2. Which species invade which habitats and why?
3. Spread of alien invasive species
4. Impacts of alien invasive species
5. Management of alien invasive species
Biological invasions have been a feature of global ecology since the origin of life: plants and animals invaded the land from the sea, and chance dispersal events have occasionally allowed species to invade new continents, islands, or bodies of water. The current wave of biological invasions is qualitatively different from these prehistoric invasions because it is mediated by human activities. It is also quantitatively different because the frequency of invasions is orders of magnitude higher than background levels.
alien invasive species. An alien species that becomes established in an ecosystem and threatens native biological diversity or has other negative ecological and economic impacts.
alien (equivalently: nonnative, nonindigenous, foreign, exotic) species. A species, subspecies, or lower taxon occurring outside its natural range (past or present) and dispersal potential (i.e., outside the range it occupies naturally or could occupy without direct or indirect introduction or care by humans); includes any part, gamete, or propagule of such species that might survive and subsequently reproduce.
ecosystem services. The conditions and processes through which ecosystems, and the species that make them up, sustain and fulfill human life.
introduction. The movement, by human agency, of a species, subspecies, or lower taxon (including any part, gamete, or propagule that might survive and subsequently reproduce) outside its natural range (past or present). This movement can be either within a country or between countries.
Before mass migrations of humans across the globe, natural dispersal of plants and animals was restricted by geographic barriers such as oceans, mountain ranges, and deserts. These barriers to migration have been lowered by human activity. The current wave of biological invasions began at the end of the Quaternary glacial period as humans began to disperse across the globe. The process began in earnest with the age of exploration in the fifteenth century and subsequent European colonization of the New World. Biological invasions accelerated rapidly in the twentieth century with the advent of international shipping and aviation, the construction of highways, and the destruction of large swathes of natural habitat. Today, virtually every location on the planet, from mountain peaks to remote oceanic islands, has recently been invaded by species that originated elsewhere. Invasive species occur in all taxonomic groups, from mammals to fungi to viruses.
Charles Darwin, on his Beagle voyage, was perhaps the first scientist to observe and note the process of biological invasion. Many of these observations led to insights that were incorporated into The Origin of Species. Charles Elton’s seminal book, The Ecology of Invasions by Animals and Plants, was published in 1958 and is considered the classic text of invasion biology. The field of invasion biology burgeoned in the latter decades of the twentieth century and is now the subject of numerous books and several specialized journals.
In this review, I first examine which species invade which habitats and address how and why these invasions occur. I next investigate models of how invasive species spread and then discuss the ecological and economic impacts of invasive alien species across the globe. Finally, I discuss management and policy options for preventing unwanted species introductions and for mitigating invasions when they do occur.
Perhaps the most infamous examples of biological invasions have resulted from deliberate introductions. In the western United States, saltcedars (Tamarix spp.), which choke out native vegetation, elevate soil salinity, and reduce river flow, were originally introduced as garden ornamentals. In eastern North America, the gypsy moth (Lymantria dispar), which causes massive defoliation of trees during periodic outbreaks, was deliberately introduced to investigate its potential for silk production in the nineteenth century. In Australia, cane toads (Bufo marinus) were originally imported to control pests of sugar cane in the 1930s but rapidly spread across the continent, poisoning pets and native wildlife that attempted to eat the toads and consuming smaller native species.
Accidental introductions are also the source of many biological invasions. Examples are zebra mussels (Dreissena polymorpha), which were introduced to the North American Great Lakes via ballast water in the late 1980s, and black rats (Rattus rattus), which have invaded numerous oceanic islands as ship stowaways. Historically, most plant and vertebrate animal invasions have resulted from deliberate introductions, whereas invertebrate animal and microbe invasions have resulted from accidental introductions. Exceptions include bumblebees (Bombus spp.) in New Zealand, which were deliberately introduced for crop pollination, and the sea lamprey (Petromyzon marinus), which was accidentally introduced into the North American Great Lakes where it parasitizes native fish species.
