Biotic Invasions:Causes,Epidemiology. Global Consequences and Control
Published by the Ecological Society of America Number 5, Spring 2000 Biotic Invasions: Causes, Epidemiology Biotic Invasions: Causes, Epidemiology, Global Consequences and Control Global Consequences and Control Global Consequences and Control Issues in Ecology Photo by Richard Mack
Issues In Ecology Number 5 Spring 2000 Biotic Invasions:Causes,Epidemiology. Global Consequences and Control SUMMARY Humans have caused an unprecedented redistribution of the earth's living things.Both incidentally and deliberately,through migration,transport,and commerce,humans are continuing to disperse an ever-increasing array of species across previously insurmountable environmental barriers such as oceans,mountain ranges,rivers,and inhospitable climate zones.Among the most far-reaching consequences of this reshuffling is a sharp increase in biotic invaders-species that establish new ranges in which they proliferate,spread,and persist to the detriment of native species and ecosystems.In a world without borders,few if any areas remain sheltered from these immigrations,and for some areas,such as oceanic islands,are subject to high rates of invasion impac eir new range zed species do b can cause severe environmental damage aint vacant The scientific literature reviewed by the panel makes it clear that: imal invaders can cause xtinctions of vunerable native species throug.and habita Plant invader scan completely alter the fire regime.nutr greatly diminish the a undance or survival ofr Many non-native animals and plants can hybridize with native species In agriculture,the principle pests of temperate crops are non-native.and the combined expenses of pest control and crop losses constitute atax"on food,fiber,and forage production. The global cost of virulent plant and animal diseases caused by organisms transported to new ranges and presented with susceptible new hosts is currently incalculable. Identifying future invaders and taking effective steps to prevent their dispersal and establishment is a major challenge to ecology. agriculture,aquaculture,horticulture and pet trades,conservation,and international commerce.The panel finds that: Identifying general attributes of future invaders has proven difficult. Predicting susceptible locales for future invasions seems even more problematic,given the enormous differences in commerce among various regions and thus in the rate of arrival of potential invaders. Eradication of an established invader is rare and control efforts vary enormously in their efficacy successful control depends more on commitment and continuing dillgence than the efficacy of specific tools themselves(trapping or spraying insecticides releasing biological control agents). Control of biotic invasions is most effective when it employs a long-term,ecosystem-wide strategy rather than a tactical post-entry control Changina national and international auarantine laws by adopting uilty until curront strat egy of den nsongentestheseofnyanetecthevwnhbeaeranrtinawhnesaehsofaarha global consea forestry and fishery resources in some regions and disruption of thec ological processes that supply natural services on which the human enterprise depends.Given their current scale,biotic invasions have also taken their place alongside human-driven atmo spheric and oceanic change as major agents of global change,and left unchecked,will influence these other forces in profound but still unpredictable ways
1 Issues in Ecology Number 5 Spring 2000 Biotic Invasions: Causes, Epidemiology Biotic Invasions: Causes, Epidemiology, Global Consequences and Control Global Consequences and Control Global Consequences and Control SUMMARY Humans have caused an unprecedented redistribution of the earth’s living things. Both incidentally and deliberately, through migration, transport, and commerce, humans are continuing to disperse an ever-increasing array of species across previously insurmountable environmental barriers such as oceans, mountain ranges, rivers, and inhospitable climate zones. Among the most far-reaching consequences of this reshuffling is a sharp increase in biotic invaders — species that establish new ranges in which they proliferate, spread, and persist to the detriment of native species and ecosystems. In a world without borders, few if any areas remain sheltered from these immigrations, and for some areas, such as oceanic islands, are subject to high rates of invasion. Despite ubiquitous arrivals of new plants, animals and microorganisms, the fate of immigrants is decidedly mixed. Few survive and only a small fraction become naturalized. Most that do become naturalized exert no demonstrable impact in their new range. However, some naturalized species do become invasive, and these can cause severe environmental damage. There are several potential reasons why immigrants succeed: Some escape constraints such as predators or parasites, some find vacant niches to occupy, some are aided by human-caused disturbance that disrupts native communities. Whatever the cause, successful invaders can in many cases inflict enormous ecological