SCOPE 44 - Introduction of Genetically Modified Organisms into the Environment

11.1 INTRODUCTION

Recent concern over the introduction of genetically engineered organisms (GEOs) into the environment has stimulated biologists to look for analogues of the invasion process and the consequences of species introductions to the open environment. Clearly, the best model of the mechanics of species invasions are actual invasion events. A project of SCOPE (Scientific Committee on Problems of the Environment) has recently summarized the global extent and effect of biological invasions across numerous taxonomic groups (Mooney and Drake, 1986; Kornberg and Williamson, 1986; MacDonald et al., 1986; Groves and Burdon, 1986; Drake et al., 1988). This comprehensive review of species introductions provides the basis for our analysis of the potential risks of introducing GEOs to the environment. Here we review the results of this program and relate them to the issues surrounding such releases.

We note at the outset that information on the consequences of species invasions may not be totally germane to considerations of the release of GEOs. Most species invasions, in the sense of the SCOPE program, are invasions from one biogeographic region to another, e.g. species movements from the Old World to the New World, or from North America to Hawaii. Most GEOs, however, will be introduced into very specific environments, often back into environments similar to that from which the immediate progenitors originated. This of course assumes we can engineer leashes of one kind or another into such organisms so that they do not spread beyond the confines of the target system. Nevertheless, an invasion is an invasion; hence we believe we are in a position to identify and address many critical aspects and consequences of such releases.

Throughout this essay we briefly discuss the nature of ecological systems, the interconnectivity, dynamics, and vulnerability of which have been partly responsible for the considerable concern voiced by many ecologists and environmentalists over the envisioned releases of GEOs. We would be remiss at this point, however, if we did not offer an important and critical distinction between `ecologists' and `environmentalists'. The lack of this distinction by the scientific and political community in general has added confusion and fueled the controversy over the release of GEOs. Environmentalists, by definition, are concerned with various sociopolitical aspects of environmental quality and management. They may or may not be experts in understanding ecological processes and the organization of ecological systems. Ecologists are scientists concerned with the fundamental properties, processes, and components of ecological systems, whether they be individuals, populations, communities, or ecosystems.

The SCOPE program was initiated in 1982 with the objectives of: (1) determining those properties of invading species that contribute to their success as invaders and (2) identifying the characteristics that make certain ecosystems more vulnerable to invasions than others. The focus of the program was on species that invade natural ecosystems rather than species that invade agroecosystems. There has been a considerable effort in studying the former because of the immediate, identifiable economic losses associated with pest invasions. Concern over the issue of invasions into natural ecosystems does not have such a long history. Indeed, the first major synthesis of knowledge concerning such invasions was produced by Charles Elton in 1958.

The SCOPE program was centered around a series of national meetings designed to summarize current knowledge concerning invasions into various continental regions. National programs included Great Britain (Kornberg and Williamson, 1986), Australia (Groves and Burdon, 1986), the United States (Mooney and Drake, 1986), the Netherlands (Joenje et al., 1987), and South Africa (Macdonald et al., 1986). In addition, a survey of invasions into nature reserves (Usher et al., 1988) and an evaluation of the utility of mathematical models of invasion processes (Drake and Williamson, 1986) were conducted. Finally, a global synthesis summarized these regional assessments (Drake et al., 1988).

11.2 PROGRAM RESULTS

The exchange of organisms between various regions of the biosphere is naturally impeded by obvious physical barriers to migration and species dispersal. These barriers include the proximity and relative global position of continental land masses, mountain ranges, bodies of water, and climatic changes. Prior to humans becoming cosmopolitan in distribution, areas geographically separated shared few species in common. Arguably, the greatest source of taxonomic affinity between the continental land masses probably resulted from species distributions before the break-up of Gondwanaland. This is not to say that intercontinental exchanges did not occur, but just that they were relatively rare events dependent on chance long-distance dispersal by some vector such as migrating birds. There is also evidence of the mixing of biota between continents that had been separated by a water barrier and were joined by a land bridge (Stehli and Webb, 1985).

