Encyclopedia of Biological Invasions

This pioneering encyclopedia illuminates a topic at the forefront of global ecology—biological invasions, or organisms that come to live in the wrong place. Written by leading scientists from around the world, Encyclopedia of Biological Invasions addresses all aspects of this subject at a global level—including invasions by animals, plants, fungi, and bacteria—in succinct, alphabetically arranged articles. Scientifically uncompromising, yet clearly written and free of jargon, the volume encompasses fields of study including biology, demography, geography, ecology, evolution, sociology, and natural history. Featuring many cross-references, suggestions for further reading, illustrations, an appendix of the world’s worst 100 invasive species, a glossary, and more, this is an essential reference for anyone who needs up-to-date information on this important topic.

Encyclopedia of Biological Invasions features articles on:

• Well-known invasive species such the zebra mussel, chestnut blight, cheatgrass, gypsy moth, Nile perch, giant African snail, and Norway rat

• Regions with especially large numbers of introduced species including the Great Lakes, Mediterranean Sea, Hawaiian Islands, Australia, and New Zealand.

• Conservation, ecological, economic, and human and animal health impacts of invasions around the world

• The processes and pathways involved in invasion

• Management of introduced species

• Language: English
• Publisher: University of California Press
• Release date: Jan 2, 2011
• ISBN: 9780520948433

Book preview

PREFACE

As you read this, thousands of species of plants, animals, fungi, and microbes have been or are being transported by humans to new locations, whether deliberately or inadvertently. This geographic rearrangement of the earth's biota is one of the great global changes now underway. Of course, species have always managed to spread, even without human assistance, but much less often, much more slowly, and not nearly so far. Over the last 150 years, beginning with the advent of steamships and accelerating with air travel, the rate of movement of some organisms has increased many-fold. Any distance can be quickly spanned by a plane; a hitchhiking seed, spore, or insect can be transported from Asia to South America, or from Africa to Australia, in a day. Although many introduced species fail to establish populations or remain restricted to the immediate vicinity of the new sites they land in, others establish populations and invade new habitats, spreading widely and sometimes well beyond the initial point of introduction. Their interactions, both within native communities and with other introduced species, have been noticed by biologists and, increasingly, by governments and the lay public.

Ecologists, evolutionists, economists, geneticists, agronomists, fisheries and forestry scientists, and many others study biological invasions for a variety of reasons. Some invaders are enormously costly, damaging agriculture, forestry, fisheries, and other human endeavors as well as natural areas. Other invaders are pathogens that cause human, animal, or plant disease; yet others are vectors that carry these pathogens. Many invaders depress populations of native species, and even threaten some with extinction, by preying on them, competing with them, hybridizing with them, infecting them with disease, or changing their habitat. The cost of biological invasions to the economy of the United States alone is estimated at over $100 billion annually.

However, trying to understand, estimate, and mitigate the damage caused by some invaders is only one reason for the rapid growth of research on biological invasions. Invasions are, in a sense, unplanned experiments in population, community, and ecosystem ecology; sometimes there are even forms of experimental control and replication—as, for example, when a species is introduced to certain islands in an archipelago but not to others. For legal, ethical, and logistic reasons, most if not all such introductions would be impossible to perform as planned scientific experiments, so it is not surprising that scientists rush to investigate them when such opportunities arise. Initially, most such purely scientific research was done by ecologists interested in such questions as what impact a wholly new species has on a native community and ecosystem, and to what extent a similar native species can impede invasion by a newly introduced species. More recently, recognition that an invasion constitutes an experiment in both evolution and ecology has led to an explosion of research on the evolutionary consequences of invasions for both invaders and residents. How, and how quickly, do invaders evolve adaptations, how do native communities adapt to an invader, and how does the small number of invading individuals affect the genetics of the expanding population of invading organisms?

Biological invasions have attracted attention for other reasons. The variety of impacts of introduced species is astounding. Many invasions have such idiosyncratic and bizarre effects that they cannot fail to arouse our curiosity simply as fascinating tales of natural history. For example, who would have predicted that introducing kokanee salmon to Flathead Lake, Montana, and, many years later, opossum shrimp to three nearby lakes would ultimately have led to population crashes of grizzly bears and bald eagles through a complicated chain reaction? Or that introducing myxoma virus to Great Britain to control introduced rabbit populations would have led to the extirpation of the large blue butterfly there? Who would have suggested that introducing a particular grass species would lead to hybridization with a native congener, subsequent polyploidization, and origin of a new vigorous invasive species that would change entire intertidal ecosystems? Teasing apart such intriguing causal chains is a scientific accomplishment of the first order. But the variety and idiosyncrasy of invasion effects also challenges attempts of invasion biologists to produce general laws or rules and to be able to explain why some introductions have no major impacts, yet others lead to huge invasions. Being able to predict which species will fall in the latter category if introduced, and which in the former, is the elusive holy grail of invasion biology.

Choosing topics for this work was difficult; even a large encyclopedia cannot contain every possible topic of interest relating to biological invasions. Had we restricted ourselves simply to species, in addition to the famed 100 of the World's Worst Invasive Alien Species (see Appendix), we would still have had to consider several hundred other noteworthy invasive species. Many kinds of habitats, and several regions, have been particularly afflicted by invasions. Certain groups of organisms are especially well represented among invasive species. As the science of invasion biology and technologies of managing invasions have matured, myriad subjects can now be treated in some depth. We could not cover all relevant topics, but we attempted to choose those that, in total, would treat the broadest possible range of subjects related to biological invasions. The additional readings suggested with the articles and at the end of this volume will help the reader further pursue individual topics and may provide an entree into topics that are not covered individually.

We are indebted to the 197 authors who contributed articles to this encyclopedia. Experts are always busy people, yet these made time to produce novel syntheses for a publication quite different from the scientific journals for which they usually write. Gail Rice of the University of California Press assisted us enormously in all facets of producing this encyclopedia—helping us locate experts and photographs, editing articles, keeping track of revisions, reminding tardy authors (and editors!), and even providing aesthetic advice on layout and formats. Her organizational and substantive skills were crucial to the project. Chuck Crumly of the University of California Press suggested the need for this encyclopedia, convinced us that we were the right people to edit it, and encouraged us as impediments arose. Finally, our families (Mary, Tander, and Ruth and Eliska, Honza, and Daniel) were enthusiastic, patient, and encouraging even as the encyclopedia, at times, dominated our lives.

Daniel Simberloff

University of Tennessee, Knoxville

Marcel Rejmánek

University of California, Davis

A

ACCLIMATIZATION

SOCIETIES

CHRISTOPHER LEVER

University of Cambridge, United Kingdom

Acclimatization societies were organizations formed by groups of like-minded but otherwise diverse individuals (aristocrats, landowners, biologists, agriculturalists, sportsmen, and others), whose mutual interest was the introduction of exotic animals and plants. These societies were formed to improve domestic stock, to supply additional food, to provide new game animals, to satisfy nostalgic yearnings, to control pests, and (in Russia) to substantiate the claims of evolutionists. They died out due to declining and unscientific membership, apathy by the public and scientific bodies, inadequate funding and dwindling revenues, increasingly strict legislation on the introduction of exotic species, and the growing realization that such introductions were ecologically unsound.

