The saprobic and fruiting abilities of the exotic forest pathogen Heterobasidion irregulare may explain its invasiveness

The North American fungal pathogen Heterobasidion irregulare is invading and threatening pine stands in Italy and is freely hybridizing with the native species Heterobasidion annosum. Susceptibility of native hosts has been excluded as a factor driving H. irregulare invasion. Here we tested whether H. irregulare and H. annosum differ in their ability to saprobically colonize pine wood, and whether saprobic growth is correlated to fruiting bodies production. When inoculated in pine logs, H. irregulare genotypes colonized a volume of wood significantly larger than H. annosum genotypes. Heterobasidion irregulare significantly exceeded H. annosum in all parameters used as metrics of fruiting body production, including number and size of fruiting bodies, and pores perimeter index (PPI), an index summarizing the amount of surface available for spore production. Number of fruiting bodies and PPI were significantly correlated with volume of wood colonized by Heterobasidion genotypes. Results may explain why H. irregulare has been reported to sporulate more abundantly than H. annosum and provide explanations for its high transmission potential in Italy. This knowledge implies that approaches to control the spread of H. irregulare should be aimed at limiting saprobic establishment of the fungus rather than focusing on identifying more tolerant tree species.     

A layover in Europe: Reconstructing the invasion route of asexual lineages of a New Zealand snail to North America

Non‐native invasive species are threatening ecosystems and biodiversity worldwide. High genetic variation is thought to be a critical factor for invasion success. Accordingly, the global invasion of a few clonal lineages of the gastropod Potamopyrgus antipodarum is thus both puzzling and has the potential to help illuminate why some invasions succeed while others fail. Here, we used SNP markers and a geographically broad sampling scheme (N = 1617) including native New Zealand populations and invasive North American and European populations to provide the first widescale population genetic assessment of the relationships between and among native and invasive P. antipodarum. We used a combination of traditional and Bayesian molecular analyses to demonstrate that New Zealand populations harbour very high diversity relative to the invasive populations and are the source of the two main European genetic lineages. One of these two European lineages was in turn the source of at least one of the two main North American genetic clusters of invasive P. antipodarum, located in Lake Ontario. The other widespread North American group had a more complex origin that included the other European lineage and two New Zealand clusters. Altogether, our analyses suggest that just a small handful of clonal lineages of P. antipodarum were responsible for invasion across continents. Our findings provide critical information for prevention of additional invasions and control of existing invasive populations and are of broader relevance towards understanding the establishment and evolution of asexual populations and the forces driving biological invasion.     

Exotic earthworm effects on hardwood forest floor, nutrient availability and native plants: a mesocosm study

A greenhouse mesocosm experiment, representing earthworm-free North American Acer-dominated forest floor and soil conditions, was used to examine the individual and combined effects of initial invasion by three European earthworm species (Dendrobaena octaedra, Lumbricus rubellus and Lumbricus terrestris) on the forest floor and upper soil horizons, N and P availability, and the mortality and biomass of four native understory plant species (Acer saccharum, Aquilegia canadensis, Aralia racemosa, and Carex pensylvanica). All the three earthworm species combined caused larger impacts on most variables measured than any single earthworm species. These included loss of O horizon mass, decreased thickness of the O horizon and increased thickness of the A horizon, and higher availability of N and P. The latter finding differs from field reports where nutrients were less available after invasion, and probably represents an initial transient increase in nutrient supply as earthworms consume and incorporate the O horizon into the A horizon. Earthworms also increased mortality of plants and decreased total mesocosm plant biomass, but here the impact of all the three earthworm species was no greater than that of L. terrestris and/or L. rubellus alone. This study corroborates field studies that European earthworm invasions alter North American forest ecosystem processes by initiating a cascade of impacts on plant community composition and soil properties.     

Infection and disintegration of vascular tissues of non-suberized roots of spruce byHeterobasidion annosum and use of antibodies for characterizing infection

Vascular disintegration mainly of medulla rays of spruce roots is of major significance in root rot disease of spruce caused byH. annosum. Using seedling roots as an experimental model, the possible routes and initial host reactions preceding invasion of vascular tissues was investigated. Transmission electron microscopy showed that penetration through the endodermis was an obvious route but not without host resistance. Using antibodies againstH. annosum hyphal materials, some labelling of vascular tissues remote from sites of fungal colonization suggest the release of fungal secretory products partly active in tissue disintegration. Similarly, intense labelling was also observed in severely colonized host tissues at late stages of infection. Strong labelling recorded at 3 d p.i. mainly on fungal hyphae and scant gold particles on invaded host tissues could imply that induction of host antifungal metabolites may have been a late event. A correlation was found between total antigenic material in root homogenates measured by ELISA, density of tissue labelling by immunocytochemistry and severity of disease symptoms. The importance of this in relation to diagnosis of biotic root rot diseases in the field is discussed.     

