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PART 5—
THREATS TO SUSTAINABILITY



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Page 301 PART 5— THREATS TO SUSTAINABILITY

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Page 303 Nature Displaced: Human Population Trends and Projections and their Meanings. Richard P. Cincotta Robert Engelman Population Action International, 1120 19th Street, NW Ste. 550, Washington, DC 20036-3678 Unlike the great species extinctions of Earth's past, the one occurring today is less an episode than a process, whose full results will not be known for hundreds of years. Between the linked human-induced phenomena of global climate change and biodiversity loss, the planet could be passing into the equivalent of an entirely new geological epoch in just a few human generations. Or it could be that biodiversity loss will amount to little more than a manageable depletion, incurring regrettable scientific and economic losses but leaving the basic services provided by most major ecosystems largely intact. The size and distribution of human population over the near and distant future will surely be a dominant factor in determining whether the loss of biodiversity that the world faces turns into merely a source of wistful regret for future generations, a planetary catastrophe, or something in between. Population growth enlarges the scale and extent of the human enterprise and hence inflates the likelihood that human activities will push native nonhuman populations and biotic communities past critical thresholds of tolerance and renewal. Demands for housing (Mason 1996), food energy and arable land (Bongaarts 1994; Engelman and LeRoy 1995; Smil 1994), freshwater (Engelman and LeRoy 1993; Falkenmark and Widstrand 1992), and industrially fixed nitrogen (Howarth and others 1996; Smil 1991; Vitousek and others 1997) appear more sensitive to the growth of human population than to the growth of per capita income or even to recent changes in technological efficiency. Habitat conversion, historically the greatest threat to biodiversity, has been driven by these very demands—by housing needs, pressures to expand and intensify agriculture, and the quest to harness

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Page 304 additional freshwater supplies. Climate change, the demise of commercial fish populations and coastal reefs, widespread soil degradation, and the re-emergence of infectious disease also reflect the strong influence of population dynamics and take a growing toll on biodiversity. These global changes threaten ecosystem function and raise the risk of future extinction. It thus makes sense to consider the prospects for human population growth. In this article, we consider those prospects by examining the United Nations (UN) population projections—both how and what they project. The methods and meaning of UN projections are poorly understood by scientists outside the field of demography. And the recent misuses of the projections in the press have confounded the public. Despite widespread perceptions to the contrary, there is nothing inevitable about most future human population growth. Our species now numbers 6 billion and is growing at a pace of just over 80 million per year. More than 95% of this growth is occurring in countries of the developing world. Most demographers expect human population at least to approach 8 billion in the next half-century. Beyond that expectation, however, no one can be certain that world population will ever rise to greater levels. There is equal uncertainty that population will stop growing at any particular time in the not too distant future. We can be certain, however, that today women in most developing countries desire fewer children than their mothers or even their older sisters sought or had (Westoff 1991). Over the last 30 years, that trend, when supplemented with access to modern contraception and the information needed to use it safely and effectively, clearly has resulted in lower rates of childbearing in countries with traditionally high fertility (Robey and others 1994). In the future, changes could occur even more rapidly. Decisions made today will have an enormous influence on the demographic future. These decisions are likely to be among the most important that we can make to conserve as much as possible of the planet's remaining biodiversity. Humanity's Place in Nature Few scientists outside the field of ecology are aware of how ecologically unprecedented is the scale of human numbers—not just present numbers, but also those of the last several millennia. No other mammal of comparable body weight has ever attained anywhere near such abundance. By manipulating the qualities and quantities of other species through agriculture, Homo sapiens broke through the energy and nutrient constraints that limited it as a hunter-gatherer. Statistical models relating the adult body weight of mammals to their observed abundance (Peters 1983, p 166–7) predict that the equilibrium density of mammalian species in their home ranges will vary according to the following relationships: DC = 15 W - 1.16 for carnivores and DH = 103 W - 0.93 for herbivores (grazers and browsers), where D is animal density expressed in individuals per square kilometer, and W is the adult body weight in kilograms. For a carnivorous mammal or herbivore the size of Homo sapiens (roughly 65 kg), these relationships predict 0.12 individual/km2, and 2.1 individuals/km2, respectively. The natural

