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An agenda for invasion biology
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Biological Conservation 78 (1996) 3-9 Copyright © 1996 Elsevier Science Limited Printed in Great Britain. All rights reserved 0006-3207/96/$15.00 +.00
A N A G E N D A FOR I N V A S I O N BIOLOGY Geerat J. Vermeij Department of Geology and Centerfor Population Biology, University of California. Davis, CA 95616, USA
Abstract
Here I advocate a comparative and systematic approach in which invasion (the extension of species ranges to areas not previously occupied by that species) is studied from the perspective of individual species as well as of the regions and biotas that export and receive invaders. In order to go beyond the particulars of invasion, it is important to ask: (1) how invaders differ from noninvaders in the arrival, establishment, and integration phases of invasion; (2) how donor regions or communities that have produced many successful invaders differ from those in which few resident species have been able to extend their ranges; (3) how recipient ecosystems with many successfully established invaders differ from those in which few species have taken hold," and (4) how invasion affects evolution not only of the invader itself, but of species in the recipient community with which the invader interacts. Copyright © 1996 Elsevier Science Limited Keywords: invasion, biotic introduced species, dispersal.
interchange,
extinction,
INTRODUCTION Few biological phenomena match species invasion in grabbing headlines and engaging the attention of the public. Zebra mussels Dreissena polymorpha from Europe interfere with shipping and with electricitygenerating plants around the American Great Lakes, ctenophores from the western Atlantic threaten fisheries in the Black Sea; rabbits Oryctolagus cuniculus from Europe and cactuses from North America destroy the Australian bush; Asian chestnut blight brings the American chestnut to the brink of extinction and forever alters forest structure in the eastern United States; the Floridian predatory snail Euglandina rosea devastates the land-snail fauna of the Society Islands but not the African land snail Achatina fulica, for whose control the introduction was intended; South American fire ants devour native ants and affect the gardening practices of home-owners in the southern United States; and rinderpest introduced with cattle from Asia causes
mass mortality among African ungulates, including the extinction of one species. A European visitor to New Zealand feels at home as he walks through pastures of European grasses and weeds and listens to European blackbirds, finches, and larks singing overhead. Invasions and introductions of species by human agency have had profound economic and cultural consequences. Scientists have responded to such crises largely in a piecemeal fashion. Particular invasions and invaders have been studied in great detail, and a few preliminary attempts at inductive generalization have been made (Elton, 1958; Ehrlich, 1986; Brown, 1989; Pimm, 1989; Lodge, 1993); but on the whole, the particulars of individual cases have obscured broader patterns, and doubts have been raised about the existence of general patterns or about the wisdom of looking for them (Ehrlich, 1986). Invasion biology has had surprisingly little guidance from, or made contributions to, the larger disciplines of ecology, biogeography, and evolutionary biology. Because of the emphasis on human-introduced species, the importance of invasion throughout the history of life has generally not been appreciated, and few researchers have taken advantage of a systematic approach to the subject. Important and illuminating as past efforts have been, I believe the time has come to emphasize a more systematic approach, one in which basic questions about the process, participants, and outcomes of invasion are asked in a broad comparative context. My aim here is to outline an agenda for invasion biology. This may strike many readers as an overly ambitious or even arrogant enterprise, but I believe that a framework of answerable scientific questions will benefit future research as well as the development of policies on the transport and introduction of species. I shall argue that invasion must be probed at each of several spatial and temporal scales, that the stages of invasion from arrival to integration must be recognized as distinct and treated with different questions, and that a comparative and systematic rather than an anecdotal approach is needed in order to achieve objectivity and perspective. D E F I N I T I O N S , SCALES AND S T A G E S
Correspondence to: G. J. Vermeij Tel.: 916 752 2234; Fax: 916 752 0951; e-mail: [email protected]
Because clear thought is contingent on the precise and consistent use of terms, I begin with a few key definitions.
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By invasion I mean the geographical expansion of a species into an area not previously occupied by that species. Invasions may occur as the result of climatic and tectonic changes as well as through introduction by humans. Immigrants are species or populations in an area not occupied by their immediate ancestors. The words emigrant and emigration should probably be avoided, because they imply that the population or species as a whole moved from one place to another. Such emigration can occur in principle, but I do not know of documented cases. Good candidates for emigrants are species whose latitudinal limits shift northward or southward as the climate changes. Usually, however, such geographical shifts do not move entire populations. Only individuals near the limits of range move or die. The word migration should be reserved for temporary movements of individuals or populations. The term biotic interchange refers to the expansion of species' ranges from one biota to another across a present or former barrier. The barrier is crossed by means of dispersal. I choose the word interchange because, at least in principle, dispersal between two biotas can proceed in either direction. Invaders come from a donor biota or region, and enter a recipient one. The species pool or donor biota from which invaders are drawn can be characterized at any of several spatial scales ranging from a local community to an entire biogeographical province. The same applies to the species assemblage or the region that is being invaded. Estimates of the relative importance of invasion (number of invaders divided by the number of species in the donor or recipient assemblage) depends critically on the spatial scale being used. Rocky-shore assemblages of molluscs in New England, for example, contain a very high proportion (about 80°/,,) of Pacific-derived invaders, whereas the cool-temperate northwestern Atlantic molluscan fauna as a whole contains only about 33% such invaders (Vermeij, 1991b). Similar contrasts exist for California grasslands as compared to the California flora as a whole (Baker, 1989). Given the large differences that exist in the extent to which particular habitats or communities in a region have been invaded, most comparisons among donor biotas or among recipient ones should probably be done within carefully specified habitat and geographical limits. Thus, the differences in the ratio of introduced to total number of species observed among countries by Heywood (1989) are done at a scale that may often be too coarse. Even small countries typically contain many different habitats as well as biogeographically distinct subregions, each of which may have a unique invasion history and be differently susceptible to invasion. I suspect that generalizations and patterns will be more discernible if ecologically and biogeographically homogeneous assemblages are compared. In particular, I think it is important to treat agricultural, aquacultural, urban, and other human-altered communities differently and separately from communi-
ties that have been less overtly affected by humans. The process of invasion can be divided somewhat arbitrarily into three successive stages: arrival, establishment, and integration. By arrival I mean the dispersal of individuals to the recipient region. This may occur naturally or with the aid of humans. Establishment implies that the new population can sustain itself through local reproduction and recruitment, which thus augments or replaces dispersal from the donor region as a means for the invading population's persistence. Integration occurs when, as the invading species forges ecological links with other species in the recipient region, evolution occurs, reflecting the changed selective regime in the recipient community. For each of these stages, we can ask how species that succeed differ from those that fail, and how success and failure are influenced by prior circumstances in the recipient biota, the donor biota, and the invading species itself. The study of the arrival phase is the study of opportunity. One approach is to assess the dispersibility and routes of transport of known invaders, but a more informative line of attack is to ask what makes some species in a given donor biota good dispersers while others perform poorly in this respect. In other words, what kind of selectivity exists among potential invaders in a donor biota for the ability to place recruits or propagules in a recipient region? The answer requires that we: (1) identify a donor region (there may be more than one); (2) identify modes and routes of transport; and (3) assess the abilities of species in the donor region to take advantage of these routes and means of transport. For cases of invasion unaided by humans, potential means of transport include ocean currents, winds, hitchhiking on the bodies of other organisms, and active locomotion (walking, swimming, or flying) across barriers that have disappeared or are no longer effective. Human-aided invasion is made possible through the accidental or deliberate transport of crops, game animals, ballast water, soil, agricultural control agents, wool, and living food organisms; and by the construction of floating or permanent islands such as ships, planes, buoys, and oil derricks, which can serve as homes or stepping stones for recruits. The emphasis in the study of the arrival phase must therefore be placed on the attributes of donor biotas and regions, potential dispersers, and the routes, means, and conditions of transport. The second stage of invasion is establishment. By establishment I mean the persistence of an immigrant population by means of local reproduction and recruitment. This may be accompanied by a continued spreading of the population in the recipient region. In practice it may often be difficult to infer whether an invader has become established. Some species may invade so frequently that they appear to maintain local populations when in fact the populations are continually being recharged by dispersers from elsewhere. The study of the establishment phase entails comparisons among arrivals as well as analyses of conditions
