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.     

Economics of invasive species policy and management

This article examines the use of economic analysis to inform bioinvasion management, with particular focus on forest resources. Economics is key for understanding invasion processes, impacts, and decision-making. Biological invasions are driven by and affect economic activities at multiple scales and stages of an invasion. Bioeconomic modeling seeks to inform how resources can be optimally allocated across invasion management activities—including prevention, surveillance programs for early detection and management, and controlling invasion populations and spread—to minimize the long-term costs and damages. Economic analysis facilitates understanding of decisions by public and private decision-makers, gaps between these, and the design of policies to achieve socially desirable outcomes. Private decision-makers may undercontrol invasions relative to socially optimal levels, because they generally account for their own costs and benefits of control but less often for broader ecosystem impacts or future spread across the landscape. Economic analysis considers approaches for increasing private invasion management and evaluates feedbacks between ecological and economic systems that can affect policy outcomes. Future research should continue evaluation and design of control strategies across the biosecurity continuum and across species to enhance cost-effectiveness, better incorporate uncertainty into policy design, increase focus on incentives and behavioral tools to influence private behaviors that affect invasion spread, and incorporate invasive species consideration within broader systems-focused science. In addition, challenges in valuing biodiversity and ecosystem service impacts and the costs and effectiveness of control measures are key data gaps. Greater collaboration between decision-makers and researchers will facilitate development and communication of usable economic research.     

Optimal surveillance strategy for invasive species management when surveys stop after detection

Invasive species are a cause for concern in natural and economic systems and require both monitoring and management. There is a trade‐off between the amount of resources spent on surveying for the species and conducting early management of occupied sites, and the resources that are ultimately spent in delayed management at sites where the species was present but undetected. Previous work addressed this optimal resource allocation problem assuming that surveys continue despite detection until the initially planned survey effort is consumed. However, a more realistic scenario is often that surveys stop after detection (i.e., follow a “removal” sampling design) and then management begins. Such an approach will indicate a different optimal survey design and can be expected to be more efficient. We analyze this case and compare the expected efficiency of invasive species management programs under both survey methods. We also evaluate the impact of mis‐specifying the type of sampling approach during the program design phase. We derive analytical expressions that optimize resource allocation between monitoring and management in surveillance programs when surveys stop after detection. We do this under a scenario of unconstrained resources and scenarios where survey budget is constrained. The efficiency of surveillance programs is greater if a “removal survey” design is used, with larger gains obtained when savings from early detection are high, occupancy is high, and survey costs are not much lower than early management costs at a site. Designing a surveillance program disregarding that surveys stop after detection can result in an efficiency loss. Our results help guide the design of future surveillance programs for invasive species. Addressing program design within a decision‐theoretic framework can lead to a better use of available resources. We show how species prevalence, its detectability, and the benefits derived from early detection can be considered.     

Plantlet recruitment is the key demographic transition in invasion by Kalanchoe daigremontiana

Biological invasions have a great impact on biodiversity and ecosystem functioning worldwide. Kalanchoe daigremontiana is a noxious invasive plant in arid zones. Besides being toxic for domestic animals and wildlife, this species inhibits the growth of native plants. Its rapid proliferation in Cerro Saroche National Park (Venezuela) is of great concern because this area hosts several species endemic to the scarce arid zones in the Caribbean. The traits of K. daigremontiana that contribute to its invasive success are unknown. Based on empirical data, we derived a stage structured, stochastic and density-dependent model, to identify characteristics relevant for its establishment. Sensitivity analyses revealed that the establishment of K. daigremontiana depends exclusively on plantlet recruitment. Because asexual plantlets reproduce in less than 1 year populations are able to increase rapidly during the initial phases of invasion, when extinction risks are higher. Sexual seedlings, on the contrary, require a minimum of 3 years to reproduce. As a result, seedling recruitment contributes little to the transient dynamics of the population and therefore cannot warrant the successful establishment of the species. Simulations of various management strategies show that eradication through plant removal may only be achieved if harvest begins shortly after introduction. If a rapid response is not possible, reducing the survival and growth rates of plantlets through biological control is an alternative option. Thus, a strict control of dispersal of plantlets by humans and a continuous monitoring of new invasions should be the first priority for reducing further impact on native species.     