We are now witnessing a phenomena similar to the creation of land bridges, but on a global scale and at a greatly accelerated rate. These new `bridges' are humans, and they connect essentially every land mass on the Earth. Humans have purposefully, as well as accidently, introduced organisms into many new environments. Further, they have altered the environments of large areas of the globe, creating new types of habitats and disturbing others. These modifications have undoubtedly changed how vulnerable or resistant these environments are to invasion. For the most part, vulnerability to invasion has increased as a result of human activity. As a result we are seeing a homogenization of the world's biota. Certain species, which in prehistoric times were limited to small isolated regions of the globe, are now widespread.

11.3 THE NUMBERS OF INVADERS

The SCOPE program summarized a great number of examples of invasion rates of organisms into various regions of the world. In many regions of the New World these rates are very high and do not yet show an asymptote. For example, the rate of successful invasion of new species of insects and arthropods into the United States is about 11 species per year (Sailer, 1983). About five species of higher plants successfully colonize eastern Australia each year (Groves, 1986). Although good data do not yet exist on the proportion of invading species which are successful, these values clearly represent a small fraction of the species that annually reach these areas.

Some ecological systems, such as islands, have been considerably more vulnerable to invasion then continental land masses. The Hawaiian Islands are a case in point. Currently 40% of both the birds and higher plants now found there are invaders, as are virtually all of the mammals (Table 11.1). New Zealand has also been particularly prone to invasion. Well over 50% of the flora of New Zealand is now composed of invaders. Unfortunately, the extinction of native species often accompanies such invasions.

Table 11.1 Total number of species and the percentage of established non-native species of the Hawaiian Islands. (From Vitousek et al.,1987)

11.4 OLD WORLD ECOSYSTEMS

One important contribution of the SCOPE program was an analysis of the numbers of invaders into nature preserves (Usher et al., 1988). It was found that nature preserves on islands, even though they are managed for minimal disturbance, are composed of as many as 30% invading species among the resident plants and 18% vertebrate invaders (Table 11.2).

Invasions into preserves where the climate is more severe, such as arid zones, have proportionately fewer invaders. There is some evidence though that it is not climatic severity per se that serves as a barrier to invasions. Opportunity of introduction plays a critical role. Usher (1988) notes that the numbers of invaders that are found in preserves is related to the numbers of visitors that frequent them. High visitation brings with it a certain amount of disturbance as well as an increased probability of inadvertent introductions of alien organisms. Reserves in climatically challenging environments are evidently less heavily used by humans.

Table 11.2 Mean percentages of introduced invasive species over total species present in nature preserves distributed world-wide in different habitat types. (From Usher, 1988)

11.5 THE TRANSPORT OF INVADING SPECIES

Many invading species could not have been introduced without the help of humans, both intentionally as well as inadvertently. Intentional introductions include organisms that have been introduced to enhance agriculture and horticulture, to provide new forms of animal protein, and to develop recreation. In earlier times, in New World regions, acclimatization societies were formed with the goal of introducing and establishing organisms from the Old World. There are of course still efforts to introduce new plant varieties and game birds and fishes into regions where they have not previously existed. These activities have resulted in literally thousands of species introductions. At the same time there have been organized efforts to stem the flow of inadvertent introductions, principally pests of economically important plants. Plant quarantine activities have stemmed, but have by no means stopped, these inadvertent introductions. Then, too, as noted below, seemingly benign and beneficial plants can become `weedy' and cause considerable economic damage in a new environment.