Although thousands of species have successfully invaded different habitats across the world, this represents only a small fraction of the species that are introduced or have the opportunity to invade. According to the “tens rule” of invasion biology, approximately 1 in 10 species that are imported will appear in the wild (become introduced), 1 in 10 of these introduced species will become established, and only 1 in 10 of these established species will actually become invasive. The tens rule encapsulates crudely what is observed in many statistical patterns of species invasions. A deeper treatment of the problem of invasions considers the factors that make particular alien species more successful invaders and particular habitats more invasible.
An overwhelming factor in the success or failure of biological invasions is propagule pressure. This conforms to intuition: species that are introduced in larger numbers are more likely to become successful invaders; and habitats that are subjected to a greater seed rain or immigration rain from potential invaders are more likely to become invaded. Studies of species invasions ought always to be set in this context because of the potential for propagule pressure to confound other factors. For example, the contrast between the high prevalence of invasive species near roads, seaports, and airports and the low prevalence of invasive species in nature reserves is at least partly explained by differences in propagule pressure. Similarly, large-flowered plants are often overrepresented among invasive taxa, not necessarily because they are inherently more invasive but because they are disproportionately selected for import by horticulturalists and therefore exert greater propagule pressure in their introduced range than small-flowered species.
The observation that many species have become successful invaders in multiple parts of the world following independent introduction events suggests that there is more to invasions than propagule pressure and random chance. Indeed, several studies have found the best predictor of invasiveness among a given group of species to be simply a previous history of invasions or widespread distribution elsewhere. This motivates the search for ecological traits associated with invasiveness. A central goal is the development of tools that predict which species will become invasive, although any such tools are unlikely to be perfect simply because highly invasive species often have physiologically similar noninvasive congeners.
Traits associated with invasive species include fast growth, generalist resource use, high reproductive output, high physiological tolerance, asexual reproduction, and long-distance dispersal capability. Invasive species are also often taxonomically distant from species in the invaded habitat. Examples of successful generalist invaders include feral cats (Felis catus) and brown tree snakes (Boiga irregularis), both of which are predators that have invaded many habitats globally that were naive to these taxonomic groups. Further insights come from taxonomic groups containing many species that have been introduced outside their natural range. For example, an analysis of the different Pinus species introduced across the globe revealed that dispersal ability, competitive ability, and adaptability to varying disturbance regimes explain almost all of the variation in invasiveness among species.
The most straightforward hypothesis to explain the invasiveness of particular alien species is the enemy release hypothesis. In their native ranges, populations of plants and animals are kept in check by a suite of predators, herbivores, and pathogens. When a species is introduced outside its native range, it will often escape the biotic constraints imposed by these enemies. This gives the invader a fitness advantage because it can reallocate resources from enemy defense to growth and reproduction. For example, the Australian brushtail possum (Trichosurus vulpecula) is a major pest in New Zealand, where it occurs at 10 times the densities seen in Australia, has fewer competitors and predators than in its home range, and has no microparasites and only 20% the number of macroparasites. The spectacular success of certain biological control programs (see section 4, below) also provides strong evidence for the enemy release hypothesis.
Although the enemy release hypothesis is certainly appealing as an explanation of alien invasions, empirical evidence for it is mixed. An observation that an alien species exhibits increased vigor and fecundity and lacks enemies from its home range is not sufficient to establish a causal relationship. Moreover, many alien species rapidly acquire enemies in their new range, especially as they spread and encounter a wider range of native species. The enemy release hypothesis may be especially applicable to specialist alien plants that have evolved chemical defenses against specialist herbivores in their home ranges—such species are less likely to acquire new enemies in the invaded range.
The complement to the question of which species are likely to invade is the question of which habitats are likely to be invaded. Characteristics of invasible habitats are geographic isolation, the occurrence of anthropogenic or natural disturbance, and high availability and quality of food, light, and other resources. That isolated habitats are more vulnerable to invasion is evidenced by the proliferation of alien species on oceanic islands such as Hawaii and New Zealand and in freshwater systems such as North America’s Great Lakes. Today, alien plant richness on islands is often equal to native plant richness, whereas on continents alien plant richness is typically about 20% of native plant richness. Disturbances that facilitate invasions include changes in fire and hydrological regimes, changes in nutrient levels, and changes in grazing regimes. Extensive plant invasions across grasslands in Australia and the Americas have been linked to changes in the fire regime.