Mating system,population growth,and management scenario for Kalanchoe pinnata in an invaded seasonally dry tropical forest

Ecological invasions are a major issue worldwide, where successful invasion depends on traits that facilitate dispersion, establishment, and population growth. The nonnative succulent plant Kalanchoe pinnata, reported as invasive in some countries, is widespread in remnants of seasonally dry tropical forest on a volcanic outcrop with high conservation value in east‐central Mexico where we assessed its mating system and demographic growth and identified management strategies. To understand its local mating system, we conducted hand‐pollination treatments, germination, and survival experiments. Based on the experimental data, we constructed a life‐stage population matrix, identified the key traits for population growth, weighted the contributions of vegetative and sexual reproduction, and evaluated management scenarios. Hand‐pollination treatments had slight effects on fruit and seed setting, as well as on germination. With natural pollination treatment, the successful germination of seeds from only 2/39 fruit suggests occasional effective natural cross‐pollination. The ratios of the metrics for self‐ and cross‐pollinated flowers suggest that K. pinnata is partially self‐compatible. Most of the pollinated flowers developed into fruit, but the seed germination and seedling survival rates were low. Thus, vegetative propagation and juvenile survival are the main drivers of population growth. Simulations of a virtual K. pinnata population suggest that an intense and sustained weeding campaign will reduce the population within at least 10 years. Synthesis and applications. The study population is partially self‐compatible, but sexual reproduction by K. pinnata is limited at the study site, and population growth is supported by vegetative propagation and juvenile survival. Demographic modeling provides key insights and realistic forecasts on invasion process and therefore is useful to design management strategies.     

An Iterative and Targeted Sampling Design Informed by Habitat Suitability Models for Detecting Focal Plant Species over Extensive Areas

Prioritizing areas for management of non-native invasive plants is critical, as invasive plants can negatively impact plant community structure. Extensive and multi-jurisdictional inventories are essential to prioritize actions aimed at mitigating the impact of invasions and changes in disturbance regimes. However, previous work devoted little effort to devising sampling methods sufficient to assess the scope of multi-jurisdictional invasion over extensive areas. Here we describe a large-scale sampling design that used species occurrence data, habitat suitability models, and iterative and targeted sampling efforts to sample five species and satisfy two key management objectives: 1) detecting non-native invasive plants across previously unsampled gradients, and 2) characterizing the distribution of non-native invasive plants at landscape to regional scales. Habitat suitability models of five species were based on occurrence records and predictor variables derived from topography, precipitation, and remotely sensed data. We stratified and established field sampling locations according to predicted habitat suitability and phenological, substrate, and logistical constraints. Across previously unvisited areas, we detected at least one of our focal species on 77% of plots. In turn, we used detections from 2011 to improve habitat suitability models and sampling efforts in 2012, as well as additional spatial constraints to increase detections. These modifications resulted in a 96% detection rate at plots. The range of habitat suitability values that identified highly and less suitable habitats and their environmental conditions corresponded to field detections with mixed levels of agreement. Our study demonstrated that an iterative and targeted sampling framework can address sampling bias, reduce time costs, and increase detections. Other studies can extend the sampling framework to develop methods in other ecosystems to provide detection data. The sampling methods implemented here provide a meaningful tool when understanding the potential distribution and habitat of species over multi-jurisdictional and extensive areas is needed for achieving management objectives.     

Integrating spread dynamics and economics of timber production to manage Chinese tallow invasions in southern U.S. forestlands

Economic costs associated with the invasion of nonnative species are of global concern. We estimated expected costs of Chinese tallow (Triadica sebifera (L.) Small) invasions related to timber production in southern U.S. forestlands under different management strategies. Expected costs were confined to the value of timber production losses plus costs for search and control. We simulated management strategies including (1) no control (NC), and control beginning as soon as the percentage of invaded forest land exceeded (2) 60 (Low Control), (3) 25 (Medium Control), or (4) 0 (High Control) using a spatially-explicit, stochastic, bioeconomic model. With NC, simulated invasions spread northward and westward into Arkansas and along the Gulf of Mexico to occupy ≈1.2 million hectares within 20 years, with associated expected total costs increasing exponentially to ≈$300 million. With LC, MC, and HC, invaded areas reached ≈275, 34, and 2 thousand hectares after 20 years, respectively, with associated expected costs reaching ≈$400, $230, and $200 million. Complete eradication would not be cost-effective; the minimum expected total cost was achieved when control began as soon as the percentage of invaded land exceeded 5%. These results suggest the importance of early detection and control of Chinese tallow, and emphasize the importance of integrating spread dynamics and economics to manage invasive species.     

