Alien futures: What is on the horizon for biological invasions?

Aim

To collect and identify the issues that may affect the future global and local management of biological invasions in the next 20–50 years and provide guidance for the prioritization of actions and policies responding to the management challenges of the future.

Location

Global

Methods

We used an open online survey to poll specialists and stakeholders from around the world as to their opinion on the three most important future issues both globally and at their respective local working level.

Results

The 240 respondents identified 629 global issues that we categorized into topics. We summarized the highest rated topics into five broad thematic areas: (1) environmental change, particularly climate change, (2) the spread of species through trade, (3) public awareness, (4) the development of new technologies to enhance management and (5) the need to strengthen policies. The respondents also identified 596 issues at their respective local working levels. Management, early detection, prevention and funding‐related issues all ranked higher than at the global level. Our global audience of practitioners, policymakers and researchers also elicited topics not identified in horizon scanning exercises led by scientists including potential human health impacts, the need for better risk assessments and legislation, the role of human migration and water management.

Main conclusions

The topic areas identified in this horizon scan provide guidance where future policy priorities for invasive alien species should be set. First, to reduce the magnitude and speed of environmental change and its impacts on biological invasions; second, to restrict the movement of potentially invasive alien species via trade; third, to raise awareness with the general public and empower them to act; and finally, to invest in innovative technologies that can detect and mitigate adverse impacts of introduced species.

     

The unified framework for biological invasions: a forest fungal pathogen perspective

Biological invasions in forests are growing in number and importance globally. The best studied examples are those caused by plants and animals, including insects. In contrast, forest invasions caused by microbes, including fungi, have received much lower levels of attention, particularly in the invasion biology literature. This can at least to some extent be due to the large number of these organisms involved and the fact that the majority of these have yet to be discovered and described. This is equally true for tree-infecting fungi, many of which are devastating pathogens responsible for dramatic invasions in natural and planted forests. This situation is changing through the application of molecular genetic tools that make it possible to accurately identify fungal tree pathogens, to determine their origins, pathways of movement, their modes of reproduction and change; all of which can influence invasions. The role and relevance of symbioses between tree pathogens and insects in forest invasions is also gaining increased attention. So too is our understanding that trees live in close association with large numbers of microbes that make up their holobiome. This has substantial relevance to invasion biology (Zenni et al. 2017). This commentary highlights four emerging issues that need to be considered regarding the invasions by fungal pathogens of trees and it emphasizes opportunities to better understand their relevance and impacts on natural and planted forests. A call is also made for plant pathologists to work more closely with ecologists such that fungal pathogens become more commonly integrated into invasion biology programmes.     

What can DNA tell us about biological invasions?

It is often hoped that population genetics can answer questions about the demographic and geographic dynamics of recent biological invasions. Conversely, invasions with well-known histories are sometimes billed as opportunities to test methods of population genetic inference. In both cases, underappreciated limitations constrain the usefulness of genetic methods. The most significant is that human-caused invasions have occurred on historical timescales that are orders of magnitude smaller than the timescales of mutation and genetic drift for most multicellular organisms. Analyses based on the neutral theory of molecular evolution cannot resolve such rapid dynamics. Invasion histories cannot be reconstructed in the same way as biogeographic changes occurring over millenia. Analyses assuming equilibrium between mutation, drift, gene flow, and selection will rarely be applicable, and even methods designed for explicitly non-equilibrium questions often require longer timescales than the few generations of most invasions of current concern. We identified only a few population genetic questions that are tractable over such short timescales. These include comparison of alternative hypotheses for the geographic origin of an invasion, testing for bottlenecks, and hybridization between native and invasive species. When proposing population genetic analysis of a biological invasion, we recommend that biologists ask (i) whether the questions to be addressed will materially affect management practice or policy, and (ii) whether the proposed analyses can really be expected to address important population genetic questions. Despite our own enthusiasm for population genetic research, we conclude that genetic analysis of biological invasions is justified only under exceptional circumstances.     

What is the biological basis of sensorimotor integration?

This Prospects presents the problems that must be solved by the vertebrate nervous system in the process of sensorimotor integration and motor control. The concepts of efference copy and inverse model are defined, and multiple biological mechanisms are described, including those that form the basis of integration, extrapolation, and comparison/cancellation operations. Open questions for future research include the biological basis of continuous and distributed versus modular control, and somatosensory-motor coordination.     