An unresolved question in invasion biology is whether high native species richness facilitates or inhibits invasion by alien species. The “invasion paradox” is that independent lines of research support both negative and positive relationships between native species richness and invasibility. Resolution of the invasion paradox requires the synthesis of data from different types of study across a broad range of spatial scales: small-scale observational and experimental studies usually report negative relationships between native and exotic species richness, whereas most larger-scale studies are observational and report positive relationships. An explanation for a positive relationship at large scales is that large areas exhibit greater spatial heterogeneity and hence greater habitat diversity, and that such regions tend to support both more native and more alien species. Notably, theoretical models have demonstrated that the different native/alien diversity patterns at different scales would be expected as statistical artifacts even in the absence of any species differences.
Once invasions are under way, an understanding of the spatial and temporal propagation of invasive species is essential for predicting their impacts and designing effective management programs. The spread of an invasion is governed by many variables, including initial population size, the age structure and breeding system of the invading species, and characteristics of the invaded environment. Despite these complications, mathematical models of the spread of invasive species have been one of ecological modeling’s great success stories.
In 1951, J. G. Skellam developed the now-classic reaction-diffusion model of invasion biology, which describes the dynamics of a population that is both growing and spreading. Skellam’s model predicts that the front of an invasion should move at a constant velocity and has been successfully applied to case studies such as muskrats (Ondatra zibethicus) invading central Europe and sea otters (Enhydra lutris) recovering from near extinction along the coast of California.
Invasions that do not fit the Skellam model have motivated the development of extended models such as stratified diffusion models (which include occasional long-distance dispersal events), advection-reaction-diffusion models (where advection accounts for species that tend to drift in a particular direction, perhaps because of wind or water flow) and models that allow for environmental heterogeneity (such as rivers and mountain ranges). An important insight from the stratified diffusion models is that occasional long-distance dispersal events can dominate a species’ spread rate. The stratified diffusion models predict that the front of an invasion should move at an accelerating speed, and these models generally provide better fits than the basic Skellam model to data of invasive plant spread. The dynamics of systems in which the invading species is a predator or competitor of a native species have been successfully modeled using variations of the classic Lotka-Volterra predator-prey and competition models.
A common feature of invasions is an initial lag phase during which the species persists at low densities. This precedes a phase of rapid growth during which the species is recognized as a problem. Although some invasive species, such as zebra mussels, have exhibited only a brief lag phase or none at all, others may persist at low densities for decades before becoming abundant. An understanding of this feature of the spread of invasions is essential for identifying potential invaders early on and developing effective management strategies. There are several possible explanations for this lag phase. The first explanation, consistent with the basic Skellam model, is that an invading species may remain below detection thresholds even though its population is growing. A second explanation, consistent with the stratified diffusion model, is that invasions often begin from only a single introduced population, whereas species spread more rapidly from multiple foci. A third explanation is that invading species may require time to adapt genetically or behaviorally to environmental conditions in the new habitat. A fourth explanation is that an invading species may require a “window of opportunity” associated with favorable environmental conditions that allows it to grow above a critical threshold beyond which more rapid growth can occur.
By definition, alien invasive species are associated with negative ecological and economic impacts, but any discussion of these negative impacts must be set in the context of benefits provided by alien species. Agricultural, pastoral, horticultural, and forestry industries across the world depend heavily or entirely on alien species. Alien species provide more than 98% of the food grown in the United States. These economic benefits have been the primary motivation for past deliberate introductions of alien species, only a small proportion of which have actually become invasive.