ACCLIMATIZATION SOCIETIES IN FRANCE

AND ITS COLONIES

From the 1780s onward, Louis Jean Marie Daubenton (1716–1799) was responsible for the increasing involvement of the Jardin des Plantes du Roi in Paris in the study of economic zoology, including the acclimatization of exotic species for commercial and agricultural purposes. In 1793 the Jardin was converted into the Muséum National d'Histoire Naturelle, which in turn was succeeded by the Jardin Zoologique d'Acclimatation.

In February 1854 a group of savants, under the chairmanship of then director Isidore Geoffroy Sainte-Hilaire (1772–1844), founded La Sociétié Zoologique d'Acclimatation for the introduction, acclimatization, and domestication of animals and for the cultivation of plants. Subsequently, satellite societies were formed in Grenoble, Nancy, Algeria, French Guyana, Guadeloupe, Martinique, and Réunion.

The most important plant introduced by the Société to France was a new variety of potato from Australia, to combat the impact of the same blight, Phytophthora infestans, that had caused the potato famine in Britain and Ireland in the 1840s. The most potentially valuable animal importations were Chinese silkworms and various species of fish.

The principal achievements of the Société were the formation of a menagerie in Paris and the development of agricultural crops in metropolitan France and Algeria.

By the late 1860s, membership of the Société and visitors to the menagerie were in decline, and government subsidies and other revenue were dwindling. In 1901 the Société was declared insolvent.

ACCLIMATIZATION SOCIETIES IN BRITAIN

The prime influence behind the acclimatization movement in Britain was Francis Trevelyan Buckland (1826–1880). At the time of his birth, Britain was still suffering from the economic consequences of the Napoleonic Wars of 1792–1815 and the Industrial Revolution. During this period, the corn harvests were exceptionally poor, and the wars hindered the importation of corn from abroad. The population, and the price of food, increased dramatically, and the rising labor pool helped to lower wages.

It was against this background that Buckland (Fig. 1) began to develop his interest in acclimatization. This concept was not new; a similar policy had been declared by the Zoological Society of London (ZSL), founded in 1826.

FIGURE 1 Frank Buckland physicking a porpoise. There was only one way; so I braved the cold water and jumped into the tank with the porpoise. I then held him up in my arms (he was very heavy), and, when I had got him in a favourable position, I poured a good dose of sal-volatile and water down his throat with a bottle. From The Curious World of Frank Buckland by G. H. O. Burgess, quoting from F. T. Buckland's Curiosities of Natural History (4 vols.) 1857–1872. Richard Bentley, London.

The trigger for the founding of the Society for the Acclimatization of Animals, Birds, Fishes, Insects, and Vegetables within the United Kingdom was a dinner held in London in 1860, attended by Buckland and presided over by the distinguished zoologist Sir Richard Owen (1804–1892), at which eland Taurotragus (Tragelaphus) oryx from London Zoo was the principal dish. So impressed by the eland were Owen, Buckland, and the other guests that later that same year, the Society was founded, with Buckland as honorary secretary. Also in the same year (1860), a branch was formed in Scotland (Glasgow), and in 1861 in the Channel Islands (Guernsey).

In 1865, the Society, clearly in financial straits, merged with the Ornithological Society of London. A decline in membership and an apparent lack of interest by the council led in 1868 to the Society's demise.

The principal reasons for the ephemeral life of the Society were its failure to attract enough scientific members, most of whom were drawn from the aristocracy and gentry; its inability to gain adequate government funding; and a lack of facilities for keeping exotic species, most of which were entrusted to the care of individual members. These factors collectively jeopardized the Society's ability to differentiate itself from such competitors as the ZSL. Nor was the Society's progress furthered by the apathy on acclimatization shown by the public and the prestigious British Association for the Advancement of Science. In contrast to the French Société, which examined the commercial and economic benefits of acclimatization to all classes, the Society inclined to the introduction of species to benefit only the upper class. Furthermore, most of the species considered for acclimatization by the Society were wholly unsuitable for that purpose.

ACCLIMATIZATION SOCIETIES IN AUSTRALIA

Acclimatization societies in Australia were formed in 1879 in New South Wales (in Sydney, having evolved from a society founded in 1852); in 1861 in Victoria (Melbourne); in 1862 in South Australia (Adelaide) and Queensland (Brisbane); in 1895 and 1899 in Tasmania (Hobart and Launceston, respectively); in 1896 in Western Australia (Perth); and at various provincial centers.

As in Algeria, the activities of acclimatization societies in Australia reached their zenith during the final days of protectionism, especially in such colonies as Victoria, which possessed the most important such society and which, even in the 1860s, depended on protective tariffs. A close parallel can be detected between the position and status of Victoria in the British Empire and Algeria in its French counterpart. The economy of both colonies was remarkably similar, and favorable tariffs on imports and government grants resulted in increasing interest in acclimatization. Algiers and Melbourne were both centers of rapid demographic growth.

In Australia, the acclimatization movement met with the same apathy as in Britain, based on the belief that the societies were acting in the interest of the privileged minority (Fig. 2).

The societies claimed that their introduction of insectivorous birds increased crop production, while pastoralists claimed that they consumed crops and displaced native birds. Deer provided sport and venison but damaged crops and trees. Eventually, many societies degenerated into importing species solely as curiosities or for ornamental purposes, and some metamorphosed into menageries. Few, if any, attempted to improve domestic stock or cultivars on which the prosperity of Australia depended. Those that survive are involved mainly with the introduction of fish.

FIGURE 2 Cartoon from the Melbourne Punch, May 26, 1884.

ACCLIMATIZATION SOCIETIES IN NEW ZEALAND

The thirty or so acclimatization societies that were formed in New Zealand between the 1860s (the first in Nelson in 1861) and the early 1900s had, as in the case of many of those elsewhere, two principal objectives: the introduction of game animals for sport and insect-eating birds to control pests.

As in other countries, some of the New Zealand societies eventually failed due to lack of support and falling revenues, coupled with increasing public criticism. Founded and run, as in Britain, by enthusiastic amateurs, they were managed unprofessionally, and they failed to keep adequate records that would have shown their critics the value of revenue derived from visiting sportsmen and the benefit to crops.

After the Second World War, control of the societies by the government increased, and their operations became mainly confined to conservation; the promotion of sport; and, in a complete role reversal, the prevention of further introductions of nonnative species.

The main income of acclimatization societies in New Zealand today comes from the sale of sporting licenses; part of this income is used to acquire wetland habitats, fund research, and educate the public on conservation issues: the balance funds the societies' own conservation programs.

ACCLIMATIZATION SOCIETIES IN RUSSIA

An interest in the acclimatization and domestication of nonnative animals and plants existed in Russia since at least the early 1840s and was led by the distinguished biologist Karl Frantsevich Rul'e (1814–1858).