Trophic consequences of a biological invasion: do plant invasions increase predator abundance?

As invasive species become integrated into existing communities, they engage in a wide variety of trophic interactions with other community members. Many of these interactions are direct (e.g. predator–prey interactions or interference competition), but invasive species also can affect native community members indirectly, by influencing the abundances of intermediary species in trophic webs. Observational studies suggest that invasive plant species affect herbivorous arthropod communities and that these effects may flow up trophic webs to influence the abundance of predators. However, few studies have experimentally manipulated the presence of invasive plants to quantify the effects of plant invasion on higher trophic levels. Here, I use comparisons across sites that have or have not been invaded by the invasive plant Medicago polymorpha, combined with experimental removals of Medicago and insect herbivores, to investigate how a plant invasion affects the abundance of predators. Both manipulative and observational experiments showed that Medicago increased the abundance of the exotic herbivore Hypera and predatory spiders, suggesting positive bottom–up effects of plant invasions on higher trophic levels. Path analyses conducted on data from natural habitats revealed that Medicago primarily increased spider abundance through herbivore‐mediated indirect pathways. Specifically, Medicago density was positively correlated with the abundance of the dominant herbivore Hypera, and increased Hypera densities were correlated with increased spider abundance. Smaller‐scale experimental studies confirmed that Medicago may increase spider abundance through herbivore‐mediated indirect pathways, but also showed that the effects of Medicago varied across sites, including having no effect or having direct effects on spider abundance. If effects of invasive species commonly flow through trophic webs, then invasive species have the potential to affect numerous species throughout the community, especially those species whose dynamics are tightly connected to highly‐impacted community members through trophic linkages.     

A case of ‘tachy-brady syndrome’: What is the mechanism?

A young male presented with incessant narrow QRS tachycardia and left ventricular dysfunction. 24-Holter monitoring revealed multiple episodes of sustained and nonsustained episodes of tachycardia with prolonged sinus pauses at termination. The analysis of the electrocardiogram, followed by an invasive electrophysiological study, suggested an unusual mechanism for this tachy-brady syndrome.     

Lipid nanovesicles for biomedical applications: ‘What is in a name’?

Vesicles, generally defined as self-assembled structures formed by single or multiple concentric bilayers that surround an aqueous core, have been widely used for biomedical applications. They can either occur naturally (e.g. exosomes) or be produced artificially and range from the micrometric scale to the nanoscale. One the most well-known vesicle is the liposome, largely employed as a drug delivery nanocarrier. Liposomes have been modified along the years to improve physicochemical and biological features, resulting in long-circulating, ligand-targeted and stimuli-responsive liposomes, among others. In this process, new nomenclatures were reported in an extensive literature. In many instances, the new names suggest the emergence of a new nanocarrier, which have caused confusion as to whether the vesicles are indeed new entities or could simply be considered modified liposomes. Herein, we discussed the extensive nomenclature of vesicles based on the suffix “some” that are employed for drug delivery and composed of various types and proportions of lipids and others amphiphilic compounds. New names have most often been selected based on changes of vesicle lipid composition, but the payload, structural complexity (e.g. multicompartment) and new/improved proprieties (e.g. elasticity) have also inspired new vesicle names. Based on this discussion, we suggested a rational classification for vesicles.     

Can ecological stoichiometry help explain patterns of biological invasions?

Several mechanisms for biological invasions have been proposed, yet to date there is no common framework that can broadly explain patterns of invasion success among ecosystems with different resource availabilities. Ecological stoichiometry (ES) is the study of the balance of energy and elements in ecological interactions. This framework uses a multi‐nutrient approach to mass‐balance models, linking the biochemical composition of organisms to their growth and reproduction, which consequently influences ecosystem structure and functioning. We proposed a conceptual model that integrates hypotheses of biological invasions within a framework structured by fundamental principles of ES. We then performed meta‐analyses to compare the growth and production performances of native and invasive organisms under low‐ and high‐nutrient conditions in terrestrial and aquatic ecosystems. Growth and production rates of invasive organisms (plants and invertebrates) under both low‐ and high‐nutrient availability were generally larger than those of natives. Nevertheless, native plants outperformed invasives in aquatic ecosystems under low‐nutrient conditions. We suggest several distinct stoichiometry‐based mechanisms to explain invasion success in low‐ versus high‐nutrient conditions; low‐nutrient conditions: higher resource‐use efficiency (RUE; C:nutrient ratios), threshold elemental ratios (TERs), and trait plasticity (e.g. ability of an organism to change its nutrient requirements in response to varying nutrient environmental supply); high‐nutrient conditions: higher growth rates and reproductive output related to lower tissue C:nutrient ratios, and increased trait plasticity. Interactions of mechanisms may also yield synergistic effects, whereby nutrient enrichment and enemy release have a disproportionate effect on invasion success. To that end, ES provides a framework that can help explain how chemical elements and energy constrain key physiological and ecological processes, which can ultimately determine the success of invasive organisms.     

