Climate change can reduce the risk of biological invasion by reducing propagule size

Climate change has been conclusively linked to species extinctions, and to expansion and contractions and shifts of species ranges. Climate change is exerting similarly profound pressures on the individual stages of biological invasion which can significantly impact the biodiversity and ecology of invaded areas. Propagule pressure is perhaps the single most important determinant of invasion success, but the effects of climate change on propagule pressure are still largely uncertain because we have few observations of introduction events (or their size) that can be analyzed together with climate records. The common surrogate variables for propagule pressure do not logically respond to climate. Here I use a process-based simulation model to examine the potential effects of climate change (specifically temperature) on propagule size of a common invading insect species by estimating in-transit survivorship rate of propagules using historical and future (projected) temperatures and two common trade routes between a donor and a recipient location (Yokohama, Japan and Sydney, Australia). Propagule size (=the number of individuals in an introduction event) was lower under climate change temperatures than under historical temperatures in both routes. The route had significant effects on propagule size through its influence on the duration (and also the timing) of exposure to temperature conditions that are of time-sensitive importance to the development of the invasive species. Under historical temperatures propagule size was higher and less variable in the direct than the indirect route in 20 independent iterations. Under the future temperatures propagule size was also higher in the direct route but it was more variable than in the indirect route. Increased trade is increasing the opportunities for introductions, but the results reported here suggest that climate change will have inconsistent effects on biological invasion because of the complex relationship between temperature and insect ontogeny.     

Determinants of vertebrate invasion success in Europe and North America

Species that are frequently introduced to an exotic range have a high potential of becoming invasive. Besides propagule pressure, however, no other generally strong determinant of invasion success is known. Although evidence has accumulated that human affiliates (domesticates, pets, human commensals) also have high invasion success, existing studies do not distinguish whether this success can be completely explained by or is partly independent of propagule pressure. Here, we analyze both factors independently, propagule pressure and human affiliation. We also consider a third factor directly related to humans, hunting, and 17 traits on each species' population size and extent, diet, body size, and life history. Our dataset includes all 2362 freshwater fish, mammals, and birds native to Europe or North America. In contrast to most previous studies, we look at the complete invasion process consisting of (1) introduction, (2) establishment, and (3) spread. In this way, we not only consider which of the introduced species became invasive but also which species were introduced. Of the 20 factors tested, propagule pressure and human affiliation were the two strongest determinants of invasion success across all taxa and steps. This was true for multivariate analyses that account for intercorrelations among variables as well as univariate analyses, suggesting that human affiliation influenced invasion success independently of propagule pressure. Some factors affected the different steps of the invasion process antagonistically. For example, game species were much more likely to be introduced to an exotic continent than nonhunted species but tended to be less likely to establish themselves and spread. Such antagonistic effects show the importance of considering the complete invasion process.     

Propagule pressure and an invasion syndrome determine invasion success in a plant community model

The success of species invasions depends on multiple factors, including propagule pressure, disturbance, productivity, and the traits of native and non‐native species. While the importance of many of these determinants has already been investigated in relative isolation, they are rarely studied in combination. Here, we address this shortcoming by exploring the effect of the above‐listed factors on the success of invasions using an individual‐based mechanistic model. This approach enables us to explicitly control environmental factors (temperature as surrogate for productivity, disturbance, and propagule pressure) as well as to monitor whole‐community trait distributions of environmental adaptation, mass, and dispersal abilities. We simulated introductions of plant individuals to an oceanic island to assess which factors and species traits contribute to invasion success. We found that the most influential factors were higher propagule pressure and a particular set of traits. This invasion trait syndrome was characterized by a relative similarity in functional traits of invasive to native species, while invasive species had on average higher environmental adaptation, higher body mass, and increased dispersal distances, that is, had greater competitive and dispersive abilities. Our results highlight the importance in management practice of reducing the import of alien species, especially those that display this trait syndrome and come from similar habitats as those being managed.     

