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Predicting Invasions of Nonindigenous Plants and Plant Pests 3 Establishment Establishment refers to the apparent persistence of a population and is equivalent to the term naturalization as used for the descendants of plant immigrants (Mack 1997). To become established or persistent, immigrant plants, arthropods, or pathogens (or their descendants) need not be widespread or growing rapidly, but they must withstand challenges to their survival. The challenges include the random events that often prove detrimental to the survival of small populations, including a potentially hostile climate; inadequacies in nutrients, hosts, or mates; and competitors and predators. The vast majority of immigrant populations do not become established. For example, although thousands of nonindigenous phytophagous insects arrive in the United States every year, establishment is a rare occurrence (Carey 1996, Lewis and Kareiva 1993). Only an estimated 10% of all nonindigenous insect species that are introduced into a new range become established. Even when insects are carefully selected for intentional introduction as biological control agents, only about 33% become established (Williamson and Fitter 1996). How does a species become established in a new geographic range? Studies dealing with that question have focused on the environmental forces that impede establishment while identifying particular circumstances of an introduction, such as the size of the founder population or the species’ traits, that might facilitate its ability to overcome that impediment. For example, it has been recognized for more than 150 years that immigrants into a new range gain a substantial potential advantage by leaving behind their native competitors, natural enemies, or other biotic constraints on growth, development, survival, and reproduction. Release from such constraints might in itself explain the superior individual growth and
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Predicting Invasions of Nonindigenous Plants and Plant Pests large increases in population that have been documented for many species in new ranges (Thebaud and Simberloff 2001). When biological control of an invasive species, which involves the deliberate introduction of parasites and predators of the species from its native range, is successful, it is powerful confirmation of the potential role of biotic constraints in curbing a species’ abundance and distribution. In this chapter, we first review the stochastic character of forces that determine the establishment or persistence of populations, especially the small populations that typify immigrants. We then illustrate how biologists have attempted to categorize the role of a population’s spatial structure in interacting with the stochastic character. Without attempting to be inclusive, we next proceed to illustrate the breadth of environmental factors, both abiotic and biotic, that form the specific forces that immigrant populations encounter. Finally, we provide illustrations of life-history traits that can influence immigrants’ tolerance of a new range. In compiling this chapter, we were aware that some aspects of the discussion of persistence are equally pertinent to the proliferation and spread of a species, the topic of Chapter 4. As a result, we introduce these shared properties or circumstances here and mention them only briefly in Chapter 4. Although additional observations, new hypotheses, and empirical testing are needed to confidently predict the net effect of these countervailing forces on the outcome of a specific species’ introduction, a body of data that underlie the basis for establishment is slowly emerging. STOCHASTIC EXTINCTION— THE PERILS OF SMALL POPULATIONS The defining demographic of an introduced species is typically its small population. Even the planet’s most abundant and widespread invasive species commonly began as “rare” species in their new ranges, compared with the size of their populations in their native ranges. (There are exceptions; see Eckert et al. 1996). Although population extinction can result from deterministic processes— ranging from direct eradication by humans to fire or flooding—a pervasive threat to the persistence of small populations is stochastic extinction. This risk of extinction for small populations transcends the taxonomic groups we examine here. For plants and arthropods, the topic is often examined in terms of the minimal viable population (see Box 3-1); for pathogenic microorganisms, it is referred to as the minimal infective dose. Consequently, our remarks should be interpreted as relevant for all taxonomic groups unless stated otherwise. Demographic models have relied on such quantities as the mean population growth rate and the variance in growth rate (Leigh 1981, Goodman 1987) and predict that persistence time increases slowly with increasing carrying capacity. As a result, extinction is predicted to be much more likely at lower population numbers, a conclusion that is biologically realistic. To facilitate discussion of the importance of stochastic extinction in the early stages of establishment, the forces
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Predicting Invasions of Nonindigenous Plants and Plant Pests BOX 3-1 Minimal Viable Population Theoretical development associated with the concept of minimal viable population (MVP) for rare taxa (Soulé 1987, Lande 1988, Menges 1991) has demonstrated the profound demographic implications of low population numbers in the extinction process. Although descriptions of what is implied by MVP have varied (Shaffer 1981), most definitions focus on estimating the minimal population density for a given probability of population persistence over a specified period. In applications of the idea of MVP for rare species, the time frames are often thousands of years (Shaffer 1987). As a result, the recommended population sizes in conservation biology are often large to reduce the likelihood of chance extinction over the long term by various stochastic processes that can differ in their frequency and their potential demographic and evolutionary impacts. Nonindigenous species are often rare during the initial phases of their colonization. By analogy, an application of the concept of MVP to a newly introduced species might be useful in predicting the likelihood of its establishment. Needed here is knowledge of the acceptable maximal persistence time for the newly introduced species. Precisely because they are at low population densities, new introductions are typically not detected, so it is difficult to know how long they persisted without obvious population growth. However, one would expect that the periods for the establishment phase of currently widespread nonindigenous plants were much less than the 1000-year persistence times sometimes recommended for rare species. Actual periods for the establishment phase in invasive species on which data are available indicate that the initial “lag phase” in the population growth trajectory is often less than 100 years. For example, after initial introduction into northern Australia around 1900, Mimosa pigra populations remained small and confined to environs around Darwin until the 1950s. After that short lag phase, this native of Mexico and South America began to spread rapidly throughout Australia’s Northern Territory; it is now a major threat to wetland areas in Kakadu National Park (Lonsdale et al. 1989, Cousens and Mortimer 1995). The population required to ensure persistence for this much shorter period could be very small and thus much more difficult to detect and eradicate. Difficulties in detection because of low population densities might be exacerbated in invasive species that can reproduce vegetatively or by uniparental forms of reproduction. The theory predicts that the population required for persistence of clonal or parthenogenic species is even smaller than those for species that reproduce sexually (MacArthur and Wilson 1967, Shaffer 1981). Efforts to predict the likelihood of establishment of a recently introduced species will need to consider how an Allee effect may influence the MVP. Life-history traits related to dispersal, reproduction, host finding, predator defense, or other factors can affect the critical density threshold, below which a population that is subject to inverse density dependence cannot recover. Characteristics of the habitat colonized by the founding population can further interact with an Allee effect; the MVP may be higher or lower, depending on the size of the founding colony and the extent of environmental stochasticity.