Preadaptation and post‐introduction evolution facilitate the invasion of Phragmites australis in North America

Compared with non‐invasive species, invasive plant species may benefit from certain advantageous traits, for example, higher photosynthesis capacity and resource/energy‐use efficiency. These traits can be preadapted prior to introduction, but can also be acquired through evolution following introduction to the new range. Disentangling the origins of these advantageous traits is a fundamental and emerging question in invasion ecology. We conducted a multiple comparative experiment under identical environmental condition with the invasive haplotype M lineage of the wetland grass Phragmites australis and compared the ecophysiological traits of this invasive haplotype M in North America with those of the European ancestor and the conspecific North American native haplotype E lineage, P. australis ssp. americanus. The invasive haplotype M differed significantly from the native North American conspecific haplotype E in several ecophysiological and morphological traits, and the European haplotype M had a more efficient photosynthetic apparatus than the native North American P. australis ssp. americanus. Within the haplotype M lineage, the introduced North American P. australis exhibited different biomass allocation patterns and resource/energy‐use strategies compared to its European ancestor group. A discriminant analysis of principal components separated the haplotype M and the haplotype E lineages completely along the first canonical axis, highly related to photosynthetic gas‐exchange parameters, photosynthetic energy‐use efficiency and payback time. The second canonical axis, highly related to photosynthetic nitrogen use efficiency and construction costs, significantly separated the introduced P. australis in North America from its European ancestor. Synthesis. We conclude that the European P. australis lineage was preadapted to be invasive prior to its introduction, and that the invasion in North America is further stimulated by rapid post‐introduction evolution in several advantageous traits. The multicomparison approach used in this study could be an effective approach for distinguishing preadaptation and post‐introduction evolution of invasive species. Further research is needed to link the observed changes in invasive traits to the genetic variation and the interaction with the environment.     

Comparison of native and non‐native predator consumption rates and prey avoidance behavior in North America and Europe

Novel predator–prey interactions can contribute to the invasion success of non‐native predators. For example, native prey can fail to recognize and avoid non‐native predators due to a lack of co‐evolutionary history and cue dissimilarity with native predators. This might result in a competitive advantage for non‐native predators. Numerous lady beetle species were globally redistributed as biological control agents against aphids, resulting in novel predator–prey interactions. Here, we investigated the strength of avoidance behavior of the pea aphid (Acyrthosiphon pisum) toward chemical cues of native lady beetles and non‐native Asian Harmonia axyridis and European Coccinella septempunctata and Hippodamia variegata in North America, hypothesizing that cues of non‐native lady beetles induce weaker avoidance behavior than cues of co‐evolved native lady beetles. Additionally, we compared aphid consumption of lady beetles, examining potential predation advantages of non‐native lady beetles. Finally, we compared cue avoidance behavior between North American and European pea aphid populations and aphid consumption of native and non‐native lady beetles in North America and Europe. In North America, pea aphids avoided chemical cues of all ladybeetle species tested, regardless of their origin. In contrast to pea aphids in North America, European pea aphids did not avoid cues of the non‐native H. axyridis. The non‐native H. axyridis and C. septempunctata were among the largest and most voracious lady beetle species tested, on both continents. Consequently, in North America non‐native lady beetle species might have a competitive advantage on shared food resources due to their relatively large body size, compared to several native American lady beetle species. In Europe, however, non‐native H. axyridis might benefit from missing aphid cue avoidance as well as a large body size. The co‐evolutionary time gap between the European and North American invasion of H. axyridis likely explains the intercontinental differences in cue avoidance behavior and might indicate evolution in aphids toward non‐native predators.     

Novel weapons and invasion: biogeographic differences in the competitive effects of Centaurea maculosa and its root exudate (±)-catechin