An agenda for invasion biology in the recipient communities. We can ask how many of the arriving species actually become established; how successfully established species differ from other arrivals in fecundity, environmental tolerance, competitive ability, vulnerability to predation and disease, and flexibility; and how communities in which a given species becomes established differ from those in which that same species fails to become self-sustaining. Aspects of the recipient biota that are likely to be important include the presence of potential hosts, competitors, predators, and parasites, the climate as compared to that of the donor region, and the biological history of the biota in the region being invaded. Other less commonly considered factors may be equally important. For example, are communities with low primary productivity more likely to resist invasion than are those with high productivity (Brown, 1989)? If low productivity or restricted access to resources implies slow growth rates and limited fecundity, establishment may be difficult to achieve. More important, environments where the rate of production is low may be generally inappropriate for the many invading species whose success hinges on high fecundity and high per-capita growth rates, characteristics that require easy access to plentiful resources. By distinguishing between arrival and establishment, we acknowledge that the factors limiting populations change during the course of an invasion. During the arrival phase, the size of the invading population may depend largely on the supply of recruits, as well as on the effectiveness of species native to the recipient biota to prevent establishment. Local recruitment of the invading populations implies that the incumbent effect, or resistance of the recipient biota to invasion, has broken down. Another important implication of this distinction is that the attributes making species good dispersers may not be the same as those that make species good at establishing a beachhead in the recipient biota. In fact, the species most apt to become established may be effective dispersers as well as defensively, competitively, and reproductively superior species. The final stage of invasion can be described as integration, a process in which the species in the recipient biota and the invader respond to each other ecologically and evolutionarily. Many invaders affect abundances of species in the recipient community more or less profoundly, and in so doing modify the agencies of selection on those species. Moreover, evidence from marine as well as terrestrial invasions implies that invaders quickly establish interactions with new hosts or parasites, which may impose new population controls and selective regimes on the invaders themselves. In the light of these outcomes, conservation biologists must ask whether any of the ecological changes wrought by invaders are reversible, and whether the elimination of invading species necessarily brings the recipient biota back to the conditions prevailing before invasion. It is also important to ask to what extent the establishment and integration of one invader affect
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invasibility by later arrivals (see Drake, 1991). Finally, does integration of invaders result in the local or global extinction of native species? In the remaining sections of this paper, I wish to return to some of these questions in detail and suggest avenues of attack that at the same time set the field of invasion biology in the broader context it deserves. Throughout, my emphasis will be on the comparative and systematic approach, which builds on the detailed piecemeal studies of individual cases of invasion. Which attributes enable species to spread from a donor to a recipient region?
Stated in explicitly comparative terms, how do species that invade differ from those in the donor region that do not? Does the answer depend on the route or means of transport, or is invasiveness predictable from a knowledge of species and populations alone? Past efforts to characterize invasibility have typically concentrated on the attributes of weedy (or opportunistic) species (see e.g. Lewontin, 1965). Such studies usually did not compare weeds with non-weeds, or even weeds with other species whose characteristics appear similar but whose populations have not spread. It may well be that invaders as a group do not differ consistently from other species in the donor biota, but without careful comparative studies we cannot make any pronouncements on the subject. One potentially promising approach derives from historical biogeography. For groups with a good fossil record and whose ancestor-descendant relationships are well understood, it is possible to identify species with contrasting histories. During the last Few million years, some species and higher-level clades have expanded their ranges through dispersal, whereas others have undergone range contractions, often fragmenting into several divergent relict populations. What circumstances and attributes enable some species to expand and other co-occurring species to contract in range? In its broadest form, this question can be rephrased as Follows. What factors prevent populations from spreading beyond their geographical limits? One answer might be that physiological tolerance is evolutionarily conservative. If so, many populations would have ranges whose limits are set by physical circumstances that prevent reproduction or survival. It is striking, For example, that very few tropical marine invertebrate lineages have given rise to species or populations capable of withstanding cold waters at higher latitudes. On the other hand, species may be prevented from extending their range by the presence of competitors, predators, or disease organisms, or the absence of critical host, food, or symbiotic species. The high frequency of host switching by parasites (Thompson, 1994) implies that some of these biological barriers may not be difficult to breach, but the whole subject requires that we move beyond the anecdotal stage in which it currently resides.
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One characteristic that invaders might have in common is flexibility or what some researchers have called plasticity. Individuals in novel situations are able to adjust physiologically or morphologically in an apparently adaptive manner. This idea is attractive, but it has never been rigorously evaluated. An obvious test would involve experiments in which a representative range of invading species and non-invading species from a given donor community is exposed to a common novel environment, such as a new host for parasites, a new set of competitors or predators, or a different climate. Another fruitful avenue is to rank species from a given donor biota according to the frequency of success with which that species has invaded a given set of recipient regions to which it was introduced. Simberloff and Boecklen (1991) pointed out that most bird species that had become successfully established on one Hawaiian island also became established on all the other islands to which they had been introduced. Species that have been introduced but have not become self-sustaining could be compared with those that have a high rate of success. Are there attributes of donor biotas or regions that make the latter good sources for invaders? This question can be phrased in explicitly comparative terms. How do donor regions that export many species differ from those from which few species spread? A promising approach to this question is to take advantage of the fact that, among two or more biotas that are exchanging species, one typically exports many more species than do the others. Traditionally, this asymmetry has been ascribed to differences in the competitive or predational environment in the donor biota. According to this view, species are more apt to spread if they have evolved in a biota in which persistence of populations requires a high degree of specialization to competition, predation, and disease (see e.g. Darwin, 1872). The idea has never been properly evaluated in part because other potential explanations have not been seriously considered. For example, routes may favor movement in one direction over that in the other between two biotas. The predominance of weeds of Mediterranean origin in many of the world's grasslands (Baker, 1989) could be the consequence of exceptional opportunity, in this case related to routes of commerce, rather than of the unusual reproductive, defensive, or competitive vigor of species native to the lands of southern Europe, western Asia, or North Africa. Grassland species from North or South America and Australia might have been less likely to be shipped back to the Mediterranean countries, instead of being less vigorous in transit or in establishing sustainable populations in the presence of Mediterranean natives. Another explanation that should be ruled out before others are considered is the null hypothesis that the asymmetry arises solely because of differences in the
donor biotas' species pools. Invasion from one biota to another may be rare because the first biota has few species to offer as potential invaders. Analyses of biotic interchange generally imply that the null hypothesis does not provide a full explanation for the observed levels of asymmetry (Vermeij, 1991a). Typically, the asymmetry is much more marked than would be expected on the basis of differences in diversity between two biotas that are exchanging species. It is, of course, also possible that asymmetry of invasion reflects differences in the recipient rather than in the donor biotas. This possibility sets the stage for the next question. Are there attributes of recipient biotas or regions that make the latter particularly susceptible to invasion? Again, this question can be posed in comparative terms. How do assemblages rich in immigrants differ from those in which few or no foreign species have become established? The difficulties that arise in comparisons among donor regions apply with equal force in comparisons among recipient ones. There may be few immigrants because barriers to dispersal from elsewhere are so effective that opportunity for invasion has been limited. On the other hand, recipient biotas may be difficult to invade because their component species singly or collectively can resist newcomers competitively. Related to the latter explanation is the hypothesis that recipient biotas become invasible after diversity has been reduced through extinction or overexploitation (Vermeij, 1991a). Quantitative studies of biotic interchange in marine as well as terrestrial communities from the last 20 million years strongly support the hypothesis that prior extinction makes recipient communities highly susceptible to invasion (Vermeij, 1991a). An experimental approach to this problem is potentially fruitful but has, as far as I know, not yet been explored. Replicate recipient communities differing in species composition (number of species, presence of predators, intensity of competition, incidence of parasitism, and presence of potential hosts) could be exposed to a given mix of invading species. Those donor communities that are poor in species or that are missing key incumbents should be most easily and most extensively invaded. How often, and under what circumstances, does invasion resolt in the extinction of native species in the recipient region? The evidence so far points to the conclusion that invaders often cause extinction on oceanic islands and in lakes, but rarely in the sea or on large land masses. Probably much more commonly, invaders restrict the ecological range of native species. Wilson (1961) proposed that, as invaders colonize terrestrial communities adjacent to shores, native species are progressively restricted to forests in the interior, especially in mon-
