Eight questions about invasions and ecosystem functioning

I pose eight questions central to understanding how biological invasions affect ecosystems, assess progress towards answering those questions and suggest ways in which progress might be made. The questions concern the frequency with which invasions affect ecosystems; the circumstances under which ecosystem change is most likely; the functions that are most often affected by invaders; the relationships between changes to ecosystems, communities, and populations; the long-term responses of ecosystems to invasions; interactions between biological invasions and other anthropogenic activities and the difficulty of managing undesirable impacts of non-native species. Some questions have been answered satisfactorily, others require more data and thought, and others might benefit from being reformulated or abandoned. Actions that might speed progress include careful development of trait-based approaches; strategic collection and publication of new data, including more frequent publication of negative results; replacement of expert opinion with hard data where needed; careful consideration of whether questions really need to be answered, especially in cases where answers are being provided for managers and policy-makers; explicit attention to and testing of the domains of theories; integrating invasions better into an ecosystem context; and remembering that our predictive ability is limited and will remain so for the foreseeable future.     

Tree invasions into treeless areas: mechanisms and ecosystem processes

Non-native tree invasions occur not only in woodland or forest vegetation, but also into areas with little or no native tree presence. Limiting factors for tree establishment and survival include seasonal or annual drought, low nutrient availability, cold temperature extremes, fire, and other abiotic conditions to which trees are poorly adapted as well as biotic conditions such as herbivory and lack of soil mutualist inoculum. Tree invasions of grasslands and semi-arid riparian areas in particular are now widespread and frequently result in the rapid conversion of these habitats to woodlands or forests. In some cases, these invasions are the result of a change in extrinsic conditions such as climate, fire, and/or grazing that remove what have been previous barriers to tree establishment. However, in other cases, tree species with particular life-history and dispersal traits fill open niches or outcompete native species. Significant examples of tree invasion into treeless areas can be seen with invasions of Pinus species into temperate grasslands and fynbos shrublands, Melaleuca quinquenervia and Triadica sebifera into grassy wetlands, Prosopis and Tamarix species into semi-arid riparian zones, and Acacia and Morella invasions into nutrient-poor shrublands and barrens. The establishment of trees into treeless areas may have strong impacts on ecosystem processes, influencing biogeochemical cycling, carbon sequestration and cycling, and ecohydrology, as well possible edaphic legacies that persist even if trees are removed.     

Biological invasions increase the richness of arbuscular mycorrhizal fungi from a Hawaiian subtropical ecosystem

Biological invasions can have various impacts on the diversity of important microbial mutualists such as mycorrhizal fungi, but few studies have tested whether the effects of invasions on mycorrhizal diversity are consistent across spatial gradients. Furthermore, few of these studies have taken place in tropical ecosystems that experience an inordinate rate of invasions into native habitats. Here, we examined the effects of plant invasions dominated by non-native tree species on the diversity of arbuscular mycorrhizal (AM) fungi in Hawaii. To test the hypothesis that invasions result in consistent changes in AM fungal diversity across spatial gradients relative to native forest habitats, we sampled soil in paired native and invaded sites from three watersheds and used amplicon sequencing to characterize AM fungal communities. Whether our analyses considered phylogenetic relatedness or not, we found that invasions consistently increased the richness of AM fungi. However, AM fungal species composition was not related to invasion status of the vegetation nor local environment, but stratified by watershed. Our results suggest that while invasions can lead to an overall increase in the diversity of microbial mutualists, the effects of plant host identity or geographic structuring potentially outweigh those of invasive species in determining the community membership of AM fungi. Thus, host specificity and spatial factors such as dispersal need to be taken into consideration when examining the effects of biological invasions on symbiotic microbes.     