Decomposing propagule pressure: the effects of propagule size and propagule frequency on invasion success

Propagule pressure quantifies the inflow of individuals to a location and appears to be a key driver of invasion success. It is often defined as the average number of individuals introduced per time unit, or equivalently as the product of the average number of individuals introduced per introduction event (propagule size) and the frequency of introduction events (propagule frequency). Here we study how the influence of propagule size, frequency, and their product depends on the underlying ecological conditions. While previous studies have focused on introductions under environmental heterogeneity or a strong Allee effect, we examine a range of ecological scenarios that differ in the type of density dependence and in the sign of per capita growth rate. Our results indicate that the relative influence of propagule size and frequency depends mainly on the sign of per capita growth rate. Given a certain average number of individuals introduced per time unit, a high propagule frequency accelerates invasions under ecological scenarios with positive average per capita growth rate throughout the invasion process (‘easy’ scenarios). If per capita growth rate is negative throughout the invasion process (‘difficult’ scenarios) or if there is both an easy and a difficult stage (‘mixed scenarios’), a high propagule size leads to a faster invasion than a high propagule frequency. To explain this finding, we argue that for a fixed value of the product of propagule size and frequency, an increase in propagule size leads to an increase in demographic variance, which promotes invasion success in difficult and mixed but not in easy scenarios. However, we also show that in many of these cases, the product of propagule size and frequency still correlates more strongly with invasion success than either of the single components. Finally, we illustrate our approach with empirical examples from the literature.     

The more you introduce the more you get: the role of colonization pressure and propagule pressure in invasion ecology

Aim  We argue that 'propagule pressure', a key term in invasion biology, has been attributed at least three distinct definitions (with usage of a related term causing additional confusion). All of the definitions refer to fundamental concepts within the invasion process, with the result that the distinct importance of these different concepts has been at best diluted, and at worst lost.
Location  Global.
Methods  We reviewed pertinent literature on propagule pressure to resolve confusion about different uses of the term 'propagule pressure' and we introduced a new term for one variant, colonization pressure. We conducted a computer simulation whereby the introduction of species is represented as a simple sampling process to elucidate the relationship between propagule and colonization pressure.
Results  We defined colonization pressure as the number of species introduced or released to a single location, some of which will go on to establish a self-sustaining population and some of which will not. We subsequently argued that colonization pressure should serve as a null hypothesis for understanding temporal or spatial differences in exotic species richness, as the more species that are introduced, the more we should expect to establish. Finally, using a simple simulation, we showed that propagule pressure is related to colonization pressure, but in a non-linear manner.
Main conclusion  We suggest that the nature of the relationship between propagule pressure and colonization pressure, as well as the efficacy of various proxy measures of each, require more detailed exploration if invasion ecology is to continue to develop into a more predictive science.     

Propagule pressure and native community connectivity interact to influence invasion success in metacommunities

Mechanistic insights from invasion biology indicate that propagule pressure of exotic species and native community structure can independently influence establishment success. The role of native community connectivity via species dispersal and its potential interaction with propagule pressure on invasion success in metacommunities, however, remains unknown. Native community connectivity may increase biotic resistance to invasion by enhancing species richness and evenness, but the effects could depend upon the level of propagule pressure. In this study, a mesocosm experiment was used to evaluate the independent and combined effects of exotic propagule pressure and native community connectivity on invasion success. The effects of three levels of exotic Daphnia lumholtzi propagule pressure on establishment success, community structure and ecosystem attributes were evaluated in native zooplankton communities connected by species dispersal versus unconnected communities, and relative to a control without native species. Establishment of the exotic species exhibited a propagule dose‐dependent relationship with high levels of propagule pressure resulting in the greatest establishment success. Native community connectivity, however, effectively reduced establishment at the low level of propagule pressure and further augmented native species richness across propagule pressure treatments. Propagule pressure largely determined the negative impacts of the exotic species on native species richness, native biomass and edible producer biomass. The results highlight that native community connectivity can reduce invasion success at a low propagule dose and decrease extinction risk of native competitors, but high propagule pressure can overcome connectivity‐mediated biotic resistance to influence establishment and impact of the exotic species. Together, the results emphasize the importance of the interaction of propagule pressure and community connectivity as a regulator of invasion success, and argue for the maintenance of metacommunity connectivity to confer invasion resistance.     