An agenda for invasion biology tane habitats. Does this pattern hold up under scrutiny, and are there other generalities to be uncovered about the way that native species are ecologically restricted by invading species? Here again, an experimental approach with replicate donor communities would seem to be promising. In this instance, recipient communities would differ in total numbers of individual organisms or in absolute size as well as in composition. Are there rules governing the order of invasion of species and the way in which invaders are ecologically and evolutionarily integrated into recipient communities? Diamond (1975) used a comparative approach to suggest that bird communities in New Guinea and surrounding islands differ in predictable ways according to the number of co-occurring species; and that enrichment and impoverishment (the addition or subtraction of species) occur with relatively precise assembly rules rather than by random addition or loss of species. In a similar vein, studies of bird introductions to Hawaii and Tahiti have suggested that only those species differing sufficiently from species already present are likely to become established (Moulton & Pimm, 1986a, b; Lockwood et al., 1993). The view of community organization encouraged by such studies is that species number and composition are relatively deterministic aspects of communities, and that the success or failure of invaders to establish themselves and to integrate into communities can be predicted a priori if enough is known about the invaders and the recipient biota. This interpretation is enforced by Wilson's (1961) taxoncycle hypothesis, according to which terrestrial invaders arrive in relatively disturbed lowland areas and progressively displace natives to more inland environments. The main arguments for such an interpretation have come from studies of ants and birds. This deterministic view of communities and invasions is by no means universally accepted, even by those who work with birds. Wiens (1989), for example, sees little evidence for deterministic assembly rules, and Simberloff and Boecklen (1991) have offered alternative plausible explanations for the observed pattern of bird invasion in Hawaii. These authors are generally convinced that invasion depends more on the characteristics of individual invaders than on the attributes of recipient communities (see also Simberloff, 1981, 1986). Those who work on invasions in the sea or on terrestrial invasions by plants and low-energy organisms generally see the world as indeterministic. Introduced insects quickly adapted to new hosts, even within periods as short as 10 years (Strong et al., 1977; Singer et al., 1993; Thompson, 1994). Similarly, introduced hosts rapidly acquire new parasites and predators. Large differences in diversity among communities (Vermeij, 1978, 1989, 1991b; Ricklefs & Latham, 1992, 1993; Cornell & Hawkins, 1993) imply that recipient communities of plants, insects, or marine invertebrates are
more forgiving of newcomers than are communities of high-energy birds, mammals, or perhaps ants. Community composition of low-energy organisms may generally be less predictable, less orderly, and less integrated than in high-energy forms. Invasion biology has much to offer ecologists and evolutionary biologists in probing the integrity and orderliness of recipient biotas. For example, we can ask whether invaders tend to usurp the ecological roles of native forms or instead to use resources and fashion ways of life not previously exploited in the recipient community. Brown (1989) believes that most invading warm-blooded animals take ecological roles not occupied by native species; but on islands, in lakes, and among land plants, such unique roles of invaders may be less common. What role does invasion play in long-term evolution? Invasion implies change. Not only is it often triggered by change - - the elimination of a barrier to dispersal, the establishment of means by which dispersal can occur, for example - - but in modifications in the recipient biota. Invasions provide opportunities and challenges. The invaders as well as the native species in the recipient communities affected by invaders must cope with and respond to the changing selective regime, or suffer the consequences of restriction and even extinction. In the absence of invasions, communities and the species and interactions comprising them may stagnate, especially if the economic base of energy and nutrients remains fixed. In other words, adaptation and accommodation by organisms to each other may quickly reach a stalemate in the absence of immigration or an economic stimulus (Vermeij, 1987, 1995). If invasions occur on a small scale as the result of minor shifts in the spatial limits of species, the resulting evolutionary realignments may be modest; but if newcomers arrive from far away as the result of large-scale alterations in geography or climate, the change in selective regime and the evolutionary responses to this change could be dramatic. These possibilities remain highly speculative at present, but they point to the potentially crucial role that invasions and invaders have played in stimulating evolution. Given the large number of species now being transported by humans, this aspect of invasion biology cannot be ignored.
EXPERIMENTS, HISTORICAL RECONSTRUCTION AND MODELING It should be clear that invasion biology will profit from a diversity of methodological approaches, and that no single style of inquiry should be seen as superior to all others. Experiments have the virtue of enabling the investigator to vary aspects of species or communities in a systematic manner, but they have the disadvantage of typically being run on small spatial and temporal scales. Moreover, there is a deep-seated tendency
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among experimentalists to view potential outcomes as mutually exclusive alternatives rather than as potentially complementary. I think most biological systems are sufficiently complex that single explanations or hypotheses will rarely suffice to account for the patterns we see. Experiments should be used not to exclude explanations, but to rank them or to explore their interdependence. It has been fashionable in ecology to regard field experiments as inherently superior to experiments carried out in the laboratory. Although field experiments clearly have their place, I believe that experiments with replicated microcosms are more informative as well as ethically more acceptable, especially in studies of invasion. Invaders can have unforeseen and often destructive effects on recipient communities. The field of invasion biology should therefore adopt the standard that work with non-native species or populations be carried out under strictly controlled laboratory conditions from which accidental release of individuals, including gametes and dispersal stages, is impossible. Experiments become impracticable at larger temporal and spatial scales. In such situations, the reconstructive techniques familiar to historians, including paleobiologists, provide the only empirical means of studying invasions. This comparative approach incorporates observations of species and communities before and after invasion, as well as the identification of invading species by means of cladistic methods in which geographical shifts in range can be traced back through time. Armed with such knowledge, we can contrast recipient communities rich in invaders with those that have received few immigrants, or compare donor biotas that have exported many species with those that have provided few invaders. For such longterm studies, groups and community types with a good fossil record clearly show the greatest promise. Although my emphasis throughout this essay has been empirical, there is much room for theoretical analyses as well. Almost all the questions I have posed can serve as guides for models that incorporate principles of population diffusion, population dynamics, community stability, probabilities of extinction, habitat size, per-capita energetics, and the like. Models, however, are a means to an end, not an end in themselves. If the science of invasion biology is to have an impact on policies, it must have at its command empirical data rather than suppositions and extrapolations. The aim of invasion biology should be to seek generalizations and principles, but we must be prepared to accept and to explain a diversity of responses and consequences. For example, whereas invasion by large endothermic mammals may result in extinctions in a recipient biota, plants and smaller animals may not have this consequence. Prior impoverishment or exploitation may provide better opportunities for subsequent invasion in many marine and terrestrial communities, but may have little effect in some lakes such
as the African rift lakes. Many of our conceptions of invasion have been based on species introductions to oceanic islands. There is currently very little understanding of long-term plant invasions, and we have scarcely begun to compare taxonomic groups or community types for their ability to invade, susceptibility to invasion, and propensity to export invaders. From these considerations, it should be obvious that we must continue to document individual cases of invasion. Because invasion biology, like extinction biology, exists in order to study a phenomenon that is justifiably perceived to be important in the human-dominated biosphere, there is a tendency to view the field as somewhat divorced from the larger enterprises of ecology and evolutionary biology. The creation of conservation biology as a discipline and as a field in which students can take advanced degrees is contributing to this isolation. I believe that the phenomenon of invasion is of fundamental importance, and that its study will contribute to an overall understanding of how species interact with each other. As I see it, the success of invasion biology will depend on our insistence that it be incorporated as an integral part of the larger science of biology. |n the long run, our understanding of invasion will be greatly enriched by broad principles, and it will in turn contribute to the further development of these ideas.