11.6 THE ORIGINS OF INVADING SPECIES

If one chooses any particular spot on earth and examines the origins of invading species, one finds that the invaders often come from radically different biogeographic realms. However, there can be significant patterns and directions of flow between certain regions. In the New World, for example, most invaders are of European origin. Is this unusually high success of European species due to some particular properties that they possess, perhaps resulting from their long association with the humans and subsequent exposure to disturbance (di Castri, 1988)? Or does this success simply reflect, in large part, opportunity for invasion due to the intensity and directionality of introductions (Simberloff, 1988)? In the New World there has been a constant flow of intentional introductions from the European and Middle Eastern centers of domestication of plants and animals. No doubt in the years ahead the patterns of biotic invasions will further change, due to changing cultural practices and transportation modes and networks, as has occurred in the past (di Castri, 1988).

11.7 THE IMPACT OF INVADERS

The economic and sociopolitical impacts of invading species have been unquestionably enormous. On the plus side one need only consider the major crop plants of the world that represent intentional and generally highly successful introductions. These species have provided the world's population with food, fiber, and fuel. Such crops, however, represent only a fraction of the species that have been intensively selected for desirable economic properties. Often this selection has taken place under monospecific conditions, and in the process such species have generally lost competitive ability and thus are no match, when not cultivated, with wild species. In contrast to the small number of major crop species there are over eight thousand weeds of agriculture, 250 of them being serious agricultural pests (Heywood, 1988). These weeds have had a very large economic impact that has been well documented.

What has not been so well documented is the impact that invaders, either intentionally or accidently introduced, have had on natural ecological systems. The SCOPE program focused on these natural systems and found examples of disruptions of virtually every ecosystem process including acceleration of erosion rates, alteration of biogeochemical cycling, alteration of geomorphological and hydrological processes, alteration of fire regimes, interference with the population dynamics of native species, and changes in community structure (Macdonald et al., 1988). Vitousek (1986) noted that it was invading species, representing new functional roles within a given ecosystem, such as tapping new water sources or fixing nitrogen, that did the most damage. He and others (Vitousek et al., 1987) have provided a recent example of a nitrogen-fixing shrub from the Canary Islands which has invaded the lava flows of Hawaii. This species has completely altered normal soil development and community successional patterns.

11.8 PREDICTING THE SUCCESS OF INVADING SPECIES

In spite of the wealth of information that we now have on the numbers, origins, and impacts of invading species we are still unable to make precise predictions about the success a given species will have in invading a particular system. We can, however, make some important general predictions. The reasons that we lack the kind of precision in predictability that we would like rests both in the complexity of the problem and in the nature of the data that we now have available. In regard to the latter most of the case histories that we have on invasions represent natural historical accounts, which generally do not provide details on quantitative population attributes such as population growth rates, rates of spread, etc. Further, there generally is not specific information available on failure rates of introductions with which to compare to successes, with some notable exceptions, e.g. data sets of Hawaiian birds (Moulton and Pimm, 1986). Finally, and probably most important, this area of study has not yet benefited from an experimental approach.

In addition to the inadequate data available on this problem are the formidable problems associated with making predictions. First, it is important to realize that there are many steps to the success of an invading species, each with numerous and different constraints. There is transport, establishment, reproduction, and, finally, spread. Thus any approach to predicting invasion success must take all the factors limiting steps into consideration. Second, ecological communities do not all behave in the same way; indeed, such systems are exceedingly complex involving processes that occur as quickly as milliseconds to those that occur on evolutionary time scales.

Several approaches have been taken toward developing the ability to predict, at some level, basic invasion processes. The first approach has been essentially correlative and comparative. This approach has sought to predict the potential success of an invading species based on morphological, physiological, ecological, and genetic characteristics which are associated with particularly successful invading species. Examples of lists of traits associated with successful species are those published for plants (Baker, 1974) and vertebrates (Ehrlich, 1988). Currently, this approach has been unable to make specific predictions. Lists of species traits are simply too general to be of value in specific instances. As noted by Ehrlich, other factors must be taken into account. These include the particular physiological and behavioral status of the founding population as well as the unique physical and biological status of the habitat being invaded (Table 11.3). Clearly, a species could be a good invader in one ecological system but a poor invader in another; conditions are rarely equal.