The ecological impacts of alien invasive species can be grouped into three categories: drivers of extinction, modifiers of ecosystem processes, and modifiers of evolution. Perhaps the most widely recognized ecological impact of alien invasive species is the extinction and decline of native species following the introduction of new predators, competitors, and pathogens. In Guam, the introduced brown tree snake has been blamed for the extinction of over 10 native bird species. In East Africa’s Lake Victoria, the introduction of the predatory Nile perch (Lates niloticus) contributed to the extinction of about 200 species of native cichlid fish. In Hawaii, the introduction of avian malaria continues to be a major factor behind the collapse of the local avifauna. The American chestnut (Castanea dentata) was once a dominant tree in the forests of eastern North America but was virtually exterminated in the early twentieth century by chestnut blight, a disease caused by an introduced fungus. In Australia, introduced red foxes (Vulpes vulpes) have been implicated in the extinctions of 10 to 15 native mammal species. Troublingly, it is likely that many parts of the world are currently in “extinction debt” because of invasive species, meaning that invasive species have driven some native species below a minimum long-term viable population size, and further extinctions can be expected even in the absence of further invasions.
At a global scale, alien invasions are undoubtedly contributing to a decline in species diversity and the homogenization of the Earth’s biota: a few successful invasive species, such as black rats and rock doves (Columba livia), have proliferated across the world at the expense of many localized endemic species. At local and regional scales, however, invasions have often led to increases in diversity: in states of the United States and Australia, the average plant species diversity has increased by about 20%; on oceanic islands average plant species diversity has increased by about 100%. Similar or greater increases in diversity are also observed at higher taxonomic levels.
Although there are many examples of extinctions caused by alien predators and pathogens, there are far fewer examples of extinction caused by competition from alien species. In Britain, the decline of the native red squirrel (Sciurus vulgaris) is often blamed on competition with the introduced eastern gray squirrel (Sciurus carolinensis) but may be driven more by a disease carried by the introduced squirrel. Other cases of competition from alien species causing extinctions have occurred over long time scales, suggesting that the competitive effects are relatively weak. For instance, in Australia, competition with the dingo (Canis lupus dingo) contributed to the extinction of the thylacine (Thylacinus cynocephalus) before European settlement, but the process apparently took several hundred years.
An important observation, which has implications for management (see section 5, below), is that the relationship between alien invasions and extinctions is often correlative rather than causative. Causal inference is confounded by other threatening processes. For instance, feral pigs and alien plants are both blamed for the decline of native plants in Hawaii, but the proliferation of alien plants may be merely a secondary outcome of disturbance by pigs. In Florida’s Everglades, extensive alien tree invasions are at least partly to blame for declines in native biodiversity, but both of these processes are outcomes of changes to the region’s hydrology that resulted from a water-diversion project.
Thorny conservation issues arise when alien invasive species are themselves endangered in their home range. In such cases, the goal of conservation at a global level may conflict with goals of eradication and control at a local level. For example, the world’s largest population of wild banteng (Bos javanicus) occurs in Australia, a country to which it was introduced and where it is considered by many to be a pest. In some cases win-win situations are possible: animals from a population of introduced tammar wallabies (Macropus eugenii) in New Zealand were repatriated to Australia after they were found to be descendants of an extinct Australian population.
Less widely acknowledged, but perhaps of greater concern, are the impacts of alien invasive species on ecosystem-level processes such as nutrient cycling, fire regimes, siltation rates, and hydrology. Particularly large alterations may be caused by the introduction of species with novel physiological traits, such as nitrogen fixers. In Hawaii, the invasion of nitrogen-limited ecosystems by the nitrogen-fixing alien tree Myrica faya has altered ecosystem development by increasing nitrogen inputs to ecosystems by about a factor of four. In South Africa, invasion by alien trees (Acacia, Hakea, and Pinus spp.) has converted native Fynbos shrublands into woodlands, accelerated nitrogen input and nitrogen cycling, reduced stream flows, and modified the fire regime to one that is characterized by less frequent, more severe fires.
By altering environmental conditions, some invaders facilitate further invasion or prevent the reestablishment of native communities. In the western United States, invasive cheatgrass (Bromus tectorum) completely alters ecosystems by increasing fire frequency to the point where native shrub-steppe communities cannot recover. In Hawaiian wet tropical forests, leaf-litter decay rates of alien understory species are, on average, several times greater than those of native understory species, suggesting that alien invasion accelerates nutrient cycling and further facilitates the invasion of alien plants adapted to nutrient-rich soils. Such circumstances pose difficulties for management because the invaders have, in effect, moved the ecosystem into an alternate stable state. Perhaps most worrying is the potential for widespread invasions to transform ecosystems and create feedbacks that influence regional or even global processes such as climate.
