Bird-plant interactions and vulnerability to biological invasions

Aims Species interactions regulate the invasiveness of non-native species and as declines of native tree species escalate, exotic tree species that offer supplementary resources to animal seed-dispersers should expand their distributions as they fill ecological roles. Our primary objective was to forecast impacts from an imminent biological invasion (laurel wilt disease) by quantifying resources provided by native (threatened) and exotic fruits (disease-resistant) and associated bird foraging preferences.Methods In the southeastern USA, we tested for redundancy among the resources provided by native and exotic fruits to overwintering birds. Comparisons between abundant subcanopy species Persea borbonia (native) and Cinnamomum camphora (exotic) were paramount considering the widespread disease-induced decline of P. borbonia, and the biological and phylogenetic similarities between these species. Across two winter survey periods, we quantified fruit removal and documented bird species using motion-activated cameras in the field. Physical and chemical fruit characteristics were also quantified.Important findings Foraging bouts on both P. borbonia and C. camphora fruits were documented for four native bird species. There was no difference in selectivity between fruit types during Year 1 of our survey, but there was a significant preference for C. camphora fruit in Year 2; the change in preference was correlated with significantly lower temperatures in Year 2. While the pulp/seed ratio and moisture content differed, the nutritional content of fruit pulp (g/100g) was similar between fruit types. Given the apparent redundancy among these native and exotic fruit resources, we forecast increases in the consumption and dispersal of exotic propagules following the widespread laurel wilt disease-induced decline of P. borbonia and other native fruit bearing members of Lauraceae. This empirically based prediction is among the first to document exotic forest pathogens as indirect threats to native bird–plant interactions and potential facilitators of exotic plant invasion.     

How to manage biological invasions under globalization

Protecting national borders against biological invasions is becoming increasingly difficult because those whose actions result in invasions seldom bear legal responsibility for those actions. Invasion costs are often an externality (an unintended side effect) of international trade. Externalities are best dealt with by internalizing them; that is, by getting those who harm society to meet the cost. This is the 'polluter pays principle', which, under current trade rules, is difficult to implement. Tariffs could, however, be used to confront exporters with the costs of their actions, and the right to do this should be embedded in trade agreements. At the same time, international aid could be used to protect donor societies against the inability of some other countries to take appropriate biosecurity measures. The impact of invasions can thus be reduced by tackling their economic externalities.     

Overlooking the smallest matter: viruses impact biological invasions

Parasites and pathogens have recently received considerable attention for their ability to affect biological invasions, however, researchers have largely overlooked the distinct role of viruses afforded by their unique ability to rapidly mutate and adapt to new hosts. With high mutation and genomic substitution rates, RNA and single‐stranded DNA (ssDNA) viruses may be important constituents of invaded ecosystems, and could potentially behave quite differently from other pathogens. We review evidence suggesting that rapidly evolving viruses impact invasion dynamics in three key ways: (1) Rapidly evolving viruses may prevent exotic species from establishing self‐sustaining populations. (2) Viruses can cause population collapses of exotic species in the introduced range. (3) Viruses can alter the consequences of biological invasions by causing population collapses and extinctions of native species. The ubiquity and frequent host shifting of viruses make their ability to influence invasion events likely. Eludicating the viral ecology of biological invasions will lead to an improved understanding of the causes and consequences of invasions, particularly as regards establishment success and changes to community structure that cannot be explained by direct interspecific interactions among native and exotic species.     

Classical biological control: exploiting enemy escape to manage plant invasions

Practitioners of classical biological control of invasive weeds are confronted with a dual expectation: to achieve successful control of plant invaders and to avoid damage to nontarget plants and adverse indirect effects. In this paper we discuss key issues that we consider to be crucial for a safe, efficient, and successful classical biological control project, and that have also caused some recent controversy. These include selection of effective control agents, host specificity of the biological control agents, implications of the genetic population structure of the target populations, and potential impact on native food webs. With regard to improving the success rate of biological control of plant invaders, we first emphasize the importance of a clear a priori definition of success and a more ecosystem-based approach to better document both negative effects of the invasive plant as well as potential positive and negative effects of introducing biological control agents. Secondly, pre-release impact assessment could be improved by better focusing on how to reach high densities of the control agents and by including tolerance to and compensation of herbivory. Thirdly, we advocate a reinforced effort to integrate and combine biological control in combination with existing or potential management options. Finally, we propose various ecological and evolutionary hypotheses in the framework of our topic to document that biological control programmes against plant invaders also offer a great opportunity to gain new insights into basic processes in ecology and evolution.     