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Predicting Invasions of Nonindigenous Plants and Plant Pests of stochasticity that can affect population persistence can be grouped into four main categories: demographics, environment, natural catastrophes, and genetics (Shaffer 1981). Demographic Stochasticity Demographic stochasticity refers to the chance variation in survival and reproductive rates in very small populations (for example, the probability that all individuals in a population will not reproduce in a given period). Although average values for survival or reproduction might remain relatively constant, chance variation can occur among individuals. As a simple example, consider an annually reproducing population with nonoverlapping age classes, whose average probability of survival to reproduction is 0.20. Despite this average survival rate, if the population is extremely small—say, 10 individuals—there is a probability of about 11% in any one year that all members of the population will die before reproducing, in which case the population will go extinct. If the population is somewhat larger–say, 50 individuals–the probability that the population will go extinct during a given year is very low, less than 0.002%. Equally important is that the probability of demographic extinction is associated with just a single “trial” (that is, a single year). As the “demographic dice” are cast each year, the cumulative probability of chance extinction increases as a simple arithmetic product of the probabilities for all consecutive years if the population does not increase. Although the numerical threshold where demographic stochasticity can cause extinction depends on the particular situation, a threshold estimate for dioecious organisms of about 50 individuals is widely cited (Pollard 1966, Keiding 1975, Shaffer 1981). The fate of a population for which this type of stochastic process becomes important is bleak; as noted by Gilpin and Soulé (1986), demographic stochasticity might well be viewed as “the immediate precursor of extinction.” Environmental Stochasticity Environmental stochasticity usually reflects the impact of random variation in the environment as it influences a population. In its simplest form, the demographic effects of environmental perturbations are assumed to be equally distributed across all individuals in a particular age or stage class in a population. For example, an increase in seed predators might reduce average reproductive output by 80% in a plant population; this decrease, because it represents a drop in average reproductive output across all individuals in the reproductive age class, can severely reduce the size of the population, regardless of its initial size. Because of its capacity to adversely affect even large populations, environmental stochasticity is considered an important force in promoting chance extinction (Sykes 1969, Cohen 1979, Leigh 1981, Menges 1990, 1991). In essence, envi-
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Predicting Invasions of Nonindigenous Plants and Plant Pests ronmental stochasticity can reduce a population’s size to a point at which demographic stochasticity becomes important and causes chance extinction. Goodman (1987) has suggested that when environmental stochasticity is present, expected population persistence time increases roughly as a linear function of population size. Given that the typical effect of increasing environmental stochasticity is to reduce the likelihood of population persistence, there should be selective value in the capacity of an organism to reduce the demographic impact of environmental variation. One potential evolutionary response is the development of adaptive phenotypic plasticity: reducing the variance in survival, growth, and reproduction buffers the adverse impact of environmental variation on population persistence (Caswell 1983). Because of plants’ modular construction, phenotypic plasticity in plant structure has been suggested as an adaptive response to buffer localized gradients in resource availability (Bradshaw 1965, Schlichting 1986). In both plants and animals, physiological plasticity in the form of acclimation to variation in climatic factors, such as temperature, has also been suggested as an adaptive plasticity response (Sultan 1987). Natural Catastrophes Floods, fires, earthquakes, droughts, ice storms, and the like, which all occur relatively infrequently and at random intervals, are also potent threats to the persistence of populations. In a sense, natural catastrophes constitute a more extreme and less predictable form of environmental stochasticity. Given the sporadic occurrence of natural catastrophes, it is difficult to characterize the disturbance caused by them and thus incorporate them realistically into models of population persistence. Some theoretical treatments of natural catastrophes indicate that there is a “diminishing-returns” effect: the average persistence time of a population increases only in correspondence to the logarithm of its size (Ewens et al. 1987). Thus, greater and greater increases in population size are required to gain the same increase in persistence time. Further work has indicated that the form of the relationship depends on the carrying capacity of the habitat and on the severity and frequency of catastrophes (Lande 1993). As a result, a population might need to be very large (in the thousands to millions) if it is to persist in spite of periodic catastrophes (Shaffer 1987). Genetic Stochasticity Stochastic forces involving founder events, genetic bottlenecks, and genetic drift play a dominant role in determining the fate of immigrant species because frequent colonizing episodes are a central feature of their population biology. These forces tend to dominate during the early stages of establishment after long-distance dispersal, when populations are often very small. Theoretical studies
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Predicting Invasions of Nonindigenous Plants and Plant Pests demonstrate that frequent bottlenecks and low effective population sizes reduce genetic variation, especially the frequencies of rare alleles (Nei et al. 1975, Sirkkomaa 1983). However, strong directional selection during the early stages of population establishment can also reduce genetic variation, particularly at loci that govern fitness. Hence, a population early in its postimmigration history is especially vulnerable because random genetic events erode the little genetic diversity that introduced populations usually contain. Low population size can also result in increased mating among related individuals; increased inbreeding can result in the expression of recessive deleterious alleles in homozygous form and cause reduced fitness or inbreeding depression in the progeny (Barrett and Husband 1990, Barrett and Kohn 1991). The input of mutational variance, recombination, and gene flow theoretically can counteract those forces. In addition, many species have become invaders despite low genetic diversity. In these cases, extensive areas of the introduced range often comprise a small number of genotypes (Moran and Marshall 1978, Scribailo et al. 1984, Barrett and Shore 1989, Novak and Mack 1993). Low diversity at the population and regional levels is especially evident in plant species that propagate by asexual reproduction, sometimes called selfing. However, effects of genetic bottlenecks associated with introduction of small populations can also be counterintuitive and complex, as evidenced by the introduction of the Argentine ant (Linepithema humile) into California. In its native Argentina, intraspecific competition limits colony size and population density, and numerous ant species co-exist with the Argentine ants. Suarez et al. (1999) found that populations of the Argentine ant in California exhibited substantially lower heterozygosity than populations in their native range. Genetic changes in the introduced ant populations were associated with altered behavior that reduced nestmate recognition and hence intraspecific competition and resulted in high population densities, competitive displacement of a majority of the native ant species, and adverse effects on ant predators, such as horned lizards (Suarez et al. 2000). Evidence suggests that the imported fire ant (Solenopsis invicta) similarly experienced a pronounced genetic bottleneck when it was introduced into North America (Ross et al. 1993). Altered ecological characteristics and population genetics of the introduced fire ant populations appear to be associated with changes in the social organization of its colonies (Ross et al. 1996). Such changes include multiple queens and zero relatedness between workers and new queens in the introduced populations, compared with few queens and significant relatedness between queens and workers in the native range. Low relatedness has potential advantages for ants and has been associated with rapid colony growth in other ant species (Cole and Wiernasz 1999).
