosystem services. Ecosystem services include natural processes, such as purification of air and water, detoxification and decomposition of waste, generation and maintenance of soil fertility, pollination of crops and natural vegetation, and control of pests (Daily 1997). These services are provided by populations, and population diversity (that is, the number of populations) at global, regional, and local levels affects the provisioning of ecosystem services. (The size and density of populations also influence the provisioning of ecosystem services. These dimensions will be discussed later. For now, we simply address numbers of populations.)
Greater global population diversity probably enhances the delivery of global ecosystem services, such as regulation of biogeochemical cycles and stabilization of climate (Alexander and others 1997). The larger the area that remains under natural tree cover in the Canadian taiga, the greater the amount of carbon stored there. Although deforestation in this region might not result in the extinction of any species, a large-scale loss of tree populations would influence the balance of greenhouse gases in the atmosphere worldwide (Woodwell and others 1983).
For many ecosystem services, however, global numbers of populations are not as important as regional population diversity. In other words, for these services, it is not only necessary that many populations exist somewhere in the world but also that they exist within the region of interest. These services include, for instance, mitigation of floods and droughts by forests and purification of water by forests and wetlands (Ewel 1997; Myers 1997). Loss of these services occurs when forests and wetlands are destroyed in a region, regardless of the continued existence of their component species elsewhere. New York City provides an excellent example of the value of regional population diversity. The city was famed for its pure water, which came from the Catskill Mountains, 100 miles to the north. For most of the city's history, natural purification processes, which are carried out by populations of soil organisms and plants, were sufficient to cleanse the water, but in recent years, land development and associated human activities reduced the efficacy of these processes. In 1996, city water officials floated an environmental bond issue to purchase land, freeze development on other lands,
and subsidize the improvement of septic tanks in the water-supply area. It is hoped that these actions will restore and safeguard the local populations that filter and purify the water. If so, an investment of $1 billion in natural purification services will have saved city taxpayers $6–$8 billion, the additional avoided cost (over 10 years) of building a water-treatment plant (Chichilnisky and Heal 1998).
Regional population diversity is also necessary for control of pests. The importance of populations that serve a pest-control function is illustrated dramatically when an organism is transplanted to a new environment that lacks populations of predators capable of keeping it from becoming a pest. The importation of the prickly pear (Cactus opuntia) into Australia by early settlers is a classic case. Apparently originally intended as an ornamental plant, in the absence of its normal predators the cactus spread over vast areas. It occupied some 25 million hectares in New South Wales and Queensland, and half the area was covered so densely that the land could not be used for farming or ranching. The costs of poisoning or removing the cactus were more than the land was worth. The problem was solved eventually by importing a moth that is a voracious cactus-eater from the South American homeland of the opuntia. Once regional populations of that moth, Cactoblastis cactorum, were established, the cactus was decimated and the problem was solved. Although the cactus still can be found in Australia, it occurs only in scattered clumps since natural pest control has been reestablished (Ehrlich 1986).
Pollinators are critical to agriculture, and the decline of regional populations of native pollinators, chiefly as a result of pesticides and destruction of habitat, has not gone unnoticed (Buchmann and Nabhan 1996). For more than 60 crops planted in the United States, farmers are forced to pay keepers of the European honeybee to transport their hives to the fields or orchards that require pollinating. Hiring beekeepers costs farmers more than $60 million a year and the federal government more than $80 million in subsidies, and these numbers are still increasing because of growing problems in the beekeeping industry (disease and hybridization with the aggressive Africanized honeybee) (Nabhan and Buchmann 1997).
Population diversity at a particular location (that is, local species diversity) also affects ecosystem functioning and thus the delivery of ecosystem services (Chapin and others 1997). In greenhouse and field experiments, plant productivity has been found to increase with species diversity (Naeem and others 1994). The stability of plant productivity also has been linked with greater richness of species. More diverse grassland plots seem to be more resistant to drought and grazing disturbances than less diverse plots (McNaughton 1977, Frank and McNaughton 1991; Tilman and Downing 1994). Thus, it appears that local population diversity is closely coupled to local ecosystem functioning.
Because regional and global services are performed by an aggregate of local ecosystems, the consequences of a reduction in local population diversity probably will extend beyond the local ecosystem. In other words, the loss of populations from one location, which alters the functioning of the local ecosystem, may in turn affect the delivery of larger-scale services. For example, the global carbon
cycle may be influenced not only by the total number of tree populations on the planet but also by the diversity of populations at many locations.
One important question that remains to be resolved is the extent to which “weedy” species, spreading into and establishing populations in areas where native populations have been extirpated, can continue to supply ecosystem services. For such services as pest control, evidence is abundant that such compensation will be rare. The cotton disaster in the Cañete Valley in Peru is a classic example. Populations of natural enemies of potential cotton pests were destroyed by repeated, heavy applications of pesticides, and no weedy species moved in to assume the role of the natural predators. As a result, numerous obscure organisms became pests and destroyed the cotton crop (Barducci 1972).
For other services, such as flood control and soil retention, the potential for substitution by weeds, at least in the short term, sometimes may be high. In many cases, however, we are largely ignorant of the ability of weeds to maintain services over the long run. Furthermore, the capacity for large-scale technological substitution of ecosystem services appears limited (Ehrlich and Mooney 1983). The Biosphere 2 project, a materially closed, human-made ecosystem, is a case in point. Despite hundreds of millions of dollars invested in development and operating costs, scientists failed to engineer a system that could support eight people with food, air, and water for 2 years (Cohen and Tilman 1996; see also Daily 2000). That venture dramatically illustrated that we do not know yet how to replicate the life-support services that the mix of populations in natural ecosystems provides for free.
The Extent of Population Diversity
Given the numerous reasons to be concerned about the fate of population diversity, we recently attempted to quantify the extent of that diversity and the rate of its loss. In this section and the next, we give an overview of these calculations (for further details, see Hughes and others 1997). Again, we define population diversity as the number of populations on the planet; another aspect of population diversity is the degree of divergence among populations, but we do not consider that aspect here.
Many of the difficulties that plague attempts to estimate species diversity also hinder an estimation of population diversity. The debate over definitions of species has persisted for decades (for example, Coyne and others 1988; Dobzhansky 1935; Ehrlich 1961; Masters and Spencer 1989; Mayr 1940 and 1969), and defining a population is no simpler. Also, the small fraction of species cataloged so far (approximately 1.75 million species of 10 million or more [Hammond 1995]) represents a regionally and taxonomically biased view of the planet's biodiversity. These problems are inherent in estimates of species diversity and are inevitably present in estimates of population diversity as well. For instance, as with most estimates of species, our population estimate is restricted to eukaryotes, because information on the diversity of bacteria and viruses is almost nonexistent, although the diversity is probably enormous. Nonetheless, just as approximations of species diversity have been made despite these difficulties, enough information
exists to allow us to make a preliminary evaluation of biodiversity at the level of the population.
Our method of estimating global population diversity involved three steps. First, we reviewed the literature on population differentiation for a broad range of taxa and estimated the average number of populations per unit area for a series of species. Then we calculated the average size of the range of a species with a sample of available species range maps. The product of the resulting two numbers yielded an approximation of the average number of populations per species. Finally, we multiplied that number by the total number of species to arrive at the number of populations on Earth.
We searched 15 journals published from 1980 to 1995 for genetic studies on population differentiation, reading more than 400 articles and finding 81 that provided appropriate data for our calculations. We were able to estimate the number of populations per unit area for 82 species. Most of the species were vertebrates (n = 35), followed by plants (n = 23), arthropods (n = 19), mollusks (n = 4), and one flatworm (platyhelminth).
To quantify the number of populations of a species per unit area, we determined whether the sampling locations described in the articles were in separate populations or were within a single population. If statistically significant differentiation between localities was reported in the paper, we considered all the localities to be separate populations. We then calculated the number of populations per unit area as the number of sampling locations divided by the extent of the entire sampling area. If the researchers did not find significant differentiation between the localities, we assumed that they had sampled from within one population and that the size of a population was the size of the sampling area. Many studies found an intermediate amount of differentiation. For instance, in some studies, a significant difference was found only between two clusters of sites. In these cases, we assumed that there were two populations within the sampling area. This procedure yielded a conservative estimate of one population per 10,000 km2 for an average species.
What are some problems with this evaluation of populations per unit area? First is the taxonomic bias mentioned above. Arthropods make up about 65% of the planet's species, and birds account for probably less than 0.01% (Hammond 1995). In our data on population structure, however, arthropods accounted for only 20% of the species, whereas birds accounted for more than 11%. Second, the evaluation of population differentiation for an average species is limited by the sampling intensity of each study. In other words, the estimate is probably conservative, since in many cases additional sampling in the study area may have revealed further differentiation. Finally, the molecular markers chosen may not always reveal notable differences between groups (for example, Legge and others 1996), again making the estimate on the conservative side.