Ultimately, the most profound impacts of biological invasions may be their effects on evolution, which occur through three mechanisms: evolutionary diversification of alien species in new environments; evolutionary adaptation of native species to altered ecological conditions; and hybridization between previously allopatric taxa.
Alien species tend to undergo genetic drift in new environments because their populations are isolated from the source population and contain only a fraction of the genetic material (the founder effect). This, combined with directional selection imposed by new ecological challenges and freedom from previous ecological constraints, provides opportunities for evolutionary innovation among alien species. The codling moth (Cydia pomonella), a pest of fruit crops, invaded North America in about 1750 and has since evolved into genetically distinct races that specialize on apple, plum, and walnut. Studies of the fruitfly Drosophila subobscura suggest that it has diversified along environmental gradients in its introduced range in the New World and that the genetic basis of this diversification is different from that along similar environmental gradients in its native Old World range.
The altered environmental conditions imposed by alien invasive species may also promote directional selection in native species. For example, native black snakes (Pseudechis porphyriacus) in Australia have evolved resistance to the toxins of invasive cane toads. Alien invasion can even promote diversification of native species. The most striking examples of this are herbivorous insects that have evolved distinct ecotypes to feed on alien plants. Diversification of native species can also occur via allopatric speciation in cases where only some populations of native species are invaded.
Hybridization occurs more rapidly than directional selection and diversification and provides the most compelling examples of evolutionary change associated with alien invasions. The most commonly observed impact of hybridization on biodiversity is negative: the loss of distinct endemic species. Both the New Zealand Gray Duck (Anas superciliosa) and the Hawaiian Duck (A. wyvilliana) are at risk of extinction through hybridization with the introduced North American Mallard (A. platyrhynchos). But hybridization can also have positive effects on biodiversity. A new, reproductively isolated species of cordgrass (Spartina anglica) evolved in England in the nineteenth century from a hybrid of one native and one exotic cordgrass. A recent case study of hybridization in fruit flies (Rhagoletis spp.) demonstrates that this phenomenon is also possible in animals.
Although this review has focused mostly on the negative impacts of alien invasions, a longer-term view reveals that the speciation processes facilitated by invasions will at least partly offset the biodiversity losses that we are currently observing. Another positive aspect of alien invasions is that they provide model systems for addressing basic research questions in ecology and evolutionary biology. Alien invasions can be viewed as experiments, albeit uncontrolled and imperfectly replicated, that would be unfeasible or unethical across the large range of spatial and temporal scales over which they occur. Examples of insights that have stemmed from studies of alien invasions are that species are not optimally adapted for their environment, that communities are usually not saturated with species, and that reproductive isolation can take millions of years.
The economic impacts of alien invasive species can be separated into damages and the costs of control. Alien invasive species are associated with economic damages to infrastructure, crops, pastures, livestock, forestry, fisheries, and human health. To the extent that environmental values can be quantified monetarily, economic damages are also associated with damages to ecosystem services, which include water supply, pollination, and the provision of recreational opportunities.
The annual economic costs of alien invasive species have been estimated at US$120 billion in the United States alone. To provide a context for these costs, alien species contribute about US$800 billion to the U.S. food system annually. About 80% of the costs in the U.S. study are attributable to a few groups of alien invaders: pests and pathogens of crop plants; crop weeds; introduced rats, which consume grain and other food intended for human consumption; feral cats, which eat native birds that have an associated recreational value; and introduced diseases of livestock and humans. Two other notable invaders of the United States, each of which is associated with roughly US$1 billion in annual economic costs, are the zebra mussel, which clogs water pipes and other equipment, and the red imported fire ant (Solenopsis invicta), which impacts wildlife, livestock, and public health.