Phylogeographic insights into the invasion history and secondary spread of the signal crayfish in Japan

Successful invasion by nonindigenous species is often attributed to high propagule pressure, yet some foreign species become widespread despite showing reduced genetic variation due to founder effects. The signal crayfish (Pacifastacus leniusculus) is one such example, where rapid spread across Japan in recent decades is believed to be the result of only three founding populations. To infer the history and explore the success of this remarkable crayfish invasion, we combined detailed phylogeographical and morphological analyses conducted in both the introduced and native ranges. We sequenced 16S mitochondrial DNA of signal crayfish from across the introduced range in Japan (537 samples, 20 sites) and the native range in western North America (700 samples, 50 sites). Because chela size is often related to aggressive behavior in crayfish, and hence, their invasion success, we also measured chela size of a subset of specimens in both introduced and native ranges. Genetic diversity of introduced signal crayfish populations was as high as that of the dominant phylogeographic group in the native range, suggesting high propagule pressure during invasion. More recently established crayfish populations in Japan that originated through secondary spread from one of the founding populations exhibit reduced genetic diversity relative to older populations, probably as a result of founder effects. However, these newer populations also show larger chela size, consistent with expectations of rapid adaptations or phenotypic responses during the invasion process. Introduced signal crayfish populations in Japan originate from multiple source populations from a wide geographic range in the native range of western North America. A combination of high genetic diversity, especially for older populations in the invasive range, and rapid adaptation to colonization, manifested as larger chela in recent invasions, likely contribute to invasion success of signal crayfish in Japan.     

Parsing propagule pressure: Number,not size,of introductions drives colonization success in a novel environment

Predicting whether individuals will colonize a novel habitat is of fundamental ecological interest and is crucial to conservation efforts. A consistently supported predictor of colonization success is the number of individuals introduced, also called propagule pressure. Propagule pressure increases with the number of introductions and the number of individuals per introduction (the size of the introduction), but it is unresolved which process is a stronger driver of colonization success. Furthermore, their relative importance may depend upon the environment, with multiple introductions potentially enhancing colonization of fluctuating environments. To evaluate the relative importance of the number and size of introductions and its dependence upon environmental variability, we paired demographic simulations with a microcosm experiment. Using Tribolium flour beetles as a model system, we introduced a fixed number of individuals into replicated novel habitats of stable or fluctuating quality, varying the number of introductions through time and size of each introduction. We evaluated establishment probability and the size of extant populations through seven generations. We found that establishment probability generally increased with more, smaller introductions, but was not affected by biologically realistic fluctuations in environmental quality. Population size was not significantly affected by environmental variability in the simulations, but populations in the microcosms grew larger in a stable environment, especially with more introduction events. In general, the microcosm experiment yielded higher establishment probability and larger populations than the demographic simulations. We suggest that genetic mechanisms likely underlie these differences and thus deserve more attention in efforts to parse propagule pressure. Our results highlight the importance of preventing further introductions of undesirable species to invaded sites and suggest conservation efforts should focus on increasing the number of introductions or reintroductions of desirable species rather than increasing the size of those introduction events into harsh environments.     

Saving camels from straws: how propagule pressure-based prevention policies can reduce the risk of biological invasion

Nonnative species that harm or have the potential to cause harm to the environment, economy, or human health are known as invasive species. Propagule pressure may be the most important factor in establishment success of nonnative species of various taxa in a variety of ecosystems worldwide, and strong evidence is emerging that propagule pressure determines both the scale of invasion extent and impact. In a limited way, the US government is applying a “propagule pressure approach” in a variety of prevention policy contexts aimed at minimizing the impact of harmful organisms. However, there are also readily apparent opportunities for enacting propagule pressure-based measures to fill current gaps in invasive species prevention and control at national, state, and local levels. An explicit focus on propagule pressure-based policies could substantially increase the effectiveness of US efforts to prevent the introduction of invasive species through by intentional and unintentional introductions. The views expressed in this paper are solely those of the authors and do not necessarily reflect those of the US government. “As the last straw breaks the laden camel’s back...” -Charles Dickens, Dombey and Son     

