Invasive Alien Species: The Nature of the Problem

Harold A. Mooney

The increasing human population is altering the natural resources on which our societies depend to an ever-greater extent. Many of these changes are purposeful and to the benefit of society. Others, although purposeful, have inadvertent negative impacts on the goods and services that natural resources deliver to society. In order to manage these resources in a sustainable manner we must understand the interactions and trade-offs between resource alteration and the natural, generally renewable processes on which we depend. This book addresses one particular driver of resource alteration: alien species invasions. In aggregate, these invasions are global in extent and are having consequences that are generally unappreciated but quite threatening to many human activities.

The vast numbers of species that populate the earth provide innumerable goods and services that society values. Equally important for society are the services that natural systems provide free of charge (Daily et al. 1997). On the other hand, invasive alien species can represent "ecosystem bads and disservices" (as characterized by Madhav Gadgil, 2000: 16) to systems on which society depends. In this introduction I concentrate not only on how invasive aliens alter ecosystem properties but also more directly on their effects on goods and services valued by society. This information provides a backdrop to the chapters that follow, which focus on what to do about this pervasive problem.

For comprehensive overviews of the problem there are a number of recent summaries (Vitousek et al. 1997; Lonsdale 1999; Parker et al. 1999; Williamson 1999; Mack et al. 2000; D'Antonio et al., 2004), edited volumes (Sandlund, Schei, and Viken 1999; Mooney and Hobbs 2000), and popular books (Bright 1998; Devine 1998).

What Do We Know in General?

The reviews just listed give us some general conclusions about the status and impacts of alien species that can be summarized as follows:

• There has been a massive global mixing of biota.

• This mixing has been both purposeful and accidental.

• There has been both biotic enrichment and impoverishment in any given area (species view).

• A small fraction of alien species have become invasive.

• Invasive alien species come from all taxonomic groups.

We know with less precision the kinds of habitats in which invasive alien species are most successful, the traits of successful invaders, and the mechanisms of habitat degradation caused by invaders. We do know that invasive alien species have altered evolutionary trajectories, can disrupt community and ecosystem processes, are causing large economic losses, and threaten human health and welfare.

Character of the New Biotic World

It is easy to demonstrate that the nature of the biological world is very different from what it was before the age of exploration. The natural ecosystems that evolved in isolation on the various continents and large islands, constrained by biogeographic barriers such as oceans, have become functionally connected through the capacity of humans to transport biological material long distances in a short amount of time. The consequences of this biotic exchange are staggering when you tally up what the biotic world looks like now in comparison with the recent past. In Hawaii, a prime example of the onslaught of alien species, there are 3,500 more species of flowering plants and insects than there were before the age of exploration. Of the flowering plants, there are more alien species than endemics (Eldredge and Miller 1997). In California, more than 1,000 established alien plant species have been added to the approximately 6,300 natives (contrast this to the 64 plant taxa that are threatened or extinct) (Hobbs and Mooney 1998).

Looking across the world, Hawaii is at the extremes of biotic introductions, as are many other islands, and California probably is somewhere in the middle. However, a survey of the number of alien plants in various parts of the world shows that established alien species are everywhere. For plants alone, the following numbers of established alien species have been noted in the large continental areas of the Russian Arctic, 104; Europe, 721; tropical Africa, 536; southern Africa, 824; Canada, 940; continental United States, 2,100; Chile, 678; and Australia, 1,952. For islands, New Zealand has 1,623, the British Isles 945, and the Canary Islands 680. These numbers indicate the extent of the changes in biotic systems that have occurred. Similar numbers, at least proportionately to natural abundance, can be seen for other taxonomic groups (Vitousek et al. 1997).

How Fast Has All of This Happened?

The exchange rate of biological material across biogeographic barriers that have separated continents for millions of years has been extremely low until very recently. Similarly, climate has been fairly constant in recently millennia. However, both climate change, as driven by the changing composition of the atmosphere, and the large-scale intercontinental movement of biological material have greatly accelerated in recent times. To get a sense of the comparative rates of change in atmospheric composition over the past 200 years and in biotic composition caused by biotic introductions, one can examine the detailed records of the changing CO2 concentration of the atmosphere. In 1800 it was 280 ppm, and in 1990 it had increased to 354 ppm, an increase of 26 percent (Boden et al. 1994). In contrast, to use one well-documented case, the numbers of established alien arthropods in the United States grew from 50 in 1800 to 2,000 in 1990 (Sailer 1983; U.S. Congress 1993: 1263), a forty-fold increase! This is not to say that the potential global environmental consequences of these changes are equivalent, but it does indicate the extent of biotic interchange and the large change in the biotic composition of the earth.