The primary topic among scientists at the time was the immutability or mutability of species. Rul'e used the transformation of species through acclimatization, domestication, and cultivation to support the theory of mutability (evolution).

Under the leadership of Rul'e, the Imperial Russian Society for the Acclimatization of Animals and Plants was formed in Moscow in January 1864; branches were later established in St Petersburg, Khar'kov, and Orel.

After Rul'e's death, his successors, led by his protégé Anatoli Petrovich Bogdanov (1834–1896), continued his work. As early as 1856, Bogdanov and his colleagues had formulated the idea of establishing a scientifically based zoo in Moscow. Almost from the start, however, dissent broke out between those who gave preference to pure research and those who favored applied research in acclimatization, domestication, and hybridization. This controversy was soon overshadowed by the zoo's financial failure, though it rumbled on well into the twentieth century and had a profound effect on the development of Russian science. Thereafter, the Society began to stagnate, although outside its ranks, the interest in acclimatization actually increased, in particular in the translocation of native fur bearers and the widespread formation of many research sad (gardens).

By the early 1900s, it had become accepted within the Society that acclimatization must give way to conservation, and that the introduction of exotics could be actually harmful. By 1930 the Society had ceased to exist.

Although during its 65 years the Society failed to acclimatize (naturalize) any alien species in Russia, it did encourage local attempts in acclimatization of a wide range of, albeit as in Britain, wholly unsuitable, species.

ACCLIMATIZATION SOCIETIES

IN THE UNITED STATES

Although since as early as 1846, songbirds, including the house sparrow Passer domesticus, were successfully released in the United States, the founding father of the acclimatization movement was a New York pharmacist, Eugene Schiefflin, who, with John Avery, in 1871 founded the American Acclimatization Society, which in 1877 successfully released the first European starlings Sturnus vulgaris in Central Park.

In 1873 Andrew Erkenbrecher formed the Cincinnati Society of Acclimatization, which in 1873–1874 unsuccessfully (except in the case of house sparrows) released in the city 21 alien bird species.

At about the same time, the Society for the Acclimatization of Foreign Birds was founded in Cambridge, Massachusetts. In 1872–1874, it freed large numbers of goldfinches Carduelis carduelis, some of which survived until at least the turn of the century.

In Portland, Oregon, in 1880, C. F. Pfluger founded the Society for the Introduction of Useful Songbirds into Oregon (the Portland Songbird Club), which in 1889 and 1892 unsuccessfully (except in the case of the European starling) released 15 species.

These societies spawned several others throughout the United States, of which the Country Club of San Francisco was formed mainly to introduce brown trout Salmo trutta to California. It also dispatched chinook salmon Oncorhynchus tshawytscha ova to New Zealand, where, under the name quinnat salmon, it became a popular game fish.

In 1884 the Cincinnati Society of Natural History rightly stated that the introduction of alien species was ecologically unsound, a pronouncement that seems to have sounded the death knell for acclimatization in the continental United States.

ACCLIMATIZATION SOCIETIES IN THE

HAWAIIAN ISLANDS

Although since 1865 private individuals had released in the Hawaiian Islands (then a territory of the United States) a number of bird species with varying degrees of success, it was not until 1930, under the presidency of Mrs. Frederick J. Lowery, that the Hui Manu (Hawaiian for bird society) was formed, for the introduction of songbirds to the islands. In the same year, immigrants from Japan founded the Honolulu Mejiro (the national name of the Japanese white-eye Zosterops japonica) Society, specifically for the introduction of Japanese songbirds. Among the species successfully freed by these two organizations were northern mockingbirds Mimus polyglottos, white-rumped shamas Copsychus malabaricus, Japanese bush-warblers Cettia diphone, varied tits Parus varius, Japanese white-eyes, red-crested cardinals Paroaria coronata, northern cardinals Cardinalis cardinalis, red avadavats Amandava amandava, and black-headed mannikins or munias Lonchura malacca.

In 1968, diminishing funds and increasingly strict regulations about importing and releasing alien birds in the islands caused the Hui Manu to disband.

ACCLIMATIZATION SOCIETIES

IN GERMANY AND ITALY

In 1858 the Akklimatisations-verein was formed in Berlin, and in 1861 the Società di Acclimazione in Palermo, Sicily.

SEE ALSO THE FOLLOWING ARTICLES

Australia: Invasions / Birds / Game Animals / Hawaiian Islands: Invasions / New Zealand: Invasions / Xenophobia

FURTHER READING

Jenkins, C. F. H. 1977. The Noah's Ark Syndrome: One Hundred Years of Acclimatization and Zoo Development in Australia. Perth: Zoological Gardens Board of Western Australia.

Lever, C. 1992. They Dined on Eland: The Story of the Acclimatization Societies. London: Quiller Press.

McDowall, R. M. 1994. Gamekeepers for the Nation: The Story of New Zealand's Acclimatisation Societies. Christchurch: Canterbury University Press.

Osborne, M. A. 1993. The Société Zoologique d'Acclimatation and the New French Empire: Science and Political Economy during the Second Empire and Third Republic. Bloomington: Indiana University Press.

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ADELGID

SEE HEMLOCK WOOLLY ADELGID

AGREEMENTS,

INTERNATIONAL

JAMIE K. REASER

Ecos Systems Institute, Stanardsville, Virginia

International agreements are used between or among national governments in order to establish mutual understanding, shared objectives, and, if legally binding, common law. Nearly 50 international agreements address some aspect of invasive species management, although the explicit prevention and control of invasive species is a relatively recent objective. International agreements focused on such issues as trade, agriculture, transportation, and energy have, however, inadvertently forged pathways for the spread of invasive species—likely for thousands of years. There is considerable need to strengthen the capacity of governments to implement international agreements on invasive species, as well as to raise awareness of the invasive species issue within the context of those international agreements that have substantial influence on the pathways of biological invasion.

CHARACTERISTICS OF INTERNATIONAL

AGREEMENTS

International agreements take many forms:

•   Bilateral agreements exist between two governments, while multilateral agreements are made by three or more governments.

•  Legally binding agreements (generally referred to as treaties or conventions) must be observed and met in good faith; in contrast, nonbinding agreements (generally called soft law—e.g., codes of conduct) provide guidance but are not enforceable. Protocols are supplementary, often more specific, guidance within the context of legally binding agreements.

•  Regional agreements are made among neighboring countries and may include the distant protectorates of those neighboring countries.

•  Nongovernmental organizations (e.g., the International Union for Conservation of Nature [IUCN]) may also develop guidelines or policy positions to inform negotiating parties.

•  The focus of international agreements may be relevant to a specific driver of biological invasion (e.g., climate change, trade, agriculture), a region (e.g., country or set of countries), an ecosystem (e.g., wetlands), or a species (e.g., migratory wild animals), or it may broadly encompass multiple dimensions of the issue.