Propagule pressure hypothesis not supported by an 80‐year experiment on woody species invasion

Ecological filters and availability of propagules play key roles structuring natural communities. Propagule pressure has recently been suggested to be a fundamental factor explaining the success or failure of biological introductions. We tested this hypothesis with a remarkable data set on trees introduced to Isla Victoria, Nahuel Huapi National Park, Argentina. More than 130 species of woody plants, many known to be highly invasive elsewhere, were introduced to this island early in the 20th century, as part of an experiment to test their suitability as commercial forestry trees for this region. We obtained detailed data on three estimates of propagule pressure (number of introduced individuals, number of areas where introduced, and number of years during which the species was planted) for 18 exotic woody species. We matched these data with a survey of the species and number of individuals currently invading the island. None of the three estimates of propagule pressure predicted the current pattern of invasion. We suggest that other factors, such as biotic resistance, may be operating to determine the observed pattern of invasion, and that propagule pressure may play a relatively minor role in explaining at least some observed patterns of invasion success and failure.     

Strength in size not numbers: propagule size more important than number in sexually reproducing populations

Propagule pressure has consistently been identified as a primary factor in invader success, and reducing it can be one of the most effective methods for preventing the establishment of non-native species. However, when policy is implemented to reduce propagule pressure it almost exclusively focuses on the size of individual introduction events (‘propagule size’), with little confirmation that controlling this single aspect of propagule pressure is the most effective strategy. The number of introduction events (‘propagule number’) can play as much, or more, of a role in invader success, yet only a small portion of propagule pressure research has studied the relative importance of size and number. We investigated the relative roles of propagule size and number in the establishment of a sexually reproducing species using a field mesocosm experiment that introduced Hemimysis anomala (a non-native mysid) across a range of propagule sizes and numbers. We found that single, large introductions had higher abundances and probabilities of survival than smaller, more frequent additions. This experiment illustrated that, for sexual reproducers, focusing on lowering propagule size can be the most effective method for reducing non-native establishment.     

Minimum threshold for establishment and dispersal of Lilioceris cheni (Coleoptera: Chrysomelidae): a biological control agent of Dioscorea bulbifera

The successful establishment or failure of a new population is often attributed to propagule pressure, the combination of the number of independent introduction events, and the number of individuals released at each event. The design of optimal release strategies for biological control agents benefits from an understanding of the impact of propagule pressure on the species being released. The dispersal rate of individuals from nascent population foci can also affect establishment success. We assessed the minimum threshold for establishment and measured dispersal of Lilioceris cheni (Coleoptera: Chrysomelidae), a biological control agent for Dioscorea bulbifera (Dioscoreales), air potato. Replicated releases of 10, 50, and 100 adults of L. cheni were conducted on the east and west coasts of south Florida. Dispersal was measured from 19 of these sites plus 19 additional release locations in south and central Florida. Lilioceris cheni established populations from all three release sizes with no apparent influence of site location. Releases of 10, 50, and 100 adults resulted in 50%, 67%, and 85% establishment, respectively. Beetles dispersed an average of 1.41?±?0.515?km/yr. Dispersal distance was significantly affected by the time since release but not the number of individuals released. Our results suggest that future releases of 100 individuals could be spaced several kilometres apart on the landscape to facilitate rapid colonisation of D. bulbifera infestations.     

Population genetics reveals origin and number of founders in a biological invasion

Propagule pressure is considered the main determinant of success of biological invasions: when a large number of individuals are introduced into an area, the species is more likely to establish and become invasive. Nevertheless, precise data on propagule pressure exist only for a small sample of invasive species, usually voluntarily introduced. We studied the invasion of the American bullfrog, Rana catesbeiana, into Europe, a species that is considered a major cause of decline for native amphibians. For this major invader with scarce historical data, we used population genetics data (a partial sequence of the mitochondrial cytochrome b gene) to infer the invasion history and to estimate the number of founders of non-native populations. Based on differences between populations, at least six independent introductions from the native range occurred in Europe, followed by secondary translocations. Genetic diversity was strongly reduced in non-native populations, indicating a very strong bottleneck during colonization. We used simulations to estimate the precise number of founders and found that most non-native populations derive from less than six females. This capability of invasion from a very small number of propagules challenges usual management strategies; species with such ability should be identified at an early stage of introduction.     