REFERENCES Baker, H. G. (1989). Sources of the naturalized grasses and herbs in California grasslands. In Grassland structure and function: California annual grassland, ed. L. F. Huenneke & H. A. Mooney. Kluwer, Dordrecht, pp. 28-38. Brown, J. H. (1989). Patterns, modes and extent of invasions by vertebrates. In Biological invasions." a global perspective, ed. J. A. Drake, H. A. Mooney, F. di Castri, R. H. Groves, F. J. Kruger, M. Rejm~mek & M. Williamson. Wiley, Chichester, pp. 85-109. Cornell, H. V. & Hawkins, B. A. (1993). Accumulation of native parasitoid species on introduced herbivores: a comparison of hosts as natives and hosts as invaders. Amer. Nat., 141, 847-65. Darwin, C. (1872). The origin of species by natural selection or the preservation of favored races in the struggle for life, 6th edn. Colliers, New York. Diamond, J. M. (1975). Assembly of species communities. In Ecology and evolution of communities, ed. M. L. Cody & J. M. Diamond. Belknap Press of Harvard University, Cambridge, MA, pp. 342-444. Drake, J. A. (1991). Community-assembly mechanics and the structure of an experimental species ensemble. Amer. Nat., 137, 1-26. Ehrlich, P. R. (1986). Which animal will invade? In Ecology of biological invasions of North America and Hawaii, ed. H. A. Mooney & J. A. Drake. Springer, New York, pp. 79-95. Elton, C. S. (1958). The ecology of invasions by animals and plants. Methuen, London. Heywood, V. H. (1989). Patterns, extents and modes of invasions by terrestrial plants. In Biological invasions: a global perspective, ed. J. A. Drake, H. A. Mooney, F. di Castri, R. H. Groves, F. J. Kruger, M. Rejm~nek & M. Williamson. Wiley, Chichester, pp. 31-55.
An agenda for invasion biology Lewontin, R. C. (1965). Selection for colonizing ability. In The genetics of colonizing species, ed. H. G. Baker & L. G. Stebbins. Academic Press, New York, pp. 77-91. Lockwood, J. L., Moulton, M. P. & Anderson, S. K. (1993). Morphological assortment of the assembly of communities of introduced passeriforms on oceanic islands: Tahiti versus Oahu. Amer. Nat., 141, 398-408. Lodge, D. M. (1993). Biological invasions: lessons from ecology. Trends Ecol. Evolut., 8, 133-7. Moulton, M. L. & Pimm, S. L. (1986a). The extent of competition in shaping an introduced avifauna. In Community ecology, ed. J. M. Diamond & T. J. Case. Harper and Row, New York, pp. 80-97. Moulton, M. L. & Pimm, S. L. (1986b). Species introductions to Hawaii. In Ecology of biological invasions of North America and Hawaii, ed. H. A. Mooney & J. A. Drake. Springer, New York, pp. 231-49. Pimm, S. L. (1989). Theories of predicting success and impact of introduced species. In Biological invasions. a global perspective, ed. J. A. Drake, H. A. Mooney, F. di Castri, R. H. Groves, F. J. Kruger, M. Rejm~inek & M. Williamson. Wiley, Chichester, pp. 351-67. Ricklefs, R. E. & Latham, R. E. (1992). Intercontinental correlation of geographical ranges suggests stasis in ecological traits of relict genera of temperate perennial herbs. Amer. Nat., 139, 1305-21. Ricklefs, R. E. & Latham, R. E. (1993). Global patterns of diversity in mangrove floras. In Species diversity in ecological communities: historical and geographical perspectives, ed. R. E. Ricklefs & D. Schluter. University of Chicago Press, Chicago, IL, pp. 215-29. Simberloff, D. E. (1981). Community effects of introduced species. In Biotic crises in ecological and evolutionary time, ed. M. H. Nitecki. Academic Press, New York, pp. 53-81.
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Simberloff, D. E. (1986). Introduced insects: a biogeographic and systematic perspective. In Ecology of biological invasions of North America and Hawaii, ed. H. A. Mooney & J. A. Drake. Springer, New York, pp. 3-26. Simberloff, D. & Boecklen, W. (1991). Patterns of extinction in the introduced Hawaiian avifauna: a reexamination of the role of competition. Amer. Nat., 138, 300-27. Singer, M. C., Thomas, C. D. & Parmesan, C. (1993). Rapid human-induced evolution of insect-host associations. Nature, Lond., 366, 681-3. Strong, D. R. Jr, McCoy, E. D. & Ray, J. R. (1977). Time and the number of herbivore species: the pests of sugar cane. Ecology 58, 167-75. Thompson, J. N. (1994). The coevolutionary process. University of Chicago Press, Chicago, IL. Vermeij, G. J. (1978). Biogeography and adaptation." patterns of marine life. Harvard University Press, Cambridge, MA. Vermeij, G. J. (1987). Evolution and escalation: an ecological history of life. Princeton University Press, Princeton, NJ. Vermeij, G. J. (1989). lnteroceanic differences in adaptation: effects of history and productivity. Mar. Ecol. Progr. Ser., 57, 293-305. Vermeij, G. J. (1991a). When biotas meet: understanding biotic interchange. Science, N. Y., 253, 1099-1104. Vermeij, G. J. (1991b). Anatomy of an invasion: the transArctic interchange. Paleobiology, 17, 281-307. Vermeij, G. J. (1995). Economics, volcanoes, and Phanerozoic revolutions. Paleobiology, 21, 125-52. Wiens, J. A. (1989). The ecology of bird communities, Vol. 1. Foundations and patterns. Cambridge University Press, Cambridge. Wilson, E. O. (1961). The nature of the taxon cycle in the Melanesian ant fauna. Amer. Nat., 95, 179-93.