To estimate the average range of a species, we digitized more than 2,400 species range maps from guidebooks for birds, mammals, fishes, and butterflies from a number of geographical regions. Equally weighting the four taxonomic groups, the mean size of the range of a species is 2.6 million square kilometers. Averaging the range size estimates of the largest group, the arthropods (here just butter-
flies), led to a range of 2.2 million square kilometers per species. These numbers are quite similar, so we conservatively used the lower number, 2.2 million square kilometers, as our estimate of the average size of the range of a species.
This evaluation of the average size of the range of a species is the most probable source of inflation in our estimate of population diversity. The shaded areas on distribution maps virtually always encompass unsuitable habitats, where populations do not occur (Gaston 1994). Also, the majority of sources we used were limited to temperate regions, even though it is estimated that two-thirds of species diversity exists in the tropics (Raven 1983). This misrepresentation also may inflate the population estimates because, in some taxa, the sizes of species ranges tend to increase toward the poles (Pagel and others 1991; Rapoport 1982).
One aspect of our method may compensate somewhat for these biases, however. The sources we used restricted their species range maps to one continent, so the full range of intercontinental species was not taken into account. Therefore, we may have underestimated considerably the size of the range of some species, such as birds that have Holarctic ranges.
The product of the estimates of the average populations of a species per unit area and the average size of the range of a species was an average of 220 populations per species. Using three published calculations of global numbers of species (5, 14, and 30 million from, respectively, Hammond 1995, Raven 1985, and Erwin 1982), we arrived at three estimates of the total number of populations: 1.1, 3.1, and 6.6 billion populations.
In presenting the methods of our estimation of the current rate of population extinction, it is useful to begin with a summary of how species extinction rates usually are assessed. Estimates are derived largely from species-area relationships and from the rate habitat loss due to deforestation (Lawton and May 1995; Wilson 1992). The most commonly used species-area model is S = cAz, in which S is the number of species, c and z are constants estimated from empirical studies, and A is the area where the species are found (Rosenzweig 1995; see also Pimm and Brooks this volume). This relationship between area (size of the habitat) and number of species is illustrated in figure 1. The graph reveals a convenient rule of thumb: a 90% decrease in area of habitat should result in roughly a 50% decrease in species diversity.
By applying estimates of rates of tropical deforestation to this model, one can approximate the rate of species extinction in tropical forests. With a very conservative estimate of tropical deforestation of 0.8% per year, the rate of extinction of tropical forest species is predicted to lie between 0.1% and 0.3% each year, depending on the value of z used in the species-area model. If we assume that 14 million species exist globally and that two-thirds of all species exist in tropical forests, species diversity in tropical forests is declining by roughly 9,000–26,000 species per year, or 1–3 species per hour (this last calculation was reported incorrectly in Hughes and others 1997).
No comparable work relates numbers of populations to area of habitat. Although a wide range of relationships could be justified, depending on the spatial and time scales considered, in the absence of information we used the simplest and most intuitive, namely, that changes in population numbers and area correspond in a roughly one-to-one fashion in ecological time. That is, when 90% of an area is destroyed, about 90% of the populations in the original area are exterminated (figure 1). The basis of the difference between the population-area relationship and the species-area relationship is the size of the unit. When a population is destroyed, other populations of the species still may exist elsewhere. Thus, initially the population-loss curve in figure 1 is steeper than the species-loss curve. Eventually, however, when the last populations are destroyed, all the species become extinct as well, and the curves converge.
If, indeed, a one-to-one population-area relationship exists, the rate of population extinction in tropical forests is estimated at 0.8% per year, directly proportional to the rate of habitat loss. Using our mid-range estimate of global population diversity (3.1 billion populations) and assuming that two-thirds of all populations exist in tropical forests (simply because species are distributed in this way), we estimate that 16 million populations per year, or roughly 1,800 per hour, are being exterminated in tropical forests alone. This is an absolute rate of 3 orders of magnitude higher and a percentage rate 3–8 times higher than conservative estimates of species extinction.
Biodiversity at Different Levels.
An investigation of population diversity does not complete the picture of biodiversity. Much remains to be explored at other levels, such as genetic, individual, and ecosystem levels, all of which are tightly interrelated. Little is known about how these different levels of biodiversity relate to ecosystem functioning. For example, for any given population, the number of individuals, the genetic variation between individuals, and the area occupied may affect the delivery of ecosystem services and other benefits provided by that population. The number of blue spruce trees may be important for global services, whereas the density of the trees may be critical for regional flood control. Similarly, although cougars exist in the San Francisco Bay area, the number of individuals is so low that numbers of local deer remain largely unchecked by these natural predators.
The effect of humans on natural areas is so extensive that every level of organization of biodiversity is threatened, even ecosystem diversity. In North America, for instance, the World Wildlife Fund estimates that 32 of a total of 116 ecoregions (that is, ecosystem types) in North America are critically threatened (Ricketts and others 1999). The consequences of the extinction of entire ecosystem types are not known, but the effect could be far-reaching if the particular assemblages of species are important for the delivery of some ecosystem services. In other words, the destruction of ecosystem types not only may result in the loss of the populations and species contained within them, but also may result in the loss of unique processes that are generated by certain combinations of species.
The crisis of biodiversity is more severe than species extinction rates alone would suggest: Population extinction is occurring at a rate that is 3 orders of magnitude higher than the rate of species extinction. The rapid loss of population diversity means the loss of the benefits described above and, in particular, the loss of the life-support systems on which humanity relies. Thus, the destruction and degradation of habitat and the decline of populations are of great concern even when they do not endanger species globally.
This conclusion has direct implications for both conservation biologists and policy-makers. Biologists must emphasize to the public and policy-makers the importance to humanity of all levels of biodiversity, instead of simply species diver-
sity. This shift will require that biologists stress the functional benefits of biodiversity rather than relying only on the charismatic appeal of individual species.
The most important message for policy-makers is one that ecologists long have recognized: Preservation of habitat is crucial for the preservation of biodiversity and the life-support systems that maintain human civilization. The current legislative focus on species conservation neglects crucial dimensions of biodiversity. To protect the benefits that humanity derives from biodiversity, an Endangered Biodiversity Act would be more appropriate than an Endangered Species Act.
Policy-makers also should be putting major effort into developing the field of restoration ecology (Ehrlich and Daily 1993). Unlike species, populations often can be re-established in a relatively short time, and they sometimes evolve with substantial genetic differences from the source populations (Johnston and Selander 1971). Thus, it may be possible to alleviate some of the effects of population extinction, but funds are needed to encourage this line of research.
Finally, the development of an economic-accounting system that internalizes the values of ecosystem goods and services (Costanza and Folke 1997; Goulder and Kennedy 1997) seems critical for the implementation of these policies.
We thank Carol Boggs, Anne Ehrlich, Jessica Hellman, Claire Kremen, John-O Niles, and Taylor Ricketts for many constructive comments. This work has been supported by Peter and Helen Bing, the Pew Charitable Trusts, the Winslow Foundation, and the late LuEsther Mertz.
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Keeping a Finger on the Pulse of Marine Biodiversity:
How Healthy is it?
“If all the beasts were gone, man would die of great loneliness of spirit.”
Chief Sealth of the Duwamish Tribe
in a letter to President Franklin Pierce, dated 1855
Setting the Stage
The world ocean stretches from pole to pole, covers 71% of Earth, and represents more than 99% of the planet's total biosphere volume, or living space. The ocean is nature's ultimate womb. Most scientists believe that life originated there. It is composed of a rich mosaic of habitats large and small, from some of the seemingly most homogeneous and remote, such as the deep-sea floor, to some of the most heterogeneous and accessible, such as the vibrant coral reefs.
The world ocean is the greatest repository of biodiversity at the second highest level of taxonomic organization, the phylum. This level distinguishes organisms according to their basic body plans. Sponges and chordates (which include humans), for example, constitute separate phyla within the animal kingdom. The sequence of phyla roughly reflects the trend in evolution. Of Earth's 33 animal phyla, 28 are found in the ocean, and only 11 are found on land. Moreover, 13 of the animal phyla are endemic (native and restricted) to the marine environment, whereas only one animal phylum is endemic to land: the ancient slug-like Onychophora. At the lowest level of taxonomic organization, the species, biodiversity apparently is much higher on land than in the sea. Yet most of the world ocean is still unsampled, and many of the species collected are still unidentified.
As ocean exploration continues, large numbers of new entries into the library of marine biodiversity are expected at virtually every level of taxonomic organization, particularly at the species level.
The relentless discovery of multitudes of new species, from microorganisms to vertebrates, has driven a revolution in marine taxonomythe identification of species. New techniques, including flow cytometry (described later) and molecular tools involving gene sequencing, now replace or augment traditional, morphology-based methods for classifying and identifying a wide variety of marine organisms. Some new taxonomic capabilities have found immediate applications in conservation. With molecular techniques, for example, some whale species now can be identified solely from the meat that is sold in the marketplace; this facilitates enforcement of restrictions on the hunting of threatened or endangered species.