Risk analysis of the invasion pathway of the Asian gypsy moth: a known forest invader

Risk is defined with many minor variations in the biological literature. Common to most definitions are the following elements: the probability of a future event; and the consequences of the event, usually with respect to some predefined human value. Risk analysis includes elements of risk assessment (quantification of risk), uncertainty (of the event and its consequences), risk management (reducing risk to an acceptable level), and development of policy to balance finite resources with uncertainty and risk tolerance. When biological invasion and its risk are jointly examined, it is common that the consequences of invasion are not explicitly quantified, but understood to be sufficiently negative that it must be minimized to the extent possible. Risk analysis then becomes quantification of the probabilities of an introduction (event) and that the introduction leads to establishment, and the uncertainty of those probabilities. I describe a risk analysis framework for the Asian gypsy moth—a known invader—in its pathway. The framework uses the available information regarding the transportation route of the vector (ships), and a phenology model that estimates vector contamination (propagule size), the probability of introduction, and the probability of initial establishment given an introduction. Reducing propagule pressure is arguably the most important factor in reducing biological invasion; propagule pressure can be reduced by inspection and sanitation of the pathway vector (e.g., ships, trucks, humans) at the point(s) of departure and at the point of entry. I demonstrate how the risk analysis framework can be used to more efficiently target incoming ships for inspection and propagule pressure reduction.     

Successful biological invasion despite a severe genetic load

Understanding the factors that influence the success of ecologically and economically damaging biological invasions is of prime importance. Recent studies have shown that invasive populations typically exhibit minimal, if any, reductions in genetic diversity, suggesting that large founding populations and/or multiple introductions are required for the success of biological invasions, consistent with predictions of the propagule pressure hypothesis. Through population genetic analysis of neutral microsatellite markers and a gene experiencing balancing selection, we demonstrate that the solitary bee Lasioglossum leucozonium experienced a single and severe bottleneck during its introduction from Europe. Paradoxically, the success of L. leucozonium in its introduced range occurred despite the severe genetic load caused by single-locus complementary sex-determination that still turns 30% of female-destined eggs into sterile diploid males, thereby substantially limiting the growth potential of the introduced population. Using stochastic modeling, we show that L. leucozonium invaded North America through the introduction of a very small number of propagules, most likely a singly-mated female. Our results suggest that chance events and ecological traits of invaders are more important than propagule pressure in determining invasion success, and that the vigilance required to prevent invasions may be considerably greater than has been previously considered.     

Relationship between propagule pressure and colonization pressure in invasion ecology: a test with ships' ballast

Increasing empirical evidence indicates the number of released individuals (i.e. propagule pressure) and number of released species (i.e. colonization pressure) are key determinants of the number of species that successfully invade new habitats. In view of these relationships, and the possibility that ships transport whole communities of organisms, we collected 333 ballast water and sediment samples to investigate the relationship between propagule and colonization pressure for a variety of diverse taxonomic groups (diatoms, dinoflagellates and invertebrates). We also reviewed the scientific literature to compare the number of species transported by ships to those reported in nature. Here, we show that even though ships transport nearly entire local communities, a strong relationship between propagule and colonization pressure exists only for dinoflagellates. Our study provides evidence that colonization pressure of invertebrates and diatoms may fluctuate widely irrespective of propagule pressure. We suggest that the lack of correspondence is explained by reduced uptake of invertebrates into the transport vector and the sensitivity of invertebrates and diatoms to selective pressures during transportation. Selection during transportation is initially evident through decreases in propagule pressure, followed by decreased colonization pressure in the most sensitive taxa.     