The fungal dimension of biological invasions

Fungi represent an essential component of biodiversity, not only because of the large number of species, but also for their ecological, evolutionary and socio-economic significance. Yet, until recently, fungi received scant consideration in ecology, especially invasion ecology. Their under-representation is largely the result of a lack of scientific knowledge of fungal biodiversity and ecology. With the exception of pathogenic fungi, which cause emergent infectious diseases, the impact of fungal invasions is often difficult to quantify owing to limited baseline data on fungal communities. Here, we aim to raise awareness among mycologists and ecologists of the fungal dimension of invasions and of the need to intensify research in fungal ecology to address issues of future introductions.     

Dispersal polymorphism and the speed of biological invasions

The speed at which biological range expansions occur has important consequences for the conservation management of species experiencing climate change and for invasion by exotic organisms. Rates of dispersal and population growth are known to affect the speed of invasion, but little is known about the effect of having a community of dispersal phenotypes on the rate of range expansion. We use reaction-diffusion equations to model the invasion of a species with two dispersal phenotypes into a previously unoccupied landscape. These phenotypes differ in both their dispersal rate and population growth rate. We find that the presence of both phenotypes can result in faster range expansions than if only a single phenotype were present in the landscape. For biologically realistic parameters, the invasion can occur up to twice as fast as a result of this polymorphism. This has implications for predicting the speed of biological invasions, suggesting that speeds cannot just be predicted from looking at a single phenotype and that the full community of phenotypes needs to be taken into consideration.     

Evolutionary indirect effects of biological invasions

Just as ecological indirect effects can have a wide range of consequences for community structure and ecosystem function, theory suggests that evolutionary indirect effects can also influence community dynamics and the outcome of species interactions. There is little empirical evidence documenting such effects, however. Here, I use a multi-generation selection experiment in the field to investigate: (1) how the exotic plant Medicago polymorpha and the exotic insect herbivore Hypera brunneipennis affect the evolution of anti-herbivore resistance traits in the native plant Lotus wrangelianus and (2) how observed Lotus evolutionary responses to Hypera alter interactions between Lotus and other members of the herbivore community. In one of two study populations, I document rapid evolutionary changes in Lotus resistance to Hypera in response to insecticide treatments that experimentally reduced Hypera abundance, and in response to Medicago-removal treatments that also reduced Hypera abundance. These evolutionary changes in response to Hypera result in reduced attack by aphids. Thus, an evolutionary change caused by one herbivore species alters interactions with other herbivore taxa, an example of an eco-evolutionary feedback. Given that many traits mediate interactions with multiple species, the effects of evolutionary changes in response to one key biotic selective agent may often cascade through interaction webs to influence additional community members.     

An evolutionary perspective of biological invasions

The workshop on the Evolutionary Perspective of Biological Invasions in Terrestrial Ecosystems was held in Halle, Germany from 30 September to 3 October 2002.     

Rapid response to changing environments during biological invasions: DNA methylation perspectives

Dissecting complex interactions between species and their environments has long been a research hot spot in the fields of ecology and evolutionary biology. The well‐recognized Darwinian evolution has well‐explained long‐term adaptation scenarios; however, “rapid” processes of biological responses to environmental changes remain largely unexplored, particularly molecular mechanisms such as DNA methylation that have recently been proposed to play crucial roles in rapid environmental adaptation. Invasive species, which have capacities to successfully survive rapidly changing environments during biological invasions, provide great opportunities to study molecular mechanisms of rapid environmental adaptation. Here, we used the methylation‐sensitive amplified polymorphism (MSAP) technique in an invasive model ascidian, Ciona savignyi, to investigate how species interact with rapidly changing environments at the whole‐genome level. We detected quite rapid DNA methylation response: significant changes of DNA methylation frequency and epigenetic differentiation between treatment and control groups occurred only after 1 hr of high‐temperature exposure or after 3 hr of low‐salinity challenge. In addition, we detected time‐dependent hemimethylation changes and increased intragroup epigenetic divergence induced by environmental stresses. Interestingly, we found evidence of DNA methylation resilience, as most stress‐induced DNA methylation variation maintained shortly (~48 hr) and quickly returned back to the control levels. Our findings clearly showed that invasive species could rapidly respond to acute environmental changes through DNA methylation modifications, and rapid environmental changes left significant epigenetic signatures at the whole‐genome level. All these results provide fundamental background to deeply investigate the contribution of DNA methylation mechanisms to rapid contemporary environmental adaptation.     