In the sea, as on land, the greatest threats to biodiversity come from one species, Homo sapiens. The imprint of humans is found throughout the world ocean, but it is most evident and poses by far the greatest threat along its marginsin the coastal zone. Still, documentation of changes in biodiversity caused by human activities is limited by the difficulty in sampling most ocean habitats and identifying the organisms collected. That is, assessing the health of marine biodiversity is seriously hindered because, in most cases, we cannot even take its pulse.
There are several excellent books on the general topic of marine biodiversity, in addition to numerous scholarly articles in the burgeoning primary literature (see list at end). Nearly all were written by scientists for scientists or for scientifically literate readers. As a complement to that literature, this paper describes for the layperson a general picture of biodiversity in the world ocean, how humans are altering it, and the threats that loom on the horizon. We also suggest some elements critical to any integrated management plan for minimizing human threats to marine biodiversity. Thus, this paper celebrates the diversity of marine life at all levels, laments the threats to it, and summons humankind to rise to the challenge of its conservation.
Exploring the Sea
Most people encounter the world ocean only at its margins and experience only a few meters of its depth. Yet the continental shelf, the shallowest region of the sea floor, constitutes a mere 7% of the ocean's area. Of the whole sea floor (about 300 million square kilometers), 83% is more than 1,000 m below the surface and constitutes a zone known as the deep sea. Deep-sea environments are far more difficult to sample and characterize than even the most remote terrestrial habitats. In fact, it is only within the last 50 years that scientists have been able to observe directly, sample, and experiment in untethered “manned” submersibles, like the deep-sea submergence vehicle Alvin (figure 1). But there is a lot of catching-up to do; the deep sea is still the most undersampled marine environment.
Most marine research is done relatively blind from surface research vessels, with nets used to sample the water column and grabs and corers to sample the sea floor. In areas of thousands to tens of thousands of square kilometers, typically less than a square kilometer of the sea has been sampled. That is equivalent to characterizing the entire fauna and flora in a backyard from a sample the size of the head of a pin! Moreover, planktonic (free-floating) and nektonic (free-swimming) marine organisms are constantly in motion, so temporal and spatial variations are easily confounded.
Because of the sampling issues, knowledge of different groups of marine organisms is strongly conditioned by their habitats, their mobility, and the scale of their distributions. In general, distributions of easily accessible, larger, and relatively sedentary organisms (for example, intertidal barnacles and mussels) are better documented than those of inaccessible, smaller, and highly mobile life forms (for example, zooplankton and deep-sea fishes). Microorganisms, which occur in virtually every marine habitat, are by far the most undersampled and undercharacterized. Whales are the largest animals in the world, yet because certain species (for example, blue and sperm whales) are so mobile and can dive deeper than 800 m, there are few accurate estimates of their population sizes, let alone knowledge of their dynamics. Until the 1960s, population sizes were estimated entirely from
visual observations made from whaling vessels. Photographic identification studies and tag-recapture estimates now provide more accurate information on some coastal species (for example, humpback and right whales), but population sizes and movements of off-shore species remain largely a mystery.
The Aqueous Medium
Marine organisms are enveloped by water, whereas terrestrial organisms are enveloped by air, and the differences between these two fluidswater and airaccount for many of the differences in life found in the marine and terrestrial environments. Water is 1,000 times denser than air, and the difference in density has a number of important consequences. First, water acts as a thermostat, buffering against rapid and large changes in temperature not only within the fluid, but for the entire planet. Second, water provides buoyancy that counteracts gravity, reduces the need for physical supporting structures, and facilitates vertical mobility of animals. Third, the much greater kinetic energy (that associated with motion) of water relative to air virtually precludes the existence in the sea of large, rigid, stationary organisms on the scale of trees. And fourth, the much greater dissolving power of water (than of the atmosphere) provides a relatively rich nutritional soup that enables marine plants to receive all their nourishment directly from the enveloping fluid; in contrast, most terrestrial plants require both the atmosphere and the soil to obtain water and nutrients. With respect to optical clarity for photosynthesis, however, the air wins hands down.
The Diversity of Habitats
On land, there are millions of distinct and fixed habitats spanning a large range in size. Some terrestrial habitats are as small as or even smaller than a single tree in a rain forest that supports numerous highly endemic species, and some are as large as the Serengeti plains, stretching for hundreds of kilometers. In the sea, particularly in the water column of the open ocean and over vast expanses of the deep-sea floor, the number of distinctly different habitats is comparatively small. The spatial extent of these habitats is large, however, and marine habitats are intimately connected via the motion and mixing of the fluid medium; thus, endemism is much rarer in the sea than on land. What is surprising is the degree of biological heterogeneitythe biodiversitythat abounds in this seemingly homogeneous seawater medium.
In the sea, organisms have evolved in response to variables other than physical spacevariables that might have no terrestrial analogues. In the open ocean, water circulation patterns can create discrete habitats. In the cold coastal waters of the western North Atlantic, for example, are “warm-core rings” that have pinched off of the swift, northward-flowing Gulf Stream (figure 2). Likewise, semienclosed pockets of cold coastal watercold-core ringscan spin off into the Gulf Stream. Because different species assemblages are associated with different water masses, regional biodiversity is enhanced by these water-mass intrusions.
In the immense sedimentary plains of the deep-sea floor, there is an extraordinary diversity of animals, perhaps rivaling the biodiversity of tropical rain forests. Organisms living on or in the relatively thin layer of sea-floor sedimentsthe
benthoshave evolved largely in response to the highly limited and unpredictable food supply in the deep ocean and thus have remarkable adaptations for exploiting ephemeral and patchily distributed organic matter. In shallow water, benthic organisms experience more habitat variability over small spatial scales than organisms in overlying waters (figure 3). There is also less direct connectivity among habitats in the benthic zone than in the pelagic zone (open water). Thus, most benthic organisms have planktonic larvae (meroplankton) that can expand species distributions over larger areas, provide some insurance against local catastrophic events, and recolonize areas where populations have been eliminated by human activities. The greater habitat diversity and lower connectivity in the benthic zone results in species diversity much greater than that in the water column. Moreover, within the world ocean, the largest number of phyla are represented in the benthos.
In contrast with the seemingly featureless sedimentary sea floor, coral reefs scream and shout with habitat complexity. Coral reefs are, in fact, analogous to rain forests in that the most conspicuous habitat in the reefs is provided by living organismsthe corals themselves. Corals create the underlying structure for the reefs and provide attachment sites for many invertebrates and protection for numerous fishes. Moreover, because corals contain their primary producerstiny algae called zooanthellae that live in the coral tissuethey have a built-in food source. Coral reefs are believed by many marine-biodiversity experts to be the
repositories of the greatest biodiversity in the world ocean if one scales them for size, that is, species per unit area. The other contender for this distinction is the deep-sea floor.
Diversity and Ecosystem Function.
Marine ecosystems are knitted together by relationships among organisms, particularly by who eats whom. In the water column, the food web involves encounters between freely moving predators and prey. Chance, random processes, and adaptation to survive for long periods without food are important driving forces in many more marine than land ecosystems.
Ecosystems have functional attributessuch as the capacity to capture, store, and transfer energy and nutrientsand they also contribute to societal needs. Estuarine ecosystems, for example, tend to have relatively low biodiversity but high productivity, and they contain many commercially important fish and shellfish species. In contrast, coral-reef ecosystems have high biodiversity but low productivity and are now exploited largely for ecotourism.
Some species are more important to the functioning of an ecosystem than others. If they are removed, their roles might be lost, leaving a hole in the food web,
such as a gap in energy transfer, in nutrient cycling, or in some other crucial function. Most critical are the “keystone” species. If one of these is removedby overexploitation or by a natural or human-assisted disasterthe ecosystem changes dramatically. Sea otters are a keystone species of eastern Pacific kelp communities. Sea otters eat sea urchins, which in turn eat kelp. When sea otters were hunted to near extinction along the US West Coast, urchin populations exploded and devoured the kelps, thus turning magnificent, highly diverse kelp forests into featureless sandflats known as “urchin barrens”.
Few marine ecological studies have identified keystone species and other critical relationships between species composition and ecosystem function. Without such knowledge, human activities that involve broad-scale removal of species or alteration of habitat can easily and inadvertently tip the delicate ecological balance, sometimes with disastrous consequences. Overfishing has already greatly diminished most of the large predators of the open ocean; the repercussions have reverberated throughout the food web (figure 4). Moreover, industrial-scale fishing has recently begun to focus on the slow-growing fishes of the largely unexplored deep sea, with unknown consequences. Researchers do not know which or how many of the commercially hunted fishes, shellfishes, or kelps are keystone
species, which or how many have functional equivalents, and whether and how their losses might unravel an ecosystem's intricate web.