Allee Effects, Propagule Pressure and the Probability of Establishment: Risk Analysis for Biological Invasions

Colonization is of longstanding interest in theoretical ecology and biogeography, and in the management of weeds and other invasive species, including insect pests and emerging infectious diseases. Due to accelerating invasion rates and widespread economic costs and environmental damages caused by invasive species, colonization theory has lately become a matter of considerable interest. Here we review the concept of propagule pressure to inquire if colonization theory might provide quantitative tools for risk assessment of biological invasions. By formalizing the concept of propagule pressure in terms of stochastic differential equation models of population growth, we seek a synthesis of invasion biology and theoretical population biology. We focus on two components of propagule pressure that affect the chance of invasion: (1) the number of individuals initially introduced, and (2) the rate of subsequent immigration. We also examine how Allee effects, which are expected to be common in newly introduced populations, may inhibit establishment of introduced propagules. We find that the establishment curve (i.e., the chance of invasion as a function of initial population size), can take a variety of shapes depending on immigration rate, carrying capacity, and the severity of Allee effects. Additionally, Allee effects can cause the stationary distribution of population sizes to be bimodal, which we suggest is a possible explanation for time lags commonly observed between the detection of an introduced population and widespread invasion of the landscape.     

Hotspots of plant invasion predicted by propagule pressure and ecosystem characteristics

Aim Biological invasions pose a major conservation threat and are occurring at an unprecedented rate. Disproportionate levels of invasion across the landscape indicate that propagule pressure and ecosystem characteristics can mediate invasion success. However, most invasion predictions relate to species’ characteristics (invasiveness) and habitat requirements. Given myriad invaders and the inability to generalize from single‐species studies, more general predictions about invasion are required. We present a simple new method for characterizing and predicting landscape susceptibility to invasion that is not species‐specific. Location Corangamite catchment (13,340 km²), south‐east Australia. Methods Using spatially referenced data on the locations of non‐native plant species, we modelled their expected proportional cover as a function of a site’s environmental conditions and geographic location. Models were built as boosted regression trees (BRTs). Results On average, the BRTs explained 38% of variation in occupancy and abundance of all exotic species and exotic forbs. Variables indicating propagule pressure, human impacts, abiotic and community characteristics were rated as the top four most influential variables in each model. Presumably reflecting higher propagule pressure and resource availability, invasion was highest near edges of vegetation fragments and areas of human activity. Sites with high vegetation cover had higher probability of occupancy but lower proportional cover of invaders, the latter trend suggesting a form of biotic resistance. Invasion patterns varied little in time despite the data spanning 34 years. Main conclusions To our knowledge, this is the first multispecies model based on occupancy and abundance data used to predict invasion risk at the landscape scale. Our approach is flexible and can be applied in different biomes, at multiple scales and for different taxonomic groups. Quantifying general patterns and processes of plant invasion will increase understanding of invasion and community ecology. Predicting invasion risk enables spatial prioritization of weed surveillance and control.     

Can model species be used to advance the field of invasion ecology?

Hypotheses for explaining plant invasions have focused on a variety of factors that may influence invasion success, including propagule pressure, interactions of the introduced species with the biotic, abiotic, or disturbance properties of the new ecosystem, or the genetic characteristics of the invader itself. Evaluating the relative importance of these factors has been difficult because for most invaders key information about the introduced population or the introduction event is not available. We propose that natural experiments using model species is an important tool to test multiple invasion hypotheses at the same time, providing a complementary approach to meta-analysis and literature review. By focusing on a single candidate species, Pinus contorta, we explore several attributes that we propose constitute a good model, including: (a) intentional and relatively well documented introduction into a wide range of environments and countries across the world during the past century, where invasion success or failure has already occurred, (b) conspicuous growth form that simplifies assessment of growth rates, and comparisons across native and introduced ecosystems around the world, and, (c) documented and replicated variability of introduction intensity, genetic characteristics of the introduced populations, contrasting biotic communities present at sites of introduction, and abiotic conditions within and across introduced ecosystems. We propose that identifying model species with these characteristics will provide opportunities to disentangle the relative importance of different mechanisms hypothesized to influence invasion success, and thereby advance the field of invasion ecology.