There are indications that the rate of exchange for certain groups of organisms is accelerating. Cohen and Carlton (1998) have shown this for organisms introduced into the San Francisco Bay and Nico and Fuller (1999) for fishes in the United States.

Success of Invasive Alien Species

Only a small fraction of the alien biotic material that lands in new territory actually becomes established, and even a smaller fraction becomes a serious problem (Williamson 1996). However, given the great numbers of alien species imports, the actual numbers of species that become established and do harm can be large. For example, of the 1,500 species of foreign insects that had become part of the insect fauna of the United States 20 years ago, 235 (16 percent) had become pests (Pimentel 1993).

Of course, native species also can harm the biotic systems on which we depend. In an analysis of the numbers of pest species, Pimentel (1993) shows that 73 percent of the 80 major crop weeds of the United States came from other regions, whereas of the 110 pasture weeds 41 percent were from out of the country, and of 70 major forest pests only 23 percent were invaders.

Complex Species Interactions Are Modified by Invasive Alien Species

It has been postulated that one reason for the great success of invasive species is the fact that they escape their natural predators when entering a new biogeographic region. This undoubtedly is the case in many instances, but experimental evidence is not well developed. Some have even postulated that escape from predators allows organisms to devote more of their resources to competitive capacity, making them even more successful (Blossey and Notzold 1995).

These relationships indicate that it is not only the nature of the habitat at the time of invasion but also the relationships that develop subsequently that influence the ultimate success of an invader. It has been proposed that with time an invader will come to a new equilibrium with its environment, and populations will stabilize. In some cases these relationships develop quickly, and others develop over long periods of time. An excellent example of the initial lack of predators on invaders is Eucalyptus spp. (native to Australia) in California. Eucalyptus species were first introduced into California in 1850. Plantings were so extensive that one could drive for miles and miles and never lose sight of an individual of this genus. Although trees of this genus have had a large impact on their new environment (Robles and Chapin 1995), they actually have not spread much from where they were originally planted. One never saw damage to leaves of these trees by herbivores because evidently none of the local fauna could overcome the abundant natural defense compounds that Eucalyptus trees produce, whereas in their native habitat herbivory is extensive.

In 1984, more than 130 years after the introduction of Eucalyptus to California, the first herbivore was noted on these trees (a long-horned borer from Australia). Since then on average about one new herbivore has become established per year (all from Australia), all inadvertent introductions. After stem borers came leaf herbivores and then sap suckers; a whole complex of herbivores has become established. However, the food web is still simple: the plant host, the Eucalyptus, and a series of herbivores. The complexity of the web is being increased by the purposeful introduction of parasites of these herbivores to protect these trees (Paine et al. 2000), which are of value for some purposes. These parasites are host specific and therefore are also from Australia originally.

This example shows that introducing a new organism into an environment often is just the first step in a complex series of interactions that happen through time, adding to the complexity of predicting consequences of invasions.

Good News about Alien Species

There is a lot of good news about alien species. They serve as the foundation for our food production systems. Only about 20 plant species are major contributors to world food supply, and these are often grown far from their places of origin. They have been purposefully transported and molded through selection, and now through engineering, to fit the local conditions in the most productive manner. Furthermore, alien species grace our gardens and parks. They provide shelter from sun and wind and stabilize our soils.

What Is the Problem: Accidental or Intended Introductions?

Many species that are now invasive to a given region were deliberately introduced. For example, of the woody plants that have been become naturalized in North America, 85 percent were introduced for horticultural purposes (Reichard and Hamilton 1997). Lonsdale (1994) found that of 463 pasture species purposefully introduced into Australia between 1947 and 1985, only 5 percent turned out to be useful in pasture improvement, whereas 13 percent subsequently became weedy.

Purposeful introductions have done much economic damage. The golden apple snail, introduced into Asia from Latin America as a potential source of protein, has escaped and is infesting rice fields. In the Philippines alone, during its initial escape in the 1980s it caused hundreds of millions of dollars of economic damage (Naylor 1996).

Thus, the case can be made that both purposeful and accidental introductions can be equally damaging through time, so developing strategies to deal with the issue is difficult.