The evolutionary consequences of biological invasions

A major challenge of invasion biology is the development of a predictive framework that prevents new invasions. This is inherently difficult because different biological characteristics are important at the different stages of invasion: opportunity/transport, establishment and spread. Here, we draw from recent research on a variety of taxa to examine the evolutionary causes and consequences of biological invasions. The process of introduction may favour species with characteristics that promote success in highly disturbed, human-dominated landscapes, thus exerting novel forms of selection on introduced populations. Moreover, evidence is accumulating that multiple introductions can often be critical to the successful establishment and spread of introduced species, as they may be important sources of genetic variation necessary for adaptation in new environments or may permit the introduction of novel traits. Thus, not only should the introduction of new species be prevented, but substantial effort should also be directed to preventing the secondary introduction of previously established species (and even movement of individuals among introduced populations). Modern molecular techniques can take advantage of genetic changes postintroduction to determine the source of introduced populations and their vectors of spread, and to elucidate the mechanisms of success of some invasive species. Moreover, the growing availability of genomic tools will permit the identification of underlying genetic causes of invasive success.     

Resource-dependent dispersal and the speed of biological invasions

Many mobile organisms exhibit resource-dependent movement in which movement rates adjust to changes in local resource densities through changes in either the probability of moving or the distance moved. Such changes may have important consequences for invasions because reductions in resources behind an invasion front may cause higher dispersal while simultaneously reducing population growth behind the front and thus lowering the number of dispersers. Intuiting how the interplay between population growth and dispersal affects invasions is difficult without mathematical models, yet most models assume dispersal rates are constant. Here we present spatial-spread models that allow for consumer-resource interactions and resource-dependent dispersal. Our results show that when resources affect the probability of dispersal, then the invasion dynamics are no different than if resources did not affect dispersal. When resources instead affect the distance dispersed, however, the invasion dynamics are strongly affected by the strength of the consumer-resource interaction, and population cycles behind the wave front lead to fluctuating rates of spread. Our results suggest that for actively dispersing invaders, invasion dynamics can be determined by species interactions. More practically, our work suggests that reducing invader densities behind the front may be a useful method of slowing an invader's rate of spread.     

External morphology explains the success of biological invasions

Biological invasions have become major players in the current biodiversity crisis, but realistic tools to predict which species will establish successful populations are still unavailable. Here we present a novel approach that requires only a morphometric characterisation of the species. Using fish invasions of the Mediterranean, we show that the abundance of non‐indigenous fishes correlates with the location and relative size of occupied morphological space within the receiving pool of species. Those invaders that established abundant populations tended to be added outside or at the margins of the receiving morphospace, whereas non‐indigenous species morphologically similar to resident ones failed to develop large populations or even to establish themselves, probably because the available ecological niches were already occupied. Accepting that morphology is a proxy for a species' ecological position in a community, our findings are consistent with ideas advanced since Darwin's naturalisation hypothesis and provide a new warning signal to identify invaders and to recognise vulnerable communities.     

Evaluating methods to quantify spatial variation in the velocity of biological invasions

Invading species rarely spread homogeneously through a landscape and invasion patterns typically display irregular frontal boundaries as the invasion progresses through space. Those irregular patterns are generally produced by local environmental factors that may slow or accelerate movement of the frontal boundary. While there is an abundant literature on species distribution modelling methods that quantify local suitability for species establishment, comparatively few studies have examined methods for measuring the local velocity of invasions that can then be statistically analysed in relation to spatially variable environmental factors. Previous studies have used simulations to compare different methods for estimating the overall rate of spread of an invasion. We adopted a similar approach of simulating invasions that resemble two real case‐studies, both in terms of their spatial resolution (i.e. considering the size of one cell as one km) and their spatial extent (> 600 000 km²). Simulations were sampled to compare how different methods used to measure local spread rate, namely the neighbouring, nearest distance and Delaunay methods, perform for spatio‐temporal comparisons. We varied the assessment using three levels of complexity of the spatio‐temporal pattern of invasion, three sample sizes (500, 1000 and 2000 points), three different spatial sampling patterns (stratified, random, aggregated), three interpolation methods (generalized linear model, kriging, thin plate spline regression) and two spatio‐temporal modelling structures (trend surface analysis and boundary displacement), resulting in a total of 486 different scenarios. The thin plate spline regression interpolation method, in combination with trend surface analysis, was found to provide the most robust local spread rate quantification as it was able to reliably accommodate different sampling conditions and invasion patterns. This best approach was successfully applied to two case‐studies, the invasion of France by the horse‐chestnut leafminer Cameraria ohridella and by the bluetongue virus, generally in agreement with previously published values of spread rates. Potential avenues for further research are discussed.     