Recent studies suggest that the invasive success of Centaurea maculosa may be related to its stronger allelopathic effects on native North American species than on related European species, one component of the “novel weapons” hypothesis. Other research indicates that C. maculosa plants from the invasive range in North America have evolved to be larger and better competitors than conspecifics from the native range in Europe, a component of the “evolution of increased competitive ability” hypothesis. These hypotheses are not mutually exclusive, but this evidence sets the stage for comparing the relative importance of evolved competitive ability to inherent competitive traits. In a competition experiment with a large number of C. maculosa populations, we found no difference in the competitive effects of C. maculosa plants from North America and Europe on other species. However, both North American and European C. maculosa were much better competitors against plants native to North America than congeners native to Romania, collected in areas where C. maculosa is also native. These results are consistent with the novel weapons hypothesis. But, in a second experiment using just one population from North America and Europe, and where North American and European species were collected from a broader range of sites, competitive interactions were weaker overall, and the competitive effects of C. maculosa were slightly stronger against European species than against North American species. Also consistent with the novel weapons hypothesis, (±)-catechin had stronger effects on native North American species than on native European species in two experiments. Our results suggest that the regional composition of the plant communities being invaded by C. maculosa may be more important for invasive success than the evolution of increased size and competitive ability. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

An ectomycorrhizal symbiosis differently affects host susceptibility to two congeneric fungal pathogens

The role of ectomycorrhizal fungi in modulating host susceptibility to fungal pathogens is poorly known. Pinus sylvestris susceptibility to two congeneric fungal pathogens was compared between mycorrhizal and non-mycorrhizal plants. The ectomycorrhizal fungus was Suillus luteus, while the pathogens were Heterobasidion irregulare and H. annosum. H. irregulare is native to North-America and invasive to Europe, whereas S. luteus and H. annosum are native to Eurasia. Non-mycorrhizal plants were equally susceptible to both pathogens. Mycorrhizal plants were significantly less susceptible to H. annosum than non-mycorrhizal plants, whereas there were no differences when considering H. irregulare. The abundance of ectomycorrhizas was negatively and significantly correlated to the level of host susceptibility only to H. annosum. This study shows that the protective role of ectomycorrhizal fungi may differ when the host is challenged by congeneric fungal pathogens. Results add a further clue to explain and predict the invasiveness of H. irregulare in Europe.     

Putative origin of clonal lineages of Amylostereum areolatum, the fungal symbiont associated with Sirex noctilio, retrieved from Pinus sylvestris, in eastern Canada

The Eurasian Sirex noctilio-Amylostereum areolatum complex was discovered and has become established close to the North American Great Lakes in the 2000s. This invasive forest insect pest represents a very high risk to native and exotic pines in North America. We investigated the geographical origin of clonal lineages of the fungal symbiont A. areolatum in the recently pest-colonized eastern Canadian region by analyzing mitochondrial and nuclear sequence variations and comparing the genetic diversity of a worldwide collection of fungal symbionts among six countries where the Sirex complex is native and four countries from which the insect-fungal complex has been introduced. In total, 102 isolates were analyzed. While 12 multilocus genotypes (MLGs) are observed in the areas where S. noctilio is native, only two MLGs are retrieved from areas where S. noctilio is not native, indicating the wide spread of clonal lineages in the introduced fungal symbiont of S. noctilio. MLG2 comprises 26% of the Canadian isolates and is also observed in Chile and South Africa, where the insect-fungal complex has also been introduced. MLG3 comprises 74% of the Canadian isolates and is also observed in the USA, but nowhere else in our worldwide collection. Thus, at least one of the Canadian clonal lineages shares a common origin with A.?areolatum isolates from the Southern Hemisphere. The source of the second clonal lineage is still unknown, but phylogenetic analyses show that MLG3 is isolated. More extended sampling is necessary to determine the origin of this fungal clonal lineage and investigate its probable symbiotic association with native North American Sirex.     

Identities and distributions of the co-invading ectomycorrhizal fungal symbionts of exotic pines in the Hawaiian Islands

Pine species have become invasive throughout the globe and threaten to replace native biota. The threat of pine invasion is particularly pressing in parts of the tropics where there are no native pines. The factors that govern pine invasion are not often well understood. However, key to pine survival is an obligate and mutualistic interaction with ectomycorrhizal fungi. Thus for pines to successfully invade new habitats compatible ectomycorrhizal fungi must already be present, or be co-introduced. The purpose of this study was to examine the community structure of non-native ectomycorrhizal fungi associated with pine invasions in the Hawaiian Islands. To accomplish this we executed a field and greenhouse study and used a molecular ecology approach to identify the fungi associating with invasive pines in Hawai‘i. We show that: (1) ectomycorrhizal fungal species richness in non-native pine plantations is far less than what is found in pine’s native range, (2) there was a significant decrease in average ectomycorrhizal fungal species richness as distance from pine plantations increased and, (3) Suillus species were the dominant fungi colonizing pines outside plantations. The keystone ectomycorrhizal fungal taxa responsible for pine establishment in Hawai‘i are within genera commonly associated with pine invasions throughout the globe. We surmise that these fungi share functional traits such as the ability for long-distance dispersal from plantations and host tree colonization via spore that lead to their success when introduced to new habitats.     