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Predicting Invasions of Nonindigenous Plants and Plant Pests Allee Effects An Allee effect occurs when low-density populations sustain a zero or even negative rate of increase because of reduced reproduction or survival when con-specifics are insufficiently abundant. Eventually, “undercrowding”—inverse density dependence at low density—drives the population below a critical threshold and extinction occurs (Allee 1931, Courchamp et al. 1999). The dynamics of Allee effects, therefore, can exert a substantial influence on whether a colony of a newly arrived organism is able to persist and become established. One frequent cause of Allee effects is a scarcity of reproductive opportunities at low densities. For example, in some insect populations, difficulty in locating conspecific mates will reduce the likelihood that individuals in the next generation will produce offspring, and in the case of arrhenotokous insects (a population in which unmated females produce only males), will result in a population with a male-biased sex ratio. Ultimately, this form of demographic stochasticity leads to collapse of the population. Other factors may also generate inverse density dependence in low-density populations, including a reduction in the ability of individuals to find or use suitable host plants (Way and Banks 1967), decreased ability to cooperate in defense against predators (Turchin and Kareiva 1993), and genetic inbreeding that leads to decreased fitness (Courchamp et al. 1999, Lamont et al. 1993). The strength of an Allee effect on the persistence of a population depends on the processes influenced by inverse density dependence. Species in which fitness is enhanced in some way by conspecific facilitation or cooperation may be subject to Allee effects only at very low densities. In contrast, species with obligate sexual reproduction may be more strongly affected by an Allee effect and at a wider range of densities (Courchamp et al. 1999). Species that are subject to a strong Allee effect may also be more vulnerable to extinction due to environmental stochasticity because the population size below which they cannot recover from an unfavorable weather event will be larger than for other species. Influence of Allee effects on establishment has been addressed by examining the dynamics of populations of nonindigenous species released in biological control programs. Hopper and Roush (1993) found that parasitoid wasp and fly species released for biological control of leaf-feeding insects were subject to an Allee effect when dispersal from low-density populations led to low mating success, which resulted in male-biased sex ratios. Modeling showed that the Allee effect could drive populations to extinction and that it limited establishment of introduced parasitoid species more than the limits imposed by stochastic environmental variation or lack of genetic variation. Grevstad (1999a,b) used simulation modeling to show that if the net reproductive rate of a newly introduced species was even slightly greater than 1.0, demographic stochasticity was unlikely to limit population persistence. Environmental stochasticity, however, interacted with an Allee effect. When an Allee effect was present and environmental conditions were relatively constant, establishment of a species was most likely to be
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Predicting Invasions of Nonindigenous Plants and Plant Pests successful if there was a single introduction of many individuals. In contrast, when environmental stochasticity was great, establishment was more likely to occur if there were many introductions of low numbers. Interactions between an Allee effect and environmental variability in larger colonies were more deleterious than the sum of their independent influences; a few years with bad conditions reduced population density to a level where negative population growth eventually led to extinction (Grevstad, 1999a,b). The need to estimate the influence of Allee effects on any immigrant population depends on the species and the circumstance, thereby complicating the population state in a new range. Effects of Spatial Structure Models estimating the persistence of a population typically consider only aggregate population statistics, not the spatial distribution of individuals. As a result, the question arises as to whether the extinction dynamics of spatially structured populations (such as a patchy distribution) might differ from those with little spatial structure (such as an aggregate). The answer is frequently yes. Effects of environmental stochasticity can be reduced if the species is patchily distributed in such a way that not all members in any age class are affected equally by environmental perturbations. The potential for spatial patchiness to function as a buffer against extinctions caused by environmental stochasticity depends, however, on the degree to which environmental fluctuations are correlated across patches (Gilpin 1987, Stacey and Taper 1992). If environmental conditions are correlated across the region occupied by subpopulations of a newly arrived species, “Moran effect” dynamics could lead to a tension between synchronizing effects of extrinsic environmental stochasticity and desynchronizing effects of nonlinear density dependence (Hudson and Cattadori 1999, Ranta et al. 1999). In the Moran effect, originally proposed as a mechanism to explain synchronized fluctuations in Canadian lynx populations (Moran 1953, Royama 1992), when disjunct populations have the same endogenous structure (such as density dependence), a correlated exogenous, density-independent factor (such as weather) will bring population fluctuations into temporal synchrony (Earn et al. 1998, Heino et al. 1997, Hudson and Cattadori 1999, Williams and Liebhold 1995). Thus, when a species is strongly influenced by Moran effect dynamics, a period of unfavorable environmental conditions will promote extirpation of all colonies. A newly arrived immigrant species will persist, therefore, only if at least some subpopulations experience “good times” while other subpopulations suffer reduced population growth during “bad times”. In contrast, spatially structured populations may be subject to inverse density dependence regardless of environmental conditions if subpopulations are diluted by dispersal. Such a scenario could increase the probability of extinction due to stochasticity or Allee effects (Hopper and Roush 1993, Lewis and Kareiva 1993).