How Invasive Alien Species Disrupt Our Lives

Article 8h of the Convention on Biological Diversity addresses only the alien species that do harm. Specifically, it calls for action to "prevent the introduction of, control or eradicate those alien species which threaten ecosystems, habitats or species." What this implies is that for consideration a species must be new to the region (alien) and must threaten the native biota in all of its dimensions. This is generally interpreted as causing ecological harm. This definition is somewhat at odds with a strictly ecological definition of an invasive that relates only to the rate of spread. Furthermore, the negative impact criterion can be ambiguous; Daehler (2000) notes that "whether ... impacts are great or small, harmful or beneficial, depends on ... personal perspective." (See the lively discussion of the definition issue in Daehler 2000, Davis and Thompson 2000, and Richardson et al. 2000.) Similarly, the definition of pest refers to a destructive or troublesome organism, without reference to origin.

There are examples of ambiguity within a particular society on whether a given alien species with invasive characteristics is doing harm. However, in most cases this is not an issue. An invasive alien species that is extending its range in a new region and is having a large negative impact on the native biota or local economies generally is easily identified and targeted. In the following examples I demonstrate the many ways in which invasive alien species can threaten the goods and services provided by natural systems on which society depends. The following list and the brief examples given illustrate only the extent of the impacts of invasive alien species on systems human societies care about. These examples are intended to show the vast array of human endeavors that are interrupted by the impact of invasive alien species. This list includes species that are

• Fire stimulators and cycle disrupters

• Water depleters

• Animal disease promoters

• Crop decimators

• Forest destroyers

• Fishery disrupters

• Impeders of navigation

• Cloggers of water works

• Destroyers of homes and gardens

• Grazing land destroyers

• Species eliminators

• Noise polluters

• Modifiers of evolution

Fire Stimulators and Cycle Disrupters

Invasive species can have a large effect on the fire regime of an area and thereby completely change the character and dynamics of ecosystems. D'Antonio and Vitousek (1992) describe a pattern that is rather general in many places in the world where woody vegetation is destroyed by land clearing and subsequently invaded by alien grasses. These grasses in turn have a short return time for fires, inhibiting woody vegetation recovery and resulting in a permanent conversion to grasslands. Similarly, alien invasions into native shrub vegetation can change the fire regime to the detriment of the shrubs, resulting in a type conversion, as happened in the Great Basin of the United States with the invasion of cheatgrass (Bromus tectorum) (Billings 1990).

Water Depleters

Invasive alien species can significantly alter the water balance of a habitat if they attain greater rooting depths than the native species or if they attain greater biomass. Because water is a limiting resource in many parts of the world, invasives that alter habitat water use are of great concern. In the southwestern United States, more than one-half million hectares of riparian areas, in 25 states, has been invaded by tamarisk (Tamarix) species. Zavaleta (2000) recently calculated that these tamarisk species are using excess water with a value of approximately $200 million per year. Similarly, in South Africa invasive alien species are taking over the watersheds in the western Cape Region. They are increasing biomass, resulting in a large loss of water. It is calculated that if they are not removed in time they will result in average losses of 30 percent of the water supply of Cape Town (van Wilgen, Cowling, and Burgers 1996).

Animal Disease Promoters

Some of the most dramatic impacts of invasive alien species have involved disease organisms transmitted by resistant populations to those that have no immunity to the disease. The impact of the so-called Columbian Encounter was devastating. In Mexico, the introduction of human diseases such as smallpox, measles, and typhus from Europe reduced the population from 20 million people to approximately 3 million between 1518 and 1568 and to about 1.6 million in the next 50 years (Dobson and Carper 1996). Although modern medicine has reduced the impact of such diseases, there is still need for concern because of the emerging immunity to antibiotics, the large numbers of people with compromised immune systems, and of course the many more opportunities for rapid transport of disease organisms around the world (Garnett and Holmes 1996). For example, recently it has been shown that cholera bacteria (Vibrio cholera) are being transported in ship ballast water around the world (Ruiz et al. 2000).

Invasive diseases also directly affect nonhuman animals, causing large-scale impacts. The introduction of rinderpest into Africa at the end of the nineteenth century devastated not only cattle but also native ungulates. Control of this disease by vaccination of cattle also resulted in a dramatic recovery of native ungulate species populations (McCallum and Dobson 1995). However, in the early days of the outbreak nearly one-quarter of the cattle-dependent Masai pastoralists starved to death (McMichael and Bouma 2000). The introduction of avian pox and malaria into Hawaii from Asia has contributed to the demise of lowland native bird species (Simberloff 1996).

The enormous economic and social costs of the transport of animal disease organisms to vulnerable new localities has been amply demonstrated in both inadvertent cases, such as the recent European mad cow disease outbreak, and the purposeful release of anthrax in the United States.