Cross-scale management strategies for optimal control of trees invading from source plantations

Biological invasion by non-native tree species can transform landscapes, and as a consequence, has received growing attention from researchers and managers alike. This problem is driven primarily by the naturalisation and invasion of tree species escaping from cultivation or forestry plantations. Furthermore, these invasions can be strongly influenced by the land-use matrix of the surrounding region, specific management of the source populations, and environmental conditions that influence seed dispersal or habitat quality for the invader. A major unresolved challenge for managing tree invasions in landscapes is how management should be deployed to contain or slow the spread of invading populations from one or more sources (e.g. plantations). We develop a spatial simulation model to test: (1) how to best prioritise the control of invasive tree populations spatially to slow or contain the biological invader when habitat quality varies in the landscape, and (2) how to allocate control effort among different management units when trees spread from many source populations. We first show that to slow down spread effectively, management strategy is less important than management effort. We then identify the conditions affecting the relative performance of different management strategies. At the landscape scale, targeting peripheral stands consistently yielded the best results whereas at the regional scale, management strategies needed to account for both habitat quality and tree life-history. Overall, our findings demonstrate that knowledge of how habitat affects tree life-history stages can improve management to contain or slow tree invasions by improving the spatial match between management effort and efficacy.     

Invasion dynamics of round goby (<Emphasis Type="Italic">Neogobius melanostomus</Emphasis>) in Hamilton Harbour,Lake Ontario

Most introduced non-native species fail to establish as a result of mortality or reproductive failure. An established population can increase the probability of survival and reproductive success of newly introduced individuals by reducing both Allee effects and demographic stochasticity. Previously, attention has been paid to the establishment phase of the invasion process and its probability modelled as a stochastic process, while the spread phase has received less attention. By analyzing data collected during the spread phase of an invasion of the round goby, Neogobius melanostomus, in Hamilton Harbour, Lake Ontario, we develop an analytical approach to backcalculate the time to establishment and to determine the time to habitat saturation. Our modelling shows that: (1) during the transition between arrival and establishment, propagule pressure in the form of new adults entering the area can be very low and still represent a significant probability of establishment; (2) much higher concentrations of juveniles would be needed to pose a significant risk of invasion; (3) the demographic contribution of propagule pressure during the spread phase is low and its total elimination will not halt population growth and spread; (4) a short elapsed time between arrival and establishment indicated that the transition between these two phases can be characterized as a deterministic process with high propagule pressure and low adult mortality rates; and, (5) very aggressive management actions would be needed to halt population growth after population establishment, suggesting that preventative measures are the most effective management options available to reduce risk of future invasions.     

动物入侵的行为机制

行为特征可在外来动物建立种群和扩张过程中发挥重要作用,因此,要正确理解动物入侵,常常需要仔细研究其行为机制。20世纪80年代以来,随着动物入侵规模在世界各地的迅速加剧,有关其行为机制的研究也受到了广泛关注。最近一些研究表明,一些入侵动物种内攻击和觅食等行为具有可塑性,因此它们能够灵活应对多变的环境条件,这对于种群的建立和维持至关重要;入侵动物与土著物种发生行为互作时,往往占据优势,从而取代土著物种,并有助于其地域扩张;入侵动物长距离扩散可以提高其地域扩张速度,许多行为可与扩散行为结合进一步促进扩张。今后需要加强对入侵动物的行为分析,使之全面地融合到生物入侵的研究之中。这不仅可以提高对外来物种入侵的预警和治理能力,而且为探索动物行为的奥秘以及动物间行为互作在物种进化中的意义提供了独特的机会。     

Invasion speeds in fluctuating environments

Biological invasions are increasingly frequent and have dramatic ecological and economic consequences. A key to coping with invasive species is our ability to predict their rates of spread. Traditional models of biological invasions assume that the environment is temporally constant. We examine the consequences for invasion speed of periodic and stochastic fluctuations in population growth rates and in dispersal distributions.     