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Predicting Invasions of Nonindigenous Plants and Plant Pests If the initial distribution of the populations of an immigrant species across a spatial hierarchy is known, this information might predict the potential for spread. The concepts developed in conservation biology for rare native species can be applied to understand the dynamics of the small populations that characterize immigration and establishment. In an attempt to understand what it means to “become rare”, Rabinowitz (1981) proposed a classification system that uses three attributes to characterize rarity: local population size, habitat specificity, and geographic range. When expressed as dichotomies, the three attributes result in an eight-cell table (Table 3-1) that describes the spatial characteristics of different forms of rarity. For plant pathogens, habitat would refer to the host infected (for example, a wide habitat would mean a wide host range for the pathogen). The upper-left cell represents the distribution pattern of a common species, but the remaining seven cells describe distinct categories of spatial patterning by which Rabinowitz classified rare taxa and asked questions about the origins of rarity. That approach has application for nonindigenous species: one can ask how nonindigenous species differ in their potential for becoming common. If we assume that immigrants initially consist of small, sparse populations, we can restrict our attention to the bottom row of the table. Even casual inspection of the categories of the bottom row suggests that some distribution patterns will be more worrisome than others as signals of a species’ potential spread in a new range. The far-right cell in the bottom row suggests a single introduction. Because of its habitat specificity and small geo TABLE 3-1 Spatial Characteristics of Different Forms of Species Rarity Local Population Size Large Geographic Range Habitat Specificity Small Geographic Range Habitat Specificity Wide Narrow Wide Narrow Large, dominant somewhere Locally abundant over a large range in several habitats Locally abundant over a large range in a specific habitats Locally abundant in several habitat but restricted geographically Locally abundant in a specific habitat but restricted geographically Small, sparse everywhere Consistently sparse over a large range and in several habitats Consistently sparse in a specific habitat but over a large geographic range Consistently sparse in several habitats but restricted geographically Consistently sparse in a specific habitat and geographically restricted SOURCE: Adapted from Rabinowitz 1981.
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Predicting Invasions of Nonindigenous Plants and Plant Pests graphic range, this type of immigrant is probably most susceptible to stochastic extinction. At the other end of the spectrum is the immigrant described by the far-left cell in the bottom row. This species inhabits a broad geographic range and is found in many habitats (or associated with many host species). Its wide distribution (both geographically and by type of habitat) might reflect multiple introductions. Stochastic extinction is very unlikely for a species with this distribution pattern. Obviously, if populations increase in size (move to the upper row), the species will become common and probably invasive. The next cell to the right represents a scenario that, again because of the broad geographic range, suggests multiple introductions. Because the species is restricted to a particular habitat, the emergence of an invader through this scenario might be predictable, and effective management and containment of the species might be quite feasible. Rabinowitz (1981) suggested that there might be no rare species in the last category (third cell, second row). There might indeed be no rare native species that are limited geographically and are found at low population density in several habitats. However, this scenario could be common among persistent nonindigenous species. It represents a situation similar to that of the most problematic category (the far-left cell) except that the limited geographic range described for this cell suggests a single introduction. One might suspect that such a species could become established, and even invasive, and is limited only by lack of additional introductions throughout its potential range. Early detection of a nonindigenous species with this distribution should evoke immediate consideration of eradication. Although those categories are admittedly simplistic, they do provide a general conceptual framework for understanding the various pathways to abundance that a newly established immigrant population might follow. Avoiding Stochasticity: Multiple Introductions and Population Size Aside from the obvious inability of a population to survive under a climatic regimen that is well beyond its tolerance, stochasticity is the greatest threat to small populations. And as stated above, small numbers typify most unintentional introductions of nonindigenous species. But if the founder population is large enough or replenished with additional propagules, it can withstand stochastic forces—provided it can tolerate the overall character of the new environment. Empirical studies of the relationship between the probability of establishment and the size of the founding population stem from evaluations of efforts to establish insects for biological control. In general, establishment is predicted to increase with population size (Grevstad 1999a). However, it is also possible that persistence is independent of population size if density-independent factors— such as weather, habitat conditions and the size of the habitat patch—are the main determinants of persistence or if the population’s numerical increase allows initially small populations to escape rapidly the risk of extinction.
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Predicting Invasions of Nonindigenous Plants and Plant Pests Bierne (1975), in a widely cited retrospective analysis of the role of initial colony size in establishment, reviewed Canadian biological control programs. He found that if fewer than 5000 individuals were released, about 9% of the species became established—a percentage that is similar to the 10% estimated for accidental introductions (Williamson 1996). If at least 30,000 individuals were released, 79% of the species became established. The average number of individuals per release site also seemed to be important; establishment rates increased from 15% to 65% of species if at least 800 individuals were released at a single location. Bierne’s (1975) approach has limitations: the role of the number of individuals released in each case might be confounded by the traits of particular species; and these traits also contribute to establishment, such as a high reproductive rate or abundant distribution in their native range (Crawley 1986, 1989b). Grevstad (1999a) took an experimental approach in assessing relationships between population size and persistence. She followed the fate of 92 experimental releases of two chrysomelid beetles for three full generations and found that the probability of establishment increased over the range of initial beetle density (20, 60, 180, and 540 beetles). Population growth rates varied among environments but were positively related to release size. In a second experiment, in 20 releases of single gravid females, only one female founded a population that persisted for the duration of the 3-year study. Although Levine and D’Antonio (1999) contend that any community, given enough propagules, can be invaded, nonindigenous insects are usually introduced accidentally and presumably arrive in low numbers in most cases. Small populations have a greater random chance of extinction than large populations and are more vulnerable to inbreeding depression, so the descendants of founders might also need propitious conditions to survive. Liebhold et al. (1995) and MacArthur and Wilson (1967) suggest that the probability of establishment can be simply described as a continuous function of initial population size. Translating these conclusions into practical terms is currently difficult because the small immigrant population that is detected may be only one of a large group of small populations that arrived at the same time. Although many may soon go extinct, some may survive unless they are deliberately eradicated. Not only a large number of immigrants per introduction, but also frequent introductions will mitigate stochastic processes and increase the likelihood of establishment. Crawley (1986) found that the probability of establishment increased with both the sizes and the number of population releases. Repeated introductions increase the chance that an immigrant species will encounter a combination of resources, scarcity of competitors, and low density of predators or pathogens that will permit establishment. That expectation appears to be borne out in the release of insects for biological control. In the Canadian biological control programs, nonindigenous species that were released in at least 10 episodes established in 70% of the cases; those released in fewer than 10 episodes established in only 10% of the cases (Bierne 1975).