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Biological Conservation 78 (1996) 3-9 Copyright © 1996 Elsevier Science Limited Printed in Great Britain. All rights reserved 0006-3207/96/$15.00 +.00
A N A G E N D A FOR I N V A S I O N BIOLOGY Geerat J. Vermeij Department of Geology and Centerfor Population Biology, University of California. Davis, CA 95616, USA
Abstract
Here I advocate a comparative and systematic approach in which invasion (the extension of species ranges to areas not previously occupied by that species) is studied from the perspective of individual species as well as of the regions and biotas that export and receive invaders. In order to go beyond the particulars of invasion, it is important to ask: (1) how invaders differ from noninvaders in the arrival, establishment, and integration phases of invasion; (2) how donor regions or communities that have produced many successful invaders differ from those in which few resident species have been able to extend their ranges; (3) how recipient ecosystems with many successfully established invaders differ from those in which few species have taken hold," and (4) how invasion affects evolution not only of the invader itself, but of species in the recipient community with which the invader interacts. Copyright © 1996 Elsevier Science Limited Keywords: invasion, biotic introduced species, dispersal.
interchange,
extinction,
INTRODUCTION Few biological phenomena match species invasion in grabbing headlines and engaging the attention of the public. Zebra mussels Dreissena polymorpha from Europe interfere with shipping and with electricitygenerating plants around the American Great Lakes, ctenophores from the western Atlantic threaten fisheries in the Black Sea; rabbits Oryctolagus cuniculus from Europe and cactuses from North America destroy the Australian bush; Asian chestnut blight brings the American chestnut to the brink of extinction and forever alters forest structure in the eastern United States; the Floridian predatory snail Euglandina rosea devastates the land-snail fauna of the Society Islands but not the African land snail Achatina fulica, for whose control the introduction was intended; South American fire ants devour native ants and affect the gardening practices of home-owners in the southern United States; and rinderpest introduced with cattle from Asia causes
mass mortality among African ungulates, including the extinction of one species. A European visitor to New Zealand feels at home as he walks through pastures of European grasses and weeds and listens to European blackbirds, finches, and larks singing overhead. Invasions and introductions of species by human agency have had profound economic and cultural consequences. Scientists have responded to such crises largely in a piecemeal fashion. Particular invasions and invaders have been studied in great detail, and a few preliminary attempts at inductive generalization have been made (Elton, 1958; Ehrlich, 1986; Brown, 1989; Pimm, 1989; Lodge, 1993); but on the whole, the particulars of individual cases have obscured broader patterns, and doubts have been raised about the existence of general patterns or about the wisdom of looking for them (Ehrlich, 1986). Invasion biology has had surprisingly little guidance from, or made contributions to, the larger disciplines of ecology, biogeography, and evolutionary biology. Because of the emphasis on human-introduced species, the importance of invasion throughout the history of life has generally not been appreciated, and few researchers have taken advantage of a systematic approach to the subject. Important and illuminating as past efforts have been, I believe the time has come to emphasize a more systematic approach, one in which basic questions about the process, participants, and outcomes of invasion are asked in a broad comparative context. My aim here is to outline an agenda for invasion biology. This may strike many readers as an overly ambitious or even arrogant enterprise, but I believe that a framework of answerable scientific questions will benefit future research as well as the development of policies on the transport and introduction of species. I shall argue that invasion must be probed at each of several spatial and temporal scales, that the stages of invasion from arrival to integration must be recognized as distinct and treated with different questions, and that a comparative and systematic rather than an anecdotal approach is needed in order to achieve objectivity and perspective. D E F I N I T I O N S , SCALES AND S T A G E S
Correspondence to: G. J. Vermeij Tel.: 916 752 2234; Fax: 916 752 0951; e-mail: [email protected]
Because clear thought is contingent on the precise and consistent use of terms, I begin with a few key definitions.
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By invasion I mean the geographical expansion of a species into an area not previously occupied by that species. Invasions may occur as the result of climatic and tectonic changes as well as through introduction by humans. Immigrants are species or populations in an area not occupied by their immediate ancestors. The words emigrant and emigration should probably be avoided, because they imply that the population or species as a whole moved from one place to another. Such emigration can occur in principle, but I do not know of documented cases. Good candidates for emigrants are species whose latitudinal limits shift northward or southward as the climate changes. Usually, however, such geographical shifts do not move entire populations. Only individuals near the limits of range move or die. The word migration should be reserved for temporary movements of individuals or populations. The term biotic interchange refers to the expansion of species' ranges from one biota to another across a present or former barrier. The barrier is crossed by means of dispersal. I choose the word interchange because, at least in principle, dispersal between two biotas can proceed in either direction. Invaders come from a donor biota or region, and enter a recipient one. The species pool or donor biota from which invaders are drawn can be characterized at any of several spatial scales ranging from a local community to an entire biogeographical province. The same applies to the species assemblage or the region that is being invaded. Estimates of the relative importance of invasion (number of invaders divided by the number of species in the donor or recipient assemblage) depends critically on the spatial scale being used. Rocky-shore assemblages of molluscs in New England, for example, contain a very high proportion (about 80°/,,) of Pacific-derived invaders, whereas the cool-temperate northwestern Atlantic molluscan fauna as a whole contains only about 33% such invaders (Vermeij, 1991b). Similar contrasts exist for California grasslands as compared to the California flora as a whole (Baker, 1989). Given the large differences that exist in the extent to which particular habitats or communities in a region have been invaded, most comparisons among donor biotas or among recipient ones should probably be done within carefully specified habitat and geographical limits. Thus, the differences in the ratio of introduced to total number of species observed among countries by Heywood (1989) are done at a scale that may often be too coarse. Even small countries typically contain many different habitats as well as biogeographically distinct subregions, each of which may have a unique invasion history and be differently susceptible to invasion. I suspect that generalizations and patterns will be more discernible if ecologically and biogeographically homogeneous assemblages are compared. In particular, I think it is important to treat agricultural, aquacultural, urban, and other human-altered communities differently and separately from communi-
ties that have been less overtly affected by humans. The process of invasion can be divided somewhat arbitrarily into three successive stages: arrival, establishment, and integration. By arrival I mean the dispersal of individuals to the recipient region. This may occur naturally or with the aid of humans. Establishment implies that the new population can sustain itself through local reproduction and recruitment, which thus augments or replaces dispersal from the donor region as a means for the invading population's persistence. Integration occurs when, as the invading species forges ecological links with other species in the recipient region, evolution occurs, reflecting the changed selective regime in the recipient community. For each of these stages, we can ask how species that succeed differ from those that fail, and how success and failure are influenced by prior circumstances in the recipient biota, the donor biota, and the invading species itself. The study of the arrival phase is the study of opportunity. One approach is to assess the dispersibility and routes of transport of known invaders, but a more informative line of attack is to ask what makes some species in a given donor biota good dispersers while others perform poorly in this respect. In other words, what kind of selectivity exists among potential invaders in a donor biota for the ability to place recruits or propagules in a recipient region? The answer requires that we: (1) identify a donor region (there may be more than one); (2) identify modes and routes of transport; and (3) assess the abilities of species in the donor region to take advantage of these routes and means of transport. For cases of invasion unaided by humans, potential means of transport include ocean currents, winds, hitchhiking on the bodies of other organisms, and active locomotion (walking, swimming, or flying) across barriers that have disappeared or are no longer effective. Human-aided invasion is made possible through the accidental or deliberate transport of crops, game animals, ballast water, soil, agricultural control agents, wool, and living food organisms; and by the construction of floating or permanent islands such as ships, planes, buoys, and oil derricks, which can serve as homes or stepping stones for recruits. The emphasis in the study of the arrival phase must therefore be placed on the attributes of donor biotas and regions, potential dispersers, and the routes, means, and conditions of transport. The second stage of invasion is establishment. By establishment I mean the persistence of an immigrant population by means of local reproduction and recruitment. This may be accompanied by a continued spreading of the population in the recipient region. In practice it may often be difficult to infer whether an invader has become established. Some species may invade so frequently that they appear to maintain local populations when in fact the populations are continually being recharged by dispersers from elsewhere. The study of the establishment phase entails comparisons among arrivals as well as analyses of conditions