damage. The scientific literature reviewed by the panel makes it clear that: • Animal invaders can cause extinctions of vulnerable native species through predation, grazing, competition, and habitat alteration. • Plant invaders can completely alter the fire regime, nutrient cycling, hydrology, and energy budgets in a native ecosystem, greatly diminish the abundance or survival of native species, and even block navigation or enhance flooding. • Many non-native animals and plants can hybridize with native species. • In agriculture, the principle pests of temperate crops are non-native, and the combined expenses of pest control and crop losses constitute a “tax” on food, fiber, and forage production. • The global cost of virulent plant and animal diseases caused by organisms transported to new ranges and presented with susceptible new hosts is currently incalculable. Identifying future invaders and taking effective steps to prevent their dispersal and establishment is a major challenge to ecology, agriculture, aquaculture, horticulture and pet trades, conservation, and international commerce. The panel finds that: • Identifying general attributes of future invaders has proven difficult. • Predicting susceptible locales for future invasions seems even more problematic, given the enormous differences in commerce among various regions and thus in the rate of arrival of potential invaders. • Eradication of an established invader is rare and control efforts vary enormously in their efficacy. Successful control depends more on commitment and continuing diligence than the efficacy of specific tools themselves (trapping or spraying insecticides, releasing biological control agents). • Control of biotic invasions is most effective when it employs a long-term, ecosystem-wide strategy rather than a tactical approach focused on battling individual invaders. • Prevention of invasions is much less costly than post-entry control. Changing national and international quarantine laws by adopting a “guilty until proven innocent” approach, instead of the current strategy of denying entry only to species already proven noxious or detrimental, would be a productive first step. The global consequences of failing to address the issue of invasions effectively would be severe, including wholesale loss of agricultural, forestry and fishery resources in some regions and disruption of the ecological processes that supply natural services on which the human enterprise depends. Given their current scale, biotic invasions have also taken their place alongside human-driven atmospheric and oceanic change as major agents of global change, and left unchecked, will influence these other forces in profound but still unpredictable ways
Issues in Ecology Number 5 Spring 2000 Biotic Invasions:Causes,Epidemiology Global Consequences and Control by Richard N.Mack,Chair,Daniel Simberloff.W.Mark Lonsdale Harry Evans,Michael Clout,and Fakhri Bazzaz INTRODUCTION effects of human-caused invasions threaten efforts to conserve biodiversity.maintain productive agricultural Biotic invasions can occur when organisms are sys tems,sustain fun tioning na al o and als transported to new,often distant,ranges where their protect human health.We outline below the epidemiol descendants proliferate.spread,and persist.In a strict ogy of invasions,hypotheses on the causes of invasions sense,invasions are neither novel nor exclusively human- the environmental and economic toll they take,and tools and strategies for reducing this toll. and the number of have grown end THE EPIDEMIOLOGY OF INVASIONS the past 200 vears.Few habitats on earth remain free o Biotic invasions constitute only one outcome species introduced by humans:far fewer can be consid- indeed,the least likely outcome-of a multi-stage pro ered immune from this dispersal.The species involved cess that begins when organisms are transported from represent an array of taxonomic categories and geo their native ranges to new reaions first many if not graphic origins that defy any ready classification most.perish en route to a new locale.if they succeed in The erse con ces of biotic i sions are reaching a new site,immigrants are likely to be destroyed Invaders can alter funda iot agents. mental ecological properties such as the dominant spe cies in a community and an ecosystem's physical features, of species that are actually dispersed from their native nutrient cycling,and plant productivity.The aggregate ranges,the number that subsequently perish,and the num Flgure 1-Some invaders,such as the shrub Lantana camara,have been introduced repeatedly in new ranges,the results of global human colonization and commerce.As the array of estimated years of introduction indicates,lantana was introduced throughout the 19th and early 20 century in new sub-tropical and tropical ra es.In each new range it has become highly destructive,both in agricultural and natural communities(Cronk and Fuller 1995)