UTILITY OF INTERNATIONAL AGREEMENTS

International trade, travel, and transport greatly facilitate the movement of species around the world. Organisms are also inadvertently relocated as hitchhikers through international military activities, famine and disaster relief, development assistance, and financing programs. Once an invasive species becomes established in one country, it can threaten the entire region, as well as every country along the network of intersecting pathways. Thus, no country can effectively prevent biological invasion without engaging in international dialogue and cooperation, as well as helping to raise the capacity of other countries to effectively manage invasion pathways and invasive species within their own borders.

Although aspects of the invasive species issue have been a topic of international agreements since the 1950s, national and international responses to the invasive species problem as a whole are very recent. The Global Invasive Species Programme (GISP) has played a significant role in advancing international agreements on invasive species by producing numerous documents (e.g., The Global Strategy on Invasive Species), as well as by hosting national and regional workshops to help governments understand and constructively engage in this technically complex issue.

The effectiveness of international agreements, however, largely depends upon the will and capacity of member governments to enforce their provisions. Despite the recent promulgation of mandates and soft law tools aimed at invasive species through various international agreements, relatively few governments are investing in the development of well-coordinated policies and programs across relevant sectors (e.g., agriculture, environment, trade, transport, defense). Many countries are constrained by lack of implementation capacity (especially financial, technical, and informational). Furthermore, competing political priorities (e.g., trade expansion versus invasion prevention) exist within and among governments and often hamper international negotiations. Governments routinely find themselves challenged by the perceived need to support economic growth while simultaneously protecting their natural environments and domestic industries from potentially harmful imports. For this reason, there is increasing interaction between the World Trade Organization (WTO) and international organizations with an invasive species mandate.

LEGALLY BINDING INTERNATIONAL

AGREEMENTS

A multiyear negotiation process is standard for binding treaties, conventions, and associated protocols. The process of agreement is commonly reached through consensus and results in general, broadly interpretable guidance. Separately negotiated, detailed rules can be developed in associated annexes, but this is rare given the length of overall negotiating time required. In most cases, the agreements must be signed and ratified by the cooperating governments in order to bind them to the provisions.

The following are examples of legally binding agreements that have an explicit focus on invasive species:

•  International Plant Protection Convention (IPPC, 1951 with revisions entering into force in 2005): Applies primarily to pests of plants that occur in international trade (quarantine pests). Member countries must implement a series of phytosanitary measures to prevent the spread of organisms potentially harmful to plants and plant products. Regional plant protection organizations (e.g., the North American Plant Protection Organization [NAPPO]) exist to facilitate implementation of the IPPC.

•  Convention on Biological Diversity (CBD, 1993): Article 8(h) calls on member governments to prevent the introduction of, or to control or eradicate, those alien species that threaten ecosystems, habitats, or species. The CBD has negotiated guiding principles and programs of work focused on invasive species, and the invasive species issue is also addressed as a topic under other thematic areas.

•  International Maritime Organization (IMO): In 2005 the Marine Environmental Protection Committee (MEPC) adopted formal guidelines for the implementation of the 2004 International Convention for the Control and Management of Ship's Ballast Water and Sediments.

•  Convention on the Conservation of European Wildlife and Natural Resources (Bern Convention, 1979): Requires member governments to strictly control the introduction of nonnative species (Article 11.2.b). This single legal provision has been used to develop a pancontinental strategy (European Strategy on Invasive Alien Species), as well as many species-specific recommendations.

•  Convention for the Protection of the Natural Resources and Environment of the South Pacific Region (SPREP, 1986): Among other things, Article 14 calls for member governments to take all actions necessary to protect rare and endangered species in the convention area, including the regulation of activities (e.g., trade) that could negatively impact them. The Invasive Species in the Pacific: A Regional Strategy has been adopted. The Protocol to the Antarctic Treaty on Environmental Protection (1991) prohibits the introduction of nonnative species to the Antarctic Treaty Area without a permit.

SOFT LAW INSTRUMENTS

Nonbinding agreements can often be reached in a much shorter timeframe than treaties or conventions and do not require a ratification process. Soft law resolutions are generally adopted within the context of intergovernmental organizations and may be produced as forwardlooking guidelines, codes of conduct, recommendations, programs of work, or declarations of principles. These nonbinding instruments often serve as precedents or complements to binding agreements.

The following are examples of soft law approaches that focus on the invasive species issue:

•  Food and Agriculture Organization of the United Nations (FAO): Addresses invasive species through a variety of economic sectors and cooperates with other international instruments. For example, codes of conduct relevant to fisheries (1995) and biocontrol agents (1995) recommend actions that member governments can take to limit the introduction of harmful nonnative species.

•  International Union for the Conservation of Nature (IUCN): Adopted IUCN Guidelines for the Prevention of Biodiversity Loss caused by Alien Invasive Species as drafted by its Invasive Species Specialist Group (ISSG). These guidelines had substantial influence on the development of GISP's Global Strategy and the CBD's Guiding Principles on invasive alien species.

•  International Civil Aviation Organization (ICAO): Three resolutions (A32-9, A33-18, and A35-19) request the ICAO Council to work with other United Nations organizations to identify and report on approaches it might take to reduce the risk of introducing potential invasive species through civil air transportation and urge member governments to support each other's efforts to reduce the risk of invasive species transport.

LOOKING AHEAD

International bodies are making substantial strides in increasing understanding and synergies among the various international agreements, even across sectors (e.g., cooperative work between the CBD and IPPC). This will help reduce the likelihood of gaps, inconsistencies, and duplication in the future and provide the clarity and consistency needed for effective implementation.

Globalization and large-scale environmental changes require that even more attention be given to the application of international agreements as a fundamental tool in the prevention and control of invasive species. The alternative energy sources being fostered in the context of climate change (e.g., biofuels) are already creating political conflicts under agreements such as the CBD, while the invasive species issue is not yet being adequately acknowledged under international agreements focused on climate or energy.

The decline in the global economy will hinder the ability of many governments to participate effectively in international negotiations and make their implementation of existing agreements even more challenging. International funding agencies (e.g., Global Biodiversity Facility [GBF]) need to support these governments by making invasive species a higher funding priority.

International governing bodies (e.g., the United Nations) are increasingly engaging nongovernmental organizations and the private sector in supportive roles. For example, the CBD recently called on the Pet Industry Joint Advisory Council (PIJAC) to work with GISP to create a toolkit of best management practices for reducing risks associated with the pet trade as a release pathway. If this trend continues, the private sector and nongovernmental organizations will be better poised to help raise the capacity of governments to participate in and enact both legally binding and soft law tools aimed at minimizing the impact of invasive species.

SEE ALSO THE FOLLOWING ARTICLES

Black, White, and Gray Lists / Laws, Federal and State / Regulation (U.S.)

FURTHER READING

McNeely, J. 2001. Global Strategy on Invasive Species. Gland: Global Invasive Species Programme/IUCN–World Conservation Union.