An agenda for invasion biology in the recipient communities. We can ask how many of the arriving species actually become established; how successfully established species differ from other arrivals in fecundity, environmental tolerance, competitive ability, vulnerability to predation and disease, and flexibility; and how communities in which a given species becomes established differ from those in which that same species fails to become self-sustaining. Aspects of the recipient biota that are likely to be important include the presence of potential hosts, competitors, predators, and parasites, the climate as compared to that of the donor region, and the biological history of the biota in the region being invaded. Other less commonly considered factors may be equally important. For example, are communities with low primary productivity more likely to resist invasion than are those with high productivity (Brown, 1989)? If low productivity or restricted access to resources implies slow growth rates and limited fecundity, establishment may be difficult to achieve. More important, environments where the rate of production is low may be generally inappropriate for the many invading species whose success hinges on high fecundity and high per-capita growth rates, characteristics that require easy access to plentiful resources. By distinguishing between arrival and establishment, we acknowledge that the factors limiting populations change during the course of an invasion. During the arrival phase, the size of the invading population may depend largely on the supply of recruits, as well as on the effectiveness of species native to the recipient biota to prevent establishment. Local recruitment of the invading populations implies that the incumbent effect, or resistance of the recipient biota to invasion, has broken down. Another important implication of this distinction is that the attributes making species good dispersers may not be the same as those that make species good at establishing a beachhead in the recipient biota. In fact, the species most apt to become established may be effective dispersers as well as defensively, competitively, and reproductively superior species. The final stage of invasion can be described as integration, a process in which the species in the recipient biota and the invader respond to each other ecologically and evolutionarily. Many invaders affect abundances of species in the recipient community more or less profoundly, and in so doing modify the agencies of selection on those species. Moreover, evidence from marine as well as terrestrial invasions implies that invaders quickly establish interactions with new hosts or parasites, which may impose new population controls and selective regimes on the invaders themselves. In the light of these outcomes, conservation biologists must ask whether any of the ecological changes wrought by invaders are reversible, and whether the elimination of invading species necessarily brings the recipient biota back to the conditions prevailing before invasion. It is also important to ask to what extent the establishment and integration of one invader affect
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invasibility by later arrivals (see Drake, 1991). Finally, does integration of invaders result in the local or global extinction of native species? In the remaining sections of this paper, I wish to return to some of these questions in detail and suggest avenues of attack that at the same time set the field of invasion biology in the broader context it deserves. Throughout, my emphasis will be on the comparative and systematic approach, which builds on the detailed piecemeal studies of individual cases of invasion. Which attributes enable species to spread from a donor to a recipient region?
Stated in explicitly comparative terms, how do species that invade differ from those in the donor region that do not? Does the answer depend on the route or means of transport, or is invasiveness predictable from a knowledge of species and populations alone? Past efforts to characterize invasibility have typically concentrated on the attributes of weedy (or opportunistic) species (see e.g. Lewontin, 1965). Such studies usually did not compare weeds with non-weeds, or even weeds with other species whose characteristics appear similar but whose populations have not spread. It may well be that invaders as a group do not differ consistently from other species in the donor biota, but without careful comparative studies we cannot make any pronouncements on the subject. One potentially promising approach derives from historical biogeography. For groups with a good fossil record and whose ancestor-descendant relationships are well understood, it is possible to identify species with contrasting histories. During the last Few million years, some species and higher-level clades have expanded their ranges through dispersal, whereas others have undergone range contractions, often fragmenting into several divergent relict populations. What circumstances and attributes enable some species to expand and other co-occurring species to contract in range? In its broadest form, this question can be rephrased as Follows. What factors prevent populations from spreading beyond their geographical limits? One answer might be that physiological tolerance is evolutionarily conservative. If so, many populations would have ranges whose limits are set by physical circumstances that prevent reproduction or survival. It is striking, For example, that very few tropical marine invertebrate lineages have given rise to species or populations capable of withstanding cold waters at higher latitudes. On the other hand, species may be prevented from extending their range by the presence of competitors, predators, or disease organisms, or the absence of critical host, food, or symbiotic species. The high frequency of host switching by parasites (Thompson, 1994) implies that some of these biological barriers may not be difficult to breach, but the whole subject requires that we move beyond the anecdotal stage in which it currently resides.
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One characteristic that invaders might have in common is flexibility or what some researchers have called plasticity. Individuals in novel situations are able to adjust physiologically or morphologically in an apparently adaptive manner. This idea is attractive, but it has never been rigorously evaluated. An obvious test would involve experiments in which a representative range of invading species and non-invading species from a given donor community is exposed to a common novel environment, such as a new host for parasites, a new set of competitors or predators, or a different climate. Another fruitful avenue is to rank species from a given donor biota according to the frequency of success with which that species has invaded a given set of recipient regions to which it was introduced. Simberloff and Boecklen (1991) pointed out that most bird species that had become successfully established on one Hawaiian island also became established on all the other islands to which they had been introduced. Species that have been introduced but have not become self-sustaining could be compared with those that have a high rate of success. Are there attributes of donor biotas or regions that make the latter good sources for invaders? This question can be phrased in explicitly comparative terms. How do donor regions that export many species differ from those from which few species spread? A promising approach to this question is to take advantage of the fact that, among two or more biotas that are exchanging species, one typically exports many more species than do the others. Traditionally, this asymmetry has been ascribed to differences in the competitive or predational environment in the donor biota. According to this view, species are more apt to spread if they have evolved in a biota in which persistence of populations requires a high degree of specialization to competition, predation, and disease (see e.g. Darwin, 1872). The idea has never been properly evaluated in part because other potential explanations have not been seriously considered. For example, routes may favor movement in one direction over that in the other between two biotas. The predominance of weeds of Mediterranean origin in many of the world's grasslands (Baker, 1989) could be the consequence of exceptional opportunity, in this case related to routes of commerce, rather than of the unusual reproductive, defensive, or competitive vigor of species native to the lands of southern Europe, western Asia, or North Africa. Grassland species from North or South America and Australia might have been less likely to be shipped back to the Mediterranean countries, instead of being less vigorous in transit or in establishing sustainable populations in the presence of Mediterranean natives. Another explanation that should be ruled out before others are considered is the null hypothesis that the asymmetry arises solely because of differences in the
donor biotas' species pools. Invasion from one biota to another may be rare because the first biota has few species to offer as potential invaders. Analyses of biotic interchange generally imply that the null hypothesis does not provide a full explanation for the observed levels of asymmetry (Vermeij, 1991a). Typically, the asymmetry is much more marked than would be expected on the basis of differences in diversity between two biotas that are exchanging species. It is, of course, also possible that asymmetry of invasion reflects differences in the recipient rather than in the donor biotas. This possibility sets the stage for the next question. Are there attributes of recipient biotas or regions that make the latter particularly susceptible to invasion? Again, this question can be posed in comparative terms. How do assemblages rich in immigrants differ from those in which few or no foreign species have become established? The difficulties that arise in comparisons among donor regions apply with equal force in comparisons among recipient ones. There may be few immigrants because barriers to dispersal from elsewhere are so effective that opportunity for invasion has been limited. On the other hand, recipient biotas may be difficult to invade because their component species singly or collectively can resist newcomers competitively. Related to the latter explanation is the hypothesis that recipient biotas become invasible after diversity has been reduced through extinction or overexploitation (Vermeij, 1991a). Quantitative studies of biotic interchange in marine as well as terrestrial communities from the last 20 million years strongly support the hypothesis that prior extinction makes recipient communities highly susceptible to invasion (Vermeij, 1991a). An experimental approach to this problem is potentially fruitful but has, as far as I know, not yet been explored. Replicate recipient communities differing in species composition (number of species, presence of predators, intensity of competition, incidence of parasitism, and presence of potential hosts) could be exposed to a given mix of invading species. Those donor communities that are poor in species or that are missing key incumbents should be most easily and most extensively invaded. How often, and under what circumstances, does invasion resolt in the extinction of native species in the recipient region? The evidence so far points to the conclusion that invaders often cause extinction on oceanic islands and in lakes, but rarely in the sea or on large land masses. Probably much more commonly, invaders restrict the ecological range of native species. Wilson (1961) proposed that, as invaders colonize terrestrial communities adjacent to shores, native species are progressively restricted to forests in the interior, especially in mon-