Issues in Ecology Number 5 Spring 2000 2 by Richard N. Mack, Chair, Daniel Simberloff, W. Mark Lonsdale, Harry Evans, Michael Clout, and Fakhri Bazzaz Biotic Invasions: Causes, Epidemiology Biotic Invasions: Causes, Epidemiology, Global Consequences and Control Global Consequences and Control Global Consequences and Control INTRODUCTION Biotic invasions can occur when organisms are transported to new, often distant, ranges where their descendants proliferate, spread, and persist. In a strict sense, invasions are neither novel nor exclusively humandriven phenomena. But the geographic scope, frequency, and the number of species involved have grown enormously as a direct consequence of expanding transport and commerce in the past 500 years, and especially in the past 200 years. Few habitats on earth remain free of species introduced by humans; far fewer can be considered immune from this dispersal. The species involved represent an array of taxonomic categories and geographic origins that defy any ready classification. The adverse consequences of biotic invasions are diverse and inter-connected. Invaders can alter fundamental ecological properties such as the dominant species in a community and an ecosystem’s physical features, nutrient cycling, and plant productivity. The aggregate effects of human-caused invasions threaten efforts to conserve biodiversity, maintain productive agricultural systems, sustain functioning natural ecosystems, and also protect human health. We outline below the epidemiology of invasions, hypotheses on the causes of invasions, the environmental and economic toll they take, and tools and strategies for reducing this toll. THE EPIDEMIOLOGY OF INVASIONS Biotic invasions constitute only one outcome - indeed, the least likely outcome - of a multi-stage process that begins when organisms are transported from their native ranges to new regions. First, many, if not most, perish en route to a new locale. If they succeed in reaching a new site, immigrants are likely to be destroyed quickly by a multitude of physical or biotic agents. It is almost impossible to obtain data quantifying the number of species that are actually dispersed from their native ranges, the number that subsequently perish, and the numFigure 1 - Some invaders, such as the shrub Lantana camara, have been introduced repeatedly in new ranges, the results of global human colonization and commerce. As the array of estimated years of introduction indicates, lantana was introduced throughout the 19th and early 20th century in many new sub-tropical and tropical ranges. In each new range it has become highly destructive, both in agricultural and natural communities (Cronk and Fuller 1995)
Issues In Ecology Number 5 Spring 2000 Flgure 2-Many invaders occupy new ranges at an accelerating rate with pro nounced"lag"and"log"phases of pro 80 liferation and spread. This initial s rate of range occupation may be indis tinguishable from the rate of spread 600 displayed by non-invasive(but neverthe less non-indigenous)species in a new 400 range.thus hamperina the early identi fication of future invaders.Terrestrial most co monly illus 200 trate this pattern (.g.the spreado Opuntia aurantiaca in South Africa) (Moran and Zimmerman 1991 and sources [numbers 1-9]therein).By 1900 1930 1960 1990 contrast.invaders in other taxonomio Year groups may show no lag in range ex. pansion and rapidly occupy new range upon entry. ber of arrivals.But aiven the number of species spotted Hemisphere and elsewhere.The manifests from colum bus'second and subsequent voyages,for instance,indi Gib8gfleregardedaspoten commerce has growr sit or soon after arrival,immigrants occasionally survive meteorically since then,providing an opportunity for a to reproduce.Even then,their descendants may survive corresponding growth in biotic invasions.As a result for only a few generations before going extinct locally. these biotic invasions can be viewed as predominantly Again,however,some small fraction of these immigrant post-Columbian events.Put in perspective,the human-driven species do persist and become naturalized.At that point movement of organisms over the past 200 to 500 years their persist ence does not depend on recuring.frequen deliberate and accidental,undou y dwarfs in scope fre re-immigration from the native range.although a greate quency and impact the movement of organisms by natura number and frequency of new arrivals do raise the prob- forces in any 500-year period in the earth's history. ability that a species will establish permanently. The proportion of various types of organisms that Among the naturalized species that persist after have invaded as a result of accidental versus deliberate this extremely severe reductive process,a few will go movement clearly varies among taxonomic groups. to become invaders.An analogy yis often made be parasite all other biotic】 nva ed.Delibera hial int sions becaus emany importan t factors in disease epidem avenstead most commonly involed ology have direct parallels in the study of invasions.Be mentation or mutualists,such as mycorrhizal fung low we explore the epidemiology and underlying mecha- that form symbiotic relationships with the roots of nisms,which allow some species to become invaders. most plants Amona insects.some deliberate introductions have Humans as Dispersal Agents of Potential Invaders have erateertmr and de New Zealand. rity of invasive insects plant,animal,and microbial immigrations worldwide Introductions of marine invertebrates probably mir roughly tracks the rise in human transport and commerce ror insects.A few species have been deliberately in. Beginning around 1500,Europeans transported Old troduced,such as the Pacific oyster imported from World species to their new settlements in the Western Japan to washinaton state.but a arowing number of