Reaser, J. K., E. E. Clark, and N. M. Meyers. 2008. All creatures great and minute: A public policy primer for companion animal zoonoses. Journal of Zoonoses and Human Health 55: 385–401.

Reaser, J. K., B. B. Yeager, P. R. Phifer, A. K. Hancock, and A.T. Gutierrez. 2004. Environmental diplomacy and the global movement of invasive alien species: A U.S. perspective (362–381). In G. Ruiz and J. Carlton, eds. Invasive Species: Vectors and Management Strategies. Washington, DC: Island Press.

Shine, C. 2008. A Toolkit for Developing Legal and Institutional Frameworks for Invasive Alien Species. Nairobi: The Global Invasive Species Programme.

Shine, C. 2007. Invasive species in an international context: IPPC, CBD, European Strategy on Invasive Alien Species and other legal instruments. OEPP/EPPO Bulletin 37: 103–113.

Shine, C., N. Williams, and L. Gündling. 2000. A Guide to Designing Legal and Institutional Frameworks on Alien Invasive Species. Gland: IUCN - The World Conservation Union/The Global Invasive Species Programme.

AGRICULTURE

ADAM S. DAVIS

USDA-ARS Invasive Weed Management Unit, Urbana, Illinois

DOUGLAS A. LANDIS

Michigan State University, East Lansing

Agricultural production of food, feed, fiber, or fuel is a local human activity with global ecological impacts, including the potential to foster invasions. Agriculture plays an unusual role in biological invasions, both because it is a source of nonindigenous invasive species (NIS) and because it is especially susceptible to invasions. A formerly innocuous species may become invasive when its environment no longer constrains its population expansion, either due to geographic dislocation or because of local environmental change. Agriculture is associated with both types of environmental alterations, triggering invasions by NIS and causing other species to become native invaders.

AGRICULTURE AS A SOURCE OF INVADERS

Intentional cultivation and dispersal of plant and animal species in an agricultural context is an ancient human activity with a modern twist. Historically, the growing of food, fiber, and fuel was fundamentally a site-specific practice; over millennia, crop cultivars and animal breeds were selected for their ability to thrive in certain environments. Long-term cultivation of specific crops in an area results in stable management practices and agroecosystem community composition. In contrast, modern agriculture frequently includes regional and international trade, with traded species changing rapidly in response to varying market demands.

Agriculture and agricultural trade may promote biological invasions in several different ways (Fig. 1). First, intentionally transporting species, allowing them to sample different environments, results in high propagule pressure. Trade can introduce commercially valuable species to areas that may benefit economically from their production, yet in a new environment, these species may become invasive. Second, the transfer of a crop species may result in the unintentional transfer of close associates, such as pathogens, weeds, or insect pests of the crop from its source range. Third, the cultivation of species in different environments promotes invasions by reducing stochastic effects on survival normally associated with founder events. Rather than one low-probability chance of establishing in a new environment, as might happen with unintentional species transfer (often resulting in very high mortality), cultivated populations are maintained under favorable conditions, with multiple chances to disperse beyond cultivated boundaries.

FIGURE 1 The relationship of agricultural systems to the spread of nonindigenous invasive species (NIS) can be defined by (1) the type of land management in the introduced range (arable or nonarable lands), and (2) whether the population is expanding or not at a given place and time, either due to saturation of the new range or due to characteristics of the species or environment that hinder invasion.

AGRICULTURE AS A SINK FOR INVADERS

Several features of agricultural management make agroecosystems particularly susceptible to biological invasions. First, all agroecosystems are intentionally simplified in time and space: one or two (at most, several) species are reared in a designated area during a defined time period. At its most extreme, this results in continuous monoculture, in which a single crop is grown repeatedly. Historically, cropping systems were more diversified, in the sense of including both plants and animals grown in complementary temporal sequences and featuring spatially heterogeneous arrangements. However, at present, cropping system diversity is low throughout many of the world's productive agricultural regions. Just as increasing ecosystem diversity can provide biotic resistance to invasions, decreasing diversity may increase vulnerability to invasion by pest organisms.

Second, all agroecosystems are subjected to repeated, predictable disturbances in the form of agricultural management, including tillage, planting, soil fertility management, and harvest. These disturbances collectively exclude many organisms, opening up biological space for colonization by those species able to exploit these conditions.

Third, resource availability, especially that of essential nutrients, in agricultural ecosystems is often much greater than in nonarable systems. Many invasive species thrive in nutrient-rich environments, outcompeting natives that are adapted to lower nutrient levels.

Finally, the high levels of connectivity in the agricultural landscape facilitate dispersal of invaders. In the northern corn belt of the United States, is it not uncommon for states to have more than two-thirds of their land area devoted to crop production. In more heterogeneous agricultural landscapes, transmission of invasive organisms from one field to another may be reduced, but the potential for ongoing host—pest cycles between agricultural hosts and overwintering hosts in nonarable lands, as with soybean aphid and buckthorn (see below), may increase.

A BESTIARY OF AGRICULTURAL INVADERS

The difference between an organism termed an agricultural pest and one labeled as an invasive species is primarily one of geographic origin. Native organisms that reduce agricultural productivity, such as the redwing blackbird (Agelaius phoeniceus) in North American maize production, are considered pests. Weeds are also considered pests, although many weeds are not native to the crop production areas they infest and therefore could be considered invasive. Here, we present examples of a variety of invasive and exotic pest species associated with agricultural systems (Table 1).

Plants

WEEDS Plants that compete with crops or other desired species for light, nutrients, and water are termed weeds. They may be of native origin or may have been brought to the production field as contaminants of soil or seed from an exotic source. Most long-term intensive agricultural systems are characterized by a relatively stable weed flora with several dominant species. Over time, these species disperse throughout the crop production range and become so highly represented in the soil seedbank that even exotic weeds can saturate the invaded range. Velvetleaf (Abutilon theophrasti) and common lambsquarters (Chenopodium album) were both brought to North America in early stages of European colonization. Their range expansion followed the plow, and both species can be found in all U.S. states and Canadian provinces.

TABLE 1

Examples of Invasive Species Associated with Agriculture

a Invader type abbreviations: C = crop introduction, H = alternate host for pest organism, HR = herbicide resistant biotype, I = insect pest, L = livestock, P = plant pathogen, W = weed

b Native range abbreviations: A = Asia, EA = Eurasia, NA = North America

CROP ESCAPEES The great majority of exotic invasive plant species were transported to their invaded range intentionally, often as ornamentals or food crops. Johnsongrass (Sorghum halapense) was imported to the United States in the early 1800s as a forage crop. Less than a century later, the United States Department of Agriculture organized a control program for this species, now found throughout North America. Ironically, although S. halapense produces large amounts of forage, it can be toxic to ruminants in early growth stages, or when trampled or stressed, severely limiting its use as a forage. Giant reed (Arundo donax) is another species disseminated for commercial purposes that later escaped cultivation. At the turn of the twentieth century, A. donax was brought to the southwestern United States for a variety of purposes, including woodwind instrument reed production and streambank stabilization. The plant proliferated rapidly in riparian areas (Fig. 2), choking out native vegetation and reducing streamflow. More recently, A. donax has been proposed for use as a biofuel feedstock, a move likely to result in further expansion of its invaded range.