The Montage of Marine Biodiversity
In this section, we reveal some of the major components of the montage of marine biodiversity and describe some characteristic properties and processes that contribute to the maintenance of the marine fabric of nature. Examples are chosen to be illustrative; it is impossible to be comprehensive. We close with some observations about the general patterns of marine biodiversity around the world.
There are many similarities between terrestrial and marine environments. Both depend ultimately on photosynthesis for nearly all their energy. Thus, it always starts with plants. Photosynthetic organisms in both environments produce organic material used as food by herbivorous animals, which are preyed on by carnivorous animals to form complex food webs. A primary difference between the terrestrial and marine environments is that in the ocean, most of the plants are microscopic cells floating in the water. These cells are known as phytoplankton.
The Greek root of the word plankton is planktos, which means “wanderer”. And phytoplankton roam the high seas. But for these plant cells to photosynthesize, they must remain in the upper sunlit layerthe euphotic zone. This layer varies in thickness depending on geographic location, but it rarely exceeds 200 m in the open ocean and can be 10 m or less in coastal areas. Staying within the euphotic zone can be challenging for phytoplankton. Gravity pulls them down, and other physical processes, such as convergences (downward-directed currents), transport them away from the light. Phytoplankton have remarkable adaptations that counteract those forces, such as bubbles of fatty material and elaborate spines that reduce sinking.
Collecting and identifying phytoplankton is demanding, to say the least. The cells are so small (0.1–100 mm) and fragile that they are damaged or destroyed by conventional sampling with nets and filters; this makes identification under a microscope laborious or impossible. In contrast, flow cytometrya new nonintrusive technique for counting and identifying phytoplanktonuses a laser to discern the fluorescence characteristics, size, and shape of each cell. In the late 1980s, the shipboard use of this technique led to the discovery of a new group of marine photosynthetic bacteria, the prochlorophytes. These tiny (0.2–2.0 mm) organisms account for up to 40% of all chlorophyll (the major photosynthetic pigment) in some regions of the ocean.
At least one-third of the annual global carbon fixation occurs in the sea. A substantial portion of this carbon is fixed by cells less than 1 mm in size because they are so numerous. Some estimates suggest that the annual fixation of carbon by phytoplankton smaller than 5 mm is similar to that by the world's rain forests. In addition to the importance of phytoplankton to carbon fixation, they can affect marine chemistry by taking up and releasing nutrients. Furthermore, because different phytoplankton species are consumed by different animals, conserving
phytoplankton diversity is critical to conserving the functioning of marine ecosystems.
Whereas phytoplankton account for more than 95% of oceanic primary productivity, the larger multicellular plantsthe macroalgaeseagrasses, and marsh grassesmight be the major producers in some near-shore regions. The kelp forests of temperate, rocky shores host a diversity of animal life, from shellfish to sea otters. Floating mats of brown algae harbor unique animal communities in the open-ocean region of the Sargasso Sea. And seagrasses and marsh plants, occupying critical coastal habitat, stabilize sediments and support distinctive populations of small fishes and invertebrates.
Because of light limitations, all marine plants attached to the bottom are restricted to shallow coastal areas. These ocean habitats are the most directly susceptible to human effects. Because they are close to the shore, attached plants are especially vulnerable to human activities in the sea, such as dredging and sewage disposal, and on land, such as agriculture and urbanization. Entry of suspended sediments and nutrients into the sea from these activities often greatly reduces water clarity (limiting photosynthesis) and degrades habitat (for example, for attachment).
The biology of the sea is driven principally by primary productivity that occurs within a region that accounts for less than 1% of the total volume of the world ocean. Most life in the remaining 99% of the ocean volume depends on food produced within the thin upper layerfood that is either preyed on directly at the surface or scavenged at great depth. Alternative pathways to energy production include sulfur-reducing bacteria that obtain their energy from chemical sources (as opposed to the sun) through a process called chemosynthesis. These primary producers are largely symbiotic, living in tissues of other organisms. Although chemosynthesis produces a small fraction of the sea's total primary productivity, it contributes to marine biodiversity by extending the living space of and facilitating a rich variety of microhabitats.
Most plant food is much smaller in the sea than on land, and so too are most marine primary consumers. The grazersthe zooplankton (“wandering animals”)are small animals that spend either all (holoplankton) or a portion (meroplankton) of their lives in the plankton. Meroplankton are the larval stages of such animals as clams, snails, worms, crabs, and flatfish that, as adults, live on or in the bottom. Meroplankton generally bear no resemblance to the adult form and, like the other plankton, are highly adapted to a suspended existence. Holoplanktonic species dominate the zooplankton in numbers and biomass. They exhibit an extraordinary diversity of form and function, ranging in size from the tiny copepods (hundreds to thousands of micrometers) to the larger jellyfish (millimeters to a few meters).
Nearly all major groups of animals on Earth, except insects, are represented in the zooplankton. Whereas insects, as a group, contain three-fourths of all known animal species on the planet and one-half of all known animal and plant species combined, copepods, the dominant animal group within the zooplankton, have
more individuals than any other group of animals on Earth, except perhaps roundworms. There are an estimated 1 quintillion (1018) copepods in the sea1,000–1,000,000 individuals under each square meter of sea surface!
Although phytoplankton are largely restricted to the upper sunlit layer, zooplankton can extend their realm vertically by migrating. This behavior enhances their living space and provides them wider access to food and more opportunity to escape from predators. Zooplankton are intermediaries in the food web. They eat the primary producersphytoplanktonand are eaten by the secondary consumersfinfish, shellfish, and some whales. Most fish and marine mammals cannot eat phytoplankton directly, but need the zooplankton to repackage them into larger and more nutritious food (like energy bars). Remarkably, however, tiny zooplankton are the major food source for baleen whales, the largest animals on Earth. The mouths of these huge whales contain large comb-like filters called a baleen (figure 5). This sievelike structure retains zooplankton-sized organisms that are slurped off by the whale's tongue. There is no terrestrial analogue for this highly size-disparate food chain, which is more extreme than if an elephant fed on a diet of ants!
There are also benthic grazersa wide variety of suspension-feeding clams, worms, and other invertebrates that extend feeding structures into the water col-
umn, where they actively or passively collect plankton. Because these animals process such large amounts of water and are essentially glued in place on the bottom, they are particularly susceptible to human activities that result in the deposition of particles or pollutants on the sea floor.
Although predatory fishthe predominant secondary consumersswim the entire world ocean, they eat and concentrate in particular areas during important stages of their life cycles, such as reproduction and early development as larvae and juveniles. Thus, for example, salmon return to spawn in the rivers of their births, and eels congregate for mass spawnings in the Sargasso Sea. Protected near-shore areas, such as estuaries and mangrove swamps, are important nurseries for a wide variety of larval and juvenile fishes. Fish can feed at several levels of the food chain, the size of the fish being a relatively good predictor of the size of the prey. Thus, small fish species and larval and juvenile fish eat zooplankton, and bigger fish eat smaller fish.
The coastal ocean has afforded great opportunity for diversification in fish species, providing a wide range of habitats, prey types, and nursery areas. The number of species (13,000) of coastal marine fishes could be more than 10 times greater than the number of species (1,200) of true oceanic fishesthose which spend their entire life cycles in the open ocean. Fish move much more than the food that they prey on. Fish mobility results in cosmopolitan species distributions and blurs the boundaries of biodiversity patterns at any given time.
Marine Mammals and Turtles
Although marine mammals are a relatively small grouponly some 119 speciestheir endearing characteristics have generated a great deal of conservation attention. The ancestors of marine mammals left the land and began their return to the ocean as early as 50 million years ago, evolving a range of diversity greater than what land mammals had left behind.
Whales, manatees, and dugongs are fully adapted to their aquatic habitats, but marine carnivoressea otters, polar bears, seals, sea lions, and walrusdivide their lives between land and sea. Although the diversity of many animal groups, both on land and in the sea, increases in habitats nearer the equator (for example, table 1), seals, sea lions, and walrus show the reverse pattern. Only the rarest species, the monk seal, occurs and breeds in the tropics. Toothed whales are the most diverse group of marine mammals. On the basis of size alone, it might be thought that all marine mammals would have been collected, identified, and described centuries ago. Yet, for the cryptic and difficult-to-study beaked whales, seven new species were described in this century, the most recent one in 1991!
Marine mammals are characterized by their radical anatomical, physiological, and behavioral adaptations to life in the ocean. Manatees and dugongs are marine herbivores; they depend on rich growths of aquatic plants. Other marine mammals are consummate divers, with thick layers of blubber, fur, streamlined bodies, fins, flippers, and other modifications that allow them to remain below the surface for long periods and at extreme depths. Dives of sperm whales and el-
ephant seals, for example, to depths of more than 1,000 m for over an hour have been recorded.