Phenotypic plasticity opposes species invasions by altering fitness surface

Understanding species invasion is a central problem in ecology because invasions of exotic species severely impact ecosystems, and because invasions underlie fundamental ecological processes. However, the influence on invasions of phenotypic plasticity, a key component of many species interactions, is unknown. We present a model in which phenotypic plasticity of a resident species increases its ability to oppose invaders, and plasticity of an invader increases its ability to displace residents. Whereas these effects are expected due to increased fitness associated with phenotypic plasticity, the model additionally reveals a new and unforeseen mechanism by which plasticity affects invasions: phenotypic plasticity increases the steepness of the fitness surface, thereby making invasion more difficult, even by phenotypically plastic invaders. Our results should apply to phenotypically plastic responses to any fluctuating environmental factors including predation risk, and to other factors that affect the fitness surface such as the generalism of predators. We extend the results to competition, and argue that phenotypic plasticity's effect on the fitness surface will destabilize coexistence at local scales, but stabilize coexistence at regional scales. Our study emphasizes the need to incorporate variable interaction strengths due to phenotypic plasticity into invasion biology and ecological theory on competition and coexistence in fragmented landscapes.     

Invisible invaders: non-pathogenic invasive microbes in aquatic and terrestrial ecosystems

Although the number of studies on invasive plants and animals has risen exponentially, little is known about invasive microbes, especially non-pathogenic ones. Microbial invasions by viruses, bacteria, fungi and protists occur worldwide but are much harder to detect than invasions by macroorganisms. Invasive microbes have the potential to significantly alter community structure and ecosystem functioning in diverse terrestrial and aquatic ecosystems. Consequently, increased attention is needed on non-pathogenic invasive microbes, both free-living and symbiotic, and their impacts on communities and ecosystems. Major unknowns include the characteristics that make microbes invasive and properties of the resident communities and the environment that facilitate invasions. A comparison of microbial invasions with invasions of macroorganisms should provide valuable insights into general principles that apply to invasions across all domains of life and to taxon-specific invasion patterns. Invasive microbes appear to possess traits thought to be common in many invasive macroorganisms: high growth rate and resource utilization efficiency, and superior competitive abilities. Invading microorganisms are often similar to native species, but with enhanced performance traits, and tend to spread in lower diversity communities. Global change can exacerbate microbial invasions; therefore, they will likely increase in the future.     

Speciation and evolutionary dynamics of asymmetric mating preference

Asymmetric mating preferences occur in two closely related species, if females of one species are highly selective against males of the second, while females of the second show less selection against males of the first species. It has been suggested that such asymmetry is an indicator of common ancestry between the two species, but actual observations are contradictory and inconclusive. We developed a scenario of speciation history and asymmetric mating preference, incorporating invasion dynamicsvia frequency-dependent interspecific sexual competition. A newly isolated (derived) species may form at the periphery of the ancestral species’ distribution by invading a new range. Only a few closely related species would be expected in the new area, while many related species are expected to coexist with the ancestral species. In a peripherally derived species, female mating preferences should be relaxed through sexual character release, owing to a lack of sympatric species and a scarcity of intraspecific mating opportunities. Secondary contacts may then happen as: 1. repeated invasions, i.e. subsequent invasion by the ancestral species into the new range or, 2. backward invasions, i.e. derived species incursions into the ancestral range. Repeated invasions could lead to the coexistence of both the derived species and the newly invading ancestor. Backward invasions by the derived species can succeed only when the derived females develop a strict mating discrimination against the ancestral males. We then expect strong character displacement in the derived species. Thus, peripheral isolation and repeated invasions lead to the relaxed female mating preferences in the derived species and backward invasions lead to stronger female mating preferences in the derived species. This agrees withDrosophila data from Hawaii and the continents. Experimental data of theDrosophila arizonaemojavensis species cluster also support the hypothesis.     

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.     

Constraints and release at different scales – The role of adaptation in biological invasions

Attempts to find a consensus on traits promoting the invasiveness of exotic species have agreed on the idiosyncrasy of successful invasions. Despite considerable efforts to integrate aspects of context-dependency into theories of invasions, none of them has provided an evolutionary perspective taking consistently into account the direction of environmental changes in terms of ‘constraint’ vs. ‘release’. Applying the filter theory of species sorting, I consider different filters at different scales explaining evolutionary changes during invasions. Within this hierarchical approach, the focus is on the factorial filters climate, abiotic environment and biotic environment, distinguishing trophic interactions and plant-plant interactions. This review summarizes the evidence of adaptive shifts from native to exotic ranges, thereby differentiating the direction of shifts with regard to either constrained or released situations. Following this systematic approach, the present paper identifies further trade-offs within hierarchical levels complementing already existing hypotheses such as those for biotic interactions. In particular, the role of climatic changes should more explicitly be linked with evolutionary responses during invasions. Studying exotic species successfully invading several regions with different environmental conditions will be a promising starting point to enlarge the understanding of context-dependency of invasions.     