Demographic Stochasticity, Environmental Variability, and Windows of Invasion Risk for Bythotrephes Longimanus in North America

Biological invasions are a leading threat to freshwater biodiversity worldwide. A central unanswered question of invasion ecology is why some introduced populations establish while most fail. Answering this question will allow resource managers to increase the specificity and effectiveness of control efforts and policy. We studied the establishment of spiny water flea (Bythotrephes longimanus) in the United States and Canada by modeling introduction failure caused by demographic stochasticity, environmental variation, and seasonal environmental forcing. We compared predicted establishment rates with observed invasions of inland lakes in Ontario, Canada. Our findings suggest that environmental forcing can cause “windows” of invasion opportunity so that timing of introductions might be a greater determinant of population establishment than demographic stochasticity and random environmental variation. We expect this phenomenon to be exhibited by species representing a wide range of life histories. For spiny water flea in North America, a large window of invasion opportunity opens around the fourth week of May, persists through the summer, and closes with decreasing water temperatures in autumn. These results show how timing of introductions with respect to seasonally forced environmental drivers can be a key determinant of establishment success. By focusing on introductions during windows of invasion opportunity, resource managers can more effectively control invasion rates.     

Sampling inspection to prevent the invasion of alien pests: statistical theory of import plant quarantine systems in Japan

The establishment of appropriate import quarantine systems is the best known method for preventing the unintentional introduction of invasive alien pests. However, quarantine systems are sometimes judged as non-tariff barriers against trade by the World Trade Organization. The construction of a common scientific theory for quarantine systems is thus extremely important to prevent invasion without causing international conflict. We explain several statistical theories that have been adopted in import plant quarantine systems in Japan. Quarantine systems include three major components: (1) import sampling inspection, (2) early detection procedures, and (3) emergency control. We first explain the principle of risk management that was commonly adopted in these components. Then, we explain the method for calculating the required sample size in the import sampling inspection. We then explain hierarchical sampling inspection for detecting alien pests inside Japan. We further explain the theory for declaring the eradication of invasive alien pests as an emergency control. Actual examples of quarantine actions against the invasion of plum pox virus disease and citrus huanglongbing are discussed.     

Dynamic expansion in recently introduced populations of fire ant parasitoids (Diptera: Phoridae)

Combating invasive species requires a detailed, mechanistic understanding of the manner and speed with which organisms expand their ranges. Biological control efforts provide an opportunity to study the process of species invasions and range expansions under known initial conditions. This study examines the rate, pattern and mechanisms of spread for two populations of the biological control agent Pseudacteon tricuspis, phorid-fly parasitoids of imported fire ants. We employ a trap-based survey method that detects phorid flies in low-density populations, and provides data on abundance. This technique allows us to differentiate between continuous population spread and effective long-distance dispersal and to examine density gradients of phorid flies across the expanding population front. We find that occupied sites in front of the leading edge of continuous populations were common; forming small populations we refer to as satellite populations. Satellite populations are tens of kilometers from the nearest possible source. Wind governs the dynamics of spread in these two central Texas populations. Population edges expanding with the wind exhibited a higher frequency of effective long-distance dispersal than did populations expanding into the wind. This enhanced effective long-distance dispersal rate translated into a five times faster rate of spread for population edges traveling with the wind. This planned invasion shares many characteristics in common with unplanned species invasions including: protracted establishment phase during which densities were below detection thresholds, and slow initial spread immediately after establishment followed by rapid, accelerating spread rates as population sizes grew.     

The vulnerability of habitats to plant invasion: disentangling the roles of propagule pressure,time and sampling effort

Aim To quantify the vulnerability of habitats to invasion by alien plants having accounted for the effects of propagule pressure, time and sampling effort. Location New Zealand. Methods We used spatial, temporal and habitat information taken from 9297 herbarium records of 301 alien plant species to examine the vulnerability of 11 terrestrial habitats to plant invasions. A null model that randomized species records across habitats was used to account for variation in sampling effort and to derive a relative measure of invasion based either on all records for a species or only its first record. The relative level of invasion was related to the average distance of each habitat from the nearest conurbation, which was used as a proxy for propagule pressure. The habitat in which a species was first recorded was compared to the habitats encountered for all records of that species to determine whether the initial habitat could predict subsequent habitat occupancy. Results Variation in sampling effort in space and time significantly masked the underlying vulnerability of habitats to plant invasions. Distance from the nearest conurbation had little effect on the relative level of invasion in each habitat, but the number of first records of each species significantly declined with increasing distance. While Urban, Streamside and Coastal habitats were over‐represented as sites of initial invasion, there was no evidence of major invasion hotspots from which alien plants might subsequently spread. Rather, the data suggest that certain habitats (especially Roadsides) readily accumulate alien plants from other habitats. Main conclusions Herbarium records combined with a suitable null model provide a powerful tool for assessing the relative vulnerability of habitats to plant invasion. The first records of alien plants tend to be found near conurbations, but this pattern disappears with subsequent spread. Regardless of the habitat where a species was first recorded, ultimately most alien plants spread to Roadside and Sparse habitats. This information suggests that such habitats may be useful targets for weed surveillance and monitoring.     