In many cases, the high economic costs of alien invasive species can justify spending on alien species control programs. The U.S. experience with red imported fire ants prompted Australian government agencies to launch a fire ant eradication campaign that has spent over US$100 million since fire ants were detected in Queensland in 2001. In South Africa, cost-benefit analyses of mountain catchment areas invaded by alien trees demonstrated that the costs of controlling alien trees were less than the projected benefits of increased water flows from catchments—across the country, approximately 3 billion cubic meters of water is lost annually to alien trees. These analyses motivated the South African government’s Working for Water Program, which has spent more than US$400 million controlling alien trees since its inception in 1996.
Such cost-benefit analyses, although useful, are plagued by uncertainty in the underlying economic and biological data. Moreover, they can only provide a lower-bound estimate of the costs associated with alien invasive species, because it is difficult or even impossible to attach a dollar value to certain impacts, such as the loss of biodiversity or the depletion of the aesthetic values of natural areas. Thus, failure to demonstrate cost efficacy of alien species control does not mean that a proposed program would not be beneficial from the standpoint of overall societal welfare.
Prevention of unwanted introductions is the most cost-effective method of dealing with the invasive species problems. For a relatively small investment in quarantine and screening procedures, government agencies can reduce accidental and unwanted deliberate introductions. As discussed earlier, predicting invasiveness based on species traits is a difficult task, and this limits the effectiveness of quarantine procedures. Several countries presently use an “innocent until proven guilty” approach, whereby only species on a list of known offenders are prohibited entry. A “guilty until proven innocent” approach, placing the burden of proof on the importer, would obviously be more effective at excluding invasive species. However, because only a small proportion of introduced species actually become invasive, such screening systems are inevitably plagued by false positives. The issue of screening policies incites conflict among environmental groups, agricultural agencies, free-trade advocates, and commodity importers such as horticulturalists, fish and game agencies, and the pet industry. A step toward resolving this problem would be the introduction of legislation holding the importer of an alien species responsible for any damages caused if the species becomes invasive. Similar considerations are also pertinent to the debate over the release of genetically modified organisms into the environment.
Once a species has been introduced and become invasive, the goal becomes control, containment, or eradication. Eradications are easiest and most cost effective early on in the process of an invasion, before an alien species has become widespread or abundant. The problem with this is that the vast majority of alien species do not become serious problems, and it is unclear which alien species should be the focus of early eradication programs. There are few examples of alien species that have been successfully eradicated once an invasion is well established. Exceptions are the successful 50-year campaign to eradicate the American nutria (Myocastor coypus) from Britain, the successful eradication of introduced mammals from several offshore islands in New Zealand, and the apparent success of the Australian government’s expensive fire ant eradication program. Factors contributing to successful eradication programs are the use of specific knowledge of the target organism’s biology and the application of sustained funding and control efforts even after the immediate ecological and economic threats have been alleviated. When eradication is not feasible, control (maintaining the alien species at acceptably low densities) or containment (restricting the geographic distribution of the alien species) may still deliver economic and ecological benefits.
Strategies for the management of alien plants include chemical control, mechanical control, and biopesticides. Chemical control is widely used for pest control in agriculture and forestry but may have adverse environmental and public health impacts. The cost of such campaigns can escalate when repeated application is required or when the target species evolves resistance to the chemical. Moreover, campaigns involving chemicals often arouse considerable public resistance. Mechanical control arouses less public resistance and can often be effective, especially for large woody plants, but is difficult or impossible for widespread species.
Strategies for the management of alien animals include poison baiting, trapping, and shooting. Poison baiting has been particularly effective on introduced mammals. The Western Shield operation in Western Australia targets introduced foxes with baits containing a poison to which many native mammals are resistant. This program has led to the resurgence of native mammal species and even the removal of three species from the endangered list. However, as with chemical control of plants, poison baiting can impact nontarget species and engender public opposition. Trapping and shooting can be effective for alien animal species with restricted distributions. Again, public opposition is a factor here, as evidenced by outcry over feral horse control in the United States, Australia, and New Zealand. Recreational hunting may help maintain feral animal populations at acceptable densities, but it is generally ineffective as a means of eradication.