The seven species of sea turtles also spend little time at the surface and cover huge distances on their migratory routes. The largest sea turtle, the leatherback, is warm-bodied, enabling it to live in waters from Venezuela to Newfoundland. Coming ashore to breed on tropical beaches every 2–3 years, these turtles can weigh up to 1,500 lb (680 kg) and dive to more than 600 m.
Some Patterns of Marine Biodiversity and Their Causes
Ptolemy once observed that it is the role of the scientist “to tell the most plausible story that saves the facts.” This charge is difficult when the facts are few and several stories could “save” them equally well. That is often the situation in attempts to generalize about patterns in marine biodiversityfor example, geographically, with depth, or across taxafrom existing data. Keeping in mind that marine biodiversity is grossly undersampled and underdescribed, in table 1 we list some of the general patterns in diversity that are fairly clear.
The Origin of Diversity
In most of this paper, we write about biodiversity as a function of natural communities. Another, fundamental way of looking at biodiversity is as the outcome
of evolutionary processes: the creation and loss of species. Today's biodiversity is only a small sample of the creatures that have come and gone over evolutionary time (Jeffries 1997). The fossil record contains the traces of plants and animals far different from those now occupying ocean habitats.
New species arise from changes in the genetic makeup of subpopulations. In sexually reproducing organisms, one species can become two when subpopulations of the original species become reproductively isolated and thus do not freely exchange genes. If their genetic makeups then diverge so much that the two populations can no longer interbreed, they become separate species. Geographycontinents, islands, submerged mountain ranges, deep-sea canyons, seamountscan isolate populations. Reproductive isolation can also lead to speciation when the breeding seasons or mating behaviors of two subpopulations become sufficiently different.
Physical structure and changes thereof provide opportunities for isolation of populations. Gyres (alterations in oceanic circulation) and land bridges can impose barriers to interbreeding. For example, the Isthmus of Panama separated the Atlantic and Pacific Oceans, isolating many populations that formerly mixed. On the two sides of the isthmus are many common species, but some populations have diverged enough to become separate species.
The Gulf of California formed only 6 million years ago. It is not part of the circulation pattern of the eastern Pacific, so not only do populations of such organisms as sardines, which occur in both water masses, fluctuate independently of one another, but the gulf has endemic species closely related to similar species in the Pacific. For example, the vaquita, an endangered marine mammal closely related to the harbor porpoises of the Pacific and Atlantic, is endemic to the Gulf.
Small marine populations, especially in the nekton, might be less likely to become isolated than terrestrial or freshwater populations of similar size, because of the more “open” nature of marine systems. For example, freshwater covers only 1% of Earth's surface but accounts for 40% of the 23,000 species of fish.
Anthropogenic Threats and Effects
Anthropogenic threats to the biodiversity of the world ocean are in five major categories: overexploitation of resources, pollution, habitat alteration, introduction of exotic species, and global climate change. The first four categories include threats that are both historical and current. Threats to marine life from global climate change are imminent. Marine biodiversity can be affected by a single threat or several threats, sometimes with devastating and unknown consequences (figure 6). The vast oyster reefs of the Chesapeake Bay, for example, that once filtered the estuary's entire volume every week, now filter it only once a year because of stock depletion due to overfishing, pollution, habitat alteration, and disease.
If we were to give the world ocean the equivalent of a physical examination to determine its fitness, a strong, rhythmic heartbeat would represent the healthy system that was characteristic of prehuman timesand indeed typical of most areas until several thousand years ago. Human activities, however, have caused
a rapid deterioration in the health of many marine ecosystems. Understanding the history of effects on marine biodiversity from the four current anthropogenic threats is important for developing strategies to minimize future effects. Maintaining healthy marine ecosystems requires constant vigilance; keeping a finger on the pulse of marine biodiversity could save its life and the critically important ecosystem services that it provides.
Overexploitation of Resources
Overfishing has dramatically reduced the stocks of many, perhaps most, of the preferred edible fish and shellfish species in the world ocean and led, for example,
to recent closures of the so-called inexhaustible great fishing banks, such as Georges Bank and the Grand Banks. Entire marine ecosystems have been severely, perhaps irreversibly, altered because of overexploitation of top carnivores and grazers. The herbivorous green turtle population in the Caribbean, for example, likely numbered 60–300 million individuals in the 17th century, before the exploration of the New World. The current population numbers only in the tens of thousandsa reduction of more than 99%! Now, several centuries later, we can only speculate on the vast changes in the natural marine ecosystem that resulted from this dramatic decline in perhaps the largest marine reptilian population in the Caribbeana decline attributable almost entirely to human hunting.
Human hunting (of fish, shellfish, vertebrates, reptiles, and birds) and collecting (of seaweeds, sea urchins, shells, and corals) has removed or nearly removed ecologically important species from otherwise balanced food webs and has had substantial indirect effects, including by-catch and by-kill (the incidental take of nontargeted species), such as the hooking of sea turtles and albatross on longlines used to fish for tuna and swordfish (figure 4); destruction or disturbance of habitat, such as critical sea-floor habitat of benthic invertebrates by shellfish dredges and bottom-fish trawls; and genetic changes, such as the regional hunting to local extinction of some whale species, which decreases the total genetic material in the species's gene pools.
For over a century, the coastal ocean has been assaulted with large quantities of various municipal, industrial, agricultural, and human wastes. For example, chemical pollutants have caused tumors and diseases in fish and shellfish and have affected reproduction in seabirds (DDT made pelican eggshells so thin that they broke when the birds sat on them); oil spills have resulted in local mass deaths of organisms at virtually every link in the food chain; agricultural fertilizers have killed coral reefs by stimulating the growth of seaweeds that overgrow them; and nutrient enrichment in estuaries has stimulated large algal blooms that sometimes lead to the consumption of most of, or all, the oxygen in the water column and deaths of immobile organisms. Although coastal habitats will continue to receive most of the human-derived wastes, the deep sea has been proposed as an additional dumping ground, especially for radioactive material. Dumping one of the most dangerous waste materials in the least-studied marine environment with, arguably, the highest biodiversity on Earth should be reason for great concern.
Coastal habitats have been decisively altered to accommodate the “needs” of human society. For example, large portions of wetlands and salt marshes have been eliminated by dredging, filling, and diking to create new fastlands (dry land), and large areas of mangrove swamps have been altered to create shrimp ponds for aquaculture. Salt marshes and mangroves are highly productive marine systems that serve as nursery grounds for young fish. Seawalls, jetties, and groins, by design, alter the natural currents and thus can affect transport of organisms in the water or organisms that depend on it for food or respiration. Mining (upland and
coastal) and deforestation cause erosion on land that ends up in the sea. Increased suspended sediment negatively affects such organisms as corals, which require clear water for photosynthesis by their symbiotic zooanthellae. Clear waters once characterized virtually all tropical areas, but no more.
Introduction of Exotic Species
A startling array and number of marine organisms have been transported around the world ocean by humans, principally in the ballast water of ships. Water is pumped into a ship's hold in one port to stabilize its load and then pumped out in another, sometimes halfway around the globe. Introduced species can outcompete and even eliminate local species. Several introductions have changed entire ecosystems. The European zebra mussel introduced into the Great Lakes led to economic losses of hundreds of millions of dollars per year, and the carnivorous American comb jellyfish introduced into the Black and Azov Seas caused declines in the zooplankton biomass of up to 90% and resulted in large declines in the anchovy fishery (anchovies eat zooplankton).
Global Climate Change
For decades, human activities have been generating compounds that rise into the atmosphere and destroy the ozone that shields the planet from the sun's ultraviolet radiation (UV). If such activities continue, marine organisms might suffer because phytoplankton, zooplankton, fish, corals, and benthic organisms experience harmful effects from biologically damaging ultraviolet radiation (UV-B). Global warming caused by enhancement of the “greenhouse effect” (wherein such gases as CO2 and CH4, generated by human activities, prevent the escape of heat radiating from Earth) is expected to cause a substantial increase in sea level and alter ocean circulation. Adaptation typically occurs over very long periodsthousands to millions of years. Thus, marine biodiversity could be seriously affected if organisms cannot adapt to human-accelerated global climate changes that take place over decades or perhaps a century.
The most vulnerable parts of the sea are the coastal areas, the focal point of most human activities that threaten marine biodiversity. Assaults on the coastal ocean have been relentless and, in many parts of the world, are still increasing in magnitude, persistence, and area affected. The cause is continuing human population growth, which is disproportionately faster in coastal areas.
Throughout the United States and the world, about 50% of the human population inhabits a narrow fringe around the periphery of the continents, a coastal region that is only 100 km wide. That percentage and the absolute numbers of human beings are increasing each year, and society as a whole is experiencing a new phenomenonthe emergence along the coasts of “mega-cities”, cities with populations over 10 million (table 2). Moreover, most mega-cities are now in the developing world. Because the developing world is concentrated in tropical and subtropical areas, mega-cities occur in coastal regions that have the highest ma-
rine biodiversity. Large human populations inevitably result in large effects on the natural environment, so all biodiversitymarine and terrestrialin these regions is at high risk.