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Page 305 availability of preagriculture human diets, however, fell between carnivorous and herbivorous diets. In fact, we are still largely grain-, fruit-, and tuber-eating with a predilection for meat. A liberal estimate of the average density that our species would likely have attained without agriculture is around 1 individual/km2—similar to the density at which hunter-gatherers and nomadic pastoralists lived until relatively recently. If preagriculture humans at that density were to exploit every square kilometer of Earth's habitable terrestrial surface, about 130 million square kilometers (Hannah and others 1994), the world would support roughly 130 million people. According to one estimate, world population surpassed that number during the early years of the Roman Empire (Biraben 1979 reprinted in Livi-Bacci 1992; Cohen 1995). The United States alone surpassed it just before World War II (US Bureau of the Census 1995). Demographics Then and Now We know with reasonable certainty that Homo sapiens has expanded in numbers from at most a few tens of millions in prehistory to nearly 6 billion at the close of the 20th century. Most of these billions arrived in the 20th century, as the march of technology (especially in sanitation, immunization, and agriculture) allowed, for the first time, the vast majority of babies born to survive to become parents themselves. Some of the most rapid population growth during the 19th century occurred in the United States, where annual increases, roughly 2.5–3%, were as high then as in sub-Saharan Africa today. The consistently high 19th-century growth rates are a major reason that the United States is today the third most populous country in the world. The result of the victory over infant and child death is evident in every region and major city. The planet sustains nearly half its humans in urban areas. Roughly three of every five people live in Asia. Each of the other major world regions is home to several hundred million people, but the populations of the continents are growing at markedly different paces: Europe, with about 730 million people, at a mere 0.2% per year (UN 1996a); North America (mostly the United States and Canada), with 300 million, at about 1.0% annually; Asia, with 3.5 billion, at about 1.5% per year; and the Latin American and Caribbean region, with about 485 million, at about 1.7% per year. Standing apart from the rest of the world demographically is Africa, with 708 million, where population growth has continued for decades at nearly 3% per year, falling slightly now to 2.7%. The average of all uneven rates of growth worldwide is equivalent to that of Asia, or about 1.5% per year. Despite the ever-larger population base, world population growth is gradually slowing. The annual rate peaked at 2.1% in the late 1960s and has drifted down since. When a growth rate decreases, however, growth itself continues until the rate reaches zero. And substantial growth continues decades after fertility descends to replacement levels (slightly more than two children per woman) or even dips below. That effect, known as population momentum, is due to the long lag time between birth and reproductive maturity that characterizes our species. The

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Page 306 lag allows past growth to continue to augment the absolute size of the reproductive segment of the population (women roughly 15–49 years old), thus supporting high numbers of births despite a decrease in fertility to replacement level. As world population increases, more modest rates of growth can add larger annual increments to the population base. That has occurred although the highest rates of global population growth, estimated to have occurred around 1970, saw only about 72 million people added to world population each year. Current lower rates of growth are adding more than 80 million people per year. The global annual growth increment itself has declined since 1988 and could continue to decline—although by how much and for how long is unknown. A previous temporary decline during the middle 1970s, reflecting devastating effects of famine and political upheaval on the age structure of China's huge population (NRC 1984), illustrates how uncertain demographic projections can be. During the 1970s and 1980s, human fertility in industrialized countries, which was already near replacement levels, declined once more. Nearly all the European countries fell below the roughly two-children-per-couple average that, in the absence of immigration, is necessary to replace each generation with the one that follows. The meaning of that trend for future population is potentially enormous. Throughout the developing world, couples desire smaller families and later childbirths and they increasingly have the means to achieve the family size they seek. Several good examples can be gleaned from East Asia and Southeast Asia. During the middle 1960s, South Korea, Taiwan, Singapore, Thailand, and the former Hong Kong Territory began effective programs to lower infant mortality, establish easy access to family-planning services (ADB 1997; Tsui 1996), and increase primary-school enrollments and educational attainment (ADB 1997; Birdsall and Sabot 1993; Birdsall and others 1996; UNDP 1996; World Bank 1993). Thirty years later, average fertility in each of these Asian states is below two children per woman (the US average). Other developing countries—including Mexico (3.1 children per woman), Brazil (2.4), Indonesia (2.9), Tunisia (3.3), and Sri Lanka (2.2)—are also experiencing downward trends in fertility (UN 1996b). A recent analysis of regional patterns of demographic change (Bongaarts and Watkins 1996) suggests that the first country in each developing region to begin its transition to lower fertility was endowed with relatively high indicators of social and economic progress, as measured by the UN's Human Development Index (UNDP 1996). In each case, however, fertility decline spread to nearby countries—probably via transfers of expertise, experience, and information at the government and local levels—despite the neighbors' lower scores for economic and social development. In most developed countries, where there is access to affordable, effective contraception and safe abortion, women are more likely to have the number of children they want than are women in developing countries. Where these circumstances prevail and where childbearing and rearing are expensive or constrain economic mobility, total fertility consistently remains below the replacement level of slightly more than two children per woman (Potts 1996). The other great trend shaping world population, aside from changes in fertility, is rapid mortality decline—or rapid increase in average life expectancy. Life