3 Issues in Ecology Number 5 Spring 2000 ber of arrivals. But, given the number of species spotted only once far beyond their native range, local extinction of immigrants soon after their arrival must be enormous. Despite such wholesale destruction either in transit or soon after arrival, immigrants occasionally survive to reproduce. Even then, their descendants may survive for only a few generations before going extinct locally. Again, however, some small fraction of these immigrant species do persist and become naturalized. At that point, their persistence does not depend on recurring, frequent re-immigration from the native range, although a greater number and frequency of new arrivals do raise the probability that a species will establish permanently. Among the naturalized species that persist after this extremely severe reductive process, a few will go on to become invaders. An analogy is often made between epidemics caused by parasites and all other biotic invasions because many important factors in disease epidemiology have direct parallels in the study of invasions. Below we explore the epidemiology and underlying mechanisms, which allow some species to become invaders. Humans as Dispersal Agents of Potential Invaders Humans have served as both accidental and deliberate dispersal agents for millennia, and the increase in plant, animal, and microbial immigrations worldwide roughly tracks the rise in human transport and commerce. Beginning around 1500, Europeans transported Old World species to their new settlements in the Western Hemisphere and elsewhere. The manifests from Columbus’ second and subsequent voyages, for instance, indicate deliberate transport of species regarded as potential crops and livestock. Global commerce has grown meteorically since then, providing an opportunity for a corresponding growth in biotic invasions. As a result, these biotic invasions can be viewed as predominantly post-Columbian events. Put in perspective, the human-driven movement of organisms over the past 200 to 500 years, deliberate and accidental, undoubtedly dwarfs in scope, frequency and impact the movement of organisms by natural forces in any 500-year period in the earth’s history. The proportion of various types of organisms that have invaded as a result of accidental versus deliberate movement clearly varies among taxonomic groups. • Few, if any, invasive microorganisms have been deliberately introduced. Deliberate microbial introductions have instead most commonly involved yeasts for fermentation or mutualists, such as mycorrhizal fungi that form symbiotic relationships with the roots of most plants. • Among insects, some deliberate introductions have had adverse consequences, including bumblebees in New Zealand. But the majority of invasive insects have probably been accidentally introduced. • Introductions of marine invertebrates probably mirror insects. A few species have been deliberately introduced, such as the Pacific oyster imported from Japan to Washington state, but a growing number of Figure 2 Figure 2 - Many invaders occupy new ranges at an accelerating rate with pronounced “lag” and “log” phases of proliferation and spread. This initial slow rate of range occupation may be indistinguishable from the rate of spread displayed by non-invasive (but nevertheless non-indigenous) species in a new range, thus hampering the early identification of future invaders. Terrestrial plant invasions most commonly illustrate this pattern (e.g. the spread of Opuntia aurantiaca in South Africa) (Moran and Zimmerman 1991 and sources [numbers 1-9] therein). By contrast, invaders in other taxonomic groups may show no lag in range expansion and rapidly occupy new range upon entry
Issues In Ecology Number 5 Spring 2000 Figure 3-Invaders often alter drastically the ecosystems they occupy,over-turning native species composition,as well as changing the fire frequency.soil chemistry and hydrology.The Florida Everglades have been much altered by the eeffects of invasive plantsn com m across much are composed of small for f by Brazilian pepper has radically transformed these ecosystems into virtual monocultures of the invasive tree with devastating effects on the native biota. invaders such as the zebra mussel have arrived as sels in the Great Lakes may go through only a brief lag accidental contaminants in ship ballast phase,or none at all.On the other hand,many immigrant In contrast,most invasive vertebrates,principally fish species do not become abundant and widespread for de cades,uring which time they may of the ertebrate invaders,how Brazilian ever,have been spread accidentally:rats,brown