Cities and countries in the developing world do not yet have the infrastructure to deal with the environmentally unforgiving consequences of highly localized human populations, such as overexploitation of resources, habitat alteration, and pollution. Thus, wave after wave of unprocessed or uncontained human, municipal, industrial, and agricultural wastes will continue to travel across the land-sea interface unless steps are taken quickly to forestall this situation.
Clearly, humans have been having large, negative effects on marine biodiversity. Luckily, they also can do something about it. It is ridiculous to ask humans, animals with a right to life on this planet, to have no impact on the environment. Virtually every other species has some impact. In fact, herein lies the origin of “ecology”the study of relationships between organisms and their environment. But what members of Homo sapiens have over other species is the right to choose their impacts and to minimize those which must occur. The foundation for such decisions is in knowledge of natural patterns of biodiversity and the processes that maintain them. Such data are, however, meager, at best, for most organisms in most environments in the sea.
Entire issues of journals and several books have been devoted to strategies and tactics for conserving marine biodiversity at all levels. Our purpose here is much more modest: to identify some critical concepts that form a foundation on which to build any comprehensive, integrated, and sustainable initiative to conserve marine biodiversityconcepts that derive principally from the distinctiveness of marine, compared with terrestrial, systems (table 3)and to emphasize the importance of raising public awareness and understanding of the need to conserve marine biodiversity.
There is no comprehensive, coherent, integrated plan for conserving the world's marine biodiversity. Development of such a plan will require far greater knowledge than exists today and far greater cooperation across multiple jurisdictions
than has ever occurred. And it all starts with goals. Goals for conserving marine biodiversity should be stipulated both in terms of values and uses important to society, with measurable and understandable performance indicators, and in terms of the fundamental value of biology. Furthermore, the effective development and execution of any conservation initiative requires a serious reconnection of people with nature. The best opportunity for broad-scale public education and involvement in conserving marine biodiversity is at the coast, where people are most likely to experience and appreciate the sea. The International Year of the Ocean, 1998, was an excellent starting point for global participation. One vehicle for raising public awareness could be the international network of aquariums, which draw more than 200 million visitors each year and where specific local and regional marine-biodiversity issues can be placed in a global context. Whatever the tactics, they must be developed now, lest our children and theirs know not the magnificent beauty and bounty of the sea.
The world ocean is experiencing substantial and startling losses of biodiversity. Arguments about whether coral reefs or rain forests support the greatest diversity are silly and dangerous; they divert attention from the real issues. Conservation of the planet's biodiversitymarine and terrestrialis critically important. We choose the word conservation advisedly. Biodiversity cannot be preserved; it can and must be protected or conserved. Evolution and extinction are natural processes. But now, for the first time in the planet's history, one speciesourshas demonstrated its capacity to destroy large numbers of other species and their habitats. Never before has one species had such a profound, pervasive, and pernicious effect on so many others. Ironically, the other creatures with which we share this planet would be far better off in the absence of “intelligent life”.
We thank Bob Beardsley, Brad Butman, Just Cebrian, Mark Chandler, Gregory Early, Scott Kraus, Ken Mallory, Dan Pearlman, Carl Safina, Vicke Starczak, Gregory Stone, and particularly Carolyn Levi, for ideas, information, and suggestions for improving this paper. Jayne Doucette and Jack Cook did the graphic illustrations, for which we are grateful. We thank Paul Erickson for the slide show that was part of the oral presentation. C.A. Butman was supported by a Pew Charitable Trusts Fellowship in Conservation and the Environment. This is Contribution 9620 from the Woods Hole Oceanographic Institution.
Suggestions for Further Reading
Angel MV. 1993. Biodiversity of the pelagic ocean. Cons Bio 7:760–72.
Butman CA, Carlton JT. 1995. Marine biodiversity: some important issues, opportunities and critical research needs. Rev Geophys Suppl:1201–9.
Chandler M, Kaufman L, Mulsow S. 1996. Human impact, biodiversity and ecosystem processes in the open ocean. In: Mooney HA, Cushman JH, Medina E, Slaad OE, Schulze ED (eds). Functional roles of biodiversity: a global perspective. New York NY: J Wiley. p 431–74.
Dobson AP. 1996. Conservation and biodiversity. New York NY: Sci Amer Lib. p 264.
Huston MA. 1994. Biological diversity: the coexistence of species on changing landscapes. New York NY: Cambridge Univ Pr. p 681.
Jackson JBC. 1997. Reefs since Columbus. Coral Reefs 16 Suppl:S23–S32.
Jeffries MJ. 1997. Biodiversity and conservation. New York NY: Routledge. p 208.
NRC [National Research Council]. 1995. Understanding marine biodiversity: a research agenda for the nation. Washington DC: National Acad Pr. p 114.
NRC [National Research Council]. 1996. Stemming the tide: controlling introductions of non-indigenous species by ships' ballast water. Washington DC: National Acad Pr. p 141.
Norse EA (ed). 1993. Global marine biodiversity: a strategy for building conservation into decision making. Washington DC: Island Pr. p 383.
Oceanus. 1995. Marine biodiversity I. Fall/Winter.
Oceanus 1996. Marine biodiversity II. Spring/Summer.
Safina C. 1995. The world's imperiled fish. Sci Amer 273:46–53.
Perlman DL, Adelson G. 1997. Biodiversity: exploring values and priorities in conservation. Malden MA: Blackwell. p 182.
Perrings C, Maler KG, Folke C, Hollings CS, Jansson BO (eds). 1995. Biodiversity loss: economic and ecological issues. New York NY: Cambridge Univ Pr.
Peterson M (ed). 1992. Diversity of oceanic life: an evaluative review. Washington DC: The Center for Strategic and Information Studies. p 108.
Reaka-Kudla ML, Wilson DE, Wilson EO (eds). 1997. Biodiversity II: understanding and protecting our biological resources. Washington DC: Joseph Henry Pr. p 551.
Wilson EO (ed). 1988. Biodiversity. Washington DC: National Acad Pr. p 521.
Countryside Biogeography and the Provision of Ecosystem Services
Humanity has become a dominant force on Earth, altering important characteristics of the atmosphere, oceans, and terrestrial systems. One of the many consequences of these alterations is the extinction of populations and species, which is projected to drive biodiversity to its lowest level since humanity came into being (Ehrlich and Ehrlich 1981; Wilson 1992). A crucial set of policy questions is when, where, and how to direct societal activities to soften or reverse their effect on biodiversity.
In addressing these questions, one is immediately confronted with a set of trade-offs in the allocation of resources (such as land and water) to competing uses, to competing individuals and groups of people, and ultimately to competing value systems. These tradeoffs are becoming increasingly vexing from both ethical and practical perspectives. They involve our most important ideals (such as ensuring a prosperous future for our children), our oldest tensions (such as between individual and societal interests), and sometimes our bloodiest tendencies (such as using genocide as a convenient way of gaining control over resources). Society is poorly equipped to handle these tradeoffs, and they are appearing everywhere; the well-being of current and future generations hinges on how the tradeoffs are dealt with.
The short-term benefits of alteration of habitats, the primary cause of loss of biodiversity, are typically clear and allow relatively small groups of immediate beneficiaries to exert great influence on the political process in favor of short-term exploitation. In contrast, the arguments for conservation tend to be diverse and difficult to measure, and the benefits of any single decision about conservation are
diffused over very large numbers of people. The arguments for conservation typically are drawn from any of four distinct lines of reasoning: ethical, aesthetic, direct economic, and indirect economic (Heywood 1995; Hughes and others 2000; Ehrlich and Ehrlich 1992). Ethical reasoning involves the conviction that, as the dominant species on the planet, humanity has the responsibility of stewardship toward “The Creation,” its only known living companions in the universe. This moral responsibility exists independent of the perceived value of nonhuman organisms to human well-being. The other three classes of argument rest on the benefits that humanity derives from other organisms, which I collectively refer to here as “ecosystem services.”
The reasons for stemming the loss of biodiversity thus range in character from the intangible, the spiritual and philosophical, to the purely anthropocentric and pragmatic (for a nice overview, see Goulder and Kennedy 1997). One might say they span the spectrum from things that make life worth living to things that make life possible at all. Clearly, both ends of the spectrum are important, although the significance ascribed to each varies considerably with social context and understanding. Lack of public understanding of societal dependence on natural ecosystems is a major hindrance to the implementation of policies needed to bring the human economy into balance with the capacity of Earth's life-support systems to sustain it.