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Page 307 expectancy began its climb in middle-18th-century Europe (figure 1). By the late 20th century, people in all corners of the world had longer life expectancies. The dominant influences are at both ends of the age spectrum: smaller proportions of children are dying in the first few years of life, and larger proportions of adults are surviving to old age. Demographers assume that the mortality decline will continue, placing some further upward pressure on the pace of population growth. Falling mortality, however, could moderate worldwide as additional improvements in health care and nutrition become more difficult to achieve. In eastern Europe, mortality has actually risen in recent years; and in sub-Saharan Africa, the AIDS pandemic is reversing recent progress in infant mortality (US Bureau of the Census 1994). Both trends and the growing specter of emerging infectious diseases (Olshansky and others 1997) raise questions about the strength of the UN's assumption of continued mortality decline well into the 21st century. The Project of Projecting In projecting an image of the future, the challenge for demographers is to understand the complex and uneven trends in fertility, mortality, and migration and to consider to what extent they are likely to continue and—perhaps most critical—at what levels they might end. Given the hodgepodge of modern demographic trends, all that can be said with certainty about future trends and end points is that we cannot be certain. The UN Population Division, which produces the most widely cited tables of international population information, has addressed such uncertainty by computing every 2 years a three-piece set of population projections. The most recent series, published in 1996, projects populations for each of the UN's 185 member countries to 2050 (see UN 1996b). Figure 1 Life expectancy in three developed countries (1750–2000) and three developing countries (1950–2000). European life expectancies for years before 1950 from tables compiled by Livi-Bacci (1992), citing various authors who have analyzed historical records. Data from 1950 and beyond from current UN tables (UN 1996b).

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Page 308 But scientists and journalists should take note: the UN projections are not statistically predictive. They are not estimates calculated from models of underlying behavioral relationships, nor are they the extrapolated curves with which biologists are most familiar. For that reason, the projections tend to be poorly understood and commonly misused. The three pieces making up the UN's set of projections are its low, medium, and high variants generated for each country. Each variant differs from the other two in just a couple of key assumptions—its fertility end point and the path of fertility to that end point (see country examples in figure 2). When plugged into a model that generates births and eliminates the dead from each age group (and adds immigrants and subtracts emigrants where necessary), each variant traces a different population trajectory through the future. To generate the medium variant's fertility curve, UN demographers use assessments of each country's situation and progress to make an educated guess of when each country will achieve replacement-level fertility. In each case, for projection purposes, this date is assumed to fall before midcentury. A fertility trajectory is then created that allows national fertility to fall—or, where needed, to rise—smoothly to its replacement-level end point. Once fertility arrives at this point, it is assumed to stay there indefinitely. By completing this exercise for fertility of each country (using standard mortality assumptions) and migration, adding all national populations for each year computed, the UN arrives at a continuous medium variant trajectory for world population. The 1996 UN medium variant projects a global population of about 9.4 billion people around the middle of the 21st century, compared with the known 2.5 billion in 1950 and the 5.9 billion in 1998. If extended beyond 2050, as the UN does in its long-range projections (UN 1992; also see Haub and Yinger 1992; McNicoll 1992), population then grows fairly slowly, stabilizing at around 12 billion early in the 22nd century. The medium variant, however, is only one element of the projections. To generate the other elements, the low and high variants, the UN adheres to the same model used to generate the medium variant but adjusts the fertility end point and the path of fertility to that point. In the low variant—a lower bound for plausible scenarios—each country's fertility end point is reset to achieve 1.6 children per woman before 2050 and held constant thereafter. To fix an upper bound of plausibility, the high variant applies the same schedule to settle at 2.6 children per woman. Those are not error limits. Instead, the low and high variants are distinct, but extreme, scenarios of demographic change applied to every country. The low variant mimics the behavior of many European and several East Asian populations that over the last 2 decades have dipped below replacement fertility (1.2–1.9 children per woman). The high variant mimics a number of Central American and South American countries that have momentarily stabilized at levels somewhat higher than replacement (Haub and Yinger 1992). For example, total fertility of both Uruguay and Argentina has fluctuated erratically below 3.5 children per woman for at least 50 years without ever having reached replacement levels. In

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Page 309 Figure 2 Fertility curves for three countries (UN 1996b)—past data and projected high-, medium-, and low-variant scenarios and corresponding national population projections (UN 1996c).

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Page 310 Costa Rica and Chile, fertility declined rapidly during the 1970s but stalled at similar levels. By generating low and high variants, the UN projections present an envelope of plausibility, suggesting that a range of population futures is possible. Those two scenarios project a 2050 world population between 7.9 billion and 11.9 billion (figure 3). A Separate Demographic Reality The demographic experience of the world suggests that total fertility is dynamic and highly responsive to the circumstances of women and couples. The UN series of projections, however, must necessarily remain mechanical and thus reproducible every 2 years. Perhaps the most mechanical feature is the UN's assumption of a stable fertility end point for each variant. But even the paths drawn to those end points often appear inconsistent with past data. Figure 3 Past and projected world population from UN estimates and projections (1996c) and annual increment of world population growth (annual change in growth) derived from these data and projections. The trough in the world-population growth increment that began in the middle 1970s was caused by irregularities in China's growth increment. China's irregular growth was due to an age structure shaped by high mortality (NRC 1984) and low fertility (Coale and Li 1987) that occurred in the wake of famine and political upheaval during the Great Leap Forward from 1958 to 1960.