tree ninet ely noticeabl snakes,sea lampreys. until the early 1960's.They are now established on more Some invasive plants have been accidentally introduced than 280.000 hectares in south Florida.often in dense as contaminants among crop seeds and other cargo. stands that exclude all other vegetation (Fig.3). Many,if not most,plant invaders have been deliberately During the lag phase,it can be difficult to distin introduced includina some of the worst pests:wate guish doomed populations from future invaders.Most ex hyacinth.melaleuca tre rick migrant pop of deliberately introduced spe yet the dynamics of such a population are cies that later become biotic invaders emphasizes that guishable from those of a future invader,which is growing not all pests arrive unheralded and inconspicuously:many slowly but inexorably larger.This similarity in the size and are the product of deliberate but disastrously flawed hu- range frustrates attempts to predict future invaders while man forethouaht(Fia 1) they are few in numbers and presumably controllable. Whether most invasic sendure lag phases,and The Transformation from Immigrant to Inva why they oc main conje ral.Any lag in popu The progression from immigrant to invader ofter lation growth and range expansio n for a pot ntial invade entails a delay or lag phase.followed by a phase of rapid most likely results from several forces and factors oper exponential increase that continues until the species ating singly or in combination: reaches the bounds of its new range and its population The number and arrangement of infestations of immi- arowth rate slackens (Fia.2).This simplified scenario has many variants,of course.First,some invasions such as those by Afric canized bees in the Americas and zebra mus single larger one
Issues in Ecology Number 5 Spring 2000 4 invaders such as the zebra mussel have arrived as accidental contaminants in ship ballast. • In contrast, most invasive vertebrates, principally fish, mammals, and birds, have been deliberately introduced. Some of the worst vertebrate invaders, however, have been spread accidentally: rats, brown tree snakes, sea lampreys. • Some invasive plants have been accidentally introduced as contaminants among crop seeds and other cargo. Many, if not most, plant invaders have been deliberately introduced, including some of the worst pests: water hyacinth, melaleuca trees, and tamarisk or salt cedar. The prominence of deliberately introduced species that later become biotic invaders emphasizes that not all pests arrive unheralded and inconspicuously; many are the product of deliberate but disastrously flawed human forethought (Fig. 1). The Transformation from Immigrant to Invader The progression from immigrant to invader often entails a delay or lag phase, followed by a phase of rapid exponential increase that continues until the species reaches the bounds of its new range and its population growth rate slackens (Fig. 2). This simplified scenario has many variants, of course. First, some invasions such as those by Africanized bees in the Americas and zebra mussels in the Great Lakes may go through only a brief lag phase, or none at all. On the other hand, many immigrant species do not become abundant and widespread for decades, during which time they may remain inconspicuous. Brazilian pepper trees were introduced to Florida in the nineteenth century but did not become widely noticeable until the early 1960’s. They are now established on more than 280,000 hectares in south Florida, often in dense stands that exclude all other vegetation (Fig. 3). During the lag phase, it can be difficult to distinguish doomed populations from future invaders. Most extinctions of immigrant populations occur during the lag phase, yet the dynamics of such a population are often indistinguishable from those of a future invader, which is growing slowly but inexorably larger. This similarity in the size and range frustrates attempts to predict future invaders while they are few in numbers and presumably controllable. Whether most invasions endure lag phases, and why they occur, remain conjectural. Any lag in the population growth and range expansion for a potential invader most likely results from several forces and factors operating singly or in combination: • The number and arrangement of infestations of immigrants. Usually invasions proceed fastest among many small, widely separated infestations compared with a single larger one. Figure 3 igure 3 - Invaders often alter drastically the ecosystems they occupy, over-turning native species composition, as well as changing the fire frequency, soil chemistry and hydrology. The Florida Everglades have been much altered by the collective effects of invasive plants, including Schinus terebinthifolius (Brazilian pepper). A) The potential natural communities across much of the Everglades are composed of small forested hammocks in a matrix of marshes. B) Invasion by Brazilian pepper has radically transformed these ecosystems into virtual monocultures of the invasive tree with devastating effects on the native biota. Photo by Richard Mack. Photo by Richard Mack