Increased population growth rate in invasive polyploid Centaurea stoebe in a common garden

Biological invasions are inherently demographic processes, but trait differences between native and introduced genotypes are rarely linked to population growth rates. Native European Centaurea stoebe occurs as two cytotypes with different life histories (monocarpic diploids, polycarpic tetraploids); however, only tetraploids have been found in its introduced range in North America. In a common garden experiment using artificial populations, we compared the demographic performance of the three geo-cytotypes in the presence and absence of a specialist herbivore using periodic matrix models. We found no difference in population growth rate between the two European cytotypes and no significant effects of herbivory in all geo-cytotypes. However, there was a pronounced increase in population growth rate for North American compared with European tetraploids due to increased seed production and juvenile establishment. These results suggest that genetic drift or rapid evolution, rather than pre-adaptation through polyploidy may explain the invasion success of tetraploids.     

Comparing methods for measuring the rate of spread of invading populations

Measuring rates of spread during biological invasions is important for predicting where and when invading organisms will spread in the future as well as for quantifying the influence of environmental conditions on invasion speed. While several methods have been proposed in the literature to measure spread rates, a comprehensive comparison of their accuracy when applied to empirical data would be problematic because true rates of spread are never known. This study compares the performances of several spread rate measurement methods using a set of simulated invasions with known theoretical spread rates over a hypothetical region where a set of sampling points are distributed. We vary the density and distribution (aggregative, random, and regular) of the sampling points as well as the shape of the invaded area and then compare how different spread rate measurement methods accommodate these varying conditions. We find that the method of regressing distance to the point of origin of the invasion as a function of time of first detection provides the most reliable method over adverse conditions (low sampling density, aggregated distribution of sampling points, irregular invaded area). The boundary displacement method appears to be a useful complementary method when sampling density is sufficiently high, as it provides an instantaneous measure of spread rate, and does not require long time series of data.     

Optimal Sampling Strategies for Detecting Zoonotic Disease Epidemics

The early detection of disease epidemics reduces the chance of successful introductions into new locales, minimizes the number of infections, and reduces the financial impact. We develop a framework to determine the optimal sampling strategy for disease detection in zoonotic host-vector epidemiological systems when a disease goes from below detectable levels to an epidemic. We find that if the time of disease introduction is known then the optimal sampling strategy can switch abruptly between sampling only from the vector population to sampling only from the host population. We also construct time-independent optimal sampling strategies when conducting periodic sampling that can involve sampling both the host and the vector populations simultaneously. Both time-dependent and -independent solutions can be useful for sampling design, depending on whether the time of introduction of the disease is known or not. We illustrate the approach with West Nile virus, a globally-spreading zoonotic arbovirus. Though our analytical results are based on a linearization of the dynamical systems, the sampling rules appear robust over a wide range of parameter space when compared to nonlinear simulation models. Our results suggest some simple rules that can be used by practitioners when developing surveillance programs. These rules require knowledge of transition rates between epidemiological compartments, which population was initially infected, and of the cost per sample for serological tests.     

Initial conditions and their effect on invasion velocity across heterogeneous landscapes

Accurate, time dependent control options are required to halt biological invasions prior to equilibrium establishment, beyond which control efforts are often impractical. Although invasions have been successfully modeled using diffusion theory, diffusion models are typically confined to providing simple range expansion estimates. In this work, we use a Susceptible/Infected cellular automaton (CA) to simulate diffusion. The CA model is coupled with a network model to track the speed and direction of simulated invasions across heterogeneous landscapes, allowing for identification of locations for targeted control in both time and space. We evaluated the role of the location of initial establishment insofar as it affected the pattern and rate of spread and how these are influenced by patch attributes such as size. Our results show that the location of initial establishment can significantly affect the temporal dynamics of an invasion. Traditional network metrics such as degree and measures of topological distance were insufficient for predicting the direction and speed of the invasion. Our coupled models allow the dynamic tracking of invasions across fragmented landscapes for both theoretical and practical applications.