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Predicting Invasions of Nonindigenous Plants and Plant Pests crossing, is the predominant form of reproduction in animals. It is also predominant among plants because of self-incompatibility mechanisms that promote crosses between individual genotypes and because of structural limitations, such as the separation of anther maturation and stigma receptivity in time (dichogamy) and space (herkogamy). Among dioecious species (in which separate plants are male or female) and those with self-incompatibility, pollen must be transferred from plant to plant if fertilization is to be achieved. Pollen flow might not occur in the absence of a suitable pollinator or if an individual is growing far from potential mates (Willson 1983). Dioecy does not, however, appear to be a major limitation for species establishment; there are dioecious invasive plant species, such as Rumex acetosella, Ailanthus altissima, and Ilex aquifolium. Uniparental sexual reproduction arises from self-fertilization and is facilitated by hermaphrodite sex expression. As long as the flowers are self-compatible, plants with perfect flowers might have the ideal mating system for establishment in a new range. Species that usually display some form of uniparental reproduction also have an advantage as founders because the lack of recombination with other plants preserves multilocus genotypes related to increased fitness. In contrast, monoecious species, which have separate male and female flowers on the same plant, might face the same limitation in pollination faced by dioecious species. Nevertheless, this limitation has clearly been overcome in some species, such as several pines (Richardson and Higgins 1998). Many perennial species that have been introduced into North America have the capacity for asexual reproduction by apomixis. Apomixis, which includes agamospermy and the clonal or vegetative regeneration of plant parts, allows isolated individuals to establish new populations and produce plants that are presumably adapted to the current environment. Agamospermy allows a plant to produce viable seed, often without the presence of any male gametes; this is an advantage of an isolated individual. In a comparative study of woody plant invaders and noninvaders, agamospermy was found to be slightly correlated with species that had become invasive (Reichard 2001). Many plants have the ability to regenerate from a stem or root fragment or to resprout from a cut stem (Bell 1991). Vegetative reproduction of this type allows a population to increase rapidly and to regenerate quickly after a trauma. If the fragments are dispersed, as during a flood, distributed populations can be created. There are many examples of invaders for which most or all reproduction in the new range is the result of asexual reproduction. Clonal propagation is especially prevalent among invasive aquatic plants (reviewed in Barrett 1989, Barrett et al. 1993). In some cases, the failure to reproduce sexually occurs because of genetic sterility (as in Salvinia molesta) or the absence of mating types required for sexual reproduction (as in Elodea canadensis); alternatively, restrictions on sexual reproduction might arise because of unfavorable environmental conditions in the introduced range (as in Eichhornia crassipes).
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Predicting Invasions of Nonindigenous Plants and Plant Pests The relation between reproductive systems and a population’s ability to become established appears linked to the association between self-fertilization and colony establishment (Marshall and Brown 1981, Barrett 1982, Gray 1986, Brown and Burdon 1987). Single self-compatible individuals, with the capacity for autonomous self-pollination (“selfers”), are capable of forming established populations through self-fertilization, whereas self-incompatible or unisexual individuals require the simultaneous arrival of mating partners and pollen vectors (in animal-pollinated species) for reproduction. That simple idea, known as Baker’s law (Baker 1955, Pannel and Barrett 1998), states that self-compatibility is favored among immigrants after long dispersal. It has also led to the prediction that annuals and nonindigenous ruderals (plants that commonly occupy rubbish piles and areas that are frequently disturbed), which depend on recurring dispersal and establishment, are more likely to be selfers than obligate outcrossers. Broad surveys generally support the association between self-fertilization and ruderals (Mulligan and Findlay 1970, Price and Jain 1981), although this pattern is less evident among perennial ruderals, many of which invest heavily in clonal offspring and are also outcrossing (Marshall and Brown 1981, Crawley 1987). Among flowering plants, increased longevity is generally associated with decreased selfing: annuals display the highest selfing rates, followed by herbaceous perennials. Woody perennials are predominantly outcrossing; few woody species are reported to have high levels of selfing (Barrett et al. 1996). Surveys of plant invaders show that those which rely on sexual reproduction are not all selfers; this indicates that some outcrossers overcome this constraint during establishment. Pannel and Barrett (1998) evaluated the benefits of reproductive assurance in selfers compared with outcrossers in the context of colony formation in a metapopulation. Their results suggest that an optimal mating system for a sexual invader should include the ability to alter selfing rates according to local environmental and demographic conditions. When populations are small or individuals are at low density during the early phases of establishment in a new range, plants should be selfers to maximize fertility, thus increasing population growth rates. However, when populations become large and pollinators or mates are not limiting, outcrossing and its attendant genetic effects will be more beneficial. Flowering and Fruiting Periods A long flowering time ensures that a plant’s flowers are receptive when pollinators are available. If a plant has a protracted season of flowering, the probability of fertilization is increased. Annual ruderals in Great Britain (Perrins et al. 1992a) and invasive woody plants in North America (Reichard 1994) have been shown to have a long flowering period. The latter study also showed that a long flowering time correlates highly with the length of the fruiting period. Similar to the case with the length of the flowering period, a long fruiting period
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Predicting Invasions of Nonindigenous Plants and Plant Pests can provide a greater opportunity for seed dispersal. So far, however, these traits have been of little use in predicting which species will be invaders across the broad taxonomic groups of potential immigrant species. Juvenile Period The juvenile period is the time from seed germination to the onset of flowering. A short juvenile period could allow a population to increase rapidly while decreasing the probability of the population’s detection by predators, foragers, and pathogens before its sexual reproduction. Annual plant species, by definition, have a short juvenile period; ruderal or weedy annuals have a shorter juvenile period than nonweedy species (Perrins et al. 1992b), as do invasive woody perennials (Reichard 1994). Length of the juvenile period can be difficult to determine accurately for woody species, for which several years can elapse before onset of reproduction. Length of the juvenile period has been used repeatedly to predict persistence of nonindigenous species (Rejmanek and Richardson 1996, Reichard and Hamilton 1997, Pheloung et al. 1999). Seed Production Species with high seed production on an annual or cyclical basis are more likely to become established if their seeds are readily dispersed (Juenger and Bergelson 2000), because the odds are greater that some fraction of the seeds will reach sites suitable for germination. But incorporating this trait into any prediction of establishment is difficult because the level of seed production can be difficult to quantify for newly introduced species, especially woody plants. Dormancy Given the influence of environmental stochasticity on establishment, there should be strong selection for life-history traits that reduce its impact on a population. Seed banks buffer against the wide swings in the size of the vegetative population that result from strong year-to-year variation in resource availability (Cohen 1979, Venable and Lawlor 1980, Brown and Venable 1986, Phillipi 1993). Germination cuing, in which environmental signals correlated by habitat quality are sensed by seeds and trigger germination or induce dormancy, is a potentially important form of adaptive dormancy in plants. Given the potential for seed dormancy and germination cuing to reduce the demographic impacts of environmental stochasticity, it is not surprising that both dormancy and germination cuing are widespread in many agricultural (and predominantly nonindigenous) weeds (Cousens and Mortimer 1995).