Even invasions by the same species into the same environment may not even result in the same outcome. Dynamical as well as stochastic processes can produce numerous alternative community states. Depending on the state of the system at the time of invasion, quantitative differences in vulnerability and resistance to invasion can occur. Even in the absence of different system states, timing can play a powerful role in invasion processes (Crawley, 1988). Attempt after attempt to establish an organism in a new environment may fail. Then a chance juxtaposition of climatic events, status of the populations of potentially interactive species, and the conditions and numbers of individuals of the invading species may result in a successful establishment. The large numbers of elements that go into a successful invasion make it striking indeed that any species actually becomes an established invader.

Considering the large numbers of crucial variables encompassed in these two realms of species traits and habitat characteristics, plus the potentially large numbers of species that are promising invaders for which we have relatively little detailed biological information, the problem in making precise predictions becomes evident. Although it may be difficult to make a priori predictions about the likelihood of establishment and spread of any particular organism, without detailed knowledge of that organism's biology and the nature of the target habitat, such studies have produced some very useful guidelines.

Table 11.3 Generalized features of populations and of communities important in the establishment of invertebrate invaders. (From Ehrlich, 1988)

A.	Population features
	1.	Number of individuals
	2.	Sex or sex ratio
	3.	Physiological statusmaturity, state in breeding cycle, health, acclimation status
	4.	Genetic compositiongenetic variability in founding population, ecotype of origin
	5.	Behavioral statusexperience of individuals, social relationships within group
B.	Habitat and community features
	1.	Season
	2.	Weather
	3.	Size and structure of populations of resource organisms
	4.	Size and structure of populations of competitors
	5.	Size and structure of populations of predators
	6.	Size and structure of populations of parasites and pathogens

Crawley (1987) has noted that species with large distributional ranges, a high intrinsic population growth rate, and a large founding population are most likely to be successful invaders. Communities with few species present, absence of congeners morphologically similar to potential invaders (Moulton and Pimm, 1986), and a high degree of habitat disturbance (Crawley, 1988) are most likely to be invaded. The greatest impacts of invaders on natural systems will be seen where predators and competitors of the invader are absent in the target community and in communities that have a relatively simple structure (e.g. those with few species). Invading species that are generalists, such as generalist herbivores, are likely to have a greater impact than those with specialized food requirements (Pimm, 1987).

Recent studies on the dynamics of community assembly provide further promise of delimiting those species which are better colonists and those ecological systems which are particularly vulnerable (e.g. Gilpin et al., 1986; Drake 1983, 1988; Sugihara 1985; Post and Pimm, 1983). Using mathematical models, both Sugihara (1983, 1985) and Drake (1983) have shown that as communities become increasingly species rich, successful invaders must become increasingly specialized (diet, habitat use, etc.). Hence, the link between species and community characteristics appears even more critical if we are to develop predictive ability.

A conclusion, then, is that with detailed knowledge of the biology of the potential invader and of the characteristics of the target environment, relatively good predictions can be made of the potential success and impact of an invading species. Obtaining this knowledge for a specific system will doubtless have a price. The costs in manpower in research could be large, but then the costs of a mistake will inevitably be larger.

An important lesson of the utility of prerelease in-depth studies can be learned from the results of biocontrol efforts. Over 180 species of insect herbivores have been utilized in weed control efforts. About two-thirds of these became established and about 50% were effective in control. These introductions have resulted in some species inadvertently becoming established; however, none have themselves become a problem (Moran et al., 1986).

11.9 AN ENVIRONMENTALIST'S VIEWPOINT

It is important to understand why environmentalists have expressed such strong concerns over the potential hazards of the introduction of genetically designed organisms. They are acutely aware of those cases where invasive species, inadvertently introduced, have disrupted natural systems or have caused enormous economic damage to crops. They can also cite many cases where species that have been purposefully introduced to serve some useful function for society have subsequently caused more damage than providing good. These latter cases represent an engineering approach to the environment in a sense that one part of the problem (e.g. economic benefit, enhancement of yield, erosion control, etc.) is considered in detail whereas other impacts or hazards are not considered.