媒介昆虫-病毒-植物互作对生物入侵的影响

媒介昆虫-病毒-植物互作关系复杂多样。虽然相关的研究较多, 然而有关三者互作对于生物入侵的影响还知之甚少。已有证据表明, 寄主植物对病毒的敏感性和对媒介昆虫的适合性、媒介昆虫对寄主的适应能力等因素影响三者互作关系。当寄主植物易感病并且对媒介昆虫的适合性低, 而媒介昆虫对寄主植物的适应能力强时, 媒介昆虫与植物病毒之间很可能建立间接互惠关系, 这种互惠可促进媒介昆虫入侵和病毒病流行。此外, 媒介昆虫与植物病毒之间中性或偏害的互作关系对于外来生物入侵的促进作用也不容忽视。鉴于三者互作对于生物入侵的重要性, 今后需要对不同物种所组成的多种组合进行比较研究, 并采用多种方法揭示互作的生理和分子机制。     

Characterizing ecosystem-level consequences of biological invasions: the role of ecosystem engineers

Invasions by exotic species represent both threats to ecosystems as well as opportunities to learn more about them. Among the invaders that will have the largest impacts are those that directly modify ecosystems and thus have cascading effects for resident biota. Exotics can affect ecosystems by altering system-level flows, availability, or quality of nutrients, food, and physical resources (e.g. living space, water, heat or light). The invader-mediated control of physical resources, typically achieved through the modification of habitats, has received limited attention in invasion biology. This reflects a general trend in ecology, and only recently has the concept of ecosystem engineering been developed to account for the role of species that shape habitats. Plants and animals in terrestrial and aquatic systems can both create and destroy structure. When introduced into ecosystems, these exotic engineers cause physical state changes with effects that ramify throughout the system. Although the consequences of these modifications are varied and complex, insight gained from general ecological principles offers an opportunity to predict what invaders will do upon their integration into systems. Examples from the literature suggest that introduced ecosystem engineers that increase habitat complexity or heterogeneity tend to cause abundances and/or species richness to rise, while those that decrease complexity tend to have the reverse effect. In assessing such patterns, however, it is critical to also consider spatial scales and the life habits of resident organisms. In addition to providing predictive power, recognition of engineering as a major means by which invasive species affect ecosystems provides a unifying theme for invasion biology and offers a chance to consider more fully the general role of species in ecosystems.     

Antarctica: The final frontier for marine biological invasions

Antarctica is experiencing significant ecological and environmental change, which may facilitate the establishment of non‐native marine species. Non‐native marine species will interact with other anthropogenic stressors affecting Antarctic ecosystems, such as climate change (warming, ocean acidification) and pollution, with irreversible ramifications for biodiversity and ecosystem services. We review current knowledge of non‐native marine species in the Antarctic region, the physical and physiological factors that resist establishment of non‐native marine species, changes to resistance under climate change, the role of legislation in limiting marine introductions, and the effect of increasing human activity on vectors and pathways of introduction. Evidence of non‐native marine species is limited: just four marine non‐native and one cryptogenic species that were likely introduced anthropogenically have been reported freely living in Antarctic or sub‐Antarctic waters, but no established populations have been reported; an additional six species have been observed in pathways to Antarctica that are potentially at risk of becoming invasive. We present estimates of the intensity of ship activity across fishing, tourism and research sectors: there may be approximately 180 vessels and 500+ voyages in Antarctic waters annually. However, these estimates are necessarily speculative because relevant data are scarce. To facilitate well‐informed policy and management, we make recommendations for future research into the likelihood of marine biological invasions in the Antarctic region.