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Page 311 Three examples illustrate these points (see figure 2). In the case of Nigeria, where there is still little evidence of substantial demographic change, all three fertility variants seem highly speculative and contrived. For Japan's projected fertility, at least two of the variants seem difficult to reconcile with past trends. In the case of Colombia, however, high-, medium-, and low-variant fertility curves all seem similarly consistent with past data. Although there are good reasons to expect fertility decline to continue where families are typically large, there is no particular reason to assume that fertility rates will settle between 2.0 and 2.1 or at 2.6 or 1.6 children per woman. In fact, Sweden, Luxembourg, the United Kingdom, and France—each below replacement-level fertility today—have been there before (UN 1996b; Livi-Bacci 1992), bobbing back up above replacement-level during national baby booms and moving downward during political and economic turmoil. Recently, the UN low-variant population projection has been used by several analysts and journalists (Buchanan 1997; Eberstadt 1997; Wattenberg 1997) as evidence that UN demographers are predicting alarming declines in global population beginning as “soon” as 2040. That is either a gross misunderstanding or a misuse of the projections. The low variant does, in fact, trace a downward path after that date. But eventually it must, by its very nature. With each national population in the world fixed forever at 1.6 children per woman—about a half-child below the replacement level—there is ultimately nowhere for the calculated population to go but down. The high variant, just as artificially, forces the trajectory upward, and the medium variant ultimately forces stability. Clearly, it makes little sense to use one variant without reference to the others. There is no good reason to assume that the below-replacement-level fertility experienced in some industrialized countries today will be sustained long enough to lead to a substantial net population decline in the long run. Fertility rates might well rise again if the direct costs or opportunity costs of childrearing decline or if larger families regain social approval. Nor does it make sense to assume that below-replacement-level fertility returns to and stabilizes exactly at replacement-level fertility. Realistically speaking, we do not know. In practice, most journalists and analysts take the UN's “medium variant,” or middle trajectory, to be the most probable one, whether for national, regional, or global population figures. It is often expressed inaccurately as the “expected” population future. That hardly makes the medium projection the “most likely” scenario within the wide range of plausible paths described by the high and low variants. True, neither the high nor the low extreme could be properly considered as “likely”—they are extremes, after all—but neither is there any special center of gravity midway between them. In fact, the medium projection uses a reasonable, repeatable method that cuts a path through a future without surprises, one in which demographic change is gradual and limited. A relative absence of demographic surprise, however, has not always been the rule. Until the 1950s, demographers most often underestimated population growth. The largest cause of failure among early population projections was that their authors missed the fact that mortality was falling at an increasing rate in the developing world. The country-by-country triumphs of sanitation, clean water

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Page 324 diffusion of ideas and values is lagging. The sheer complexity of global society is complicating matters, for it takes much time for our social habits and customs to be established and even longer for international institutions to evolve. The time scales involved can be traced to the fact that it takes only 9 months to produce a human's “hardware” but at least 20 years to program a human's “software”. These are the fundamental biological and human constants that finally determine both our personal development and the fate of humankind. Ultimately, it is the interplay and balance of matter and mind that will resolve our predicament. References Atiyah M, Press F. 1993. Population growth, resource consumption, and a sustainable world. Statement of the Royal Society of London and US National Academy of Sciences. Washington DC: National Academy Press. Cohen J. 1995. How many people can the world support? New York: Norton. Holdren J. 1991. Population and the energy problem. Population and environment. J Interdisc Stud 12(3):231–55. Kapitza SP. 1995. Population dynamics and the future of the world. In: Towards a war-free world. Proceedings of the 44th Pugwash conference on science and world affairs. Singapore: World Scientific. Kapitza SP. 1996a. The phenomenological theory of world population growth. Physics—Uspekhi 39(1):57–72 Kapitza SP. 1994. The impact of the demographic transition. In: Schwab K (ed). Overcoming indifference: ten key challenges in today's world. New York NY: New York Univ Pr. Kapitza SP. 1996b. Population: past and future. A mathematical model of the world population system. Science Spectra 2(4). Kapitza SP. 1996c. Population dynamics and the West-East Development. Annals of the 7th Engelberg Forum. Kapitza SP. 1997 Population growth and sustainable development. The 47th Pugwash Conference on Science and World Affairs. Lillehammer, Norway: World Scientific. Lutz W (ed). 1994. The future population of the world: what can we assume today? London UK: IIASA and Earthscan Press. Lutz W, Sanderson W, Scherbov S. 1997. Doubling of world population unlikely. Nature (387):803–5. Meadows D and others. 1972. Limits to growth. New York NY: Universe Bk.