FIGURE 2 Arundo donax (giant reed) is a warm-season perennial grass that spreads primarily via clonal expansion and fragmentation. Native to the Indian subcontinent, it has invaded riparian areas with Mediterranean climates worldwide. It is currently being considered as a biofuel feedstock crop in the southeastern United States. (Photograph courtesy of Dr. John Goolsby, USDA-ARS Beneficial Insects Research Unit, Weslaco, Texas.)

HITCHHIKERS OF GLOBAL TRADE Not all invasive plant species associated with agriculture are disseminated intentionally. Some are dispersed as byproducts of global agricultural trade. Seed sold for use in planting crops is generally certified as being nearly weed-free, but feed grains are not subject to the same level of cleaning or scrutiny. The seeds that move with grains tend to be of a similar size and density, thus avoiding separation through sieving or forced-air cleaning. One plant invader that has gained notoriety recently via this pathway is giant ragweed (Ambrosia trífida), a native of North America and a common weed of corn and soybeans. It has recently invaded agricultural lands in both Europe and Asia, bringing with it the allergenic pollen that causes hay fever.

EVOLUTION OF INVASIVE GENOTYPES With the development of herbicide-tolerant crop cultivars at the close of the twentieth century, agricultural impacts on weed communities changed profoundly. Previously, weed management had varied considerably over time, with one technique having been the use of herbicides with different modes of physiological action; now, stresses have become highly predictable and uniform. Unsurprisingly, weeds have adapted to these stresses, with over 180 weed species having become herbicide resistant. Glyphosate-tolerant soybean and corn cultivars dominate crop sequences throughout much of the field crop production area of the Americas. An increasing number of weed species, including marestail (Conyza canadensis), common waterhemp (Amaranthus rudis), and Palmer amaranth (Amaranthus palmeri), all of which were once thought to be immune to the development of herbicide resistance, have now become resistant to glyphosate. These invasive biotypes often start out being highly localized, but seed and pollen dispersal via wind and human activities help them rapidly to invade new territory, leaving behind obsolete herbicide modes of action.

Animals

INSECTS Similar to weeds, insects can be native pests, escapees from cultivation, or exotic invaders. In North America, the Colorado potato beetle, or CPB (Leptinotarsa decimlineata), is an example of an endemic insect pest. The CPB is believed native to central Mexico but is now the principal pest of cultivated potatoes throughout the continent. In the past, CPB fed on native Solanaceae, but it switched to cultivated potato when this crop was introduced into the beetles' native range. Following this host switch, CPB expanded its range, eventually cooccurring with potatoes throughout much of the northern hemisphere.

While insects are seldom managed as strictly agricultural species, the gypsy moth (Lymantrea dispar) was originally brought to the United States from Europe for experiments in silk production. In its native range, it naturally feeds on a variety of deciduous trees. It escaped and is now a major pest of forests throughout the northeastern United States west to the Great Lakes region.

New exotic insects also continue to colonize agricultural systems. Soybean aphid (Aphis glycines) and associated species provide excellent examples of how agricultural- and natural-area invaders can interact. Soybean aphids were first discovered in the United States in the summer of 2000, when they were found feeding on cultivated soybeans in southern Wisconsin. Currently, the aphids occur from the northeastern United States west to the Dakotas and south to Missouri, and they can reach populations of up to 60,000 aphids or more per plant. The rapid expansion of the soybean aphid was fostered by the prior establishment of its primary overwintering host in North America, common buckthorn (Rhamnus cathartica). Common buckthorn was originally imported into the United States for use as a hedging plant. It escaped cultivation, colonizing fencerows, woodlots, and natural forests throughout much of the eastern and north central United States. Thus, the widespread cooccurrence of the soybean aphid's overwintering host (common buckthorn) and summer host (cultivated soybean) provided an ideal situation for rapid landscape spread of this exotic insect. Moreover, outbreak populations of soybean aphid favor another exotic, the multicolored Asian lady beetle (Harmonia axyridis). The Harmonia beetle is a natural predator of the soybean aphid (Fig. 3) and can build to large numbers in aphid-infested soybeans. It is also an intraguild predator, known to eat the eggs and larvae of other lady beetles, and it has been associated with declines in native lady beetle species. Finally, Harmonia has the habit of overwintering in large numbers in homes and other buildings, where it can cause human allergies.

VERTEBRATES Rodents, including rats, mice, and rabbits, are serious invasive pests in cropping systems throughout the globe. Rats and mice have been widely transported via human activities, including agricultural trade. These species may cause losses in the growing crop, or more frequently, in stored agricultural products. It is estimated that rats cause losses of $25 billion per year in India alone. Endemic vertebrates are a common cause of crop losses as well. In the United States, whitetail deer (Odocoileus virginianus) and Eastern wild turkey (Meleagris gallopavo) and geese are common direct pests in agricultural crops. Feeding in agricultural fields subsidizes their populations and can heighten their impacts on natural ecosystems. For example, snow geese (Chen caerulescens) in North America spend the winter feeding in agricultural fields in their overwintering range. Given this highly nutritious food source, they return to their breeding grounds in better condition, where they then produce more offspring. In some areas, they have increased to the point that they are causing ecological damage to the tundra.

FIGURE 3 Aphis glycines (soybean aphid) is a phytophagous insect pest of soybean fields that originated in East Asia. In both its native and exotic ranges, it is frequently attacked by Harmonia axyridis. (Photograph courtesy of Kurt Stepnitz, Michigan State University.)

Agricultural livestock, including feral swine, goats, and rabbits, cause damage in natural ecosystems. Feral swine (Sus scrofa) are generalist feeders and have been reported to cause harm to native plant, insect, amphibian, reptile, and vertebrate communities. The European rabbit (Oryctolagus cuniculus) was imported into Australia by European settlers. In the absence of natural predators, populations exploded, causing widespread damage in crop and natural habitats. Extensive feeding on native plants left soil unprotected and exposed to erosion.

Pathogens

Plant pathogens may invade a new geographic region through several pathways, including transportation of infected plant tissue, wind and rain dispersal, and movement of animal vectors. Late blight of potato, caused by the pathogenic fungus Phytophthora infestans, requires overwintering potato tubers to survive. When infected tubers are brought to a new location, this devastating disease follows, wiping out entire crops. The primary defense against this, and many other plant pathogens, is to breed resistant crop varieties.

FIGURE 4 Phakopsora pachyrhìzì (soybean rust) is a soybean pathogen that originated in East Asia and is increasingly common in soybean production worldwide. (Photograph courtesy of Dr. Glen Hartman, USDA-ARS National Soybean Research Laboratory, Urbana, Illinois.)