Classical biological control, the deliberate introduction of predators or pathogens can be particularly effective for regulating populations of invaders. Although only about 30-40% of biological controls on weeds and 10-15% of biological controls on arthropods are successful, the net benefit of biological control programs is positive because some are so spectacularly successful. On St. Helena, the gumwood tree (Commidendrum robstum) was threatened with extinction by an alien herbivorous insect (Orthezia insignis) but saved by the deliberate introduction of a predatory insect (Hyperaspis pantherina). In Australia, dense infestations of prickly pear cactus (Opuntia spp.) covered an area the size of the British Isles until the introduction of the cactoblastis moth (Cactoblastis cactorum) in the 1920s. In South Africa, the introduction of herbivores and pathogens of alien trees has had some success: an introduced gall-rust fungus of Acacia saligna has reduced stem densities by up to 98%.
Other forms of biological control include the release of sterile individuals into a population of an alien species or the introduction of novel genetic material. In the United States, the screwworm fly (Cochliomyia hominivorax) was successfully eradicated by introducing sterile males into the population. In Australia, current research efforts seek to control the European carp (Cyprinus carpio) by releasing transgenic individuals carrying a “daughterless gene.”
There is rising concern about the potential impacts of biological control on nontarget species. The small Indian mongoose, released onto numerous islands across the world to control introduced rats, has contributed to the decline of numerous native bird species. In Hawaii, the introduction of a predatory snail (Euglandina rosea) to control the giant African snail (Achatina fulica) led to the extinction of numerous native snail species. The myxomatosis virus from South America was used successfully to control introduced European rabbits (Oryctolagus cuniculus) in Australia in the 1950s; however, the virus subsequently spread to Europe, where it devastated native rabbit populations and thereby endangered species that prey on rabbits, such as the Spanish lynx. Even biological control agents that have been subject to stringent host-specificity testing have attacked nontarget species: a Eurasian weevil, Rhinocyllus conicus, introduced for the control of an invasive thistle in North America, has begun to attack native thistles. Furthermore, host-specificity testing cannot guard against indirect impacts of alien species on, for example, food chains or virus reservoirs. Although the likelihood of biological control agents having unintended consequences may be small, the magnitude of these consequences may be large, and so this possibility needs to be incorporated into cost-benefit analyses of biological control programs.
Habitat or ecosystem management is often prescribed as a holistic approach to alien invasive species problems. Such approaches target the overall condition of the ecosystem rather than individual alien species by focusing on processes such as native vegetation restoration, fire regimes, grazing regimes, and nutrient inputs. This can be seen as a shift from the symptoms of environmental problems to the fundamental causes. Numerous studies have shown that fertilization and disturbance promote alien plant invasion in grassland ecosystems. Success of native grassland restoration projects depends on the reduction of nutrient loads, the introduction of appropriate fire regimes, the existence of sufficient propagules of native species, and the control of alien species. In South Africa, alien plant management programs use a multispecies approach that incorporates numerous control methods and acknowledges the need for native vegetation restoration and appropriate fire regimes.
Management of alien invasive species becomes problematic when invasion is attributable to global change processes. Research on the impacts of global climate change has shown that some invasive species such as cheatgrass and kudzu (Pueraria lobata) respond positively to elevated carbon dioxide and that other species respond positively to elevated temperature and rainfall. Although habitat management and other control methods can still be used to manage these species, it is unclear what the desirable end state should be if external conditions, such as climate and nitrogen deposition rates, have changed.
Biological invasions have occurred throughout Earth’s history, but the current wave of anthropogenic invasions is occurring on an unprecedented scale. The small proportion of introduced alien species that become invasive cause massive ecological and economic damage. Ecological theories of invasions give us some guidance as to which species are likely to invade, how they will spread, and how they can be controlled or eradicated. The most effective method of managing the global biological invasion would be to strengthen international quarantine regulations. Once a species has already invaded, eradication is sometimes possible but difficult; more commonly, the invasion will necessitate ongoing control costs. Cost-benefit analyses can help determine which invasive species are worth controlling and where conservation funds can be directed. In conducting such cost-benefit analyses, it should be acknowledged that part of the problem with invasive species, as with other environmental issues, is that ecological values cannot easily be translated into dollar values.