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Page 325 Nonindigenous Species—A Global Threat to Biodiversity and Stability Daniel Simberloff Department of Ecology and Evolutionary Biology, University of Tennessee, 569 Dabney Hall, Knoxville, TN 37996 The world's biota is being rapidly homogenized. This global change constitutes a major threat to biodiversity and to our ability to extract resources sustainably from many ecosystems. The threat was first recognized 50 years ago, but its extent is only now being realized as burgeoning tourism and unfettered international trade expand the opportunity for species to get from one region to another. In the past, a desired immigrant species or one furtively hitching a ride often had to survive a sea voyage of months. Now, over 280 million passengers use commercial airliners each year worldwide, as do millions of tons of cargo. The brown tree snake (Boiga irregularis) occasionally arrives in Honolulu in wheel wells and cargo bays of planes from Guam, where it has devastated forest birds after introduction from the Admiralty Islands (Rodda and others 1992). Similarly, mosquitoes arrive in Great Britain from Africa in airliner passenger cabins (Bright 1996), and the giant African snail (Achatina fulica), which has ravaged agriculture on many Pacific islands, was carried by a boy from Hawaii to Florida as a gift to his grandmother (Simberloff 1997a). Of course, on every continent, many of the most venerated plants and animals were introduced intentionally. In many parts of the world, the major crop plants are almost all introduced, as are livestock. For example, of nine crop plants in the United States classified as “major” (USDA 1997), one (corn) is native and five were introduced from the Old World, one from the Andes, and two from Central America. Pets and ornamental plants are also usually of exotic origin. So what is the threat, exactly?

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Page 326 Effects of Nonindigenous Species The biggest threat posed by introduced species is the disruption of ecosystems, often by invasive plant species that replace the native species. The Australian tree Melaleuca quinquenervia, until recently increasing its range in southern Florida by more than 20 ha/day, replaces cypress and other native plants. It now covers about 200,000 ha, provides poor habitat for many native animals, affects the fire regime, and causes water loss (Schmitz and others 1997). South American water hyacinth (Eichhornia crassipes) now blankets many near-shore areas of Africa's Lake Victoria, blocking light and killing plants at the bottom of the food chain. The death and decay of plants that make up the water hyacinth mat remove still more oxygen from the water, and the major fisheries are in drastic decline. In addition to the ecological damage, water hyacinths are an economic nightmare, fouling engines and propellers of cargo ships and ferries, preventing docking, and clogging power-plant pipes and so causing numerous blackouts (McKinley 1996). Introduced plants can also change an ecosystem without smothering the native plants. For example, on the island of Hawaii, the eastern Atlantic island shrub Myrica faya has invaded nitrogen-poor lava flows and ash deposits. A nitrogenfixer, it favors other introduced species over the native plants adapted to low nitrogen (Vitousek 1986). In much of the American West and in Hawaii, Old World grasses, such as cheatgrass (Bromus tectorum), increase the frequency and intensity of fires to the great detriment of native plants and the animals that use them (D'Antonio and Vitousek 1992; Macdonald and others 1989). Entire marine ecosystems can be radically changed by the invasion of a single plant species. The Pacific seaweed Caulerpa taxifolia, released from the Oceanographic Museum of Monaco into the Mediterranean about 15 years ago, now covers over 4,000 ha and has locally smothered native seagrass beds that harbor many native animals (Boudouresque and others 1994; Simons 1997). Introduced red mangrove (Rhizophora mangle) trees from Florida on the coasts of the Hawaiian islands and Australian “pine” trees (Casuarina spp.) on the Florida coast have come to dominate their new homes, displacing native plants and animals (Schmitz and others 1997; Walsh 1967). Just as an introduced plant can modify an ecosystem, a species that eliminates a plant can have a drastic effect. The Asian chestnut blight fungus (Cryphonectria parasitica), which arrived in New York City on nursery stock in the late 19th century, spread over about 100 million ha of the eastern United States in less than 50 years, destroying almost all chestnut trees (von Broembsen 1989). Chestnut had been the most common tree in many forests, making up one-fourth or more of the canopy trees, so the cascading ecosystem effects of this invasion were substantial. For example, several insect species that were host-specific to chestnuts were extinguished (Opler 1979); that chestnut leaves decompose faster than leaves of the oaks that largely replaced them suggests that the invasion greatly affected nutrient cycling (K. Cromack, Oregon State University, pers. comm.), although systematic data were not gathered. The North American pine wood nematode (Bursaphelenchus xylophilus) reached Japan in timber and spread