Examples of such an approach in the United States must surely be the purposeful introduction of crabgrass and dandelions, the scourge of gardeners everywhere. One can say, quite correctly, that these particular introductions were made before we had a sophisticated understanding of the potential hazards that might ensue. However, even in relatively recent times, examples can be cited where purposeful introductions have been made with very good intent and expectations. In 1957, for example, the Nile perch was introduced into Lake Victoria. In this case the intent was to increase human food supply. Apparently even this objective was not fully realized, yet considerable ecological damage ensued including the apparent extinction of numerous endemic fish species (Barel et al., 1985). It is no wonder, then, that even the words employed to describe the process of utilizing genetically modified organisms in natural environments'the release of genetically engineered organisms'conjures images to some biologists of yet one more well-intentioned but potentially damaging activity. Many engineering projects in natural environments have had, in past times, at least before the era of environmental impact considerations, rather devastating ecological effects. A combination of an engineering approach and releases of organisms thus brings double fears to environmentalists.

Despite such fears we have learned much since the days when species were intentionally introduced without the slightest consideration of the ultimate consequences. We must ask whether or not our new knowledge is adequate to prevent the catastrophies of history? We must be willing to evaluate the long-term consequences of our activities.

11.10 TODAY'S ENVIRONMENT

At present, there are drastically different configurations of the world's biota than there were even a few hundred years ago. We have seen an homogenization of the world's biota, as well as an enormous loss of species. These changes have accompanied, and have partly resulted from, large-scale modifications of pristine landscapes by human activities including agriculture, animal husbandry, water diversions, construction, and so forth.

As the human population grows there will be increasing impacts on the earth's biota, both directly, through the activities listed above, as well as indirectly, through the effects of increasing global interconnectivity. Of course it would be a mistake to assume that any cost associated with human activities that modify the Earth are unacceptable. It has been suggested that the inadvertent escapes among these intentional introductions represent, in a sense, a tax on the good that has been provided (Wells et al., 1986). The damage that many of the escapes has wrought has been considerable; however, cost versus benefit is an ecological reality.

Do we now have the knowledge to more precisely utilize purposeful introductions without incurring environmental damage or to prevent inadvertent introductions that may also do damage? To a certain extent yes, as noted above, but unfortunately this knowledge is not often fully applied. Clearly, ecologists and molecular biologists must work together in the development, testing, and application of engineered species for use in the open environment.

11.11 SUMMARY

There are certainly lessons from the study of biological invasions that are of value in considering the deliberate introduction of engineered organisms. First, a detailed evaluation of traits of the organism and of the properties of the host environment are required before release. This analysis must be made in an ecological context that considers both the short- and long-term consequences of the introduction since it is clear that once an introduction is successful there will be no easy recall. If the history of introductions serves as a guide, we can predict that although there are great potential benefits to be derived from the considered utilization of biological materials in a given area, no matter what its origins, there will be mistakes due to unforeseen circumstances. As noted in the introduction, such mistakes will be minimal with the controlled introduction of engineered organisms since in most cases this will not involve moving organisms from one ecological setting into an entirely different one. It would appear that the potential benefits of engineeered organisms are enormous, not only in enhancing agricultural productive capacity but also in providing new tools with which to restore properties of natural ecosystems that have been inadvertently damaged through the activities of humans.

REFERENCES

Barel, C.D.N., Dorit, R., Greenwood, P.H., Fryer, G., Hughes, N., Jackson P.B.N., Kawanabe, H., Lowe-McConnell, R.H., Nagoshi, M., Ribbink, A.J., Trewavas, E., Witle, F. and Yamaoka, K. (1985) Destruction of fisheries in Africa's lakes. Nature 315, 19-20.