An agenda for invasion biology tane habitats. Does this pattern hold up under scrutiny, and are there other generalities to be uncovered about the way that native species are ecologically restricted by invading species? Here again, an experimental approach with replicate donor communities would seem to be promising. In this instance, recipient communities would differ in total numbers of individual organisms or in absolute size as well as in composition. Are there rules governing the order of invasion of species and the way in which invaders are ecologically and evolutionarily integrated into recipient communities? Diamond (1975) used a comparative approach to suggest that bird communities in New Guinea and surrounding islands differ in predictable ways according to the number of co-occurring species; and that enrichment and impoverishment (the addition or subtraction of species) occur with relatively precise assembly rules rather than by random addition or loss of species. In a similar vein, studies of bird introductions to Hawaii and Tahiti have suggested that only those species differing sufficiently from species already present are likely to become established (Moulton & Pimm, 1986a, b; Lockwood et al., 1993). The view of community organization encouraged by such studies is that species number and composition are relatively deterministic aspects of communities, and that the success or failure of invaders to establish themselves and to integrate into communities can be predicted a priori if enough is known about the invaders and the recipient biota. This interpretation is enforced by Wilson's (1961) taxoncycle hypothesis, according to which terrestrial invaders arrive in relatively disturbed lowland areas and progressively displace natives to more inland environments. The main arguments for such an interpretation have come from studies of ants and birds. This deterministic view of communities and invasions is by no means universally accepted, even by those who work with birds. Wiens (1989), for example, sees little evidence for deterministic assembly rules, and Simberloff and Boecklen (1991) have offered alternative plausible explanations for the observed pattern of bird invasion in Hawaii. These authors are generally convinced that invasion depends more on the characteristics of individual invaders than on the attributes of recipient communities (see also Simberloff, 1981, 1986). Those who work on invasions in the sea or on terrestrial invasions by plants and low-energy organisms generally see the world as indeterministic. Introduced insects quickly adapted to new hosts, even within periods as short as 10 years (Strong et al., 1977; Singer et al., 1993; Thompson, 1994). Similarly, introduced hosts rapidly acquire new parasites and predators. Large differences in diversity among communities (Vermeij, 1978, 1989, 1991b; Ricklefs & Latham, 1992, 1993; Cornell & Hawkins, 1993) imply that recipient communities of plants, insects, or marine invertebrates are
more forgiving of newcomers than are communities of high-energy birds, mammals, or perhaps ants. Community composition of low-energy organisms may generally be less predictable, less orderly, and less integrated than in high-energy forms. Invasion biology has much to offer ecologists and evolutionary biologists in probing the integrity and orderliness of recipient biotas. For example, we can ask whether invaders tend to usurp the ecological roles of native forms or instead to use resources and fashion ways of life not previously exploited in the recipient community. Brown (1989) believes that most invading warm-blooded animals take ecological roles not occupied by native species; but on islands, in lakes, and among land plants, such unique roles of invaders may be less common. What role does invasion play in long-term evolution? Invasion implies change. Not only is it often triggered by change - - the elimination of a barrier to dispersal, the establishment of means by which dispersal can occur, for example - - but in modifications in the recipient biota. Invasions provide opportunities and challenges. The invaders as well as the native species in the recipient communities affected by invaders must cope with and respond to the changing selective regime, or suffer the consequences of restriction and even extinction. In the absence of invasions, communities and the species and interactions comprising them may stagnate, especially if the economic base of energy and nutrients remains fixed. In other words, adaptation and accommodation by organisms to each other may quickly reach a stalemate in the absence of immigration or an economic stimulus (Vermeij, 1987, 1995). If invasions occur on a small scale as the result of minor shifts in the spatial limits of species, the resulting evolutionary realignments may be modest; but if newcomers arrive from far away as the result of large-scale alterations in geography or climate, the change in selective regime and the evolutionary responses to this change could be dramatic. These possibilities remain highly speculative at present, but they point to the potentially crucial role that invasions and invaders have played in stimulating evolution. Given the large number of species now being transported by humans, this aspect of invasion biology cannot be ignored.
EXPERIMENTS, HISTORICAL RECONSTRUCTION AND MODELING It should be clear that invasion biology will profit from a diversity of methodological approaches, and that no single style of inquiry should be seen as superior to all others. Experiments have the virtue of enabling the investigator to vary aspects of species or communities in a systematic manner, but they have the disadvantage of typically being run on small spatial and temporal scales. Moreover, there is a deep-seated tendency
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among experimentalists to view potential outcomes as mutually exclusive alternatives rather than as potentially complementary. I think most biological systems are sufficiently complex that single explanations or hypotheses will rarely suffice to account for the patterns we see. Experiments should be used not to exclude explanations, but to rank them or to explore their interdependence. It has been fashionable in ecology to regard field experiments as inherently superior to experiments carried out in the laboratory. Although field experiments clearly have their place, I believe that experiments with replicated microcosms are more informative as well as ethically more acceptable, especially in studies of invasion. Invaders can have unforeseen and often destructive effects on recipient communities. The field of invasion biology should therefore adopt the standard that work with non-native species or populations be carried out under strictly controlled laboratory conditions from which accidental release of individuals, including gametes and dispersal stages, is impossible. Experiments become impracticable at larger temporal and spatial scales. In such situations, the reconstructive techniques familiar to historians, including paleobiologists, provide the only empirical means of studying invasions. This comparative approach incorporates observations of species and communities before and after invasion, as well as the identification of invading species by means of cladistic methods in which geographical shifts in range can be traced back through time. Armed with such knowledge, we can contrast recipient communities rich in invaders with those that have received few immigrants, or compare donor biotas that have exported many species with those that have provided few invaders. For such longterm studies, groups and community types with a good fossil record clearly show the greatest promise. Although my emphasis throughout this essay has been empirical, there is much room for theoretical analyses as well. Almost all the questions I have posed can serve as guides for models that incorporate principles of population diffusion, population dynamics, community stability, probabilities of extinction, habitat size, per-capita energetics, and the like. Models, however, are a means to an end, not an end in themselves. If the science of invasion biology is to have an impact on policies, it must have at its command empirical data rather than suppositions and extrapolations. The aim of invasion biology should be to seek generalizations and principles, but we must be prepared to accept and to explain a diversity of responses and consequences. For example, whereas invasion by large endothermic mammals may result in extinctions in a recipient biota, plants and smaller animals may not have this consequence. Prior impoverishment or exploitation may provide better opportunities for subsequent invasion in many marine and terrestrial communities, but may have little effect in some lakes such
as the African rift lakes. Many of our conceptions of invasion have been based on species introductions to oceanic islands. There is currently very little understanding of long-term plant invasions, and we have scarcely begun to compare taxonomic groups or community types for their ability to invade, susceptibility to invasion, and propensity to export invaders. From these considerations, it should be obvious that we must continue to document individual cases of invasion. Because invasion biology, like extinction biology, exists in order to study a phenomenon that is justifiably perceived to be important in the human-dominated biosphere, there is a tendency to view the field as somewhat divorced from the larger enterprises of ecology and evolutionary biology. The creation of conservation biology as a discipline and as a field in which students can take advanced degrees is contributing to this isolation. I believe that the phenomenon of invasion is of fundamental importance, and that its study will contribute to an overall understanding of how species interact with each other. As I see it, the success of invasion biology will depend on our insistence that it be incorporated as an integral part of the larger science of biology. |n the long run, our understanding of invasion will be greatly enriched by broad principles, and it will in turn contribute to the further development of these ideas.