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Page 327 among the islands, killing more than 10 million pine trees and affecting 25% of Japan's pine forests (von Broembsen 1989). The effects on other forest species must have been dramatic. In addition to ecosystem effects, nonindigenous species have myriad effects on particular native species or groups of them. They can eat them, for example. The Nile perch (Lates niloticus), after introduction into Lake Victoria, eliminated many species of endemic cichlid fishes, which had undergone perhaps the greatest evolutionary radiation that scientists have studied (Goldschmidt 1996). Introduced rats (Rattus spp.) on many islands have destroyed at least 37 species and subspecies of island birds (Atkinson 1985; King 1985). The impact of the brown tree snake on the Guam avifauna is noted above. Introduced herbivores can similarly drive species to extinction, especially on islands where plants are less likely to have a refuge, an area that herbivores cannot reach. For example, goats introduced to St. Helena in 1513 almost certainly eliminated over 50 endemic plant species, although only seven were scientifically described before they disappeared (Groombridge 1992). Introduced pathogens, often carried by introduced plants and animals, can also devastate native species. The chestnut blight was noted above. As another example, in the Hawaiian islands, the extensive introduction of Asian songbirds has brought avian pox and avian malaria, which have contributed to the decline and extinction of numerous native forest-bird species (van Riper and others 1986). The introduction into Africa of the virus rinderpest, native to India, in cattle in the 1890s led to the infection of many native ungulate species; mortality in some species reached 90%, and the distribution of some species is still affected by the virus (Dobson 1995). Nonindigenous species can compete with native ones, although competition for resources is often difficult to demonstrate. Some well-studied examples provide good evidence. The house gecko (Hemidactylus frenatus) has invaded many Pacific islands; this has led to drastic declines in the population of some native gecko species. Experiments suggest that at least one of the natives, Lepidodactylus lugubris, avoids the larger house gecko, thereby suffering food shortage (Petren and others 1993), and that the invader depletes the insect food base sufficiently to reduce the food available for the native (Petren and Case 1996). The continuing replacement in the United Kingdom of the native red squirrel (Sciurus vulgaris) with the introduced American gray squirrel (S. carolinensis) is now attributed largely to the greater foraging efficiency of the invader and concomitant lowering of food available to the native (Williamson 1996). Many instances are known in which introduced species affect native ones by interfering with them directly rather than indirectly through resource depletion. The South American fire ant (Solenopsis invicta), which has spread throughout the southeastern United States, attacks individuals of native ant species and is replacing the latter in many habitats (Tschinkel 1993). In a plant analogue of aggression, the African crystalline ice plant (Mesembryanthemum crystallinum) accumulates salt, which remains in the soil when the plant decomposes. In California, this plant thus excludes native plants that are intolerant of such salty soil (Vivrette and Muller 1977).

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Page 328 Nonindigenous species also eliminate native species by mating with them; this threat is especially strong if the native species is much less numerous than the introduced one. For example, the New Zealand gray duck (Anas superciliosa superciliosa) and the Hawaiian duck (A. wyvilliana) are threatened with a sort of genetic extinction because of rampant hybridization and introgression with the introduced North American mallard (A. Platyrhynchos) (Rhymer and Simberloff 1996). Likewise, Europe's rarest duck, the white-headed duck (Oxyura leucocephala), is threatened in its last redoubt in Spain by hybridization and introgression with North American ruddy ducks (O. jamaicensis), which were introduced into England as an amenity, escaped, and made their way to Spain (Rhymer and Simberloff 1996). This sort of threat is far more common in regions that exchange closely related species (such as Europe and North America) than in those whose species are so distantly related that they are unlikely to be able to mate and exchange genes (such as Australia and either Europe or North America). A native species can be threatened by hybridization with an introduced one even if no genes are exchanged, simply by the reproductive reduction effected by fruitless matings. Females of the endangered European mink (Mustela lutreola) mate with male introduced American mink (M. vision); although the embryos are aborted, the loss of reproduction by the European mink exacerbates their population decline (Rozhnov 1993). Slowing the Flow The first line of defense against nonindigenous species is to keep them from being introduced. There are both practical and legal impediments to doing so. The sheer volume of tourism and trade dictates that inspection is destined to miss many inadvertent immigrants. Agricultural pests insinuate themselves into foodstuffs, woodboring beetles into timber, rodents into cargo containers—virtually any product shipped in bulk can carry many hitchhikers. Routine purging of ship's ballast water has released hundreds of nonindigenous species in waters throughout the world (Carlton and Geller 1993). Tourists can easily import species inadvertently in baggage, even if they heed warnings about which items are the most likely carriers of immigrants. In 1990, about 333 million nonindigenous plants were imported into the United States through Miami International Airport alone (OTA 1993). Economic resources are insufficient to examine everything that crosses a nation's borders. Furthermore, liberalization of trade through such treaties as the General Agreement on Tariffs and Trade (GATT) and the North American Free Trade Agreement (NAFTA) is bound to increase the flow of nonindigenous species, and not only as a result of the increased volume. Under GATT and NAFTA, restrictions claimed as environmental measures can be challenged on the grounds that they are protectionist. The relevant regulatory authority must then adjudicate the dispute. Aside from the overwhelming appeal of free trade, both GATT and NAFTA require that species exclusions be based on risk assessments. However, risk-assessment procedures for introduced species are in their infancy and