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Predicting Invasions of Nonindigenous Plants and Plant Pests Light Requirements The ability to use light efficiently may enhance a plant’s ability to live in areas with extensive canopies. Consequently, the ability to establish may be related to this trait. The extent to which shade tolerance is an attribute shared widely among naturalized plants is unknown but deserves systematic survey. Baruch et al. (2000) examined 10 physiological and morphological plant traits of four invasive members of the Melastomataceae (two herbs, a shrub, and a tree) in Hawaii and found that the invasive species were better suited to capturing and using light than a large group of natives. Pathogens Life-history traits important for the establishment of plant pathogens include reproductive strategies and genetic variability related to fitness, virulence, and host compatibility. Reproductive Strategies As with plants, pathogens use many reproductive strategies. Some pathogens (such as viruses and some fungi) reproduce only in the presence of their hosts, whereas others (for example, many fungi) are facultative saprophytes and do not require the plant host for reproduction. Some fungi reproduce only sexually, whereas many pathogens, such as viruses and some fungi, reproduce only asexually. Some pathogens can complete several generations in a single year, whereas others require several years to complete a single generation. Asexually reproducing pathogens are thought to establish most easily (Agrios 1988). Another major characteristic of invasive pathogens is a high rate of survival when the plant host is not present (for example, in the winter for pathogens that infect the leaves of annual plants and deciduous perennials) or when the physical environment is totally unfavorable. Survival can occur in a dormant state (for example, in overwintering spores), in a saprophytic condition, or as infections in alternative hosts (Agrios 1988). The most successful pathogens display a short time between one infection cycle and the next, have a high rate of production of infectious units (spores, bacterial cells, nematode cysts or eggs, or viruses), and have a long infectious period–the time that infectious units are produced or plants are contagious (Campbell and Madden 1990). Races of Puccinia helianthi, the sunflower rust pathogen, illustrate this point. The rust’s superior colonizers have higher spore germinability, more rapid spore germination, more rapid formation of appressoria (spore-producing structures), and higher spore production than other genotypes or races (Prudhomme and Sackston 1990).
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Predicting Invasions of Nonindigenous Plants and Plant Pests Genetic Variability in Fitness and Virulence The characteristics described above might increase the potential for establishment, provided that the pathogens are carried to a genetically compatible host. Although it could be predicted that successfully established pathogen populations would have a wide range of virulence genes (Lawrence and Burdon 1989), this is not routinely the case, particularly in an agricultural context. Pathogen populations typically have the smallest number of virulence genes needed for survival, presumably because carrying unneeded virulence genes imposes a fitness penalty on the pathogen. Common, widespread pathotypes of Pyricularia grisea, the fungal cause of rice blast, always have fewer virulence genes than rare pathotypes–an observation that is consistent with the theory of a fitness disadvantage of accumulated virulence genes (Mekwatanakarn et al. 2000). It is, however, the continuous generation of novel pathogenic variation that enables pathogen populations to overcome resistance and find susceptible hosts (Mekwatanakarn et al. 2000). A large local effect on the diversity of races and complexity of virulence occur in a pathogen population as it changes in response to host resistance (Andrivon and de Vallavielle-Pope 1995). The importance of variability in virulence for establishment tends to be greater among pathogen populations with narrow host ranges. High complexity for virulence is often found in clonally (asexually) reproducing pathogens, such as Pyricularia grisea tritici, that have long faced race-specific host-resistance genes (Marshall 1989; 1993). Conversely, populations of fungi with frequent sexual reproduction, such as the powdery mildews, often have fewer races but a greater diversity of virulence phenotypes (Roelfs and Groth 1980, Groth and Roelfs 1982). Because of the local effect of selection by host resistance on the diversity and complexity of the pathogen population, immigrations by new genotypes are often detected on the basis of abrupt changes in pathogenicity or mating type. That was the case in Europe with Phytophthora infestans, the late blight disease pathogen (Fry et al. 1992). Some migrations are cryptic, especially if the virulence pattern of a pathogen population has not been monitored. However, information about the genetic diversity in pathogen populations can also help to reveal new introductions. For example, Sphaeropsis sapinea is an asexually reproducing fungus on Pinus spp. in South Africa, so it could be predicted that its population should consist of clonal lineages. But surveys revealed populations of high genetic diversity, a situation consistent with the occurrence of multiple introductions from different sources over a long period (Smith et al. 2000). Finally, in some wild host-pathogen combinations, extinction and recolonization occur routinely, and these outcomes suggest that migration and gene flow are important contributions to the genotype diversity of the pathogen (Burdon et al. 1995).