Prevailing winds can carry fungal spores hundreds of miles. Soybean rust (Phakopsora pachyrhizi; Fig. 4), native to East Asia, was first identified in the U.S. soybean production region in 2004. Soybeans are the main economic species affected by this fungus, but there are many alternate hosts, including another invader, kudzu (Pueraria montana), and so soybean rust can overwinter easily and infect new plants. Wind then disperses new spores to uninfected regions. Fortunately, fungicides have proven very effective against this pathogen.

Sometimes, one pest may facilitate another. In the case of maize dwarf mosaic virus (MDMV), three pests interact to complete the disease cycle. Aphids that feed on infected maize can be infected within minutes; they then carry it to other maize plants or S. halepense, an alternate host. Because S. halepense is a perennial, it provides an excellent overwintering location for MDMV to begin the infection cycle anew the following growing season.

PREVENTING FUTURE AGRICULTURAL

INVASIONS

Preventing agricultural invaders is considered the best strategy for reducing their impacts on both agriculture and natural ecosystems. This should involve careful screening of new crop species and varieties for potential invasiveness and to ensure that insects and diseases are not introduced along with crop material. Increased interest in biofuel production means active interest in new crop introductions in many parts of the world. Biofuel crops share many characteristics with invasive plants and should be subjected to particularly stringent review.

There is much scope for managing agricultural systems to reduce the opportunity for invasion, the impacts of invaders, and the invaders that agricultural systems supply to natural areas. These include improved sanitation to prevent transport of propagules from one field to another, improved monitoring to facilitate early detection and eradication or containment of invaders, and increased crop and landscape diversity, which can improve biotic resistance to invaders.

SEE ALSO THE FOLLOWING ARTICLES

Genotypes, Invasive / Herbicides / Integrated Pest Management / Native Invaders / Parasitic Plants / Pathogens, Plant / Seed Ecology / Weeds

REFERENCES

Buddenhagen, C. E., C. Chimera, and P. Clifford. 2009. Assessing biofuel crop invasiveness: A case study. PLoS ONE 4(4), e5261: 1–6.

Clements, D. R., A. DiTommaso, N. Jordan, B. D. Booth, J. Cardina, D. Doohan, C. L. Mohler, S. D. Murphy, and C. J. Swanton. 2004. Adaptability of plants invading North American cropland. Agriculture, Ecosystems and Environment 104: 379–398.

Mack, R. N., and M. Erneberg. 2002. The United States naturalized flora: Largely the product of deliberate introductions. Annals of the Missouri Botanical Garden 89: 176–189.

Margosian, M. L., K.A. Garrett, J. M. S. Hutchinson, and K. A. With. 2009. Connectivity of the American agricultural landscape: Assessing the national risk of crop pest and disease spread. BioScience 59: 141–151.

Pimentel, D., ed. 2002. Biological Invasions: Economic and Environmental Costs of Alien Plant, Animal, and Microbe Species. Boca Raton, FL: CRC Press.

Raghu, S., R. C. Anderson, C. C. Daehler, A. S. Davis, R. N. Wiedenmann, D. Simberloff, and R. N. Mack. 2006. Adding biofuels to the invasive species fire? Science 313: 1742.

Rossman, A. Y. 2009. The impact of invasive fungi on agricultural ecosystems in the United States. Biological Invasions 11: 97–107.

Seward, N. W., K. C. Ver Cauteren, G. W. Witmer, and R. M. Engeman. 2004. Feral swine impacts on agriculture and the environment. Sheep and Goat Research Journal 19: 34–40.

Smith, R. G., B. D. Maxwell, F. D. Menalled, and L. J. Rew. 2006. Lessons from agriculture may improve the management of invasive plants in wildland systems. Frontiers in Ecology and the Environment 4: 428–434.

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AGROFORESTRY

SEE FORESTRY AND AGROFORESTRY

ALGAE

JENNIFER E. SMITH

University of California, San Diego

Algae are an exceptionally diverse group of generally autotrophic marine, freshwater, and terrestrial organisms that lack true tissues and organs and are thus not typically considered true plants. They comprise a group of eukaryotic uni- or multicellular organisms that possess nuclei and chloroplasts bound with one or more membranes. While cyanobacteria (blue-green algae) were once lumped into the group algae, they are not eukaryotes and so are not treated as algae here. Small single-celled algae are often described as phytoplankton, while larger multicellular species are described as macrophytes, if growing in freshwater, or seaweeds, if growing in the ocean. In this article invasive introduced algae are treated as any species of marine, freshwater, or terrestrial algae that has been introduced into a region where it does not naturally occur, has become highly successful, and is causing ecological or economic harm.

ALGAL INVASIONS

Algae can take on numerous growth forms and can exist as single cells, colonies, or more complex multicellular forms (e.g., filamentous forms, cylindrical forms, sheets, crusts, etc.). These primary producers are common components of most ecosystems around the world and are responsible for producing more than 70 percent of the world's oxygen. Algae can form blooms in their native environments, where they may grow excessively in response to some biotic or abiotic trigger (e.g., nutrient enrichment, pollution), and they may form blooms associated with being introduced into new environments.

While many species of algae have been introduced around the world to new environments, marine algae appear to be the most invasive. Marine algal invasions have occurred and continue to occur around the world as a result of many vectors, including intentional aquaculture introductions as well as accidental introductions associated with shellfish aquaculture and ship traffic. While few introduced algal species become invasive, those that do have been shown to have large negative impacts on associated species and communities. Control or eradication of algal invaders is extremely costly and has been successful in very few cases.

GLOBAL PATTERNS

The majority of documented cases of invasive introduced algae involve marine seaweeds. Out of some 277 species of marine algae that have been introduced around the world, only 13 can be considered invasive. However, many of these species are invasive in more than one locale, region, or ocean basin. Invasive introduced marine algae include members of the Chlorophyta (3), Phaeophyta (3), and Rhodophyta (7), with the number of invaders being proportional to the size of the taxonomic group. While many phytoplankton species can form massive blooms in their native ranges and cause adverse ecological impacts, very few species have been definitively identified as being invasive, probably because of difficulties in taxonomy and incomplete distributional data. Among freshwater taxa, many flowering plants are known to be invasive, but only a few species of algae, specifically some diatoms, have become successful invaders.

Despite the large number of algal species that are considered to be nonnative introductions, very little is known about most species. In fact, the majority of studies that have examined invasive algae have focused on a few high-profile species. Furthermore, many algal invasions are likely to have occurred prior to scientific study or the emergence of the field of invasion biology. Thus, the results and summaries presented below should be treated with caution, as it is difficult to make generalizations about the effects of invasive introduced algae on invaded communities.