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Page 329 do not appear to be scientific, often resting on undefended judgments by experts and on arbitrary algorithms for combining risks (Simberloff and Alexander 1998). Furthermore, these risk assessments are expensive; one conducted by the US Department of Agriculture (USDA) on risks associated with importing larch from Siberia into the United States (USDA 1991) cost $500,000 (Jenkins 1996). It is difficult to imagine finding funding sources sufficient to mount risk assessments for all the challenges that might appear even to an educated layperson to be justified on prima facie grounds. Virtually every specialist in invasion biology who has examined the matter concludes that aspects of the ecological impact of a nonindigenous species are inherently unpredictable (for example, Hobbs and Humphries 1995), and many scientists argue that every species should be considered a potential threat to biodiversity and sustainability if it were to be introduced (for example, Ruesink and others 1995). That implies that every species proposed for deliberate introduction, whether or not it appears superficially to be innocuous, necessitates some formal risk assessment. The cost would be staggering if the USDA process (USDA 1991) were the model. In addition, many parties introduce species not inadvertently, but deliberately. These range from the boy smuggling giant African snails to his grandmother, who released them in her yard in Miami (Simberloff 1997a), to such large industries as the pet and ornamental-pet trades, which lobby vigorously against many restrictions. In the United States, recommendations that all species proposed for introduction must be on “white lists”—lists of species whose invasive potential has been assessed and has been approved for introduction—have been systematically attacked by those interest groups. Rather, the major laws that restrict entry of species use “black lists”lists of species that have already been shown to be damaging or are strongly suspected of being dangerous; a species is prohibited only if it is on such a list (Schmitz and Simberloff 1997). Rarely is blacklisting forward-looking. Thus, there will always be a flow of nonindigenous species. However, the flow can be lessened. Undoubtedly, increased public education as to the risks would lead to fewer deliberate and inadvertent introductions as people strive to be good environmental citizens. The Convention on Biological Diversity mandates that its signatories “as far as possible and as appropriate . . .prevent the introduction of . . .those alien species which threaten ecosystems, habitats, or species.” Bean (1996) suggests that this statement reflects widespread recognition that nations are obliged to attempt to prevent introductions, and he cites as an example New Zealand's 1993 Biosecurity Act, which subjects all incoming persons and goods to rigorous inspection and prevents the importation of any species not already cleared by government authorities for inclusion on a white list. He also notes the increasing international and national regulation of purging of ballast water and points out that the considerable legal framework and effort that many nations use to attempt to prevent agriculturally harmful introductions could be adapted and expanded to prevent ecologically harmful ones. The problem is educating the public sufficiently that they demand regulation of nonindigenous species.

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Page 330 Managing Nonindigenous Species Once a species enters a new region, there are several options for managing it. The most obvious one is to attempt to eradicate it. This approach is often feasible if the invasion is recognized and targeted early enough (Simberloff 1997a), but several factors militate against its success. Perhaps foremost, almost no countries have an early-warning system in place that is charged with determining when an invasion has occurred, much less a procedure to generate a rapid, coordinated response while the invasion is still restricted geographically. The reaction is usually only after an invasion has existed for so long that it has become noticeable, and by then eradication is often impossible (Schmitz and Simberloff 1997). Second, for species deliberately introduced, the same forces that conspired to allow introduction in the first place act to prevent eradication. In addition, many invasions appear innocuous for long periods (Crooks and Soulé 1996; Williamson 1996); by the time they are recognized as ecologically or economically damaging, they are so widespread that they cannot be eradicated. Minimizing ecological and economic damage if eradication proves impossible is usually attempted by one or more of three routes (Simberloff 1996): chemical, mechanical, and biological control. The environmental and human health effects of broad-spectrum pesticides are legendary. Although some newer chemicals have far fewer side effects, their high cost and the necessity of repeated application and the frequent evolution of resistance by the target pest have led to great interest in alternative methods. Also, if pesticides were used to prevent damage by introduced species both to vast areas of natural habitats and to agriculture, all the above problems would be exacerbated. Mechanical methods, either alone or in concert with pesticides, are sometimes feasible. For example, water hyacinth has been successfully controlled in Florida for over 20 years by a combination of mechanical harvesting and treatment with the herbicide 2,4-D (Schardt 1997). However, mechanical devices are often expensive and would be less likely to work on widespread invasions. Biological control—the introduction of a natural enemy of the pest—has seemed an extremely attractive alternative to chemical and mechanical control on both ecological and economic grounds. Many biological-control projects have provided continuing suppression of a pest to acceptably low levels with the sole costs being those of the initial exploration to find natural enemies and the testing for efficacy and safety. Odour (1996) cites the control of water hyacinth in Sudan by three South American insects, of prickly pear cactus (Opuntia inermis and O. stricta) in Australia by the moth Cactoblastis cactorum from Argentina, and of the South American cassava mealybug (Phenacoccus manihoti) in Africa by a South American encyrtid wasp. In each instance, the natural enemies maintain populations in perpetuity without further human intercession. More recently, biological control has been subjected to critical scrutiny on the grounds that nontarget species, some of conservation concern, have been attacked and even driven to extinction (Howarth 1991; Simberloff 1992). Early biological control projects using vertebrates, such as the small Indian mongoose or the cane toad, and the widespread dissemination of the New World predatory snail