The ‘shifting baseline’ phenomenon: a global perspective

In this paper we demonstrate that low level ‘artisanal’ fishing can dramatically affect populations of slow-growing, late-maturing animals and that even on remote oceanic islands, stocks have been depleted and ecosystems degraded for millennia. Industrialised fisheries have developed during different decades in different regions of the world, and this has almost always been followed by a period of massive stock decline. However, ecosystems were not pristine before the onset of industrial fishing and it is difficult to assess the ‘virgin’ state of a population given that it may have been subject to moderate or even high levels of fishing mortality for many centuries. A wide range of information is available to help define or deduce historic marine population status. These include ‘traditional’ written sources but also less conventional sources such as archaeological remains, genetic analyses or simple anecdotal evidence. Detailed information, collected specifically for the purpose of determining fish stock biomass tends to exist only for recent decades, and most fishery assessments around the world (and thus time-series of biomass estimates), are less than 30 years long. Here we advocate using a wider range of multidisciplinary data sources, although we also recognise that it can be difficult to separate natural variability associated with changing climatic conditions from human-induced changes through fishing. We consider whether or not recovery of degraded ecosystems is ever possible and discuss a series of one-way ratchet like processes that can make it extremely difficult to return to a former ecosystem state.     

Low conductance states of a single ion channel are not ‘closed’

We have used a polymer-exclusion method to estimate the sizes of the high and low-conductance states of Staphylococcus aureus -toxin channels across planar lipid bilayers. Despite a >10-fold difference in conductance between high and low-conductance states, the size differs by <2-fold. We conclude that factors other than the dimensions have a strong influence on the conductance of -toxin channels. We also show that the high conductance state is destabilized by the presence of high molecular weight polymers outside the channel, compatible with the removal of channel water as the high conductance state shrinks to the low conductance state.We are grateful to Drs. D.T. Edmonds, A.A. Lev and V.A. Parsegian for fruitful discussion and to the Cell Surface Research Fund, the Science and Engineering Research Council, The Wellcome Trust, UNESCO (Molecular and Cellular Biology Network) and the National Academy of Sciences/National Research Council for financial support.     

What is a 'low dose' of radiation?

Although the expression of radiation-induced biological effects and responses may be at either the cell, organ or organism level, induction of some of these phenomena (e.g. cancer of clastogenic and genetic effects) can have their origin in the interaction of a single charged particle with the target-containing volume (TCV) of the cell, e.g. the cell nucleus. However, the independent variable now used in both organ and cell population studies, the absorbed dose to the organ, provides no information directly on particle-TCV interactions. Even if calculated as a mean to an organized population of cells, the absorbed dose becomes a composite and confounded quantity, (FzN), in which F is the fraction of TCVs 'hit' by a particle during a given exposure, z is the mean value of z1, the energy absorbed in the TCV in a single hit, and N is the mean number of hits per affected TCV. Scientific precepts demand the avoidance of such confounded variables by achieving their isolation. The needed separation can be effected by the use of microdosimetric techniques, which make it possible to hold one component quantity constant while the others are varied. As an example, low-level radiation exposure (LLE) can be used to hold F at a constant value of 0.2 where, on average, there is but one hit per TCV. The probability of a cellular quantal response, as a function of z1 only, can then be determined by use of LLE to radiations covering a wide span of LETs. Conversely, the effect of varying only the fraction of cells hit can be studied by holding z constant. This can be accomplished by working within a narrow band of LET, but only in the LLE range. The effectiveness of preirradiation altering cell sensitivity as a function of the number of hits per TCV can be determined by working within, and somewhat above, the LLE range. In either risk assessment or the application of radiation as a pretreatment, minimal consequences can be assured only if very low-level exposure is employed in order that F will be small, and if the exposure is in a field of radiation of very low LET so that z1 will be as small as possible. That is to say, exposure conditions with low consequences cannot be specified in terms of any single quantity.     