First detailed report of brood parasitoidism in the invasive population of the paper wasp Polistes dominulus (Hymenoptera, Vespidae) in North America

The European paper wasp Polistes dominulus (Christ) is a model system in the fields of behavioral ecology, ecological immunology, and invasion biology. Since its introduction to the US in 1978, its invasion success has been attributed, in part, to a lack of parasites or parasitoids infecting this population. This is despite the number of parasites which infest the native population and the generalist polistine parasites and parasitoids documented in sympatric North American species. Multiple studies have cited low parasite pressure as evidence that the invasive population of P. dominulus is benefiting from a post-invasion release from enemies. Here, we present the first well documented case of parasitoidism of the invasive population of P. dominulus in North America.     

Callose Synthase in Pinus sylvestris Response during Infection by Species of Heterobasidion annosum sensu lato with Varied Host Preferences

Strengthening of plant cell walls at the site of fungal entry is one of the earliest plant responses to fungal pathogens. The aim of our study was to characterize the pattern of callose synthase localization and callose deposition in roots of Pinus sylvestris after infection by species of the Heterobasidion annosum s.l. complex with different host specificity: H. annosum s.s., H. parviporum and H. abietinum. To address this, sense‐labelled probes and ribonuclease‐treated samples were used to determine in situ hybridizations of callose synthase by FISH method. Furthermore, determination of callose accumulation within P. sylvestris cells was carried out using aniline blue. The different species of H. annosum s.l. had distinct impacts on the callose synthase staining within plant tissues. Moreover, while inoculation with strains of H. abietinum resulted in callose synthase accumulation at the point of hyphae contact with the host cell, this was not observed with the other species. A significant difference in callose synthesis localization was observed after inoculation with varied species of H. annosum s.l. as a result of the specific interactions with the host.     

Invasive host for invasive pest: when the Asiatic cherry fly (Drosophila suzukii) meets the American black cherry (Prunus serotina) in Europe

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DNA-barcoding evidence for widespread introductions of a leech from the South American<Emphasis Type="Italic">Helobdella triserialis</Emphasis> complex

Morphological examination and a molecular phylogenetic analysis of leeches from Australia, New Zealand, South Africa and Hawaii show that these specimens are members of a species in the South American Helobdella triserialis species complex. Though it has been seen before, this leech was not recognized as an invasive species. Rather, it was first described as Helobdella striata from Germany later renamed Helobdella europaea and then independently described as Helobdella papillornata from Australia. Because the appropriate name for this leech from its South American endemic locale, Helobdella (triserialis) lineata, is preoccupied by a North American species, we formally recognize H. europaea as the valid taxon name. Although this invader is not a bloodfeeder it may be expected to have an impact on native annelid and mollusk faunas.     

Beneath the bark: associations among Sirex noctilio development,bluestain fungi,and pine host species in North America

1. Invasive species with global distributions encounter unique environmental and biotic variables that can greatly affect the magnitude of their impact. The European woodwasp, Sirex noctilio Fabricius, is a prime example that has invaded climatically and ecologically distinct ecosystems across the Southern Hemisphere and, more recently, North America. 2. Northeastern North America presents a unique set of conditions, including pine host species, native parasitoids, a diverse assemblage of native co‐colonising insects, and fungal associates of these co‐colonisers. In North America, S. noctilio attacks both a naturalised ancestral host (Pinus sylvestris L.) from Europe and a naïve native host (P. resinosa). A large assemblage of insects and their associated bluestaining ophiostomatoid fungi colonise these pines. Competition between S. noctilio and this group is a hypothesised mechanism of biotic resistance in the invaded region of North America, possibly via superior resource capture abilities or alteration of host tissue by bluestain fungi. 3. Investigating these ecological interactions is challenging because they manifest deep in the xylem tissue. To overcome this, 30 experimentally stressed trees were systematically dissected with an electric log splitter to investigate the effects of bluestain fungi and tree factors on S. noctilio development and parasitism by native hymenopterans. 4. Body size and colonisation density were affected by pine species, with S. noctilio being 25% larger and densities three‐fold greater in P. sylvestris than P. resinosa. Survivorship was slightly negatively correlated with the proportional volume of bluestain infection. Interestingly, rhyssine (Rhyssa and Megarhyssa spp.) parasitism responded positively to greater S. noctilio density, but there was no density relationship with Ibalia leucospoides ensiger parasitism. Pine host species appears to play a strong role in S. noctilio development, which is important considering uninvaded regions of North America have a diversity of pine species that likely vary in their susceptibility to this woodborer.     