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Page 331 Euglandina rosea to control the giant African snail were disastrous, and biological control professionals now eschew the use of vertebrates, except for fishes. However, insects tested for host specificity have also attacked nontarget species. For example, the Eurasian weevil Rhinocyllus conicus, introduced into North America to control musk thistle (Carduus nutans), is now attacking native nonpest thistles, including narrowly restricted endemic species in nature reserves (Louda and others 1997). Although the extent of such problems is controversial, the fact that biological control agents can both disperse and evolve, just as any other introduced species can, suggests great caution in their use and extensive preliminary testing before their release. Action Needed Now Burgeoning international interest in invasive nonindigenous species has led to several international meetings (for example, Sandlund and others 1996), new monographs (for example, Williamson 1996; Simberloff and others 1997), increased news coverage (for example, McKinley 1996; Simons 1997), and widespread appeals for action (for example, Glowka and de Klemm 1996). Nevertheless, there is no evidence that the flow of exotics is decelerating under the pressures of increased trade and tourism described above. What else must be done? Glowka and de Klemm (1996) feel that inclusion of nonindigenous species as a priority item for the Conference of Parties to the Convention on Biological Diversity, which has been ratified by 172 nations, is necessary to prevent a fragmented approach to the problem. Schmitz and Simberloff (1997) see the effort in the United States as also bedeviled by fragmentation. In short, as long as one program deals with aquatic plants, another aquatic animals, another agricultural weeds, and yet another bird introductions, the effort is bound to be frustrated if only because species often interact synergistically to generate an environmental or economic problem (Simberloff 1997b). Furthermore, because nonindigenous species do not recognize political boundaries, both regulatory and management responsibility must also cross for them to be effective. Thus, the Convention on Biological Diversity, an international instrument, is highly appropriate as one locus of action. It is important to observe, however, that, even if no species were henceforth able to cross a national border, introduced species would still be a major problem. In the United States, for example, interstate movement of introduced species has the same effect as importing such species from other countries: ecosystems are subjected to invasion and disruption by species that have evolved elsewhere. And, within-country transport can threaten invasion of neighboring countries. A major current lacuna is a comprehensive database on introduced species that is associated with an early-warning system and a rapid-response team. For most taxa in most countries, someone who finds a species suspected to be nonindigenous and potentially invasive has nowhere to turn to examine this possibility. There is no emergency telephone number to use to determine whether it is a newly recorded species or a species that is spreading after introduction. Even if

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Page 332 there were an organization charged with receiving such queries, there is no list of species to which it could turn to give an answer. For most species, there is no systematic effort to record where they have been introduced or their suspected effects. And there is rarely a procedure in place to respond rapidly to a newly recorded invasion, partly because of the fragmentation of authority described above. The white-list approach advocated by Ruesink and others (1995) and Wade (1995) and discussed above needs to be adopted in some form both nationally and internationally. Black lists have never worked well, and the inherent unpredictability and idiosyncrasy of introductions dictate that all potential introductions be subjected to scrutiny—with no blanket exceptions. That requirement, of course, would mean that funding would be needed to process applications and to give them the necessary attention. Whether the costs of white listing are borne by the party wishing to import a species or by society as a whole will have to be addressed. For that matter, so will the costs of an unforeseen disaster if a white-listed species turned out not to be innocuous. Should an applicant be required to post a bond? Should an applicant be able to be indemnified by purchasing disaster insurance? Should society as a whole bear the cost? These matters have barely been broached. How a species proposed for introduction should be assessed is yet another crucial issue that has been at best cursorily considered. As noted above, standard risk-assessment procedures for chemical and physical stressors do not appear to work well for biological introductions, for which the probabilities of such events as evolution and long-distance dispersal are so difficult to evaluate as to be mere guesses (Simberloff and Alexander 1998). The concatenation of guesses and arbitrary assignment of risk categories that pervades the current USDA risk-assessment procedure (see, for example, USDA 1991) hardly seems scientific, but no general alternative has been widely considered (O'Brien 1994). Having agreed that risk assessment will be the appropriate procedure to adjudicate disputes, we must determine how to do risk assessments en masse for nonindigenous species. References Atkinson IAE. 1985. The spread of commensal species of Rattus to oceanic islands and their effects on island avifaunas. In: Moors PJ (ed). Conservation of island birds. Cambridge UK: International Council for Bird Preservation. p 35–81. Bean MJ. 1996. Legal authorities for controlling alien species: a survey of tools and their effectiveness. In: Sandlund OT, Schei PJ, Viken A (eds). Proceedings of the Norway/UN conference on alien species. Trondheim Norway: Dir for Nature Management and Norwegian Inst for Nature Research. p 204–10. Boudouresque CF, Meinesz A, Gravez V (eds). 1994. First international workshop on Caulerpa taxifolia. Marseille France: GIS Posidonie. Bright C. 1996. Understanding the threat of bioinvasions. In: Worldwatch Institute, State of the World 1996. New York NY: WW Norton. p 95–113. Carlton JT, Geller J. 1993. Ecological roulette: the global transport and invasion of nonindigenous marine organisms. Science 261:78–82. Crooks J, Soulé ME. 1996. Lag times in population explosions of invasive species: causes and implications. In: Sandlund OT, Schei PJ, Viken A (eds). Proceedings of the Norway/UN Conference on

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