The elephant in the room: the role of failed invasions in understanding invasion biology

Most species introductions are not expected to result in invasion, and species that are invasive in one area are frequently not invasive in others. However, cases of introduced organisms that failed to invade are reported in many instances as anecdotes or are simply ignored. In this analysis, we aimed to find common characteristics between non‐invasive populations of known invasive species and evaluated how the study of failed invasions can contribute to research on biological invasions. We found intraspecific variation in invasion success and several recurring explanations for why non‐native species fail to invade; these included low propagule pressure, abiotic resistance, biotic resistance, genetic constraints and mutualist release. Furthermore, we identified key research topics where ignoring failed invasions could produce misleading results; these include studies on historical factors associated with invasions, distribution models of invasive species, the effect of species traits on invasiveness, genetic effects, biotic resistance and habitat invasibility. In conclusion, we found failed invasions can provide fundamental information on the relative importance of factors determining invasions and might be a key component of several research topics. Therefore, our analysis suggests that more specific and detailed studies on invasion failures are necessary.     

Recent emergence and worldwide spread of the red tomato spider mite, <Emphasis Type="Italic">Tetranychus evansi</Emphasis>: genetic variation and multiple cryptic invasions

Plant biosecurity is increasingly challenged by emerging crop pests. The spider mite Tetranychus evansi has recently emerged as a new threat to solanaceous crops in Africa and the Mediterranean basin, with invasions characterized by a high reproductive output and an ability to withstand a wide range of temperatures. Mitochondrial (868 bp of COI) and nuclear (1,137 bp of ITS) loci were analyzed in T. evansi samples spanning the current geographical distribution to study the earliest stages of the invasive process. The two sets of markers separate the samples into two main clades that are only present together in South America and Southern Europe. The highest COI diversity was found in South America, consistent with the hypothesis of a South American origin of T. evansi. Among the invaded areas, the Mediterranean region displayed a high level of genetic diversity similar to that present in South America, that is likely the result of multiple colonization events. The invasions of Africa and Asia by T. evansi are characterized by a low genetic variation associated with distinct introductions. Genetic data demonstrate two different patterns of invasions: (1) populations in the Mediterranean basin that are a result of multiple cryptic introductions and (2) emerging invasions of Africa and Asia, each likely the result of propagules from one or limited sources. The recent invasions of T. evansi illustrate not only the importance of human activities in the spread of agricultural pests, but also the limits of international quarantine procedures, particularly for cryptic invasions.     

Habitat invasion research: where vegetation science and invasion ecology meet

In the last decade, habitat‐oriented studies of plant invasions, performed at broad scales and using large data sets of vegetation plots, have focused on quantifying the representation of alien species in vegetation or habitat types, identifying factors underlying invasions, and exploring the pools of species available for invasion into particular habitats. In this essay we summarize what we have learned, discuss constraints associated with this kind of data and outline promising research topics to which a macroecological perspective of habitat invasions can contribute. Such topics include, among others: integrating species‐specific information on invasion status, residence time in the region, biological and ecological traits and phylogenetic relationships into habitat invasion research to better capture the context‐dependence of invasions; focusing on the functional role that alien species, relative to natives, play in plant communities; and obtaining insights into the role of pre‐adaptation for invasion by comparing the functional composition of habitat species pools in the native range. There is still a strong geographic bias, with detailed assessments across broader ranges of habitat types in large regions available only from Europe, the United States and New Zealand, which call for extension of this research to other continents.     

Can Invasive Species Facilitate Native Species? Evidence of How, When, and Why These Impacts Occur

Although the predatory and competitive impacts of biological invasions are well documented, facilitation of native species by non-indigenous species is frequently overlooked. A search through recent ecological literature found that facilitative interactions between invasive and native species occur in a wide range of habitats, can have cascading effects across trophic levels, can re-structure communities, and can lead to evolutionary changes. These are critical findings that, until now, have been mostly absent from analyses of ecological impacts of biological invasions. Here I present evidence for several mechanisms that exemplify how exotic species can facilitate native species. These mechanisms include habitat modification, trophic subsidy, pollination, competitive release, and predatory release. Habitat modification is the most frequently documented mechanism, reflecting the drastic changes generated by the invasion of functionally novel habitat engineers. Further, I predict that facilitative impacts on native species will be most likely when invasive species provide a limiting resource, increase habitat complexity, functionally replace a native species, or ameliorate predation or competition. Finally, three types of facilitation (novel, substitutive, and indirect) define why exotic species can lead to facilitation of native species. It is evident that understanding biological invasions at the community and ecosystem levels will be more accurate if we integrate facilitative interactions into future ecological research. Since facilitative impacts of biological invasions can occur with native endangered species, and can have wide-ranging impacts, these results also have important implications for management, eradication, and restoration.Contribution Number 2293, Bodega Marine Laboratory, University of California at Davis.     

Pine invasions in the southern hemisphere: modelling interactions between organism,environment and disturbance

Current theories of plant invasion have been criticized for their limited heuristic and predictive value. We explore the heuristic and predictive potential of a model which explicitly simulates the mechanisms of plant invasion. The model, a spatially-explicit individual-based simulation, is applied to the invasion of pine trees (Pinus spp.; Pinaceae) in three vegetation types in the southern hemisphere. The model simulates factors which have been invoked as major determinants of invasive success: plant traits, environmental features and disturbance level. Results show that interactions between these determinants of invasive success are at least as important as the main effects. The complexity of invasions has promoted the belief that many factors must be invoked to explain invasions. This study shows that by incorporating interactions and mechanisms into our models we can potentially reduce the number of factors needed to predict plant invasions. The importance of interactions, however, means that predictions about invasions must be context-specific. The search for all-encompassing rules for invasions is therefore futile. The model presented here is of heuristic value since it improves our understanding of invasions, and of management value since it defines the data and models needed for predicting invasions.     

Species richness and interacting factors control invasibility of a marine community

Anthropogenic vectors have moved marine species around the world leading to increased invasions and expanded species'' ranges. The biotic resistance hypothesis of Elton (in The ecology of invasions by animals and plants, 1958) predicts that more diverse communities should have greater resistance to invasions, but experiments have been equivocal. We hypothesized that species richness interacts with other factors to determine experimental outcomes. We manipulated species richness, species composition (native and introduced) and availability of bare space in invertebrate assemblages in a marina in Monterey, CA. Increased species richness significantly interacted with both initial cover of native species and of all organisms to collectively decrease recruitment. Although native species decreased recruitment, introduced species had a similar effect, and we concluded that biotic resistance is conferred by total species richness. We suggest that contradictory conclusions in previous studies about the role of diversity in regulating invasions reflect uncontrolled variables in those experiments that modified the effect of species richness. Our results suggest that patches of low diversity and abundance may facilitate invasions, and that such patches, once colonized by non-indigenous species, can resist both native and non-indigenous species recruitment.     

Partial migration to seasonally‐unstable habitat facilitates biological invasions in a predator‐dominated system

Although partial migration, a phenomenon in which some individuals in a population conduct seasonal migrations while others remain resident, is common among animals, its importance in facilitating biological invasions has not been demonstrated. To illustrate how partial migration might facilitate invasions in spatially complex habitats, we developed an individual‐based model of common carp Cyprinus carpio in systems of lakes and winterkill‐prone marshes in the Upper Mississippi River Basin (UMRB). Our model predicted that common carp are unable to become invasive in lakes of the UMRB unless they conduct partial migrations into winterkill‐prone marshes in which recruitment rates are high in the absence of native predators that forage on carp eggs and larvae. Despite low dispersal rates of juveniles and higher mortality rates of migrants, partial migration was adaptive across a wide range of migration rates and winterkill frequencies. Partial migration rates as low as 10% and winterkill occurrence as infrequent as once in 20 years were sufficient to cause invasiveness because of carp's reproductive potential and longevity. Consistent with the results of our model, empirical data showed that lake connectivity to winterkill‐prone marshes was an important driver of carp abundance within the study region. Our results demonstrate that biological invasions may be driven by a small, migratory contingent of a population that exploits more beneficial reproductive habitats.     

Superior structure stability and selectivity of hairpin nucleic acid probes with an L-DNA stem

Hairpin nucleic acid probes have been highly useful in many areas, especially for intracellular and in vitro nucleic acid detection. The success of these probes can be attributed to the ease with which their conformational change upon target binding can be coupled to a variety of signal transduction mechanisms. However, false-positive signals arise from the opening of the hairpin due mainly to thermal fluctuations and stem invasions. Stem invasions occur when the stem interacts with its complementary sequence and are especially problematic in complex biological samples. To address the problem of stem invasions in hairpin probes, we have created a modified molecular beacon that incorporates unnatural enantiomeric l-DNA in the stem and natural d-DNA or 2'-O-Me-modified RNA in the loop. l-DNA has the same physical characteristics as d-DNA except that l-DNA cannot form stable duplexes with d-DNA. Here we show that incorporating l-DNA into the stem region of a molecular beacon reduces intra- and intermolecular stem invasions, increases the melting temperature, improves selectivity to its target, and leads to enhanced bio-stability. Our results suggest that l-DNA is useful for designing functional nucleic acid probes especially for biological applications.     

Controlling Meiotic Recombinational Repair – Specifying the Roles of ZMMs,Sgs1 and Mus81/Mms4 in Crossover Formation

Crossovers (COs) play a critical role in ensuring proper alignment and segregation of homologous chromosomes during meiosis. How the cell balances recombination between CO vs. noncrossover (NCO) outcomes is not completely understood. Further lacking is what constrains the extent of DNA repair such that multiple events do not arise from a single double-strand break (DSB). Here, by interpreting signatures that result from recombination genome-wide, we find that synaptonemal complex proteins promote crossing over in distinct ways. Our results suggest that Zip3 (RNF212) promotes biased cutting of the double Holliday-junction (dHJ) intermediate whereas surprisingly Msh4 does not. Moreover, detailed examination of conversion tracts in sgs1 and mms4-md mutants reveal distinct aberrant recombination events involving multiple chromatid invasions. In sgs1 mutants, these multiple invasions are generally multichromatid involving 3–4 chromatids; in mms4-md mutants the multiple invasions preferentially resolve into one or two chromatids. Our analysis suggests that Mus81/Mms4 (Eme1), rather than just being a minor resolvase for COs is crucial for both COs and NCOs in preventing chromosome entanglements by removing 3′- flaps to promote second-end capture. Together our results force a reevaluation of how key recombination enzymes collaborate to specify the outcome of meiotic DNA repair.     

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.     

Unveiling an ancient biological invasion: molecular analysis of an old European alien, the crested porcupine (Hystrix cristata)

Background  

Biological invasions can be considered one of the main threats to biodiversity, and the recognition of common ecological and evolutionary features among invaders can help developing a predictive framework to control further invasions. In particular, the analysis of successful invasive species and of their autochthonous source populations by means of genetic, phylogeographic and demographic tools can provide novel insights into the study of biological invasion patterns. Today, long-term dynamics of biological invasions are still poorly understood and need further investigations. Moreover, distribution and molecular data on native populations could contribute to the recognition of common evolutionary features of successful aliens.     

Intraspecific diversity and dominant genotypes resist plant invasions

Numerous studies have asked whether communities with many species deter invasions more so than do species-poor communities or whether dominant species deter invasion by colonizing species. However, little is known about whether high intraspecific diversity can deter biological invasions or whether particular genotypes might deter invasions. In this study, we present experimental evidence that intraspecific diversity and particular genotypes of tall goldenrod, Solidago altissima , can act as a barrier to colonization by new species. We found that biomass of colonizing species was negatively correlated with genotypic diversity, and particular genotypes affected the richness, cover, and biomass of colonizing species. Stem density of S. altissima increased with genotypic diversity and varied among genotypes, suggesting that stem density is a key mechanism in limiting colonization dynamics in this system. Our results indicate that the loss of intraspecific diversity within a dominant plant species can increase susceptibility to plant invasions.