Bridging the explanatory gaps: What can we learn from a biological agency perspective?

We begin this article by delineating the explanatory gaps left by prevailing gene-focused approaches in our understanding of phenotype determination, inheritance, and the origin of novel traits. We aim not to diminish the value of these approaches but to highlight where their implementation, despite best efforts, has encountered persistent limitations. We then discuss how each of these explanatory gaps can be addressed by expanding research foci to take into account biological agency—the capacity of living systems at various levels to participate in their own development, maintenance, and function by regulating their structures and activities in response to conditions they encounter. Here we aim to define formally what agency and agents are and—just as importantly—what they are not, emphasizing that agency is an empirical property connoting neither intention nor consciousness. Lastly, we discuss how incorporating agency helps to bridge explanatory gaps left by conventional approaches, highlight scientific fields in which implicit agency approaches are already proving valuable, and assess the opportunities and challenges of more systematically incorporating biological agency into research programs.     

Implementation of a ‘standard’ LIMS

This article is an extract of a presentation given at the LIMS conference in the Hague June 4, 1997 [S.M. Fransen et al., Presentation given at the conference LIMS 97, June 4 1997 in the Hague.]. It describes the project steps for the LIMS project in the Danish company Novo Nordisk, with focus on vendor evaluation, validation and implementation of a ‘Standard’ LIMS software. The main project steps are described and experiences gained are discussed.     

Synaptic vesicles: is kissing a matter of competence?

The "kiss-and-run" model of exocytosis and endocytosis predicts that synaptic vesicles can undergo fast and efficient recycling, after fusion with the plasmalemma, without intermixing of membranes. Evidence is mounting from several new experimental approaches that kiss-and-run occurs at synapses. Distinct vesicle pools, which initially were identified in morphological terms, are now being characterized in biochemical and functional terms. In addition, at least two functional recycling pathways, operating on different time scales (from milliseconds to tens of seconds), have been shown to coexist in the same synaptic system, and the two pathways appear to be differentially regulated. Taken together, these data suggest that kiss-and-run operates in parallel with the classical, coated-vesicle recycling. Here, we review recent evidence for kiss-and-run recycling and discuss whether it is a distinct process, dependent on the molecular organization of the fusing vesicle. We propose that vesicles undergo a process of "competence maturation". According to this view, the specific molecular make-up of the vesicles, their location and their interactions with nerve terminal proteins might determine not only the differential availability of the vesicles for fusion and neurotransmitter release but also the recycling path that they will follow.     

A ‘Goldilocks’ hypothesis for dispersal of biological control agents

The rate at which biological control agents disperse from release sites has important implications for their establishment and spread. Low rates of dispersal can yield spread that is too slow and may necessitate redistribution efforts for importation biological control and a high density of release sites for augmentation. Low dispersal rates may also lead to inbreeding at the site of release. On the other hand, high rates of dispersal can lead to Allee effects at the leading edge of the invasion front, potentially reducing the likelihood of establishment. Given these disadvantages associated with both low and high dispersal rates, we argue that intermediate rates of dispersal are likely to maximize the probability of establishment and appropriate spread for biological control agents released in the context of either importation or augmentative biological control. We consider this putative relationship a ‘Goldilocks hypothesis’ since it posits an optimum at intermediate values. In this review paper we begin by discussing the rationale for the Goldilocks hypothesis and then provide a case study from our work on importation biological control of the soybean aphid, Aphis glycines. Work on the soybean aphid parasitoid Binodoxys communis has shown that long-distance dispersal of immature parasitoids within winged migrating aphids is unlikely. This is likely good news for importation biological control because parasitoids dispersed in this manner would likely encounter crippling Allee effects. On the other hand, results from a field release study also suggest that female B. communis females (but not males) disperse actively from release sites. This female-biased dispersal may lead to strong mate-finding Allee effects and therefore may make establishment less likely.