The purpose of this paper is to explain this dependence briefly, to describe how recognition of it can help resolve the tradeoffs that society now faces, and to indicate where society could invest profitably in broadening and deepening the scientific understanding of ecosystem services. First, I briefly characterize ecosystem services in biophysical and economic terms. Then, I indicate how the concept provides a framework that, if supported with appropriate institutions and policies, allows us to incorporate ecosystem-service values into decision-making. Finally, I turn to a key underlying biological issue: the capacity of human-dominated landscapes to support biodiversity and sustain ecosystem services. My emphasis throughout is on the anthropocentric and pragmatic.
Life on the Moon.
Society derives a wide array of life-support benefits from biodiversity and the natural ecosystems within which it exists. These benefits are captured in the term “ecosystem services”, the conditions and processes through which natural ecosystems, and the species that are a part of them, sustain and fulfill human life (Daily 1997; Holdren and Ehrlich 1974). These services include the production of ecosystem goods, such as seafood, timber, forage, and many pharmaceuticals, which represent an important and familiar part of the economy.
Perhaps the easiest way to appreciate the importance of biodiversity in supplying life-support goods and services is by way of a thought experiment that removes the familiar backdrop of Earth. Imagine trying to set up a happy life on the moon. Assume for the sake of argument that the moon miraculously already had some of the basic conditions for supporting human life, such as an atmosphere, a climate, and a physical soil structure similar to those on Earth. After packing one's
possessions and coaxing one's family and friends into coming along, the big question would be, Which of Earth's millions of species would be needed to make the sterile moonscape habitable?
One could choose first from among all the species used directly for food, drink, spices, fiber, timber, pharmaceuticals, and industrial products, such as waxes, rubber, and oils. Even if one were selective, this list could amount to hundreds or even thousands of species. And one would not have begun considering the species needed to support those used directly: the bacteria, fungi, and invertebrates that recycle wastes and help make soil fertile; the insects, bats, and birds that pollinate flowers; and the herbaceous plants, shrubs, and trees that hold soil in place, nourish animals, and help control the gaseous composition of the atmosphere that influences Earth's climate. No one knows exactly how many or which combinations of species would be required to support human life. So, rather than listing individual species, one would have to list instead the life-support services required by the lunar colony and try to choose groups of species able to perform them. A partial list of such services includes the following (Daily 1997):
• production of a wide variety of ecosystem goods;
• purification of air and water;
• mitigation of flood and drought;
• detoxification and decomposition of wastes and cycling of nutrients;
• generation and preservation of soils and renewal of their fertility;
• pollination of crops and natural vegetation;
• dispersal of seeds;
• control of the vast majority of agricultural pests;
• maintenance of biodiversity;
• protection from the sun's harmful ultraviolet rays;
• partial stabilization of climate;
• moderation of weather extremes and their effects; and
• provision of aesthetic beauty and intellectual stimulation that lift the human spirit.
The closest attempt to carry out this experiment here on Earth was the first Biosphere 2 “mission” (Cohen and Tilman 1996). A facility was constructed on 3.15 acres in Arizona that sealed off its inhabitants as much as possible from the outside world; eight people were meant to live inside for 2 years without the transfer of materials in or out. The experimenters had to decide which species to use to populate the closed ecosystem. They moved in tons of soil (with its huge abundance and variety of little-known fungi, arthropods, worms, and microorganisms), added numerous other animals and plants, and fueled the system with sunlight (through transparent walls) and electricity (at an annual cost of about $1 million). Biosphere 2 featured agricultural land and elements of a variety of natural ecosystems, such as forest, savanna, desert, and even a miniature ocean.
In spite of an investment of $200 million in the design, construction, and operation of this model Earth, it proved impossible to supply the material and physical needs of the eight “Biospherians” for the intended stay. Many unexpected and
unpleasant problems arose, including a drop in the concentration of oxygen from 21% to 14%, a level normally found at an elevation of 17,500 ft; skyrocketing concentrations of carbon dioxide with large daily and seasonal fluctuations; high concentrations of nitrous oxide to the point where brain functioning can be impaired; extinction of 19 of 25 vertebrate species; extinction of all pollinators (thereby dooming most of the plant species to eventual extinction); population explosions of aggressive vines and crazy ants; and failure of water-purification systems.
The basic conclusion from this experiment is that there is no demonstrated alternative to maintaining the viability of “Biosphere 1,” Earth (Cohen and Tilman 1996). Ecosystem services operate on such a grand scale and in such intricate and little-explored ways that most could not be replaced by technological means (Ehrlich and Mooney 1983). They existed for millions or billions of years before humanity evolved, making them easy to take for granted and hard to imagine disrupting beyond repair. Yet escalating effects of human activities on natural ecosystems now imperil the delivery of these services. The primary threats are changes in the uses of lands, causing loss of biodiversity and facilitating biotic invasion, and synergisms of these with alteration of biogeochemical cycles, release of toxic substances, possible rapid change of climate, and depletion of stratospheric ozone (Daily 1997b).
Management of Natural Capital
Maintaining Earth as a suitable habitat for Homo sapiens will require society to begin to recognize natural ecosystems and their biodiversity as capital assets, which, if properly managed, will yield a flow of benefits over time. Relative to physical capital (buildings, equipment, and so on), human capital (skills, knowledge, health, and so on, embodied in the labor force), and financial capital, natural capital is poorly understood, little valued, scarcely monitored, and undergoing rapid depletion. Sustainable management of ecosystem services will require a systematic characterization of the services, in biophysical, economic, and other terms along with the development of financial mechanisms and policy institutions to provide the means of monitoring and safeguarding them.
Characterization involves an explicit cataloging of important services on a variety of scales. In other words, which ecosystems supply what services? For a given location, which are supplied locally, which are imported, and which are exported? Characterization also involves finding answers to other questions (Costanza and Folke 1997; Daily 1997c; Holdren 1991), such as, what is the effect of alternative human activities on the supply of services?
The administration of New York City first considered replacing its natural water-purification system (the Catskill Mountains) with a filtration plant but found that it would cost an estimated $6–8 billion in capital plus $300 million per year to operate. The high costs prompted investigation of an alternative solution, namely restoring and safeguarding the natural purification services of the Catskills. That would involve purchasing land in and around the watershed to protect it and subsidizing several changes on privately owned land: upgrading sewage-treat-
ment plants; improving practices on dairy farms and undertaking “environmentally sound” economic development. The total cost of this option was estimated at about $1.5 billion (Revkin 1997).
Thus, New York City had a choice of investing in $6–8 billion in physical capital or $1.5 billion in natural capital. It chose the latter option, raising an environmental bond issue to fund its implementation. This financial mechanism captured the important economic and public-health values of a natural asset (the watershed) and distributed them to those assuming the responsibilities of stewardship for the asset and its services.
The Catskills supply many other valuable services, such as control of flooding, sequestration of carbon, conservation of biodiversity, and, perhaps above all, beauty, serenity, and spiritual inspiration. Moreover, these services benefit others besides consumers of water in New York City. It would be absurd to try to express the full value of the ecosystem services provided by the Catskills in dollars. In this case, fortunately, there was no reason to try: even a lower estimate of the value of the natural asset was sufficient to induce adopting a policy of conservation.
The challenge is to extend this model to other geographic locations and to other services. The US Environmental Protection Agency recently estimated that treating, storing, and delivering safe drinking water to the United States without taking this approach would require an investment in physical capital of $138.4 billion over the next 20 years. More than 140 municipalities in the United States now are considering watershed protection, an option that aligns market forces with the environment, as a more cost-effective option than building artificial treatment facilities (The Trust for the Public Land 1997). Indeed, interest is growing worldwide in adopting watershed conservation. Rio de Janeiro and Buenos Aires, for example, are investigating this option; both have highly threatened watersheds of enormous biotic value (Chichilnisky and Heal 1998).
Extending this model to other services requires that an ecosystem meet two conditions. First, it must supply at least one good or service to which a commercial value can be attached. Second, some of that value must be appropriable by the steward of the ecosystem (Chichilnisky and Heal 1998). Public goods and services are difficult to privatize: if provided for one, they are provided for all, so their providers typically cannot appropriate all the value of the good or service. Natural water purification is a public service, but access to the resulting high-quality water is excludable; thus, the case of a watershed works by bundling a public service with a private good. Private capital could be mobilized in this cause to the benefit of both individual investors and society at large (Chichilnisky and Heal 1998).
In principle, this approach could be made to work for other ecosystem goods and services, such as for realizing and safeguarding biodiversity, ecotourism, and carbon-sequestration values. With appropriate institutional support (such as that needed for the management of common property resources), mechanisms for safeguarding sources of flood control, pollination, and pest-control services also may be developed. This is an important subject for further interdisciplinary investigation by persons from academe, government, and the private sector.
Attaining the ultimate goal of sustainably managing natural capital will require a deeper understanding of the relative effects of alternative activities on biodiversity and ecosystem services. A key question is, Where do critical thresholds lie in the relationships between the condition and extent of an ecosystem and the quality of the services that it supplies? Let us explore this issue from the perspective of the modification of ecosystems by agricultural activities.