The news on alien species is, however, not all bad. Large sectors of our economies are based on products derived from introduced alien species, most of which are not invasive. In many cases, alien invasions are symptoms of other problems such as climate change, changes to the nutrient cycle, changes to hydrology, and habitat clearance. Historically, alien invasions have increased local biodiversity at the expense of global biodiversity and heterogeneity, but over longer time scales, evolutionary diversification promoted by alien invasions may at least partly compensate for this lost biodiversity. Furthermore, alien invasions provide unparalleled opportunities for understanding the forces that shape ecological communities.
Invasion by alien species is now, along with climate change, habitat clearance, and changes to the nitrogen cycle, a major global change process. The biological communities of the future will likely be assembled from collections of species that originated in different corners of the globe and are able to adapt to the new environmental conditions. Understanding how alien invasions will interact with other global change processes to shape these communities is a fundamental challenge for ecologists.
A final point is that there is a strong geographic bias in research on biological invasions: most studies are of invasions in North America, Western Europe, South Africa, Australia, and New Zealand. These areas have probably historically been more prone to invasion because of their economic history and trading patterns, but the science of biological invasions would benefit from more research into invasions in the tropics and other understudied regions.
Cox, G. W. 2004. Alien Species and Evolution: The Evolutionary Ecology of Exotic Plants, Animals, Microbes, and Interacting Native Species. Washington, DC: Island Press. A comprehensive review of the interactions between alien invasions and evolution.
Elton, C. S. 1958. The Ecology of Invasions by Animals and Plants. Chicago: University of Chicago Press. Charles Elton’s classic book.
Fridley J. D., J. J. Stachowicz, S. Naeem, D. F. Sax, E. W. Seabloom, M. D. Smith, T. J. Stohlgren, D. Tilman, and B. Von Holle. 2007. The invasion paradox: Reconciling pattern and process in species invasions. Ecology 88: 317. A review of the observational, experimental, and theoretical evidence describing the invasion paradox.
Mack, R. N., D. Simberloff, W. M. Lonsdale, H. Evans, M. Clout, and F. A. Bazzaz. 2000. Biotic invasions: Causes, epidemiology, global consequences, and control. Ecological Applications 10: 689–710. A review of invasive species with a global perspective.
Mooney, H. A., R. N. Mack, J. A. McNeely, L. E. Neville, P. J. Schei, and J. K. Waage, eds. 2005. Invasive Alien Species: A New Synthesis. Washington, DC: Island Press. An edited volume reviewing the ecology, economics, and management of biological invasions. Pimentel, D., L. Lach, R. Zuniga, and D. Morrison. 2000. Environmental and economic costs of nonindigenous species in the United States. Bioscience 50: 53–65. An analysis of the costs of alien invasive species in the United States.
Sax, D. F., J. J. Stachowicz, and S. D. Gaines, eds. 2005. Species Invasions: Insights into Ecology, Evolution and Biogeography. Sunderland, MA: Sinauer Associates. An edited volume examining the scientific insights provided by alien invasions.
Shigesada, N., and K. Kawasaki. 1997. Biological Invasions: Theory and Practice. New York: Oxford University Press. A clear and accessible introduction to mathematical models of biological invasions.
Trends in Ecology and Evolution. 2005. Volume 20, issue 5. A special issue on invasions including articles on the management and risk assessment of invasions, and the role of propagule pressure in explaining invasions. Trends in Ecology and Evolution. 2007. Volume 22, issue 9. An issue containing several articles on biological invasions, covering biological control, the evolutionary impacts of alien species, and the interaction of habitat modification and species invasions.
IUCN. Invasive species specialist group’s global invasive species database. Download from http://www.issg.org/database/. A database that facilitates information sharing on invasive species internationally.
IUCN. Guidelines for the prevention of biodiversity loss caused by alien invasive species. Download from http://www.issg.org/infpaper_invasive.pdf. Information intended to assist governments and management agencies in preventing the introduction of alien species, and controlling or eradicating those that become invasive.