SPECIES OF CONCERN

Among the marine algae or seaweeds, only two species are currently listed on the IUCN Invasive Species Specialist Group's list of the 100 worst invaders in the world (see Appendix); these are the green alga Caulerpa taxifolia and the brown alga Undaria pinnatifida (Figs. 1A and B, respectively). Caulerpa taxifolia, otherwise known as the killer alga for its reputation in the Mediterranean Sea, has been introduced to three oceanic basins: the Mediterranean, Australia, and the west coast of North America. In all cases, it has become highly invasive. Caulerpa is native to tropical waters around the world, but a cold water—tolerant strain was first introduced to the Mediterranean via accidental release from the Monaco Aquarium in the 1980s. This aquarium strain grows nearly ten times larger than Caulerpa in its native habitats and is known for monopolizing soft-bottom and seagrass habitats, where it outcompetes native species and impacts the livelihoods of fishermen. The kelp Undaria pinnatifida is native to Asia and has been introduced to Europe, the Mediterranean, Australia, New Zealand, and the west coast of North America, where it has become highly successful in most cases. This species is cultivated in Japan (where it is known as wakame) for human consumption, and it was intentionally introduced to parts of Europe. Causes of Undaria introductions in other parts of the world remain unknown but are believed to be associated with ship traffic (hull fouling and ballast water). Impacts of Undaria on native communities remain undocumented in many cases, but it has been shown to alter community structure and reduce native species diversity.

FIGURE 1 Photographs of some of the most invasive introduced algae from around the world. (A) Caulerpa taxifolia (the killer alga) dominating habitat in the Mediterranean; (B) the invasive kelp Undaria pinnatifida from Monterey Bay, California; (C) Kappaphycus spp. in Kane‘ohe Bay, Hawai; and (D) the invasive freshwater diatom Didymosphenia geminata in lakes of the northeastern United States. (Photographs courtesy of the author.)

Numerous other species of marine algae have been considered to be invasive based on studies that have explicitly examined the ecological impacts of the invaders on communities in which they have been introduced. These include (1) the red algae Gracilaria salicornia, Dasya sessilis, Acrothamnion preisii, Womersleyella setacea, Kappaphycus alvarezii (Fig. 1C), and Eucheuma denticulatum; (2) the brown algae Fucus evanescens and Sargassum muticum; and (3) the green algae Codium fragile and Caulerpa racemosa.

The freshwater diatom Didymosphenia geminata, otherwise known as Didymo or rock snot, is native to the cool temperate regions of the northern hemisphere (Fig. 1D). However, it was recently found in New Zealand and appears to be spreading out within its native range in North America and Europe; it is now considered to be one of the worst freshwater invasive introduced algal species. Although it is a single-celled alga, it can form large colonies that attach to the bottom of both lakes and streams where it smothers native biota including fish, plants, and invertebrates. It is described as having an unpleasant appearance and may cause adverse effects to the fishing and tourism industry. Didymo is believed to spread to new locations though human activity, primarily as a result of algal cells hitchhiking on footwear or fishing gear.

VECTORS OF INTRODUCTION

Based on a recent review of seaweed invasions around the world, a number of vectors were identified and ranked according to prevalence. Interestingly, the mode of introduction for the majority of introduced seaweeds has been undocumented. Of those introductions where the vectors have been identified, ship traffic (including both ballast water and hull fouling) was the most significant source of algal introductions. Because algae are photosynthetic organisms and require sunlight to grow, ballast introductions are not as likely as hull fouling to transport algal propagules. A number of algal introductions have also occurred as a result of aquaculture. Several seaweed species are cultivated around the world in open water cultures both for human consumption and for production of colloids (agar and carrageenan), which are used as thickening agents in a number of human products such as toothpaste, shaving cream, hair products, lowfat foods, ice cream, and even beer. In most cases, these seaweed introductions have not resulted in severe invasions. However, in the Hawaiian Islands, a number of seaweeds introduced for experimental aquaculture in the 1970s have become invasive on the coral reefs, where they cause large ecological and economic impacts (Fig. 1C; see section below on impacts of seaweed invasions). A number of other invasive introduced algae arrive in new locations indirectly through shellfish aquaculture. Algae can hitchhike on the shells of oysters and other shellfish, and as these species are transported around the world for human consumption, the algae go with them. Algae have also been commonly used as packing material to pad shellfish when they are transported from one location to the next. Other common vectors for the introduction of algae to new locations include fishing gear, SCUBA gear, and clothing, as small algal fragments can become entangled in these items when they move from location to location. Aquarium introductions have also occurred accidentally though discharge pipes or intentionally when people want to free or discard the organisms living in their home aquaria. Lastly, in the past researchers introduced algae to new environments for the purpose of research, but today, intentional introductions are no longer common outside of the aquaculture industry.

IMPACTS OF INVASIVE INTRODUCED ALGAE

Despite the large number of algae (277 species of marine algae and an unknown number of freshwater algae) that are known to have been introduced to new locations around the world either intentionally or accidentally, very little is known about the impacts these species are having since introduction. A recent review of the scientific literature revealed a total of 68 published studies that have explicitly examined the ecological impacts of seaweed invaders on the invaded communities. A variety of response variables have been used to assess impacts, including changes in the abundance and diversity of the native biota and changes in productivity, community structure, community function, and feeding and performance of native species. The majority of these studies reported that the seaweed invaders caused negative impacts or changed community structure in the invaded communities. However, in some cases, seaweed invaders have been shown to increase the abundance, diversity, and feeding rates of native species. It is important to note here that although the majority of studies have documented negative impacts of invaders on the native biota, only a very small number of seaweed invaders have been studied in any detail. Of the 277 species of introduced marine algae, only a small number of these species are truly considered invasive, but those that are invasive have had large negative impacts. Caulerpa taxifolia is the best studied of the invasive seaweeds, and it has been shown to negatively affect performance, feeding, diversity, community function, and abundance of native species. Other species that have been shown to have negative effects on invaded communities in at least ten different cases include Codium fragile ssp. tomentosoides, Sargassum muticum, Caulerpa racemosa, and Euchema denticulatum. In the case of freshwater algal invasions, few studies have quantified impacts, but anecdotal evidence suggests that when the diatom Didymo blooms, it may reduce oxygen levels in water bodies at night while the algae are respiring and cause hypoxia and subsequent harm to native species. Didymo blooms also reduce light levels and may negatively affect other plant or algae species growing nearby. Didymo blooms, along with many other algal blooms, appear unpleasant to tourists and may negatively impact recreational activities.

At least one study has documented the economic costs associated with an invasive introduced alga. The red seaweed Hypnea musciformis was first introduced to the island of Oahu in the Hawaiian Islands in the 1970s for experimental aquaculture. Over the next several decades, this species spread to a number of other islands in the main Hawaiian Islands, and it began forming extensive, large blooms on the island of Maui. The blooms, which are believed to be associated with nitrogen and phosphorus pollution occurring in the nearshore environment, result in large amounts of rotting algal biomass that accumulates on the beaches and creates an unpleasant environment and a very foul odor. In a formal economic analysis, Van Beukering and Caesar (2004) determined that the city and county of Maui were losing an estimated $20 million per year in costs associated with beach cleanups, reduced property values, and reduced occupancy rates in hotels and condominiums in bloomaffected areas. The authors concluded