Food production is arguably humanity's most important activity. It is also the most important proximate cause of the loss of biodiversity worldwide, involving major direct and indirect effects, including conversion of natural habitat to agricultural use, facilitation of biotic invasion through trade (thereby increasing the rate of introduction of exotic species) and alteration of habitat (thereby increasing the susceptibility of native communities to invasion), and application of chemical fertilizers and pesticides.
In the face of such effects, the fates of organisms that once made their homes in unbroken expanses of natural habitat range along a broad continuum. At one end is the decline of population to local and eventually global extinction; at the other end is expansion into human-controlled landscapes. Biologists have paid considerable attention to the status of the biotas of fragments of natural habitat, such as forest patches, and comparably little attention (outside the context of pest management) to the organisms that occupy the highly disturbed matrix in which those fragments occur. One reason for this emphasis is undoubtedly the crisis nature of extinction: given the justified panic to save remaining natural habitat, it is taking some time to appreciate a complementary opportunity, namely, to enhance the hospitability of agricultural landscapes for biodiversity. The emphasis traces to other factors, including the prominence of the theories of island biogeography and the island paradigm in conservation biology; the assumption that a very small fraction of species is capable of persisting outside of “islands” of natural habitat, that is, in human-controlled habitats; and the frequent (although often subconscious) projection of disdain for humanity's destruction of natural habitat onto the organisms that profit from it.
The organisms that can take advantage of countryside, rural and suburban landscapes devoted primarily to human activities, deserve more attention for a series of reasons. First, it is unlikely that many large, relatively undisturbed tracts of natural habitat will remain in the face of projected growth in the size, food needs, and environmental effects of the human population. Second, the potential for conserving many species might rest on preserving or enhancing some aspects of rural landscapes that contain remnants of native habitat in lieu of protecting large tracts of undisturbed habitat, which is generally much less feasible socioeconomically. Third, the supply of some important ecosystem servicessuch as pest control, pollination, and water purificationwill depend in many instances on the biodiversity that occurs locally, in the vicinity of human habitation, in countryside habitats. Finally, a growing interest in restoration also will require comparing the conservation value of alternative sites for the establishment and succession of desired community assemblages.
Countryside biogeography is the study of the diversity, abundance, conservation, and restoration of biodiversity in rural and other human-dominated landscapes. Broad issues in this area pertain to the future course, societal consequences, and appropriate policy responses to the mass extinction currently under way. They include the following sorts of questions.
• What is the relationship between levels of agricultural intensification and biodiversity in countryside landscapes? Measures of agricultural intensification include the frequency distribution of clearing sizes, the ratio of clearing to hedgerow areas, the spatial configuration and relative coverage of native and human-dominated habitats within the countryside landscape, the diversity of crops under cultivation, modification of the hydrological cycle, and the levels and types of chemical fertilizers and pesticides applied.
• Which species traits confer an advantage for survival in the face of tropical deforestation and other major alterations of habitat?
• Are these traits distributed randomly across taxa, or are some groups of organisms especially resistant and others especially prone to extinction? In other words, will the current episode of extinction nip off the buds of the evolutionary tree of life relatively uniformly, or will it eliminate some major limbs, dramatically reshaping the future diversity and evolution of life?
• Can simple mathematical theory be developed to predict patterns of persistence of biodiversity in countryside landscapes?
• How accurately can patterns of biodiversity in countryside habitats be predicted on the basis of remotely sensed information on land use (for example, with images from satellites)?
• How effectively can countryside biotas perform ecosystem services?
• What practical measures can be taken to enhance the capacity of countryside habitats to sustain biodiversity and ecosystem services as well as human activities?
This is not the place for a comprehensive review of work addressing those issues. I offer instead a few illustrative findings to date:
• In Europe, more than 50% of the land area with high conservation value is under low-intensity farming. Examples of these habitat types include blanket bog, northern Atlantic wet heath, lowland hay meadow, heather moorlands, wood pasture, alpine pasture, and nonirrigated cereal steppe (Bignal and McCracken 1996). Intensification of farming practices in recent decades has resulted in declining populations of many species of birds throughout Europe. For instance, nine of the 11 species of waders listed in the Red Data Book that occur in Sweden are seriously threatened by changes in farming practices there (Johansson and Blomqvist 1996).
• Recent studies are beginning to illuminate the strength and type of biotic control over the functioning of ecosystems (Chapin and others 1997). Greater richness of species can enhance the stability of the ecosystem. In species-poor plots of grassland in Minnesota, for example, a severe drought caused a reduction
in productivity of more than 90% from predrought levels, whereas productivity in species-rich plots was reduced by 50% (Tilman 1994). Alterations in habitat that change the functional diversity and composition of plant species appear especially likely to have major effects on various properties of ecosystems (Hooper and Vitousek 1997; Tilman and others 1997).
• In the vicinity of Las Cruces in southern Costa Rica, a significant fraction of the native avian species appear to be persisting, at least temporarily, in open countryside habitats in a mixed-agricultural landscape that retains 27% of its once-continuous forest cover. Of possible original totals in the 33 species of birds under consideration, it appears that 1–9% have become extinct locally, 50–54% are restricted to habitats of forested countryside, and 36–40% occur in habitats of open countryside that are as far as 6 km from the nearest large tracts (at least 200 hectares) of forest (Daily and others in review).
• Some systems of cultivation used in coffee production appear to have high potential for conserving birds and other elements of the native biota. Systems of cultivation that use shade trees, plantations with tall canopy cover, diverse stratification, little pruning, and low levels of insecticides are especially rich in birds, including both resident and neotropical migrant species (Greenberg and others 1997). Strikingly high abundances of arthropods and richness of species have also been found. For example, fogging of shade trees with pyrethrins in a Costa Rican coffee plantation in formerly upland-rainforest habitat yielded a richness of coleopteran and hymenopteran species comparable with that of samples from trees in upland rainforests in Peru and Brazil (Perfecto and others 1996).
• Nocturnality might confer an advantage of dispersal and possibly of survival in the face of tropical deforestation. Surveys of the diversity of diurnal birds and butterflies and nocturnal beetles and moths in forested patches reveal the classic island biogeographic pattern for birds and butterflies (in other words, fewer in smaller patches) but similarly high diversities of moths and beetles among forested patches of all sizes (0.1–225 hectares). A possible mechanism explaining this apparent advantage is that typically the movement of nocturnal species occurs when the conditions of thermal, humidity, and solar radiation are similar between native forest and cleared areas; during the day, the hot, dry, and bright conditions in open areas might impede dispersal seriously for many organisms (Daily and Ehrlich 1996).
Ideally, further effort in empirical and theoretical research on issues of countryside biogeography eventually will allow us to predict patterns of biodiversity in human-dominated landscapes worldwide (White and others 1997). This would be an important step toward characterizing and monitoring the effects of humans on ecosystems and the services they supply.
The human population and its standards of living are maintained by a steady depletion of natural capital assets, including renewable-resource stocks and waste sinks that, if they were safeguarded, could sustain a flow of ecosystem goods and
services through time. In our collective behavior, there is little recognition or systematic accounting, let alone nurturing, of these critical capital assets.
Tremendous payoff could result from further research on managing Earth's life-support systems. Such research should be oriented toward developing the following:
• a broader and deeper understanding of the functioning of Earth's life-support systems and the effects of humanity on them, especially in countryside habitats;
• systematic accounting and monitoring of the condition of these systems;
• ways of quantifying the importance of ecosystems at the margin, from biophysical, economic, and cultural (aesthetic and spiritual) perspectives, that is, ways of determining, for instance, how much importance should be attached to the preservation or destruction of the next unit of habitat;
• ways of incorporating these values into a framework for decision-making; and
• ways of creating appropriate institutions and policies to allow the individuals or societies that safeguard life-support systems for the public good to realize the value of their stewardship.
In the market-driven culture that prevails today, the concept of ecosystem services offers a new way to approach actions of conservation by confronting market forces on their own terms. This concept has promise because it integrates biophysical and social dimensions of managing the biosphere; it offers rational, practical solutions to tradeoffs in allocation of resources to competing uses and people; and it is adaptable to different economic and cultural circumstances. Similarly, countryside biogeography can reveal new strategies for preserving biodiversity and ecosystem services in the context of some of humanity's most important activities. Nevertheless, these frameworks are just two tools to complement the many others required for protecting biodiversity (Raven 1990; Raven and Wilson 1992). In our quest to safeguard the systems that make life possible, it is critical that we not lose sight of what makes life worth living.
I am grateful for insightful comments from Scott Daily, Michael Dalton, Paul Ehrlich, Geoffrey Heal, and Jennifer Hughes. This work was supported by the generosity of Peter and Helen Bing, the Pew Charitable Trusts, and the Winslow Foundation.
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