Evidence for multiple introductions of Centaurea stoebe micranthos (spotted knapweed,Asteraceae) to North America

Invasive species’ success may depend strongly on the genetic resources they maintain through the invasion process. We ask how many introductions have occurred in the North American weed Centaurea stoebe micranthos (Asteraceae), and explore whether genetic diversity and population structure have changed as a result of introduction. We surveyed individuals from 15 European native range sites and 11 North American introduced range sites at six polymorphic microsatellite loci. No significant difference existed in the total number of alleles or in the number of private alleles found in each range. Shannon–Weaver diversity of phenotype frequencies was also not significantly different between the ranges, while expected heterozygosity was significantly higher in the invasive range. Population structure was similar between the native range and the invasive range, and isolation by distance was not significant in either range. Traditional assignment methods did not allocate any North American individuals to the sampled European populations, while Bayesian assignment methods grouped individuals into nine genetic clusters, with three of them shared between North America and Europe. Invasive individuals tended to have genetically admixed profiles, while natives tended to assign more strongly to a single cluster. Many North American individuals share assignment with Romania and Bulgaria, suggesting two separate invasions that have undergone gene flow in North America. Samples from three other invasive range sites were genetically distinct, possibly representing three other unique introductions. Multiple introductions and the maintenance of high genetic diversity through the introduction process may be partially responsible for the invasive success of C. stoebe micranthos.     

Reed Canary Grass (Phalaris arundinacea) as a Biological Model in the Study of Plant Invasions

Invasive species pose a serious threat to native plant communities and are an important contributor to loss of biodiversity. In the case of Phalaris arundinacea, L. (Poaceae), reed canary grass, a cool-season, long-lived perennial plant native to Eurasia and North America, nonnative agronomically important genotypes were introduced to North America for numerous uses such as forage and soil stabilization. Following repeated introductions, reed canary grass became an aggressive invader that takes over natural wet prairies, stream-banks and wetlands. Reed canary grass can outcompete native plant species, resulting in monospecific stands with concomitant loss of plant and insect diversity and ultimately to alteration in ecosystem function. Abiotic factors such as disturbance, changes in hydrological regime, and particularly nutrient runoff to wetlands can enhance reed canary grass establishment and vegetative spread. In addition, the species' capacity for early season growth, rapid vegetative spread, high stem elongation potential, wide physiological tolerance, and high architectural plasticity make the species highly aggressive under a wide range of ecological conditions. The change in life-history and environmental conditions responsible for the enhanced aggressiveness observed between native and invasive genotypes are not yet understood. Hence, reed canary grass provides an ideal study system to test a number of ecological and genetic hypotheses to explain why some plant species become extremely aggressive when transported into a new geographical area. To date, genetic studies have found that invasive populations have high genetic diversity and that genotypes differ in their phenotypic plasticity and response to ecological conditions, which may contribute to their invasion success. Finally comparative studies currently underway on European native and American invasive genotypes of reed canary grass should shed light on the mechanisms responsible for reed canary grass's aggressiveness and should provide an experimental protocol to test ecological and genetic hypotheses about what makes a species invasive.     

Effects of European Earthworm Invasion on Soil Characteristics in Northern Hardwood Forests of Minnesota, USA

European earthworms are colonizing worm-free hardwood forests across North America. Leading edges of earthworm invasion in forests of northern Minnesota provide a rare opportunity to document changes in soil characteristics as earthworm invasions are occurring. Across leading edges of earthworm invasion in four northern hardwood stands, increasing total earthworm biomass was associated with rapid disappearance of the O horizon. Concurrently, the thickness, bulk density and total soil organic matter content of the A horizon increased, and it’s percent organic matter and fine root density decreased. Different earthworm species assemblages influenced the magnitude and type of change in these soil parameters. Soil N and P availability were lower in plots with high earthworm biomass compared to plots with low worm biomass. Decreases in soil nitrogen availability associated with high earthworm biomass were reflected in decreased foliar nitrogen content for Carex pensylvanica, Acer saccharum and Asarum canadense but increased foliar N for Athyrium felix-femina. Overall, high earthworm biomass resulted in increased foliar carbon to nitrogen ratios. The effects of earthworm species assemblages on forest soil properties are related to their feeding and burrowing habits in addition to effects related to total biomass. The potential for large ecosystem consequences following exotic earthworm invasion has only recently been recognized by forest ecologists. In the face of rapid change and multiple pressures on native forest ecosystems, the impacts of earthworm invasion on forest soil structure and function must be considered.