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Predicting Invasions of Nonindigenous Plants and Plant Pests Rate of Population Growth The net effect of whether a pathogen will come into contact with a susceptible host and the chance that such a contact will result in infection are summarized by the intrinsic rate of increase (r) or, more mechanistically, the basic reproduction number (R0), sometimes called the progeny-parent ratio (Madden et al. 2000, Swinton and Gilligan 1996). A pathogen will be established only if R0 is greater than a threshold, which is typically 1.0 (higher for small founder populations subject to the effects of stochasticity). An adequate way of determining a threshold of R0 for persistence over more than one growing season, which incorporates survival and within-season dynamics, has not yet emerged, because of the difficulty of incorporating temporal discontinuities (periods without a susceptible crop) into the predictions (Gubins and Gilligan 1997, Madden and van den Bosch 2000). Insects Mating Systems Insects and other arthropods usually arrive in a new range in small numbers and must reproduce and increase in density rapidly if they are to become established. Parthenogenesis and other forms of uniparental reproduction, such as mother-son or sibling mating, can facilitate survival of low-density populations or populations surviving in small refugia. Parthenogenesis results in a relatively high ratio of reproductive potential for each unit of resource, enabling nonindigenous organisms to exploit a resource rapidly when ephemerally favorable conditions arise (Niemelä and Mattson 1996). The search for mates can impede establishment if the loss of individuals dispersing to search for mates exceeds the rate of population growth (Lewis and Kareiva 1993). Parthenogenic forms of reproduction can reduce or even eliminate the need to locate mates. Uniparental reproduction can facilitate the survival of a small population, but inbreeding depression can eventually become problematic in such populations, depending on the rate of mutation or the rate at which new, unrelated individuals join the population. However, populations of parthenogenic insects that are highly inbred might exhibit little inbreeding depression in fitness if most individuals with deleterious recessive alleles are lost. In addition, parthenogenesis is often linked with polyploidy and high heterozygosity, facilitated by apomixis. These traits presumably confer broad ecological tolerances for new and varying environments (Bullini and Nascetti 1990, Craig and Mopper 1993, Niemelä and Mattson 1996). Parthenogenesis does appear to be frequently associated with establishment of nonindigenous insects. A large fraction of the nonindigenous invertebrates that became established in Hawaii are parthenogenic or hermaphroditic (Howarth
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Predicting Invasions of Nonindigenous Plants and Plant Pests 1985 cited in Simberloff 1989). In Europe, parthenogenic polyploid species of weevils have a much greater range than ancestral species that retain bisexual, diploid reproduction (Suomalainen et al. 1976), and several of these polyploid species have become established in North America. Parthenogenesis is more common among European than North American phytophagous insects and might partly explain the asymmetrical proportion of European invaders around the world. For example, roughly 40% of nonindigenous tree-feeding insects exhibit some form of parthenogenesis, compared with an estimated 11% of native tree-feeding insects in North America (Niemelä and Mattson 1996). Several parthenogenic insect taxa have been particularly invasive in North America. At least 45 species of Coccoidea scales are established on North American woody plants (Mattson et al. 1994, Niemelä and Mattson 1996); these scale insects are characterized by several types of parthenogenesis and collectively display the most diverse chromosome system of any animal group (Kosztarab 1987). All 60 of the nonindigenous sawfly species and all 23 aphid species established on North American trees and shrubs are parthenogenic (Smith 1993, Niemelä and Mattson 1996). At least 65% of the 33 nonindigenous species of bark beetles (in the family Scolytidae) are facultatively parthenogenic (Atkinson et al. 1990). Establishment of parasitic hymenopterans introduced for biological control is probably favored by reduced inbreeding depression arising from haplodiploidy and the ability to adjust sex ratio according to population density, host condition, or other factors (Simberloff 1989). Although parthenogenesis is associated with some insect invaders, this trait is not common to all invasive insect taxa. Niemelä and Mattson (1996) compiled data for eight dominant taxa of nonindigenous insect herbivores of woody plants established in North America. Two insect families—including leaf hoppers (Cicadellidae), plant bugs (Miridae), and one moth family (Tortricidae)—have no parthenogenic species. Thus, parthenogenesis or other forms of uniparental reproduction may contribute to the establishment of some taxa but not all. Rate of Population Growth The likelihood of establishment of nonindigenous insects has long been assumed to be related to the intrinsic rate of population growth, r. It has been argued that the relative amplitude (coefficient of variation) of a population’s fluctuations is the most important variable affecting the average lifetime of that population (Leigh 1981) and that a high r can reduce the chance of extinction in a founding population (Lawton and Brown 1986). In a review of biological control projects Crawley (1986) found that arthropods with high fecundity, short generation time, or female-biased sex ratios were more likely to establish than comparable arthropods with lower population growth rates. Pimm (1989) noted that across animal taxa, r is inversely correlated with individual longevity. He found that the combination of small body and high r was advantageous for the
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Predicting Invasions of Nonindigenous Plants and Plant Pests establishment of a founder population except at very low population densities (such as six pairs or fewer), when long-lived species would be expected to have a lower extinction rate. In two other studies, insects with small bodies and high r were found to be more likely to establish than insects with large bodies (Crawley 1986, Lawton and Brown 1986). Limitations in prediction arise, however, if estimates of r are used to predict the likelihood of establishment for a given arthropod species. One problem is that establishment can be linked to other life-history strategies. For example, in Crawley’s (1986) review of biological control introductions, insects with long-lived adult stages were found more likely to establish. Adult longevity presumably enabled oviposition to occur over a protracted period, increasing the probability that the nonindigenous arthropod would encounter suitable conditions for establishment. In addition, r is often considered on a relative or qualitative basis, and it is not clear how large it would need to be to enhance the probability of establishment. Furthermore, it is difficult to disassociate r from other traits, such as reproduction strategy, dispersal, and interactions with predators or other taxa in a new habitat. KEY FINDINGS The numerous factors identified in this chapter form a basis for predicting the establishment of a nonindigenous plant or plant pest. The degree of uncertainty in our ability to measure these factors depends on whether the identity of the immigrant is known, whether important information about its life history is available, and whether the circumstances of its introduction have been accurately assessed. Stochastic Forces The likelihood of establishment of nonindigenous plants and plant pests depends in part on the number of organisms that are introduced and the frequency of the introductions. Nonindigenous plants and plant pests typically arrive in small numbers and are vulnerable to demographic, environmental, and other stochastic forces that drive small populations to extinction. The chance of extinction due to demographic stochasticity is a function of the number of immigrants, their reproductive rate, and, if sexually reproducing, their success in finding mates. Populations of plants and arthropods of fewer than 50 individuals are highly vulnerable to extinction. Genetic bottlenecks, small size of the founder population, and strong directional selection on immigration can reduce the probability of establishment. Inbreeding in low-density populations can reduce the fitness of progeny. There are cases, however, where reduced heterozygosity resulting from a genetic bottleneck has enhanced the success of a nonindigenous species. Effects of such