REFERENCES Baker, H. G. (1989). Sources of the naturalized grasses and herbs in California grasslands. In Grassland structure and function: California annual grassland, ed. L. F. Huenneke & H. A. Mooney. Kluwer, Dordrecht, pp. 28-38. Brown, J. H. (1989). Patterns, modes and extent of invasions by vertebrates. In Biological invasions." a global perspective, ed. J. A. Drake, H. A. Mooney, F. di Castri, R. H. Groves, F. J. Kruger, M. Rejm~mek & M. Williamson. Wiley, Chichester, pp. 85-109. Cornell, H. V. & Hawkins, B. A. (1993). Accumulation of native parasitoid species on introduced herbivores: a comparison of hosts as natives and hosts as invaders. Amer. Nat., 141, 847-65. Darwin, C. (1872). The origin of species by natural selection or the preservation of favored races in the struggle for life, 6th edn. Colliers, New York. Diamond, J. M. (1975). Assembly of species communities. In Ecology and evolution of communities, ed. M. L. Cody & J. M. Diamond. Belknap Press of Harvard University, Cambridge, MA, pp. 342-444. Drake, J. A. (1991). Community-assembly mechanics and the structure of an experimental species ensemble. Amer. Nat., 137, 1-26. Ehrlich, P. R. (1986). Which animal will invade? In Ecology of biological invasions of North America and Hawaii, ed. H. A. Mooney & J. A. Drake. Springer, New York, pp. 79-95. Elton, C. S. (1958). The ecology of invasions by animals and plants. Methuen, London. Heywood, V. H. (1989). Patterns, extents and modes of invasions by terrestrial plants. In Biological invasions: a global perspective, ed. J. A. Drake, H. A. Mooney, F. di Castri, R. H. Groves, F. J. Kruger, M. Rejm~nek & M. Williamson. Wiley, Chichester, pp. 31-55.
An agenda for invasion biology Lewontin, R. C. (1965). Selection for colonizing ability. In The genetics of colonizing species, ed. H. G. Baker & L. G. Stebbins. Academic Press, New York, pp. 77-91. Lockwood, J. L., Moulton, M. P. & Anderson, S. K. (1993). Morphological assortment of the assembly of communities of introduced passeriforms on oceanic islands: Tahiti versus Oahu. Amer. Nat., 141, 398-408. Lodge, D. M. (1993). Biological invasions: lessons from ecology. Trends Ecol. Evolut., 8, 133-7. Moulton, M. L. & Pimm, S. L. (1986a). The extent of competition in shaping an introduced avifauna. In Community ecology, ed. J. M. Diamond & T. J. Case. Harper and Row, New York, pp. 80-97. Moulton, M. L. & Pimm, S. L. (1986b). Species introductions to Hawaii. In Ecology of biological invasions of North America and Hawaii, ed. H. A. Mooney & J. A. Drake. Springer, New York, pp. 231-49. Pimm, S. L. (1989). Theories of predicting success and impact of introduced species. In Biological invasions. a global perspective, ed. J. A. Drake, H. A. Mooney, F. di Castri, R. H. Groves, F. J. Kruger, M. Rejm~inek & M. Williamson. Wiley, Chichester, pp. 351-67. Ricklefs, R. E. & Latham, R. E. (1992). Intercontinental correlation of geographical ranges suggests stasis in ecological traits of relict genera of temperate perennial herbs. Amer. Nat., 139, 1305-21. Ricklefs, R. E. & Latham, R. E. (1993). Global patterns of diversity in mangrove floras. In Species diversity in ecological communities: historical and geographical perspectives, ed. R. E. Ricklefs & D. Schluter. University of Chicago Press, Chicago, IL, pp. 215-29. Simberloff, D. E. (1981). Community effects of introduced species. In Biotic crises in ecological and evolutionary time, ed. M. H. Nitecki. Academic Press, New York, pp. 53-81.
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Simberloff, D. E. (1986). Introduced insects: a biogeographic and systematic perspective. In Ecology of biological invasions of North America and Hawaii, ed. H. A. Mooney & J. A. Drake. Springer, New York, pp. 3-26. Simberloff, D. & Boecklen, W. (1991). Patterns of extinction in the introduced Hawaiian avifauna: a reexamination of the role of competition. Amer. Nat., 138, 300-27. Singer, M. C., Thomas, C. D. & Parmesan, C. (1993). Rapid human-induced evolution of insect-host associations. Nature, Lond., 366, 681-3. Strong, D. R. Jr, McCoy, E. D. & Ray, J. R. (1977). Time and the number of herbivore species: the pests of sugar cane. Ecology 58, 167-75. Thompson, J. N. (1994). The coevolutionary process. University of Chicago Press, Chicago, IL. Vermeij, G. J. (1978). Biogeography and adaptation." patterns of marine life. Harvard University Press, Cambridge, MA. Vermeij, G. J. (1987). Evolution and escalation: an ecological history of life. Princeton University Press, Princeton, NJ. Vermeij, G. J. (1989). lnteroceanic differences in adaptation: effects of history and productivity. Mar. Ecol. Progr. Ser., 57, 293-305. Vermeij, G. J. (1991a). When biotas meet: understanding biotic interchange. Science, N. Y., 253, 1099-1104. Vermeij, G. J. (1991b). Anatomy of an invasion: the transArctic interchange. Paleobiology, 17, 281-307. Vermeij, G. J. (1995). Economics, volcanoes, and Phanerozoic revolutions. Paleobiology, 21, 125-52. Wiens, J. A. (1989). The ecology of bird communities, Vol. 1. Foundations and patterns. Cambridge University Press, Cambridge. Wilson, E. O. (1961). The nature of the taxon cycle in the Melanesian ant fauna. Amer. Nat., 95, 179-93.