Crawley, M.J. (1988) Chance and timing in biological invasions. In: Drake, J., diCastri, F., Groves, R., Kruger, F., Mooney, H., Rejmanek, M. and Williamson M. (Eds.) Biological Invasions: A Global Perspective, John Wiley, Chichester.

Drake, J.A, (1983) Invasibility in LotkaVolterra interaction webs. In DeAngelis, D., Post, W.M., and Sugihara, G. (Eds.) Current Trends in Food Web Theory, Oak Ridge National Lab. TM5983, pp. 83-90.

Drake, J.A., diCastri, F., Groves, R., Kruger, F., Mooney, H., Rejmanek, A., and Williamson, M. (Eds.) (1988) Biological Invasions: A Global Perspective, John Wiley, Chichester.

Ehrlich, P.R. (1988) Attributes of invaders and invading processes. In: Drake, J., diCastri, F., Groves, R., Kruger, F., Mooney, H., Rejmanek, A., and Williamson, M. (Eds.) Biological Invasions: A Global Perspective, John Wiley, Chichester. 

Gilpin, M.E., Carpenter, M.P., and Pomerantz, M. (1986) The assembly of a laboratory community: multispecies competition in Drosophila. In Diamond, J. and Case, T.J. (Eds.) Community Ecology, pp. 23-40, Harper and Row, New York.

Groves, R.H. and Burdon, J.J. (Eds.) (1986) Ecology of Biological Invasions, Australian Academy of Science, Canberra.

Joenje, W., Bakker, K. and Vlijm, L. (Eds.) (1987) Proceedings, Series C, Koninklijke Nederlandse Akademie van Wetenschappen, Vol. 90 (1).

Macdonald, I.A.W., Kruger, F.J. and Ferrar, A.A. (1986) The Ecology and Management of Biological Invasions in Southern Africa, Oxford University Press, Cape Town, 324 pp.

Mooney, H.A. and Drake, J.A. (Eds.) (1986) Ecology of Biological Invasions of North America and Hawaii, Ecological Studies 58, Springer Verlag, New York. 

Moran, V.C., Neser, S. and Hoffmann, J.H. (1986) The potential of insect herbivores for the biological control of invasive plants in South Africa. In: Macdonald, I.A.W., Kruger, F.J. and Ferrar, A.A. (Eds.) The Ecology and Management of Biological Invasions in Southern Africa, Oxford University Press, Cape Town, pp. 261-80.

Pimm, S.L. (1987) Determining the effects of introduced species. Trends in Ecology and Evolution 2, 106-8.

Sailer, R.I. (1983) History of insect introductions. In: Exotic Plant Pests and North American Agriculture, Academic Press, New York, pp. 15-38.

Stehli, F.G. and Webb, S.D. (1985) The Great American Biotic Interchange, Plenum Press, New York, 532 pp.

Sugihara, G. (1985) Graph theory, homology, and food webs. Symp. in Appl. Math. 30, 83-101.

Usher, M.B., Kruger, F.J., Macdonald, I.A.W., Loope, L.L. and Brockie, R.E. (1988) The ecology of biological invasions into nature reserves: an introduction. Biological Conservation 44, 1-8.

Vitousek, P.M. (1986) Biological invasions and ecosystem properties: can species make a difference? In: Mooney, H.A. and Drake, J.A. (Eds.) Ecology of Biological Invasions of North America and Hawaii, pp. 163-176. Springer Verlag, New York.

Wells, M.J., Poynton, R.J., Balsinhas, A.A., Musil, K.J., Loffe, H., van Hoegsen, E. and Abbott, S.K. (1986) The history of introductions of invasive alien plants to southern Africa. In: Macdonald, I.A.W., Kruger, F.J. and Ferrar, A.A. (Eds.) The Ecology and Management of Biological Invasions in Southern Africa, Oxford University Press, Cape Town, pp. 21-35.