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Predicting Invasions of Nonindigenous Plants and Plant Pests genetic changes can profoundly alter behavior and social organization and alter ecological interactions between nonindigenous and native species. Environmental stochasticity can reduce populations to the level at which demographic stochasticity becomes important. Models derived for plants suggest that when deterministic growth rates of newly arrived species exceed 1.2, effects of environmental stochasticity will be reduced and extinction will occur only as a result of extreme environmental events. Weather, the random expression of the amplitude of climate, is an important source of adverse environmental stochasticity. Natural catastrophes—such as fires, floods, and earthquakes—are difficult to predict but can cause the extirpation of populations of less than several thousand individuals. An Allee effect arising from low reproductive success or survival in low-density populations can strongly influence the ability of a newly arrived, nonindigenous species to persist. Whether a founder population persists or is driven to extinction can depend on the strength of this inverse density dependence, the population process that is subject to the Allee effect, and interactions with environmental stochasticity. Phenotypic plasticity, including acclimation, may buffer populations from environmental stochasticity. Human-generated disturbance can reduce populations to the point where demographic stochasticity causes extinction. But cultivation, whether deliberate or inadvertent, can promote persistence of nonindigenous plant pests by increasing resource availability and decreasing environmental stochasticity. Spatial distribution of newly arrived populations can affect the influence of stochastic forces. Small populations that are restricted to a specific habitat or host are more susceptible to extinction from stochastic forces than populations distributed across a large geographic area or populations that occupy multiple habitats or infest several hosts. Demographic, environmental, and other stochastic forces can be overcome by repeated introductions of a species that increase its population number, by introductions that spatially distribute the population, and by the life-history traits (such as diapause and dormancy) that minimize the consequences of stochasticity. Estimates (based on interception or other data) of the size of an immigrant population, the frequency of introduction, and opportunities for it to be introduced in multiple locations could be useful in determining the likelihood that a nonindigenous population will become established. Climate The geographic distribution and range of climates known to be suitable for the immigrant species in its native range or in previously invaded regions provide some indication of new habitats in which the immigrant population could
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Predicting Invasions of Nonindigenous Plants and Plant Pests persist. However, commodities that may harbor pests are often distributed from their initial entry point to other areas in the United States, which together encompass broad climatic variation (from arctic to generally tropical climates). Newly arrived organisms must be in seasonal synchrony with conditions in the new range. Nonindigenous organisms must enter and break diapause or dormancy at appropriate times. Among arthropod introductions in the Northern Hemisphere, species from northern latitudes that are introduced into southern latitudes may be more likely to become established than vice versa. Host Plants Availability of suitable host plants is a critical factor in the establishment of nonindigenous arthropods and pathogens. Taxonomic similarity (at the genus or even family level) between host plants of insects or pathogens in the native and new ranges increases likelihood of establishment, although this relationship requires further testing. Broad diet breadth may enhance the likelihood of a phytophagous arthropod’s establishment, especially if the flora in the new habitat is phylogenetically distant from flora in the native habitat. Most nonindigenous insects known to be established in North America, however, have specialized diets. Host plants must be temporally and spatially available to newly arriving nonindigenous insects and pathogens for their establishment in the new range. A vector is necessary for the establishment of some pathogens; in these cases, abundance, spatial distribution, and temporal availability of the vector will affect establishment. Natural Enemies and Competitors The presence of competitors and natural enemies in the new range of a nonindigenous plant or plant pest may prevent its establishment. Effects of these biotic forces on new species are difficult to predict, however, and often require detailed ecological information that is rarely available. Immigrant arthropods or pathogens without a morphological counterpart or close familial relative among the native species could have an advantage in establishment if native natural enemies do not attack them. Native insect predators are more likely than native parasitoids to prevent establishment of new arrivals of herbivorous insects. Effects of entomopathogens on new arrivals of insects are largely unknown. There is little evidence that competition with native species has prevented establishment of new arrivals of insects or pathogens, although this could theoretically occur. Competition, especially for light, can substantially affect the establishment of nonindigenous plants.
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Predicting Invasions of Nonindigenous Plants and Plant Pests Species Traits Selected life-history traits are frequently associated with persistent nonindigenous species and may be useful in predicting or assessing the likelihood of establishment of a given species. However, many exceptions occur for any given trait, and most can be evaluated only subjectively or qualitatively. Quantitative comparisons between the traits of species that have become established and the traits of species that have failed to establish are rare, especially for arthropods and pathogens. Nevertheless, there are traits that appear to enhance establishment, and these require much further study. The ability to change from outcrossing to selfing in response to local environmental conditions could optimize the opportunity for establishment. Species with high phenotypic plasticity among many ecologically important traits (for example, the traits collectively considered in connection with phenology) also have an advantage in a new environment. Possession of a resistant dormant phase, particularly a resistant seed bank, appears important, as do alternative forms of asexual and sexual reproduction, rapid growth, and high fecundity. Nonindigenous plant pathogens with genetic variability in traits associated with reproduction have a higher probability of establishment. Traits of plant pathogens that appear to enhance establishment include a short infection cycle, high productivity of infectious units, and a long infectious period. High intrinsic rate of increase, uniparental reproduction, and a dormant or resilient life stage that permits surviving temporally unfavorable conditions characterize many insect invaders. Other life-history strategies, such as long-lived adult stages, are common among established nonindigenous insects.
Representative terms from entire chapter: