Secondary invasion: When invasion success is contingent on other invaders altering the properties of recipient ecosystems

Positive interactions between exotic species may increase ecosystem‐level impacts and potentially facilitate the entry and spread of other exotic species. Invader‐facilitated invasion success—”secondary invasion”—is a key conceptual aspect of the well‐known invasional meltdown hypothesis, but remains poorly defined and empirically underexplored. Drawing from heuristic models and published empirical studies, we explore this form of “secondary invasion” and discuss the phenomenon within the recognized conceptual framework of the determinants of invasion success. The term “secondary invasion” has been used haphazardly in the literature to refer to multiple invasion phenomena, most of which have other more accepted titles. Our usage of the term secondary invasion is akin to “invader‐facilitated invasion,” which we define as the phenomenon in which the invasion success of one exotic species is contingent on the presence, influence, and impacts of one or more other exotic species. We present case studies of secondary invasion whereby primary invaders facilitate the entry or establishment of exotic species into communities where they were previously excluded from becoming invasive. Our synthesis, discussion, and conceptual framework of this type of secondary invasion provides a useful reference to better explain how invasive species can alter key properties of recipient ecosystems that can ultimately determine the invasion success of other species. This study increases our appreciation for complex interactions following invasion and highlights the impacts of invasive species themselves as possible determinants of invasion success. We anticipate that highlighting “secondary invasion” in this way will enable studies reporting similar phenomena to be identified and linked through consistent terminology.     

Qualitative and quantitative agar invasion test based on bacterial colony/biofilm

Invasion of the culture medium is a feature frequently studied in yeasts, in which it has been related to a greater virulence, but it is practically unknown in bacteria. Recently, it has been demonstrated that several clinically relevant bacterial species were also able of invading agar media, so it was necessary to design a microbiological assay to study the expression of this character in bacteria. Accordingly, a bacterial agar invasion test based on colony/biofilm development was designed, which allows qualitative and quantitative characterization of bacterial growth into the agar culture medium. Once the culture conditions were optimized, the test was applied to 90 strains from nine bacterial species, validating its usefulness for differentiating invasive strains (positive) from those non invasive (negative). The test also allows sorting invasive strains according to agar invasion intensity (low, moderate, high) and topographic invasion pattern (peripheral, homogeneous, mixed). Moreover, an image analysis routine to quantify the invasion was developed. Implemented method enables direct measuring of two invasion parameters (invasion area and number of invasion dots), automated calculation of three relative variables (invasion relative area, invasion dots relative density, and invasion dot average area), and the establishment of strain specific frequency histograms.     

AP-1-mediated invasion requires increased expression of the hyaluronan receptor CD44.

Fibroblasts transformed by Fos oncogenes display increased expression of a number of genes implicated in tumor cell invasion and metastasis. In contrast to normal 208F rat fibroblasts, Fos-transformed 208F fibroblasts are growth factor independent for invasion. We demonstrate that invasion of v-Fos- or epidermal growth factor (EGF)-transformed cells requires AP-1 activity. v-Fos-transformed cell invasion is inhibited by c-jun antisense oligonucleotides and by expression of a c-jun dominant negative mutant, TAM-67. EGF-induced invasion is inhibited by both c-fos and c-jun antisense oligonucleotides. CD44s, the standard form of a transmembrane receptor for hyaluronan, is implicated in tumor cell invasion and metastasis. We demonstrate that increased expression of CD44 in Fos- and EGF-transformed cells is dependent upon AP-1. CD44 antisense oligonucleotides reduce expression of CD44 in v-Fos- or EGF-transformed cells and inhibit invasion but not migration. Expression of a fusion protein between human CD44s and Aequorea victoria green fluorescent protein (GFP) in 208F cells complements the inhibition of invasion by the rat-specific CD44 antisense oligonucleotide. We further show that both v-Fos and EGF transformations result in a concentration of endogenous CD44 or exogenous CD44-GFP at the ends of pseudopodial cell extensions. These results support the hypothesis that one role of AP-1 in transformation is to activate a multigenic invasion program.     

Characterisation of erythrocyte invasion by Babesia bovis merozoites efficiently released from their host cell after high-voltage pulsing

Apicomplexa are a phylum of obligate intracellular parasites critically dependent on invasion of a host cell. An in vitro assay for erythrocyte invasion by Babesia bovis was established, employing free merozoites obtained after the application of high-voltage to the parasitised erythrocytes. The invasion proceeds efficiently in phosphate-buffered saline solution without the requirement for any serum or medium components. The kinetics of invasion can be measured over a time span of 5-60 min after which invasion is completed at an average efficiency of 41%. The fast kinetics and high efficiency exceed those of most previously established apicomplexan invasion assays. The manipulation of intracellular calcium concentration inhibits invasion. Preincubation of merozoites at 37 degrees C also reduces invasion, possibly by the premature secretion of protein. Proteins that are shed into the environment during invasion were directly detectable by protein staining after 2-D gel electrophoresis. The limitations posed by the immunological detection of proteins released during in vitro invasion by other apicomplexan parasites can, therefore, be avoided by this method. A unique feature of the assay is the reversible uncoupling of invasion and intracellular development, the latter taking place only under serum-rich medium conditions. In addition, host cell attachment is uncoupled from invasion by cytochalasin B.     

3D Traction Stresses Activate Protease-Dependent Invasion of Cancer Cells

Cell invasion and migration that occurs, for example, in cancer metastasis is rooted in the ability of cells to navigate through varying levels of physical constraint exerted by the extracellular matrix. Cancer cells can invade matrices in either a protease-independent or a protease-dependent manner. An emerging critical component that influences the mode of cell invasion is the traction stresses generated by the cells in response to the physicostructural properties of the extracellular matrix. In this study, we have developed a reference-free quantitative assay for measuring three-dimensional (3D) traction stresses generated by cells during the initial stages of invasion into matrices exerting varying levels of mechanical resistance. Our results show that as cells encounter higher mechanical resistance, a larger fraction of them shift to protease-mediated invasion, and this process begins at lower values of cell invasion depth. On the other hand, the compressive stress generated by the cells at the onset of protease-mediated invasion is found to be independent of matrix stiffness, suggesting that 3D traction stress is a key factor in triggering protease-mediated cancer cell invasion. At low 3D compressive traction stresses, cells utilize bleb formation to indent the matrix in a protease independent manner. However, at higher stress values, cells utilize invadopodia-like structures to mediate protease-dependent invasion into the 3D matrix. The critical value of compressive traction stress at the transition from a protease-independent to a protease-dependent mode of invasion is found to be ∼165 Pa.     

Applying competition theory to invasion: resource impacts indicate invasion mechanisms in California shrublands

Despite widespread work documenting invasion, it remains a challenge to determine invasion mechanisms and incorporate them into invasive species management. Competition theory presents a strong model for evaluating the role of resource reduction and requirements in invasion. Additionally, alternative models suggest fluctuations in resources, niche differences, or non-resource priority effects are key factors determining invasion success. We propose a comparative framework that incorporates resource impacts of native and invasive species, performance in controlled invasion trials, and long-term natural invasion patterns to elucidate relative importance of these invasion mechanisms. To demonstrate this framework, we established monocultures of two representative native and two invasive plant species in Southern California’s coastal sage scrub (CSS), measured resource impacts (i.e., R*), and conducted invasion trials to test whether resource impacts predicted invasion success. We then related experimental results to field invasion patterns. Compared to exotic herbaceous species, native shrubs were associated with greater resource depletion of key resources: light, soil water (at multiple depths), and soil inorganic nitrogen (particularly at depth). In invasion trials, natives resisted invasion by the exotics, as resource depletion measures would predict. However, these results did not follow long-term natural invasion patterns indicating that these exotic species invade areas once dominated by native shrubland. Applying our results to the invasion framework, we conclude that disturbance, or a similar mechanism causing resources to fluctuate, is needed for exotics to invade CSS habitats. This resource-based comparative analysis of invasion mechanisms can point out important processes and help suggest effective management actions.     

Invasion triangle: an organizational framework for species invasion

Species invasion is a complex, multifactor process. To encapsulate this complexity into an intuitively appealing, simple, and straightforward manner, we present an organizational framework in the form of an invasion triangle. The invasion triangle is an adaptation of the disease triangle used by plant pathologists to help envision and evaluate interactions among a host, a pathogen, and an environment. Our modification of this framework for invasive species incorporates the major processes that result in invasion as the three sides of the triangle: (1) attributes of the potential invader; (2) biotic characteristics of a potentially invaded site; and (3) environmental conditions of the site. The invasion triangle also includes the impact of external influences on each side of the triangle, such as climate and land use change. This paper introduces the invasion triangle, discusses how accepted invasion hypotheses are integrated in this framework, describes how the invasion triangle can be used to focus research and management, and provides examples of application. The framework provided by the invasion triangle is easy to use by both researchers and managers and also applicable at any level of data intensity, from expert opinion to highly controlled experiments. The organizational framework provided by the invasion triangle is beneficial for understanding and predicting why species are invasive in specific environments, for identifying knowledge gaps, for facilitating communication, and for directing management in regard to invasive species.     

Fire as a driver of pine invasions in the Southern Hemisphere: a review

Contrasting evidence in the degree of post-fire conifer invasion reported for different regions of the Southern Hemisphere (SH) raises questions about the role of fire as a presumed driver of invasion. We studied the influence of fire on invasion responses (assessing ‘serotiny’ and ‘time’ as key factors to determine invasion) based on a review of case studies performed in natural habitats of the SH. Our work showed that burned environments have no lag time with respect to invasion and are more susceptible to serotinous pine invasion than are unburned environments. Also, serotinous pines reached extremely high densities in burned habitats, exceeding records for the same species in unburned habitats, as well as for non-serotinous pines in any habitat condition. Therefore, burned environments are impacted by conifer invasion earlier and more intensively than unburned ones. Overall, our work indicates that fire is a leading driver of invasion, but only for serotinous pines. This highlights the importance of considering life history traits of introduced species to determine the probability and extent of invasion in relation to disturbance. We discuss the implications of introducing serotinous species in regions of the SH where serotiny is absent from native flora. Lastly, we provide suggestions for prioritizing management and further study.     

毛竹入侵对森林植物和土壤的影响研究进展

植物与土壤稳定性和动态变化反映了森林生态系统在复杂生境下的自我调控和适应能力。毛竹入侵森林生态系统造成的诸多影响已经成为新的研究热点。系统综述了毛竹入侵的机制,以及对植物生存能力、物种多样性、植被碳储量,土壤理化性质以及土壤微生物结构与功能影响的最新研究进展。针对目前研究存在的问题,提出了丰富毛竹入侵管控手段、着重不同类型毛竹—森林临界面演替长期监测、明确毛竹入侵阶段划分、加强毛竹入侵生态后效研究等研究展望。有助于理解森林与毛竹入侵之间的相互作用、森林对毛竹入侵的响应和适应对策,对了解毛竹入侵机制,预测植物和土壤在毛竹入侵后的变化特征具有一定的借鉴意义。     

外来种入侵的不确定性动态模拟

外来种的入侵性和生境的可入侵性是研究生物入侵机制的两个关键因素。总结多数学者的研究成果,认为外来种的拓殖率(迁移率或繁殖率)、死亡率及在新生境中的竞争力是衡量外来种能否入侵成功的内在实质。从全新的角度出发,将引入的外来种看作是对原有生态系统的一种干扰,并在此基础上结合Tilman的多物种共存模型提出了外来种干扰模型。模拟发现外来种在入侵时具有明显的不确定性。拓殖率小的外来种在新的生态系统中由于不能适应环境无法成功定殖,被排斥在系统之外;相反,拓殖率足够大的话,外来种由于自身优势具有很强的入侵性,在几年或几十年的时间内就会成功地在新的环境中建立种群并拓殖入侵,影响了当地物种的生存及原有生态系统的稳定。研究还发现,物种入侵也存在一定的不确定性,入侵不一定会一直持续下去,或许在百年或几百年的时间内入侵种会突然灭绝,原生态系统又恢复到原来的水平。     

Sex‐specific recombination rates and allele frequencies affect the invasion of sexually antagonistic variation on autosomes

The introduction and persistence of novel, sexually antagonistic alleles can depend upon factors that differ between males and females. Understanding the conditions for invasion in a two‐locus model can elucidate these processes. For instance, selection can act differently upon the sexes, or sex linkage can facilitate the invasion of genetic variation with opposing fitness effects between the sexes. Two factors that deserve further attention are recombination rates and allele frequencies – both of which can vary substantially between the sexes. We find that sex‐specific recombination rates in a two‐locus diploid model can affect the invasion outcome of sexually antagonistic alleles and that the sex‐averaged recombination rate is not necessarily sufficient to predict invasion. We confirm that the range of permissible recombination rates is smaller in the sex benefitting from invasion and larger in the sex harmed by invasion. However, within the invasion space, male recombination rate can be greater than, equal to or less than female recombination rate in order for a male‐benefit, female‐detriment allele to invade (and similarly for a female‐benefit, male‐detriment allele). We further show that a novel, sexually antagonistic allele that is also associated with a lowered recombination rate can invade more easily when present in the double heterozygote genotype. Finally, we find that sexual dimorphism in resident allele frequencies can impact the invasion of new sexually antagonistic alleles at a second locus. Our results suggest that accounting for sex‐specific recombination rates and allele frequencies can determine the difference between invasion and non‐invasion of novel, sexually antagonistic alleles in a two‐locus model.     

外来种隐蔽入侵： 类型及影响

隐蔽入侵（cryptic invasion）是指在形态上与土著种（或早期建群种）不能或难以区分的外来种在人们未觉察的状态下成功入侵的过程。人们对这类入侵方式往往视而不觉。本文综述了外来种隐蔽入侵的类型以及生态影响。隐蔽入侵的类型主要包括外来姊妹种形式的隐蔽入侵、 不同遗传支系的隐蔽入侵、 不同地理种群的隐蔽入侵以及“返传入”。其中, “返传入”目前还是一种假说。由于这类入侵外来种更容易与土著种（或早期建群种）杂交或基因渗透, 因而可对入侵种自身或土著种产生深远的生态影响。鉴于隐蔽入侵现象的广泛性, 建议进一步加强该方面的研究。     

Cooperativity between Plasmodium falciparum adhesive proteins for invasion into erythrocytes

Plasmodium falciparum is the most virulent of the Plasmodium species infective to humans. Different P. falciparum strains vary in their dependence on erythrocyte receptors for invasion and their ability to switch in their utilization of different receptor repertoires. Members of the reticulocyte-binding protein-like (RBL) family of invasion ligands are postulated to play a central role in defining ligand–receptor interactions, known as invasion pathways. Here we report the targeted gene disruption of PfRh2b and PfRh2a in W2mef, a parasite strain that is heavily dependent on sialic-acid receptors for invasion, and show that the PfRh2b ligand is functional in this parasite background. Like the parental line, parasites lacking either PfRh2a or PfR2b can switch to a sialic acid-independent invasion pathway. However, both of the switched lines exhibit a reduced efficiency for invasion into sialic acid-depleted cells, suggesting a role for both PfRh2b and PfRh2a in invasion via sialic acid-independent receptors. We also find a strong selective pressure for the reconstitution of PfRh2b expression at the expense of PfRh2a. Our results reveal the importance of genetic background in ligand–receptor usage by P. falciparum parasites, and suggest that the co-ordinate expression of PfRh2a, PfRh2b together mediate efficient sialic acid-independent erythrocyte invasion.     

Prolonged diapause: a trait increasing invasion speed?

Invasive species are considered to be the second cause of biodiversity erosion, and one challenge is to determine the life history traits that cause an increased invasion capacity. Prolonged diapause is a major trait in evolution and insect population dynamics, but its effects on invasion speed remain unknown. From a recently developed mathematical approach (integro-difference equations) applied to the insect dormancy, we show that despite a dispersal cost, bet-hedging diapause strategies with low (0.1-0.2) prolonged diapause frequency (emergence after 1 or 2 years) can have a higher invasion speed than a simple diapause strategy (emergence after 1 year) when the environmental stochasticity is sufficiently high. In such conditions, prolonged diapause is a trait supporting invasion capacity by increasing population stochastic growth rate. This conclusion, which applies to a large range of demographic parameters, is in opposition to the usual view that prolonged dormancy is an alternative strategy to dispersal. However, prolonged diapause does not support invasion if the level of environmental stochasticity is low. Therefore, conclusion about its influence on invasion ability needs a good knowledge of environmental stochasticity in the introduction area of considered species.     

Cell: sporozoite interactions and invasion by apicomplexan parasites of the genus Eimeria

The site specificity that avian Eimeria sporozoites and, to a more limited degree, other apicomplexan parasites exhibit for invasion in vivo suggests that specific interactions between the sporozoites and the target host cells may mediate the invasion process. Although sporozoite motility and structural and secreted antigens appear to provide the mechanisms for propelling the sporozoite into the host cell,there is a growing body of evidence that the host cell provides characteristics by which the sporozoites recognise and interact with the host cell as a prelude to invasion. Molecules on the surface of cells in the intestinal epithelium, that act as receptor or recognition sites for sporozoite invasion, may be included among these characteristics. The existence of receptor molecules for invasion by apicomplexan parasites was suggested by in vitro studies in which parasite invasion was inhibited in cultured cells that were treated with a variety of substances designed to selectively alter the host cell membrane. These substance included cationic compounds or molecules, enzymes that cleave specific linkages, protease inhibitors, monoclonal antibodies, etc. More specific evidence for the presence of receptors was provided by the binding of parasite antigens to specific host cell surface molecules.Analyses of host cells have implicated 22, 31, and 37 kDa antigens, surface membrane glycoconjugates,conserved epitopes of host cells and sporozoites, etc., but no treatment that perturbs these putative receptors has completely inhibited invasion of the cells by parasites. Regardless of the mechanism,sporozoites of the avian Eimeria also invade the same specific sites in foreign host birds that they invade in the natural host. Thus, site specificity for invasion may be a response to characteristics of the intestine that are shared by a number of hosts rather than to a unique trait of the natural host. Protective immunity elicited against avian Eimeria species is not manifested in a total blockade of parasite invasion. In fact, the effect of immunity on invasion differs according to the eliciting species and depends upon the area of the intestine that is invaded. Immunity produced against caecal species of avian Eimeria, for example Eimeria tenella and Eimeria adenoeides, inhibits subsequent invasion by homologous or heterologous challenge species, regardless of the area of the intestine that the challenge species invade. Conversely, in birds immunised with upper intestinal species, Eimeria acervulina and Eimeria meleagrimitis, invasion by challenge species is not decreased and often is significantly increased.     

Sphingosine-1-phosphate markedly induces matrix metalloproteinase and integrin-dependent human endothelial cell invasion and lumen formation in three-dimensional collagen and fibrin matrices

Endothelial cell invasion is a key step in angiogenic blood vessel formation. Sphingosine-1-phosphate (S1P) has been previously reported to play a role in endothelial cell proliferation, survival, migration, and angiogenesis. Here, we examine the ability of S1P to regulate human endothelial cell invasion into three-dimensional collagen or fibrin matrices. We show that S1P potently stimulated human endothelial cell invasion, lumen formation, and branching morphogenesis in collagen, and fibrin matrices, (5- and 15-fold increases in invasion were observed, respectively). The S1P-induced invasion response was pertussis-toxin sensitive and completely dependent on integrins. Addition of integrin blocking reagents revealed that the alpha2beta1 integrin regulated invasion in collagen matrices, while a combination of alphavbeta3 and alpha5beta1 integrins regulated invasion in fibrin. Additionally, the S1P-induced invasion response was dependent on matrix metalloproteinases (MMPs). Tissue inhibitor of metalloproteinase-3 (TIMP-3) was the only physiologic inhibitor of metalloproteinases that completely inhibited the potent stimulation of invasion induced by S1P. In contrast, TIMP-1 had no blocking effect on invasion or morphogenesis, while TIMP-2 and TIMP-4 partially reduced invasion but completely blocked lumen formation events. Collectively, these data reveal a marked ability of S1P to induce metalloproteinase- and integrin-dependent human endothelial cell invasion and morphogenesis in both collagen and fibrin three-dimensional matrices, the two most physiologically relevant matrices for angiogenesis.     

Intercellular invasion and the organizational stability of tissues: a role for fibronectin

Intracellular invasion is the movement of cells of one type into the fabric of other, contiguous tissues. Invasion is a signature behavior of the malignant tumor and also is found as part of the normal behavior of inflammatory blood cells and tissues engaged in the morphogenetic movements of normal embryogenesis and in a number of instances of normal and pathological tissue remodeling in the adult. Informed by the view that the underlying mechanisms of invasion will be similar for tumor cells and invasive blood and embryonic cells, this review adopts a comparative approach to the analysis of invasion. Invasion results in the development of a diffuse interface between contiguous tissues. Its alternative is the maintenance of stable, planar tissue boundaries. This is the more usual condition for contiguous tissues in the animal. This review will focus on the processes that, on the one hand, stabilize planar contact interfaces between tissues, and, on the other, promote the destabilization of tissue integrity by fostering intercellular invasion. Particular attention is devoted to a role for adhesive interactions mediated by the matrix adhesion molecule, fibronectin. In certain instances, fibronectin in the matrix promotes invasion whereas in others, the presence of fibronectin prevents invasion. The distinction appears to depend on whether the invasive tissue is migrating into an acellular extracellular matrix or whether invasion involves densely cellular tissues. In the first instance, fibronectin promotes invasion, whereas in the second, it stabilizes the interface of the contacting tissues and prevents invasion.     

Structural diversity of target-specific homopyrimidine peptide nucleic acid-dsDNA complexes

Sequence-selective recognition of double-stranded (ds) DNA by homopyrimidine peptide nucleic acid (PNA) oligomers can occur by major groove triplex binding or by helix invasion via triplex P-loop formation. We have compared the binding of a decamer, a dodecamer and a pentadecamer thymine–cytosine homopyrimidine PNA oligomer to a sequence complementary homopurine target in duplex DNA using gel-shift and chemical probing analyses. We find that all three PNAs form stable triplex invasion complexes, and also conventional triplexes with the dsDNA target. Triplexes form with much faster kinetics than invasion complexes and prevail at lower PNA concentrations and at shorter incubation times. Furthermore, increasing the ionic strength strongly favour triplex formation over invasion as the latter is severely inhibited by cations. Whereas a single triplex invasion complex is formed with the decameric PNA, two structurally different target-specific invasion complexes were characterized for the dodecameric PNA and more than five for the pentadecameric PNA. Finally, it is shown that isolated triplex complexes can be converted to specific invasion complexes without dissociation of the Hoogsteen base-paired triplex PNA. These result demonstrate a clear example of a ‘triplex first’ mechanism for PNA helix invasion.     

Coexistence, saturation and invasion resistance in simulated plant assemblages

A popular hypothesis is that species-rich systems are less susceptible to invasion. This hypothesis is based on the idea that species richness correlates with community saturation so that establishment by a new species is more difficult in saturated communities. Little attention has been focussed on how changing assumptions about the processes regulating species richness will alter community properties such as invasion resistance. Here, we simulate plant community assembly using four models that have different underlying coexistence mechanisms (and so differ in the amount of available niche space) and subject them to invasion. We created species richness gradients by comparing between models or by considering the output of a single model with different parameter values. We found that the relation between species richness and invasion resistance depends critically on the model considered and the cause of the species richness gradient. Overall, our results suggest that species richness does not necessarily correlate with saturation and is likely to be a poor predictor of invasion resistance. These results provide a possible explanation for the variety of outcomes reported in recent experimental and observational studies that examine the relationship between species richness and invasion resistance. We conclude that consideration of the processes regulating species richness is crucial for a successful understanding of invasion resistance along species richness gradients.